FSH调控小鼠卵泡闭锁及卵泡颗粒细胞Cyp1b1基因表达机制
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摘要
原始卵泡募集后脱离原始卵泡库开始启动发育,经过初级、次级卵泡逐渐发育成有腔卵泡,有腔卵泡对促性腺激素更加敏感开始加速生长并逐渐优势化形成优势化卵泡,优势化的卵泡命运有两个即排卵和闭锁。优势化卵泡的闭锁跟卵泡内雌激素浓度降低不能引起LH峰有很大的关系,卵泡内颗粒细胞凋亡也是卵泡闭锁的潜在机制。长期以来,人们对卵泡闭锁做了大量的相关研究工作,但调控卵泡闭锁的分子机制还不完全清楚,仍然需要进一步的研究和探索。阐明这一生理过程的分子机理对于提高动物繁殖力、治疗动物排卵障碍等生殖疾病具有十分重要的意义。
本论文选取小鼠为试验动物,研究FSH调控延时排卵优势卵泡闭锁及雌激素代谢相关基因Cyplbl的分子机制。主要进行了以下几方面的研究：(1)检测FSH对延时排卵优势卵泡内颗粒细胞凋亡及凋亡相关基因的影响。(2)检测延时排卵优势卵泡内雌激素代谢相关基因的表达情况。(3)FSH对雌激素代谢关键基因Cyplbl表达调控和雌激素代谢产物四羟基雌二醇对颗粒细胞的影响。(4) Cyplbl启动子区转录因子分析。(5)FSH对Cyplbl转录因子Statl的调控作用。(6)FSH调控Statl磷酸化水平的机制研究。
综合本论文的研究结果,主要得出以下结论：
(1)FSH通过抑制颗粒细胞凋亡抑制延时排卵优势卵泡的闭锁
颗粒细胞的凋亡是小鼠卵泡闭锁的最主要诱因之一,研究发现FSH可以抑制延时排卵优势卵泡内颗粒细胞凋亡和凋亡相关基因如Caspase-3,9, BIM等的表达。
(2)FSH抑制颗粒细胞雌激素代谢相关基因Cyplbl的表达
研究发现小鼠卵泡内颗粒细胞雌激素代谢相关基因中只有Cyplbl一直表达,Cyplal, Cypla2, Cyp3a在小鼠颗粒细胞中几乎不表达。FSH在体内和体外环境都可以抑制颗粒细胞内Cyplbl基因的表达,Cyplbl催化雌二醇产生的代谢产物四羟基雌二醇(兰10μM)对体外培养的颗粒细胞也有显著的促凋亡作用。
(3)FSH通过调控Statl磷酸化水平调控Cyplbl表达
通过网站预测和实验分析发现Statl是Cyplbl的主要转录因子之一,染色质免疫共沉淀CHIP分析发现FSH可能通过调节转录因子Statl在Cyplbl启动子区的富集度调控Cyplbl的表达。研究发现FSH对Statl蛋白水平并没有显著的调控作用且Statl酪氨酸701位点磷酸化在颗粒细胞中检测为阴性,通过信号通路分析发现FSH可以通过p38MAPK信号通路激活ser、thr磷酸酯酶PP2A的活性,致使Statl丝氨酸727位点去磷酸化,使其从基因Cyplbl启动子区脱离调控卵泡颗粒细胞雌激素代谢相关基因Cyplbl的表达。
本文在FSH抑制卵泡闭锁和雌激素代谢方面做了生理生化相关的研究,确定了FSH可以通过抑制颗粒细胞凋亡来抑制延时排卵优势卵泡的闭锁。阐明了FSH调控卵泡内雌激素代谢相关基因Cyplbl的分子机制。有助于卵泡闭锁分子机制的进一步阐明。
Primordial follicles raised from the primordial follicles library started development. After primary, secondary follicles gradually develops into antral follicles, antral follicles are more sensitive to gonadotropin began to accelerate growth and form of dominant follicle. The fate of the dominant follicles is ovulation or atresia. The concentration of estrogen reduce within the follicle can not cause the LH peak have a great relationship with dominant follicle atresia, and granulosa cells apoptosis is also a potential mechanism of follicular atresia. Long time, people have done a lot of research work on the follicular atresia, but the molecular mechanism of regulation of follicular atresia is not entirely clear, still need further research and exploration. Clarify the molecular mechanism of this physiological process has a very important significance for improving animal fertility, reproductive diseases, treatment of animal ovulation disorders.
The papers selected mice as experimental animals, studies FSH regulation of delayed ovulation dominant follicle atresia and estrogen metabolism genes Cyplbl molecular mechanisms. Conducted a study of the following aspects:(1) Detection the function of FSH on granulosa cell apoptosis in delayed ovulation dominant follicle and related apoptosis genes.(2) Detection of the delayed ovulation dominant follicle estrogen synthesis and metabolism gene expression.(1) Detection of FSH impact on granulosa cell apoptosis and related genes of delayeded ovulation dominant follicles.(2) Detection the expression estrogen metabolism-related genes of the delayeded ovulation follicles.(3) FSH regulated estrogen metabolism key gene Cyplbl expression and estrogen metabolite4-hydroxy-estradiol effect on the granulosa cells.(4) The transcription factor analysis of Cyp1b1promoter region.(5) The role of FSH on Cyplbl transcription factor Statl.(6) FSH regulation of Statl phosphorylation level mechanism. Comprehensive results of this thesis, the following conclusions:
(1) FSH suppression delayeded ovulation dominant follicle atresia by inhibiting apoptosis of granulosa cells
Granulosa cell apoptosis is one of the main cause of mouse follicular atresia, we found that FSH can inhibit granulosa cell apoptosis and apoptosis-related genes expressios, such as Caspase-3,9, BIM to rescue delayeded ovulation dominant follicle atresia.
(2) FSH suppression granulosa cell estrogen metabolism genes Cyplbl expression
The study found that the crucial gene of delayed ovulation dominant follicle granulosa cells estrogen metabolism is Cyplbl. The genes Cyplal, Cypla2, Cyp3a in granulosa cells almost no expression. FSH can inhibit Cyplbl expression in granulosa cells in vitro and in vivo, estrogen metabolite4-hydroxy-estradiol (≧10μM) by Cyplbl has a significant effect on cultured granulosa cells apoptosis.
(3) FSH regulation of Statl phosphorylation levels of regulation of Cyplbl expression
Site prediction and experimental analysis found that Statl is one of the important transcription factors of Cyp1b1. Chromatin immunoprecipitation analysis showed that FSH may through the transcription factor Statl in Cyplbl promoter region play a regulatory role. Further studies showed that levels of Statl protein is not a significant regulatory by FSH. Statl tyrosine701phosphorylation is not detected in the granulosa cells, but FSH could via p38MAPK activate ser, thr phosphatase PP2A activities lead dephosphorylation of Statl on ser727, and drop from the promoter region of Cyp1b1to regulate expression of estrogen metabolism-related gene Cyplbl in follicle granulosa cells.
FSH suppression delayed ovulation follicles atresia and estrogen metabolism, physiological and biochemical studies to determine FSH suppression follicular atresia by inhibiting apoptosis of granulosa cells. Elucidate the molecular mechanism of FSH regulation of follicular estrogen metabolism gene Cyplbl. Help to further elucidate the molecular mechanism of follicular atresia.
本论文选取小鼠为试验动物,研究FSH调控延时排卵优势卵泡闭锁及雌激素代谢相关基因Cyplbl的分子机制。主要进行了以下几方面的研究：(1)检测FSH对延时排卵优势卵泡内颗粒细胞凋亡及凋亡相关基因的影响。(2)检测延时排卵优势卵泡内雌激素代谢相关基因的表达情况。(3)FSH对雌激素代谢关键基因Cyplbl表达调控和雌激素代谢产物四羟基雌二醇对颗粒细胞的影响。(4) Cyplbl启动子区转录因子分析。(5)FSH对Cyplbl转录因子Statl的调控作用。(6)FSH调控Statl磷酸化水平的机制研究。
综合本论文的研究结果,主要得出以下结论：
(1)FSH通过抑制颗粒细胞凋亡抑制延时排卵优势卵泡的闭锁
颗粒细胞的凋亡是小鼠卵泡闭锁的最主要诱因之一,研究发现FSH可以抑制延时排卵优势卵泡内颗粒细胞凋亡和凋亡相关基因如Caspase-3,9, BIM等的表达。
(2)FSH抑制颗粒细胞雌激素代谢相关基因Cyplbl的表达
研究发现小鼠卵泡内颗粒细胞雌激素代谢相关基因中只有Cyplbl一直表达,Cyplal, Cypla2, Cyp3a在小鼠颗粒细胞中几乎不表达。FSH在体内和体外环境都可以抑制颗粒细胞内Cyplbl基因的表达,Cyplbl催化雌二醇产生的代谢产物四羟基雌二醇(兰10μM)对体外培养的颗粒细胞也有显著的促凋亡作用。
(3)FSH通过调控Statl磷酸化水平调控Cyplbl表达
通过网站预测和实验分析发现Statl是Cyplbl的主要转录因子之一,染色质免疫共沉淀CHIP分析发现FSH可能通过调节转录因子Statl在Cyplbl启动子区的富集度调控Cyplbl的表达。研究发现FSH对Statl蛋白水平并没有显著的调控作用且Statl酪氨酸701位点磷酸化在颗粒细胞中检测为阴性,通过信号通路分析发现FSH可以通过p38MAPK信号通路激活ser、thr磷酸酯酶PP2A的活性,致使Statl丝氨酸727位点去磷酸化,使其从基因Cyplbl启动子区脱离调控卵泡颗粒细胞雌激素代谢相关基因Cyplbl的表达。
本文在FSH抑制卵泡闭锁和雌激素代谢方面做了生理生化相关的研究,确定了FSH可以通过抑制颗粒细胞凋亡来抑制延时排卵优势卵泡的闭锁。阐明了FSH调控卵泡内雌激素代谢相关基因Cyplbl的分子机制。有助于卵泡闭锁分子机制的进一步阐明。
Primordial follicles raised from the primordial follicles library started development. After primary, secondary follicles gradually develops into antral follicles, antral follicles are more sensitive to gonadotropin began to accelerate growth and form of dominant follicle. The fate of the dominant follicles is ovulation or atresia. The concentration of estrogen reduce within the follicle can not cause the LH peak have a great relationship with dominant follicle atresia, and granulosa cells apoptosis is also a potential mechanism of follicular atresia. Long time, people have done a lot of research work on the follicular atresia, but the molecular mechanism of regulation of follicular atresia is not entirely clear, still need further research and exploration. Clarify the molecular mechanism of this physiological process has a very important significance for improving animal fertility, reproductive diseases, treatment of animal ovulation disorders.
The papers selected mice as experimental animals, studies FSH regulation of delayed ovulation dominant follicle atresia and estrogen metabolism genes Cyplbl molecular mechanisms. Conducted a study of the following aspects:(1) Detection the function of FSH on granulosa cell apoptosis in delayed ovulation dominant follicle and related apoptosis genes.(2) Detection of the delayed ovulation dominant follicle estrogen synthesis and metabolism gene expression.(1) Detection of FSH impact on granulosa cell apoptosis and related genes of delayeded ovulation dominant follicles.(2) Detection the expression estrogen metabolism-related genes of the delayeded ovulation follicles.(3) FSH regulated estrogen metabolism key gene Cyplbl expression and estrogen metabolite4-hydroxy-estradiol effect on the granulosa cells.(4) The transcription factor analysis of Cyp1b1promoter region.(5) The role of FSH on Cyplbl transcription factor Statl.(6) FSH regulation of Statl phosphorylation level mechanism. Comprehensive results of this thesis, the following conclusions:
(1) FSH suppression delayeded ovulation dominant follicle atresia by inhibiting apoptosis of granulosa cells
Granulosa cell apoptosis is one of the main cause of mouse follicular atresia, we found that FSH can inhibit granulosa cell apoptosis and apoptosis-related genes expressios, such as Caspase-3,9, BIM to rescue delayeded ovulation dominant follicle atresia.
(2) FSH suppression granulosa cell estrogen metabolism genes Cyplbl expression
The study found that the crucial gene of delayed ovulation dominant follicle granulosa cells estrogen metabolism is Cyplbl. The genes Cyplal, Cypla2, Cyp3a in granulosa cells almost no expression. FSH can inhibit Cyplbl expression in granulosa cells in vitro and in vivo, estrogen metabolite4-hydroxy-estradiol (≧10μM) by Cyplbl has a significant effect on cultured granulosa cells apoptosis.
(3) FSH regulation of Statl phosphorylation levels of regulation of Cyplbl expression
Site prediction and experimental analysis found that Statl is one of the important transcription factors of Cyp1b1. Chromatin immunoprecipitation analysis showed that FSH may through the transcription factor Statl in Cyplbl promoter region play a regulatory role. Further studies showed that levels of Statl protein is not a significant regulatory by FSH. Statl tyrosine701phosphorylation is not detected in the granulosa cells, but FSH could via p38MAPK activate ser, thr phosphatase PP2A activities lead dephosphorylation of Statl on ser727, and drop from the promoter region of Cyp1b1to regulate expression of estrogen metabolism-related gene Cyplbl in follicle granulosa cells.
FSH suppression delayed ovulation follicles atresia and estrogen metabolism, physiological and biochemical studies to determine FSH suppression follicular atresia by inhibiting apoptosis of granulosa cells. Elucidate the molecular mechanism of FSH regulation of follicular estrogen metabolism gene Cyplbl. Help to further elucidate the molecular mechanism of follicular atresia.
引文
1.田允波,曾书琴,陈学进,施振旦.(2006)哺乳动物卵泡生长发育的调控。广西农业生物科学.127-134。
2. Kimura F, Bonomi LM, Schneyer AL (2011) Follistatin regulates germ cell nest breakdown and primordial follicle formation. Endocrinology 152:697-706.
3.芮荣,钱菊汾.(1998)卵泡发育及其控制。草食家畜.16-22。
4.彭宇洪,庄广伦,周灿权.(2006)小鼠体外发育卵母细胞生长分化因子-9基因表达。南方医科大学学报.1341-1345。
5. Kobayashi N, Orisaka M, Cao M, Kotsuji F, Leader A, Sakuragi N, Tsang BK (2009) Growth differentiation factor-9 mediates follicle-stimulating hormone-thyroid hormone interaction in the regulation of rat preantral follicular development. Endocrinology 150:5566-5574.
6. Zerek-Melen G, Lewinski A, Pawlikowski M, Sewerynek E, Kunert-Radek J (1987) Influence of somatostatin and epidermal growth factor (EGF) on the proliferation of follicular cells in the organ-cultured rat thyroid. Res Exp Med (Berl) 187:415-421.
7. Hirshfield AN (1991) Development of follicles in the mammalian ovary. Int Rev Cytol 124:43-101.
8. Richards JS, Ireland JJ, Rao MC, Bernath GA, Midgley AR, Reichert Jr LE (1976) Ovarian follicular development in the rat:hormone receptor regulation by estradiol, follicle stimulating hormone and luteinizing hormone. Endocrinology 99:1562-1570.
9. Chada M, Prusa R, Bronsky J, Pechova M, Kotaska K, Lisa L (2003) Inhibin B follicle stimulating hormone, luteinizing hormone, and estradiol and their relationship to the regulation of follicle development in girls during childhood and puberty. Physiol Res 52:341-346.
10.王海滨,谢辉蓉,夏国良.(2002)哺乳动物卵泡早期发育调控的研究进展。国外畜牧科技.29：37-42。
11. Guo CJ, Pan Q, Li DG, Sun H, Liu BW (2009) miR-15b and miR-16 are implicated in activation of the rat hepatic stellate cell:An essential role for apoptosis. J Hepatol 50:766-778.
12. Roberts AJ, Skinner MK (1990) Hormonal regulation of thecal cell function during antral follicle development in bovine ovaries. Endocrinology 127:2907-2917.
13. Mihm M, Bleach ECL (2003) Endocrine regulation of ovarian antral follicle development in cattle. Anim Reprod Sci 78:217-237.
14. Mott JL, Kobayashi S, Bronk SF, Gores GJ (2007) mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26:6133-6140.
15. Matsuda-Minehata F, Inoue N, Goto Y, Manabe N (2006) The regulation of ovarian granulosa cell death by pro-and anti-apoptotic molecules. J Reprod Dev 52:695-705.
16. Baerwald AR, Adams GP, Pierson RA (2003) Characterization of ovarian follicular wave dynamics in women. Biol Reprod 69:1023-1031.
17. Mihm M, Good TE, Ireland JL, Ireland JJ, Knight PG, Roche JF (1997) Decline in serum follicle-stimulating hormone concentrations alters key intrafollicular growth factors involved in selection of the dominant follicle in heifers. Biol Reprod 57:1328-1337.
18. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
19. Richards JS, Hedin L (1988) Molecular aspects of hormone action in ovarian follicular development, ovulation, and luteinization. Annu Rev Physiol 50:441-463.
20. Fortune JE (1994) Ovarian follicular growth and development in mammals. Biol Reprod 50: 225-232.
21. Greenwald GS, Roy SK (1994) Follicular development and its control. In:Knobil E, Neill JD (eds.). The Physiology of Reproduction 1:629-724.
22. Vander AJ, Sherman JH, Luciano DS (1994) Reproduction In:Prancan KM, Bradley JW (eds.). Human Physiology:The Mechanisms of Body Function. New York:McGraw-Hill:661-692.
23. Donath J, Nishino Y, Schulz T, Michna H (2000) The antiovulatory potential of progesterone antagonists correlates with a down-regulation of progesterone receptor in hypothalamus, pituitary and ovary. AnatAnz 182:143-145.
24. Richards JS, Ireland JJ, Rao MC, Bernath GA, Midgley AR, Reichert Jr LE (1976) Ovarian follicular development in the rat:hormone receptor regulation by estradiol, follicle stimulating hormone and luteinizing hormone. Endocrinology 99:1562-1570.
25. Chada M, Prusa R, Bronsky J, Pechova M, Kotaska K, Lisa L (2003) Inhibin B, follicle stimulating hormone, luteinizing hormone, and estradiol and their relationship to the regulation of follicle development in girls during childhood and puberty. Physiol Res 52:341-346.
1. Lebedeva I, Denisenko Y, Lebedev V.A, Kuzmina TI (1998) Prolactin in follicular fluid and intracellular store calcium in follicular cells are related to morphological signs of ovarian follicle atresia in cows:work in progress. Theriogenology 49:509-519.
2. Bjersing L (1967) On the ultrastructure of follicles and isolated follicular granulosa cells of porcine ovary. Cell and Tissue Research 82:173-186.
3. Bhardwaj JK, Sharma RK (2011) Changes in Trace Elements during Follicular Atresia in Goat (Capra hircus) Ovary. Biol Trace Elem Res 140:291-298.
4. Oakberg EF (1979) Follicular growth and atresia in the mouse. In Vitro 15:41-49.
5. Manabe N, Matsuda-Minehata F, Goto Y, Maeda A, Cheng Y, Nakagawa S, Inoue N, Wongpanit K, Jin H, Gonda H, Li J (2008) Role of cell death ligand and receptor system on regulation of follicular atresia in pig ovaries. Reprod Domest Anim 43:268-272.
6. Sai T, Goto Y, Yoshioka R, Maeda A, Matsuda F, Sugimoto M, Wongpanit K, Jin HZ, Li JY, Manabe N (2011) Bid and Bax are involved in granulosa cell apoptosis during follicular atresia in porcine ovaries. J Reprod Dev 57:421-427.
7. Yu YS, Sui HS, Han ZB, Li Wei, Luo MJ, Tan JH (2004) Apoptosis in granulosa cells during follicular atresia:relationship with steroids and insulin-like growth factors. Cell Res 14:341-6
8. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection, dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
9. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, Ireland JJ, Roche JF (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64:839-848.
10. Vaskivuo TE, Tapanainen JS (2003) Apoptosis in the human ovary. Reprod Biomed Online 6:24-35.
11. Manabe N, Goto Y, Matsuda-Minehata F, Inoue N, Maeda A, Sakamaki K, Miyano T (2004) Regulation mechanism of selective atresia in porcine follicles:regulation of granulosa cell apoptosis during atresia. J Reprod Dev 50:493-514.
12. Hirshfield AN (1991) Development of follicles in the mammalian ovary. Int Rev Cytol 124:43-101.
13. Fortune, JE (2003) The early stages of follicular development:activation of primordial follicles and growth of preantral follicles. Animal Reproduction Science 78:135-163
14. Oktem O, Urman B (2010) Understanding follicle growth in vivo. Hum Reprod 25:2944-2954.
15. Rajakoski E (1960) The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical, end left-right variations. Acta Endocrinol Suppl 34:61-68.
16. Marion GB, Gier HT, Choudary JB (1968) Micromorphology of the bovine ovarian follicular system. J Anim Sci 27:451-465.
17. Irving-Rodgers H, Wezel I, Mussard M, Kinder J, Rodgers R (2001) Atresia revisited:two basic patterns of atresia of bovine antral follicles. Reproduction 122:761-775.
18. Cheng Y, Inoue N, Matsuda-Minehata F, Goto Y, Maeda A, Manabe N (2005) Changes in expression and localization of connexin 43 mRNA and protein in porcine ovary granulosa cells during follicular atresia. J Reprod Dev 51:627-637.
19. Bosu WT, Perez GI, Kujjo LL (1996) Natural and endotoxin-induced atresia of preantral and early antral follicles is characterized by DNA internucleosomal cleavage. Mol Reprod Dev 44:352-359.
20. Manabe N, Matsuda-Minehata F, Goto Y, Maeda A, Cheng Y, Nakagawa S, Inoue N, Wongpanit K, Jin H, Gonda H, Li J (2008) Role of cell death ligand and receptor system on regulation of follicular atresia in pig ovaries. Reprod Domest Anim 43:268-272.
21. Sai T, Goto Y, Yoshioka R, Maeda A, Matsuda F, Sugimoto M, Wongpanit K, Jin HZ, Li JY, Manabe N (2011) Bid and Bax are involved in granulosa cell apoptosis during follicular atresia in porcine ovaries. J Reprod Dev 57:421-427.
22. Kim JM, Boone DL, Auyeung A, Tsang BK (1998) Granulosa cell apoptosis induced at the penultimate stage of follicular development is associated with increased levels of Fas and Fas ligand in the rat ovary. Biol Reprod 58:1170-1176.
23. D'Haeseleer M, Cocquyt G, Van Cruchten S, Simoens P, Broeck WV (2006) Cellspecific localisation of apoptosis in the bovine ovary at different stages of the oestrous cycle. Theriogenology 65:757-772.
24. Peluffo MC, Stouffer RL, Tesone M (2007) Activity and expression of different members of the caspase family in the rat corpus luteum during pregnancy and postpartum. Am J Physiol Endocrinol Metab 293:1215-1223.
25. Tilly, JL (1996) Apoptosis and ovarian function. Rev Reprod 1:162-172.
26. Chun SY, Hsueh AJ (1998) Paracrine mechanisms of ovarian follicle apoptosis. J Reprod Immunol 39:63-75.
27. Johnson AL (2003) Intracellular mechanisms regulating cell survival in ovarian follicles. Animal Reproduction Science 78:185-201.
28. Basini G, Mainardi GL, Bussolati S, Tamanini C (2002) Steroidogenesis, proliferation and apoptosis in bovine granulosa cells:role of tumour necrosis factor; and its possible signalling mechanisms. Reproduction. Fertility and Development.14:141-150.
29. Sasson R, Winder N, Kees S, Amsterdam A (2002) Induction of apoptosis in granulosa cells by TNF[alpha] and its attenuation by glucocorticoids involve modulation of Bcl-2. Biochemical and Biophysical Research Communications 294:51-59.
30. Porter DA, Vickers SL, Cowan RG, Huber SC, Quirk SM (2000) Expression and function of Fas antigen vary in bovine granulosa and theca cells during ovarian follicular development and atresia. Biol Reprod 62:62-66.
31. Johnson AL, Ratajczak C, Haugen MJ, Liu HK, Woods DC (2007) Tumor necrosis factor-related apoptosis inducing ligand expression and activity in hen granulosa cells. Reproduction 133: 609-616.
32. Jaaskelainen M, Kyronlahti A, Anttonen M, Nishi Y, Yanase T, Secchiero P, Zauli G, Tapanainen JS, Heikinheimo M, Vaskivuo TE (2009) TRAIL pathway components and their putative role in granulosa cell apoptosis in the human ovary. Differentiation 4:369-376.
33. Quirk SM, Harman RM, Cowan RG (2000) Regulation of Fas Antigen (Fas, CD95)-Mediated Apoptosis of Bovine Granulosa Cells by Serum and Growth Factors. Biology of Reproduction 63: 1278-1284.
34. Vickers SL, Cowan RG, Harman RM, Porter DA, Quirk SM (2000) Expression and Activity of the Fas Antigen in Bovine Ovarian Follicle Cells. Biology of Reproduction 62:54-61.
35. Hussein MR (2005) Apoptosis in the ovary:molecular mechanisms. Human Reproduction Update 11:162-178.
36. Hennebold JD (2010) Preventing Granulosa Cell Apoptosis Through the Action of a Single MicroRNA. Biology of Reproduction 83:165-167.
37. Carletti MZ, Fiedler SD, Christenson LK (2010) MicroRNA 21 Blocks Apoptosis in Mouse Periovulatory Granulosa Cells. Biology of Reproduction 83:286-295.
38. Wajant H (2002) The Fas signaling pathway:more than a paradigm. Science's STKE 296:1635.
39. Berry D (2007) Molecular animation of cell death mediated by the Fas pathway. Science's STKE:trl.
40. Dlamini Z, Mbita Z, Zungu M (2004) Genealogy expression, and molecular mechanisms in apoptosis. Pharmacol Ther 101:1-15.
41. Hirshfield AN (1991) Development of follicles in the mammalian ovary. Int Rev Cytol 124:43-101
42. Pederson T (1970) Follicular kinetics in the ovary of the cyclic mouse. Acta Endocrinol (Copenh) 64: 304-323
43. Richards JS (1978) Hormonal control of follicular growth and maturation in mammals. In:Jones RE (ed) The Vertebrate Ovary:Comparative Biology and Evolution. Plenum Press, New York: 331-360.
44. Richards JS (1980) Maturation of ovarian follicles:actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol Rev.60:51-89
45. Richards JS (1975) Estradiol receptor content in rat granulose cells during follicular development. Endocrinology 97:1174-1184
46. Rao MC, Midgley Jr AR, Richards JS (1978) Hormonal regulation of ovarian cellular proliferation. Cell 14:71-78
47. Richards JS, Midgley Jr AR (1976) Protein hormone action:a key to understanding ovarian follicular and luteal cell development. Biol Reprod 14:82-94
48. Mason AJ, Hayflick JS, Zoeller RT, Young WS, Phillips HS, Nikolics K, Seeburg PH (1986) A deletion truncating the gonadotropin-releasing hormone gene is responsible for hypogonadism in the hpg mouse. Science 234:1366-1371
49. Mason AJ, Pitts SL, Nikolics K, Szonyi E, Wilcox JN, Seeburg PH, Stewart TA (1986) The hypogonadal mouse:reproductive functions restored by gene therapy. Science 234:1372-1378
50. Kumar TR, Wang Y, Lu N, Matzuk MM (1997) Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 15:201-204
51. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90:11162-11166
52. Richards JS (1994) Hormonal control of gene expression in the ovary. Endocr Rev 15:725-751
53. Richards JS, Hedin L, Caston L (1986) Differentiation of rat ovarian cells:evidence for functional luteinization. Endocrinology 118:1660-1668
54. Oonk RB, Beattie WG, Richards JS (1989) Cyclic AMP dependent and -independent regulation of cholesterol side-chain cleavage P450 (P450scc) in rat ovarian granulosa cells and corpora lutea: cDNA and deduced amino acid sequence of rat P450scc. J Biol Chem 264:21934-21942
55. Engelberg-Kulka, H, Amitai, S, Kolodkin-Gal, I, and Hazan, R (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2:e135.
56. Schwartz LM, Smith SW, Jones M, Osborne BA (1993) Do all programmed cell deaths occur via apoptosis. Proceedings of the National Academy of Sciences 90:980.
57. Smith CC, Yellon DM (2011) Necroptosis, necrostatins and tissue injury. J Cell Mol Med 15: 1797-1806.
58. Kroemer G, Martin SJ (2005) Caspase-independent cell death. Nat Med 11:725-730.
59. Mizuho N, Noboru M, Susumu N, Mlyamoto H (2000) Species-specific Differences in Apoptotic Cell Localization in Granulosa and Theca Interna Cells during Follicular Atresia in Porcine and Bovine Ovaries. Journal of Reproduction and Development 46:147-156.
60.苟德明,李文鑫,黄健等.(1999)人绒毛促性腺激素α、β亚基cDNA的筛选与序列分析。中国生物化学与分子生物学学报.15：899-902。
61.李凤娥,熊远.(2001)卵泡刺激素基因研究概况。国外畜牧学猪与禽.2001：35-37,65-67。
62. Blum WF, Riegelbauer G, Gupta D (1985) Heterogeneity of Rat FSH by Chromatofocusing:Studies on in-Vitro Bioactivity of Pituitary FSH Forms and Effect of Neuraminidase treatment. Endocrine 105:17-27.
63. Gharid SD, Wierman ME, Shupnik MA, Chin WW (1990) Molecular Biology of the Pituitary Gonadotropins. Eedocr Rev 11:177-199.
64. Keith EL, Bautista FDM, Hirao Y (1999) Comparis on of protein synthesis patterns in mouse cumulus cells and granulosa cells:Effects of follicle-stimulating hormone and insulin on granulosa cell differentiation in vitro. Biology of Reproduction 61:482-492.
65. Ferasin L, Gabai G, et al (1997) Enhancement of FSH bioactivity in vivo using site-specific antisera. Journal of Endocrinology 152:355-363.
66. Kazuya M, Taisuke N, Harumi S, Kentaro T, Hitoshi O, Eimei S, Joh-E I (1999) Neuronal apoptosis inhibitory protein (NAIP) may enhance the survival of granulosa cells thus indirectly affecting oocyte survival. Molecular Reproduction and Development 54:103-111.
67. Chun SY, Eisenhauer KM, Minami S, Billig H, Perlas E, Hsueh AJ (1996) Hormonal regulation of apoptosis in early antral follicles:follicle-stimulating hormone as a major survival factor. Endocrinology 137:1447-1456.
68. Sasson R, Dantes A, Tajima K, msterdam A (2003) Novel genes modulated by FSH in normal and immortalized FSH-responsive cells:new insights into the mechanism of FSH action. FASEB J 17: 1256-1266.
69. Grieshaber NA, Ko C, Grieshaber SS, Ji I, Ji TH (2003) Follicle-stimulating hormone responsive cytoskeletal genes in rat granulosa cells:class I beta-tubulin, tropomyosin-4, and kinesin heavy chain. Endocrinology 144:29-39.
70. Tanaka M, Hennebold JD, Miyakoshi K, Teranishi T, Ueno K, Adashi EY (2003) The generation and characterization of an ovary-selective cDNA library. Mol Cell Endocrinol 202:67-69.
71. Ratoosh SL, Lifka J, Hedin L, Jahsen T, Richards JS (1987) Hormonal regulation of the synthesis and mRNA content of the regulatory subunit of cyclic AMP-dependent protein kinase type Ⅱ in cultured rat ovarian granulosa cells. J Biol Chem 262:7306-7313.
72. Oh DY, Wang L, Ahn RS, Park JY, Seong JY, Kwon HB (2003) Differential G protein coupling preference of mammalian and nonmammalian gonadotropin-releasing hormone receptors. Mol Cell Endocrinol 205:89-98.
73. Alliston TN, Maiyar AC, Buse P, Firestone GL, Richards JS (1997) Follicle stimulating hormone-regulated expression of serum/glucocorticoid inducible kinase in rat ovarian granulosa cells:a functional role for the Spl family in promoter activity. Mol Endocrinol 11:1934-1949.
74. Salvador LM, Flynn MP, Avila J, Reierstad S, Maizels ET, Alam H, Park Y, Scott JD, Carr DW, Hunzicker-Dunn M (2004) Neuronal microtubule-associated protein 2D is a dual a-kinase anchoring protein expressed in rat ovarian granulosa cells. J Biol Chem 279:27621-27632.
75. Russell DL, Doyle KM, Gonzales-Robayna I, Pipaon C, Richards JS (2003) Egr-1 induction in rat granulosa cells by follicle-stimulating hormone and luteinizing hormone:combinatorial regulation by transcription factors cyclic adenosine 3',5'-monophosphate regulatory element binding protein, serum response factor, spl, and early growth response factor-1. Mol Endocrinol 17:520-533.
76. Little TH, Zhang Y, Matulis CK, Week J, Zhang Z, Ramachandran A, Mayo KE, Radhakrishnan I (2006) Sequence-specific deoxyribonucleic acid (DNA) recognition by steroidogenic factor 1:a helix at the carboxy terminus of the DNA binding domain is necessary for complex stability. Mol Endocrinol 20:831-843.
77. Falender AE, Lanz R, Malenfant D, Belanger L, Richards JS (2003) Differential expression of steroidogenic factor-1 and FTF/LRH-1 in the rodent ovary. Endocrinology 144:3598-3610.
78. Yazawa T, Mizutani T, Yamada K, Kawata H, Sekiguchi T, Yoshino M, Kajitani T, Shou Z, Miyamoto K (2003) Involvement of cyclic adenosine 5'-monophosphate response element-binding protein, steroidogenic factor 1, and Dax-1 in the regulation of gonadotropin-inducible ovarian transcription factor 1 gene expression by follicle-stimulating hormone in ovarian granulosa cells. Endocrinology 144:1920-1930.
79. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913-922.
80. Covarrubias L, Hernandez-Garcia D, Schnabel D, Salas-Vidal E, Castro-Obregon S (2008) Function of reactive oxygen species during animal development:passive or active? Dev Biol 320:1-11.
81. Circu ML, Aw TY (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48:749-762.
82. Carmody RJ, Cotter TG (2001) Signalling apoptosis:a radical approach. Redox Rep 6:77-90.
83. Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M, Yodoi J (2002) Redox control of cell death. Antioxid Redox Signal 4:405-414.
84. Kwon YW, Masutani H, Nakamura H, Ishii Y, Yodoi J (2003) Redox regulation of cell growth and cell death. Biol Chem 384:991-996.
85. Circu ML, Aw TY (2008) Glutathione and apoptosis. Free Radic Res 42:689-706.
86. Matsuda-Minehata F, Goto Y, Inoue N, Sakamaki K, Chedrese PJ, Manabe N (2007) Anti-apoptotic activity of porcine cFLIP in ovarian granulosa cell lines. Mol Reprod Dev 74:1165-1170.
87. Cheng Y, Maeda A, Goto Y, Matsuda F, Miyano T, Inoue N, Sakamaki K, Manabe N (2008) Changes in expression and localization of X-linked inhibitor of apoptosis protein (XIAP) in follicular granulosa cells during atresia in porcine ovaries. J Reprod Dev 54:454-459.
88. Maeda A, Goto Y, Matsuda-Minehata F, Cheng Y, Inoue N, Manabe N (2007) Changes in expression of interleukin-6 receptors in granulosa cells during follicular atresia in pig ovaries. J Reprod Dev 53: 727-736.
89. Nakayama M, Manabe N, Inoue N, Matsui T, Miyamoto H (2003) Changes in the expression of tumor necrosis factor (TNF) alpha, TNFalpha receptor (TNFR) 2, and TNFR-associated factor 2 in granulosa cells during atresia in pig ovaries. Biol Reprod 68:530-535.
90. Matsui T, Manabe N, Goto Y, Inoue N, Nishihara S, Miyamoto H (2003) Expression and activity of Apafl and caspase-9 in granulosa cells during follicular atresia in pig ovaries. Reproduction.126: 113-120.
91. Hojo T, Al-Zi'abi MO, Komiyama J, Manabe N, Acosta TJ, Okuda K (2010) Expression and localization of cFLIP, an anti-apoptotic factor, in the bovine corpus luteum. J Reprod Dev 56: 230-235.
92. Inoue N, Maeda A, Matsuda-Minehata F, Fukuta K, Manabe N (2006) Expression and localization of Fas ligand and Fas during atresia in porcine ovarian follicles. J Reprod Dev 52:723-730.
93. Wajant H, Scheurich P (2001) Tumor necrosis factor receptor-associated factor (TRAF) 2 and its role in TNF signaling. Int J Biochem Cell Biol 33:19-32.
94. Zheng X, Boerboom D Carriere& PD (2009) Transforming growth factor-beta 1 inhibits luteinization and promotes apoptosis in bovine granulosa cells. Reproduction 137:969-977.
95. Yang MY, Rajamahendran R (2000) Morphological and Biochemical Identification of Apoptosis in Small, Medium, and Large Bovine Follicles and the Effects of Follicle-Stimulating Hormone and Insulin-Like Growth Factor-I on Spontaneous Apoptosis in Cultured Bovine Granulosa Cells. Biology of Reproduction 62:1209-1217.
96. Mani AM, Fenwick MA, Cheng Z, Sharma M.K., Singh D, Wathes, DC (2010) IGF1 induces up-regulation of steroidogenic and apoptotic regulatory genes via activation of phosphatidylinositol-dependent kinase/AKT in bovine granulosa cells. Reproduction 139:139-151.
97. Hu CL, Cowan RG, Harman RM, Quirk& SM (2004) Cell cycle progression and activation of Akt kinase are required for insulin-like growth factor I-mediated suppression of apoptosis in granulosa cells. Mol Endocrinol 18:326-338.
98. Ratts VS, Flaws JA, Kolp R, Sorenson CM, Tilly JL (1995) Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 136:3665-3668.
99. Tilly JL, Tilly KI, Kenton ML, Johnson AL (1995) Expression of members of the bcl-2 gene family in the immature rat ovary:equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology 136:232-241.
100. Kugu K, Ratts VS, Piquette GN, Tilly KI, Tao XJ, Martimbeau S, Aberdeen GW, Krajewski S, Reed JC, Pepe GJ, Albrecht ED, Tilly JL (1998) Analysis of apoptosis and expression of bcl-2 gene family members in the human and baboon ovary. Cell Death Differ 5:67-76.
101. Salvetti NR, Stangaferro ML, Palomar MM, Alfaro NS, Rey F, Gimeno EJ, Ortega HH (2010) Cell proliferation and survival mechanisms underlying the abnormal persistence of follicular cysts in bovines with cystic ovarian disease induced by ACTH. Anim Reprod Sci 122:98-110.
102. Quirk SM, Cowan RG, Harman RM (2006) The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle. Journal of Endocrinology 189:441-453.
103. Kayamori T, Kosaka N, Miyamoto A, Shimizu& T (2009) The differential pathways of bone morphogenetic protein (BMP)-4 and -7 in the suppression of the bovine granulosa cell apoptosis. Mol Cell Biochem 323:161-168.
104. Inoue N, Matsuda F, Goto Y, Manabe N (2011) Role of cell-death ligand-receptor system of granulosa cells in selective follicular atresia in porcine ovary. J Reprod Dev 57:169-175.
105. Grotowski W, Lecybyl R, Warenik-Szymankiewicz A, Trzeciak WH (1997) The role of apoptosis of granulosa cells in follicular atresia. Ginekol Pol 68:317-326.
106. Pan Z, Zhang J, Lin F, Ma X, Wang X, Liu, H (2012) Expression profiles of key candidate genes involved in steroidogenesis during follicular atresia in the pig ovary. Mol Biol Rep 39: 10823-10832.
107. Yu YS, Sui HS, Han ZB, Li W, Luo M.J, Tan JH (2004) Apoptosis in granulosa cells during follicular atresia:relationship with steroids and insulin-like growth factors. Cell Res 14:341-346.
108. Zhang C, Xia G, aTsang BK (2011) Interactions of thyroid hormone and FSH in the regulation of rat granulosa cell apoptosis. Front Biosci 3:1401-1413.
109. Garside SA, Harlow CR, Hillier SG, Fraser HM, Thomas FH (2010) Thrombospondin-1 inhibits angiogenesis and promotes follicular atresia in a novel in vitro angiogenesis assay. Endocrinology 151:1280-1289.
110. Parborell F, Abramovich D, Irusta G, aTesone M (2011) Angiopoietin 1 reduces rat follicular atresia mediated by apoptosis through the PI3K/Akt pathway. Mol Cell Endocrinol 343:79-87.
111. Lin F, Li R, Pan ZX, Zhou B, Yu deB, Wang XG, Ma XS, Han J, Shen M, Liu HL (2012) miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary. PLoS One 7:e38640.
112. Lin P, Yang Y, Li X, Chen F, Cui C, Hu L, Li Q, Liu W, Jin Y (2012) Endoplasmic reticulum stress is involved in granulosa cell apoptosis during follicular atresia in goat ovaries. Mol Reprod Dev 79: 423-432.
113. Sugimoto M, Kagawa N, Morita M, Kume S, Wongpanit K, Jin H, Manabe N (2010) Changes in the expression of decoy receptor 3 in granulosa cells during follicular atresia in porcine ovaries. J Reprod Dev 56:467-474.
114. Orimoto AM, Dumaresq-Doiron K, Jiang JY, Tanphaichitr N, Tsang BK, Carmona E (2008) Mammalian hyaluronidase induces ovarian granulosa cell apoptosis and is involved in follicular atresia. Endocrinology 149:5835-5847.
115. Maeda A, Inoue N, Matsuda-Minehata F, Goto Y, Cheng Y, aManabe N (2007) The role of interleukin-6 in the regulation of granulosa cell apoptosis during follicular atresia in pig ovaries. J Reprod Dev 53:481-490.
116. Zwain I, Amato P (2000) Clusterin protects granulosa cells from apoptotic cell death during follicular atresia. Exp Cell Res 257:101-110.
117. Alonso-Pozos I, Rosales-Torres AM, Avalos-Rodriguez A, Vergara-Onofre M, Rosado-Garcia A (2003) Mechanism of granulosa cell death during follicular atresia depends on follicular size. Theriogenology 60:1071-1081.
118. Xu JP, Li X, Mori E, Sato E, Saito S, Guo MW, Mori T (1997) Expression of Fas-Fas ligand system associated with atresia in murine ovary. Zygote 5:321-327.
119. Monniaux D, Huet C, Pisselet C, Mandon-Pepin B, Monget P (1998) Mechanism, regulation, and manipilations of follicular atresia. Contracept Fertil Sex 26:528-535.
120. Salvetti NR, Gimeno EJ, Lorente JA, Ortega HH (2004) Expression of cytoskeletal proteins in the follicular wall of induced ovarian cysts. Cells Tissues Organs 178:117-125.
121. Ortega HH, Salvetti NR, Muller LA, Amable P, Lorente JA, Barbeito CG, Gimeno EJ (2007) Characterization of Cytoskeletal Proteins in Follicular Structures of Cows with Cystic Ovarian Disease. Journal of Comparative Pathology 136:222-230.
122. Allworth AE, Albertini DF (1993) Meiotic Maturation in Cultured Bovine Oocytes Is Accompanied by Remodeling of the Cumulus Cell Cytoskeleton. Developmental Biology 158: 101-112.
123. Gilbert S, Loranger A, Daigle N, Marceau N (2001) Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J Cell Biol 154:763-773.
124. Ku NO, Soetikno RM, Omary MB (2003) Keratin mutation in transgenic mice predisposes to Fas but not TNF-induced apoptosis and massive liver injury. Hepatology 37:1006-1014.
125. Caulin C, Ware CF, Magin TM, Oshima& RG (2000) Keratin-dependent, epithelial resistance to tumor necrosis factor-induced apoptosis. J Cell Biol 149:17-22.
126. Oshima RG (2002) Apoptosis and keratin intermediate filaments. Cell Death Differ 9:486-492.
127. Gilbert S, Ruel A, Loranger A, Marceau N (2008) Switch in Fas-activated death signaling pathway as result of keratin 8/18-intermediate filament loss. Apoptosis 13:1479-1493.
128. Best CL, Pudney J, Welch WR, Burger N, Hill JA (1996) Localization and characterization of white blood cell populations within the human ovary throughout the menstrual cycle and menopause. Hum Reprod 11:790-797.
129. Takaya R, Fukaya T, Sasano H, Suzuki T, Tamura M, Yajima A (1997) Macrophages in normal cycling human ovaries; immunohistochemical localization and characterization. Hum Reprod 12: 1508-1512.
130. Van der Hoek KH, Maddocks S, Woodhouse CM, van Rooijen N, Robertson SA, Norman RJ (2000) Intrab.ursal injection of clodronate liposomes causes macrophage depletion and inhibits ovulation in the mouse ovary. Biol Reprod 62:1059-1066.
131. Turner EC, Hughes J, Wilson H, Clay M, Mylonas KJ, Kipari T, Duncan WC, Fraser HM (2011) Conditional ablation of macrophages disrupts ovarian vasculature. Reproduction 141:821-831.
132. Cohen PE, Zhu L, Pollard JW (1997) Absence of colony stimulating factor-1 in osteopetrotic (csfinop/csfinop) mice disrupts estrous cycles and ovulation. Biol Reprod 56:110-118.
133. Petrovska M, Dimitrov DG, Michael SD (1996) Quantitative changes in macrophage distribution in normal mouse ovary over the course of the estrous cycle examined with an image analysis system. Am J Reprod Immunol 36:175-183.
1. Fortune JE (1994) Ovarian follicular growth and development in mammals. Biol Reprod 50:225-232.
2. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection,dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
3. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, Ireland JJ, Roche JF (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64:839-848.
4. Hsueh AJ, Billig H, Tsafriri A (1994) Ovarian follicle atresia:a hormonally controlled apoptotic process. Endocr Rev 15:707-724.
5. Endo M, Kimura K, Kuwayama T, Monji Y, Iwata H (2012) Effect of estradiol during culture of bovine oocyte-granulosa cell complexes on the mitochondrial DNA copies of oocytes and telomere length of granulosa cells. Zygote 1-9.
6. Sharma I, Singh D (2012) Conjugated linoleic acids attenuate FSH-and IGF 1-stimulated cell proliferation; IGF1, GATA4, and aromatase expression; and estradiol-17beta production in buffalo granulosa cells involving PPARgamma, PTEN, and PI3K/Akt. Reproduction 144:373-383.
7. Quirk SM, Cowan RG, Harman RM (2006) The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle. Journal of Endocrinology 189:441-453.
8. Quirk SM, Cowan RG, Harman RM (2004) Progesterone Receptor and the Cell Cycle Modulate Apoptosis in Granulosa Cells. Endocrinology 145:5033-5043.
9. Peluso JJ, Liu X, Gawkowska A, Johnston-MacAnanny E (2009) Progesterone Activates a Progesterone Receptor Membrane Component 1-Dependent Mechanism That Promotes Human Granulosa/Luteal Cell Survival But Not Progesterone Secretion. Journal of Clinical Endocrinology & Metabolism 94:2644-2649.
10. McNatty KP, Baird DT, Bolton A, Chambers P, Corker CS, McLean H (1976) Concentration of oestrogens and androgens in human ovarian venous plasma and follicular fluid throughout the menstrual cycle. J Endocrinol 71:77-85.
11. Kaipia A, Hsueh& AJ (1997) Regulation of ovarian follicle atresia. Annu Rev Physiol 59:349-363.
12. Sowers MR, Wilson AL, Kardia SR, Chu J, McConnell DS (2006) CYP1A1 and CYP1B1 polymorphisms and their association with estradiol and estrogen metabolites in women who are premenopausal and perimenopausal. Am J Med 119:44-51.
13. Gonzales F (1988) The molecular biology of cytochrome P450s. Pharmacol Rev 40:243-288.
14. Guengerich FP (1994) Analysis and characterization of enzymes. In:Principles and methods of toxicology. Hayes AW (ed). Raven Press, New York, pp 1259-1313.
15. Guengerich FP (2008) Cytochrome p450 and chemical toxicology. Chem Res Toxicol 21:70-83.
16. Lamb DC, Lei L, Warrilow AQ Lepesheva GI, Mullins JG, Waterman MR, Kelly SL (2009) The first virally encoded cytochrome P450. Journal of Virology 83:8266-8269.
17. Roland S, Sigel A, Sigel H (2007) The Ubiquitous Roles of Cytochrome P450 Proteins:Metal Ions in Life Sciences. New York:Wiley.
18. Danielson PB (2002) The cytochrome P450 superfamily:biochemistry, evolution and drug metabolism in humans. Curr Drug Metab 3:561-597.
19. Hakkola J, PasanenM, Pelkonen O, Hukkanen J, Evisalmi S, Antilla S, Rane A, Mantyla M, Purkunen R, Saarikoski S, Tooming M, Raunio H (1997) Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis 18:391-397.
20. Huang ZQ, Fasco MJ, Figge HL, Keyomarsi K, Kaminsky LS (1996) Expression of cytochrome P450 in human breast tissue and tumors. Drug Metab Dispos 24:899-905.
21. Rieder CRM, Ramsden DB, Williams AC (1998) Cytochrome P4501B1 mRNA in the human central nervous system. J Clin Pathol Mol Pathol 51:138-142.
22. Shimada T, Hayes CL, Yamazaki H, Shantu A, Hecht SS, Guengerich FP, Sutter TR (1996) Activation of chemically diverse procarcinogen s by human cytochrome P-4501B1. Cancer Res 56: 2979-2984.
23. Sutter TR, Tang YM, Hayes CL, Wo YY, Jabs EW, Li X, Yin H, Cody CW, Greenlee WF (1994) Complete cDNA sequence of a human dioxininducible mRNA identi. es a new gene subfamily of cytochrome p450 that maps to chromosome 2. J Bio Chem 269:13092-13099.
24. Tang YM, Chen GF, Thompson PA, Lin D, Lang NP, Kadlubar FF (1999) Development of an antipeptide antibody that binds to the c-terminal region of human CYP1B1. Drug Metab Dispos 27: 274-280.
25. Vadlamuri SV, Glover DD, Turner T, Sarkar MA (1998) Regiospecic expression of cytochrome P4501A1 and 1B1 in human uterine tissue. Cancer Lett 122:143-150.
26. Iwanari M, Nakajima M, Kizu R, Hayakawa K, Yokoi T (2002) Induction of CYP1A1, CYP1A2, and CYP1B1 mRNAs by nitropolycyclic aromatic hydrocarbons in various human tissue-derived cells:chemical-, cytochrome P450 isoform-, and cell-specific differences. Arch Toxicol 76: 287-298.
27. Hankinson O (1995) The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 35:307-340.
28. Schmidt JV, Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Biol 12:55-89.
29. Hayes C, Spink D, Spink B, Cao J, Walker N, Sutter T (1996) Estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc Natl Acad Sci USA 193:9776-9781.
30. Spink DC, Spink BC, Cao JQ, et al (1997) Induction of cytochrome P450 1B1 and catechol estrogen metabolism in ACHN human renal adenocarcinoma cells. J Steroid Biochem Mol Biol 62:223-232.
31. Lee AJ, Cai MX, Thomas PE, Conney AH, Zhu BT (2003) Characterization of the oxidative metabolites of estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 144:3382-3398.
32. Shimada T, Hayes CL, Yamazaki H, et al (1996) Activation of chemically diverse procarcinogens by human cytochrome P450 1B1. Cancer Res 56:2979-2984.
33. Hakkola J, Pasanen M, Pelkonen O, et al (1997) Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis 18:391-397.
34. Tsuchiya Y, Nakajima M, Kyo S, Kanaya T, Inoue M, Yokoi T (2004) Human CYP1B1 is regulated by estradiol via estrogen receptor. Cancer Res 64:3119-3125.
35. Leung GS, Kawai M, Tai JK, Chen J, Bandiera SM, Chang TK (2009) Developmental expression and endocrine regulation of CYP1B1 in rat testis. Drug Metab Dispos 37:523-528.
36. Bhattacharyya KK, Brake PB, Eltom SE, Otto SA, Jefcoate CR (1995) Identification of a rat adrenal cytochrome P450 active in polycyclic hydrocarbon metabolism as rat CYP1B1. Demonstration of a unique tissue-specific pattern of hormonal and aryl hydrocarbon receptorlinked regulation. J Biol Chem 270:11595-11602.
37. Leung GS, Kawai M, Tai JK, Chen J, Bandiera SM, and Chang, TK (2009) Developmental expression and endocrine regulation of CYP1B1 in rat testis. Drug Metab Dispos 37:23-528.
38. Haider SG (2004) Cell biology of Leydig cells in the testis. Int Rev Cytol 233:181-241.
39. Lee AJ, Cai MX, Thomas PE, Conney AH, Zhu BT (2003) Characterization of the oxidative metabolites of 17beta-estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 144:3382-3398.
40. Suchar LA, Chang RL, Rosen RT, Lech J, Conney AH (1995) High performance liquid chromatography separation of hydroxylated estradiol metabolites:formation of estradiol metabolites by liver microsomes from male and female rats. J. Pharmacol. Exp. Ther 272:197-206.
41. Yang HP, Bosquet JG, Li Q, etc (2010) Common genetic variation in the sex hormone metabolic pathway and endometrial cancer risk. Arcinogenesis 31:827-833.
42. Spink DC, Hayes CL, Young NR, Christou M, Sutter TR, Jefcoate CR, Gierthy JF (1994) The effects of 2,3,7,8-tetrachlorodibenzo-pdioxin on estrogen metabolism in MCF-7 breast cancer cells: evidence for induction of a novel 17 β-estradiol 4-hydroxylase. J Steroid Biochem Mol Biol 51: 251-258.
43. Spink DC, Hayes CL, Young NR, Christou M, Sutter TR, Jefcoate CR, Gierthy JF (1994) The effects of 2,3,7,8-tetrachlorodibenzo-pdioxin on estrogen metabolism in MCF-7 breast cancer cells: evidence for induction of a novel 17 h-estradiol 4-hydroxylase. J. SteroidBiochem. Mol. Biol 51: 251-258.
44. Zhu BT, Conney AH (1998) Functional role of estrogen metabolism in target cells:review and perspectives. Carcinogenesis 19:1-27.
45. Zhu BT, Roy D, Liehr JG (1993) The carcinogenic activity of ethinyl estrogens is determined by both their hormonal characteristics and their conversion to catechol metabolites. Endocrinology 131: 577-583.
46. Li KM, Todorovic R, Devanesan P, Higginbotham S, Kofeler H, Ramanathan R, Gross ML, Rogan EG, Cavalieri EL (2004) Metabolism and DNA binding studies of 4-hydroxyestradiol and estradiol-3,4-quinone in vitro and in female ACI rat mammary gland in vivo. Carcinogenesis 25: 289-297.
47. Newbold RR, Liehr JG (2000) Induction of uterine adenocarcinoma in CD-I mice by catechol estrogens. Cancer Res 60:235-237.
48. Rogan EG, Badawi AF, Devanesan PD, Meza JL, Edney JA, West WW, Higginbotham SM, Cavalieri EL (2003) Relative imbalances in estrogen metabolism and conjugation in breast tissue of women with carcinoma:potential biomarkers of susceptibility to cancer. Carcinogenesis 24:697-702.
49. Hiraku Y, Yamashita N, Nishiguchi M, Kawanishi S, (2001) Catechol estrogens induce oxidative DNA damage and estradiol enhances cell proliferation. Int. J. Cancer 92:333-337.
50. Thibodeau PA, Paquette B (1999) DNA damage induced by catecholestrogens in the presence of copper (II):generation of reactive oxygen species and enhancement by NADH. Free Radical Biol. Med 27:1367-1377.
51. Chen ZH, Na HK., Hurh YJ, Surh YJ (2005) 4-Hydroxyestradiol induces oxidative stress and apoptosis in human mammary epithelial cells:possible protection by NF-kappaB and ERK/MAPK. Toxicol Appl Pharmacol 208:46-56.
52. Liehr JG, Roy D, (1990) Free radical generation by redox cycling of estrogens. Free Radical Biol. Med 8:415-423.
53. Liehr, J.G., (1990). Genotoxic effects of estrogens. Mutat. Res 238:269-276.
54. Samuni AM, Chuang EY, Krishna MC, Stein W, DeGraff W, Russo A, Mitchell JB (2003) Semiquinone radical intermediate in catecholic estrogen-mediated cytotoxicity and mutagenesis: chemoprevention strategies with antioxidants. Proc. Natl. Acad. Sci. U.S.A 100:5390-5395.
55. Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D (2000) Estrogens as endogenous genotoxic agents DNA adducts and mutations. J. Natl. Cancer Inst Monogr.27:75-93.
56. Hayes CL, Spink DC, Spink BC, Cao JQ, Walker NJ, Sutter TR (1996) 17h-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A 93:9776-9781.
57. Murray GI, Taylor MC, McFadyen MC, McKay JA, Greenlee WF, Burke MD, Melvin WT, (1997) Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res 57:3026-3031.
1. Kaipia A, Hsueh AJ (1997) Regulation of ovarian follicle atresia. Annu Rev Physiol 59:349-363.
2. Jang JH, Surh, YJ (2003) Protective effect of resveratrol on [beta]-amyloid induced oxidative PC 12 cell death. Free Radical Biology and Medicine 34:1100-1110.
3. Asahara S, Sato A, Aljonaid AA, Maruo T (2003) Thyroid hormone synergizes with follicle stimulating hormone to inhibit apoptosis in porcine granulosa cells selectively from small follicles. Kobe J Med Sci 49:107-116.
4. Yang MY, Rajamahendran R (2000) Morphological and biochemical identification of apoptosis in small, medium, and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured bovine granulosa cells. Biology of Reproduction 62:1209-1217.
5. Fortune JE (1994) Ovarian follicular growth and development in mammals. Biol Reprod 50:225-232.
6. Lunenfeld B, Insler V (1993) Follicular development and its control. Gynecological Endocrinology 7: 285-291.
7. Vander AJ, Sherman JH, Luciano DS (1994) Human Physiology:The Mechanisms of Body Function. New York:McGraw-Hill:661-692.
8. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
9. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, Ireland JJ, Roche JF (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64:839-848.
10. Satosi K, Motoaki U (2004) Histological analysis of the'critical point' in follicular development in mice. Reproductive Medicine and Biology 3:141-145.
11. Manabe, N (2008) Regulation of granulosa cell apoptosis by death ligand-receptor signaling. Animal Science Journal 79:1-10.
12. Sai T, Goto Y, Yoshioka R, Maeda A, Matsuda F, Sugimoto M, Wongpanit K, Jin H. Z Li, JY, Manabe N (2011) Bid and Bax are involved in granulosa cell apoptosis. J Repord Dev 57:421-427.
13. Smith CC, Yellon DM (2011) Necroptosis, necrostatins and tissue injury. J Cell Mol Med 15: 1797-1806.
14. Kroemer, G, and Martin, SJ (2005) Caspase-independent cell death. Nat Med 11:725-730.
15. Wajant H (2002) The Fas signaling pathway:more than a paradigm. Science's STKE 296:1635.
16. Berry D (2007) Molecular animation of cell death mediated by the Fas pathway. Science's STK trl.
17. Borutaite V (2010) Mitochondria as decision-makers in cell death. Environmental and molecular mutagenesis 51:406-416.
18. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770-776.
19. McStay G, Salvesen G, Green D (2007) Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death & Differentiation 15:322-331.
20. Harris CA, Johnson Jr EM (2001) BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. Journal of Biological Chemistry 276: 37754-37760.
21. Hunzicker-Dunn M, Maizels ET (2006) FSH signaling pathways in immature granulosa cells that regulate target gene expression:branching out from protein kinase A. Cell Signal 18:1351-1359.
22. Manabe N, Imai Y, Kimura Y, Myoumoto A, Sugimoto M, Miyamoto H, Okamura Y, Fukumoto M (1996) Ca 2+/Mg 2+-Dependent endonuclease but not Ca 2+-Dependent, Mg 2+-Dependent or cation-independent endonuclease is involved in granulosa cell apoptosis of pig atretic follicles. Journal of Reproduction and Development 42:247-253.
23. Asahara S, Sato A, Aljonaid AA, Maruo T (2003) Thyroid hormone synergizes with follicle stimulating hormone to inhibit apoptosis in porcine granulosa cells selectively from small follicles. Kobe J Med Sci 49:107-116.
24. Yang MY, Rajamahendran R (2000) Morphological and biochemical identification of apoptosis in small, medium, and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured bovine granulosa cells. Biology of Reproduction 62:1209-1217.
1. Fortune JE (1994) Ovarian follicular growth and development in mammals. Biol Reprod 50:225-232.
2. Lunenfeld B, Insler V (1993) Follicular development and its control. Gynecological Endocrinology 7: 285-291.
3. Vander AJ, Sherman JH, Luciano DS (1994) Human Physiology:The Mechanisms of Body Function New York:McGraw-Hill:661-692.
4. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection, dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
5. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, Ireland JJ, Roche JF (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64:839-848.
6. Guengerich FP (2008) Cytochrome p450 and chemical toxicology. Chem. Res. Toxicol 21:70-83.
7. Suchar LA, Chang RL, Rosen RT, Lech J, Conney AH (1995) High performance liquid chromatography separation of hydroxylated estradiol metabolites:formation of estradiol metabolites by liver microsomes from male and female rats. J. Pharmacol. Exp. Ther 272:197-206.
8. John L Rinn, Joel S Rozowsky, Ian J Laurenzi, Petur H. Petersen, Kaiyong Zou, Weimin Zhong, Mark Gerstein, Michael Snyder (2004) Major Molecular Differences between mammalian sexes are involved in drug metabolism and Renal Function. Developmental Cell 6:791-800.
9. Campbell SJ, Henderson CJ, Anthony DC, Davidson D, Clark AJ, Wolf CR (2005) The murine Cyp1a1 gene is expressed in a restricted spatial and temporal pattern during embryonic development. J Biol Chem 280:5828-5835.
10. Dorrington JH, Bendell JJ, Khan SA (1993) Interactions between FSH, estradiol-17 beta and transforming growth factor-beta regulate growth and differentiation in the rat gonad. J Steroid Biochem Mol Biol 44:441-447.
11. Richards JS, Jonassen JA, Rolfes AI, Kersey K, Reichert LE (1979) Adenosine 3',5'-monophosphate, luteinizing hormone receptor, and progesterone during granulosa cell differentiation:effects of estradiol and follicle-stimulating hormone. Endocrinology 104:765-773.
12. Hsueh AJ, Billig H, Tsafriri A (1994) Ovarian follicle atresia:a hormonally controlled apoptotic process. Endocr Rev 15:707-724.
13. Nimz M, Spitschak M, Furbass R, Vanselow J (2010) The pre-ovulatory luteinizing hormone surge is followed by down-regulation of CYP19A1, HSD3B1, and CYP17A1 and chromatin condensation of the corresponding promoters in bovine follicles. Mol Reprod Dev 77:1040-1048.
14. Lv L, Jimenez-Krassel F, Sen A, Bettegowda A, Mondal M, Folger JK, Lee KB, Ireland JJ, Smith GW (2009) Evidence supporting a role for cocaine-and amphetamine-regulated transcript (CARTPT) in control of granulosa cell estradiol production associated with dominant follicle selection in cattle. Biol Reprod 81:580-586.
15. Manabe N, Imai Y, Kimura Y, Myoumoto A (1996) Ca2+/Mg2+-Dependent endonuclease but not Ca2+-Dependent, Mg2+-Dependent or cation-independent endonuclease is involved in granulosa cell apoptosis of pig atretic follicles. Journal of Reproduction and Development 42:247-253.
16. Spink DC, Hayes CL, Young NR, Christou M, Sutter TR, Jefcoate CR, Gierthy JF (1994) The effects of 2,3,7,8-tetrachlorodibenzo-pdioxin on estrogen metabolism in MCF-7 breast cancer cells: evidence for induction of a novel 17 β-estradiol 4-hydroxylase. J Steroid Biochem Mol Biol 51: 251-258.
17. Chen ZH, Na HK, Hurh YJ, Surh YJ (2005) 4-Hydroxyestradiol induces oxidative stress and apoptosis in human mammary epithelial cells:possible protection by NF-kappaB and ERK/MAPK. Toxicol Appl Pharmacol 208:46-56.
18. Ollinger K, Buffinton GD, Ernster L, Cadenas E (1990) Effect of superoxide dismutase on the autoxidation of substituted hydro-and semi-naphthoquinones. Chem Biol Interact 73:53-76.
19. Samuni AM, Chuang EY, Krishna MC, Stein W, DeGraff W, Russo A, Mitchell JB (2003) Semiquinone radical intermediate in catecholic estrogen-mediated cytotoxicity and mutagenesis: chemoprevention strategies with antioxidants. Proc Natl Acad Sci USA 100:5390-5395.
20. Liehr JG, Roy D (1990) Free radical generation by redox cycling of estrogens. Free Radic Biol Med 8:415-423.
21. Shen M, Lin F, Zhang J, Tang Y, Chen WK, Liu H (2012) Involvement of the up-regulated FoxOl expression in follicular granulosa cell apoptosis induced by oxidative stress. J Biol Chem 287: 25727-25740.
22. Denison MS, Nagy SR (2003) Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43:309-334.
23. Bussmann UA, Baranao JL (2006) Regulation of aryl hydrocarbon receptor expression in rat granulosa cells. Biol Reprod 75:360-369.
24. Jacob A, Hartz AM, Potin S, Coumoul X, Yousif S, Scherrmann JM, Bauer B, Decleves X (2011) Aryl hydrocarbon receptor-dependent upregulation of Cyplbl by TCDD and diesel exhaust particles in rat brain microvessels. Fluids Barriers CNS 8:23.
25. Heim MH (1999) The Jak-STAT pathway:cytokine signalling from the receptor to the nucleus. J Recept Signal Transduct Res 19:75-120.
26. Durbin JE, Hackenmiller R, Simon MC, Levy DE (1996) Targeted disruption of the mouse Statl gene results in compromised innate immunity to viral disease. Cell 3:443-450.
27. Meraz MA, White JM, Sheehan KC, etc (1996) Targeted disruption of the Statl gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 3:431-442.
28. Ihle JN, Witthuhn BA, Quelle FW, Yamamoto K, Thierfelder WE, Kreider B, Silvennoinen O (1994) Signaling by the cytokine receptor superfamily:JAKs and STATs. Trends Biochem Sci 5:222-227.
29. Anastasis S, Tiziano MS, Bhawanjit KB, Yoshinobu N, Miho M, Richard AK (2001) Induction of Apoptosis and Fas Receptor/Fas Ligand Expression by Ischemia/Reperfusion in Cardiac Myocytes Requires Serine 727 of the STAT-1 Transcription Factor but Not Tyrosine 701. The Journal Of Biological Chemisitry.276:28340-28347.
30. Stephanou A, Scarabelli TM, Brar BK, Nakanishi Y, Matsumura M, Knight RA, Latchman DS (2001) Induction of apoptosis and Fas receptor/Fas ligand expression by ischemia/reperfusion in cardiac myocytes requires Serine 727 of the STAT-1 transcription factor but not tyrosine 701. J Biol Chem 276:28340-28347.
31. Goh KC, Haque SJ, Williams BR (1999) p38 MAP kinase is required for Statl Serine phosphorylation and transcriptional activation induced by interferons. EMBO J 18:5601-5608.
32. Stoiber D, Kovarik P, Cohney S, Johnston JA, Steinlein P, Decker T (1999) Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-gamma. J Immunol 163:2640-2647.
33. Russell DL, Richards JS (1999) Differentiation-dependent prolactin responsiveness and stat (signal transducers and activators of transcription) signaling in rat ovarian cells. Mol Endocrinol 13: 2049-2064.
34. Lee T, Kim SJ, Sumpio BE (2003) Role of PP2A in the regulation of p38 MAPK activation in bovine aortic endothelial cells exposed to cyclic strain. J Cell Physiol 194:349-355.
35. Strack S, Cribbs JT, Gomez L (2004) Critical role for protein phosphatase 2A heterotrimers in mammalian cell survival. J Biol Chem 279:47732-47739.
36. Xu Z, Williams BR (2000) The B56alpha regulatory subunit of protein phosphatase 2A is a target for regulation by double-stranded RNAdependent protein kinase PKR. Mol Cell Biol 20:5285-5299.
37. Liu Q, Hofmann PA (2004) Protein phosphatase 2A-mediated cross-talk between p38 MAPK and ERK in apoptosis of cardiac myocytes. Am J Physiol Heart Circ Physiol 286:2204-2212.
38. Alvarado-Kristensson M, Andersson T (2005) Protein phosphatase 2A regulates apoptosis in neutrophils by dephosphorylating both p38 MAPK and its substrate caspase 3. J Biol Chem 280: 6238-6244.
39. Baharians Z, Schonthal AH (1998) Autoregulation of protein phosphatase type 2A expression. J Biol Chem 273:19019-19024.
40. Levallet G, Levallet J, and Bonnamy PJ (2008) FSH-induced phosphoprotein phosphatase 2A-mediated deactivation of particulate phosphodiesterase-4 activities is abolished after alteration in proteoglycan synthesis in immature rat Sertoli cells. J Endocrinol 197:45-54.
41. Woetmann A, Nielsen M, Christensen ST, Brockdorff J, Kaltoft K, Engel AM, Skov S, Brender C, Geisle C, Svejgaard A, et al (1999) Inhibition of protein phosphatase 2A induces Serine/threonine phosphorylation, subcellular redistribution, and functional inhibition of STAT3. Proc Natl Acad Sci USA 96:10620-10625.
42. Lutticken C, Coffer P, Yuan J, Schwartz C, Caldehoven E, Schindler C, Kruijer W, Heinrich, PC, Horn F (1995) Interleukin-6-induced Serine phosphorylation of transcription factor APRF:evidence for a role in interleukin-6 target gene induction. FEBS Lett 360:137-143.
43. Brockdorff J, Nielsen M, Dobson P, Geisler C, Ropke C, Svejgaard A, Odum, N (1997) Interleukin 2 induces a transient downregulation of protein phosphatase 1 and 2A activity in human T cells. Tissue Antigens 49:228-235.
44. Grillo MA, Colombatto S (2005) S-adenosylmethionine and protein methylation. Amino Acids 28: 357-362.
45. Chen J, Martin BL, Brautigan DL (1992) Regulation of protein Serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 257:1261-1264.
46. Chen J, Parsons S, Brautigan DL (1994) Tyrosine phosphorylation of protein phosphatase 2A in response to growth stimulation and v-src transformation of fibroblasts. J Biol Chem 269: 7957-7962.
47. Brautigan DL (1995) Flicking the switches:phosphorylation of Serine/threonine protein phosphatases. Semin Cancer Biol 6:211-217.
48. Janssens V, Goris, J (2001) Protein phosphatase 2A:a highly regulated family of Serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353:417-439.
2. Kimura F, Bonomi LM, Schneyer AL (2011) Follistatin regulates germ cell nest breakdown and primordial follicle formation. Endocrinology 152:697-706.
3.芮荣,钱菊汾.(1998)卵泡发育及其控制。草食家畜.16-22。
4.彭宇洪,庄广伦,周灿权.(2006)小鼠体外发育卵母细胞生长分化因子-9基因表达。南方医科大学学报.1341-1345。
5. Kobayashi N, Orisaka M, Cao M, Kotsuji F, Leader A, Sakuragi N, Tsang BK (2009) Growth differentiation factor-9 mediates follicle-stimulating hormone-thyroid hormone interaction in the regulation of rat preantral follicular development. Endocrinology 150:5566-5574.
6. Zerek-Melen G, Lewinski A, Pawlikowski M, Sewerynek E, Kunert-Radek J (1987) Influence of somatostatin and epidermal growth factor (EGF) on the proliferation of follicular cells in the organ-cultured rat thyroid. Res Exp Med (Berl) 187:415-421.
7. Hirshfield AN (1991) Development of follicles in the mammalian ovary. Int Rev Cytol 124:43-101.
8. Richards JS, Ireland JJ, Rao MC, Bernath GA, Midgley AR, Reichert Jr LE (1976) Ovarian follicular development in the rat:hormone receptor regulation by estradiol, follicle stimulating hormone and luteinizing hormone. Endocrinology 99:1562-1570.
9. Chada M, Prusa R, Bronsky J, Pechova M, Kotaska K, Lisa L (2003) Inhibin B follicle stimulating hormone, luteinizing hormone, and estradiol and their relationship to the regulation of follicle development in girls during childhood and puberty. Physiol Res 52:341-346.
10.王海滨,谢辉蓉,夏国良.(2002)哺乳动物卵泡早期发育调控的研究进展。国外畜牧科技.29：37-42。
11. Guo CJ, Pan Q, Li DG, Sun H, Liu BW (2009) miR-15b and miR-16 are implicated in activation of the rat hepatic stellate cell:An essential role for apoptosis. J Hepatol 50:766-778.
12. Roberts AJ, Skinner MK (1990) Hormonal regulation of thecal cell function during antral follicle development in bovine ovaries. Endocrinology 127:2907-2917.
13. Mihm M, Bleach ECL (2003) Endocrine regulation of ovarian antral follicle development in cattle. Anim Reprod Sci 78:217-237.
14. Mott JL, Kobayashi S, Bronk SF, Gores GJ (2007) mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26:6133-6140.
15. Matsuda-Minehata F, Inoue N, Goto Y, Manabe N (2006) The regulation of ovarian granulosa cell death by pro-and anti-apoptotic molecules. J Reprod Dev 52:695-705.
16. Baerwald AR, Adams GP, Pierson RA (2003) Characterization of ovarian follicular wave dynamics in women. Biol Reprod 69:1023-1031.
17. Mihm M, Good TE, Ireland JL, Ireland JJ, Knight PG, Roche JF (1997) Decline in serum follicle-stimulating hormone concentrations alters key intrafollicular growth factors involved in selection of the dominant follicle in heifers. Biol Reprod 57:1328-1337.
18. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
19. Richards JS, Hedin L (1988) Molecular aspects of hormone action in ovarian follicular development, ovulation, and luteinization. Annu Rev Physiol 50:441-463.
20. Fortune JE (1994) Ovarian follicular growth and development in mammals. Biol Reprod 50: 225-232.
21. Greenwald GS, Roy SK (1994) Follicular development and its control. In:Knobil E, Neill JD (eds.). The Physiology of Reproduction 1:629-724.
22. Vander AJ, Sherman JH, Luciano DS (1994) Reproduction In:Prancan KM, Bradley JW (eds.). Human Physiology:The Mechanisms of Body Function. New York:McGraw-Hill:661-692.
23. Donath J, Nishino Y, Schulz T, Michna H (2000) The antiovulatory potential of progesterone antagonists correlates with a down-regulation of progesterone receptor in hypothalamus, pituitary and ovary. AnatAnz 182:143-145.
24. Richards JS, Ireland JJ, Rao MC, Bernath GA, Midgley AR, Reichert Jr LE (1976) Ovarian follicular development in the rat:hormone receptor regulation by estradiol, follicle stimulating hormone and luteinizing hormone. Endocrinology 99:1562-1570.
25. Chada M, Prusa R, Bronsky J, Pechova M, Kotaska K, Lisa L (2003) Inhibin B, follicle stimulating hormone, luteinizing hormone, and estradiol and their relationship to the regulation of follicle development in girls during childhood and puberty. Physiol Res 52:341-346.
1. Lebedeva I, Denisenko Y, Lebedev V.A, Kuzmina TI (1998) Prolactin in follicular fluid and intracellular store calcium in follicular cells are related to morphological signs of ovarian follicle atresia in cows:work in progress. Theriogenology 49:509-519.
2. Bjersing L (1967) On the ultrastructure of follicles and isolated follicular granulosa cells of porcine ovary. Cell and Tissue Research 82:173-186.
3. Bhardwaj JK, Sharma RK (2011) Changes in Trace Elements during Follicular Atresia in Goat (Capra hircus) Ovary. Biol Trace Elem Res 140:291-298.
4. Oakberg EF (1979) Follicular growth and atresia in the mouse. In Vitro 15:41-49.
5. Manabe N, Matsuda-Minehata F, Goto Y, Maeda A, Cheng Y, Nakagawa S, Inoue N, Wongpanit K, Jin H, Gonda H, Li J (2008) Role of cell death ligand and receptor system on regulation of follicular atresia in pig ovaries. Reprod Domest Anim 43:268-272.
6. Sai T, Goto Y, Yoshioka R, Maeda A, Matsuda F, Sugimoto M, Wongpanit K, Jin HZ, Li JY, Manabe N (2011) Bid and Bax are involved in granulosa cell apoptosis during follicular atresia in porcine ovaries. J Reprod Dev 57:421-427.
7. Yu YS, Sui HS, Han ZB, Li Wei, Luo MJ, Tan JH (2004) Apoptosis in granulosa cells during follicular atresia:relationship with steroids and insulin-like growth factors. Cell Res 14:341-6
8. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection, dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
9. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, Ireland JJ, Roche JF (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64:839-848.
10. Vaskivuo TE, Tapanainen JS (2003) Apoptosis in the human ovary. Reprod Biomed Online 6:24-35.
11. Manabe N, Goto Y, Matsuda-Minehata F, Inoue N, Maeda A, Sakamaki K, Miyano T (2004) Regulation mechanism of selective atresia in porcine follicles:regulation of granulosa cell apoptosis during atresia. J Reprod Dev 50:493-514.
12. Hirshfield AN (1991) Development of follicles in the mammalian ovary. Int Rev Cytol 124:43-101.
13. Fortune, JE (2003) The early stages of follicular development:activation of primordial follicles and growth of preantral follicles. Animal Reproduction Science 78:135-163
14. Oktem O, Urman B (2010) Understanding follicle growth in vivo. Hum Reprod 25:2944-2954.
15. Rajakoski E (1960) The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical, end left-right variations. Acta Endocrinol Suppl 34:61-68.
16. Marion GB, Gier HT, Choudary JB (1968) Micromorphology of the bovine ovarian follicular system. J Anim Sci 27:451-465.
17. Irving-Rodgers H, Wezel I, Mussard M, Kinder J, Rodgers R (2001) Atresia revisited:two basic patterns of atresia of bovine antral follicles. Reproduction 122:761-775.
18. Cheng Y, Inoue N, Matsuda-Minehata F, Goto Y, Maeda A, Manabe N (2005) Changes in expression and localization of connexin 43 mRNA and protein in porcine ovary granulosa cells during follicular atresia. J Reprod Dev 51:627-637.
19. Bosu WT, Perez GI, Kujjo LL (1996) Natural and endotoxin-induced atresia of preantral and early antral follicles is characterized by DNA internucleosomal cleavage. Mol Reprod Dev 44:352-359.
20. Manabe N, Matsuda-Minehata F, Goto Y, Maeda A, Cheng Y, Nakagawa S, Inoue N, Wongpanit K, Jin H, Gonda H, Li J (2008) Role of cell death ligand and receptor system on regulation of follicular atresia in pig ovaries. Reprod Domest Anim 43:268-272.
21. Sai T, Goto Y, Yoshioka R, Maeda A, Matsuda F, Sugimoto M, Wongpanit K, Jin HZ, Li JY, Manabe N (2011) Bid and Bax are involved in granulosa cell apoptosis during follicular atresia in porcine ovaries. J Reprod Dev 57:421-427.
22. Kim JM, Boone DL, Auyeung A, Tsang BK (1998) Granulosa cell apoptosis induced at the penultimate stage of follicular development is associated with increased levels of Fas and Fas ligand in the rat ovary. Biol Reprod 58:1170-1176.
23. D'Haeseleer M, Cocquyt G, Van Cruchten S, Simoens P, Broeck WV (2006) Cellspecific localisation of apoptosis in the bovine ovary at different stages of the oestrous cycle. Theriogenology 65:757-772.
24. Peluffo MC, Stouffer RL, Tesone M (2007) Activity and expression of different members of the caspase family in the rat corpus luteum during pregnancy and postpartum. Am J Physiol Endocrinol Metab 293:1215-1223.
25. Tilly, JL (1996) Apoptosis and ovarian function. Rev Reprod 1:162-172.
26. Chun SY, Hsueh AJ (1998) Paracrine mechanisms of ovarian follicle apoptosis. J Reprod Immunol 39:63-75.
27. Johnson AL (2003) Intracellular mechanisms regulating cell survival in ovarian follicles. Animal Reproduction Science 78:185-201.
28. Basini G, Mainardi GL, Bussolati S, Tamanini C (2002) Steroidogenesis, proliferation and apoptosis in bovine granulosa cells:role of tumour necrosis factor; and its possible signalling mechanisms. Reproduction. Fertility and Development.14:141-150.
29. Sasson R, Winder N, Kees S, Amsterdam A (2002) Induction of apoptosis in granulosa cells by TNF[alpha] and its attenuation by glucocorticoids involve modulation of Bcl-2. Biochemical and Biophysical Research Communications 294:51-59.
30. Porter DA, Vickers SL, Cowan RG, Huber SC, Quirk SM (2000) Expression and function of Fas antigen vary in bovine granulosa and theca cells during ovarian follicular development and atresia. Biol Reprod 62:62-66.
31. Johnson AL, Ratajczak C, Haugen MJ, Liu HK, Woods DC (2007) Tumor necrosis factor-related apoptosis inducing ligand expression and activity in hen granulosa cells. Reproduction 133: 609-616.
32. Jaaskelainen M, Kyronlahti A, Anttonen M, Nishi Y, Yanase T, Secchiero P, Zauli G, Tapanainen JS, Heikinheimo M, Vaskivuo TE (2009) TRAIL pathway components and their putative role in granulosa cell apoptosis in the human ovary. Differentiation 4:369-376.
33. Quirk SM, Harman RM, Cowan RG (2000) Regulation of Fas Antigen (Fas, CD95)-Mediated Apoptosis of Bovine Granulosa Cells by Serum and Growth Factors. Biology of Reproduction 63: 1278-1284.
34. Vickers SL, Cowan RG, Harman RM, Porter DA, Quirk SM (2000) Expression and Activity of the Fas Antigen in Bovine Ovarian Follicle Cells. Biology of Reproduction 62:54-61.
35. Hussein MR (2005) Apoptosis in the ovary:molecular mechanisms. Human Reproduction Update 11:162-178.
36. Hennebold JD (2010) Preventing Granulosa Cell Apoptosis Through the Action of a Single MicroRNA. Biology of Reproduction 83:165-167.
37. Carletti MZ, Fiedler SD, Christenson LK (2010) MicroRNA 21 Blocks Apoptosis in Mouse Periovulatory Granulosa Cells. Biology of Reproduction 83:286-295.
38. Wajant H (2002) The Fas signaling pathway:more than a paradigm. Science's STKE 296:1635.
39. Berry D (2007) Molecular animation of cell death mediated by the Fas pathway. Science's STKE:trl.
40. Dlamini Z, Mbita Z, Zungu M (2004) Genealogy expression, and molecular mechanisms in apoptosis. Pharmacol Ther 101:1-15.
41. Hirshfield AN (1991) Development of follicles in the mammalian ovary. Int Rev Cytol 124:43-101
42. Pederson T (1970) Follicular kinetics in the ovary of the cyclic mouse. Acta Endocrinol (Copenh) 64: 304-323
43. Richards JS (1978) Hormonal control of follicular growth and maturation in mammals. In:Jones RE (ed) The Vertebrate Ovary:Comparative Biology and Evolution. Plenum Press, New York: 331-360.
44. Richards JS (1980) Maturation of ovarian follicles:actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol Rev.60:51-89
45. Richards JS (1975) Estradiol receptor content in rat granulose cells during follicular development. Endocrinology 97:1174-1184
46. Rao MC, Midgley Jr AR, Richards JS (1978) Hormonal regulation of ovarian cellular proliferation. Cell 14:71-78
47. Richards JS, Midgley Jr AR (1976) Protein hormone action:a key to understanding ovarian follicular and luteal cell development. Biol Reprod 14:82-94
48. Mason AJ, Hayflick JS, Zoeller RT, Young WS, Phillips HS, Nikolics K, Seeburg PH (1986) A deletion truncating the gonadotropin-releasing hormone gene is responsible for hypogonadism in the hpg mouse. Science 234:1366-1371
49. Mason AJ, Pitts SL, Nikolics K, Szonyi E, Wilcox JN, Seeburg PH, Stewart TA (1986) The hypogonadal mouse:reproductive functions restored by gene therapy. Science 234:1372-1378
50. Kumar TR, Wang Y, Lu N, Matzuk MM (1997) Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 15:201-204
51. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90:11162-11166
52. Richards JS (1994) Hormonal control of gene expression in the ovary. Endocr Rev 15:725-751
53. Richards JS, Hedin L, Caston L (1986) Differentiation of rat ovarian cells:evidence for functional luteinization. Endocrinology 118:1660-1668
54. Oonk RB, Beattie WG, Richards JS (1989) Cyclic AMP dependent and -independent regulation of cholesterol side-chain cleavage P450 (P450scc) in rat ovarian granulosa cells and corpora lutea: cDNA and deduced amino acid sequence of rat P450scc. J Biol Chem 264:21934-21942
55. Engelberg-Kulka, H, Amitai, S, Kolodkin-Gal, I, and Hazan, R (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2:e135.
56. Schwartz LM, Smith SW, Jones M, Osborne BA (1993) Do all programmed cell deaths occur via apoptosis. Proceedings of the National Academy of Sciences 90:980.
57. Smith CC, Yellon DM (2011) Necroptosis, necrostatins and tissue injury. J Cell Mol Med 15: 1797-1806.
58. Kroemer G, Martin SJ (2005) Caspase-independent cell death. Nat Med 11:725-730.
59. Mizuho N, Noboru M, Susumu N, Mlyamoto H (2000) Species-specific Differences in Apoptotic Cell Localization in Granulosa and Theca Interna Cells during Follicular Atresia in Porcine and Bovine Ovaries. Journal of Reproduction and Development 46:147-156.
60.苟德明,李文鑫,黄健等.(1999)人绒毛促性腺激素α、β亚基cDNA的筛选与序列分析。中国生物化学与分子生物学学报.15：899-902。
61.李凤娥,熊远.(2001)卵泡刺激素基因研究概况。国外畜牧学猪与禽.2001：35-37,65-67。
62. Blum WF, Riegelbauer G, Gupta D (1985) Heterogeneity of Rat FSH by Chromatofocusing:Studies on in-Vitro Bioactivity of Pituitary FSH Forms and Effect of Neuraminidase treatment. Endocrine 105:17-27.
63. Gharid SD, Wierman ME, Shupnik MA, Chin WW (1990) Molecular Biology of the Pituitary Gonadotropins. Eedocr Rev 11:177-199.
64. Keith EL, Bautista FDM, Hirao Y (1999) Comparis on of protein synthesis patterns in mouse cumulus cells and granulosa cells:Effects of follicle-stimulating hormone and insulin on granulosa cell differentiation in vitro. Biology of Reproduction 61:482-492.
65. Ferasin L, Gabai G, et al (1997) Enhancement of FSH bioactivity in vivo using site-specific antisera. Journal of Endocrinology 152:355-363.
66. Kazuya M, Taisuke N, Harumi S, Kentaro T, Hitoshi O, Eimei S, Joh-E I (1999) Neuronal apoptosis inhibitory protein (NAIP) may enhance the survival of granulosa cells thus indirectly affecting oocyte survival. Molecular Reproduction and Development 54:103-111.
67. Chun SY, Eisenhauer KM, Minami S, Billig H, Perlas E, Hsueh AJ (1996) Hormonal regulation of apoptosis in early antral follicles:follicle-stimulating hormone as a major survival factor. Endocrinology 137:1447-1456.
68. Sasson R, Dantes A, Tajima K, msterdam A (2003) Novel genes modulated by FSH in normal and immortalized FSH-responsive cells:new insights into the mechanism of FSH action. FASEB J 17: 1256-1266.
69. Grieshaber NA, Ko C, Grieshaber SS, Ji I, Ji TH (2003) Follicle-stimulating hormone responsive cytoskeletal genes in rat granulosa cells:class I beta-tubulin, tropomyosin-4, and kinesin heavy chain. Endocrinology 144:29-39.
70. Tanaka M, Hennebold JD, Miyakoshi K, Teranishi T, Ueno K, Adashi EY (2003) The generation and characterization of an ovary-selective cDNA library. Mol Cell Endocrinol 202:67-69.
71. Ratoosh SL, Lifka J, Hedin L, Jahsen T, Richards JS (1987) Hormonal regulation of the synthesis and mRNA content of the regulatory subunit of cyclic AMP-dependent protein kinase type Ⅱ in cultured rat ovarian granulosa cells. J Biol Chem 262:7306-7313.
72. Oh DY, Wang L, Ahn RS, Park JY, Seong JY, Kwon HB (2003) Differential G protein coupling preference of mammalian and nonmammalian gonadotropin-releasing hormone receptors. Mol Cell Endocrinol 205:89-98.
73. Alliston TN, Maiyar AC, Buse P, Firestone GL, Richards JS (1997) Follicle stimulating hormone-regulated expression of serum/glucocorticoid inducible kinase in rat ovarian granulosa cells:a functional role for the Spl family in promoter activity. Mol Endocrinol 11:1934-1949.
74. Salvador LM, Flynn MP, Avila J, Reierstad S, Maizels ET, Alam H, Park Y, Scott JD, Carr DW, Hunzicker-Dunn M (2004) Neuronal microtubule-associated protein 2D is a dual a-kinase anchoring protein expressed in rat ovarian granulosa cells. J Biol Chem 279:27621-27632.
75. Russell DL, Doyle KM, Gonzales-Robayna I, Pipaon C, Richards JS (2003) Egr-1 induction in rat granulosa cells by follicle-stimulating hormone and luteinizing hormone:combinatorial regulation by transcription factors cyclic adenosine 3',5'-monophosphate regulatory element binding protein, serum response factor, spl, and early growth response factor-1. Mol Endocrinol 17:520-533.
76. Little TH, Zhang Y, Matulis CK, Week J, Zhang Z, Ramachandran A, Mayo KE, Radhakrishnan I (2006) Sequence-specific deoxyribonucleic acid (DNA) recognition by steroidogenic factor 1:a helix at the carboxy terminus of the DNA binding domain is necessary for complex stability. Mol Endocrinol 20:831-843.
77. Falender AE, Lanz R, Malenfant D, Belanger L, Richards JS (2003) Differential expression of steroidogenic factor-1 and FTF/LRH-1 in the rodent ovary. Endocrinology 144:3598-3610.
78. Yazawa T, Mizutani T, Yamada K, Kawata H, Sekiguchi T, Yoshino M, Kajitani T, Shou Z, Miyamoto K (2003) Involvement of cyclic adenosine 5'-monophosphate response element-binding protein, steroidogenic factor 1, and Dax-1 in the regulation of gonadotropin-inducible ovarian transcription factor 1 gene expression by follicle-stimulating hormone in ovarian granulosa cells. Endocrinology 144:1920-1930.
79. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913-922.
80. Covarrubias L, Hernandez-Garcia D, Schnabel D, Salas-Vidal E, Castro-Obregon S (2008) Function of reactive oxygen species during animal development:passive or active? Dev Biol 320:1-11.
81. Circu ML, Aw TY (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48:749-762.
82. Carmody RJ, Cotter TG (2001) Signalling apoptosis:a radical approach. Redox Rep 6:77-90.
83. Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M, Yodoi J (2002) Redox control of cell death. Antioxid Redox Signal 4:405-414.
84. Kwon YW, Masutani H, Nakamura H, Ishii Y, Yodoi J (2003) Redox regulation of cell growth and cell death. Biol Chem 384:991-996.
85. Circu ML, Aw TY (2008) Glutathione and apoptosis. Free Radic Res 42:689-706.
86. Matsuda-Minehata F, Goto Y, Inoue N, Sakamaki K, Chedrese PJ, Manabe N (2007) Anti-apoptotic activity of porcine cFLIP in ovarian granulosa cell lines. Mol Reprod Dev 74:1165-1170.
87. Cheng Y, Maeda A, Goto Y, Matsuda F, Miyano T, Inoue N, Sakamaki K, Manabe N (2008) Changes in expression and localization of X-linked inhibitor of apoptosis protein (XIAP) in follicular granulosa cells during atresia in porcine ovaries. J Reprod Dev 54:454-459.
88. Maeda A, Goto Y, Matsuda-Minehata F, Cheng Y, Inoue N, Manabe N (2007) Changes in expression of interleukin-6 receptors in granulosa cells during follicular atresia in pig ovaries. J Reprod Dev 53: 727-736.
89. Nakayama M, Manabe N, Inoue N, Matsui T, Miyamoto H (2003) Changes in the expression of tumor necrosis factor (TNF) alpha, TNFalpha receptor (TNFR) 2, and TNFR-associated factor 2 in granulosa cells during atresia in pig ovaries. Biol Reprod 68:530-535.
90. Matsui T, Manabe N, Goto Y, Inoue N, Nishihara S, Miyamoto H (2003) Expression and activity of Apafl and caspase-9 in granulosa cells during follicular atresia in pig ovaries. Reproduction.126: 113-120.
91. Hojo T, Al-Zi'abi MO, Komiyama J, Manabe N, Acosta TJ, Okuda K (2010) Expression and localization of cFLIP, an anti-apoptotic factor, in the bovine corpus luteum. J Reprod Dev 56: 230-235.
92. Inoue N, Maeda A, Matsuda-Minehata F, Fukuta K, Manabe N (2006) Expression and localization of Fas ligand and Fas during atresia in porcine ovarian follicles. J Reprod Dev 52:723-730.
93. Wajant H, Scheurich P (2001) Tumor necrosis factor receptor-associated factor (TRAF) 2 and its role in TNF signaling. Int J Biochem Cell Biol 33:19-32.
94. Zheng X, Boerboom D Carriere& PD (2009) Transforming growth factor-beta 1 inhibits luteinization and promotes apoptosis in bovine granulosa cells. Reproduction 137:969-977.
95. Yang MY, Rajamahendran R (2000) Morphological and Biochemical Identification of Apoptosis in Small, Medium, and Large Bovine Follicles and the Effects of Follicle-Stimulating Hormone and Insulin-Like Growth Factor-I on Spontaneous Apoptosis in Cultured Bovine Granulosa Cells. Biology of Reproduction 62:1209-1217.
96. Mani AM, Fenwick MA, Cheng Z, Sharma M.K., Singh D, Wathes, DC (2010) IGF1 induces up-regulation of steroidogenic and apoptotic regulatory genes via activation of phosphatidylinositol-dependent kinase/AKT in bovine granulosa cells. Reproduction 139:139-151.
97. Hu CL, Cowan RG, Harman RM, Quirk& SM (2004) Cell cycle progression and activation of Akt kinase are required for insulin-like growth factor I-mediated suppression of apoptosis in granulosa cells. Mol Endocrinol 18:326-338.
98. Ratts VS, Flaws JA, Kolp R, Sorenson CM, Tilly JL (1995) Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 136:3665-3668.
99. Tilly JL, Tilly KI, Kenton ML, Johnson AL (1995) Expression of members of the bcl-2 gene family in the immature rat ovary:equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology 136:232-241.
100. Kugu K, Ratts VS, Piquette GN, Tilly KI, Tao XJ, Martimbeau S, Aberdeen GW, Krajewski S, Reed JC, Pepe GJ, Albrecht ED, Tilly JL (1998) Analysis of apoptosis and expression of bcl-2 gene family members in the human and baboon ovary. Cell Death Differ 5:67-76.
101. Salvetti NR, Stangaferro ML, Palomar MM, Alfaro NS, Rey F, Gimeno EJ, Ortega HH (2010) Cell proliferation and survival mechanisms underlying the abnormal persistence of follicular cysts in bovines with cystic ovarian disease induced by ACTH. Anim Reprod Sci 122:98-110.
102. Quirk SM, Cowan RG, Harman RM (2006) The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle. Journal of Endocrinology 189:441-453.
103. Kayamori T, Kosaka N, Miyamoto A, Shimizu& T (2009) The differential pathways of bone morphogenetic protein (BMP)-4 and -7 in the suppression of the bovine granulosa cell apoptosis. Mol Cell Biochem 323:161-168.
104. Inoue N, Matsuda F, Goto Y, Manabe N (2011) Role of cell-death ligand-receptor system of granulosa cells in selective follicular atresia in porcine ovary. J Reprod Dev 57:169-175.
105. Grotowski W, Lecybyl R, Warenik-Szymankiewicz A, Trzeciak WH (1997) The role of apoptosis of granulosa cells in follicular atresia. Ginekol Pol 68:317-326.
106. Pan Z, Zhang J, Lin F, Ma X, Wang X, Liu, H (2012) Expression profiles of key candidate genes involved in steroidogenesis during follicular atresia in the pig ovary. Mol Biol Rep 39: 10823-10832.
107. Yu YS, Sui HS, Han ZB, Li W, Luo M.J, Tan JH (2004) Apoptosis in granulosa cells during follicular atresia:relationship with steroids and insulin-like growth factors. Cell Res 14:341-346.
108. Zhang C, Xia G, aTsang BK (2011) Interactions of thyroid hormone and FSH in the regulation of rat granulosa cell apoptosis. Front Biosci 3:1401-1413.
109. Garside SA, Harlow CR, Hillier SG, Fraser HM, Thomas FH (2010) Thrombospondin-1 inhibits angiogenesis and promotes follicular atresia in a novel in vitro angiogenesis assay. Endocrinology 151:1280-1289.
110. Parborell F, Abramovich D, Irusta G, aTesone M (2011) Angiopoietin 1 reduces rat follicular atresia mediated by apoptosis through the PI3K/Akt pathway. Mol Cell Endocrinol 343:79-87.
111. Lin F, Li R, Pan ZX, Zhou B, Yu deB, Wang XG, Ma XS, Han J, Shen M, Liu HL (2012) miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary. PLoS One 7:e38640.
112. Lin P, Yang Y, Li X, Chen F, Cui C, Hu L, Li Q, Liu W, Jin Y (2012) Endoplasmic reticulum stress is involved in granulosa cell apoptosis during follicular atresia in goat ovaries. Mol Reprod Dev 79: 423-432.
113. Sugimoto M, Kagawa N, Morita M, Kume S, Wongpanit K, Jin H, Manabe N (2010) Changes in the expression of decoy receptor 3 in granulosa cells during follicular atresia in porcine ovaries. J Reprod Dev 56:467-474.
114. Orimoto AM, Dumaresq-Doiron K, Jiang JY, Tanphaichitr N, Tsang BK, Carmona E (2008) Mammalian hyaluronidase induces ovarian granulosa cell apoptosis and is involved in follicular atresia. Endocrinology 149:5835-5847.
115. Maeda A, Inoue N, Matsuda-Minehata F, Goto Y, Cheng Y, aManabe N (2007) The role of interleukin-6 in the regulation of granulosa cell apoptosis during follicular atresia in pig ovaries. J Reprod Dev 53:481-490.
116. Zwain I, Amato P (2000) Clusterin protects granulosa cells from apoptotic cell death during follicular atresia. Exp Cell Res 257:101-110.
117. Alonso-Pozos I, Rosales-Torres AM, Avalos-Rodriguez A, Vergara-Onofre M, Rosado-Garcia A (2003) Mechanism of granulosa cell death during follicular atresia depends on follicular size. Theriogenology 60:1071-1081.
118. Xu JP, Li X, Mori E, Sato E, Saito S, Guo MW, Mori T (1997) Expression of Fas-Fas ligand system associated with atresia in murine ovary. Zygote 5:321-327.
119. Monniaux D, Huet C, Pisselet C, Mandon-Pepin B, Monget P (1998) Mechanism, regulation, and manipilations of follicular atresia. Contracept Fertil Sex 26:528-535.
120. Salvetti NR, Gimeno EJ, Lorente JA, Ortega HH (2004) Expression of cytoskeletal proteins in the follicular wall of induced ovarian cysts. Cells Tissues Organs 178:117-125.
121. Ortega HH, Salvetti NR, Muller LA, Amable P, Lorente JA, Barbeito CG, Gimeno EJ (2007) Characterization of Cytoskeletal Proteins in Follicular Structures of Cows with Cystic Ovarian Disease. Journal of Comparative Pathology 136:222-230.
122. Allworth AE, Albertini DF (1993) Meiotic Maturation in Cultured Bovine Oocytes Is Accompanied by Remodeling of the Cumulus Cell Cytoskeleton. Developmental Biology 158: 101-112.
123. Gilbert S, Loranger A, Daigle N, Marceau N (2001) Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J Cell Biol 154:763-773.
124. Ku NO, Soetikno RM, Omary MB (2003) Keratin mutation in transgenic mice predisposes to Fas but not TNF-induced apoptosis and massive liver injury. Hepatology 37:1006-1014.
125. Caulin C, Ware CF, Magin TM, Oshima& RG (2000) Keratin-dependent, epithelial resistance to tumor necrosis factor-induced apoptosis. J Cell Biol 149:17-22.
126. Oshima RG (2002) Apoptosis and keratin intermediate filaments. Cell Death Differ 9:486-492.
127. Gilbert S, Ruel A, Loranger A, Marceau N (2008) Switch in Fas-activated death signaling pathway as result of keratin 8/18-intermediate filament loss. Apoptosis 13:1479-1493.
128. Best CL, Pudney J, Welch WR, Burger N, Hill JA (1996) Localization and characterization of white blood cell populations within the human ovary throughout the menstrual cycle and menopause. Hum Reprod 11:790-797.
129. Takaya R, Fukaya T, Sasano H, Suzuki T, Tamura M, Yajima A (1997) Macrophages in normal cycling human ovaries; immunohistochemical localization and characterization. Hum Reprod 12: 1508-1512.
130. Van der Hoek KH, Maddocks S, Woodhouse CM, van Rooijen N, Robertson SA, Norman RJ (2000) Intrab.ursal injection of clodronate liposomes causes macrophage depletion and inhibits ovulation in the mouse ovary. Biol Reprod 62:1059-1066.
131. Turner EC, Hughes J, Wilson H, Clay M, Mylonas KJ, Kipari T, Duncan WC, Fraser HM (2011) Conditional ablation of macrophages disrupts ovarian vasculature. Reproduction 141:821-831.
132. Cohen PE, Zhu L, Pollard JW (1997) Absence of colony stimulating factor-1 in osteopetrotic (csfinop/csfinop) mice disrupts estrous cycles and ovulation. Biol Reprod 56:110-118.
133. Petrovska M, Dimitrov DG, Michael SD (1996) Quantitative changes in macrophage distribution in normal mouse ovary over the course of the estrous cycle examined with an image analysis system. Am J Reprod Immunol 36:175-183.
1. Fortune JE (1994) Ovarian follicular growth and development in mammals. Biol Reprod 50:225-232.
2. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection,dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
3. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, Ireland JJ, Roche JF (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64:839-848.
4. Hsueh AJ, Billig H, Tsafriri A (1994) Ovarian follicle atresia:a hormonally controlled apoptotic process. Endocr Rev 15:707-724.
5. Endo M, Kimura K, Kuwayama T, Monji Y, Iwata H (2012) Effect of estradiol during culture of bovine oocyte-granulosa cell complexes on the mitochondrial DNA copies of oocytes and telomere length of granulosa cells. Zygote 1-9.
6. Sharma I, Singh D (2012) Conjugated linoleic acids attenuate FSH-and IGF 1-stimulated cell proliferation; IGF1, GATA4, and aromatase expression; and estradiol-17beta production in buffalo granulosa cells involving PPARgamma, PTEN, and PI3K/Akt. Reproduction 144:373-383.
7. Quirk SM, Cowan RG, Harman RM (2006) The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle. Journal of Endocrinology 189:441-453.
8. Quirk SM, Cowan RG, Harman RM (2004) Progesterone Receptor and the Cell Cycle Modulate Apoptosis in Granulosa Cells. Endocrinology 145:5033-5043.
9. Peluso JJ, Liu X, Gawkowska A, Johnston-MacAnanny E (2009) Progesterone Activates a Progesterone Receptor Membrane Component 1-Dependent Mechanism That Promotes Human Granulosa/Luteal Cell Survival But Not Progesterone Secretion. Journal of Clinical Endocrinology & Metabolism 94:2644-2649.
10. McNatty KP, Baird DT, Bolton A, Chambers P, Corker CS, McLean H (1976) Concentration of oestrogens and androgens in human ovarian venous plasma and follicular fluid throughout the menstrual cycle. J Endocrinol 71:77-85.
11. Kaipia A, Hsueh& AJ (1997) Regulation of ovarian follicle atresia. Annu Rev Physiol 59:349-363.
12. Sowers MR, Wilson AL, Kardia SR, Chu J, McConnell DS (2006) CYP1A1 and CYP1B1 polymorphisms and their association with estradiol and estrogen metabolites in women who are premenopausal and perimenopausal. Am J Med 119:44-51.
13. Gonzales F (1988) The molecular biology of cytochrome P450s. Pharmacol Rev 40:243-288.
14. Guengerich FP (1994) Analysis and characterization of enzymes. In:Principles and methods of toxicology. Hayes AW (ed). Raven Press, New York, pp 1259-1313.
15. Guengerich FP (2008) Cytochrome p450 and chemical toxicology. Chem Res Toxicol 21:70-83.
16. Lamb DC, Lei L, Warrilow AQ Lepesheva GI, Mullins JG, Waterman MR, Kelly SL (2009) The first virally encoded cytochrome P450. Journal of Virology 83:8266-8269.
17. Roland S, Sigel A, Sigel H (2007) The Ubiquitous Roles of Cytochrome P450 Proteins:Metal Ions in Life Sciences. New York:Wiley.
18. Danielson PB (2002) The cytochrome P450 superfamily:biochemistry, evolution and drug metabolism in humans. Curr Drug Metab 3:561-597.
19. Hakkola J, PasanenM, Pelkonen O, Hukkanen J, Evisalmi S, Antilla S, Rane A, Mantyla M, Purkunen R, Saarikoski S, Tooming M, Raunio H (1997) Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis 18:391-397.
20. Huang ZQ, Fasco MJ, Figge HL, Keyomarsi K, Kaminsky LS (1996) Expression of cytochrome P450 in human breast tissue and tumors. Drug Metab Dispos 24:899-905.
21. Rieder CRM, Ramsden DB, Williams AC (1998) Cytochrome P4501B1 mRNA in the human central nervous system. J Clin Pathol Mol Pathol 51:138-142.
22. Shimada T, Hayes CL, Yamazaki H, Shantu A, Hecht SS, Guengerich FP, Sutter TR (1996) Activation of chemically diverse procarcinogen s by human cytochrome P-4501B1. Cancer Res 56: 2979-2984.
23. Sutter TR, Tang YM, Hayes CL, Wo YY, Jabs EW, Li X, Yin H, Cody CW, Greenlee WF (1994) Complete cDNA sequence of a human dioxininducible mRNA identi. es a new gene subfamily of cytochrome p450 that maps to chromosome 2. J Bio Chem 269:13092-13099.
24. Tang YM, Chen GF, Thompson PA, Lin D, Lang NP, Kadlubar FF (1999) Development of an antipeptide antibody that binds to the c-terminal region of human CYP1B1. Drug Metab Dispos 27: 274-280.
25. Vadlamuri SV, Glover DD, Turner T, Sarkar MA (1998) Regiospecic expression of cytochrome P4501A1 and 1B1 in human uterine tissue. Cancer Lett 122:143-150.
26. Iwanari M, Nakajima M, Kizu R, Hayakawa K, Yokoi T (2002) Induction of CYP1A1, CYP1A2, and CYP1B1 mRNAs by nitropolycyclic aromatic hydrocarbons in various human tissue-derived cells:chemical-, cytochrome P450 isoform-, and cell-specific differences. Arch Toxicol 76: 287-298.
27. Hankinson O (1995) The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 35:307-340.
28. Schmidt JV, Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Biol 12:55-89.
29. Hayes C, Spink D, Spink B, Cao J, Walker N, Sutter T (1996) Estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc Natl Acad Sci USA 193:9776-9781.
30. Spink DC, Spink BC, Cao JQ, et al (1997) Induction of cytochrome P450 1B1 and catechol estrogen metabolism in ACHN human renal adenocarcinoma cells. J Steroid Biochem Mol Biol 62:223-232.
31. Lee AJ, Cai MX, Thomas PE, Conney AH, Zhu BT (2003) Characterization of the oxidative metabolites of estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 144:3382-3398.
32. Shimada T, Hayes CL, Yamazaki H, et al (1996) Activation of chemically diverse procarcinogens by human cytochrome P450 1B1. Cancer Res 56:2979-2984.
33. Hakkola J, Pasanen M, Pelkonen O, et al (1997) Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis 18:391-397.
34. Tsuchiya Y, Nakajima M, Kyo S, Kanaya T, Inoue M, Yokoi T (2004) Human CYP1B1 is regulated by estradiol via estrogen receptor. Cancer Res 64:3119-3125.
35. Leung GS, Kawai M, Tai JK, Chen J, Bandiera SM, Chang TK (2009) Developmental expression and endocrine regulation of CYP1B1 in rat testis. Drug Metab Dispos 37:523-528.
36. Bhattacharyya KK, Brake PB, Eltom SE, Otto SA, Jefcoate CR (1995) Identification of a rat adrenal cytochrome P450 active in polycyclic hydrocarbon metabolism as rat CYP1B1. Demonstration of a unique tissue-specific pattern of hormonal and aryl hydrocarbon receptorlinked regulation. J Biol Chem 270:11595-11602.
37. Leung GS, Kawai M, Tai JK, Chen J, Bandiera SM, and Chang, TK (2009) Developmental expression and endocrine regulation of CYP1B1 in rat testis. Drug Metab Dispos 37:23-528.
38. Haider SG (2004) Cell biology of Leydig cells in the testis. Int Rev Cytol 233:181-241.
39. Lee AJ, Cai MX, Thomas PE, Conney AH, Zhu BT (2003) Characterization of the oxidative metabolites of 17beta-estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 144:3382-3398.
40. Suchar LA, Chang RL, Rosen RT, Lech J, Conney AH (1995) High performance liquid chromatography separation of hydroxylated estradiol metabolites:formation of estradiol metabolites by liver microsomes from male and female rats. J. Pharmacol. Exp. Ther 272:197-206.
41. Yang HP, Bosquet JG, Li Q, etc (2010) Common genetic variation in the sex hormone metabolic pathway and endometrial cancer risk. Arcinogenesis 31:827-833.
42. Spink DC, Hayes CL, Young NR, Christou M, Sutter TR, Jefcoate CR, Gierthy JF (1994) The effects of 2,3,7,8-tetrachlorodibenzo-pdioxin on estrogen metabolism in MCF-7 breast cancer cells: evidence for induction of a novel 17 β-estradiol 4-hydroxylase. J Steroid Biochem Mol Biol 51: 251-258.
43. Spink DC, Hayes CL, Young NR, Christou M, Sutter TR, Jefcoate CR, Gierthy JF (1994) The effects of 2,3,7,8-tetrachlorodibenzo-pdioxin on estrogen metabolism in MCF-7 breast cancer cells: evidence for induction of a novel 17 h-estradiol 4-hydroxylase. J. SteroidBiochem. Mol. Biol 51: 251-258.
44. Zhu BT, Conney AH (1998) Functional role of estrogen metabolism in target cells:review and perspectives. Carcinogenesis 19:1-27.
45. Zhu BT, Roy D, Liehr JG (1993) The carcinogenic activity of ethinyl estrogens is determined by both their hormonal characteristics and their conversion to catechol metabolites. Endocrinology 131: 577-583.
46. Li KM, Todorovic R, Devanesan P, Higginbotham S, Kofeler H, Ramanathan R, Gross ML, Rogan EG, Cavalieri EL (2004) Metabolism and DNA binding studies of 4-hydroxyestradiol and estradiol-3,4-quinone in vitro and in female ACI rat mammary gland in vivo. Carcinogenesis 25: 289-297.
47. Newbold RR, Liehr JG (2000) Induction of uterine adenocarcinoma in CD-I mice by catechol estrogens. Cancer Res 60:235-237.
48. Rogan EG, Badawi AF, Devanesan PD, Meza JL, Edney JA, West WW, Higginbotham SM, Cavalieri EL (2003) Relative imbalances in estrogen metabolism and conjugation in breast tissue of women with carcinoma:potential biomarkers of susceptibility to cancer. Carcinogenesis 24:697-702.
49. Hiraku Y, Yamashita N, Nishiguchi M, Kawanishi S, (2001) Catechol estrogens induce oxidative DNA damage and estradiol enhances cell proliferation. Int. J. Cancer 92:333-337.
50. Thibodeau PA, Paquette B (1999) DNA damage induced by catecholestrogens in the presence of copper (II):generation of reactive oxygen species and enhancement by NADH. Free Radical Biol. Med 27:1367-1377.
51. Chen ZH, Na HK., Hurh YJ, Surh YJ (2005) 4-Hydroxyestradiol induces oxidative stress and apoptosis in human mammary epithelial cells:possible protection by NF-kappaB and ERK/MAPK. Toxicol Appl Pharmacol 208:46-56.
52. Liehr JG, Roy D, (1990) Free radical generation by redox cycling of estrogens. Free Radical Biol. Med 8:415-423.
53. Liehr, J.G., (1990). Genotoxic effects of estrogens. Mutat. Res 238:269-276.
54. Samuni AM, Chuang EY, Krishna MC, Stein W, DeGraff W, Russo A, Mitchell JB (2003) Semiquinone radical intermediate in catecholic estrogen-mediated cytotoxicity and mutagenesis: chemoprevention strategies with antioxidants. Proc. Natl. Acad. Sci. U.S.A 100:5390-5395.
55. Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D (2000) Estrogens as endogenous genotoxic agents DNA adducts and mutations. J. Natl. Cancer Inst Monogr.27:75-93.
56. Hayes CL, Spink DC, Spink BC, Cao JQ, Walker NJ, Sutter TR (1996) 17h-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A 93:9776-9781.
57. Murray GI, Taylor MC, McFadyen MC, McKay JA, Greenlee WF, Burke MD, Melvin WT, (1997) Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res 57:3026-3031.
1. Kaipia A, Hsueh AJ (1997) Regulation of ovarian follicle atresia. Annu Rev Physiol 59:349-363.
2. Jang JH, Surh, YJ (2003) Protective effect of resveratrol on [beta]-amyloid induced oxidative PC 12 cell death. Free Radical Biology and Medicine 34:1100-1110.
3. Asahara S, Sato A, Aljonaid AA, Maruo T (2003) Thyroid hormone synergizes with follicle stimulating hormone to inhibit apoptosis in porcine granulosa cells selectively from small follicles. Kobe J Med Sci 49:107-116.
4. Yang MY, Rajamahendran R (2000) Morphological and biochemical identification of apoptosis in small, medium, and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured bovine granulosa cells. Biology of Reproduction 62:1209-1217.
5. Fortune JE (1994) Ovarian follicular growth and development in mammals. Biol Reprod 50:225-232.
6. Lunenfeld B, Insler V (1993) Follicular development and its control. Gynecological Endocrinology 7: 285-291.
7. Vander AJ, Sherman JH, Luciano DS (1994) Human Physiology:The Mechanisms of Body Function. New York:McGraw-Hill:661-692.
8. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
9. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, Ireland JJ, Roche JF (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64:839-848.
10. Satosi K, Motoaki U (2004) Histological analysis of the'critical point' in follicular development in mice. Reproductive Medicine and Biology 3:141-145.
11. Manabe, N (2008) Regulation of granulosa cell apoptosis by death ligand-receptor signaling. Animal Science Journal 79:1-10.
12. Sai T, Goto Y, Yoshioka R, Maeda A, Matsuda F, Sugimoto M, Wongpanit K, Jin H. Z Li, JY, Manabe N (2011) Bid and Bax are involved in granulosa cell apoptosis. J Repord Dev 57:421-427.
13. Smith CC, Yellon DM (2011) Necroptosis, necrostatins and tissue injury. J Cell Mol Med 15: 1797-1806.
14. Kroemer, G, and Martin, SJ (2005) Caspase-independent cell death. Nat Med 11:725-730.
15. Wajant H (2002) The Fas signaling pathway:more than a paradigm. Science's STKE 296:1635.
16. Berry D (2007) Molecular animation of cell death mediated by the Fas pathway. Science's STK trl.
17. Borutaite V (2010) Mitochondria as decision-makers in cell death. Environmental and molecular mutagenesis 51:406-416.
18. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770-776.
19. McStay G, Salvesen G, Green D (2007) Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death & Differentiation 15:322-331.
20. Harris CA, Johnson Jr EM (2001) BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. Journal of Biological Chemistry 276: 37754-37760.
21. Hunzicker-Dunn M, Maizels ET (2006) FSH signaling pathways in immature granulosa cells that regulate target gene expression:branching out from protein kinase A. Cell Signal 18:1351-1359.
22. Manabe N, Imai Y, Kimura Y, Myoumoto A, Sugimoto M, Miyamoto H, Okamura Y, Fukumoto M (1996) Ca 2+/Mg 2+-Dependent endonuclease but not Ca 2+-Dependent, Mg 2+-Dependent or cation-independent endonuclease is involved in granulosa cell apoptosis of pig atretic follicles. Journal of Reproduction and Development 42:247-253.
23. Asahara S, Sato A, Aljonaid AA, Maruo T (2003) Thyroid hormone synergizes with follicle stimulating hormone to inhibit apoptosis in porcine granulosa cells selectively from small follicles. Kobe J Med Sci 49:107-116.
24. Yang MY, Rajamahendran R (2000) Morphological and biochemical identification of apoptosis in small, medium, and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured bovine granulosa cells. Biology of Reproduction 62:1209-1217.
1. Fortune JE (1994) Ovarian follicular growth and development in mammals. Biol Reprod 50:225-232.
2. Lunenfeld B, Insler V (1993) Follicular development and its control. Gynecological Endocrinology 7: 285-291.
3. Vander AJ, Sherman JH, Luciano DS (1994) Human Physiology:The Mechanisms of Body Function New York:McGraw-Hill:661-692.
4. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ (1994) Selection, dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 101:547-555.
5. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, Ireland JJ, Roche JF (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64:839-848.
6. Guengerich FP (2008) Cytochrome p450 and chemical toxicology. Chem. Res. Toxicol 21:70-83.
7. Suchar LA, Chang RL, Rosen RT, Lech J, Conney AH (1995) High performance liquid chromatography separation of hydroxylated estradiol metabolites:formation of estradiol metabolites by liver microsomes from male and female rats. J. Pharmacol. Exp. Ther 272:197-206.
8. John L Rinn, Joel S Rozowsky, Ian J Laurenzi, Petur H. Petersen, Kaiyong Zou, Weimin Zhong, Mark Gerstein, Michael Snyder (2004) Major Molecular Differences between mammalian sexes are involved in drug metabolism and Renal Function. Developmental Cell 6:791-800.
9. Campbell SJ, Henderson CJ, Anthony DC, Davidson D, Clark AJ, Wolf CR (2005) The murine Cyp1a1 gene is expressed in a restricted spatial and temporal pattern during embryonic development. J Biol Chem 280:5828-5835.
10. Dorrington JH, Bendell JJ, Khan SA (1993) Interactions between FSH, estradiol-17 beta and transforming growth factor-beta regulate growth and differentiation in the rat gonad. J Steroid Biochem Mol Biol 44:441-447.
11. Richards JS, Jonassen JA, Rolfes AI, Kersey K, Reichert LE (1979) Adenosine 3',5'-monophosphate, luteinizing hormone receptor, and progesterone during granulosa cell differentiation:effects of estradiol and follicle-stimulating hormone. Endocrinology 104:765-773.
12. Hsueh AJ, Billig H, Tsafriri A (1994) Ovarian follicle atresia:a hormonally controlled apoptotic process. Endocr Rev 15:707-724.
13. Nimz M, Spitschak M, Furbass R, Vanselow J (2010) The pre-ovulatory luteinizing hormone surge is followed by down-regulation of CYP19A1, HSD3B1, and CYP17A1 and chromatin condensation of the corresponding promoters in bovine follicles. Mol Reprod Dev 77:1040-1048.
14. Lv L, Jimenez-Krassel F, Sen A, Bettegowda A, Mondal M, Folger JK, Lee KB, Ireland JJ, Smith GW (2009) Evidence supporting a role for cocaine-and amphetamine-regulated transcript (CARTPT) in control of granulosa cell estradiol production associated with dominant follicle selection in cattle. Biol Reprod 81:580-586.
15. Manabe N, Imai Y, Kimura Y, Myoumoto A (1996) Ca2+/Mg2+-Dependent endonuclease but not Ca2+-Dependent, Mg2+-Dependent or cation-independent endonuclease is involved in granulosa cell apoptosis of pig atretic follicles. Journal of Reproduction and Development 42:247-253.
16. Spink DC, Hayes CL, Young NR, Christou M, Sutter TR, Jefcoate CR, Gierthy JF (1994) The effects of 2,3,7,8-tetrachlorodibenzo-pdioxin on estrogen metabolism in MCF-7 breast cancer cells: evidence for induction of a novel 17 β-estradiol 4-hydroxylase. J Steroid Biochem Mol Biol 51: 251-258.
17. Chen ZH, Na HK, Hurh YJ, Surh YJ (2005) 4-Hydroxyestradiol induces oxidative stress and apoptosis in human mammary epithelial cells:possible protection by NF-kappaB and ERK/MAPK. Toxicol Appl Pharmacol 208:46-56.
18. Ollinger K, Buffinton GD, Ernster L, Cadenas E (1990) Effect of superoxide dismutase on the autoxidation of substituted hydro-and semi-naphthoquinones. Chem Biol Interact 73:53-76.
19. Samuni AM, Chuang EY, Krishna MC, Stein W, DeGraff W, Russo A, Mitchell JB (2003) Semiquinone radical intermediate in catecholic estrogen-mediated cytotoxicity and mutagenesis: chemoprevention strategies with antioxidants. Proc Natl Acad Sci USA 100:5390-5395.
20. Liehr JG, Roy D (1990) Free radical generation by redox cycling of estrogens. Free Radic Biol Med 8:415-423.
21. Shen M, Lin F, Zhang J, Tang Y, Chen WK, Liu H (2012) Involvement of the up-regulated FoxOl expression in follicular granulosa cell apoptosis induced by oxidative stress. J Biol Chem 287: 25727-25740.
22. Denison MS, Nagy SR (2003) Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43:309-334.
23. Bussmann UA, Baranao JL (2006) Regulation of aryl hydrocarbon receptor expression in rat granulosa cells. Biol Reprod 75:360-369.
24. Jacob A, Hartz AM, Potin S, Coumoul X, Yousif S, Scherrmann JM, Bauer B, Decleves X (2011) Aryl hydrocarbon receptor-dependent upregulation of Cyplbl by TCDD and diesel exhaust particles in rat brain microvessels. Fluids Barriers CNS 8:23.
25. Heim MH (1999) The Jak-STAT pathway:cytokine signalling from the receptor to the nucleus. J Recept Signal Transduct Res 19:75-120.
26. Durbin JE, Hackenmiller R, Simon MC, Levy DE (1996) Targeted disruption of the mouse Statl gene results in compromised innate immunity to viral disease. Cell 3:443-450.
27. Meraz MA, White JM, Sheehan KC, etc (1996) Targeted disruption of the Statl gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 3:431-442.
28. Ihle JN, Witthuhn BA, Quelle FW, Yamamoto K, Thierfelder WE, Kreider B, Silvennoinen O (1994) Signaling by the cytokine receptor superfamily:JAKs and STATs. Trends Biochem Sci 5:222-227.
29. Anastasis S, Tiziano MS, Bhawanjit KB, Yoshinobu N, Miho M, Richard AK (2001) Induction of Apoptosis and Fas Receptor/Fas Ligand Expression by Ischemia/Reperfusion in Cardiac Myocytes Requires Serine 727 of the STAT-1 Transcription Factor but Not Tyrosine 701. The Journal Of Biological Chemisitry.276:28340-28347.
30. Stephanou A, Scarabelli TM, Brar BK, Nakanishi Y, Matsumura M, Knight RA, Latchman DS (2001) Induction of apoptosis and Fas receptor/Fas ligand expression by ischemia/reperfusion in cardiac myocytes requires Serine 727 of the STAT-1 transcription factor but not tyrosine 701. J Biol Chem 276:28340-28347.
31. Goh KC, Haque SJ, Williams BR (1999) p38 MAP kinase is required for Statl Serine phosphorylation and transcriptional activation induced by interferons. EMBO J 18:5601-5608.
32. Stoiber D, Kovarik P, Cohney S, Johnston JA, Steinlein P, Decker T (1999) Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-gamma. J Immunol 163:2640-2647.
33. Russell DL, Richards JS (1999) Differentiation-dependent prolactin responsiveness and stat (signal transducers and activators of transcription) signaling in rat ovarian cells. Mol Endocrinol 13: 2049-2064.
34. Lee T, Kim SJ, Sumpio BE (2003) Role of PP2A in the regulation of p38 MAPK activation in bovine aortic endothelial cells exposed to cyclic strain. J Cell Physiol 194:349-355.
35. Strack S, Cribbs JT, Gomez L (2004) Critical role for protein phosphatase 2A heterotrimers in mammalian cell survival. J Biol Chem 279:47732-47739.
36. Xu Z, Williams BR (2000) The B56alpha regulatory subunit of protein phosphatase 2A is a target for regulation by double-stranded RNAdependent protein kinase PKR. Mol Cell Biol 20:5285-5299.
37. Liu Q, Hofmann PA (2004) Protein phosphatase 2A-mediated cross-talk between p38 MAPK and ERK in apoptosis of cardiac myocytes. Am J Physiol Heart Circ Physiol 286:2204-2212.
38. Alvarado-Kristensson M, Andersson T (2005) Protein phosphatase 2A regulates apoptosis in neutrophils by dephosphorylating both p38 MAPK and its substrate caspase 3. J Biol Chem 280: 6238-6244.
39. Baharians Z, Schonthal AH (1998) Autoregulation of protein phosphatase type 2A expression. J Biol Chem 273:19019-19024.
40. Levallet G, Levallet J, and Bonnamy PJ (2008) FSH-induced phosphoprotein phosphatase 2A-mediated deactivation of particulate phosphodiesterase-4 activities is abolished after alteration in proteoglycan synthesis in immature rat Sertoli cells. J Endocrinol 197:45-54.
41. Woetmann A, Nielsen M, Christensen ST, Brockdorff J, Kaltoft K, Engel AM, Skov S, Brender C, Geisle C, Svejgaard A, et al (1999) Inhibition of protein phosphatase 2A induces Serine/threonine phosphorylation, subcellular redistribution, and functional inhibition of STAT3. Proc Natl Acad Sci USA 96:10620-10625.
42. Lutticken C, Coffer P, Yuan J, Schwartz C, Caldehoven E, Schindler C, Kruijer W, Heinrich, PC, Horn F (1995) Interleukin-6-induced Serine phosphorylation of transcription factor APRF:evidence for a role in interleukin-6 target gene induction. FEBS Lett 360:137-143.
43. Brockdorff J, Nielsen M, Dobson P, Geisler C, Ropke C, Svejgaard A, Odum, N (1997) Interleukin 2 induces a transient downregulation of protein phosphatase 1 and 2A activity in human T cells. Tissue Antigens 49:228-235.
44. Grillo MA, Colombatto S (2005) S-adenosylmethionine and protein methylation. Amino Acids 28: 357-362.
45. Chen J, Martin BL, Brautigan DL (1992) Regulation of protein Serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 257:1261-1264.
46. Chen J, Parsons S, Brautigan DL (1994) Tyrosine phosphorylation of protein phosphatase 2A in response to growth stimulation and v-src transformation of fibroblasts. J Biol Chem 269: 7957-7962.
47. Brautigan DL (1995) Flicking the switches:phosphorylation of Serine/threonine protein phosphatases. Semin Cancer Biol 6:211-217.
48. Janssens V, Goris, J (2001) Protein phosphatase 2A:a highly regulated family of Serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353:417-439.