氧化应激对动物有腔卵泡闭锁的影响及机制
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摘要
氧化应激被认为是影响动物繁殖性能和造成人类不孕不育的重要因素,氧化应激诱导卵泡颗粒细胞凋亡,进而诱发卵泡闭锁是其影响动物繁殖性能的重要途径。近年来,针对氧化应激对有腔卵泡闭锁的影响研究取得了系列进展,主要包括:氧化应激对卵泡闭锁具有重要调控作用;叉头盒转录因子O1(FoxO1)是氧化应激诱发卵泡闭锁的关键性调控因子;卵泡液因子能够调控卵泡颗粒细胞氧化损伤的发生与程度。
Oxidative stress is considered to be an important factor affecting animal reproductive performance and causing infertility in humans. Oxidative stress induces apoptosis of follicular granulosa cells,which in turn induces follicular atresia as an important way to influence animal reproductive performance. In recent years,a series of research progress has been made on the effects of oxidative stress on antral follicular atresia,including: oxidative stress plays an important role in regulating follicular atresia; transcription factor forkhead box O1( FoxO1) is a key regulator of oxidative stress-induced follicular atresia; follicular fluid factors can regulate the occurrence and degree of oxidative damage of follicular granule cells.
Oxidative stress is considered to be an important factor affecting animal reproductive performance and causing infertility in humans. Oxidative stress induces apoptosis of follicular granulosa cells,which in turn induces follicular atresia as an important way to influence animal reproductive performance. In recent years,a series of research progress has been made on the effects of oxidative stress on antral follicular atresia,including: oxidative stress plays an important role in regulating follicular atresia; transcription factor forkhead box O1( FoxO1) is a key regulator of oxidative stress-induced follicular atresia; follicular fluid factors can regulate the occurrence and degree of oxidative damage of follicular granule cells.
引文
[1] Grant S A,Hunter M G,Foxcroft G R. Morphological and biochemical characteristics during ovarian follicular development in the pig[J]. J Reprod Fertil,1989,86:171-183.
[2] Morbech D E,Esbenshade K L,Flowers W L,et al. Kinetics of follicle growth in the prepuberal gilt[J]. Biol Reprod,1992,47:485-491.
[3] Dailey R A,Clark J R,Staigmiller R B,et al. Growth of new follicles following electrocautery in four genetic groups of swine[J]. J Anim Sci,1976,43:175-183.
[4] Foxcroft G R,Hunter M G. Basic physiology of follicular maturation in the pig[J]. J Reprod Fertil,1985,33:1-19.
[5] Guthrie H D,Cooper B S,Welch G R,et al. Atresia in follicles grown after ovulation in the pig:measurement of increased apoptosis in granulosacells and reduced follicular fluid estradiol-17 beta[J]. Biol Reprod,1995,52(4):920-927.
[6] Miller A T,Picton H M,Craigon J,et al. Follicle dynamics and aromatase activity in high-ovulating Meishan sows and in Large-White hybrid contemporaries[J]. Biol Reprod,1998,58:1372-1378.
[7] Manabe N,Imai Y,Ohno H,et al. Apoptosis occurs in granulosa cells but not cumulus cells in the atretic antral follicles in pig ovaries[J].Experientia,1996,52(7):647-651.
[8] Manabe N,Goto Y,Matsuda-Minehata F,et al. Regulation mechanism of selective atresia in porcine follicles:regulation of granulosa cell apoptosis during atresia[J]. J Reprod Dev,2004,50(5):493-514.
[9] Nakayama M,Manabe N,Inoue N,et al. 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[J]. Biol Reprod,2003,68(2):530-535.
[10] Inoue N,Maeda A,Matsuda-Minehata F,et al. Expression and localization of Fas ligand and Fas during atresia in porcine ovarian follicles[J].J Reprod Dev,2006,52(6):723-730.
[11] Worku T,Rehman Z,Talpur H,et al. MicroRNAs:new insight in modulating follicular atresia:a review[J]. Int J Mol Sci,2017,18(2):333.
[12] Lin F,Li R,Pan Z X,et al. miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary[J]. PLoS One,2012,7(6):e38640.
[13] Liu J,Du X,Zhou J,et al. MicroRNA-26b functions as a proapoptotic factor in porcine follicular granulosa cells by targeting Sma and Mad-related protein 4[J]. Biol Reprod,2014,91(6):1-12.
[14] Cao R,Wu W,Zhou X,et al. Let-7g induces granulosa cell apoptosis by targeting MAP3K1 in the porcine ovary[J]. Int J Biochem Cell Biol,2015,68:148-157.
[15] Zhou J L,Liu J Y,Pan Z X,et al. The let-7g microRNA promotes follicular granulosa cell apoptosis by targeting transforming growth factor-βtype 1 receptor[J]. Molecular and Cellular Endocrinology,2015,409:103-112.
[16] Liu J,Yao W,Yao Y,et al. MiR-92a inhibits porcine ovarian granulosa cell apoptosis by targeting Smad7 gene[J]. FEBS Letters,2014,588:4497-4503.
[17] Cassano E,Tosto L,Balestrieri M,et al. Antioxidant defense in the follicular fluid of water buffalo[J]. Cell Physiol Biochem,1999,9(2):106-116.
[18] Giuseppina B,Federico B,Francesca G,et al. The effects of reduced oxygen tension on swine granulosa cell[J]. Regulatory Peptides,2004,120:69-75.
[19] Lopez-Barneo J,Pardal R,Ortega-Saenz P. Cellular mechanism of oxygen sensing[J]. Annu Rev Physiol,2001,63:259-287.
[20] Gupta S,Choi A,Yu H Y,et al. Fluctuations in total antioxidant capacity,catalase activity and hydrogen peroxide levels of follicular fluid during bovine folliculogenesis[J]. Reprod Fertil Dev,2011,23(5):673-680.
[21] Margo L,Hope H,Yu Y,et al. Follicular fluid hydrogen peroxide and lipid hydroperoxide in bovine antral follicles of various size,atresia,and dominance status[J]. J Assist Reprod Genet,2013,30:333-340.
[22] Singh A K,Chattopadhyay R,Chakravarty B,et al. Markers of oxidative stress in follicular fluid of women with endometriosis and tubal infertility undergoing IVF[J]. Reprod Toxicol,2013,42:116-124.
[23] Jana S K,Chattopadhyay R,Chakravarty B,et al. Upper control limit of reactive oxygen species in follicular fluid beyond which viable embryo formation is not favorable[J]. Reprod Toxicol,2010,29(4):447-451.
[24] Basini G,Simona B,Santini S E,et al. Reactive oxygen species and anti-oxidant defences in swine follicular fluids[J]. Reprod Fertil Dev,2008,20:269-274.
[25] Matzuk M M,Dionne L,Guo Q,et al. Ovarian function in superoxide dismutase 1 and 2 knockout mice[J]. Endocrinology,1998,139:4008-4011.
[26] Ho Y S,Gargano M,Cao J,et al. Reduced fertility in female mice lacking copper-zinc superoxide dismutase[J]. J Biol Chem,1998,273:7765-7769.
[27] Wong P C,Waggoner D,Subramaniam J R,et al. Copper chaperone for superoxide dismutase is essential to activate mammalian cu/zn superoxide dismutase[J]. Proc Natl Acad Sci USA,2000,97:2886-2891.
[28] Kumar T R,Wiseman A L,Kala G,et al. Reproductive defects inγ-glutamyl transpeptidase deficient mice[J]. Endocrinology,2000,141:4270-4277.
[29] Lin J,Nakamura B N,Mohar L,et al. Glutamate cysteine ligase modifier subunit(Gclm)null mice have increased ovarian oxidative stress and accelerated age-related ovarian failure[J]. Endocrinology,2015,156(9):3329-3343.
[30] Patrick J D,Sally D P,Luderer U. Role of reactive oxygen species and antioxidants in ovarian toxicity[J]. Biol Reprod,2012,86(2):1-10.
[31] Zhang J Q,Shen M,Zhu C C,et al. 3-nitropropionic acid induces ovarian oxidative stress and impairs follicle in mouse[J]. PLoS One,2014,9(2):e86589.
[32] Luderer U. Ovarian toxicity from reactive oxygen species[J]. Vitam Horm,2014,94:99-127.
[33] Lopez S G,Luderer U. Effects of cyclophosphamide and buthionine sulfoximine on ovarian glutathione and apoptosis[J]. Free Radic Biol Med,2004,36:1366-1377.
[34] Tsai-Turton M,Luderer U. Gonadotropin regulation of glutamate cysteine ligase catalytic and modifier subunit expression in rat ovary is subunit and follicle stage specific[J]. Am J Physiol Endocrinol Metab,2005,289:E391-E402.
[35] Tsai-Turton M,Luderer U. Opposing effects of glutathione depletion and FSH on reactive oxygen species and apoptosis in cultured preovulatory rat follicles[J]. Endocrinology,2006,147:1224-1236.
[36] Shen M,Lin F,Zhang J Q,et al. Involvement of the up-regulated FoxO 1 expression in follicular granulosa cell apoptosis induced by oxidative stress[J]. J Biol Chem,2012,287(31):25727-25740.
[37] Liu Z Q,Shen M,Wu W J,et al. Expression of PUMA in follicular granulosa cells regulated by FoxO 1 activation during oxidative stress[J].Reprod Sci,2015,22(6):696-705.
[38] Essers M A G,Weijzen S,de Vries-Smits A M M,et al. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK[J]. The EMBO Journal,2004,23(24):4802-4812.
[39] Sunayama J,Tsuruta F,Masuyama N,et al. JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3[J]. The Journal of Cell Biology,2005,170(2):295-304.
[40] Weng Q,Liu Z,Li B,et al. Oxidative stress induces mouse follicular granulosa cells apoptosis via JNK/FoxO 1 pathway[J]. PLoS One,2016,11(12):e0167869.
[41] He C J,Wang J,Zhang Z Z,et al. Mitochondria synthesize melatonin to ameliorate its function and improve mice oocyte’s quality under in vitro conditions[J]. International Journal of Molecular Sciences,2016,17(6):939-945.
[42] Tamura H,Takasaki A,Taketani T,et al. Melatonin and female reproduction[J]. Journal of Obstetrics and Gynaecology,2014,40(1):1-11.
[43] Tamura H,Takasaki A,Taketani T,et al. Melatonin as a free radical scavenger in the ovarian follicle[J]. Endocrine Journal,2013,60(1):1-13.
[44] Woo M M M,Tai C J,Kang K,et al. Direct action of melatonin in human granulosa-luteal cells[J]. The Journal of Clinical Endocrinology&Metabolism,2001,86(10):4789-4797.
[45] Shi J M,Tian X Z,Zhou G B,et al. Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes[J]. Journal of Pineal Research,2009,47(4):318-323.
[46] Tian X Z,Wang F,He C J,et al. Beneficial effects of melatonin on bovine oocytes maturation:a mechanistic approach[J]. Journal of Pineal Research,2014,57(3):239-247.
[47] Tian X Z,Wang F,Zhang L,et al. Beneficial effects of melatonin on the in vitro maturation of sheep oocytes and its relation to melatonin receptors[J].International Journal of Molecular Sciences,2017,18:834.
[48] Li Y,Zhang Z Z,He C J,et al. Melatonin protects porcine oocyte in vitro maturation from heat stress[J]. Journal of Pineal Research,2015,59(3):365-375.
[49] Shen M,Liu Z,Li B,et al. Involvement of FoxO 1 in the effects of follicle stimulating hormone on inhibition of apoptosis in mouse granulosa cells[J].Cell Death and Disease,2014,5:e1475.
[50] Shen M,Jiang Y,Guan Z,et al. Protective mechanism of FSH against oxidative damage in mouse ovarian granulosa cells by repressing autophagy[J].Autophagy,2017,13(8):1364-1385.
[51]王文绍,程玲,赵肖,等. miR-15a对猪卵泡颗粒细胞BDNF基因表达的影响[J].畜牧与兽医,2018,50(3):14-19.Wang W S,Cheng L,Zhao X,et al. MiR-15a inhibits the levels of porcine ovarian granulosa cell’s BDNF[J]. Animal Husbandry&Veterinary Medicine,2018,50(3):14-19(in Chinese with English abstract).
[52] Murdoch W J. Inhibition by oestradiol of oxidative stress-induced apoptosis in pig ovarian tissues[J]. J Reprod Fertil,1998,114:127-130.
[53] Besnard N,Pisselet C,Monniaux D,et al. Expression of messenger ribonucleic acids of insulin-like growth factor binding protein-2,-4,and-5 in the ovine ovary:localization and changes during growth and atresia of antral follicles[J]. Biol Reprod,1996,55(6):1356-1367.
[54] Teerds K J,Dorrington J H. Immunolocalization of transforming growth factor alpha and luteinizing hormone receptor in healthy and atretic follicles of the adult rat ovary[J]. Biol Reprod,1995,52(3):500-508.
[2] Morbech D E,Esbenshade K L,Flowers W L,et al. Kinetics of follicle growth in the prepuberal gilt[J]. Biol Reprod,1992,47:485-491.
[3] Dailey R A,Clark J R,Staigmiller R B,et al. Growth of new follicles following electrocautery in four genetic groups of swine[J]. J Anim Sci,1976,43:175-183.
[4] Foxcroft G R,Hunter M G. Basic physiology of follicular maturation in the pig[J]. J Reprod Fertil,1985,33:1-19.
[5] Guthrie H D,Cooper B S,Welch G R,et al. Atresia in follicles grown after ovulation in the pig:measurement of increased apoptosis in granulosacells and reduced follicular fluid estradiol-17 beta[J]. Biol Reprod,1995,52(4):920-927.
[6] Miller A T,Picton H M,Craigon J,et al. Follicle dynamics and aromatase activity in high-ovulating Meishan sows and in Large-White hybrid contemporaries[J]. Biol Reprod,1998,58:1372-1378.
[7] Manabe N,Imai Y,Ohno H,et al. Apoptosis occurs in granulosa cells but not cumulus cells in the atretic antral follicles in pig ovaries[J].Experientia,1996,52(7):647-651.
[8] Manabe N,Goto Y,Matsuda-Minehata F,et al. Regulation mechanism of selective atresia in porcine follicles:regulation of granulosa cell apoptosis during atresia[J]. J Reprod Dev,2004,50(5):493-514.
[9] Nakayama M,Manabe N,Inoue N,et al. 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[J]. Biol Reprod,2003,68(2):530-535.
[10] Inoue N,Maeda A,Matsuda-Minehata F,et al. Expression and localization of Fas ligand and Fas during atresia in porcine ovarian follicles[J].J Reprod Dev,2006,52(6):723-730.
[11] Worku T,Rehman Z,Talpur H,et al. MicroRNAs:new insight in modulating follicular atresia:a review[J]. Int J Mol Sci,2017,18(2):333.
[12] Lin F,Li R,Pan Z X,et al. miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary[J]. PLoS One,2012,7(6):e38640.
[13] Liu J,Du X,Zhou J,et al. MicroRNA-26b functions as a proapoptotic factor in porcine follicular granulosa cells by targeting Sma and Mad-related protein 4[J]. Biol Reprod,2014,91(6):1-12.
[14] Cao R,Wu W,Zhou X,et al. Let-7g induces granulosa cell apoptosis by targeting MAP3K1 in the porcine ovary[J]. Int J Biochem Cell Biol,2015,68:148-157.
[15] Zhou J L,Liu J Y,Pan Z X,et al. The let-7g microRNA promotes follicular granulosa cell apoptosis by targeting transforming growth factor-βtype 1 receptor[J]. Molecular and Cellular Endocrinology,2015,409:103-112.
[16] Liu J,Yao W,Yao Y,et al. MiR-92a inhibits porcine ovarian granulosa cell apoptosis by targeting Smad7 gene[J]. FEBS Letters,2014,588:4497-4503.
[17] Cassano E,Tosto L,Balestrieri M,et al. Antioxidant defense in the follicular fluid of water buffalo[J]. Cell Physiol Biochem,1999,9(2):106-116.
[18] Giuseppina B,Federico B,Francesca G,et al. The effects of reduced oxygen tension on swine granulosa cell[J]. Regulatory Peptides,2004,120:69-75.
[19] Lopez-Barneo J,Pardal R,Ortega-Saenz P. Cellular mechanism of oxygen sensing[J]. Annu Rev Physiol,2001,63:259-287.
[20] Gupta S,Choi A,Yu H Y,et al. Fluctuations in total antioxidant capacity,catalase activity and hydrogen peroxide levels of follicular fluid during bovine folliculogenesis[J]. Reprod Fertil Dev,2011,23(5):673-680.
[21] Margo L,Hope H,Yu Y,et al. Follicular fluid hydrogen peroxide and lipid hydroperoxide in bovine antral follicles of various size,atresia,and dominance status[J]. J Assist Reprod Genet,2013,30:333-340.
[22] Singh A K,Chattopadhyay R,Chakravarty B,et al. Markers of oxidative stress in follicular fluid of women with endometriosis and tubal infertility undergoing IVF[J]. Reprod Toxicol,2013,42:116-124.
[23] Jana S K,Chattopadhyay R,Chakravarty B,et al. Upper control limit of reactive oxygen species in follicular fluid beyond which viable embryo formation is not favorable[J]. Reprod Toxicol,2010,29(4):447-451.
[24] Basini G,Simona B,Santini S E,et al. Reactive oxygen species and anti-oxidant defences in swine follicular fluids[J]. Reprod Fertil Dev,2008,20:269-274.
[25] Matzuk M M,Dionne L,Guo Q,et al. Ovarian function in superoxide dismutase 1 and 2 knockout mice[J]. Endocrinology,1998,139:4008-4011.
[26] Ho Y S,Gargano M,Cao J,et al. Reduced fertility in female mice lacking copper-zinc superoxide dismutase[J]. J Biol Chem,1998,273:7765-7769.
[27] Wong P C,Waggoner D,Subramaniam J R,et al. Copper chaperone for superoxide dismutase is essential to activate mammalian cu/zn superoxide dismutase[J]. Proc Natl Acad Sci USA,2000,97:2886-2891.
[28] Kumar T R,Wiseman A L,Kala G,et al. Reproductive defects inγ-glutamyl transpeptidase deficient mice[J]. Endocrinology,2000,141:4270-4277.
[29] Lin J,Nakamura B N,Mohar L,et al. Glutamate cysteine ligase modifier subunit(Gclm)null mice have increased ovarian oxidative stress and accelerated age-related ovarian failure[J]. Endocrinology,2015,156(9):3329-3343.
[30] Patrick J D,Sally D P,Luderer U. Role of reactive oxygen species and antioxidants in ovarian toxicity[J]. Biol Reprod,2012,86(2):1-10.
[31] Zhang J Q,Shen M,Zhu C C,et al. 3-nitropropionic acid induces ovarian oxidative stress and impairs follicle in mouse[J]. PLoS One,2014,9(2):e86589.
[32] Luderer U. Ovarian toxicity from reactive oxygen species[J]. Vitam Horm,2014,94:99-127.
[33] Lopez S G,Luderer U. Effects of cyclophosphamide and buthionine sulfoximine on ovarian glutathione and apoptosis[J]. Free Radic Biol Med,2004,36:1366-1377.
[34] Tsai-Turton M,Luderer U. Gonadotropin regulation of glutamate cysteine ligase catalytic and modifier subunit expression in rat ovary is subunit and follicle stage specific[J]. Am J Physiol Endocrinol Metab,2005,289:E391-E402.
[35] Tsai-Turton M,Luderer U. Opposing effects of glutathione depletion and FSH on reactive oxygen species and apoptosis in cultured preovulatory rat follicles[J]. Endocrinology,2006,147:1224-1236.
[36] Shen M,Lin F,Zhang J Q,et al. Involvement of the up-regulated FoxO 1 expression in follicular granulosa cell apoptosis induced by oxidative stress[J]. J Biol Chem,2012,287(31):25727-25740.
[37] Liu Z Q,Shen M,Wu W J,et al. Expression of PUMA in follicular granulosa cells regulated by FoxO 1 activation during oxidative stress[J].Reprod Sci,2015,22(6):696-705.
[38] Essers M A G,Weijzen S,de Vries-Smits A M M,et al. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK[J]. The EMBO Journal,2004,23(24):4802-4812.
[39] Sunayama J,Tsuruta F,Masuyama N,et al. JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3[J]. The Journal of Cell Biology,2005,170(2):295-304.
[40] Weng Q,Liu Z,Li B,et al. Oxidative stress induces mouse follicular granulosa cells apoptosis via JNK/FoxO 1 pathway[J]. PLoS One,2016,11(12):e0167869.
[41] He C J,Wang J,Zhang Z Z,et al. Mitochondria synthesize melatonin to ameliorate its function and improve mice oocyte’s quality under in vitro conditions[J]. International Journal of Molecular Sciences,2016,17(6):939-945.
[42] Tamura H,Takasaki A,Taketani T,et al. Melatonin and female reproduction[J]. Journal of Obstetrics and Gynaecology,2014,40(1):1-11.
[43] Tamura H,Takasaki A,Taketani T,et al. Melatonin as a free radical scavenger in the ovarian follicle[J]. Endocrine Journal,2013,60(1):1-13.
[44] Woo M M M,Tai C J,Kang K,et al. Direct action of melatonin in human granulosa-luteal cells[J]. The Journal of Clinical Endocrinology&Metabolism,2001,86(10):4789-4797.
[45] Shi J M,Tian X Z,Zhou G B,et al. Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes[J]. Journal of Pineal Research,2009,47(4):318-323.
[46] Tian X Z,Wang F,He C J,et al. Beneficial effects of melatonin on bovine oocytes maturation:a mechanistic approach[J]. Journal of Pineal Research,2014,57(3):239-247.
[47] Tian X Z,Wang F,Zhang L,et al. Beneficial effects of melatonin on the in vitro maturation of sheep oocytes and its relation to melatonin receptors[J].International Journal of Molecular Sciences,2017,18:834.
[48] Li Y,Zhang Z Z,He C J,et al. Melatonin protects porcine oocyte in vitro maturation from heat stress[J]. Journal of Pineal Research,2015,59(3):365-375.
[49] Shen M,Liu Z,Li B,et al. Involvement of FoxO 1 in the effects of follicle stimulating hormone on inhibition of apoptosis in mouse granulosa cells[J].Cell Death and Disease,2014,5:e1475.
[50] Shen M,Jiang Y,Guan Z,et al. Protective mechanism of FSH against oxidative damage in mouse ovarian granulosa cells by repressing autophagy[J].Autophagy,2017,13(8):1364-1385.
[51]王文绍,程玲,赵肖,等. miR-15a对猪卵泡颗粒细胞BDNF基因表达的影响[J].畜牧与兽医,2018,50(3):14-19.Wang W S,Cheng L,Zhao X,et al. MiR-15a inhibits the levels of porcine ovarian granulosa cell’s BDNF[J]. Animal Husbandry&Veterinary Medicine,2018,50(3):14-19(in Chinese with English abstract).
[52] Murdoch W J. Inhibition by oestradiol of oxidative stress-induced apoptosis in pig ovarian tissues[J]. J Reprod Fertil,1998,114:127-130.
[53] Besnard N,Pisselet C,Monniaux D,et al. Expression of messenger ribonucleic acids of insulin-like growth factor binding protein-2,-4,and-5 in the ovine ovary:localization and changes during growth and atresia of antral follicles[J]. Biol Reprod,1996,55(6):1356-1367.
[54] Teerds K J,Dorrington J H. Immunolocalization of transforming growth factor alpha and luteinizing hormone receptor in healthy and atretic follicles of the adult rat ovary[J]. Biol Reprod,1995,52(3):500-508.