外源物暴露所致卵巢发育毒性相关发生机制的研究进展
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摘要
卵巢的结构和功能对于女性生育力的维系具有重要意义,大量流行病学调查和动物实验研究表明,孕期所接触的多种外源物,如有机挥发物等的环境毒物、含有可卡因等成分的药物、吸烟或过量饮用酒及咖啡等不良生活习惯,不仅影响母体健康,更会对其子代的卵巢发育、功能维护及成年后生殖健康产生不利影响。故就孕期外源物暴露对子代卵巢发育的影响及其机制作一综述。
The structure and function of ovary is of great significance to the maintenance of female fertility. A large number of epidemiological surveys and animal studies have shown that a variety of exogenous substances exposure during pregnancy not only affect the mother's health, but also adversely affect the offspring's ovarian development, ovarian function, and adult reproductive health.Exogenous substances contrain environmental toxicants such as organic volatile, drugs containing cocaine, smoking, excessive drinking and coffee. This article reviews the influence of prenatal xenobiotic exposure to ovarian development and the potential mechanisms.
The structure and function of ovary is of great significance to the maintenance of female fertility. A large number of epidemiological surveys and animal studies have shown that a variety of exogenous substances exposure during pregnancy not only affect the mother's health, but also adversely affect the offspring's ovarian development, ovarian function, and adult reproductive health.Exogenous substances contrain environmental toxicants such as organic volatile, drugs containing cocaine, smoking, excessive drinking and coffee. This article reviews the influence of prenatal xenobiotic exposure to ovarian development and the potential mechanisms.
引文
[1]Adams GP,Jaiswal R,Singh J,et al.Progress in understanding ovarian follicular dynamics in cattle[J].Theriogenology,2008,69(1):72-80.DOI:10.1016/j.theriogenology.2007.09.026.
[2]Johansson H,Svingen T,Fowler PA,et al.Environmental influences on ovarian dysgenesis-developmental windows sensitive to chemical exposures[J].Nat Rev Endocrinol,2017,13(7):400-414.DOI:10.1038/nrendo.2017.36.
[3]Saatcioglu HD,Cuevas I,Castrillon DH.Control of oocyte reawakening by kit[J].PLoS Genet,2016,12(8):e1006215.DOI:10.1371/journal.pgen.1006215.
[4]Wang C,Zhou B,Xia G.Mechanisms controlling germline cyst breakdown and primordial follicle formation[J].Cell Mol Life Sci,2017,74(14):2547-2566.DOI:10.1007/s00018-017-2480-6.
[5]Anderson RA,Mcilwain L,Coutts S,et al.Activation of the aryl hydrocarbon receptor by a component of cigarette smoke reduces germ cell proliferation in the human fetal ovary[J].Mol Hum Reprod,2014,20(1):42-48.DOI:10.1093/molehr/gat059.
[6]Gosden R,Lee B.Portrait of an oocyte:our obscure origin[J].J Clin Invest,2010,120(4):973-983.DOI:10.1172/JCI41294.
[7]Seki Y,Okashita N.Epigenetic reprogramming in primordial germ cells in mice[J].J Mammalian Ova Res,2013,30(3):95-100.DOI:10.1274/jmor.30.95.
[8]Saitou M,Yamaji M.Primordial germ cells in mice[J].Cold Spring Harb Perspect Biol,2012,4(11):59-66.DOI:10.1101/cshperspect.a008375.
[9]Pepling ME.Follicular assembly:mechanisms of action[J].Reproduction,2012,143(2):139-149.DOI:10.1530/REP-11-0299.
[10]Pepling ME,Sundman EA,Patterson NL,et al.Differences in oocyte development and estradiol sensitivity among mouse strains[J].Reproduction,2010,139(2):349-357.DOI:10.1530/REP-09-0392.
[11]Kezele P,Nilsson E,Skinner MK.Cell-cell interactions in primordial follicle assembly and development[J].Front Biosci,2002,7:d1990-d1996.DOI:10.2741/kezele.
[12]Sarraj MA,Drummond AE.Mammalian foetal ovarian development:consequences for health and disease[J].Reproduction,2012,143(2):151-163.DOI:10.1530/REP-11-0247.
[13]Nikolaou D,Templeton A.Early ovarian ageing[J].Eur J Obstet Gynecol Reprod Biol,2004,113(2):126-133.DOI:10.1016/j.ejogrb.2003.09.024.
[14]Ding X,Zhang X,Mu Y,et al.Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via upregulation of Sohlh2 and c-kit[J].Mol Reprod Dev,2013,80(1):70-78.DOI:10.1002/mrd.22138.
[15]Feng L,Wang Y,Cai H,et al.ADAM10-Notch signaling governs the recruitment of ovarian pregranulosa cells and controls folliculogenesis in mice[J].J Cell Sci,2016,129(11):2202-2212.DOI:10.1242/jcs.184267.
[16]Gustin SE,Hogg K,Stringer JM,et al.WNT/beta-catenin and p27/FOXL2 differentially regulate supporting cell proliferation in the developing ovary[J].Dev Biol,2016,412(2):250-260.DOI:10.1016/j.ydbio.2016.02.024.
[17]Diaz FJ,O’Brien MJ,Wigglesworth K,et al.The preantral granulosa cell to cumulus cell transition in the mouse ovary:development of competence to undergo expansion[J].Dev Biol,2006,299(1):91-104.DOI:10.1016/j.ydbio.2006.07.012.
[18]Su YQ,Sugiura K,Woo Y,et al.Selective degradation of transcripts during meiotic maturation of mouse oocytes[J].Dev Biol,2007,302(1):104-117.DOI:10.1016/j.ydbio.2006.09.008.
[19]Zhang C,Liu XR,Cao YC,et al.Mammalian target of rapamycin/eukaryotic initiation factor 4F pathway regulates follicle growth and development of theca cells in mice[J].Reprod Fertil Dev,2017,29(4):768-777.DOI:10.1071/RD15230.
[20]Ding X,Zhang X,Mu Y,et al.Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via upregulation of Sohlh2 and c-kit[J].Mol Reprod Dev,2013,80(1):70-78.DOI:10.1002/mrd.22138.
[21]Terauchi KJ,Shigeta Y,Iguchi T,et al.Role of Notch signaling in granulosa cell proliferation and polyovular follicle induction during folliculogenesis in mouse ovary[J].Cell Tissue Res,2016,365(1):197-208.DOI:10.1007/s00441-016-2371-4.
[22]Feng L,Wang Y,Cai H,et al.ADAM10-Notch signaling governs the recruitment of ovarian pregranulosa cells and controls folliculogenesis in mice[J].J Cell Sci,2016,129(11):2202-2212.DOI:10.1242/jcs.184267.
[23]Hernandez GJ.The role of WNT signaling in adult ovarian folliculogenesis[J].Reproduction,2015,150(4):R137-R148.DOI:10.1530/REP-14-0685.
[24]Forbes K,Shah VK,Siddals K,et al.Statins inhibit insulin-like growth factor action in first trimester placenta by altering insulin-like growth factor 1 receptor glycosylation[J].Mol Hum Reprod,2015,21(1):105-114.DOI:10.1093/molehr/gau093.
[25]Depalo R,Nappi L,Loverro G,et al.Evidence of apoptosis in human primordial and primary follicles[J].Hum Reprod,2003,18(12):2678-2682.DOI:10.1093/humrep/deg507.
[26]Scaramuzzi RJ,Brown HM,Dupont J.Nutritional and metabolic mechanisms in the ovary and their role in mediating the effects of diet on folliculogenesis:a perspective[J].Reprod Domest Anim,2010,45Suppl 3:32-41.DOI:10.1111/j.1439-0531.2010.01662.x
[27]Liang B,Wei DL,Cheng YN,et al.Restraint stress impairs oocyte developmental potential in mice:role of CRH-induced apoptosis of ovarian cells[J].Biol Reprod,2013,89(3):64.DOI:10.1095/biolreprod.113.110619.
[28]Uzumcu M,Zachow R.Developmental exposure to environmental endocrine disruptors:consequences within the ovary and on female reproductive function[J].Reprod Toxicol,2007,23(3):337-352.DOI:10.1016/j.reprotox.2006.10.006.
[29]Rimon-Dahari N,Yerushalmi-Heinemann L,Alyagor L,et al.Ovarian Folliculogenesis[J].Results Probl Cell Differ,2016,58:167-190.DOI:10.1007/978-3-319-31973-5_7.
[30]USEPA.Guidelines for Reproductive Toxicity Risk Assessment[S].1996.
[31]Mamsen LS,Lutterodt MC,Andersen EW,et al.Cigarette smoking during early pregnancy reduces the number of embryonic germ and somatic cells[J].Hum Reprod,2010,25(11):2755-2761.DOI:10.1093/humrep/deq215.
[32]Ronnbock C.Effects of 3,3’,4,4’-tetrachlorobiphenyl(TCB)on ovaries of foetal mice[J].Pharmacol Toxicol,1991,68(5):340-345.DOI:10.1111/j.1600-0773.1991.tb01250.x.
[33]Ronnback C,de Rooij DG.Effects of 3,3’,4,4’-tetrachlorobiphenyl on foetal germ cells in two mouse strains after repeated treatment of the dams during and after pregnancy[J].Pharmacol Toxicol,1994,74(4/5):287-293.DOI:10.1111/j.1600-0773.1994.tb01113.x.
[34]Hoyer PB,Sipes IG.Assessment of follicle destruction in chemicalinduced ovarian toxicity[J].Annu Rev Pharmacol Toxicol,1996,36:307-331.DOI:10.1146/annurev.pa.36.040196.001515.
[35]Susiarjo M,Hassold TJ,Freeman E,et al.Bisphenol A exposure in utero disrupts early oogenesis in the mouse[J].PLoS Genet,2007,3(1):e5.DOI:10.1371/journal.pgen.0030005.
[36]Signorile PG,Spugnini EP,Citro G,et al.Endocrine disruptors in utero cause ovarian damages linked to endometriosis[J].Front Biosci(Elite Ed),2012,4:1724-1730.DOI:10.2741/493.
[37]Zhang HQ,Zhang XF,Zhang LJ,et al.Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes[J].Mol Biol Rep,2012,39(5):5651-5657.DOI:10.1007/s11033-011-1372-3.
[38]Matikainen TM,Moriyama T,Morita Y,et al.Ligand activation of the aromatic hydrocarbon receptor transcription factor drives Baxdependent apoptosis in developing fetal ovarian germ cells[J].Endocrinology,2002,143(2):615-620.DOI:10.1210/endo.143.2.8624.
[39]Barker DJ.Fetal origins of coronary heart disease[J].BMJ,1995,311(6998):171-174.DOI:10.1136/bmj.311.6998.171.
[40]Richardson MC,Guo M,Fauser BC,et al.Environmental and developmental origins of ovarian reserve[J].Hum Reprod Update,2014,20(3):353-369.DOI:10.1093/humupd/dmt057.
[41]Lilienthal H,Hack A,Roth-Harer A,et al.Effects of developmental exposure to 2,2,4,4,5-pentabromodiphenyl ether(PBDE-99)on sex steroids,sexual development,and sexually dimorphic behavior in rats[J].Environ Health Perspect,2006,114(2):194-201.DOI:10.1289/ehp.8391.
[42]Windham GC,Bottomley C,Birner C,et al.Age at menarche in relation to maternal use of tobacco,alcohol,coffee,and tea during pregnancy[J].Am J Epidemiol,2004,159(9):862-871.DOI:10.1093/aje/kwh117.
[43]Shrestha A,Nohr EA,Bech BH,et al.Smoking and alcohol use during pregnancy and age of menarche in daughters[J].Hum Reprod,2011,26(1):259-265.DOI:10.1093/humrep/deq316.
[44]Carter RC,Jacobson JL,Molteno CD,et al.Effects of heavy prenatal alcohol exposure and iron deficiency anemia on child growth and body composition through age 9 years[J].Alcohol Clin Exp Res,2012,36(11):1973-1982.DOI:10.1111/j.1530-0277.2012.01810.x.
[45]Pan Z,Zhang X,Shangguan Y,et al.Suppressed osteoclast differentiation at the chondro-osseous junction mediates endochondral ossification retardation in long bones of Wistar fetal rats with prenatal ethanol exposure[J].Toxicol Appl Pharmacol,2016,305:234-241.DOI:10.1016/j.taap.2016.06.021.
[46]Ibanez L,Potau N,Enriquez G,et al.Reduced uterine and ovarian size in adolescent girls born small for gestational age[J].Pediatr Res,2000,47(5):575-577.DOI:10.1203/00006450-200005000-00003.
[47]Manikkam M,Guerrero-Bosagna C,Tracey R,et al.Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures[J].PLoSOne,2012,7(2):e31901.DOI:10.1371/journal.pone.0031901.
[48]Hruska KS,Furth PA,Seifer DB,et al.Environmental factors in infertility[J].Clin Obstet Gynecol,2000,43(4):821-829.DOI:10.1097/00003081-200012000-00014.
[49]Kilic S,Yuksel B,Lortlar N,et al.Environmental tobacco smoke exposure during intrauterine period promotes granulosa cell apoptosis:a prospective,randomized study[J].J Matern Fetal Neonatal Med,2012,25(10):1904-1908.DOI:10.3109/14767058.2012.678440.
[50]Lutterodt MC,Sorensen KP,Larsen KB,et al.The number of oogonia and somatic cells in the human female embryo and fetus in relation to whether or not exposed to maternal cigarette smoking[J].Hum Reprod,2009,24(10):2558-2566.DOI:10.1093/humrep/dep226.
[51]Wo l f C J,Ostby J S,Gray LJ.Ges t a t ional exposure to2,3,7,8-tetrachlorodibenzo-p-dioxin(TCDD)severely alters reproductive function of female hamster offspring[J].Toxicol Sci,1999,51(2):259-264.DOI:10.1093/toxsci/51.2.259.
[52]Jablonska O,Shi Z,Valdez KE,et al.Temporal and anatomical s e n s i t i v i t i e s to t h e a r y l hydrocarbon r ec e p to r a g o n i s t2,3,7,8-tetrachlorodibenzo-p-dioxin leading to premature acyclicity with age in rats[J].Int J Androl,2010,33(2):405-412.DOI:10.1111/j.1365-2605.2009.01031.x.
[53]Xita N,Tsatsoulis A.Review:fetal programming of polycystic ovary syndrome by androgen excess:evidence from experimental,clinical,and genetic association studies[J].J Clin Endocrinol Metab,2006,91(5):1660-1666.DOI:10.1210/jc.2005-2757.
[54]Hague WM,Adams J,Rodda C,et al.The prevalence of polycystic ovaries in patients with congenital adrenal hyperplasia and their close relatives[J].Clin Endocrinol(Oxf),1990,33(4):501-510.DOI:10.1111/j.1365-2265.1990.tb03887.x.
[55]Rutkowska AZ,Diamanti-Kandarakis E.Polycystic ovary syndrome and environmental toxins[J].Fertil Steril,2016,106(4):948-958.DOI:10.1016/j.fertnstert.2016.08.031.
[56]Hewlett M,Chow E,Aschengrau A,et al.Prenatal exposure to endocrine disruptors:a developmental etiology for polycystic ovary syndrome[J].Reprod Sci,2016,pii:1933719116654992.DOI:10.1177/1933719116654992.
[57]Grossniklaus U,Ke l l y WG,Ferguson-Smith AC,e t a l.Transgenerational epigenetic inheritance:how important is it?[J].Nat Rev Genet,2013,14(3):228-235.DOI:10.1038/nrg3435.
[58]Pocar P,Augustin R,Gandolfi F,et al.Toxic effects of in vitro exposure to p-tert-octylphenol on bovine oocyte maturation and developmental competence[J].Biol Reprod,2003,69(2):462-468.DOI:10.1095/biolreprod.102.010355.
[59]Bhattacharya P,Keating AF.Impact of environmental exposures on ovarian function and role of xenobiotic metabolism during ovotoxicity[J].Toxicol Appl Pharmacol,2012,261(3):227-235.DOI:10.1016/j.taap.2012.04.009.
[60]Fowler PA,Childs AJ,Courant F,et al.In utero exposure to cigarette smoke dysregulates human fetal ovarian developmental signalling[J].Hum Reprod,2014,29(7):1471-1489.DOI:10.1093/humrep/deu117.
[61]Bhattacharya P,Sen N,Hoyer PB,et al.Ovarian expressed microsomal epoxide hydrolase:role in detoxification of 4-vinylcyclohexene diepoxide and regulation by phosphatidylinositol-3 kinase signaling[J].Toxicol Appl Pharmacol,2012,258(1):118-123.DOI:10.1016/j.taap.2011.10.014.
[62]Xu J,Osuga Y,Yano T,et al.Bisphenol A induces apoptosis and G2-to-M arrest of ovarian granulosa cells[J].Biochem Biophys Res Commun,2002,292(2):456-462.DOI:10.1006/bbrc.2002.6644.
[63]Piferrer F.Epigenetics of sex determination and gonadogenesis[J].Dev Dyn,2013,242(4):360-370.DOI:10.1002/dvdy.23924.
[64]Zhang T,Shen W,De Felici M,et al.Di(2-ethylhexyl)phthalate:Adverse effects on folliculogenesis that cannot be neglected[J].Environ Mol Mutagen,2016,57(8):579-588.DOI:10.1002/em.22037.
[65]Haddad R,Kasneci A,Mepham K,et al.Gestational exposure to diethylstilbestrol alters cardiac structure/function,protein expression and DNA methylation in adult male mice progeny[J].Toxicol Appl Pharmacol,2013,266(1):27-37.DOI:10.1016/j.taap.2012.10.018.
[66]Bohacek J,Gapp K,Saab BJ,et al.Transgenerational epigenetic effects on brain functions[J].Biol Psychiatry,2013,73(4):313-320.DOI:10.1016/j.biopsych.2012.08.019.
[67]Martinez-Arguelles DB,Papadopoulos V.Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action[J].Steroids,2010,75(7):467-476.DOI:10.1016/j.steroids.2010.02.004.
[68]Li H,Liu J,Sun Y,et al.N-hexane inhalation during pregnancy alters DNA promoter methylation in the ovarian granulosa cells of rat offspring[J].J Appl Toxicol,2014,34(8):841-856.DOI:10.1002/jat.2893.
[69]Li H,Zhang C,Ni F,et al.Gestational N-hexane inhalation alters the expression of genes related to ovarian hormone production and DNAmethylation states in adult female F1 rat offspring[J].Toxicol Lett,2015,239(3):141-151.DOI:10.1016/j.toxlet.2015.09.018.
[70]Xia Y,Shen S,Zhang X,et al.Epigenetic pattern changes in prenatal female Sprague-Dawley rats following exposure to androgen[J].Reprod Fertil Dev,2015.DOI:10.1071/RD14292.
[71]Feng YM,Liang GJ,Pan B,et al.Notch pathway regulates female germ cell meiosis progression and early oogenesis events in fetal mouse[J].Cell Cycle,2014,13(5):782-791.DOI:10.4161/cc.27708.
[72]Zhang XF,Zhang T,Han Z,et al.Transgenerational inheritance of ovarian development deficiency induced by maternal diethylhexyl phthalate exposure[J].Reprod Fertil Dev,2015,27(8):1213-1221.DOI:10.1071/RD14113.
[73]Li L,Zhang T,Qin XS,et al.Exposure to diethylhexyl phthalate(DEHP)results in a heritable modification of imprint genes DNA methylation in mouse oocytes[J].Mol Biol Rep,2014,41(3):1227-1235.DOI:10.1007/s11033-013-2967-7.
[74]Feng X,Wang X,Cao X,et al.Chronic exposure of female mice to an environmental level of perfluorooctane sulfonate suppresses estrogen synthesis through reduced histone H3K14 acetylation of the StARpromoter leading to deficits in follicular development and ovulation[J].Toxicol Sci,2015,148(2):368-379.DOI:10.1093/toxsci/kfv197.
[75]Govorko D,Bekdash RA,Zhang C,et al.Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations[J].Biol Psychiatry,2012,72(5):378-388.DOI:10.1016/j.biopsych.2012.04.006.
[76]Iqbal M,Moisiadis VG,Kostaki A,et al.Transgenerational effects of prenatal synthetic glucocorticoids on hypothalamic-pituitary-adrenal function[J].Endocrinology,2012,153(7):3295-3307.DOI:10.1210/en.2012-1054.
[77]Liu T,Li N,Zhu J,et al.Effects of di-(2-ethylhexyl)phthalate on the hypothalamus-pituitary-ovarian axis in adult female rats[J].Reprod Toxicol,2014,46:141-147.DOI:10.1016/j.reprotox.2014.03.006.
[78]Sun Y,Lin Y,Li H,et al.2,5-Hexanedione induces human ovarian granulosa cell apoptosis through BCL-2,BAX,and CASPASE-3signaling pathways[J].Arch Toxicol,2012,86(2):205-215.DOI:10.1007/s00204-011-0745-7.
[79]Zhang W,Huang L,Kong C,et al.Apoptosis of rat ovarian granulosa cells by 2,5-hexanedione in vitro and its relevant gene expression[J].JAppl Toxicol,2013,33(7):661-669.DOI:10.1002/jat.2714.
[80]Zama AM,Uzumcu M.Targeted genome-wide methylation and gene expression analyses reveal signaling pathways involved in ovarian dysfunction after developmental EDC exposure in rats[J].Biol Reprod,2013,88(2):52.DOI:10.1095/biolreprod.112.104802.
[81]Kwintkiewicz J,Nishi Y,Yanase T,et al.Peroxisome proliferatoractivated receptor-gamma mediates bisphenol A inhibition of FSHstimulated IGF-1,aromatase,and estradiol in human granulosa cells[J].Environ Health Perspect,2010,118(3):400-406.DOI:10.1289/ehp.0901161.
[82]Abolaji AO,Adedara IA,Soladogun A,et al.Exposure to2,5-hexanedione is accompanied by ovarian and uterine oxidative stress and disruption of endocrine balance in rats[J].Drug Chem Toxicol,2015,38(4):400-407.DOI:10.3109/01480545.2014.974265.
[83]Sliwowska JH,Comeau WL,Bodnar TS,et al.Prenatal alcohol exposure and pair feeding differentially impact puberty and reproductive development in female rats:role of the Kisspeptin system[J].Alcohol Clin Exp Res,2016,40(11):2368-2376.DOI:10.1111/acer.13233.
[84]Lan N,Yamashita F,Halpert AG,et al.Effects of prenatal ethanol exposure on hypothalamic-pituitary-adrenal function across the estrous cycle[J].Alcohol Clin Exp Res,2009,33(6):1075-1088.DOI:10.1111/j.1530-0277.2009.00929.x.
[85]Dees WL,Hiney JK,Srivastava VK.Alcohol alters hypothalamic glialneuronal communications involved in the neuroendocrine control of puberty:In vivo and in vitro assessments[J].Alcohol,2015,49(7):631-637.DOI:10.1016/j.alcohol.2015.08.001.
[86]Gamez JM,Penalba R,Cardoso N,et al.Exposure to a low dose of bisphenol A impairs pituitary-ovarian axis in prepubertal rats:effects on early folliculogenesis[J].Environ Toxicol Pharmacol,2015,39(1):9-15.DOI:10.1016/j.etap.2014.10.015.
[2]Johansson H,Svingen T,Fowler PA,et al.Environmental influences on ovarian dysgenesis-developmental windows sensitive to chemical exposures[J].Nat Rev Endocrinol,2017,13(7):400-414.DOI:10.1038/nrendo.2017.36.
[3]Saatcioglu HD,Cuevas I,Castrillon DH.Control of oocyte reawakening by kit[J].PLoS Genet,2016,12(8):e1006215.DOI:10.1371/journal.pgen.1006215.
[4]Wang C,Zhou B,Xia G.Mechanisms controlling germline cyst breakdown and primordial follicle formation[J].Cell Mol Life Sci,2017,74(14):2547-2566.DOI:10.1007/s00018-017-2480-6.
[5]Anderson RA,Mcilwain L,Coutts S,et al.Activation of the aryl hydrocarbon receptor by a component of cigarette smoke reduces germ cell proliferation in the human fetal ovary[J].Mol Hum Reprod,2014,20(1):42-48.DOI:10.1093/molehr/gat059.
[6]Gosden R,Lee B.Portrait of an oocyte:our obscure origin[J].J Clin Invest,2010,120(4):973-983.DOI:10.1172/JCI41294.
[7]Seki Y,Okashita N.Epigenetic reprogramming in primordial germ cells in mice[J].J Mammalian Ova Res,2013,30(3):95-100.DOI:10.1274/jmor.30.95.
[8]Saitou M,Yamaji M.Primordial germ cells in mice[J].Cold Spring Harb Perspect Biol,2012,4(11):59-66.DOI:10.1101/cshperspect.a008375.
[9]Pepling ME.Follicular assembly:mechanisms of action[J].Reproduction,2012,143(2):139-149.DOI:10.1530/REP-11-0299.
[10]Pepling ME,Sundman EA,Patterson NL,et al.Differences in oocyte development and estradiol sensitivity among mouse strains[J].Reproduction,2010,139(2):349-357.DOI:10.1530/REP-09-0392.
[11]Kezele P,Nilsson E,Skinner MK.Cell-cell interactions in primordial follicle assembly and development[J].Front Biosci,2002,7:d1990-d1996.DOI:10.2741/kezele.
[12]Sarraj MA,Drummond AE.Mammalian foetal ovarian development:consequences for health and disease[J].Reproduction,2012,143(2):151-163.DOI:10.1530/REP-11-0247.
[13]Nikolaou D,Templeton A.Early ovarian ageing[J].Eur J Obstet Gynecol Reprod Biol,2004,113(2):126-133.DOI:10.1016/j.ejogrb.2003.09.024.
[14]Ding X,Zhang X,Mu Y,et al.Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via upregulation of Sohlh2 and c-kit[J].Mol Reprod Dev,2013,80(1):70-78.DOI:10.1002/mrd.22138.
[15]Feng L,Wang Y,Cai H,et al.ADAM10-Notch signaling governs the recruitment of ovarian pregranulosa cells and controls folliculogenesis in mice[J].J Cell Sci,2016,129(11):2202-2212.DOI:10.1242/jcs.184267.
[16]Gustin SE,Hogg K,Stringer JM,et al.WNT/beta-catenin and p27/FOXL2 differentially regulate supporting cell proliferation in the developing ovary[J].Dev Biol,2016,412(2):250-260.DOI:10.1016/j.ydbio.2016.02.024.
[17]Diaz FJ,O’Brien MJ,Wigglesworth K,et al.The preantral granulosa cell to cumulus cell transition in the mouse ovary:development of competence to undergo expansion[J].Dev Biol,2006,299(1):91-104.DOI:10.1016/j.ydbio.2006.07.012.
[18]Su YQ,Sugiura K,Woo Y,et al.Selective degradation of transcripts during meiotic maturation of mouse oocytes[J].Dev Biol,2007,302(1):104-117.DOI:10.1016/j.ydbio.2006.09.008.
[19]Zhang C,Liu XR,Cao YC,et al.Mammalian target of rapamycin/eukaryotic initiation factor 4F pathway regulates follicle growth and development of theca cells in mice[J].Reprod Fertil Dev,2017,29(4):768-777.DOI:10.1071/RD15230.
[20]Ding X,Zhang X,Mu Y,et al.Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via upregulation of Sohlh2 and c-kit[J].Mol Reprod Dev,2013,80(1):70-78.DOI:10.1002/mrd.22138.
[21]Terauchi KJ,Shigeta Y,Iguchi T,et al.Role of Notch signaling in granulosa cell proliferation and polyovular follicle induction during folliculogenesis in mouse ovary[J].Cell Tissue Res,2016,365(1):197-208.DOI:10.1007/s00441-016-2371-4.
[22]Feng L,Wang Y,Cai H,et al.ADAM10-Notch signaling governs the recruitment of ovarian pregranulosa cells and controls folliculogenesis in mice[J].J Cell Sci,2016,129(11):2202-2212.DOI:10.1242/jcs.184267.
[23]Hernandez GJ.The role of WNT signaling in adult ovarian folliculogenesis[J].Reproduction,2015,150(4):R137-R148.DOI:10.1530/REP-14-0685.
[24]Forbes K,Shah VK,Siddals K,et al.Statins inhibit insulin-like growth factor action in first trimester placenta by altering insulin-like growth factor 1 receptor glycosylation[J].Mol Hum Reprod,2015,21(1):105-114.DOI:10.1093/molehr/gau093.
[25]Depalo R,Nappi L,Loverro G,et al.Evidence of apoptosis in human primordial and primary follicles[J].Hum Reprod,2003,18(12):2678-2682.DOI:10.1093/humrep/deg507.
[26]Scaramuzzi RJ,Brown HM,Dupont J.Nutritional and metabolic mechanisms in the ovary and their role in mediating the effects of diet on folliculogenesis:a perspective[J].Reprod Domest Anim,2010,45Suppl 3:32-41.DOI:10.1111/j.1439-0531.2010.01662.x
[27]Liang B,Wei DL,Cheng YN,et al.Restraint stress impairs oocyte developmental potential in mice:role of CRH-induced apoptosis of ovarian cells[J].Biol Reprod,2013,89(3):64.DOI:10.1095/biolreprod.113.110619.
[28]Uzumcu M,Zachow R.Developmental exposure to environmental endocrine disruptors:consequences within the ovary and on female reproductive function[J].Reprod Toxicol,2007,23(3):337-352.DOI:10.1016/j.reprotox.2006.10.006.
[29]Rimon-Dahari N,Yerushalmi-Heinemann L,Alyagor L,et al.Ovarian Folliculogenesis[J].Results Probl Cell Differ,2016,58:167-190.DOI:10.1007/978-3-319-31973-5_7.
[30]USEPA.Guidelines for Reproductive Toxicity Risk Assessment[S].1996.
[31]Mamsen LS,Lutterodt MC,Andersen EW,et al.Cigarette smoking during early pregnancy reduces the number of embryonic germ and somatic cells[J].Hum Reprod,2010,25(11):2755-2761.DOI:10.1093/humrep/deq215.
[32]Ronnbock C.Effects of 3,3’,4,4’-tetrachlorobiphenyl(TCB)on ovaries of foetal mice[J].Pharmacol Toxicol,1991,68(5):340-345.DOI:10.1111/j.1600-0773.1991.tb01250.x.
[33]Ronnback C,de Rooij DG.Effects of 3,3’,4,4’-tetrachlorobiphenyl on foetal germ cells in two mouse strains after repeated treatment of the dams during and after pregnancy[J].Pharmacol Toxicol,1994,74(4/5):287-293.DOI:10.1111/j.1600-0773.1994.tb01113.x.
[34]Hoyer PB,Sipes IG.Assessment of follicle destruction in chemicalinduced ovarian toxicity[J].Annu Rev Pharmacol Toxicol,1996,36:307-331.DOI:10.1146/annurev.pa.36.040196.001515.
[35]Susiarjo M,Hassold TJ,Freeman E,et al.Bisphenol A exposure in utero disrupts early oogenesis in the mouse[J].PLoS Genet,2007,3(1):e5.DOI:10.1371/journal.pgen.0030005.
[36]Signorile PG,Spugnini EP,Citro G,et al.Endocrine disruptors in utero cause ovarian damages linked to endometriosis[J].Front Biosci(Elite Ed),2012,4:1724-1730.DOI:10.2741/493.
[37]Zhang HQ,Zhang XF,Zhang LJ,et al.Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes[J].Mol Biol Rep,2012,39(5):5651-5657.DOI:10.1007/s11033-011-1372-3.
[38]Matikainen TM,Moriyama T,Morita Y,et al.Ligand activation of the aromatic hydrocarbon receptor transcription factor drives Baxdependent apoptosis in developing fetal ovarian germ cells[J].Endocrinology,2002,143(2):615-620.DOI:10.1210/endo.143.2.8624.
[39]Barker DJ.Fetal origins of coronary heart disease[J].BMJ,1995,311(6998):171-174.DOI:10.1136/bmj.311.6998.171.
[40]Richardson MC,Guo M,Fauser BC,et al.Environmental and developmental origins of ovarian reserve[J].Hum Reprod Update,2014,20(3):353-369.DOI:10.1093/humupd/dmt057.
[41]Lilienthal H,Hack A,Roth-Harer A,et al.Effects of developmental exposure to 2,2,4,4,5-pentabromodiphenyl ether(PBDE-99)on sex steroids,sexual development,and sexually dimorphic behavior in rats[J].Environ Health Perspect,2006,114(2):194-201.DOI:10.1289/ehp.8391.
[42]Windham GC,Bottomley C,Birner C,et al.Age at menarche in relation to maternal use of tobacco,alcohol,coffee,and tea during pregnancy[J].Am J Epidemiol,2004,159(9):862-871.DOI:10.1093/aje/kwh117.
[43]Shrestha A,Nohr EA,Bech BH,et al.Smoking and alcohol use during pregnancy and age of menarche in daughters[J].Hum Reprod,2011,26(1):259-265.DOI:10.1093/humrep/deq316.
[44]Carter RC,Jacobson JL,Molteno CD,et al.Effects of heavy prenatal alcohol exposure and iron deficiency anemia on child growth and body composition through age 9 years[J].Alcohol Clin Exp Res,2012,36(11):1973-1982.DOI:10.1111/j.1530-0277.2012.01810.x.
[45]Pan Z,Zhang X,Shangguan Y,et al.Suppressed osteoclast differentiation at the chondro-osseous junction mediates endochondral ossification retardation in long bones of Wistar fetal rats with prenatal ethanol exposure[J].Toxicol Appl Pharmacol,2016,305:234-241.DOI:10.1016/j.taap.2016.06.021.
[46]Ibanez L,Potau N,Enriquez G,et al.Reduced uterine and ovarian size in adolescent girls born small for gestational age[J].Pediatr Res,2000,47(5):575-577.DOI:10.1203/00006450-200005000-00003.
[47]Manikkam M,Guerrero-Bosagna C,Tracey R,et al.Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures[J].PLoSOne,2012,7(2):e31901.DOI:10.1371/journal.pone.0031901.
[48]Hruska KS,Furth PA,Seifer DB,et al.Environmental factors in infertility[J].Clin Obstet Gynecol,2000,43(4):821-829.DOI:10.1097/00003081-200012000-00014.
[49]Kilic S,Yuksel B,Lortlar N,et al.Environmental tobacco smoke exposure during intrauterine period promotes granulosa cell apoptosis:a prospective,randomized study[J].J Matern Fetal Neonatal Med,2012,25(10):1904-1908.DOI:10.3109/14767058.2012.678440.
[50]Lutterodt MC,Sorensen KP,Larsen KB,et al.The number of oogonia and somatic cells in the human female embryo and fetus in relation to whether or not exposed to maternal cigarette smoking[J].Hum Reprod,2009,24(10):2558-2566.DOI:10.1093/humrep/dep226.
[51]Wo l f C J,Ostby J S,Gray LJ.Ges t a t ional exposure to2,3,7,8-tetrachlorodibenzo-p-dioxin(TCDD)severely alters reproductive function of female hamster offspring[J].Toxicol Sci,1999,51(2):259-264.DOI:10.1093/toxsci/51.2.259.
[52]Jablonska O,Shi Z,Valdez KE,et al.Temporal and anatomical s e n s i t i v i t i e s to t h e a r y l hydrocarbon r ec e p to r a g o n i s t2,3,7,8-tetrachlorodibenzo-p-dioxin leading to premature acyclicity with age in rats[J].Int J Androl,2010,33(2):405-412.DOI:10.1111/j.1365-2605.2009.01031.x.
[53]Xita N,Tsatsoulis A.Review:fetal programming of polycystic ovary syndrome by androgen excess:evidence from experimental,clinical,and genetic association studies[J].J Clin Endocrinol Metab,2006,91(5):1660-1666.DOI:10.1210/jc.2005-2757.
[54]Hague WM,Adams J,Rodda C,et al.The prevalence of polycystic ovaries in patients with congenital adrenal hyperplasia and their close relatives[J].Clin Endocrinol(Oxf),1990,33(4):501-510.DOI:10.1111/j.1365-2265.1990.tb03887.x.
[55]Rutkowska AZ,Diamanti-Kandarakis E.Polycystic ovary syndrome and environmental toxins[J].Fertil Steril,2016,106(4):948-958.DOI:10.1016/j.fertnstert.2016.08.031.
[56]Hewlett M,Chow E,Aschengrau A,et al.Prenatal exposure to endocrine disruptors:a developmental etiology for polycystic ovary syndrome[J].Reprod Sci,2016,pii:1933719116654992.DOI:10.1177/1933719116654992.
[57]Grossniklaus U,Ke l l y WG,Ferguson-Smith AC,e t a l.Transgenerational epigenetic inheritance:how important is it?[J].Nat Rev Genet,2013,14(3):228-235.DOI:10.1038/nrg3435.
[58]Pocar P,Augustin R,Gandolfi F,et al.Toxic effects of in vitro exposure to p-tert-octylphenol on bovine oocyte maturation and developmental competence[J].Biol Reprod,2003,69(2):462-468.DOI:10.1095/biolreprod.102.010355.
[59]Bhattacharya P,Keating AF.Impact of environmental exposures on ovarian function and role of xenobiotic metabolism during ovotoxicity[J].Toxicol Appl Pharmacol,2012,261(3):227-235.DOI:10.1016/j.taap.2012.04.009.
[60]Fowler PA,Childs AJ,Courant F,et al.In utero exposure to cigarette smoke dysregulates human fetal ovarian developmental signalling[J].Hum Reprod,2014,29(7):1471-1489.DOI:10.1093/humrep/deu117.
[61]Bhattacharya P,Sen N,Hoyer PB,et al.Ovarian expressed microsomal epoxide hydrolase:role in detoxification of 4-vinylcyclohexene diepoxide and regulation by phosphatidylinositol-3 kinase signaling[J].Toxicol Appl Pharmacol,2012,258(1):118-123.DOI:10.1016/j.taap.2011.10.014.
[62]Xu J,Osuga Y,Yano T,et al.Bisphenol A induces apoptosis and G2-to-M arrest of ovarian granulosa cells[J].Biochem Biophys Res Commun,2002,292(2):456-462.DOI:10.1006/bbrc.2002.6644.
[63]Piferrer F.Epigenetics of sex determination and gonadogenesis[J].Dev Dyn,2013,242(4):360-370.DOI:10.1002/dvdy.23924.
[64]Zhang T,Shen W,De Felici M,et al.Di(2-ethylhexyl)phthalate:Adverse effects on folliculogenesis that cannot be neglected[J].Environ Mol Mutagen,2016,57(8):579-588.DOI:10.1002/em.22037.
[65]Haddad R,Kasneci A,Mepham K,et al.Gestational exposure to diethylstilbestrol alters cardiac structure/function,protein expression and DNA methylation in adult male mice progeny[J].Toxicol Appl Pharmacol,2013,266(1):27-37.DOI:10.1016/j.taap.2012.10.018.
[66]Bohacek J,Gapp K,Saab BJ,et al.Transgenerational epigenetic effects on brain functions[J].Biol Psychiatry,2013,73(4):313-320.DOI:10.1016/j.biopsych.2012.08.019.
[67]Martinez-Arguelles DB,Papadopoulos V.Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action[J].Steroids,2010,75(7):467-476.DOI:10.1016/j.steroids.2010.02.004.
[68]Li H,Liu J,Sun Y,et al.N-hexane inhalation during pregnancy alters DNA promoter methylation in the ovarian granulosa cells of rat offspring[J].J Appl Toxicol,2014,34(8):841-856.DOI:10.1002/jat.2893.
[69]Li H,Zhang C,Ni F,et al.Gestational N-hexane inhalation alters the expression of genes related to ovarian hormone production and DNAmethylation states in adult female F1 rat offspring[J].Toxicol Lett,2015,239(3):141-151.DOI:10.1016/j.toxlet.2015.09.018.
[70]Xia Y,Shen S,Zhang X,et al.Epigenetic pattern changes in prenatal female Sprague-Dawley rats following exposure to androgen[J].Reprod Fertil Dev,2015.DOI:10.1071/RD14292.
[71]Feng YM,Liang GJ,Pan B,et al.Notch pathway regulates female germ cell meiosis progression and early oogenesis events in fetal mouse[J].Cell Cycle,2014,13(5):782-791.DOI:10.4161/cc.27708.
[72]Zhang XF,Zhang T,Han Z,et al.Transgenerational inheritance of ovarian development deficiency induced by maternal diethylhexyl phthalate exposure[J].Reprod Fertil Dev,2015,27(8):1213-1221.DOI:10.1071/RD14113.
[73]Li L,Zhang T,Qin XS,et al.Exposure to diethylhexyl phthalate(DEHP)results in a heritable modification of imprint genes DNA methylation in mouse oocytes[J].Mol Biol Rep,2014,41(3):1227-1235.DOI:10.1007/s11033-013-2967-7.
[74]Feng X,Wang X,Cao X,et al.Chronic exposure of female mice to an environmental level of perfluorooctane sulfonate suppresses estrogen synthesis through reduced histone H3K14 acetylation of the StARpromoter leading to deficits in follicular development and ovulation[J].Toxicol Sci,2015,148(2):368-379.DOI:10.1093/toxsci/kfv197.
[75]Govorko D,Bekdash RA,Zhang C,et al.Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations[J].Biol Psychiatry,2012,72(5):378-388.DOI:10.1016/j.biopsych.2012.04.006.
[76]Iqbal M,Moisiadis VG,Kostaki A,et al.Transgenerational effects of prenatal synthetic glucocorticoids on hypothalamic-pituitary-adrenal function[J].Endocrinology,2012,153(7):3295-3307.DOI:10.1210/en.2012-1054.
[77]Liu T,Li N,Zhu J,et al.Effects of di-(2-ethylhexyl)phthalate on the hypothalamus-pituitary-ovarian axis in adult female rats[J].Reprod Toxicol,2014,46:141-147.DOI:10.1016/j.reprotox.2014.03.006.
[78]Sun Y,Lin Y,Li H,et al.2,5-Hexanedione induces human ovarian granulosa cell apoptosis through BCL-2,BAX,and CASPASE-3signaling pathways[J].Arch Toxicol,2012,86(2):205-215.DOI:10.1007/s00204-011-0745-7.
[79]Zhang W,Huang L,Kong C,et al.Apoptosis of rat ovarian granulosa cells by 2,5-hexanedione in vitro and its relevant gene expression[J].JAppl Toxicol,2013,33(7):661-669.DOI:10.1002/jat.2714.
[80]Zama AM,Uzumcu M.Targeted genome-wide methylation and gene expression analyses reveal signaling pathways involved in ovarian dysfunction after developmental EDC exposure in rats[J].Biol Reprod,2013,88(2):52.DOI:10.1095/biolreprod.112.104802.
[81]Kwintkiewicz J,Nishi Y,Yanase T,et al.Peroxisome proliferatoractivated receptor-gamma mediates bisphenol A inhibition of FSHstimulated IGF-1,aromatase,and estradiol in human granulosa cells[J].Environ Health Perspect,2010,118(3):400-406.DOI:10.1289/ehp.0901161.
[82]Abolaji AO,Adedara IA,Soladogun A,et al.Exposure to2,5-hexanedione is accompanied by ovarian and uterine oxidative stress and disruption of endocrine balance in rats[J].Drug Chem Toxicol,2015,38(4):400-407.DOI:10.3109/01480545.2014.974265.
[83]Sliwowska JH,Comeau WL,Bodnar TS,et al.Prenatal alcohol exposure and pair feeding differentially impact puberty and reproductive development in female rats:role of the Kisspeptin system[J].Alcohol Clin Exp Res,2016,40(11):2368-2376.DOI:10.1111/acer.13233.
[84]Lan N,Yamashita F,Halpert AG,et al.Effects of prenatal ethanol exposure on hypothalamic-pituitary-adrenal function across the estrous cycle[J].Alcohol Clin Exp Res,2009,33(6):1075-1088.DOI:10.1111/j.1530-0277.2009.00929.x.
[85]Dees WL,Hiney JK,Srivastava VK.Alcohol alters hypothalamic glialneuronal communications involved in the neuroendocrine control of puberty:In vivo and in vitro assessments[J].Alcohol,2015,49(7):631-637.DOI:10.1016/j.alcohol.2015.08.001.
[86]Gamez JM,Penalba R,Cardoso N,et al.Exposure to a low dose of bisphenol A impairs pituitary-ovarian axis in prepubertal rats:effects on early folliculogenesis[J].Environ Toxicol Pharmacol,2015,39(1):9-15.DOI:10.1016/j.etap.2014.10.015.