Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0011
Animal Reproduction (AR)
Conference Paper

Factors influencing establishment of the ovarian reserve and their effects on fertility

Danielle Monniaux

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Abstract

A reserve of primordial follicles is set up in the ovaries of fetuses or neonates, depending on the species, and serves as the source of developing follicles throughout the reproductive lifespan. This review focuses on the cellular and molecular mechanisms currently known to control the establishment of this reserve, and their regulation by environmental factors. Most mutations in genes controlling germ cell proliferation and survival, meiosis or follicle assembly lead to the absence of primordial follicles or a sharp reduction in their number, incompatible with fertility in adults. Inadequate maternal nutrition affects the cellular metabolism, increases the oxidative stress and delays follicle formation in fetal ovaries. Despite the existence of compensation mechanisms of some developmental processes, the early-life nutritional environment imprints the long-term ability of follicles to enter growth and develop in adult ovaries. However, maternal undernutrition, overfeeding or high-fat diet during the establishment of the ovarian reserve does not seem to affect the fertility of the female offspring, unless their metabolism or neuroendocrine status is altered. Exposure of fetal or neonatal ovaries to excess steroids inhibits or stimulates follicle formation in a complex manner depending on the nature of the steroid, the dose and the animal species. Estrogens can control follicle formation through intra-ovarian mechanisms involving members of the TGF-beta family such as activin and BMP2. Early-life exposure to synthetic estrogens or environmental pollutants with estrogen-like activity impairs meiotic progression and follicle assembly, and affects long-term primordial follicle activation in adult ovaries. The effects of compounds with estrogen-like activity on the ovarian reserve can be transmitted to several generations through the female germline. Further investigations are needed to establish the early-life effects of the environmental factors on the female reproductive lifespan and decipher the mechanisms of their epigenetic effects on the size and quality of the ovarian reserve.

Keywords

cyst breakdown, germ cells, oocyte, ovary, primordial follicle.

References

Attig L, Brisard D, Larcher T, Mickiewicz M, Guilloteau P, Boukthir S, Niamba CN, Gertler A, Djiane J, Monniaux D, Abdennebi-Najar L. 2013. Postnatal leptin promotes organ maturation and development in IUGR piglets. PLoS One, 8:e64616. doi.org/10.1371/journal.pone.0064616.

Aye IL, Lager S, Ramirez VI, Gaccioli F, Dudley DJ, Jansson T, Powell TL. 2014. Increasing maternal body mass index is associated with systemic inflammation in the mother and the activation of distinct placental inflammatory pathways. Biol Reprod, 90:129. doi: 10.1095/biolreprod.113.116186.

Baillet A, Mandon-Pépin B. 2012. Mammalian ovary differentiation - a focus on female meiosis. Mol Cell Endocrinol, 356:13-23.

Baker TG. 1963. A quantitative and cytological study of germ cells in human ovaries. Proc R Soc Lond B Biol Sci, 158:417-433.

Bellingham M, Amezaga MR, Mandon-Pépin B, Speers CJ, Kyle CE, Evans NP, Sharpe RM, Cotinot C, Rhind SM, Fowler PA. 2013. Exposure to chemical cocktails before or after conception--- the effect of timing on ovarian development. Mol Cell Endocrinol, 376:156-172.

Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM. 2010. Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One, 5:e15558. doi.org/10.1371/journal.pone.0015558.

Billiar RB, Zachos NC, Burch MG, Albrecht ED, Pepe GJ. 2003. Up-regulation of alpha-inhibin expression in the fetal ovary of estrogen-suppressed baboons is associated with impaired fetal ovarian folliculogenesis. Biol Reprod, 68:1989-1996.

Birch RA, Padmanabhan V, Foster DL, Unsworth WP, Robinson JE. 2003. Prenatal programming of reproductive neuroendocrine function: fetal androgen exposure produces progressive disruption of reproductive cycles in sheep. Endocrinology, 144:1426-1434.

Black JL, Erickson BH. 1968. Oogenesis and ovarian development in the prenatal pig. Anat Rec, 161: 45-55.

Block E. 1952. Quantitative morphological investigations of the follicular system in women; variations at different ages. Acta Anat (Basel), 14:108-123.

Borwick SC, Rhind SM, McMillen SR, Racey PA. 1997. Effect of undernutrition of ewes from the time of mating on fetal ovarian development in mid gestation. Reprod Fertil Dev, 9:711-715.

Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW, Kipp JL, Shea LD, Mayo KE, Woodruff TK. 2006. Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool. Dev Biol, 298:132-148.

Britt KL, Drummond AE, Cox VA, Dyson M, Wreford NG, Jones ME, Simpson ER, Findlay JK. 2000. An age-related ovarian phenotype in mice with targeted disruption of the Cyp 19 (aromatase) gene. Endocrinology, 141:2614-2623.

Britt KL, Saunders PK, McPherson SJ, Misso ML, Simpson ER, Findlay JK. 2004. Estrogen actions on follicle formation and early follicle development. Biol Reprod, 71:1712-1723.

Burkhart MN, Juengel JL, Smith PR, Heath DA, Perry GA, Smith MF, Garverick HA. 2010. Morphological development and characterization of aromatase and estrogen receptors alpha and beta in fetal ovaries of cattle from days 110 to 250. Anim Reprod Sci, 117:43-54.

Chakraborty P, Roy SK. 2017. Stimulation of primordial follicle assembly by estradiol-17beta requires the action of bone morphogenetic protein-2 (BMP2). Sci Rep, 7:15581. doi:10.1038/s41598-017-15833-4.

Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. 2007. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology, 148:3580-3590.

Clarke IJ, Scaramuzzi RJ, Short RV. 1977. Ovulation in prenatally androgenized ewes. J Endocrinol, 73:385-389.

Comim FV, Hardy K, Robinson J, Franks S. 2015. Disorders of follicle development and steroidogenesis in ovaries of androgenised foetal sheep. J Endocrinol, 225:39-46.

Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM. 2001. Influence of placentally mediated fetal growth restriction on the onset of puberty in male and female lambs. Reproduction, 122:375-383.

Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM. 2003. Effect of maternal overnutrition during pregnancy on pituitary gonadotrophin gene expression and gonadal morphology in female and male foetal sheep at day 103 of gestation. Placenta, 24:248-257.

de Bruin JP, Dorland M, Bruinse HW, Spliet W, Nikkels PG, Te Velde ER. 1998. Fetal growth retardation as a cause of impaired ovarian development. Early Hum Dev, 51:39-46.

Dutta S, Mark-Kappeler CJ, Hoyer PB, Pepling ME. 2014. The steroid hormone environment during primordial follicle formation in perinatal mouse ovaries. Biol Reprod, 91:68. doi: 10.1095/biolreprod.114.119214.

Edson MA, Nagaraja AK, Matzuk MM. 2009. The mammalian ovary from genesis to revelation. Endocr Rev, 30:624-712.

Erickson BH. 1966. Development and radio-response of the prenatal bovine ovary. J Reprod Fertil, 10:97-105.

Feng L, Wang Y, Cai H, Sun G, Niu W, Xin Q, Tang X, Zhang J, Wang C, Zhang H, Xia G. 2016. ADAM10-Notch signaling governs the recruitment of ovarian pregranulosa cells and controls folliculogenesis in mice. J Cell Sci, 129:2202-2212.

Feng XL, Sun YC, Zhang M, Cheng SF, Feng YN, Liu JC, Wang HH, Li L, Qin GQ, Shen W. 2015. Insulin regulates primordial-follicle assembly in vitro by affecting germ-cell apoptosis and elevating oestrogen. Reprod Fertil Dev, 27:1197-1204.

Findlay JK, Hutt KJ, Hickey M, Anderson RA. 2015. How is the number of primordial follicles in the ovarian reserve established? Biol Reprod, 93:111. doi: 10.1095/ biolreprod.115.133652.

Flaws JA, Hirshfield AN, Hewitt JA, Babus JK, Furth PA. 2001. Effect of bcl-2 on the primordial follicle endowment in the mouse ovary. Biol Reprod, 64:1153-1159.

Forabosco A, Sforza C. 2007. Establishment of ovarian reserve: a quantitative morphometric study of the developing human ovary. Fertil Steril, 88:675-683.

Fortune JE, Yang MY, Muruvi W. 2010. The earliest stages of follicular development: follicle formation and activation. Soc Reprod Fertil Suppl, 67:203-216.

Fortune JE, Yang MY, Allen JJ, Herrick SL. 2013. Triennial Reproduction Symposium: the ovarian follicular reserve in cattle: what regulates its formation and size? J Anim Sci, 91:3041-3050.

Fowler PA, Dora NJ, McFerran H, Amezaga MR, Miller DW, Lea RG, Cash P, McNeilly AS, Evans NP, Cotinot C, Sharpe RM, Rhind SM. 2008. In utero exposure to low doses of environmental pollutants disrupts fetal ovarian development in sheep. Mol Hum Reprod, 14:269-280.

Fowler PA, Anderson RA, Saunders PT, Kinnell H, Mason JI, Evans DB, Bhattacharya S, Flannigan S, Franks S, Monteiro A, O'Shaughnessy PJ. 2011. Development of steroid signaling pathways during primordial follicle formation in the human fetal ovary. J Clin Endocrinol Metab, 96:1754-162.

Gardner DS, Ozanne SE, Sinclair KD. 2009. Effect of the early-life nutritional environment on fecundity and fertility of mammals. Philos Trans R Soc Lond B Biol Sci, 364:3419-3427.

Garverick HA, Juengel JL, Smith P, Heath DA, Burkhart MN, Perry GA, Smith MF, McNatty KP. 2010. Development of the ovary and ontongeny of mRNA and protein for P450 aromatase (arom) and estrogen receptors (ER) alpha and beta during early fetal life in cattle. Anim Reprod Sci, 117:24-33.

Grieve KM, McLaughlin M, Dunlop CE, Telfer EE, Anderson RA. 2015. The controversial existence and functional potential of oogonial stem cells. Maturitas, 82:278-281.

Grive KJ, Seymour KA, Mehta R, Freiman RN. 2014. TAF4b promotes mouse primordial follicle assembly and oocyte survival. Dev Biol, 392:42-51.

Grive KJ, Freiman RN. 2015. The developmental origins of the mammalian ovarian reserve. Development, 142:2554-2563.

Guo F, Yan L, Guo H, Li L, Hu B, Zhao Y, Yong J, Hu Y, Wang X, Wei Y, Wang W, Li R, Yan J, Zhi X, Zhang Y, Jin H, Zhang W, Hou Y, Zhu P, Li J, Zhang L, Liu S, Ren Y, Zhu X, Wen L, Gao YQ, Tang F, Qiao J. 2015. The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell, 161:1437-1452.

Hirshfield AN. 1992. Heterogeneity of cell populations that contribute to the formation of primordial follicles in rats. Biol Reprod, 47:466-472.

Hummitzsch K, Irving-Rodgers HF, Hatzirodos N, Bonner W, Sabatier L, Reinhardt DP, Sado Y, Ninomiya Y, Wilhelm D, Rodgers RJ. 2013. A new model of development of the mammalian ovary and follicles. PLoS One, 8:e55578. doi.org/10.1371/ journal.pone.0055578.

Hummitzsch K, Anderson RA, Wilhelm D, Wu J, Telfer EE, Russell DL, Robertson SA, Rodgers RJ. 2015. Stem cells, progenitor cells, and lineage decisions in the ovary. Endocr Rev, 36:65-91

Ireland JJ, Smith GW, Scheetz D, Jimenez-Krassel F, Folger JK, Ireland JL, Mossa F, Lonergan P, Evans AC. 2011. Does size matter in females? An overview of the impact of the high variation in the ovarian reserve on ovarian function and fertility, utility of anti-Mullerian hormone as a diagnostic marker for fertility and causes of variation in the ovarian reserve in cattle. Reprod Fertil Dev, 23:1-14. doi: 10.1071/RD10226.

Jagarlamudi K, Reddy P, Adhikari D, Liu K. 2010. Genetically modified mouse models for premature ovarian failure (POF). Mol Cell Endocrinol, 315:1-10. doi: 10.1016/j.mce.2009.07.016.

Jefferson W, Newbold R, Padilla-Banks E, Pepling M. 2006. Neonatal genistein treatment alters ovarian differentiation in the mouse: inhibition of oocyte nest breakdown and increased oocyte survival. Biol Reprod, 74:161-168.

Juengel JL, Sawyer HR, Smith PR, Quirke LD, Heath DA, Lun S, Wakefield SJ, McNatty KP. 2002. Origins of follicular cells and ontogeny of steroidogenesis in ovine fetal ovaries. Mol Cell Endocrinol, 191:1-10.

Juengel JL, Bodensteiner KJ, Heath DA, Hudson NL, Moeller CL, Smith P, Galloway SM, Davis GH, Sawyer HR, McNatty KP. 2004. Physiology of GDF9 and BMP15 signalling molecules. Anim Reprod Sci, 82/83:447-460.

Juengel JL, Heath DA, Quirke LD, McNatty KP. 2006. Oestrogen receptor alpha and beta, androgen receptor and progesterone receptor mRNA and protein localisation within the developing ovary and in small growing follicles of sheep. Reproduction, 131:81-92.

Jung D, Xiong J, Ye M, Qin X, Li L, Cheng S, Luo M, Peng J, Dong J, Tang F, Shen W, Matzuk MM, Kee K. 2017. In vitro differentiation of human embryonic stem cells into ovarian follicle-like cells. Nat Commun, 8:15680. doi: 10.1038/ncomms15680.

Karavan JR, Pepling ME. 2012. Effects of estrogenic compounds on neonatal oocyte development. Reprod Toxicol, 34:51-56.

Kerr B, Garcia-Rudaz C, Dorfman M, Paredes A, Ojeda SR. 2009. NTRK1 and NTRK2 receptors facilitate follicle assembly and early follicular development in the mouse ovary. Reproduction, 138:131-40.

Kerr JB, Myers M, Anderson RA. 2013. The dynamics of the primordial follicle reserve. Reproduction, 146:R205-215.

Kezele P, Skinner MK. 2003. Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: endocrine model of follicle assembly. Endocrinology, 144:3329-3337.

Kimura F, Bonomi LM, Schneyer AL. 2011. Follistatin regulates germ cell nest breakdown and primordial follicle formation. Endocrinology, 152:697-706.

Kobayashi T, Zhang H, Tang WWC, Irie N, Withey S, Klisch D, Sybirna A, Dietmann S, Contreras DA, Webb R, Allegrucci C, Alberio R, Surani MA. 2017. Principles of early human development and germ cell program from conserved model systems. Nature, 546:416-420.

Konishi I, Fujii S, Okamura H, Parmley T, Mori T. 1986. Development of interstitial cells and ovigerous cords in the human fetal ovary: an ultrastructural study. J Anat, 148:121-135.

Lea RG, Amezaga MR, Loup B, Mandon-Pépin B, Stefansdottir A, Filis P, Kyle C, Zhang Z, Allen C, Purdie L, Jouneau L, Cotinot C, Rhind SM, Sinclair KD, Fowler PA. 2016. The fetal ovary exhibits temporal sensitivity to a 'real-life' mixture of environmental chemicals. Sci Rep, 6:22279. doi:10.1038/srep22279.

Lechowska A, Bilinski S, Choi Y, Shin Y, Kloc M, Rajkovic A. 2011. Premature ovarian failure in nobox-deficient mice is caused by defects in somatic cell invasion and germ cell cyst breakdown. J Assist Reprod Genet, 28:583-589.

Lei L, Spradling AC. 2013. Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles. Proc Natl Acad Sci USA, 110:8585-8590.

Lei L, Spradling AC. 2016. Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells. Science, 352:95-99.

Leveillé P, Tarrade A, Dupont C, Larcher T, Dahirel M, Poumerol E, Cordier AG, Picone O, Mandon-Pépin B, Jolivet G, Levy R, Chavatte-Palmer P. 2014. Maternal high-fat diet induces follicular atresia but does not affect fertility in adult rabbit offspring. J Dev Orig Health Dis, 5:88-97.

Li L, Zhang T, Qin XS, Ge W, Ma HG, Sun LL, Hou ZM, Chen H, Chen P, Qin GQ, Shen W, Zhang XF. 2014. Exposure to diethylhexyl phthalate (DEHP) results in a heritable modification of imprint genes DNA methylation in mouse oocytes. Mol Biol Rep, 41:1227-1235.

Liu KH, Sun XF, Feng YZ, Cheng SF, Li B, Li YP, Shen W, Li L. 2017. The impact of Zearalenone on the meiotic progression and primordial follicle assembly during early oogenesis. Toxicol Appl Pharmacol, 329:9-17.

Mandon-Pépin B, Oustry-Vaiman A, Vigier B, Piumi F, Cribiu E, Cotinot C. 2003. Expression profiles and chromosomal localization of genes controlling meiosis and follicular development in the sheep ovary. Biol Reprod, 68:985-995.

McNatty KP, Smith P, Hudson NL, Heath DA, Tisdall DJ, O WS, Braw-Tal R. 1995. Development of the sheep ovary during fetal and early neonatal life and the effect of fecundity genes. J Reprod Fertil Suppl, 49:123-135.

McNatty KP, Fidler AE, Juengel JL, Quirke LD, Smith PR, Heath DA, Lundy T, O'Connell A, Tisdall DJ. 2000. Growth and paracrine factors regulating follicular formation and cellular function. Mol Cell Endocrinol, 163:11-20.

Monget P, Bobe J, Gougeon A, Fabre S, Monniaux D, Dalbies-Tran R. 2012. The ovarian reserve in mammals: a functional and evolutionary perspective. Mol Cell Endocrinol, 356:2-12.

Monniaux D, Clément F, Dalbies-Tran R, Estienne A, Fabre S, Mansanet C, Monget P. 2014. The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: what is the link? Biol Reprod, 90:85. doi: 10.1095/biolreprod.113.117077.

Monniaux D. 2016. Driving folliculogenesis by the oocyte-somatic cell dialog: lessons from genetic models. Theriogenology, 86:41-53.

Mork L, Maatouk DM, McMahon JA, Guo JJ, Zhang P, McMahon AP, Capel B. 2012. Temporal differences in granulosa cell specification in the ovary reflect distinct follicle fates in mice. Biol Reprod, 86:37. doi: 10.1095/biolreprod.111.095208.

Mossa F, Carter F, Walsh SW, Kenny DA, Smith GW, Ireland JL, Hildebrandt TB, Lonergan P, Ireland JJ, Evans AC. 2013. Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biol Reprod, 88:92. doi: 10.1095/biolreprod.112.107235.

Mu X, Liao X, Chen X, Li Y, Wang M, Shen C, Zhang X, Wang Y, Liu X, He J. 2015. DEHP exposure impairs mouse oocyte cyst breakdown and primordial follicle assembly through estrogen receptor-dependent and independent mechanisms. J Hazard Mater, 298:232-240.

Myers M, Morgan FH, Liew SH, Zerafa N, Gamage TU, Sarraj M, Cook M, Kapic I, Sutherland A, Scott CL, Strasser A, Findlay JK, Kerr JB, Hutt KJ. 2014. PUMA regulates germ cell loss and primordial follicle endowment in mice. Reproduction, 148:211-219.

Nilsson EE, Skinner MK. 2009. Progesterone regulation of primordial follicle assembly in bovine fetal ovaries. Mol Cell Endocrinol, 313:9-16.

Padmanabhan V, Veiga-Lopez A. 2013. Sheep models of polycystic ovary syndrome phenotype. Mol Cell Endocrinol, 373:8-20.

Pelosi E, Forabosco A, Schlessinger D. 2015. Genetics of the ovarian reserve. Front Genet, 6:308. doi: 10.3389/fgene.2015.00308.

Pepe GJ, Lynch TJ, Albrecht ED. 2013. Regulation of baboon fetal ovarian development by placental estrogen: onset of puberty is delayed in offspring deprived of estrogen in utero. Biol Reprod, 89:132. doi: 10.1095/biolreprod.112.107318.

Pepling ME, Spradling AC. 1998. Female mouse germ cells form synchronously dividing cysts. Development, 125:3323-3328.

Pepling ME, Spradling AC. 2001. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol, 234:339-351.

Pepling ME. 2012. Follicular assembly: mechanisms of action. Reproduction, 143:139-49.

Pepling ME. 2016. Development. Nursing the oocyte. Science, 352:35-36.

Perez GI, Robles R, Knudson CM, Flaws JA, Korsmeyer SJ, Tilly JL. 1999. Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat Genet, 21:200-203.

Pocar P, Fiandanese N, Berrini A, Secchi C, Borromeo V. 2017. Maternal exposure to di(2-ethylhexyl)phthalate (DEHP) promotes the transgenerational inheritance of adult-onset reproductive dysfunctions through the female germline in mice. Toxicol Appl Pharmacol, 322:113-121.

Qiu XH, Li ML, Li N, Sun Q, Zhou J, Ma RJ, Lin Y, Xie M, Ge X, Chen L, Yao B. 2017. Maternal diabetes impairs the initiation of meiosis in murine female germ cells. Mol Med Rep, 16:5189-5194.

Quirke LD, Juengel JL, Tisdall DJ, Lun S, Heath DA, McNatty KP. 2001. Ontogeny of steroidogenesis in the fetal sheep gonad. Biol Reprod, 65:216-228.

Rae MT, Palassio S, Kyle CE, Brooks AN, Lea RG, Miller DW, Rhind SM. 2001. Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction, 122:915-922.

Rae MT, Kyle CE, Miller DW, Hammond AJ, Brooks AN, Rhind SM. 2002. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci, 72:63-71.

Rawlings NC, Evans AC, Honaramooz A, Bartlewski PM. 2003. Antral follicle growth and endocrine changes in prepubertal cattle, sheep and goats. Anim Reprod Sci, 78:259-270.

Reader KL, Haydon LJ, Littlejohn RP, Juengel JL, McNatty KP. 2012. Booroola BMPR1B mutation alters early follicular development and oocyte ultrastructure in sheep. Reprod Fertil Dev, 24:353-361.

Rhind SM, Rae MT, Brooks AN. 2001. Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction, 122:205-214.

Rodrigues P, Limback D, McGinnis LK, Plancha CE, Albertini DF. 2009. Multiple mechanisms of germ cell loss in the perinatal mouse ovary. Reproduction, 137:709-720.

Ruoss C, Tadros A, O'Shea T, McFarlane J, Almahbobi G. 2009. Ovarian follicle development in Booroola sheep exhibiting impaired bone morphogenetic protein signalling pathway. Reproduction, 138:689-696.

Salvetti NR, Ortega HH, Veiga-Lopez A, Padmanabhan V. 2012. Developmental programming: impact of prenatal testosterone excess on ovarian cell proliferation and apoptotic factors in sheep. Biol Reprod, 87:22, 1-10. doi: 10.1095/biolreprod.112.100024.

Sawyer HR, Smith P, Heath DA, Juengel JL, Wakefield SJ, McNatty KP. 2002. Formation of ovarian follicles during fetal development in sheep. Biol Reprod, 66:1134-1150.

Sloboda DM, Hickey M, Hart R. 2011. Reproduction in females: the role of the early life environment. Hum Reprod Update, 17:210-227.

Smith P, O WS, Hudson NL, Shaw L, Heath DA, Condell L, Phillips DJ, McNatty KP. 1993. Effects of the Booroola gene (FecB) on body weight, ovarian development and hormone concentrations during fetal life. J Reprod Fertil, 98:41-54.

Smith P, Steckler TL, Veiga-Lopez A, Padmanabhan V. 2009. Developmental programming: differential effects of prenatal testosterone and dihydrotestosterone on follicular recruitment, depletion of follicular reserve, and ovarian morphology in sheep. Biol Reprod, 80:726-736.

Sominsky L, Ziko I, Soch A, Smith JT, Spencer SJ. 2016. Neonatal overfeeding induces early decline of the ovarian reserve: Implications for the role of leptin. Mol Cell Endocrinol, 431:24-35.

Soyal SM, Amleh A, Dean J. 2000. FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development, 127:4645-4654.

Spadotto R, Damasceno DC, Godinho AF, Amorim EM, Perobelli JE, Kempinas Wde G. 2012. Reproductive physiology, and physical and sexual development of female offspring born to diabetic dams. Arq Bras Endocrinol Metabol, 56:96-103.

Steckler T, Wang J, Bartol FF, Roy SK, Padmanabhan V. 2005. Fetal programming: prenatal testosterone treatment causes intrauterine growth retardation, reduces ovarian reserve and increases ovarian follicular recruitment. Endocrinology, 146:3185-3193.

Sullivan TM, Micke GC, Greer RM, Irving-Rodgers HF, Rodgers RJ, Perry VE. 2009. Dietary manipulation of Bos indicus x heifers during gestation affects the reproductive development of their heifer calves. Reprod Fertil Dev, 21: 773-84.

Tang WW, Kobayashi T, Irie N, Dietmann S, Surani MA. 2016. Specification and epigenetic programming of the human germ line. Nat Rev Genet, 17:585-600.

Truman AM, Tilly JL, Woods DC. 2017. Ovarian regeneration: the potential for stem cell contribution in the postnatal ovary to sustained endocrine function. Mol Cell Endocrinol, 445:74-84.

Tsoulis MW, Chang PE, Moore CJ, Chan KA, Gohir W, Petrik JJ, Vickers MH, Connor KL, Sloboda DM. 2016. Maternal high-fat diet-induced loss of fetal oocytes is associated with compromised follicle growth in adult rat offspring. Biol Reprod, 94:94. doi: 10.1095/biolreprod.115.135004.

Wang C, Roy SK. 2007. Development of primordial follicles in the hamster: role of estradiol-17beta. Endocrinology, 148:1707-1716.

Wang YY, Sun YC, Sun XF, Cheng SF, Li B, Zhang XF, De Felici M, Shen W. 2017. Starvation at birth impairs germ cell cyst breakdown and increases autophagy and apoptosis in mouse oocytes. Cell Death Dis, 8:e2613. doi: 10.1038/cddis.2017.3.

Weller M, Fortes MRS, Marcondes MI, Rotta PP, Gionbeli TRS, Valadares Filho SC, Campos MM, Silva FF, Silva W, Moore S, Guimaraes SEF. 2016. Effect of maternal nutrition and days of gestation on pituitary gland and gonadal gene expression in cattle. J Dairy Sci, 99:3056-3071.

White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. 2012. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med, 18:413-421.

Xu J, Gridley T. 2013. Notch2 is required in somatic cells for breakdown of ovarian germ-cell nests and formation of primordial follicles. BMC Biol, 11:13. doi.org/10.1186/1741-7007-11-13.

Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, Celeste AJ, Matzuk MM. 2001. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol, 15:854-866.

Yang MY, Fortune JE. 2008. The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biol Reprod, 78:1153-1161.

Yu N, Roy SK. 1999. Development of primordial and prenatal follicles from undifferentiated somatic cells and oocytes in the hamster prenatal ovary in vitro: effect of insulin. Biol Reprod, 61:1558-1567.

Zachos NC, Billiar RB, Albrecht ED, Pepe GJ. 2002. Developmental regulation of baboon fetal ovarian maturation by estrogen. Biol Reprod, 67:1148-1156.

Zachos NC, Billiar RB, Albrecht ED, Pepe GJ. 2004. Regulation of oocyte microvilli development in the baboon fetal ovary by estrogen. Endocrinology, 145:959-966.

Zamboni L, Bézard J, Mauléon P. 1979. The role of the mesonephros in the development of the sheep fetal ovary. Ann Biol Anim Biochim Biophys, 19:1153-1178.

Zambrano E, Guzman C, Rodriguez-Gonzalez GL, Durand-Carbajal M, Nathanielsz PW. 2014. Fetal programming of sexual development and reproductive function. Mol Cell Endocrinol, 382:538-549.

Zhang H, Liu L, Li X, Busayavalasa K, Shen Y, Hovatta O, Gustafsson JA, Liu K. 2014. Life-long in vivo cell-lineage tracing shows that no oogenesis originates from putative germline stem cells in adult mice. Proc Natl Acad Sci USA, 111:17983-17988.

Zhang XF, Zhang T, Han Z, Liu JC, Liu YP, Ma JY, Li L, Shen W. 2015. Transgenerational inheritance of ovarian development deficiency induced by maternal diethylhexyl phthalate exposure. Reprod Fertil Dev, 27:1213-1221.

Zhao L, Du X, Huang K, Zhang T, Teng Z, Niu W, Wang C, Xia G. 2016. Rac1 modulates the formation of primordial follicles by facilitating STAT3-directed Jagged1, GDF9 and BMP15 transcription in mice. Sci Rep, 6:23972. doi:10.1038/srep23972.

Zheng W, Zhang H, Gorre N, Risal S, Shen Y, Liu K. 2014a. Two classes of ovarian primordial follicles exhibit distinct developmental dynamics and physiological functions. Hum Mol Genet, 23:920-928.

Zheng W, Zhang H, Liu K. 2014b. The two classes of primordial follicles in the mouse ovary: their development, physiological functions and implications for future research. Mol Hum Reprod, 20:286-292.

Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, Xiang J, Shi L, Yu Q, Zhang Y, Hou R, Wu J. 2009. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol, 11:631-636.

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