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Cellular and Molecular Life Sciences

, Volume 74, Issue 14, pp 2547–2566 | Cite as

Mechanisms controlling germline cyst breakdown and primordial follicle formation

  • Chao Wang
  • Bo Zhou
  • Guoliang XiaEmail author
Review

Abstract

In fetal females, oogonia proliferate immediately after sex determination. The progress of mitosis in oogonia proceeds so rapidly that the incompletely divided cytoplasm of the sister cells forms cysts. The oogonia will then initiate meiosis and arrest at the diplotene stage of meiosis I, becoming oocytes. Within each germline cyst, oocytes with Balbiani bodies will survive after cyst breakdown (CBD). After CBD, each oocyte is enclosed by pre-granulosa cells to form a primordial follicle (PF). Notably, the PF pool formed perinatally will be the sole lifelong oocyte source of a female. Thus, elucidating the mechanisms of CBD and PF formation is not only meaningful for solving mysteries related to ovarian development but also contributes to the preservation of reproduction. However, the mechanisms that regulate these phenomena are largely unknown. This review summarizes the progress of cellular and molecular research on these processes in mice and humans.

Keywords

Preservation of fertility Premature ovarian failure Apoptosis Autophagy Reconstituted follicle 

Abbreviations

PF

Primordial follicle

CBD

Cyst breakdown

POI

Primary ovarian insufficiency

POF

Premature ovarian failure

MOF

Multi-oocyte follicle

JNK

c-Jun amino-terminal kinase

mTORC1

Mechanistic target of rapamycin complex 1

PI3K

Phosphatidyl inositol 3-kinase

PGCs

Primordial germ cells

Dpc

Day post coitus

Wpc

Week post conception

FOXL2

Forkhead box L2

WNT4

Canonical wingless-type MMTV integration site family member 4

RA

Retinoic acid

RARs

RA receptors

RXRs

Retinoid X receptors

RALDHs

Retinaldehyde dehydrogenases

Act

Activin

TGF

Transforming growth factor

DSBs

DNA double-strand breaks

PAR6

Partitioning-defective Protein 6

AJs

Adherens junctions

Cads

Cadherins

GJs

Gap junctions

NICD

Notch intercellular domain

ADAM10

A disintegrin and metalloproteinase domain10

Bax

Bcl2-associated X protein

Casp2

Caspase 2

FSH

Follicle-stimulating hormone

PCD

Programmed cell death

SOHLH2

Spermatogenesis- and oogenesis-specific helix-loop-helix transcription factor 2

AQP8

Water channel aquaporin-8

Fst

Follistatin

Inh

Inhibin

LGR5

Leucine-rich repeat-containing G-protein-coupled receptor 5

Bcl-2

B-cell lymphoma 2

References

  1. 1.
    Zuckerman S (1951) The number of oocytes in the mouse ovary. Recent Prog Horm Res 6:63–108Google Scholar
  2. 2.
    Zhang H, Adhikari D, Zheng WJ, Liu K (2013) Combating ovarian aging depends on the use of existing ovarian follicles, not on putative oogonial stem cells. Reproduction 146:R229–R233PubMedCrossRefGoogle Scholar
  3. 3.
    Aaron JWH (2014) Fertility: the role of mTOR signaling and KIT ligand. Curr Biol 24(21):1040–1042CrossRefGoogle Scholar
  4. 4.
    Okeke T, Anyaehie U, Ezenyeaku C (2013) Premature menopause. Ann Med Health Sci Res 3:90–95PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Grive KJ, Freiman RN (2015) The developmental origins of the mammalian ovarian reserve. Development 142:2554–2563Google Scholar
  6. 6.
    Pelosi E, Simonsick E, Forabosco A, Garcia-Ortiz JE, Schlessinger D (2015) Dynamics of the ovarian reserve and impact of genetic and epidemiological factors on age of menopause. Biol Reprod 92:130PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Justine B, Isabelle B, Sara B, Valérie B, Kemal A, Jérôme F, Anne F, Anne LT, Reiner AV, Chérif B, Brigitte D, Catherine D, Jacques Y, Nadine B (2016) Identification of multiple gene mutations accounts for a new genetic architecture of primary ovarian insufficiency. J Clin Endocrinol Metab 101(12):4541–4550CrossRefGoogle Scholar
  8. 8.
    Jeruss JS, Woodruff TK (2009) Preservation of fertility in patients with cancer. N Engl J Med 360:902–911PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Partridge AH, Gelber S, Peppercorn J, Sampson E, Knudsen K, Laufer M, Rosenberg R, Przypyszny M, Rein A, Winer EP (2004) Web-based survey of fertility issues in young women with breast cancer. J Clin Oncol 22:4174–4183PubMedCrossRefGoogle Scholar
  10. 10.
    Kim SS (2006) Fertility preservation in female cancer patients: current developments and future directions. Fertil Steril 85:1–11PubMedCrossRefGoogle Scholar
  11. 11.
    Kim SS (2013) Oocyte biology in fertility preservation. (eBook) Springer New York Heidelberg Dordrecht London. doi: 10.1007/978-1-4614-8214-7
  12. 12.
    Newton H, Aubard Y, Rutherford A, Sharma V, Gosden R (1996) Low temperature storage and grafting of human ovarian tissue. Hum Reprod 11:1487–1491PubMedCrossRefGoogle Scholar
  13. 13.
    Gook DA, Edgar DH, Stern C (1999) Effect of cooling rate and dehydration regimen on the histological appearance of human ovarian cortex following cryopreservation in 1, 2-propanediol. Hum Reprod 14:2061–2068PubMedCrossRefGoogle Scholar
  14. 14.
    Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hämäläinen T, Peng SL, Lan ZJ, Cooney AJ, Huhtaniemi I, Liu K (2008) Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319:611–613PubMedCrossRefGoogle Scholar
  15. 15.
    John GB, Gallardo TD, Shirley LJ, Castrillon DH (2008) Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 321:197–204PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Li J, Kawamura K, Cheng Y, Liu S, Klein C, Liu S, Duan EK, Hsueh AJ (2010) Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci USA 107:10280–10284PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Zhang H, Risal S, Gorre N, Busayavalasa K, Li X, Shen Y, Bosbach B, Bra¨nnstro¨m M, Liu K (2014) Somatic cells initiate primordial follicle activation and govern the development of dormant oocytes in mice. Curr Biol 24:2501–2508PubMedCrossRefGoogle Scholar
  18. 18.
    Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, Ho CH, Kawamura N, Tamura M, Hashimoto S, Sugishita Y, Morimoto Y, Hosoi Y, Yoshioka N, Ishizuka B, Hsueh AJ (2013) Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci USA 110:17474–17479PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Monk M, McLaren A (1981) X-chromosome activity in foetal germ cells of the mouse. J Embryol Exp Morphol 63:75–84PubMedGoogle Scholar
  20. 20.
    Motta PM, Makabe S, Nottola SA (2000) The ultrastructure of human reproduction. I. The natural history of the female germ cell: origin, migration and differentiation inside the developing ovary. Hum Reprod Update 3:281–295CrossRefGoogle Scholar
  21. 21.
    Kerr CL, Hill CM, Blumenthal PD, Gearhart JD (2008) Expression of pluripotent stem cell markers in the human fetal ovary. Hum Reprod 23:589–599PubMedCrossRefGoogle Scholar
  22. 22.
    Cohen PE, Holloway JK (2010) Predicting gene networks in human oocyte meiosis. Biol Reprod 82:469–472PubMedCrossRefGoogle Scholar
  23. 23.
    Pepling ME, Spradling AC (1998) Female mouse germ cells form synchronously dividing cysts. Development 125:3323–3328Google Scholar
  24. 24.
    Jung D, Kee K (2015) Insights into female germ cell biology: from in vivo development to in vitro derivations. Asian J Androl 17(3):415–420PubMedPubMedCentralGoogle Scholar
  25. 25.
    Baker TG (1963) A quantitative and cytological study of germ cells in human ovaries. Proc R Soc Lond Ser B 158:417–433CrossRefGoogle Scholar
  26. 26.
    Hitomi S, Masami KA, Yoshiakira K (2015) From sex determination to initial folliculogenesis in mammalian ovaries: morphogenetic waves along the anteroposterior and dorsoventral axes. Sex Dev 9:190–204. doi: 10.1159/000440689 CrossRefGoogle Scholar
  27. 27.
    Menke DB, Koubova J, Page DC (2003) Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave. Dev Biol 262:303–312PubMedCrossRefGoogle Scholar
  28. 28.
    De Felici M, Klinger FG, Farini D, Scaldaferri ML, Iona S, Lobascio M (2005) Establishment of oocyte population in the fetal ovary: primordial germ cell proliferation and oocyte programmed cell death. Reprod Biomed Online 10:182–191PubMedCrossRefGoogle Scholar
  29. 29.
    Mazaud S, Guyot R, Guigon CJ, Coudouel N, Le Magueresse-Battistoni B, Magre S (2005) Basal membrane remodeling during follicle histogenesis in the rat ovary: contribution of proteinases of the MMP and PA families. Dev Biol 277:403–416PubMedCrossRefGoogle Scholar
  30. 30.
    Pepling ME, Sundman EA, Patterson NL, Gephardt GW, Medico L Jr, Wilson KI (2010) Differences in oocyte development and estradiol sensitivity among mouse strains. Reproduction 139:349–357PubMedCrossRefGoogle Scholar
  31. 31.
    Anderson RA, Fulton N, Cowan G, Coutts S, Saunders PT (2007) Conserved and divergent patterns of expression of DAZL, VASA and OCT4 in the germ cells of the human fetal ovary and testis. BMC Dev Biol 7:136PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    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 86:37PubMedCrossRefGoogle Scholar
  33. 33.
    Rajah R, Glaser EM, Hirshfield AN (1992) The changing architecture of the neonatal rat ovary during histogenesis. Dev Dyn 194:177–192PubMedCrossRefGoogle Scholar
  34. 34.
    De Pol A, Vaccina F, Forabosco A, Cavazzuti E, Marzona L (1997) Apoptosis of germ cells during human prenatal oogenesis. Hum Reprod 12:2235–2241PubMedCrossRefGoogle Scholar
  35. 35.
    De Felici M, Di Carlo A, Pesce M, Iona S, Farrace MG, Piacentini M (1999) Bcl-2 and Bax regulation of apoptosis in germ cells during prenatal oogenesis in the mouse embryo. Cell Death. Differentiation 6:908–915CrossRefGoogle Scholar
  36. 36.
    Ghafari F, Gutierrez CG, Hartshorne GM (2007) Apoptosis in mouse fetal and neonatal oocytes during meiotic prophase one. BMC Dev Biol 7:87PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Zheng W, Zhang H, Gorre N, Risal S, Shen Y, Liu K (2014) Two classes of ovarian primordial follicles exhibit distinct developmental dynamics and physiological functions. Hum Mol Genet 23:920–928PubMedCrossRefGoogle Scholar
  38. 38.
    Hirshfield AN (1992) Heterogeneity of cell populations that contribute to the formation of primordial follicles in rats. Biol Reprod 47:466–472PubMedCrossRefGoogle Scholar
  39. 39.
    Eppig JJ, Handel MA (2012) Origins of granulosa cells clarified and complexified by waves. Biol Reprod 86(2):34, 1–2Google Scholar
  40. 40.
    Peters H (1969) The development of the mouse ovary from birth to maturity. Acta Endocrinol 62:98–116PubMedGoogle Scholar
  41. 41.
    Hirshfield AN, DeSanti AM (1995) Patterns of ovarian cell proliferation in rats during the embryonic period and the first three weeks postpartum. Biol Reprod 53:1208–1221PubMedCrossRefGoogle Scholar
  42. 42.
    Pepling ME (2006) From primordial germ cell to primordial follicle:mammalian female germ cell development. Genesis 44:622–632PubMedCrossRefGoogle Scholar
  43. 43.
    Lei L, Zhang H, Jin SY, Wang FC, Fu MY, Wang HB, Xia GL (2006) Stage-specific germ-somatic cell interaction directs the primordial folliculogenesis in mouse Stage-specific ovarian somatic cells in primordial folliculogenesis fetal ovaries. J Cell Physi 208:640–647CrossRefGoogle Scholar
  44. 44.
    Joan SJ (2013) Defining the neighborhoods that escort the oocyte through its early life events and into a functional follicle. Mol Reprod Dev 80(12):960–976CrossRefGoogle Scholar
  45. 45.
    Gilchrist RB, Ritter LJ, Armstrong DT (2004) Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 82–83:431–446PubMedCrossRefGoogle Scholar
  46. 46.
    Chang CL, Wang HS, Soong YK, Huang SY, Pai SY, Hsu SY (2011) Regulation of oocyte and cumulus cell interactions by intermedin/adrenomedullin 2. J Biol Chem 286:43193–43203PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Borum K (1961) Oogenesis in the mouse. A study of the origin of the mature ova. Exp Cell Res 45:39–47CrossRefGoogle Scholar
  48. 48.
    Byskov AG, Guoliang X, Andersen CY (1997) The cortex-medulla oocyte growth pattern is organized during fetal life: an in-vitro study of the mouse ovary. Mol Hum Reprod 3:795–800PubMedCrossRefGoogle Scholar
  49. 49.
    Uda M, Ottolenghi C, Crisponi L, Garcia JE, Deiana M, Kimber W, Forabosco A, Cao A, Schlessinger D, Pilia G (2004) Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum Mol Genet 13:1171–1181PubMedCrossRefGoogle Scholar
  50. 50.
    Ottolenghi C, Pelosi E, Tran J, Colombino M, Douglass E, Nedorezov T, Cao A, Forabosco A, Schlessinger D (2007) Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet 16:2795–2804PubMedCrossRefGoogle Scholar
  51. 51.
    Qing T, Liu H, Wei W, Ye X, Shen W, Zhang D, Song Z, Yang W, Ding M, Deng H (2008) Mature oocytes derived from purified mouse fetal germ cells. Hum Reprod 23:54–61PubMedCrossRefGoogle Scholar
  52. 52.
    Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier AC, Klugmann C, Klasen C, Holter NI, Riethmacher D, Schütz G, Cooney AJ, Lovell-Badge R, Treier M (2009) Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139:1130–1142PubMedCrossRefGoogle Scholar
  53. 53.
    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:e55578PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Nicol B, Yao HH (2014) Building an ovary: insights into establishment of somatic cell lineages in the mouse. Sex Dev 8(5):243–251PubMedCrossRefGoogle Scholar
  55. 55.
    Schmidt D, Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, Treier AC, Treier M (2004) The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131(4):933–942Google Scholar
  56. 56.
    Li G, Zhang H, Wang YJ, Wen J, Teng Z, Mao GP, Wang JW, Guo M, Mu XY, Xia GL (2011) Stage-specific mice ovarian somatic cell is involved in primordial folliculogenesis. Front Biosci (Elite Ed) 3:1025–1033Google Scholar
  57. 57.
    Ottolenghi C, Omari S, Garcia-Ortiz JE, Uda M, Crisponi L, Forabosco A, Pilia G, Schlessinger D (2005) Foxl2 is required for commitment to ovary differentiation. Hum Mol Genet 14:2053–2062PubMedCrossRefGoogle Scholar
  58. 58.
    Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P, Bisceglia L, Zelante L, Nagaraja R, Porcu S, Ristaldi MS, Marzella R, Rocchi M, Nicolino M, Lienhardt-Roussie A, Nivelon A, Verloes A, Schlessinger D, Gasparini P, Bonneau D, Cao A, Pilia G (2001) The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat Genet 27:159–166PubMedCrossRefGoogle Scholar
  59. 59.
    Ng A, Tan S, Singh G, Rizk P, Swathi Y, Tan TZ, Huang RY, Leushacke M, Barker N (2014) Lgr5 marks stem/progenitor cells in ovary and tubal epithelia. Nat Cell Biol 16(8):745–757PubMedCrossRefGoogle Scholar
  60. 60.
    Rastetter RH, Bernard P, Palmer JS, Chassot AA, Chen H, Western PS, Ramsay RG, Chaboissier MC, Wilhelm D (2014) Marker genes identify three somatic cell types in the fetal mouse ovary. Dev Biol 394(2):242–252PubMedCrossRefGoogle Scholar
  61. 61.
    Chassot AA, Bradford ST, Auguste A, Gregoire EP, Pailhoux E, de Rooij DG, Schedl A, Chaboissier MC (2012) WNT4 and RSPO1 together are required for cell proliferation in the early mouse gonad. Development 139(23):4461–72Google Scholar
  62. 62.
    Capel B (2014) Ovarian epithelium regeneration by Lgr5(+) cells. Nat Cell Biol 16(8):743–744PubMedCrossRefGoogle Scholar
  63. 63.
    Schuijers J, Clevers H (2012) Adult mammalian stem cells: the role of Wnt, Lgr5 and R-spondins. EMBO J 31(12):2685–2696PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Hsueh AJ, Kawamura K, Cheng Y, Fauser BC (2015) Intraovarian control of early folliculogenesis. Endocr Rev 36(1):1–24PubMedCrossRefGoogle Scholar
  65. 65.
    Suzuki H, Kanai-Azuma M, Kanai Y (2015) From sex determination to initial folliculogenesis in mammalian ovaries: morphogenetic waves along the anteroposterior and dorsoventral axes. Sex Dev 9(4):190–204PubMedCrossRefGoogle Scholar
  66. 66.
    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(11):2202–2212PubMedCrossRefGoogle Scholar
  67. 67.
    Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, Hamada H, Koopman P (2006) Retinoid signaling determines germ cell fate in mice. Science 312:596–600PubMedCrossRefGoogle Scholar
  68. 68.
    Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci USA 103:2474–2479PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Le Bouffant R, Guerquin MJ, Duquenne C, Frydman N, Coffigny H, Rouiller-Fabre V, Frydman R, Habert R, Livera G (2010) Meiosis initiation in the human ovary requires intrinsic retinoic acid synthesis. Hum Reprod 25:2579–2590PubMedCrossRefGoogle Scholar
  70. 70.
    Childs AJ, Cowan G, Kinnell HL, Anderson RA, Saunders PT (2011) Retinoic Acid signalling and the control of meiotic entry in the human fetal gonad. PLoS One 6:e20249PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Mu XY, WEN J, Guo M, Wang JW, Li G, Wang ZP, Wang YJ, Teng Z, Cui Y, Xia GL (2013) Retinoic acid derived from the fetal ovary initiates meiosis in mouse germ cells. J Cell Physiol 228(3):627–639PubMedCrossRefGoogle Scholar
  72. 72.
    Mammadova A, Zhou H, Carels CE, Von den Hoff JW (2016) Retinoic acid signalling in the development of the epidermis, the limbs and the secondary palate. Differentiation 92(5):326–335PubMedCrossRefGoogle Scholar
  73. 73.
    Xu H, Beasley MD, Warren WD, van der Horst GT, McKay MJ (2005) Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 8:949–961PubMedCrossRefGoogle Scholar
  74. 74.
    Griswold MD, Hogarth CA, Bowles J, Koopman P (2012) Initiating meiosis: the case for retinoic acid. Biol Reprod 86(2):35PubMedCrossRefGoogle Scholar
  75. 75.
    Niederreither K, McCaffery P, Dräger UC, Chambon P, Dollé P (1997) Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech Dev 62(1):67–78PubMedCrossRefGoogle Scholar
  76. 76.
    Tahayato A, Dollé P, Petkovich M (2003) Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development. Gene Expr Patterns 3(4):449–454PubMedCrossRefGoogle Scholar
  77. 77.
    Liang GJ, Zhang XF, Wang JJ, Sun YC, Sun XF, Cheng SF, Li L, De Felici Massimo, Shen W (2015) Activin A accelerates the progression of fetal oocytes throughout meiosis and early oogenesis in the mouse. Stem Cells Develop 24(20):2455–2465Google Scholar
  78. 78.
    Kipp JL, Golebiowski A, Rodriguez G, Demczuk M, Kilen SM, Mayo KE (2011) Gene expression profiling reveals Cyp26b1 to be an activin regulated gene involved in ovarian granulosa cell proliferation. Endocrinology 152:303–312PubMedCrossRefGoogle Scholar
  79. 79.
    Tedesco M, Desimio MG, Klinger FG, De Felici M, Farini D (2013) Minimal concentrations of retinoic acid induce stimulation by retinoic acid 8 and promote entry into meiosis in isolated pregonadal and gonadal mouse primordia germ cells. Biol Reprod 88:145PubMedCrossRefGoogle Scholar
  80. 80.
    Liu CF, Parker K, Yao HH (2010) WNT4/beta-catenin pathway maintains female germ cell survival by inhibiting activin betaB in the mouse fetal ovary. PLoS One 5(4):e10382PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Chassot AA, Gregoire EP, Lavery R, Taketo MM, de Rooij DG, Adams IR, Chaboissier MC (2011) RSPO1/β-catenin signaling pathway regulates oogonia differentiation and entry into meiosis in themouse fetal ovary. PLoS One 6(10):e25641PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Chassot AA, Gregoire EP, Magliano M, Lavery R, Chaboissier MC (2008) Genetics of ovarian differentiation: Rspo1, a major player. Sex Dev 2(4–5):219–227PubMedCrossRefGoogle Scholar
  83. 83.
    Maatouk DM, DiNapoli L, Alvers A, Parker KL, Taketo MM, Capel B (2008) Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. Hum Mol Genet 17(19):2949–2955PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Tingen CM, Kim A, Woodruff TK (2009) The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 15(12):795–803PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Klinger FG, Rossi V, De Felici M (2015) Multifaceted programmed cell death in the mammalian fetal ovary. Int J Dev Biol 59(1–3):51–54PubMedCrossRefGoogle Scholar
  86. 86.
    Mandon-Pépin B, Touraine P, Kuttenn F, Derbois C, Rouxel A, Matsuda F, Nicolas A, Cotinot C, Fellous M (2008) Genetic investigation of four meiotic genes in women with premature ovarian failure. Eur J Endocrinol 158:107–115PubMedCrossRefGoogle Scholar
  87. 87.
    Pelosi E, Forabosco A, Schlessinger D (2015) Genetics of the ovarian reserve (OR). Front Genet 6:308. doi: 10.3389/fgene.2015.00308
  88. 88.
    de Vries SS, Baart EB, Dekker M, Siezen A, deRooij DG, deBoer P (1999) Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev 13:523–531PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, Hou HJ (2000) MutS homolog4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14:1085–1097PubMedPubMedCentralGoogle Scholar
  90. 90.
    Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, Brignull E (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific Rec A homolog. Mol Cell 1:697–705PubMedCrossRefGoogle Scholar
  91. 91.
    Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975–987PubMedCrossRefGoogle Scholar
  92. 92.
    Dokshin GA, Baltus AE, Eppig JJ, Page DC (2013) Oocyte differentiation is genetically dissociable from meiosis in mice. Nat Genet 45:877–883PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Paredes A, Garcia-Rudaz C, Kerr B, Tapia V, Dissen GA, Costa M, Cornea A, Ojeda S (2005) Loss of synaptonemal complex protein-1, asynaptonemal complex protein, contributes to the initiation of follicular assembly in the developing rat ovary. Endocrinology 146:5267–5277PubMedCrossRefGoogle Scholar
  94. 94.
    Voronina E, Lovasco LA, Gyuris A, Baumgartner RA, Parlow AF, Freiman RN (2007) Ovarian granulosa cell survival and proliferation requires the gonad-selective TFIID subunit TAF4b. Dev Biol 303(2):715–726PubMedCrossRefGoogle Scholar
  95. 95.
    Grive KJ, Seymour KA, Mehta R, Freiman RN (2014) TAF4b promotes mouse primordial follicle assembly and oocyte survival. Dev Biol 392:42–51PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Di Pietro C, Vento M, Ragusa M, Barbagallo D, Guglielmino MR, Maniscalchi T, Duro LR (2008) Expression analysis of TFIID in single human oocytes: new potential molecular markers of oocyte quality. Reprod Biomed Online 17:338–349PubMedCrossRefGoogle Scholar
  97. 97.
    Knauff EA, Franke L, van Es MA, van den Berg LH, van der Schouw YT, Laven JS, Lambalk CB, Hoek A, Goverde AJ, Christin-Maitre S, Hsueh AJ, Wijmenga C, Fauser BC; Dutch POF Consortium (2009) Genome-wide association study in premature ovarian failure patients suggests ADAMTS19 as a possible candidate gene. Hum Reprod 24(9):2372–2378PubMedCrossRefGoogle Scholar
  98. 98.
    Lovasco LA, Seymour KA, Zafra K, O’Brien CW, Schorl C, Freiman RN (2010) Accelerated ovarian aging in the absence of the transcription regulator TAF4B in mice. Biol Reprod 82(1):23–34PubMedCrossRefGoogle Scholar
  99. 99.
    Ongeri EM, Verderame MF, Hammond JM (2007) The TATA binding protein associated factor 4b (TAF4b) mediates FSH stimulation of the IGFBP-3 promoter in cultured porcine ovarian granulosa. Cells Mol Cell Endocrinol 278(1–2):29–35Google Scholar
  100. 100.
    Wardell JR, Hodgkinson KM, Binder AK, Seymour KA, Korach KS, Vanderhyden BC, Freiman RN (2013) Estrogen responsiveness of the TFIID subunit TAF4B in the normal mouse ovary and in ovarian tumors. Biol Reprod 89(5):116PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Geles KG, Freiman RN, Liu WL, Zheng S, Voronina E, Tjian R (2006) Cell-type-selective induction of C-jun by TAF4b directs ovarian-specific transcription networks. Proc Natl Acad Sci USA 103(8):2594–2599PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Wang Y, Teng Z, Li G, Mu X, Wang Z, Feng L, Niu W, Huang K, Xiang X, Wang C, Zhang H, Xia G (2015) Cyclic AMP in oocytes controls meiotic prophase I and primordial folliculogenesis in the perinatal mouse ovary. Development 142(2):343–351Google Scholar
  103. 103.
    Ginsburg M, Snow MH, McLaren A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110:521–528Google Scholar
  104. 104.
    Edson MA, Nagaraja AK, Matzuk MM (2009) The mammalian ovary from genesis to revelation. Endocr Rev 30:624–712PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Pepling ME (2012) Follicular assembly: mechanisms of action. Reprod 143:139–149Google Scholar
  106. 106.
    Lei L, Spradling AC (2016) Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells. Science 352(6281):95–99PubMedCrossRefGoogle Scholar
  107. 107.
    Gomperts M, Garcia-Castro M, Wylie C, Heasman J (1994) Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120:135–141Google Scholar
  108. 108.
    Bendel-Stenzel MR, Gomperts M, Anderson R, Heasman J, Wylie C (2000) The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech Dev 91:143–152PubMedCrossRefGoogle Scholar
  109. 109.
    Lei L, Spradling AC (2013) Mouse primordial germ cells produce cysts that partially fragment prior to meiosis. Development 140:2075–2081Google Scholar
  110. 110.
    Pepling ME, Spradling AC (2001) Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 234:339–351PubMedCrossRefGoogle Scholar
  111. 111.
    Carlson JL, Bakst MR, Ottinger MA (1996) Developmental stages of primary oocytes in turkeys. Poult Sci 75:1569–1578PubMedCrossRefGoogle Scholar
  112. 112.
    Pepling ME, Wilhelm JE, O’Hara AL, Gephardt GW, Spradling AC (2007) Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc Natl Acad Sci USA 104:187–192PubMedCrossRefGoogle Scholar
  113. 113.
    Aravin AA, van der Heijden GW, Castañeda J, Vagin VV, Hannon GJ, Bortvin A (2009) Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLOS Genet 5:e1000764Google Scholar
  114. 114.
    Lim K, Lorthongpanich C, Chew TG, Tan CW, Shue YT, Balu S, Gounko N, Kuramochi-Miyagawa S, Matzuk MM, Chuma S, Messerschmidt DM, Solter D, Knowles BB (2013) The nuage mediates retrotransposon silencing in mouse primordial ovarian follicles. Development 140:3819–3825Google Scholar
  115. 115.
    Malki S, van der Heijden GW, O’Donnell KA, Martin SL, Bortvin A (2014) A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev Cell 29:521–533PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    de Cuevas M, Lilly MA, Spradling AC (1997) Germline cyst formation in Drosophila. Ann Rev Genet 31:405–428PubMedCrossRefGoogle Scholar
  117. 117.
    Wen J, Zhang H, Li G, Mao G, Chen X, Wang J, Guo M, Mu X, Ouyang H, Zhang M, Xia GL (2009) PAR6, a potential marker for the germ cells selected to form primordial follicles in mouse ovary. PLoS One 4(10):e7372PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Macara IG (2004) Par proteins: partners in polarization. Curr Biol 14:160–162CrossRefGoogle Scholar
  119. 119.
    Cox DN, Seyfried SA, Jan LY, Jan YN (2001) Bazooka and atypical protein kinase C are required to regulate oocyte differentiation in the Drosophila ovary. Proc Natl Acad Sci USA 98:14475–14480PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Benton R, Palacios IM, St Johnston D (2002) Drosophila 14-3-3/PAR-5 is an essential mediator of PAR-1 function in axis formation. Dev Cell 3:659–671PubMedCrossRefGoogle Scholar
  121. 121.
    Hurov JB, Watkins JL, Piwnica-Worms H (2004) Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Curr Biol 14:736–741PubMedCrossRefGoogle Scholar
  122. 122.
    Gumbiner BM (1996) Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84(3):345–357PubMedCrossRefGoogle Scholar
  123. 123.
    Takeichi M (2014) Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling. Nat Rev Mol Cell Biol 15:397–410PubMedCrossRefGoogle Scholar
  124. 124.
    Shapiro L, Fannon AM, Kwong PD, Thompson A, Lehmann MS, Grübel G, Legrand JF, Shimasaki S, Moore RK, Otsuka F, Erickson GF (2004) The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25:72–101CrossRefGoogle Scholar
  125. 125.
    Roggiani F, Mezzanzanica D, Rea K, Tomassetti A (2016) Guidance of signaling activations by cadherins and integrins in epithelial ovarian cancer cells. Int J Mol Sci 17(9):E1387PubMedCrossRefGoogle Scholar
  126. 126.
    Lechowska A, Bilinksi 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 break down. J Assist Reprod Genet 28(7):583–589PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Wang C, Roy SK (2010) Expression of E-cadherin and N-cadherin in perinatal hamster ovary: possible involvement in primordial follicle formation and regulation by follicle-stimulating hormone. Endocrinology 151:2319–2330PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Reddy P, Liu L, Ren C, Lindgren P, Boman K, Shen Y, Lundin E, Ottander U, Rytinki M, Liu K (2005) Formation of E-cadherin-mediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol Endocrinol 19:2564–2578PubMedCrossRefGoogle Scholar
  129. 129.
    Huber MA, Kraut N, Beug H (2005) Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 17:548–558PubMedCrossRefGoogle Scholar
  130. 130.
    Niu WB, Wang YJ, Wang ZP, Xin QL, Wang Y, Feng LZ, Zhao LH, Wen J, Zhang H, Wang C, Xia G (2016) JNK signaling regulates E-cadherin junctions in germline cysts and determines primordial follicle formation in mice. Development 143(10):1778–1787Google Scholar
  131. 131.
    Smith SR, Fulton N, Collins CS, Welsh M, Bayne RA, Coutts SM, Childs AJ, Anderson RA (2010) N- and E-cadherin expression in human ovarian and urogenital duc development. Fertil Steril 93:2348–2353PubMedCrossRefGoogle Scholar
  132. 132.
    Mitchell PA, Burghardt RC (1986) The ontogeny of nexuses (gap junctions) in the ovary of the fetal mouse. Anat Rec 214(3):283–288PubMedCrossRefGoogle Scholar
  133. 133.
    Pérez-Armendariz EM, Sáez JC, Bravo-Moreno JF, López-Olmos V, Enders GC, Villalpando I (2003) Connexin43 is expressed in mouse fetal ovary. Anat Rec A Discov Mol Cell Evol Biol 271(2):360–367PubMedCrossRefGoogle Scholar
  134. 134.
    Teng Z, Wang C, Wang Y, Huang K, Xiang X, Niu W, Feng L, Zhao L, Yan H, Zhang H (2016) Gap junctions are essential for murine primordial follicle assembly immediately before birth. Reproduction 151(2):105–115PubMedCrossRefGoogle Scholar
  135. 135.
    Juneja SC (2003) mRNA expression pattern of multiple members of connexin gene family in normal and abnormal fetal gonads in mouse. Indian J Physiology. Pharmacology 47:147–156Google Scholar
  136. 136.
    Fagbohun C, Downs S (1991) Metabolic coupling and ligand stimulated meiotic maturation in the mouse oocyte–cumulus cell complex. Biol Reprod 45:851–859PubMedCrossRefGoogle Scholar
  137. 137.
    Downs SM (1995) The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocyte. Dev Biol 167:502–512PubMedCrossRefGoogle Scholar
  138. 138.
    Simon AM, Goodenough DA, Li E, Paul DL (1997) Female infertility in mice lacking connexin 37. Nature 385:525–529PubMedCrossRefGoogle Scholar
  139. 139.
    Juneja SC, Barr KJ, Enders GC, Kidder GM (1999) Defects in the germ line and gonads of mice lacking Connexin43. Biol Reprod 60:1263–1270PubMedCrossRefGoogle Scholar
  140. 140.
    Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ (2001) Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121:647–653PubMedCrossRefGoogle Scholar
  141. 141.
    Combelles CM, Carabatsos MJ, Kumar TR, Matzuk MM, Albertini DF (2004) Hormonal control of somatic cell oocyte interactions during ovarian follicle development. Mol Reprod Dev 69:347–355PubMedCrossRefGoogle Scholar
  142. 142.
    Liu K (2006) Stem cell factor (SCF)-kit mediated phosphatidylinositol 3 (PI3) kinase signaling during mammalian oocyte growth and early follicular development. Front Biosci 11:126–135PubMedCrossRefGoogle Scholar
  143. 143.
    Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP (1999) Female development in mammals is regulated by Wnt-4 signalling. Nature 397:405–409PubMedCrossRefGoogle Scholar
  144. 144.
    Soyal SM, Amleh A, Dean J (2000) FIGα, a germ cell-specific transcription factor required for ovarian follicle formation. Development 127:4645–4654Google Scholar
  145. 145.
    Hori K, Sen A, Artavanis-Tsakonas S (2013) Notch signaling at a glance. J Cell Sci 126:2135–2140PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Johnson J, Espinoza T, McGaughey RW, Rawls A, Wilson-Rawls J (2001) Notch pathway genes are expressed in mammalian ovarian follicles. Mech Dev 109:355–361PubMedCrossRefGoogle Scholar
  147. 147.
    Hahn KL, Johnson J, Beres BJ, Howard S, Wilson-Rawls J (2005) Lunatic fringe null female mice are infertile due to defects in meiotic maturation. Development 132:817–828Google Scholar
  148. 148.
    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 11:13PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Manosalva I, Gonzalez A, Kageyama R (2013) Hes1 in the somatic cells of the murine ovary is necessary for oocyte survival and maturation. Dev Biol 375:140–151PubMedCrossRefGoogle Scholar
  150. 150.
    Trombly DJ, Woodruff TK, Mayo KE (2009) Suppression of notch signaling in the neonatal mouse ovary decreases primordial follicle formation. Endocrinology 150:1014–1024PubMedCrossRefGoogle Scholar
  151. 151.
    Borggrefe T, Oswald F (2009) The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 66:1631–1646PubMedCrossRefGoogle Scholar
  152. 152.
    Vanorny DA, Prasasya RD, Chalpe AJ, Kilen SM, Mayo KE (2014) Notch signaling regulates ovarian follicle formation and coordinates follicular growth. Mol Endocrinol 28:499–511PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Vincent B (2016) Regulation of the α-secretase ADAM10 at transcriptional, translational and post-translational levels. Brain Res Bull 126(Pt 2):154–169PubMedCrossRefGoogle Scholar
  154. 154.
    Hayashida K, Bartlett AH, Chen Y, Park PW (2010) Molecular and cellular mechanisms of ectodomain shedding. Anat Rec (Hoboken) 293:925–937CrossRefGoogle Scholar
  155. 155.
    Reiss K, Saftig P (2009) The “a disintegrin and metalloprotease” (ADAM) family of sheddases: physiological and cellular functions. Semin Cell Dev Biol 20:126–137PubMedCrossRefGoogle Scholar
  156. 156.
    Weber S, Saftig P (2012) Ectodomain shedding and ADAMs in development. Development 139: 3693–3709Google Scholar
  157. 157.
    Zhao L, Du X, Huang K, Zhang T, Teng Z, Niu W, Wang C, Xia GL (2016) Rac1 modulates the formation of primordial follicles by facilitating STAT3-directed Jagged1, GDF9 and BMP15 transcription in mice. Sci Rep 6:23972Google Scholar
  158. 158.
    Gu Y, Runyan C, Shoemaker A, Surani A, Wylie C (2009) Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration. Development 136:1295–1303Google Scholar
  159. 159.
    Richardson BE, Lehmann R (2010) Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 11:37–49PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Coutts SM, Childs AJ, Fulton N, Collins C, Bayne RAL, McNeilly AS, Anderson RA (2008) Activin signals via SMAD2/3 between germ and somatic cells in the human fetal ovary and regulates kit ligand expression. Dev Biol 314:189–199PubMedCrossRefGoogle Scholar
  161. 161.
    Jones RL, Pepling ME (2013) KIT signaling regulates primordial follicle formation in the neonatal mouse ovary. Dev Biol 382:186–197PubMedCrossRefGoogle Scholar
  162. 162.
    Findlay JK, Drummond AE, Dyson ML, Baillie AJ, Robertson DM, Ethier JF (2002) Recruitment and development of the follicle; the roles of the transforming growth factor-beta superfamily. Mol Cell Endocrinol 191:35–43Google Scholar
  163. 163.
    Knight PG, Glister C (2003) Local roles of TGF-beta superfamily members in the control of ovarian follicle development. Anim Reprod Sci 78:165–183PubMedCrossRefGoogle Scholar
  164. 164.
    Knight PG, Glister C (2006) TGF-beta superfamily members and ovarian follicle development. Reproduction 132(2):191–206PubMedCrossRefGoogle Scholar
  165. 165.
    Shimasaki S, Moore RK, Otsuka F, Erickson GF (2004) The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25:72–101PubMedCrossRefGoogle Scholar
  166. 166.
    Childs AJ, Anderson RA (2009) Activin A selectively represses expression of the membrane bound isoform of Kit ligand in human fetal ovary. Fertil Steril 92(4):1416–1419PubMedCrossRefGoogle Scholar
  167. 167.
    Deng Y, Ren X, Yang L, Lin Y Wu X (2003) A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 115:61–70PubMedCrossRefGoogle Scholar
  168. 168.
    Huang C, Rajfur Z, Borchers C, Schaller MD, Jacobson K (2003) JNK phosphorylates paxillin and regulates cell migration. Nature 424:219–223PubMedCrossRefGoogle Scholar
  169. 169.
    Pallavi SK, Ho DM, Hicks C, Miele L, Artavanis-Tsakonas S (2012) Notch and Mef2 synergize to promote proliferation and metastasis through JNK signal activation in Drosophila. EMBO J 31:2895–2907PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Bagowski CP, Xiong W, Ferrell JEJr (2001) c-Jun N-terminal kinase activation in Xenopus laevis eggs and embryos. A possible non-genomic role for the JNK signaling pathway. J Biol Chem 276:1459–1465PubMedCrossRefGoogle Scholar
  171. 171.
    Oktem O, Buyuk E, Oktay K (2011) Preantral follicle growth is regulated by c-Jun-N-terminal kinase (JNK) pathway. Reprod Sci 18:269–276Google Scholar
  172. 172.
    Etchegaray JI, Timmons AK, Klein AP, Pritchett TL, Welch E, Meehan TL, Li C, McCall K (2012) Draper acts through the JNK pathway to control synchronous engulfment of dying germline cells by follicular epithelial cells. Development 139:4029–4039Google Scholar
  173. 173.
    Igaki T, Pagliarini RA, Xu T (2006) Loss of cell polarity drives tumor growth and invasion through JNK activation in Drosophila. Curr Biol 16:1139–1146PubMedCrossRefGoogle Scholar
  174. 174.
    Flora Llense, Enrique, Martı´n-Blanco (2008) JNK Signaling Controls Border Cell Cluster Integrity and Collective Cell Migration. Curr Biol 18:538–544PubMedCrossRefGoogle Scholar
  175. 175.
    Liao G, Tao Q, Kofron M, Chen JS, Schloemer A, Davis RJ, Hsieh JC, Wylie C, Heasman J, Kuan CY (2006) Jun NH2-terminal kinase (JNK) prevents nuclear beta-catenin accumulation and regulates axis formation in Xenopus embryos. Proc Natl Acad Sci U S A 103:16313–16318PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    Lee MH, Koria P, Qu J, Andreadis ST (2009) JNK phosphorylates beta-catenin and regulates adherens junctions. FASEB J 23:3874–3883PubMedPubMedCentralCrossRefGoogle Scholar
  177. 177.
    Lee MH, Padmashali R, Koria P, Andreadis ST (2011) JNK regulates binding of alpha-catenin to adherens junctions and cell-cell adhesion. FASEB J 25:613–623PubMedPubMedCentralCrossRefGoogle Scholar
  178. 178.
    Aktories K (1997) Bacterial toxins that target Rho proteins. J Clin Invest 99:827PubMedPubMedCentralCrossRefGoogle Scholar
  179. 179.
    Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509PubMedCrossRefGoogle Scholar
  180. 180.
    Halet G, Carroll J (2007) Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev Cell 12:309–317PubMedCrossRefGoogle Scholar
  181. 181.
    Nicola C, Lala PK, Chakraborty C (2008) Prostaglandin E2-mediated migration of human trophoblast requires RAC1 and CDC42. Biol Reprod 78:976PubMedCrossRefGoogle Scholar
  182. 182.
    Ma HL, Gong F, Tang Y, Li X, Li X, Yang X, Lu G (2015) Inhibition of endometrial Tiam1/Rac1 signals induced by miR-22 up-regulation leads to the failure of embryo implantation during the implantation window in pregnant mice. Biol Reprod 92:152PubMedCrossRefGoogle Scholar
  183. 183.
    Tu Z, Wang Q, Cui T, Wang J, Ran H, Bao H, Lu J, Wang B, Lydon JP, DeMayo F, Zhang S, Kong S, Wu X, Wang H (2016) Uterine RAC1 via Pak1-ERM signaling directs normal luminal epithelial integrity conducive to on-time embryo implantation in mice. Cell Death Differ 23:169–181PubMedCrossRefGoogle Scholar
  184. 184.
    Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL (2001) Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol (Baltimore, Md.) 15:854–866PubMedCrossRefGoogle Scholar
  185. 185.
    Suzumori N, Yan C, Matzuk MM, Rajkovic A (2002) Nobox is a homeoboxencoding gene preferentially expressed in primordial and growing oocytes. Mech Dev 111:137–141PubMedCrossRefGoogle Scholar
  186. 186.
    Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM (2004) NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305:1157–1159PubMedCrossRefGoogle Scholar
  187. 187.
    Elvin JA, Yan C, Matzuk MM (2000) Oocyte-expressed TGF-beta superfamily members in female fertility. Mol Cell Endo 159:1–5Google Scholar
  188. 188.
    Teng Z, Wang C, Wang Y, Huang K, Xiang X, Niu W, Feng L, Zhao L, Yan H, Zhang H, Xia G (2015) S100A8, an oocyte-specific chemokine, directs the migration of ovarian somatic cells during mouse primordial follicle assembly. J Cell Physiol 230(12):2998–3008PubMedCrossRefGoogle Scholar
  189. 189.
    Greenfeld CR, Roby KF, Pepling ME, Babus JK, Terranova PF, Flaws JA (2007) Tumor necrosis factor (TNF) receptor type 2 is an important mediator of TNF alpha function in the mouse ovary. Biol Reprod 76:224–231PubMedCrossRefGoogle Scholar
  190. 190.
    Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, Jurisicova A, Varmuza S, Latham KE, Flaws JA, Salter JC, Hara H, Moskowitz MA, Li E, Greenberg A, Tilly JL, Yuan J (1998) Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 12:1304–1314PubMedPubMedCentralCrossRefGoogle Scholar
  191. 191.
    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 21:200–203PubMedCrossRefGoogle Scholar
  192. 192.
    Wordinger R, Sutton J, Brun-Zinkernagel AM (1990) Ultrastructure of oocyte migration through the mouse ovarian surface epithelium during neonatal development. Anat Rec 227:187–198PubMedCrossRefGoogle Scholar
  193. 193.
    Mackay S, Smith RA, Haig T (1992) An investigation of the migratory potential of mouse oocytes in vitro. J Anatom 181:437–446Google Scholar
  194. 194.
    Ruma IM, Putranto EW, Kondo E, Murata H, Watanabe M, Huang P, Kinoshita R, Futami J, Inoue Y, Yamauchi A, Sumardika IW, Youyi C, Yamamoto K, Nasu Y, Nishibori M, Hibino T, Sakaguchi M (2016) MCAM, as a novel receptor for S100A8/A9, mediates progression of malignant melanoma through prominent activation of NF-κB and ROS formation upon ligand binding. Clin Exp Metastasis 33(6):609–627PubMedCrossRefGoogle Scholar
  195. 195.
    He Z, Riva M, Björk P, Swärd K, Mörgelin M, Leanderson T, Ivars F (2016) CD14 is a co-receptor for TLR4 in the S100A9-induced pro-inflammatory response in monocytes. PLoS One 11(5):e0156377PubMedPubMedCentralCrossRefGoogle Scholar
  196. 196.
    Iguchi T, Fukazawa Y, Uesugi Y, Takasugi N (1990) Polyovular follicles in mouse ovaries exposed neonatally to diethylstilbestrol in vivo and in vitro. Biol Reprod 43:478–484PubMedCrossRefGoogle Scholar
  197. 197.
    Zhang HQ, Zhang XF, Zhang LJ, Chao HH, Pan B, Feng YM, Li L, Sun XF, Shen W (2012) Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes. Mol Biol Rep 39(5):5651–5657PubMedCrossRefGoogle Scholar
  198. 198.
    Jefferson WN, Couse JF, Padilla-Banks E, Korach KS, Newbold RR (2002) Neonatal exposure to genistein induces estrogen receptor (ER)α expression and multioocyte follicles in the maturing mouse ovary: evidence for ERβ-mediated and nonestrogenic actions. Biol Reprod 67:1285–1296PubMedCrossRefGoogle Scholar
  199. 199.
    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 148:3580–3590PubMedCrossRefGoogle Scholar
  200. 200.
    Kipp JL, Kilen SM, Bristol-Gould S, Woodruff TK, Mayo KE (2007) Neonatal exposure to estrogens suppresses activin expression and signaling in the mouse ovary. Endocrinology 148:1968–1976PubMedCrossRefGoogle Scholar
  201. 201.
    Guo M, Zhang H, Bian F, Li G, Mu X, Wen J, Mao G, Teng Z, Xia G, Zhang M (2012) P4 down-regulates Jagged2 and Notch1 expression during primordial folliculogenesis. Front Biosci (Elite Ed) 4:2731–2744Google Scholar
  202. 202.
    Guo M, Zhang C, Wang Y, Feng LZ, Wang ZP, Niu WB, Du XY, Tang W, Li Y, Wang C, Chen ZW (2016) Progesterone receptor membrane component 1 mediates progesterone-induced suppression of oocyte meiotic prophase I and primordial folliculogenesis. Sci Rep 6:36869Google Scholar
  203. 203.
    Dutta S, Mark-Kappeler CJ, Hoyer PB, Pepling ME (2014) The steroid hormone environment during primordial follicle formation in perinatal mouse ovaries. Biol Reprod 91:68PubMedCrossRefGoogle Scholar
  204. 204.
    Levin ER (2005) Integration of the extranuclear and nuclear actions of estrogen. Mol Endocrinol 19(8):1951–1959PubMedPubMedCentralCrossRefGoogle Scholar
  205. 205.
    Morohaku K, Tanimoto R, Sasaki K, Kawahara-Miki R, Kono T, Hayashi K, Hirao Y, Obata Y (2016) Complete in vitro generation of fertile oocytes from mouse primordial germ cells. Proc Natl Acad Sci USA 113(32):9021–9026PubMedPubMedCentralCrossRefGoogle Scholar
  206. 206.
    Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, Shimamoto S, Imamura T, Nakashima K, Saitou M, Hayashi K (2016) Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature. doi: 10.1038/nature20104 PubMedGoogle Scholar
  207. 207.
    Nicholas CZ, Reinhart BB, Eugene DA, Gerald JP (2002) Developmental regulation of baboon fetal ovarian maturation by estrogen. Biol Reprod 67(4):1148–1156CrossRefGoogle Scholar
  208. 208.
    Wang C, Roy SK (2007) Development of primordial follicles in the hamster: role of estradiol-17beta. Endocrinology 148:1707–1716PubMedCrossRefGoogle Scholar
  209. 209.
    Wang C, Prossnitz ER, Roy SK (2008) G protein-coupled receptor 30 expression is required for estrogen stimulation of primordial follicle formation in the hamster ovary. Endocrinology 149:4452–4461PubMedPubMedCentralCrossRefGoogle Scholar
  210. 210.
    Zachos NC, Billiar RB, Albrecht ED, Pepe GJ (2004) Regulation of oocyte microvilli development in the baboon fetal ovary by estrogen. Endocrinology 145:959–966PubMedCrossRefGoogle Scholar
  211. 211.
    Pepe GJ, Billiar RB, Albrecht ED (2006) Regulation of baboon fetal ovarian folliculogenesis by estrogen. Mol Cell Endocrinol 247(1–2):41–46Google Scholar
  212. 212.
    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 96:1754–1762PubMedCrossRefGoogle Scholar
  213. 213.
    Nagamani M, McDonough PG, Ellegood JO, Mahesh VB (1979) Maternal and amniotic fluid steroids throughout human pregnancy. Am J Obstet Gynecol 134:674–680PubMedCrossRefGoogle Scholar
  214. 214.
    Wu CH, Mennuti MT, Mikhail G (1979) Free and protein-bound steroids in amniotic fluid of midpregnancy. Am J Obstet Gynecol 133:666–672PubMedCrossRefGoogle Scholar
  215. 215.
    Martins da Silva SJ, Bayne RAL, Cambray N, Hartley PS, McNeilly AS, Anderson RA (2004) Expression of activin subunits and receptors in the developing human ovary: activin A promotes germ cell survival and proliferation before primordial follicle formation. Dev Biol 266:334–345PubMedCrossRefGoogle Scholar
  216. 216.
    Nilsson E, Dole G, Skinner MK (2009) Neurotrophin NT3 promotes ovarian primordial to primary follicle transition. Reproduction 138:697–707PubMedCrossRefGoogle Scholar
  217. 217.
    Lei L, Jin S, Gonzalez G, Behringer RR, Woodruff TK (2010) The regulatory role of Dicer in folliculogenesis in mice. Mol Cell Endocrinol 315(1–2):63–73PubMedCrossRefGoogle Scholar
  218. 218.
    Chakraborty P, Roy SK (2014) Expression of FSH receptor in the hamster ovary during perinatal development. Mol Cell Endocrinol 400:41–47Google Scholar
  219. 219.
    Vomachka AJ, Greenwald GS (1979) The development of gonadotropin and steroid hormone patterns in male and female hamsters from birth to puberty. Endocrinology 105:960–966PubMedCrossRefGoogle Scholar
  220. 220.
    Halpin DM, Jones A, Fink G, Charlton HM (1986) Postnatal ovarian follicle development in hypogonadal (hpg) and normal mice and associated changes in the hypothalamic–pituitary ovarian axis. J Reprod Fert 77:287–296CrossRefGoogle Scholar
  221. 221.
    O’Shaughnessy PJ, Marsh P, Dudley K (1994) Follicle-stimulating hormone receptor mRNA in the mouse ovary during post-natal development in the normal mouse and in the adult hypogonadal (hpg) mouse: structure of alternate transcripts. Mol Cell Endocrino 101:197–201Google Scholar
  222. 222.
    Roy SK, Albee L (2000) Requirement for follicle-stimulating hormone action in the formation of primordial follicles during perinatal ovarian development in the hamster. Endocrinology 141:4449–4456PubMedCrossRefGoogle Scholar
  223. 223.
    Wang J, Roy SK (2004) Growth differentiation factor-9 and stem cell factor promote primordial follicle formation in the hamster: modulation by follicle-stimulating hormone. Biol Reprod 70:577–585PubMedCrossRefGoogle Scholar
  224. 224.
    Saatcioglu HD, Cuevas I, Castrillon DH (2016) Control of oocyte reawakening by kit. PLoS Genet 12(8):e1006215PubMedPubMedCentralCrossRefGoogle Scholar
  225. 225.
    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 298:132–148PubMedCrossRefGoogle Scholar
  226. 226.
    Kimura F, Bonomi LM, Schneyer AL (2011) Follistatin regulates germ cell nest breakdown and primordial follicle formation. Endocrinology 152:697–706PubMedCrossRefGoogle Scholar
  227. 227.
    Wang Z, Niu W, Wang Y, Teng Z, Wen J, Xia G, Wang C (2015) Follistatin288 regulates germ cell cyst breakdown and primordial follicle assembly in the mouse ovary. PLoS One 10(6):e0129643PubMedPubMedCentralCrossRefGoogle Scholar
  228. 228.
    Kelly LW, Yogeshwar M, Craig A (2012) Harrison New insights into the mechanisms of activin action and inhibition. Mol Cell Endo 359:2–12Google Scholar
  229. 229.
    Freiman RN, Albright SR, Zheng S, Sha WC, Hammer RE, Tjian R (2001) Requirement of tissue-selective TBP-associated factor TAFII105 in ovarian development. Science 293:2084–2087PubMedCrossRefGoogle Scholar
  230. 230.
    Brambell FWR (1927) The Development and Morphology of the Gonads of the Mouse—Part I. The morphogenesis of the indifferent gonad and of the ovary. Proc R Soc B 101:391–409Google Scholar
  231. 231.
    Hirshfield AN (1991) Development of follicles in the mammalian ovary. Int Rev Cytol 124:43–99PubMedCrossRefGoogle Scholar
  232. 232.
    Findlay JK, Hutt KJ, Hickey M, Anderson RA (2015) How is the number of primordial follicles in the ovarian reserve established? Biol Reprod 93(5):111PubMedCrossRefGoogle Scholar
  233. 233.
    Motta PM, Nottola SA, Makabe S, Heyn R (2000) Mitochondrial morphology in human fetal and adult female germ cells. Hum Reprod 2:129–147CrossRefGoogle Scholar
  234. 234.
    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 148:121–135PubMedPubMedCentralGoogle Scholar
  235. 235.
    Leung P, Adashi E (2003) The ovary. Elsevier Academic Press, San DiegoGoogle Scholar
  236. 236.
    Shuster LT, Rhodes DJ, Gostout BS, Grossardt BR, Rocca WA (2010) Premature menopause or early menopause: long-term health consequences. Maturitas 65:161–166PubMedCrossRefGoogle Scholar
  237. 237.
    Peterson JS, Timmons AK, Mondragon AA, McCall K (2015) The end of the beginning: cell death in the germline. Curr Top Dev Biol 114:93–119PubMedCrossRefGoogle Scholar
  238. 238.
    Gozuacik D, Kimchi A (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23(16):2891–2906PubMedCrossRefGoogle Scholar
  239. 239.
    Coucouvanis EC, Sherwood SW, Carswell-Crumpton C, Spack EG, Jones PP (1993) Evidence that the mechanism of prenatal germ cell death in the mouse is apoptosis. Exp Cell Res 209:238–247PubMedCrossRefGoogle Scholar
  240. 240.
    Bergeron JM, Gahr M, Horan K, Wibbels T, Crews D (1998) Cloning and in situ hybridization analysis of estrogen receptor in the developing gonad of the red-eared slider turtle, a species with temperaturedependent sex determination. Dev Growth Diff 40:243–254Google Scholar
  241. 241.
    De Felici M, Lobascio AM, Klinger FG (2008) Cell death in fetal oocytes: many players for multiple pathways. Autophagy 4(2):240–242PubMedCrossRefGoogle Scholar
  242. 242.
    Takai Y, Matikainen T, Jurisicova A, Kim MR, Trbovich AM, Fujita E, Nakagawa T (2007) Caspase-12 compensates for lack of caspase-2 and caspase-3 in female germ cells. Apoptosis 12:791–800PubMedCrossRefGoogle Scholar
  243. 243.
    Xu B, Hua J, Zhang Y, Jiang X, Zhang H, Ma T, Zheng W, Sun R, Shen W, Sha J (2011) Proliferating cell nuclear antigen (PCNA) regulates primordial follicle assembly by promoting apoptosis of oocytes in fetal and neonatal mouse ovaries. PLoS ONE 6:e16046PubMedPubMedCentralCrossRefGoogle Scholar
  244. 244.
    Morita Y, Maravei DV, Bergeron L, Wang S, Perez GI, Tsutsumi O, Taketani Y, Asano M, Horai R, Korsmeyer SJ (2001) Caspase-2 deficiency prevents programmed germ cell death resulting from cytokine insufficiency but not meiotic defects caused by loss of ataxia telangiectasia mutated (Atm) gene function. Cell Death Differ 8:614–620PubMedCrossRefGoogle Scholar
  245. 245.
    Lobascio AM, Klinger FG, Scaldaferri ML, Farini D, De Felici M (2007) Analysis of programmed cell death in mouse fetal oocytes. Reproduction 134(2):241–252PubMedCrossRefGoogle Scholar
  246. 246.
    Rodrigues P, Limback D, McGinnis LK, Plancha CE Albertini DF (2009) Multiple mechanisms of germ cell loss in the perinatal mouse ovary. Reproduction 137:709–720PubMedCrossRefGoogle Scholar
  247. 247.
    Gawriluk TR, Hale AN, Flaws JA, Dillon CP, Green DR, Rucker EB III (2011) Autophagy is a cell survival program for female germ cells in the murine ovary. Reproduction 141:759–765PubMedCrossRefGoogle Scholar
  248. 248.
    Gump JM, Thorburn A (2011) Autophagy and apoptosis: what is the connection? Trends Cell Biol 21(7):387–392PubMedPubMedCentralCrossRefGoogle Scholar
  249. 249.
    Mukhopadhyay S, Panda PK, Sinha N, Das DN, Bhutia SK (2014) Autophagy and apoptosis: where do they meet? Apoptosis 19(4):555–566PubMedCrossRefGoogle Scholar
  250. 250.
    Wei Y, Sinha S, Levine B (2008) Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4:949–951PubMedPubMedCentralCrossRefGoogle Scholar
  251. 251.
    Danial NN (2007) BCL-2 family proteins: critical checkpoints of apoptotic cell death. Clin Cancer Res 13:7254–7263PubMedCrossRefGoogle Scholar
  252. 252.
    Alton M, Taketo T (2007) Switch from BAX-dependent to BAX-independent germ cell loss during the development of fetal mouse ovaries. J Cell Sci 120:417–424PubMedCrossRefGoogle Scholar
  253. 253.
    Greenfeld CR, Pepling ME, Babus JK, Furth PA, Flaws JA (2007) BAX regulates follicular endowment in mice. Reproduction, vol 133, Cambridge, England, pp 865–876Google Scholar
  254. 254.
    Chen Y, Breen K, Pepling ME (2009) Estrogen can signal through multiple pathways to regulate oocyte cyst breakdown and primordial follicle assembly in the neonatal mouse ovary. J Endocrinol 202:407–417PubMedCrossRefGoogle Scholar
  255. 255.
    Omari S, Waters M, Naranian T, Kim K, Perumalsamy AL, Chi M, Greenblatt E, Moley KH, Opferman JT, Jurisicova A (2015) Mcl-1 is a key regulator of the ovarian reserve. Cell Death and Disease 6:e1755Google Scholar
  256. 256.
    Hartley PS, Bayne RAL, Robinson LLL, Fulton N, Anderson RA (2002) Developmental changes in expression of myeloid cell leukaemia-1 in human germ cells during oogenesis and early folliculogenesis. J Clin Endocrinol Metab 87:3417–3427PubMedCrossRefGoogle Scholar
  257. 257.
    Perez GI, Trbovich AM, Gosden RG, Tilly JL (2000) Mitochondria and the death of oocytes. Nature 403:500–501PubMedCrossRefGoogle Scholar
  258. 258.
    Zhang J, Ji X, Zhou D, Li Y, Lin J, Liu J, Luo H, Cui S (2013) miR-143 is critical for the formation of primordial follicles in mice. Front Biosci (Landmark) 18:588–597CrossRefGoogle Scholar
  259. 259.
    Zhang H, Jiang XH, Zhang YW, Xu B, Hua J, Ma TL, Zheng W, Sun R, Shen W, Cooke HJ, Hao QM, Qiao J, Shi QH (2014) microRNA 376a regulates follicle assembly by targeting Pcna in fetal and neonatal mouse ovaries. Reproduction 148:43–54PubMedCrossRefGoogle Scholar
  260. 260.
    Kanninen TT, de Andrade Ramos BR, Tomi WSS (2013) The role of autophagy in reproduction from gametogenesis to parturition. Euro obestetrics genecology. Reprod Biol 171:3–8Google Scholar
  261. 261.
    Hulas-Stasiak M, Gawron A (2011) Follicular atresia in the prepubertal spiny mouse (Acomys cahirinus) ovary. Apoptosis 16:967–975PubMedCrossRefGoogle Scholar
  262. 262.
    Song ZH, Yu HY, Wang P, Mao GK, Liu WX, Li MN, Wang HN, Shang YL, Liu C, Xu ZL, Sun QY, Li W (2015) Germ cell-specific Atg7 knockout results in primary ovarian insufficiency in female mice. Cell Death Dis 6:e1589Google Scholar
  263. 263.
    Packer AI, Hsu YC, Besmer P, Bachvarova RF (1994) The ligand of the c-kit receptor promotes oocyte growth. Dev Biol 161:194–205PubMedCrossRefGoogle Scholar
  264. 264.
    Huang EJ, Manova K, Packer AI, Sanchez S, Bachvarova RF, Besmer P (1993) The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev Biol 157:100–109PubMedCrossRefGoogle Scholar
  265. 265.
    Bedell MA, Brannan CI, Evans EP, Copeland NG, Jenkins NA, Donovan PJ (1995) DNA rearrangements located over 100 kb 50 of the Steel (Sl)-coding region in Steel-panda and Steel-contrasted mice deregulate Sl expression and cause female sterility by disrupting ovarian follicle development. Genes Dev 9:455–470PubMedCrossRefGoogle Scholar
  266. 266.
    Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley L (2002) Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/Akt pathway. Mol Cell 10(1):151–162PubMedCrossRefGoogle Scholar
  267. 267.
    Zhang X, Zhang H, Gao Q, Ji S, Bing L, Hao J (2015) Sohlh2 inhibits the apoptosis of mouse primordial follicle oocytes via C-kit/PI3K/Akt/Foxo3a signalling pathway. Reprod Biomed Online 30(5):514–521PubMedCrossRefGoogle Scholar
  268. 268.
    Sawyer H, Smith P, Heath DA, Juengel JL, Wakefield SJ, McNatty KP (2002) Formation of ovarian follicles during fetal development in sheep. Biol Reprod 66:1134–1150PubMedCrossRefGoogle Scholar
  269. 269.
    Norah S, Michael DM, Lynne LLR, Norma F, Helen C, Kohji S, Evelyn ET, Richard AA, David JP (2003) The role of neurotrophin receptors in female germ-cell survival in mouse and human. Development 130:5481–5491Google Scholar
  270. 270.
    Su WH, Guan XG, Di Z, Sun MY, Yang LF, Yi F, Feng H, Feng XC, Ma TH (2013) Occurrence of multi-oocyte follicles in aquaporin8-deficient mice. Reprod Biol Endocrinol 11:88PubMedPubMedCentralCrossRefGoogle Scholar
  271. 271.
    Jablonski EM, Webb AN, McConnell NA, Riley MC, Hughes FM Jr (2004) Plasma membrane aquaporin activity can affect the rate of apoptosis but is inhibited after apoptotic volume decrease. Am J Physiol Cell Physiol 286:975–985CrossRefGoogle Scholar
  272. 272.
    Su W, Qiao Y, Yi F, Guan X, Zhang D, Zhang S, Hao F, Xiao Y, Zhang H, Guo L, Yang L, Feng X, Ma T (2010) Increased female fertility in aquaporin 8-deficient mice. IUBMB Life 62:852–857PubMedCrossRefGoogle Scholar
  273. 273.
    Sakata S, Sakamaki K, Watanabe K, Nakamura N, Toyokuni S, Nishimune Y, Mori C, Yonehara S (2003) Involvement of death receptor Fas in germ cell degeneration in gonads of Kit-deficient Wv/Wv mutant mice. Cell Death Differ 10:676–686PubMedCrossRefGoogle Scholar
  274. 274.
    Moniruzzaman M, Sakamaki K, Akazawa Y, Miyano T (2007) Oocyte growth and follicular development in KIT-deficient Fas-knockout mice. Reproduction 133:117–125PubMedCrossRefGoogle Scholar
  275. 275.
    Cui LL, Yang G, Pan J, Zhang C (2011) Tumor necrosis factor alpha knockout increases fertility of mice. Theriogenology 75:867–876PubMedCrossRefGoogle Scholar
  276. 276.
    Kashimada K, Pelosi E, Chen H, Schlessinger D, Willhelm D, Koopman P (2011) FOXL2 and BMP2 act cooperatively to regulate Follistatin gene expression during ovarian development. Endocrinology 152(1):272–280PubMedCrossRefGoogle Scholar
  277. 277.
    Yao HH, Matzuk MM, Jorgez CJ, Menke DB, Page DC, Swain A, Capel B (2004) Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev Dyn 230:210–215PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing 2017

Authors and Affiliations

  1. 1.State Key Laboratory for Agro-Biotechnology, College of Biological ScienceChina Agricultural UniversityBeijingChina

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