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Control of Oocyte Growth and Development by Intercellular Communication Within the Follicular Niche

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Molecular Mechanisms of Cell Differentiation in Gonad Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 58))

Abstract

In the mammalian ovary, each oocyte grows and develops within its own structural and developmental niche—the follicle. Together with the female germ cell in the follicle are somatic granulosa cells, specialized companion cells that surround the oocyte and provide support to it, and an outer layer of thecal cells that serve crucial roles including steroid synthesis. These follicular compartments function as a single physiological unit whose purpose is to produce a healthy egg, which upon ovulation can be fertilized and give rise to a healthy embryo, thus enabling the female germ cell to fulfill its reproductive potential. Beginning from the initial stage of follicle formation and until terminal differentiation at ovulation, oocyte and follicle growth depend absolutely on cooperation between the different cellular compartments. This cooperation synchronizes the initiation of oocyte growth with follicle activation. During growth, it enables metabolic support for the follicle-enclosed oocyte and allows the follicle to fulfill its steroidogenic potential. Near the end of the growth period, intra-follicular interactions prevent the precocious meiotic resumption of the oocyte and ensure its nuclear differentiation. Finally, cooperation enables the events of ovulation, including meiotic maturation of the oocyte and expansion of the cumulus granulosa cells. In this chapter, we discuss the cellular interactions that enable the growing follicle to produce a healthy oocyte, focusing on the communication between the germ cell and the surrounding granulosa cells.

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References

  • Abe K, Inoue A, Suzuki MG, Aoki F (2010) Global gene silencing is caused by the dissociation of RNA polymerase II from DNA in mouse oocytes. J Reprod Dev 56:502–507

    Article  CAS  PubMed  Google Scholar 

  • Adashi EY (1994) Endocrinology of the ovary. Hum Reprod 9:815–827

    Article  CAS  PubMed  Google Scholar 

  • Adhikari D, Flohr G, Gorre N et al (2009) Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol Hum Reprod 15:765–770

    Article  CAS  PubMed  Google Scholar 

  • Adhikari D, Zheng W, Shen Y et al (2010) Tsc/mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum Mol Genet 19:397–410

    Article  CAS  PubMed  Google Scholar 

  • Albertini DF, Rider V (1994) Patterns of intercellular connectivity in the mammalian cumulus-oocyte complex. Microsc Res Tech 27:125–133

    Article  CAS  PubMed  Google Scholar 

  • Anderson E, Albertini DF (1976) Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol 71:680–686

    Article  CAS  PubMed  Google Scholar 

  • Andreu-Vieyra CV, Chen R, Agno JE et al (2010) MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol 8:e1000453

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arakane F, Sugawara T, Nishino H et al (1996) Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mitochondrial import sequence: implications for the mechanism of StAR action. Proc Natl Acad Sci U S A 93:13731–13736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashkenazi H, Cao X, Motola S et al (2005) Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146:77–84

    Article  CAS  PubMed  Google Scholar 

  • Bachvarova R (1985) Gene expression during oogenesis and oocyte development in mammals. Dev Biol (N Y 1985) 1:453–524

    CAS  Google Scholar 

  • Balasubramanian K, Lavoie HA, Garmey JC et al (1997) Regulation of porcine granulosa cell steroidogenic acute regulatory protein (StAR) by insulin-like growth factor I: synergism with follicle-stimulating hormone or protein kinase A agonist. Endocrinology 138:433–439

    CAS  PubMed  Google Scholar 

  • Baranova NS, Inforzato A, Briggs DC et al (2014) Incorporation of pentraxin 3 into hyaluronan matrices is tightly regulated and promotes matrix cross-linking. J Biol Chem 289:30481–30498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berisha B, Pfaffl MW, Schams D (2002) Expression of estrogen and progesterone receptors in the bovine ovary during estrous cycle and pregnancy. Endocrine 17:207–214

    Article  CAS  PubMed  Google Scholar 

  • Billig H, Furuta I, Hsueh AJ (1993) Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 133:2204–2212

    CAS  PubMed  Google Scholar 

  • Boland NI, Humpherson PG, Leese HJ, Gosden RG (1994) The effect of glucose metabolism on murine follicle development and steroidogenesis in vitro. Hum Reprod 9:617–623

    CAS  PubMed  Google Scholar 

  • Bornslaeger EA, Wilde MW, Schultz RM (1984) Regulation of mouse oocyte maturation: involvement of cyclic AMP phosphodiesterase and calmodulin. Dev Biol 105:488–499

    Article  CAS  PubMed  Google Scholar 

  • Borum K (1961) Oogenesis in the mouse. A study of the meiotic prophase. Exp Cell Res 24:495–507

    Article  CAS  PubMed  Google Scholar 

  • Bouniol-Baly C, Hamraoui L, Guibert J et al (1999) Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biol Reprod 60:580–587

    Article  CAS  PubMed  Google Scholar 

  • Braw-Tal R (2002) The initiation of follicle growth: the oocyte or the somatic cells? Mol Cell Endocrinol 187:11–18

    Article  CAS  PubMed  Google Scholar 

  • Brinster RL (1971) Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey. J Reprod Fertil 24:187–191

    Article  CAS  PubMed  Google Scholar 

  • Britt KL, Drummond AE, Cox VA et al (2000) An age-related ovarian phenotype in mice with targeted disruption of the Cyp 19 (aromatase) gene. Endocrinology 141:2614–2623

    CAS  PubMed  Google Scholar 

  • Brunet S, Maro B (2005) Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 130:801–811

    Article  CAS  PubMed  Google Scholar 

  • Brunet A, Bonni A, Zigmond MJ et al (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–868

    Article  CAS  PubMed  Google Scholar 

  • Brunn GJ, Hudson CC, Sekulic A et al (1997) Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277:99–101

    Article  CAS  PubMed  Google Scholar 

  • Buccione R, Vanderhyden BC, Caron PJ, Eppig JJ (1990) FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev Biol 138:16–25

    Article  CAS  PubMed  Google Scholar 

  • Camp TA, Rahal JO, Mayo KE (1991) Cellular localization and hormonal regulation of follicle-stimulating hormone and luteinizing hormone receptor messenger RNAs in the rat ovary. Mol Endocrinol 5:1405–1417

    Article  CAS  PubMed  Google Scholar 

  • Carabatsos MJ, Elvin J, Matzuk MM, Albertini DF (1998) Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol 204:373–384

    Article  CAS  PubMed  Google Scholar 

  • Castrillon DH, Miao L, Kollipara R et al (2003) Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301:215–218

    Article  CAS  PubMed  Google Scholar 

  • Chang HC, Liu H, Zhang J et al (2005) Developmental incompetency of denuded mouse oocytes undergoing maturation in vitro is ooplasmic in nature and is associated with aberrant Oct-4 expression. Hum Reprod 20:1958–1968

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Russell PT, Larsen WJ (1993) Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol Reprod Dev 34:87–93

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Zhang H, Powers RW et al (1996) Covalent linkage between proteins of the inter-alpha-inhibitor family and hyaluronic acid is mediated by a factor produced by granulosa cells. J Biol Chem 271:19409–19414

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Melton C, Suh N et al (2011) Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev 25:755–766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Torcia S, Xie F et al (2013) Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nat Cell Biol 15:1415–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho WK, Stern S, Biggers JD (1974) Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool 187:383–386

    Article  CAS  PubMed  Google Scholar 

  • Choi Y, Ballow DJ, Xin Y, Rajkovic A (2008a) Lim homeobox gene, lhx8, is essential for mouse oocyte differentiation and survival. Biol Reprod 79:442–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi Y, Yuan D, Rajkovic A (2008b) Germ cell-specific transcriptional regulator sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. Biol Reprod 79:1176–1182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christians E, Boiani M, Garagna S et al (1999) Gene expression and chromatin organization during mouse oocyte growth. Dev Biol 207:76–85

    Article  CAS  PubMed  Google Scholar 

  • Clark BJ, Wells J, King SR, Stocco DM (1994) The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). J Biol Chem 269:28314–28322

    CAS  PubMed  Google Scholar 

  • Clarke HJ (2012) Post-transcriptional control of gene expression during mouse oogenesis. Results Probl Cell Differ 55:1–21

    Article  CAS  PubMed  Google Scholar 

  • Collado-Fernandez E, Picton HM, Dumollard R (2012) Metabolism throughout follicle and oocyte development in mammals. Int J Dev Biol 56:799–808

    Article  CAS  PubMed  Google Scholar 

  • Colonna R, Mangia F (1983) Mechanisms of amino acid uptake in cumulus-enclosed mouse oocytes. Biol Reprod 28:797–803

    Article  CAS  PubMed  Google Scholar 

  • Comiskey M, Warner CM (2007) Spatio-temporal localization of membrane lipid rafts in mouse oocytes and cleaving preimplantation embryos. Dev Biol 303:727–739

    Article  CAS  PubMed  Google Scholar 

  • Conley AJ, Howard HJ, Slanger WD, Ford JJ (1994) Steroidogenesis in the preovulatory porcine follicle. Biol Reprod 51:655–661

    Article  CAS  PubMed  Google Scholar 

  • Conti M, Hsieh M, Zamah AM, Oh JS (2012) Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol Cell Endocrinol 356:65–73

    Article  CAS  PubMed  Google Scholar 

  • Corbett HE, Dube CD, Slow S et al (2014) Uptake of betaine into mouse cumulus-oocyte complexes via the SLC7A6 isoform of y+L transporter. Biol Reprod 90:81

    Article  PubMed  CAS  Google Scholar 

  • Coskun S, Uzumcu M, Lin YC et al (1995) Regulation of cumulus cell steroidogenesis by the porcine oocyte and preliminary characterization of oocyte-produced factor(s). Biol Reprod 53:670–675

    Article  CAS  PubMed  Google Scholar 

  • Couse JF, Yates MM, Deroo BJ, Korach KS (2005) Estrogen receptor-beta is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 146:3247–3262

    Article  CAS  PubMed  Google Scholar 

  • Dalton CM, Carroll J (2013) Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J Cell Sci 126:2955–2964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Da Silva-Buttkus P, Jayasooriya GS, Mora JM et al (2008) Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci 121:3890–3900

    Article  PubMed  CAS  Google Scholar 

  • Davis BJ, Lennard DE, Lee CA et al (1999) Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta. Endocrinology 140:2685–2695

    CAS  PubMed  Google Scholar 

  • De La Fuente R (2006) Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol 292:1–12

    Article  CAS  Google Scholar 

  • De La Fuente R, O’Brien MJ, Eppig JJ (1999) Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum Reprod 14:3060–3068

    Article  Google Scholar 

  • De Smedt V, Szollosi D (1991) Cytochalasin D treatment induces meiotic resumption in follicular sheep oocytes. Mol Reprod Dev 29:163–171

    Article  PubMed  Google Scholar 

  • Dekel N, Beers WH (1978) Rat oocyte maturation in vitro: relief of cyclic AMP inhibition by gonadotropins. Proc Natl Acad Sci U S A 75:4369–4373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dekel N, Beers WH (1980) Development of the rat oocyte in vitro: inhibition and induction of maturation in the presence or absence of the cumulus oophorus. Dev Biol 75:247–254

    Article  CAS  PubMed  Google Scholar 

  • Dekel N, Hillensjo T, Kraicer PF (1979) Maturational effects of gonadotropins on the cumulus-oocyte complex of the rat. Biol Reprod 20:191–197

    Article  CAS  PubMed  Google Scholar 

  • Devoto L, Christenson LK, McAllister JM et al (1999) Insulin and insulin-like growth factor-I and -II modulate human granulosa-lutein cell steroidogenesis: enhancement of steroidogenic acute regulatory protein (StAR) expression. Mol Hum Reprod 5:1003–1010

    Article  CAS  PubMed  Google Scholar 

  • Diaz FJ, O’Brien MJ, Wigglesworth K, Eppig JJ (2006) The preantral granulosa cell to cumulus cell transition in the mouse ovary: development of competence to undergo expansion. Dev Biol 299:91–104

    Article  CAS  PubMed  Google Scholar 

  • Diaz FJ, Wigglesworth K, Eppig JJ (2007) Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 120:1330–1340

    Article  CAS  PubMed  Google Scholar 

  • Dissen GA, Romero C, Hirshfield AN, Ojeda SR (2001) Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 142:2078–2086

    CAS  PubMed  Google Scholar 

  • Dong J, Albertini DF, Nishimori K et al (1996) Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383:531–535

    Article  CAS  PubMed  Google Scholar 

  • Dorrington JH, Moon YS, Armstrong DT (1975) Estradiol-17beta biosynthesis in cultured granulosa cells from hypophysectomized immature rats; stimulation by follicle-stimulating hormone. Endocrinology 97:1328–1331

    Article  CAS  PubMed  Google Scholar 

  • Downs SM, Chen J (2008) EGF-like peptides mediate FSH-induced maturation of cumulus cell-enclosed mouse oocytes. Mol Reprod Dev 75:105–114

    Article  PubMed  CAS  Google Scholar 

  • Dragovic RA, Ritter LJ, Schulz SJ et al (2005) Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology 146:2798–2806

    Article  CAS  PubMed  Google Scholar 

  • Dragovic RA, Ritter LJ, Schulz SJ et al (2007) Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod 76:848–857

    Article  CAS  PubMed  Google Scholar 

  • Dupont S, Krust A, Gansmuller A et al (2000) Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127:4277–4291

    CAS  PubMed  Google Scholar 

  • Egbert JR, Shuhaibar LC, Edmund AB et al (2014) Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes. Development 141:3594–3604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eggan K, Jurga S, Gosden R et al (2006) Ovulated oocytes in adult mice derive from non-circulating germ cells. Nature 441:1109–1114

    Article  CAS  PubMed  Google Scholar 

  • Eisenbach M (1999) Mammalian sperm chemotaxis and its association with capacitation. Dev Genet 25:87–94

    Article  CAS  PubMed  Google Scholar 

  • el-Fouly MA, Cook B, Nekola M, Nalbandov AV (1970) Role of the ovum in follicular luteinization. Endocrinology 87:286–293

    Article  CAS  PubMed  Google Scholar 

  • Emmen JM, Couse JF, Elmore SA et al (2005) In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER){alpha} and ER{beta} null mice indicate a role for ER{beta} in follicular maturation. Endocrinology 146:2817–2826

    Article  CAS  PubMed  Google Scholar 

  • Emori C, Sugiura K (2014) Role of oocyte-derived paracrine factors in follicular development. Anim Sci J 85:627–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emori C, Wigglesworth K, Fujii W et al (2013) Cooperative effects of 17beta-estradiol and oocyte-derived paracrine factors on the transcriptome of mouse cumulus cells. Endocrinology 154:4859–4872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ene AC, Park S, Edelmann W, Taketo T (2013) Caspase 9 is constitutively activated in mouse oocytes and plays a key role in oocyte elimination during meiotic prophase progression. Dev Biol 377:213–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eppig JJ (1976) Analysis of mouse oogenesis in vitro. Oocyte isolation and the utilization of exogenous energy sources by growing oocytes. J Exp Zool 198:375–382

    Article  CAS  PubMed  Google Scholar 

  • Eppig JJ (1979) Gonadotropin stimulation of the expansion of cumulus oophori isolated from mice: general conditions for expansion in vitro. J Exp Zool 208:111–120

    Article  CAS  PubMed  Google Scholar 

  • Eppig JJ (1980) Regulation of cumulus oophorus expansion by gonadotropins in vivo and in vitro. Biol Reprod 23:545–552

    Article  CAS  PubMed  Google Scholar 

  • Eppig JJ (1981) Prostaglandin E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice. Biol Reprod 25:191–195

    Article  CAS  PubMed  Google Scholar 

  • Eppig JJ, Schroeder AC (1989) Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod 41:268–276

    Article  CAS  PubMed  Google Scholar 

  • Eppig JJ, Wigglesworth K, Pendola F, Hirao Y (1997) Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol Reprod 56:976–984

    Article  CAS  PubMed  Google Scholar 

  • Eppig JJ, Pendola FL, Wigglesworth K, Pendola JK (2005) Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol Reprod 73:351–357

    Article  CAS  PubMed  Google Scholar 

  • Erickson GF, Wang C, Hsueh AJ (1979) FSH induction of functional LH receptors in granulosa cells cultured in a chemically defined medium. Nature 279:336–338

    Article  CAS  PubMed  Google Scholar 

  • Espey LL (1980) Ovulation as an inflammatory reaction—a hypothesis. Biol Reprod 22:73–106

    Article  CAS  PubMed  Google Scholar 

  • Fagbohun CF, Downs SM (1992) Requirement for glucose in ligand-stimulated meiotic maturation of cumulus cell-enclosed mouse oocytes. J Reprod Fertil 96:681–697

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick SL, Richards JS (1991) Regulation of cytochrome P450 aromatase messenger ribonucleic acid and activity by steroids and gonadotropins in rat granulosa cells. Endocrinology 129:1452–1462

    Article  CAS  PubMed  Google Scholar 

  • Fortune JE, Armstrong DT (1977) Androgen production by theca and granulosa isolated from proestrous rat follicles. Endocrinology 100:1341–1347

    Article  CAS  PubMed  Google Scholar 

  • Franciosi F, Coticchio G, Lodde V et al (2014) Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol Reprod 91:61

    Article  PubMed  CAS  Google Scholar 

  • Fuhrer F, Mayr B, Schellander K et al (1989) Maturation competence and chromatin behaviour in growing and fully grown cattle oocytes. Zentralbl Veterinarmed A 36:285–291

    Article  CAS  PubMed  Google Scholar 

  • Fulop C, Kamath RV, Li Y et al (1997a) Coding sequence, exon-intron structure and chromosomal localization of murine TNF-stimulated gene 6 that is specifically expressed by expanding cumulus cell-oocyte complexes. Gene 202:95–102

    Article  CAS  PubMed  Google Scholar 

  • Fulop C, Salustri A, Hascall VC (1997b) Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus-oocyte complex. Arch Biochem Biophys 337:261–266

    Article  CAS  PubMed  Google Scholar 

  • Fulop C, Szanto S, Mukhopadhyay D et al (2003) Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 130:2253–2261

    Article  CAS  PubMed  Google Scholar 

  • Galloway SM, McNatty KP, Cambridge LM et al (2000) Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 25:279–283

    Article  CAS  PubMed  Google Scholar 

  • Gilchrist RB, Lane M, Thompson JG (2008) Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 14:159–177

    Article  CAS  PubMed  Google Scholar 

  • Glister C, Tannetta DS, Groome NP, Knight PG (2001) Interactions between follicle-stimulating hormone and growth factors in modulating secretion of steroids and inhibin-related peptides by nonluteinized bovine granulosa cells. Biol Reprod 65:1020–1028

    Article  CAS  PubMed  Google Scholar 

  • Glister C, Groome NP, Knight PG (2003) Oocyte-mediated suppression of follicle-stimulating hormone- and insulin-like growth factor-induced secretion of steroids and inhibin-related proteins by bovine granulosa cells in vitro: possible role of transforming growth factor alpha. Biol Reprod 68:758–765

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Haghighat N, Van Winkle LJ (1990) Developmental change in follicular cell-enhanced amino acid uptake into mouse oocytes that depends on intact gap junctions and transport system Gly. J Exp Zool 253:71–82

    Article  CAS  PubMed  Google Scholar 

  • Han SJ, Chen R, Paronetto MP, Conti M (2005) Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr Biol 15:1670–1676

    Article  CAS  PubMed  Google Scholar 

  • Harris SE, Adriaens I, Leese HJ, Gosden RG, Picton HM (2007) Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro. Reproduction 134:415–424

    Article  CAS  PubMed  Google Scholar 

  • Harris SE, Leese HJ, Gosden RG, Picton HM (2009) Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Mol Reprod Dev 76:231–238

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa A, Mochida N, Ogasawara T, Koyama K (2006) Pup birth from mouse oocytes in preantral follicles derived from vitrified and warmed ovaries followed by in vitro growth, in vitro maturation, and in vitro fertilization. Fertil Steril 86:1182–1192

    Article  PubMed  Google Scholar 

  • Hertig AT, Adams EC (1967) Studies on the human oocyte and its follicle. I. Ultrastructural and histochemical observations on the primordial follicle stage. J Cell Biol 34:647–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hess KA, Chen L, Larsen WJ (1998) The ovarian blood follicle barrier is both charge- and size-selective in mice. Biol Reprod 58:705–711

    Article  CAS  PubMed  Google Scholar 

  • Hickey GJ, Chen SA, Besman MJ et al (1988) Hormonal regulation, tissue distribution, and content of aromatase cytochrome P450 messenger ribonucleic acid and enzyme in rat ovarian follicles and corpora lutea: relationship to estradiol biosynthesis. Endocrinology 122:1426–1436

    Article  CAS  PubMed  Google Scholar 

  • Hinrichs K, Schmidt AL, Friedman PP et al (1993) In vitro maturation of horse oocytes: characterization of chromatin configuration using fluorescence microscopy. Biol Reprod 48:363–370

    Article  CAS  PubMed  Google Scholar 

  • Hirshfield AN (1991) Development of follicles in the mammalian ovary. Int Rev Cytol 124:43–101

    Article  CAS  PubMed  Google Scholar 

  • Hosaka T, Biggs WH 3rd, Tieu D et al (2004) Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci U S A 101:2975–2980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh M, Lee D, Panigone S et al (2007) Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 27:1914–1924

    Article  CAS  PubMed  Google Scholar 

  • Hsieh M, Thao K, Conti M (2011) Genetic dissection of epidermal growth factor receptor signaling during luteinizing hormone-induced oocyte maturation. PLoS One 6:e21574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu CJ, Hammond JM (1987) Gonadotropins and estradiol stimulate immunoreactive insulin-like growth factor-I production by porcine granulosa cells in vitro. Endocrinology 120:198–207

    Article  CAS  PubMed  Google Scholar 

  • Hutt KJ (2015) The role of BH3-only proteins in apoptosis within the ovary. Reproduction 149:R81–R89

    Article  CAS  PubMed  Google Scholar 

  • Ievoli E, Lindstedt R, Inforzato A et al (2011) Implication of the oligomeric state of the N-terminal PTX3 domain in cumulus matrix assembly. Matrix Biol 30:330–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igarashi H, Takahashi T, Takahashi E et al (2005) Aged mouse oocytes fail to readjust intracellular adenosine triphosphates at fertilization. Biol Reprod 72:1256–1261

    Article  CAS  PubMed  Google Scholar 

  • Jensen JT, Schwinof KM, Zelinski-Wooten MB et al (2002) Phosphodiesterase 3 inhibitors selectively block the spontaneous resumption of meiosis by macaque oocytes in vitro. Hum Reprod 17:2079–2084

    Article  CAS  PubMed  Google Scholar 

  • John GB, Gallardo TD, Shirley LJ, Castrillon DH (2008) Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 321:197–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • John GB, Shidler MJ, Besmer P, Castrillon DH (2009) Kit signaling via PI3K promotes ovarian follicle maturation but is dispensable for primordial follicle activation. Dev Biol 331:292–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jorgensen JS (2013) Defining the neighborhoods that escort the oocyte through its early life events and into a functional follicle. Mol Reprod Dev 80:960–976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joyce IM, Pendola FL, O’Brien M, Eppig JJ (2001) Regulation of prostaglandin-endoperoxide synthase 2 messenger ribonucleic acid expression in mouse granulosa cells during ovulation. Endocrinology 142:3187–3197

    CAS  PubMed  Google Scholar 

  • Kang MK, Han SJ (2011) Post-transcriptional and post-translational regulation during mouse oocyte maturation. BMB Rep 44:147–157

    Article  CAS  PubMed  Google Scholar 

  • Kawamura K, Cheng Y, Kawamura N et al (2011) Pre-ovulatory LH/hCG surge decreases C-type natriuretic peptide secretion by ovarian granulosa cells to promote meiotic resumption of pre-ovulatory oocytes. Hum Reprod 26:3094–3101

    Article  CAS  PubMed  Google Scholar 

  • Kessel RG, Tung HN, Roberts R, Beams HW (1985) The presence and distribution of gap junctions in the oocyte-follicle cell complex of the zebrafish, Brachydanio rerio. J Submicrosc Cytol 17:239–253

    CAS  PubMed  Google Scholar 

  • Kezele P, Nilsson EE, Skinner MK (2005) Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biol Reprod 73:967–973

    Article  CAS  PubMed  Google Scholar 

  • Khalid M, Haresign W, Luck MR (2000) Secretion of IGF-1 by ovine granulosa cells: effects of growth hormone and follicle stimulating hormone. Anim Reprod Sci 58:261–272

    Article  CAS  PubMed  Google Scholar 

  • Kidder GM, Mhawi AA (2002) Gap junctions and ovarian folliculogenesis. Reproduction 123:613–620

    Article  CAS  PubMed  Google Scholar 

  • Kissel H, Timokhina I, Hardy MP et al (2000) Point mutation in kit receptor tyrosine kinase reveals essential roles for kit signaling in spermatogenesis and oogenesis without affecting other kit responses. EMBO J 19:1312–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krege JH, Hodgin JB, Couse JF et al (1998) Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A 95:15677–15682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaVoie HA, DeSimone DC, Gillio-Meina C, Hui YY (2002) Cloning and characterization of porcine ovarian estrogen receptor beta isoforms. Biol Reprod 66:616–623

    Article  CAS  PubMed  Google Scholar 

  • Lee WS, Otsuka F, Moore RK, Shimasaki S (2001) Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol Reprod 65:994–999

    Article  CAS  PubMed  Google Scholar 

  • Lee KB, Zhang M, Sugiura K et al (2013) Hormonal coordination of natriuretic peptide type C and natriuretic peptide receptor 3 expression in mouse granulosa cells. Biol Reprod 88:42

    Article  PubMed  CAS  Google Scholar 

  • Lei L, Spradling AC (2013) Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles. Proc Natl Acad Sci U S A 110:8585–8590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei ZM, Mishra S, Zou W et al (2001) Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene. Mol Endocrinol 15:184–200

    Article  CAS  PubMed  Google Scholar 

  • Lew DJ, Kornbluth S (1996) Regulatory roles of cyclin dependent kinase phosphorylation in cell cycle control. Curr Opin Cell Biol 8:795–804

    Article  CAS  PubMed  Google Scholar 

  • Li R, Norman RJ, Armstrong DT, Gilchrist RB (2000) Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol Reprod 63:839–845

    Article  CAS  PubMed  Google Scholar 

  • Li J, Kawamura K, Cheng Y et al (2010) Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci U S A 107:10280–10284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lincoln AJ, Wickramasinghe D, Stein P et al (2002) Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat Genet 30:446–449

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Sims D, Calarco P, Talbot P (2003) Biochemical heterogeneity, migration, and pre-fertilization release of mouse oocyte cortical granules. Reprod Biol Endocrinol 1:77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu K, Rajareddy S, Liu L, Jagarlamudi K et al (2006) Control of mammalian oocyte growth and early follicular development by the oocyte PI3 kinase pathway: new roles for an old timer. Dev Biol 299:1–11

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Xie F, Zamah AM et al (2014) Multiple pathways mediate luteinizing hormone regulation of cGMP signaling in the mouse ovarian follicle. Biol Reprod 91:9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu C, Peng J, Matzuk MM, Yao HH (2015) Lineage specification of ovarian theca cells requires multicellular interactions via oocyte and granulosa cells. Nat Commun 6:6934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lodde V, Modina S, Maddox-Hyttel P et al (2008) Oocyte morphology and transcriptional silencing in relation to chromatin remodeling during the final phases of bovine oocyte growth. Mol Reprod Dev 75:915–924

    Article  CAS  PubMed  Google Scholar 

  • Luciano AM, Franciosi F, Modina SC, Lodde V (2011) Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol Reprod 85:1252–1259

    Article  CAS  PubMed  Google Scholar 

  • Lund SA, Murdoch J, Van Kirk EA, Murdoch WJ (1999) Mitogenic and antioxidant mechanisms of estradiol action in preovulatory ovine follicles: relevance to luteal function. Biol Reprod 61:388–392

    Article  CAS  PubMed  Google Scholar 

  • Macaulay AD, Gilbert I, Caballero J et al (2014) The gametic synapse: RNA transfer to the bovine oocyte. Biol Reprod 91:90

    Article  PubMed  CAS  Google Scholar 

  • Malki S, van der Heijden GW, O’Donnell KA et al (2014) A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev Cell 29:521–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manova K, Huang EJ, Angeles M et al (1993) The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia. Dev Biol 157:85–99

    Article  CAS  PubMed  Google Scholar 

  • Mattson BA, Albertini DF (1990) Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol Reprod Dev 25:374–383

    Article  CAS  PubMed  Google Scholar 

  • Mazerbourg S, Klein C, Roh J et al (2004) Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Mol Endocrinol 18:653–665

    Article  CAS  PubMed  Google Scholar 

  • McArthur ME, Irving-Rodgers HF, Byers S, Rodgers RJ (2000) Identification and immunolocalization of decorin, versican, perlecan, nidogen, and chondroitin sulfate proteoglycans in bovine small-antral ovarian follicles. Biol Reprod 63:913–924

    Article  CAS  PubMed  Google Scholar 

  • McGee EA, Sawetawan C, Bird I et al (1996) The effect of insulin and insulin-like growth factors on the expression of steroidogenic enzymes in a human ovarian thecal-like tumor cell model. Fertil Steril 65:87–93

    Article  CAS  PubMed  Google Scholar 

  • Mehlmann LM, Terasaki M, Jaffe LA, Kline D (1995) Reorganization of the endoplasmic reticulum during meiotic maturation of the mouse oocyte. Dev Biol 170:607–615

    Article  CAS  PubMed  Google Scholar 

  • Mehlmann LM, Jones TL, Jaffe LA (2002) Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science 297:1343–1345

    Article  CAS  PubMed  Google Scholar 

  • Mehlmann LM, Saeki Y, Tanaka S et al (2004) The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306:1947–1950

    Article  CAS  PubMed  Google Scholar 

  • Meinecke B, Meinecke-Tillmann S (1979) Effects of gonadotropins on oocyte maturation and progesterone production by porcine ovarian follicles cultured in vitro. Theriogenology 11:351–365

    Article  CAS  PubMed  Google Scholar 

  • Miller WL (1988) Molecular biology of steroid hormone synthesis. Endocr Rev 9:295–318

    Article  CAS  PubMed  Google Scholar 

  • Monniaux D, Pisselet C (1992) Control of proliferation and differentiation of ovine granulosa cells by insulin-like growth factor-I and follicle-stimulating hormone in vitro. Biol Reprod 46:109–119

    Article  CAS  PubMed  Google Scholar 

  • Moore RK, Otsuka F, Shimasaki S (2003) Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem 278:304–310

    Article  CAS  PubMed  Google Scholar 

  • Nagyova E, Prochazka R, Vanderhyden BC (1999) Oocytectomy does not influence synthesis of hyaluronic acid by pig cumulus cells: retention of hyaluronic acid after insulin-like growth factor-I treatment in serum-free medium. Biol Reprod 61:569–574

    Article  CAS  PubMed  Google Scholar 

  • Nakamura T, Iwase A, Bayasula B et al (2015) CYP51A1 induced by growth differentiation factor 9 and follicle-stimulating hormone in granulosa cells is a possible predictor for unfertilization. Reprod Sci 22:377–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neal P, Baker TG (1975) Response of mouse graafian follicles in organ culture to varying doses of follicle-stimulating hormone and luteinizing hormone. J Endocrinol 65:27–32

    Article  CAS  PubMed  Google Scholar 

  • Nekola MV, Nalbandov AV (1971) Morphological changes of rat follicular cells as influenced by oocytes. Biol Reprod 4:154–160

    CAS  PubMed  Google Scholar 

  • Nicosia SV, Wolf DP, Inoue M (1977) Cortical granule distribution and cell surface characteristics in mouse eggs. Dev Biol 57:56–74

    Article  CAS  PubMed  Google Scholar 

  • Nilsson E, Skinner MK (2001) Cellular interactions that control primordial follicle development and folliculogenesis. J Soc Gynecol Investig 8:S17–S20

    Article  CAS  PubMed  Google Scholar 

  • Nilsson EE, Detzel C, Skinner MK (2006) Platelet-derived growth factor modulates the primordial to primary follicle transition. Reproduction 131:1007–1015

    Article  CAS  PubMed  Google Scholar 

  • Norris RP, Ratzan WJ, Freudzon M et al (2009) Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136:1869–1878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norris RP, Freudzon M, Nikolaev VO, Jaffe LA (2010) Epidermal growth factor receptor kinase activity is required for gap junction closure and for part of the decrease in ovarian follicle cGMP in response to LH. Reproduction 140:655–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oatley JM, Brinster RL (2012) The germline stem cell niche unit in mammalian testes. Physiol Rev 92:577–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ochsner SA, Day AJ, Rugg MS et al (2003a) Disrupted function of tumor necrosis factor-alpha-stimulated gene 6 blocks cumulus cell-oocyte complex expansion. Endocrinology 144:4376–4384

    Article  CAS  PubMed  Google Scholar 

  • Ochsner SA, Russell DL, Day AJ et al (2003b) Decreased expression of tumor necrosis factor-alpha-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice. Endocrinology 144:1008–1019

    Article  CAS  PubMed  Google Scholar 

  • Oh JS, Han SJ, Conti M (2010) Wee1B, Myt1, and Cdc25 function in distinct compartments of the mouse oocyte to control meiotic resumption. J Cell Biol 188:199–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsiewski PJ, Beers WH (1983) cAMP synthesis in the rat oocyte. Dev Biol 100:287–293

    Article  CAS  PubMed  Google Scholar 

  • Packer AI, Hsu YC, Besmer P, Bachvarova RF (1994) The ligand of the c-kit receptor promotes oocyte growth. Dev Biol 161:194–205

    Article  PubMed  Google Scholar 

  • Pangas SA, Choi Y, Ballow DJ et al (2006) Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. Proc Natl Acad Sci U S A 103:8090–8095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parfenov V, Potchukalina G, Dudina L et al (1989) Human antral follicles: oocyte nucleus and the karyosphere formation (electron microscopic and autoradiographic data). Gamete Res 22:219–231

    Article  CAS  PubMed  Google Scholar 

  • Park JY, Su YQ, Ariga M et al (2004) EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682–684

    Article  CAS  PubMed  Google Scholar 

  • Parker KL, Schimmer BP (1995) Transcriptional regulation of the genes encoding the cytochrome P-450 steroid hydroxylases. Vitam Horm 51:339–370

    Article  CAS  PubMed  Google Scholar 

  • Parrott JA, Skinner MK (1999) Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140:4262–4271

    CAS  PubMed  Google Scholar 

  • Payne C, Schatten G (2003) Golgi dynamics during meiosis are distinct from mitosis and are coupled to endoplasmic reticulum dynamics until fertilization. Dev Biol 264:50–63

    Article  CAS  PubMed  Google Scholar 

  • Paynton BV, Bachvarova R (1994) Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. Mol Reprod Dev 37:172–180

    Article  CAS  PubMed  Google Scholar 

  • Pelland AM, Corbett HE, Baltz JM (2009) Amino Acid transport mechanisms in mouse oocytes during growth and meiotic maturation. Biol Reprod 81:1041–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pepling ME (2012) Follicular assembly: mechanisms of action. Reproduction 143:139–149

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pescador N, Houde A, Stocco DM, Murphy BD (1997) Follicle-stimulating hormone and intracellular second messengers regulate steroidogenic acute regulatory protein messenger ribonucleic acid in luteinized porcine granulosa cells. Biol Reprod 57:660–668

    Article  CAS  PubMed  Google Scholar 

  • Pesce M, Di Carlo A, De Felici M (1997) The c-kit receptor is involved in the adhesion of mouse primordial germ cells to somatic cells in culture. Mech Dev 68:37–44

    Article  CAS  PubMed  Google Scholar 

  • Peter M, Dubuis JM (2000) Transcription factors as regulators of steroidogenic P-450 enzymes. Eur J Clin Invest 30(Suppl 3):14–20

    Article  CAS  PubMed  Google Scholar 

  • Piquette GN, LaPolt PS, Oikawa M, Hsueh AJ (1991) Regulation of luteinizing hormone receptor messenger ribonucleic acid levels by gonadotropins, growth factors, and gonadotropin-releasing hormone in cultured rat granulosa cells. Endocrinology 128:2449–2456

    Article  CAS  PubMed  Google Scholar 

  • Pirino G, Wescott MP, Donovan PJ (2009) Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle 8:665–670

    Article  CAS  PubMed  Google Scholar 

  • Pratt HP (1982) Preimplantation mouse embryos synthesize membrane sterols. Dev Biol 89:101–110

    Article  CAS  PubMed  Google Scholar 

  • Prochazka R, Nagyova E, Rimkevicova Z et al (1991) Lack of effect of oocytectomy on expansion of the porcine cumulus. J Reprod Fertil 93:569–576

    Article  CAS  PubMed  Google Scholar 

  • Prochazka R, Nagyova E, Brem G et al (1998) Secretion of cumulus expansion-enabling factor (CEEF) in porcine follicles. Mol Reprod Dev 49:141–149

    Article  CAS  PubMed  Google Scholar 

  • Quirk SM, Cowan RG, Harman RM (2006) The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle. J Endocrinol 189:441–453

    Article  CAS  PubMed  Google Scholar 

  • Rajah R, Glaser EM, Hirshfield AN (1992) The changing architecture of the neonatal rat ovary during histogenesis. Dev Dyn 194:177–192

    Article  CAS  PubMed  Google Scholar 

  • Ralph JH, Telfer EE, Wilmut I (1995) Bovine cumulus cell expansion does not depend on the presence of an oocyte secreted factor. Mol Reprod Dev 42:248–253

    Article  CAS  PubMed  Google Scholar 

  • Reddy P, Shen L, Ren C et al (2005) Activation of Akt (PKB) and suppression of FKHRL1 in mouse and rat oocytes by stem cell factor during follicular activation and development. Dev Biol 281:160–170

    Article  CAS  PubMed  Google Scholar 

  • Reddy P, Liu L, Adhikari D et al (2008) Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319:611–613

    Article  CAS  PubMed  Google Scholar 

  • Ren Y, Suzuki H, Jagarlamudi K et al (2015) Lhx8 regulates primordial follicle activation and postnatal folliculogenesis. BMC Biol 13:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Richani D, Wang X, Zeng HT et al (2014) Pre-maturation with cAMP modulators in conjunction with EGF-like peptides during in vitro maturation enhances mouse oocyte developmental competence. Mol Reprod Dev 81:422–435

    Article  CAS  PubMed  Google Scholar 

  • Richard S, Baltz JM (2014) Prophase I arrest of mouse oocytes mediated by natriuretic peptide precursor C requires GJA1 (connexin-43) and GJA4 (connexin-37) gap junctions in the antral follicle and cumulus-oocyte complex. Biol Reprod 90:137

    Article  PubMed  CAS  Google Scholar 

  • Richard FJ, Tsafriri A, Conti M (2001) Role of phosphodiesterase type 3A in rat oocyte maturation. Biol Reprod 65:1444–1451

    Article  CAS  PubMed  Google Scholar 

  • Richards JS (1980) Maturation of ovarian follicles: actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol Rev 60:51–89

    CAS  PubMed  Google Scholar 

  • Richards JS (1994) Hormonal control of gene expression in the ovary. Endocr Rev 15:725–751

    Article  CAS  PubMed  Google Scholar 

  • Richards JS, Jahnsen T, Hedin L et al (1987) Ovarian follicular development: from physiology to molecular biology. Recent Prog Horm Res 43:231–276

    CAS  PubMed  Google Scholar 

  • Richards JS, Russell DL, Ochsner S et al (2002) Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog Horm Res 57:195–220

    Article  CAS  PubMed  Google Scholar 

  • Robinson JW, Zhang M, Shuhaibar LC et al (2012) Luteinizing hormone reduces the activity of the NPR2 guanylyl cyclase in mouse ovarian follicles, contributing to the cyclic GMP decrease that promotes resumption of meiosis in oocytes. Dev Biol 366:308–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robker RL, Richards JS (1998) Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Mol Endocrinol 12:924–940

    Article  CAS  PubMed  Google Scholar 

  • Rosenfeld CS, Wagner JS, Roberts RM, Lubahn DB (2001) Intraovarian actions of oestrogen. Reproduction 122:215–226

    Article  CAS  PubMed  Google Scholar 

  • Salustri A, Ulisse S, Yanagishita M, Hascall VC (1990) Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-beta. J Biol Chem 265:19517–19523

    CAS  PubMed  Google Scholar 

  • Salustri A, Camaioni A, Di Giacomo M et al (1999) Hyaluronan and proteoglycans in ovarian follicles. Hum Reprod Update 5:293–301

    Article  CAS  PubMed  Google Scholar 

  • Salustri A, Garlanda C, Hirsch E et al (2004) PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 131:1577–1586

    Article  CAS  PubMed  Google Scholar 

  • Sanggaard KW, Sonne-Schmidt CS, Krogager TP et al (2008) The transfer of heavy chains from bikunin proteins to hyaluronan requires both TSG-6 and HC2. J Biol Chem 283:18530–18537

    Article  CAS  PubMed  Google Scholar 

  • Sasseville M, Ritter LJ, Nguyen TM et al (2010) Growth differentiation factor 9 signaling requires ERK1/2 activity in mouse granulosa and cumulus cells. J Cell Sci 123:3166–3176

    Article  CAS  PubMed  Google Scholar 

  • Sato H, Kajikawa S, Kuroda S et al (2001) Impaired fertility in female mice lacking urinary trypsin inhibitor. Biochem Biophys Res Commun 281:1154–1160

    Article  CAS  PubMed  Google Scholar 

  • Sato N, Kawamura K, Fukuda J et al (2003) Expression of LDL receptor and uptake of LDL in mouse preimplantation embryos. Mol Cell Endocrinol 202:191–194

    Article  CAS  PubMed  Google Scholar 

  • Scarchilli L, Camaioni A, Bottazzi B et al (2007) PTX3 interacts with inter-alpha-trypsin inhibitor: implications for hyaluronan organization and cumulus oophorus expansion. J Biol Chem 282:30161–30170

    Article  CAS  PubMed  Google Scholar 

  • Schindler R, Nilsson E, Skinner MK (2010) Induction of ovarian primordial follicle assembly by connective tissue growth factor CTGF. PLoS One 5:e12979

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmidt D, Ovitt CE, Anlag K et al (2004) The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131:933–942

    Article  CAS  PubMed  Google Scholar 

  • Schoppee PD, Garmey JC, Veldhuis JD (2002) Putative activation of the peroxisome proliferator-activated receptor gamma impairs androgen and enhances progesterone biosynthesis in primary cultures of porcine theca cells. Biol Reprod 66:190–198

    Article  CAS  PubMed  Google Scholar 

  • Schroeder TE (1981) Microfilament-mediated surface change in starfish oocytes in response to 1-methyladenine: implications for identifying the pathway and receptor sites for maturation-inducing hormones. J Cell Biol 90:362–371

    Article  CAS  PubMed  Google Scholar 

  • Schultz RM, Letourneau GE, Wassarman PM (1979) Program of early development in the mammal: changes in patterns and absolute rates of tubulin and total protein synthesis during oogenesis and early embryogenesis in the mouse. Dev Biol 68:341–359

    Article  CAS  PubMed  Google Scholar 

  • Schultz RM, Montgomery RR, Belanoff JR (1983) Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol 97:264–273

    Article  CAS  PubMed  Google Scholar 

  • Segaloff DL, Wang HY, Richards JS (1990) Hormonal regulation of luteinizing hormone/chorionic gonadotropin receptor mRNA in rat ovarian cells during follicular development and luteinization. Mol Endocrinol 4:1856–1865

    Article  CAS  PubMed  Google Scholar 

  • Sekar N, Garmey JC, Veldhuis JD (2000) Mechanisms underlying the steroidogenic synergy of insulin and luteinizing hormone in porcine granulosa cells: joint amplification of pivotal sterol-regulatory genes encoding the low-density lipoprotein (LDL) receptor, steroidogenic acute regulatory (stAR) protein and cytochrome P450 side-chain cleavage (P450scc) enzyme. Mol Cell Endocrinol 159:25–35

    Article  CAS  PubMed  Google Scholar 

  • Shitsukawa K, Andersen CB, Richard FJ et al (2001) Cloning and characterization of the cyclic guanosine monophosphate-inhibited phosphodiesterase PDE3A expressed in mouse oocyte. Biol Reprod 65:188–196

    Article  CAS  PubMed  Google Scholar 

  • Shuhaibar LC, Egbert JR, Norris RP et al (2015) Intercellular signaling via cyclic GMP diffusion through gap junctions restarts meiosis in mouse ovarian follicles. Proc Natl Acad Sci U S A 112:5527–5532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva JM, Price CA (2002) Insulin and IGF-I are necessary for FSH-induced cytochrome P450 aromatase but not cytochrome P450 side-chain cleavage gene expression in oestrogenic bovine granulosa cells in vitro. J Endocrinol 174:499–507

    Article  CAS  PubMed  Google Scholar 

  • Simon AM, Goodenough DA, Li E, Paul DL (1997) Female infertility in mice lacking connexin 37. Nature 385:525–529

    Article  CAS  PubMed  Google Scholar 

  • Simone DA, Chorich LP, Mahesh VB (1993) Mechanisms of action for an androgen-mediated autoregulatory process in rat thecal-interstitial cells. Biol Reprod 49:1190–1201

    Article  CAS  PubMed  Google Scholar 

  • Simpson ER, Mahendroo MS, Means GD et al (1994) Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15:342–355

    CAS  PubMed  Google Scholar 

  • Sirois J, Simmons DL, Richards JS (1992) Hormonal regulation of messenger ribonucleic acid encoding a novel isoform of prostaglandin endoperoxide H synthase in rat preovulatory follicles. Induction in vivo and in vitro. J Biol Chem 267:11586–11592

    CAS  PubMed  Google Scholar 

  • Smyth CD, Gosden RG, McNeilly AS, Hillier SG (1994) Effect of inhibin immunoneutralization on steroidogenesis in rat ovarian follicles in vitro. J Endocrinol 140:437–443

    Article  CAS  PubMed  Google Scholar 

  • Sorensen RA, Wassarman PM (1976) Relationship between growth and meiotic maturation of the mouse oocyte. Dev Biol 50:531–536

    Article  CAS  PubMed  Google Scholar 

  • Spicer LJ, Chamberlain CS, Maciel SM (2002) Influence of gonadotropins on insulin- and insulin-like growth factor-I (IGF-I)-induced steroid production by bovine granulosa cells. Domest Anim Endocrinol 22:237–254

    Article  CAS  PubMed  Google Scholar 

  • Spicer LJ, Aad PY, Allen DT et al (2008) Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9. Biol Reprod 78:243–253

    Article  CAS  PubMed  Google Scholar 

  • Sretarugsa P, Wallace RA (1997) The developing Xenopus oocyte specifies the type of gonadotropin-stimulated steroidogenesis performed by its associated follicle cells. Dev Growth Differ 39:87–97

    Article  CAS  PubMed  Google Scholar 

  • Sternlicht AL, Schultz RM (1981) Biochemical studies of mammalian oogenesis: kinetics of accumulation of total and poly(A)-containing RNA during growth of the mouse oocyte. J Exp Zool 215:191–200

    Article  CAS  PubMed  Google Scholar 

  • Stocco DM (2001) Tracking the role of a star in the sky of the new millennium. Mol Endocrinol 15:1245–1254

    Article  CAS  PubMed  Google Scholar 

  • Su YQ, Denegre JM, Wigglesworth K et al (2003) Oocyte-dependent activation of mitogen-activated protein kinase (ERK1/2) in cumulus cells is required for the maturation of the mouse oocyte-cumulus cell complex. Dev Biol 263:126–138

    Article  CAS  PubMed  Google Scholar 

  • Su YQ, Sugiura K, Woo Y et al (2007) Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev Biol 302:104–117

    Article  CAS  PubMed  Google Scholar 

  • Su YQ, Sugiura K, Wigglesworth K et al (2008) Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135:111–121

    Article  CAS  PubMed  Google Scholar 

  • Su YQ, Sugiura K, Li Q et al (2010) Mouse oocytes enable LH-induced maturation of the cumulus-oocyte complex via promoting EGF receptor-dependent signaling. Mol Endocrinol 24:1230–1239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiura K, Pendola FL, Eppig JJ (2005) Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev Biol 279:20–30

    Article  CAS  PubMed  Google Scholar 

  • Sugiura K, Su YQ, Diaz FJ et al (2007) Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134:2593–2603

    Article  CAS  PubMed  Google Scholar 

  • Sugiura K, Su YQ, Eppig JJ (2009) Targeted suppression of Has2 mRNA in mouse cumulus cell-oocyte complexes by adenovirus-mediated short-hairpin RNA expression. Mol Reprod Dev 76:537–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki T, Sasano H, Takaya R et al (1998) Cyclic changes of vasculature and vascular phenotypes in normal human ovaries. Hum Reprod 13:953–959

    Article  CAS  PubMed  Google Scholar 

  • Thomas FH, Ismail RS, Jiang JY, Vanderhyden BC (2008) Kit ligand 2 promotes murine oocyte growth in vitro. Biol Reprod 78:167–175

    Article  CAS  PubMed  Google Scholar 

  • Tian XC, Berndtson AK, Fortune JE (1995) Differentiation of bovine preovulatory follicles during the follicular phase is associated with increases in messenger ribonucleic acid for cytochrome P450 side-chain cleavage, 3 beta-hydroxysteroid dehydrogenase, and P450 17 alpha-hydroxylase, but not P450 aromatase. Endocrinology 136:5102–5110

    CAS  PubMed  Google Scholar 

  • Toda K, Takeda K, Okada T et al (2001) Targeted disruption of the aromatase P450 gene (Cyp19) in mice and their ovarian and uterine responses to 17beta-oestradiol. J Endocrinol 170:99–111

    Article  CAS  PubMed  Google Scholar 

  • Trigatti B, Rayburn H, Vinals M et al (1999) Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc Natl Acad Sci U S A 96:9322–9327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsafriri A, Chun SY, Zhang R et al (1996) Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev Biol 178:393–402

    Article  CAS  PubMed  Google Scholar 

  • Tsutsumi O, Yano T, Satoh K et al (1990) Studies of hexokinase activity in human and mouse oocyte. Am J Obstet Gynecol 162:1301–1304

    Article  CAS  PubMed  Google Scholar 

  • Tsutsumi O, Satoh K, Taketani Y, Kato T (1992) Determination of enzyme activities of energy metabolism in the maturing rat oocyte. Mol Reprod Dev 33:333–337

    Article  CAS  PubMed  Google Scholar 

  • Uda M, Ottolenghi C, Crisponi L et al (2004) Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum Mol Genet 13:1171–1181

    Article  CAS  PubMed  Google Scholar 

  • Urner F, Herrmann WL, Baulieu EE, Schorderet-Slatkine S (1983) Inhibition of denuded mouse oocyte meiotic maturation by forskolin, an activator of adenylate cyclase. Endocrinology 113:1170–1172

    Article  CAS  PubMed  Google Scholar 

  • Van Blerkom J, Davis PW, Lee J (1995) ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod 10:415–424

    CAS  PubMed  Google Scholar 

  • Van Blerkom J, Davis P, Alexander S (2003) Inner mitochondrial membrane potential (DeltaPsim), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes. Hum Reprod 18:2429–2440

    Article  PubMed  CAS  Google Scholar 

  • Vanderhyden BC (1993) Species differences in the regulation of cumulus expansion by an oocyte-secreted factor(s). J Reprod Fertil 98:219–227

    Article  CAS  PubMed  Google Scholar 

  • Vanderhyden BC, Tonary AM (1995) Differential regulation of progesterone and estradiol production by mouse cumulus and mural granulosa cells by A factor(s) secreted by the oocyte. Biol Reprod 53:1243–1250

    Article  CAS  PubMed  Google Scholar 

  • Vanderhyden BC, Caron PJ, Buccione R, Eppig JJ (1990) Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev Biol 140:307–317

    Article  CAS  PubMed  Google Scholar 

  • Vanderhyden BC, Cohen JN, Morley P (1993) Mouse oocytes regulate granulosa cell steroidogenesis. Endocrinology 133:423–426

    CAS  PubMed  Google Scholar 

  • Vanderhyden BC, Macdonald EA, Nagyova E, Dhawan A (2003) Evaluation of members of the TGFbeta superfamily as candidates for the oocyte factors that control mouse cumulus expansion and steroidogenesis. Reprod Suppl 61:55–70

    CAS  PubMed  Google Scholar 

  • Van Soom A, Tanghe S, De Pauw I et al (2002) Function of the cumulus oophorus before and during mammalian fertilization. Reprod Domest Anim 37:144–151

    Article  PubMed  Google Scholar 

  • Varnosfaderani ShR, Ostadhosseini S, Hajian M et al (2013) Importance of the GDF9 signaling pathway on cumulus cell expansion and oocyte competency in sheep. Theriogenology 80:470–478

    Google Scholar 

  • Vitt UA, McGee EA, Hayashi M, Hsueh AJ (2000) In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 141:3814–3820

    CAS  PubMed  Google Scholar 

  • Vivarelli E, Conti M, De Felici M, Siracusa G (1983) Meiotic resumption and intracellular cAMP levels in mouse oocytes treated with compounds which act on cAMP metabolism. Cell Differ 12:271–276

    Article  CAS  PubMed  Google Scholar 

  • Wallace WH, Kelsey TW (2010) Human ovarian reserve from conception to the menopause. PLoS One 5:e8772

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Walters KA, Middleton LJ, Joseph SR et al (2012) Targeted loss of androgen receptor signaling in murine granulosa cells of preantral and antral follicles causes female subfertility. Biol Reprod 87:151

    Article  PubMed  CAS  Google Scholar 

  • Wang Q, Chi MM, Schedl T, Moley KH (2012) An intercellular pathway for glucose transport into mouse oocytes. Am J Physiol Endocrinol Metab 302:E1511–E1518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson LN, Mottershead DG, Dunning KR et al (2012) Heparan sulfate proteoglycans regulate responses to oocyte paracrine signals in ovarian follicle morphogenesis. Endocrinology 153:4544–4555

    Article  CAS  PubMed  Google Scholar 

  • Whitelaw PF, Smyth CD, Howles CM, Hillier SG (1992) Cell-specific expression of aromatase and LH receptor mRNAs in rat ovary. J Mol Endocrinol 9:309–312

    Article  CAS  PubMed  Google Scholar 

  • Wickramasinghe D, Ebert KM, Albertini DF (1991) Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. Dev Biol 143:162–172

    Article  CAS  PubMed  Google Scholar 

  • Wigglesworth K, Lee KB, O’Brien MJ et al (2013) Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. Proc Natl Acad Sci U S A 110:E3723–E3729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wigglesworth K, Lee KB, Emori C et al (2015) Transcriptomic diversification of developing cumulus and mural granulosa cells in mouse ovarian follicles. Biol Reprod 92:23

    Article  PubMed  Google Scholar 

  • Willis D, Mason H, Gilling-Smith C, Franks S (1996) Modulation by insulin of follicle-stimulating hormone and luteinizing hormone actions in human granulosa cells of normal and polycystic ovaries. J Clin Endocrinol Metab 81:302–309

    CAS  PubMed  Google Scholar 

  • Worrad DM, Ram PT, Schultz RM (1994) Regulation of gene expression in the mouse oocyte and early preimplantation embryo: developmental changes in Sp1 and TATA box-binding protein, TBP. Development 120:2347–2357

    CAS  PubMed  Google Scholar 

  • Yamamoto K, Otoi T, Koyama N et al (1999) Development to live young from bovine small oocytes after growth, maturation and fertilization in vitro. Theriogenology 52:81–89

    Article  CAS  PubMed  Google Scholar 

  • Yoshida H, Takakura N, Kataoka H et al (1997) Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev Biol 184:122–137

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y (1998) Insulin-like growth factors and ovarian physiology. J Obstet Gynaecol Res 24:305–323

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Tischkau SA, Bahr JM (1994) Destruction of the germinal disc region of an immature preovulatory follicle suppresses follicular maturation and ovulation. Biol Reprod 51:229–233

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka S, Ochsner S, Russell DL et al (2000) Expression of tumor necrosis factor-stimulated gene-6 in the rat ovary in response to an ovulatory dose of gonadotropin. Endocrinology 141:4114–4119

    CAS  PubMed  Google Scholar 

  • Zeleznik AJ, Midgley AR Jr, Reichert LE Jr (1974) Granulosa cell maturation in the rat: increased binding of human chorionic gonadotropin following treatment with follicle-stimulating hormone in vivo. Endocrinology 95:818–825

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Garmey JC, Veldhuis JD (2000) Interactive stimulation by luteinizing hormone and insulin of the steroidogenic acute regulatory (StAR) protein and 17alpha-hydroxylase/17,20-lyase (CYP17) genes in porcine theca cells. Endocrinology 141:2735–2742

    CAS  PubMed  Google Scholar 

  • Zhang X, Wu XQ, Lu S et al (2006) Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res 16:841–850

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang Z, Xu XY et al (2008) Protein kinase A modulates Cdc25B activity during meiotic resumption of mouse oocytes. Dev Dyn 237:3777–3786

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ (2010) Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330:366–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Su YQ, Sugiura K et al (2011) Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology 152:4377–4385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Liu L, Li X et al (2014a) Life-long in vivo cell-lineage tracing shows that no oogenesis originates from putative germline stem cells in adult mice. Proc Natl Acad Sci U S A 111:17983–17988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Risal S, Gorre N et al (2014b) Somatic cells initiate primordial follicle activation and govern the development of dormant oocytes in mice. Curr Biol 24:2501–2508

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Panula S, Petropoulos S et al (2015) Adult human and mouse ovaries lack DDX4-expressing functional oogonial stem cells. Nat Med 21:1116–1118

    Article  CAS  PubMed  Google Scholar 

  • Zuccotti M, Ponce RH, Boiani M et al (2002) The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote 10:73–78

    Article  PubMed  Google Scholar 

  • Zuelke KA, Brackett BG (1992) Effects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro. Endocrinology 131:2690–2696

    CAS  PubMed  Google Scholar 

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Competing Interests

The authors declare no competing interests.Grant Support Supported by the Canadian Institutes for Health Research (H.J.C.). S.E.H. was supported by the CIHR Training Program in Reproduction, Early Development, and the Impact on Health, by the Réseau Québécois en Reproduction, and by the Research Institute of the McGill University Health Centre.

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Correspondence to Hugh J. Clarke .

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El-Hayek, S., Clarke, H.J. (2016). Control of Oocyte Growth and Development by Intercellular Communication Within the Follicular Niche. In: Piprek, R. (eds) Molecular Mechanisms of Cell Differentiation in Gonad Development. Results and Problems in Cell Differentiation, vol 58. Springer, Cham. https://doi.org/10.1007/978-3-319-31973-5_8

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