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Preparing for Fertilization: Intercellular Signals for Oocyte Maturation

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Reproductive and Developmental Strategies

Part of the book series: Diversity and Commonality in Animals ((DCA))

Abstract

In the hours preceding fertilization, oocytes prepare to begin development in a process known as maturation. This includes progression of the meiotic cell cycle and development of the ability to undergo the release of calcium that activates development at fertilization. In many species, the signal for oocyte maturation acts initially on somatic cells surrounding the oocyte, rather than on the oocyte itself. This chapter concerns the intercellular signaling events by which the maturation-inducing signal travels from the somatic cells to the oocyte. We first discuss how meiotic prophase arrest is maintained in mammalian oocytes, and how luteinizing hormone (LH) action on receptors in the cells of the surrounding follicle causes meiosis to resume. The LH receptors are located exclusively in the outer granulosa cells of the follicle and signal through a Gs-linked receptor to cause a decrease in cyclic guanosine monophosphate (cGMP). The LH-induced signal propagates inwards to the oocyte by way of cGMP diffusion out of the oocyte through gap junctions. We then briefly discuss the similarities and differences in mechanisms controlling oocyte maturation in animals other than mammals, focusing on hydrozoan jellyfish to emphasize the early evolutionary origin of these regulatory processes. G-protein-coupled receptors and cyclic nucleotides are common regulators in many animals. However, the assembly of these components into a regulatory system differs among species.

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References

  • Ballard WW (1942) The mechanism for synchronous spawning in Hydractinia and Pennaria. Biol Bull 82:329–339

    Article  Google Scholar 

  • Blake CA (1976) A detailed characterization of the proestrous luteinizing hormone surge. Endocrinology 98:445–450

    Article  CAS  PubMed  Google Scholar 

  • Bornslaeger EA, Mattei P, Schultz RM (1986) Involvement of cAMP-dependent protein kinase and protein phosphorylation in regulation of mouse oocyte maturation. Dev Biol 114:453–462

    Article  CAS  PubMed  Google Scholar 

  • Bortolussi M, Marini G, Dal Lago A (1977) Autoradiographic study of the distribution of LH (HCG) receptors in the ovary of untreated and gonadotrophin-primed immature rats. Cell Tissue Res 183:329–342

    Article  CAS  PubMed  Google Scholar 

  • Browne CL, Wiley HS, Dumont JN (1979) Oocyte-follicle cell gap junctions in Xenopus laevis and the effects of gonadotropin on their permeability. Science 203:182–183

    Article  CAS  PubMed  Google Scholar 

  • Cerda JL, Petrino TR, Wallace RA (1993) Functional heterologous gap junctions in Fundulus ovarian follicles maintain meiotic arrest and permit hydration during oocyte maturation. Dev Biol 160:228–235

    Article  CAS  PubMed  Google Scholar 

  • Cheon B, Lee HC, Wakai T, Fissore RA (2013) Ca2+ influx and the store-operated Ca2+ entry pathway undergo regulation during mouse oocyte maturation. Mol Biol Cell 24:1396–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chesnel F, Eppig JJ (1995) Synthesis and accumulation of p34cdc2 and cyclin B in mouse oocytes during acquisition of competence to resume meiosis. Mol Reprod Dev 40:503–508

    Article  CAS  PubMed  Google Scholar 

  • Chiba K, Kado RT, Jaffe LA (1990) Development of calcium release mechanisms during starfish oocyte maturation. Dev Biol 140:300–306

    Article  CAS  PubMed  Google Scholar 

  • Clarke HJ (2018) Regulation of germ cell development by intercellular signaling in the mammalian ovarian follicle. WIREs Dev Biol 7:e294

    Article  CAS  Google Scholar 

  • Clift D, Schuh M (2015) A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat Commun 6:7217

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Deguchi R, Takeda N, Stricker SA (2011) Comparative biology of cAMP-induced germinal vesicle breakdown in marine invertebrate oocytes. Mol Reprod Dev 78:708–725

    Article  CAS  PubMed  Google Scholar 

  • DiLuigi A, Weitzman VN, Pace MC, Siano LJ, Maier D, Mehlmann LM (2008) Meiotic arrest in human oocytes is maintained by a Gs signaling pathway. Biol Reprod 78:667–672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dungan HM, Clifton DK, Steiner RA (2006) Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 147:1154–1158

    Article  CAS  PubMed  Google Scholar 

  • Dupré A, Daldello EM, Nairn AC, Jessus C, Haccard O (2014) Phosphorylation of ARPP19 by protein kinase A prevents meiosis resumption in Xenopus oocytes. Nat Commun 5:3318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egbert JR, Shuhaibar LC, Edmund AB, Van Helden DA, Robinson JW, Uliasz TF, Baena V, Geerts A, Wunder F, Potter LR, Jaffe LA (2014) Dephosphorylation and inactivation of the NPR2 guanylyl cyclase in the granulosa cells contributes to the LH-induced cGMP decrease that causes resumption of meiosis in rat oocytes. Development 141:3594–3604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egbert JR, Uliasz TF, Shuhaibar LC, Geerts A, Wunder F, Kleiman RJ, Humphrey JM, Lampe PD, Artemyev NO, Rybalkin SD, Beavo JA, Movsesian MA, Jaffe LA (2016) Luteinizing hormone causes phosphorylation and activation of the cGMP phosphodiesterase PDE5 in rat ovarian follicles, contributing, together with PDE1 activity, to the resumption of meiosis. Biol Reprod 94(5):110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egbert JR, Yee SP, Jaffe LA (2018) Luteinizing hormone signaling phosphorylates and activates the cyclic GMP phosphodiesterase PDE5 in mouse ovarian follicles, contributing an additional component to the hormonally induced decrease in cyclic GMP that reinitiates meiosis. Dev Biol 435:6–14

    Article  CAS  PubMed  Google Scholar 

  • Firmani LD, Uliasz TF, Mehlmann LM (2017) The switch from cAMP-independent to cAMP-dependent arrest of meiotic prophase is associated with coordinated GPR3 and CDK1 expression in mouse oocytes. Dev Biol 434:196–205

    Article  CAS  PubMed  Google Scholar 

  • Freeman G (1987) The role of oocyte maturation in the ontogeny of the fertilization site in the hydrozoan Hydractinia echinata. Roux Arch Dev Biol 196:83–92

    Article  PubMed  Google Scholar 

  • Freeman G, Ridgway EB (1988) The role of cAMP in oocyte maturation and the role of the germinal vesicle contents in mediating maturation and subsequent developmental events in hydrozoans. Roux Arch Dev Biol 197:197–211

    Article  CAS  PubMed  Google Scholar 

  • Geister KA, Brinkmeier ML, Hsieh M, Faust SM, Karolyi IJ, Perosky JE, Kozloff KM, Conti M, Camper SA (2013) A novel loss-of-function mutation in Npr2 clarifies primary role in female reproduction and reveals a potential therapy for acromesomelic dysplasia, Maroteaux type. Hum Mol Genet 22:345–357

    Article  CAS  PubMed  Google Scholar 

  • Gilbert SF (2014) Developmental biology, 10th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Gilula NB, Epstein ML, Beers WH (1978) Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J Cell Biol 78:58–75

    Article  CAS  PubMed  Google Scholar 

  • Haccard O, Dupré A, Liere P, Pianos A, Eychenne B, Jessus C, Ozon R (2012) Naturally occurring steroids in Xenopus oocyte during meiotic maturation. Unexpected presence and role of steroid sulfates. Mol Cell Endocrinol 362:110–119

    Article  CAS  PubMed  Google Scholar 

  • Haraguchi S, Ikeda N, Abe M, Tsutsui K, Mita M (2016) Nucleotide sequence and expression of relaxin-like gonad-stimulating peptide gene in starfish Asterina pectinifera. Gen Comp Endocrinol 227:115–119

    Article  CAS  PubMed  Google Scholar 

  • Hinckley M, Vaccari S, Horner K, Chen R, Conti M (2005) The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Dev Biol 287:249–261

    Article  CAS  PubMed  Google Scholar 

  • Holt JE, Lane SIR, Jones KT (2013) The control of meiotic maturation in mammalian oocytes. Curr Top Dev Biol 102:207–226

    Article  CAS  PubMed  Google Scholar 

  • Horner K, Livera G, Hinckley M, Trinh K, Storm D, Conti M (2003) Rodent oocytes express an active adenylyl cyclase required for meiotic arrest. Dev Biol 258:385–396

    Article  CAS  PubMed  Google Scholar 

  • Houliston E, Momose T, Manuel M (2010) Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends Genet 26:159–167

    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 

  • Hunzicker-Dunn M, Mayo K (2015) Gonadotropin signaling in the ovary. In: Plant TM, Zeleznik AJ (eds) Knobil and Neill’s physiology of reproduction, 4th edn. Academic, San Diego, pp 895–945

    Chapter  Google Scholar 

  • Ikegami S, Honji N, Yoshida M (1978) Light-controlled production of spawning-inducing substance in jellyfish ovary. Nature 272:611–612

    Article  Google Scholar 

  • Jaffe LA, Egbert JR (2017) Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle. Annu Rev Physiol 10:237–260

    Article  CAS  Google Scholar 

  • Jones KT (2004) Turning it on and off: M-phase promoting factor during meiotic maturation and fertilization. Mol Hum Reprod 10:1–5

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski RR, Berlot CH, Jones TL, Ross LF, Jaffe LA, Mehlmann LM (2004) Maintenance of meiotic prophase arrest in vertebrate oocytes by a Gs protein-mediated pathway. Dev Biol 267:1–13

    Article  CAS  PubMed  Google Scholar 

  • Kanatani H, Shirai H, Nakanishi K, Kurokawa T (1969) Isolation and identification of meiosis inducing substance in starfish Asterias amurensis. Nature 221:273–274

    Article  CAS  PubMed  Google Scholar 

  • Kawamura K, Cheng Y, Kawamura N, Takae S, Okada A, Kawagoe Y, Mulders S, Terada Y, Hsueh AJ (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 

  • Kim S, Spike C, Greenstein D (2013) Control of oocyte growth and meiotic maturation in Caenorhabditis elegans. Adv Exp Med Biol 757:277–320

    Article  CAS  PubMed  Google Scholar 

  • Kishimoto T (2011) A primer on meiotic resumption in starfish oocytes: the proposed signaling pathway triggered by maturation-inducing hormone. Mol Reprod Dev 78:704–707

    Article  CAS  PubMed  Google Scholar 

  • Kovacic N, Parlow AF (1972) Alterations in serum FSH-LH ratios in relation to the estrous cycle, pseudopregnancy, and gonadectomy in the mouse. Endocrinology 91:910–915

    Article  CAS  PubMed  Google Scholar 

  • Kovo M, Kandli-Cohen M, Ben-Haim M, Galiani D, Carr DW, Dekel N (2006) An active protein kinase A (PKA) is involved in meiotic arrest of rat growing oocytes. Reproduction 132:33–43

    Article  CAS  PubMed  Google Scholar 

  • Kume S, Yamamoto A, Inoue T, Muto A, Okano H, Mikoshiba K (1997) Developmental expression of the inositol 1,4,5-trisphosphate receptor and structural changes in the endoplasmic reticulum during oogenesis and meiotic maturation of Xenopus laevis. Dev Biol 15:228–239

    Article  Google Scholar 

  • Ledent C, Demeestere I, Blum D, Petermans J, Hämälälnen T, Smits G, Vassart G (2005) Premature ovarian aging in mice deficient for Gpr3. Proc Natl Acad Sci U S A 102:8922–8926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee B, Vermassen E, Yoon SY, Vanderheyden V, Ito J, Alfandari D, De Smedt H, Parys JB, Fissore RA (2006) Phosphorylation of IP3R1 and the regulation of [Ca2+]i responses at fertilization: a role for the MAP kinase pathway. Development 133:4355–4365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Xie F, Zamah AM, Cao B, Conti M (2014) Multiple pathways mediate luteinizing hormone regulation of cGMP signaling in the mouse ovarian follicle. Biol Reprod 91(1):9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mann JS, Lowther KM, Mehlmann LM (2010) Reorganization of the endoplasmic reticulum and development of Ca2+ release mechanisms during meiotic maturation of human oocytes. Biol Reprod 83:578–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masui Y, Clarke HJ (1979) Oocyte maturation. Int Rev Cytol 57:185–282

    Article  CAS  PubMed  Google Scholar 

  • Mehlmann LM (2005) Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130:791–799

    Article  CAS  PubMed  Google Scholar 

  • Mehlmann LM (2013) Signaling for meiotic resumption in granulosa cells, cumulus cells, and oocyte. In: Coticchio G, Albertini DF, De Santis L (eds) Oogenesis. Springer, London, pp 171–182

    Chapter  Google Scholar 

  • Mehlmann LM, Kline D (1994) Regulation of intracellular calcium in the mouse egg: calcium release in response to sperm or inositol trisphosphate is enhanced after meiotic maturation. Biol Reprod 51:1088–1098

    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, Mikoshiba K, Kline D (1996) Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte. Dev Biol 180:489–498

    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, Brennan TJ, Evsikov AV, Pendola FL, Knowles BB, Eppig JJ, Jaffe LA (2004) The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306:1947–1950

    Article  CAS  PubMed  Google Scholar 

  • Mita M (2013) Relaxin-like gonad-stimulating substance in an echinoderm, the starfish: a novel relaxin system in reproduction of invertebrates. Gen Comp Endocrinol 181:241–245

    Article  CAS  PubMed  Google Scholar 

  • Mita M, Yoshikuni M, Ohno K, Shibata Y, Paul-Prasanth B, Pitchayawasin S, Isobe M, Nagahama Y (2009) A relaxin-like peptide purified from radial nerves induces oocyte maturation and ovulation in the starfish, Asterina pectinifera. Proc Natl Acad Sci U S A 106:9507–9512

    Article  PubMed  PubMed Central  Google Scholar 

  • Nader N, Dib M, Daalis A, Kulkarni RP, Machaca K (2014) Role for endocytosis of a constitutively active GPCR (GPR185) in releasing vertebrate oocyte meiotic arrest. Dev Biol 15:355–366

    Article  CAS  Google Scholar 

  • Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Develop Growth Differ 50(Suppl 1):S195–S219

    Article  CAS  Google Scholar 

  • Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul DL, Lampe PD, Jaffe LA (2008) Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: one of two paths to meiotic resumption. Development 135:3229–3238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, Wang H, Ke H, Nikolaev VO, Jaffe LA (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 

  • Oakley AE, Clifton DK, Steiner RA (2009) Kisspeptin signaling in the brain. Endocrin Rev 30:713–743

    Article  CAS  Google Scholar 

  • Panigone S, Hsieh M, Fu M, Persani L, Conti M (2008) Luteinizing hormone signaling in preovulatory follicles involves early activation of the epidermal growth factor receptor pathway. Mol Endocrinol 22:924–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park JY, YQ S, Ariga M, Law E, Jin SL, Conti M (2004) EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682–684

    Article  CAS  PubMed  Google Scholar 

  • Pincus G, Enzmann EV (1935) The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. J Exp Med 62:665–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potter LR (2011) Natriuretic peptide metabolism, clearance and degradation. FEBS J 278:1808–1817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quiroga Artigas G, Lapébie P, Leclère L, Takeda N, Deguchi R, Jékely G, Momose T, Houliston E (2018) A gonad-expressed opsin mediates light-induced spawning in the jellyfish Clytia. Elife 7:e29555

    Google Scholar 

  • Racowsky C, Baldwin KV (1989) In vitro and in vivo studies reveal that hamster oocyte meiotic arrest is maintained only transiently by follicular fluid, but persistently by membrana/cumulus granulosa cell contact. Dev Biol 134:297–306

    Article  CAS  PubMed  Google Scholar 

  • Reizel Y, Elbaz J, Dekel N (2010) Sustained activity of the EGF receptor is an absolute requisite for LH-induced oocyte maturation and cumulus expansion. Mol Endocrinol 24:402–411

    Article  CAS  PubMed  PubMed Central  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(6):137

    Article  CAS  PubMed  Google Scholar 

  • Robinson JW, Zhang M, Shuhaibar LC, Norris RP, Geerts A, Wunder F, Eppig JJ, Potter LR, Jaffe LA (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 

  • Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130:484–498

    Article  CAS  PubMed  Google Scholar 

  • Sela-Abramovich S, Chorev E, Galiani D, Dekel N (2005) Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocyte maturation in rat ovarian follicles. Endocrinology 146:1236–1244

    Article  CAS  PubMed  Google Scholar 

  • Sela-Abramovich S, Edry I, Galiani D, Nevo N, Dekel N (2006) Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation. Endocrinology 147:2280–2286

    Article  CAS  PubMed  Google Scholar 

  • Shuhaibar LC, Egbert JR, Norris RP, Lampe PD, Nikolaev VO, Thunemann M, Wen L, Feil R, Jaffe LA (2015) Intercellular signaling via cyclic GMP diffusion through gap junctions in the mouse ovarian follicle. Proc Natl Acad Sci U S A 112:5527–5532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shuhaibar LC, Egbert JR, Edmund AB, Uliasz TF, Dickey DM, Yee SP, Potter LR, Jaffe LA (2016) Dephosphorylation of juxtamembrane serines and threonines of the NPR2 guanylyl cyclase is required for the rapid resumption of oocyte meiosis in response to luteinizing hormone. Dev Biol 409:194–201

    Article  CAS  PubMed  Google Scholar 

  • Silvestre F, Gallo A, Cuomo A, Covino T, Tosti E (2010) Role of cyclic AMP in the maturation of Ciona intestinalis oocytes. Zygote 19:365–371

    Article  CAS  Google Scholar 

  • Takeda N, Kyozuka K, Deguchi R (2006) Increase in intracellular cAMP is a prerequisite signal for initiation of physiological oocyte meiotic maturation in the hydrozoan Cytaeis uchidae. Dev Biol 298:248–258

    Article  CAS  PubMed  Google Scholar 

  • Takeda N, Nakajima Y, Koizumi O, Fujisawa T, Takahashi T, Matsumoto M, Deguchi R (2013) Neuropeptides trigger oocyte maturation and subsequent spawning in the hydrozoan jellyfish Cytaeis uchidae. Mol Reprod Dev 80:223–232

    Article  CAS  PubMed  Google Scholar 

  • Takeda N, Kon Y, Quiroga Artigas G, Lapébie P, Barreau C, Koizumi O, Kishimoto T, Tachibana K, Houliston E, Deguchi R (2018) Identification of jellyfish neuropeptides that act directly as oocyte maturation-inducing hormones. Development 145:dev156786

    Article  CAS  PubMed  Google Scholar 

  • Törnell J, Billig H, Hillensjo T (1991) Regulation of oocyte maturation by changes in ovarian levels of cyclic nucleotides. Hum Reprod 6:411–422

    Article  PubMed  Google Scholar 

  • Tsafriri A, Motola S (2007) Are steroids dispensable for meiotic resumption in mammals? Trends Endocrinol Metab 18:321–327

    Article  CAS  PubMed  Google Scholar 

  • Tsuji T, Kiyosu C, Akiyama K, Kunieda T (2012) CNP/NPR2 signaling maintains oocyte meiotic arrest in early antral follicles and is suppressed by EGFR-mediated signaling in preovulatory follicles. Mol Reprod Dev 79:795–802

    Article  CAS  PubMed  Google Scholar 

  • Vaccari S, Weeks JL, Hsieh M, Menniti FS, Conti M (2009) Cyclic GMP signaling is involved in the LH-dependent meiotic maturation of mouse oocytes. Biol Reprod 81:595–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wakai T, Vanderheyden V, Yoon SY, Cheon B, Zhang N, Parys JB, Fissore RA (2012) Regulation of inositol 1,4,5-trisphosphate receptor function during mouse oocyte maturation. J Cell Physiol 227:705–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Greenwald GS (1993) Hypophysectomy of the cyclic mouse. II. Effects of follicle-stimulating hormone (FSH) and luteinizing hormone on folliculogenesis, FSH and human chroionic gonadotropin receptors, and steroidogenesis. Biol Reprod 48:595–605

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Kong N, Li N, Hao X, Wei K, Xiang X, Xia G, Zhang M (2013) Epidermal growth factor receptor signaling-dependent calcium elevation in cumulus cells is required for NPR2 inhibition and meiotic resumption in mouse oocytes. Endocrinology 154:3401–3409

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Y-Q S, 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 

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Acknowledgements

We thank Lisa Mehlmann and Evelyn Houliston for reviewing the manuscript. Work in the authors’ laboratory is supported by the Eunice Kennedy Shriver National Institute of Child Health and Human Development (R37HD014939 to LAJ).

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Authors and Affiliations

  1. Department of Cell Biology, University of Connecticut Health Center, Farmington, CT, USA

    Leia C. Shuhaibar & Laurinda A. Jaffe

  2. Department of Biological Sciences, Florida Institute of Technology, Melbourne, FL, USA

    David J. Carroll

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  1. Leia C. Shuhaibar
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  2. David J. Carroll
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  3. Laurinda A. Jaffe
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Correspondence to Laurinda A. Jaffe .

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Editors and Affiliations

  1. Department of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Japan

    Kazuya Kobayashi

  2. Department of Biological Sciences, Graduate School of Science and Technology Kumamoto University, Kumamoto, Japan

    Takeshi Kitano

  3. Laboratory of Reproductive Developmental Biology, Division of Earth Sciences, Biology, and Chemistry, Graduate School of Sciences and Technology for Innovation Yamaguchi University, Yamaguchi, Japan

    Yasuhiro Iwao

  4. Misaki Marine Biological Station, Graduate School of Science The University of Tokyo, Miura, Japan

    Mariko Kondo

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Shuhaibar, L.C., Carroll, D.J., Jaffe, L.A. (2018). Preparing for Fertilization: Intercellular Signals for Oocyte Maturation. In: Kobayashi, K., Kitano, T., Iwao, Y., Kondo, M. (eds) Reproductive and Developmental Strategies. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56609-0_25

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