Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-669899f699-qzcqf Total loading time: 0 Render date: 2025-05-02T21:41:12.005Z Has data issue: false hasContentIssue false

10 - Hormones and growth factors in the regulation of oocyte maturation

from Section 3 - Developmental biology

Published online by Cambridge University Press:  05 October 2013

By
Marco Conti
Edited by
Alan Trounson ,
Roger Gosden  and
Ursula Eichenlaub-Ritter
Marco Conti
Affiliation:
Center for Reproductive Sciences and The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, Department of Obstetrics and Gynecology and Reproductive Sciences, University of California, San Francisco, CA, USA
Alan Trounson
Affiliation:
California Institute for Regenerative Medicine
Roger Gosden
Affiliation:
Center for Reproductive Medicine and Infertility, Cornell University, New York
Ursula Eichenlaub-Ritter
Affiliation:
Universität Bielefeld, Germany
Get access

Summary

Introduction

Oocyte maturation is the process by which a fully grown oocyte completes the developmental program initiated during fetal life to become a fertilizable egg. It has long been known that this process is triggered by endocrine signals generated by the pituitary. However, only recently has it become clear that the extensive reprogramming of the oocyte and somatic cells associated with ovulation also requires local paracrine and autocrine signals. These local regulations functioning within the periovulatory follicle will be the focus of this chapter.

Oocyte development and the follicle environment

A unique property of the female germ cell is the specialized meiotic cell cycle. Female meiosis initiates in the fetal gonad but will be completed only at the time the follicle is preparing for ovulation [1]. Thus, completion of meiosis may take more than 40 years in a woman. Although recent data in mouse and human have challenged the dogma that meiosis initiation does not occur in the postnatal life [2], the most widely held view is that a neonatal ovary is endowed with a finite number of oocytes that have completed the meiotic prophase but are held in a suspended state of the cell cycle, termed the dictyate state or germinal vesicle (GV) stage.

Type
Chapter
Information
Biology and Pathology of the Oocyte
Role in Fertility, Medicine and Nuclear Reprograming
 , pp. 109 - 118
Publisher: Cambridge University Press
Print publication year: 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Book purchase

Temporarily unavailable

References

Gosden, R, Lee, B.Portrait of an oocyte: our obscure origin. J Clin Invest 2010; 120: 973–83.CrossRefGoogle ScholarPubMed
White, YA, Woods, DC, Takai, Y, et al. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med 2012; 18: 413–21.CrossRefGoogle ScholarPubMed
Anderson, E, Albertini, DF.Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol 1976; 71: 680–6.CrossRefGoogle ScholarPubMed
Pincus, G, Enzmann, EV.The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. J Exp Med 1935; 62: 665–75.CrossRefGoogle ScholarPubMed
Edwards, RG.Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 1965; 208: 349–51.CrossRefGoogle ScholarPubMed
Segaloff, DL, Ascoli, M.The lutropin/choriogonadotropin receptor…4 years later. Endocr Rev 1993; 14: 324–47.Google Scholar
Conti, M, Hsieh, M, Zamah, AM, Oh, JS.Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol Cell Endocrinol 2012; 356: 65–73.CrossRefGoogle ScholarPubMed
Ferrell, JEXenopus oocyte maturation: new lessons from a good egg. Bioessays 1999; 21: 833–42.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Han, SJ, Conti, M.New pathways from PKA to the Cdc2/cyclin B complex in oocytes: Wee1B as a potential PKA substrate. Cell Cycle 2006; 5: 227–31.CrossRefGoogle ScholarPubMed
Conti, M, Andersen, CB, Richard, F, et al. Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol 2002; 187: 153–9.CrossRefGoogle ScholarPubMed
Mehlmann, LM, Saeki, Y, Tanaka, S, et al. The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 2004; 306: 1947–50.CrossRefGoogle ScholarPubMed
Hinckley, M, Vaccari, S, Horner, K, Chen, R, Conti, M.The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Dev Biol 2005; 287: 249–61.CrossRefGoogle ScholarPubMed
Reis, A, Madgwick, S, Chang, HY, et al. Prometaphase APCcdh1 activity prevents non-disjunction in mammalian oocytes. Nat Cell Biol. 2007; 9(10): 1192–8.CrossRefGoogle ScholarPubMed
Dekel, N, Lawrence, TS, Gilula, NB, Beers, WH.Modulation of cell-to-cell communication in the cumulus-oocyte complex and the regulation of oocyte maturation by LH. Dev Biol 1981; 86: 356–62.CrossRefGoogle ScholarPubMed
Tsafriri, A, Pomerantz, SH, Channing, CP.Inhibition of oocyte maturation by porcine follicular fluid: partial characterization of the inhibitor. Biol Reprod 1976; 14: 511–16.CrossRefGoogle ScholarPubMed
Masciarelli, S, Horner, K, Liu, C, et al. Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest 2004; 114: 196–205.CrossRefGoogle ScholarPubMed
Norris, RP, Ratzan, WJ, Freudzon, M, et al. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 2009; 136: 1869–78.CrossRefGoogle ScholarPubMed
Vaccari, S, Weeks, JL, 2nd, Hsieh, M, Menniti, FS, Conti, M.Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod 2009; 81: 595–604.CrossRefGoogle ScholarPubMed
Manganiello, VC, Smith, CJ, Degerman, E, Belfrage, P.Cyclic GMP-inhibited cyclic nucleotide phosphodiesterase. In: Beavo, JA, Houslay, MD, eds. Cyclic Nucleotide Phosphodiesterases: Structure, Regulation and Drug Action. Chichester: John Wiley and Sons. 1990; 87–116.Google Scholar
Zhang, M, Su, YQ, Sugiura, K, Xia, G, Eppig, JJ.Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 2010; 330: 366–9.CrossRefGoogle ScholarPubMed
Schulz, S.C-type natriuretic peptide and guanylyl cyclase B receptor. Peptides 2005; 26: 1024–34.CrossRefGoogle ScholarPubMed
Kolena, J, Danisová, A, Matulová, L, Scsuková, S. Stimulatory action of porcine follicular fluid on granulosa cell secretion of cyclic GMP. Exp Clin Endocrinol 1993; 101(4): 262–4.CrossRefGoogle ScholarPubMed
Kawamura, K, Cheng, Y, Kawamura, N, et al. 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 2011; 26: 3094–101.CrossRefGoogle ScholarPubMed
Richards, JS, Russell, DL, Ochsner, S, et al. Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog Horm Res 2002; 57: 195–220.CrossRefGoogle ScholarPubMed
May, JV, Frost, JP, Schomberg, DW.Differential effects of epidermal growth factor, somatomedin-C/insulin-like growth factor I, and transforming growth factor-beta on porcine granulosa cell deoxyribonucleic acid synthesis and cell proliferation. Endocrinology 1988; 123: 168–79.CrossRefGoogle ScholarPubMed
Dekel, N, Sherizly, I.Epidermal growth factor induces maturation of rat follicle-enclosed oocytes. Endocrinology 1985; 116: 406–9.CrossRefGoogle ScholarPubMed
Downs, SM.Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro. Biol Reprod 1989; 41: 371–9. Epub 2007 Sep 23.CrossRefGoogle ScholarPubMed
Westergaard, LG, Andersen, CY.Epidermal growth factor (EGF) in human preovulatory follicles. Hum Reprod 1989; 4: 257–60.CrossRefGoogle Scholar
Reeka, N, Berg, FD, Brucker, C.Presence of transforming growth factor alpha and epidermal growth factor in human ovarian tissue and follicular fluid. Hum Reprod 1998; 13: 2199–205.CrossRefGoogle ScholarPubMed
Bublil, EM, Yarden, Y.The EGF receptor family: spearheading a merger of signaling and therapeutics. Curr Opin Cell Biol 2007; 19: 124–34.CrossRefGoogle ScholarPubMed
Park, JY, Su, YQ, Ariga, M, et al. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004; 303: 682–4.CrossRefGoogle ScholarPubMed
Sekiguchi, T, Mizutani, T, Yamada, K, et al. Expression of epiregulin and amphiregulin in the rat ovary. J Mol Endocrinol 2004; 33: 281–91.CrossRefGoogle ScholarPubMed
Fru, KN, Cherian-Shaw, M, Puttabyatappa, M, VandeVoort, CA, Chaffin, CL.Regulation of granulosa cell proliferation and EGF-like ligands during the periovulatory interval in monkeys. Hum Reprod 2007; 22: 1247–52.CrossRefGoogle ScholarPubMed
Chen, X, Zhou, B, Yan, J, et al. Epidermal growth factor receptor activation by protein kinase C is necessary for FSH-induced meiotic resumption in porcine cumulus-oocyte complexes. J Endocrinol 2008; 197: 409–19.CrossRefGoogle ScholarPubMed
Lindbloom, SM, Farmerie, TA, Clay, CM, Seidel, GE, Carnevale, EM.Potential involvement of EGF-like growth factors and phosphodiesterases in initiation of equine oocyte maturation. Anim Reprod Sci 2008; 103: 187–92.CrossRefGoogle ScholarPubMed
Inoue, Y, Miyamoto, S, Fukami, T, et al. Amphiregulin is much more abundantly expressed than transforming growth factor-alpha and epidermal growth factor in human follicular fluid obtained from patients undergoing in vitro fertilization-embryo transfer. Fertil Steril 2009; 91: 1035–41.CrossRefGoogle ScholarPubMed
Zamah, AM, Hsieh, M, Chen, J, et al. Human oocyte maturation is dependent on LH-stimulated accumulation of the epidermal growth factor-like growth factor, amphiregulin. Hum Reprod 2010; 25: 2569–78.CrossRefGoogle ScholarPubMed
Curry, TE, Osteen, KG.The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 2003; 24: 428–65.CrossRefGoogle ScholarPubMed
Ashkenazi, H, Cao, X, Motola, S, et al. Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 2005; 146: 77–84.CrossRefGoogle ScholarPubMed
Panigone, S, Hsieh, M, Fu, M, Persani, L, Conti, M.Luteinizing hormone signaling in preovulatory follicles involves early activation of the epidermal growth factor receptor pathway. Mol Endocrinol 2008; 22: 924–36.CrossRefGoogle ScholarPubMed
Peluffo, MC, Ting, AY, Zamah, AM, et al. Amphiregulin promotes the maturation of oocytes isolated from the small antral follicles of the rhesus macaque. Hum Reprod. 2012; 27(8): 2430–7. .CrossRefGoogle ScholarPubMed
Shimada, M, Hernandez-Gonzalez, I, Gonzalez-Robayna, I, Richards, JS.Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 2006; 20: 1352–65.CrossRefGoogle ScholarPubMed
Hsieh, M, Lee, D, Panigone, S, et al. Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 2007; 27: 1914–24.CrossRefGoogle ScholarPubMed
Kim, K, Lee, H, Threadgill, DW, Lee, D.Epiregulin-dependent amphiregulin expression and ERBB2 signaling are involved in luteinizing hormone-induced paracrine signaling pathways in mouse ovary. Biochem Biophys Res Commun 2011; 405: 319–24.CrossRefGoogle ScholarPubMed
Hsieh, M, Thao, K, Conti, M.Genetic dissection of epidermal growth factor receptor signaling during luteinizing hormone-induced oocyte maturation. PLoS One 2011; 6: e21574. .CrossRefGoogle ScholarPubMed
Norris, RP, Freudzon, M, Nikolaev, VO, Jaffe, LA.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 2010; 140: 655–62.CrossRefGoogle ScholarPubMed
Robinson, JW, Zhang, M, Shuhaibar, LC, et al. 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 2012; 366: 308–16.CrossRefGoogle ScholarPubMed
Ben-Ami, I, Freimann, S, Armon, L, et al. PGE2 up-regulates EGF-like growth factor biosynthesis in human granulosa cells: new insights into the coordination between PGE2 and LH in ovulation. Mol Hum Reprod 2006; 12: 593–9.CrossRefGoogle ScholarPubMed
Kawamura, K, Ye, Y, Liang, CG, et al. Paracrine regulation of the resumption of oocyte meiosis by endothelin-1. Dev Biol 2009; 327: 62–70.CrossRefGoogle ScholarPubMed
Richard, FJ, Sirard, MA.Effects of follicular cells on oocyte maturation. II: Theca cell inhibition of bovine oocyte maturation in vitro. Biol Reprod 1996; 54: 22–8.CrossRefGoogle ScholarPubMed
Kawamura, K, Kumagai, J, Sudo, S, et al. Paracrine regulation of mammalian oocyte maturation and male germ cell survival. Proc Natl Acad Sci USA 2004; 101: 7323–8.CrossRefGoogle ScholarPubMed
Mehlmann, LM, Kalinowski, RR, Ross, LF, et al. Meiotic resumption in response to luteinizing hormone is independent of a Gi family G protein or calcium in the mouse oocyte. Dev Biol 2006; 299: 345–55.CrossRefGoogle ScholarPubMed
Byskov, AG, Andersen, CY, Nordholm, L, et al. Chemical structure of sterols that activate oocyte meiosis. Nature 1995; 374: 559–62.CrossRefGoogle ScholarPubMed
Cao, X, Pomerantz, SH, Popliker, M, Tsafriri, A.Meiosis-activating sterol synthesis in rat preovulatory follicle: is it involved in resumption of meiosis?Biol Reprod 2004; 71: 1807–12.CrossRefGoogle ScholarPubMed
Marin Bivens, CL, Grondahl, C, Murray, A, et al. Meiosis-activating sterol promotes the metaphase I to metaphase II transition and preimplantation developmental competence of mouse oocytes maturing in vitro. Biol Reprod 2004; 70: 1458–64.CrossRefGoogle ScholarPubMed
Luciano, AM, Lodde, V, Beretta, MS, et al. Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus-oocyte complexes: role of cumulus cells, cyclic adenosine 3´,5´-monophosphate, and glutathione. Mol Reprod Dev 2005; 71: 389–97.CrossRefGoogle Scholar
De La, Fuente R, O’Brien, MJ, Eppig, JJ.Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum Reprod 1999; 14: 3060–8.CrossRefGoogle Scholar
Richani, D, Ritter, LJ, Thompson, JG, Gilchrist, RB. Mode of oocyte maturation affects EGF-like peptide function and oocyte competence. Mol Hum Reprod 2013; 19: 500–9.CrossRef
Seifer, DB, Feng, B, Shelden, RM, Chen, S, Dreyfus, CF.Neurotrophin-4/5 and neurotrophin-3 are present within the human ovarian follicle but appear to have different paracrine/autocrine functions. J Clin Endocrinol Metab 2002; 87: 4569–71.CrossRefGoogle ScholarPubMed
Kawamura, K, Kawamura, N, Mulders, SM, Sollewijn, Gelpke MD, Hsueh, AJ.Ovarian brain-derived neurotrophic factor (BDNF) promotes the development of oocytes into preimplantation embryos. Proc Natl Acad Sci USA 2005; 102: 9206–11.CrossRefGoogle ScholarPubMed
Linher, K, Wu, D, Li, J. Glial cell line-derived neurotrophic factor: an intraovarian factor that enhances oocyte developmental competence in vitro. Endocrinology. 2007; 148(9): 4292–301. Epub 2007 May 31.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×