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A New Understanding on the Regulation of Oocyte Meiotic Prophase Arrest and Resumption

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Book cover Development of In Vitro Maturation for Human Oocytes

Abstract

In mammals, oocyte maturation must be remained precisely in synchrony with ovulation for normal female fertility. Signals from ovarian somatic cells prevent precocious resumption of meiosis until a surge of luteinizing hormone (LH) from the pituitary stimulates oocyte maturation and ovulation. Natriuretic peptide type C (NPPC) produced by mural granulosa cells stimulates the generation of cyclic guanosine 3′,5′-monophosphate (cGMP) by natriuretic peptide receptor 2 (NPR2) of cumulus cells. The cGMP then diffuses into oocytes and arrests meiotic progression by inhibiting oocyte-specific phosphodiesterase 3A (PDE3A) activity and cyclic adenosine 3′,5′-monophosphate (cAMP) hydrolysis. Intraoocyte cAMP is produced by G-protein-coupled receptor GPR3/12 activation of adenylyl cyclase endogenous to the oocyte. Oocyte itself also promotes cumulus cell expression of NPR2 and inosine monophosphate dehydrogenase (IMPDH) to elevate cGMP levels for meiotic arrest. Follicle-stimulating hormone (FSH), through estradiol (E2), enhances NPPC/NPR2 expression to ensure meiotic arrest during antral follicular development. LH-induced epidermal growth factor (EGF)-like growth factors decrease NPPC content and NPR2 activity, resulting in cGMP decrease and meiotic resumption. A better understanding of these signaling networks on the regulation of oocyte meiotic progress will provide new opportunities for the manipulation of follicular functions for contraception or the treatment of infertility.

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References

  1. Eppig JJ, Vivieros MM, Marin-Bivens C, De La Fuente R. Regulation of mammalian oocyte maturation. In: Leung PCK, Adashi EY, editors. The ovary. Amsterdam: Elsevier Academic Press; 2004. p. 113–29.

    Chapter  Google Scholar 

  2. Solc P, Schultz RM, Motlik J. Prophase I arrest and progression to metaphase I in mouse oocytes: comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Mol Hum Reprod. 2010;16:654–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Szybek K. In-vitro maturation of oocytes from sexually immature mice. J Endocrinol. 1972;54:527–8.

    Article  CAS  PubMed  Google Scholar 

  4. Erickson GF, Sorensen RA. In vitro maturation of mouse oocytes isolated from late, middle, and pre-antral graafian follicles. J Exp Zool. 1974;190:123–7.

    Article  CAS  PubMed  Google Scholar 

  5. Sorensen RA, Wassarman PM. Relationship between growth and meiotic maturation of the mouse oocyte. Dev Biol. 1976;50:531–6.

    Article  CAS  PubMed  Google Scholar 

  6. Ducibella T. The cortical reaction and development of activation competence in mammalian oocytes. Hum Reprod Update. 1996;2:29–42.

    Article  CAS  PubMed  Google Scholar 

  7. Mehlmann LM, Mikoshiba K, Kline D. Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte. Dev Biol. 1996;180:489–98.

    Article  CAS  PubMed  Google Scholar 

  8. Ducibella T. Biochemical and cellular insights into the temporal window of normal fertilization. Theriogenology. 1998;49:53–65.

    Article  CAS  PubMed  Google Scholar 

  9. Dekel N. Molecular control of meiosis. Trends Endocrinol Metab (TEM). 1995;6:165–9.

    Article  CAS  Google Scholar 

  10. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Edwards RG. Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature. 1965;208:349–51.

    Article  CAS  PubMed  Google Scholar 

  12. Tsafriri A, Pomerantz SH. Oocyte maturation inhibitor. Clin Endocrinol Metab. 1986;15:157–70.

    Article  CAS  PubMed  Google Scholar 

  13. Tsafriri A, Dekel N, Bar-Ami S. The role of oocyte maturation inhibitor in follicular regulation of oocyte maturation. J Reprod Fertil. 1982;64:541–51.

    Article  CAS  PubMed  Google Scholar 

  14. Horner K, Livera G, Hinckley M, Trinh K, Storm D, Conti M. Rodent oocytes express an active adenylyl cyclase required for meiotic arrest. Dev Biol. 2003;258:385–96.

    Article  CAS  PubMed  Google Scholar 

  15. Mehlmann LM, Saeki Y, Tanaka S, Brennan TJ, Evsikov AV, Pendola FL, Knowles BB, Eppig JJ, Jaffe LA. The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science. 2004;306:1947–50.

    Article  CAS  PubMed  Google Scholar 

  16. 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.

    Article  CAS  PubMed  Google Scholar 

  17. Mehlmann LM. Oocyte-specific expression of Gpr3 is required for the maintenance of meiotic arrest in mouse oocytes. Dev Biol. 2005;288:397–404.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Zhang M, Xia G. Hormonal control of mammalian oocyte meiosis at diplotene stage. Cell Mol Life Sci (CMLS). 2012;69:1279–88.

    Article  CAS  Google Scholar 

  19. Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, Wang H, Ke H, Nikolaev VO, Jaffe LA. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development. 2009;136:1869–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ledent C, Demeestere I, Blum D, Petermans J, Hamalainen T, Smits G, Vassart G. Premature ovarian aging in mice deficient for Gpr3. Proc Natl Acad Sci U S A. 2005;102:8922–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zhang M, Ouyang H, Xia G. The signal pathway of gonadotrophins-induced mammalian oocyte meiotic resumption. Mol Hum Reprod. 2009;15:399–409.

    Article  PubMed  CAS  Google Scholar 

  23. Conti M, Andersen CB, Richard F, Mehats C, Chun SY, Horner K, Jin C, Tsafriri A. Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol. 2002;187:153–9.

    Article  CAS  PubMed  Google Scholar 

  24. Zhang M, Xia G, Zhou B, Wang C. Gonadotropin-controlled mammal oocyte meiotic resumption. Front Biosci: J Virtual Libr. 2007;12:282–96.

    Article  CAS  Google Scholar 

  25. Cho WK, Stern S, Biggers JD. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool. 1974;187:383–6.

    Article  CAS  PubMed  Google Scholar 

  26. Hambleton R, Krall J, Tikishvili E, Honeggar M, Ahmad F, Manganiello VC, Movsesian MA. Isoforms of cyclic nucleotide phosphodiesterase PDE3 and their contribution to cAMP hydrolytic activity in subcellular fractions of human myocardium. J Biol Chem. 2005;280:39168–74.

    Article  CAS  PubMed  Google Scholar 

  27. Törnell J, Billig H, Hillensjo T. Resumption of rat oocyte meiosis is paralleled by a decrease in guanosine 3′,5′-cyclic monophosphate (cGMP) and is inhibited by microinjection of cGMP. Acta Physiol Scand. 1990;139:511–7.

    Article  PubMed  Google Scholar 

  28. Törnell J, Carlsson B, Billig H. Atrial natriuretic peptide inhibits spontaneous rat oocyte maturation. Endocrinology. 1990;126:1504–8.

    Article  PubMed  Google Scholar 

  29. Grøndahl C, Breinholt J, Wahl P, Murray A, Hansen TH, Faerge I, Stidsen CE, Raun K, Hegele-Hartung C. Physiology of meiosis-activating sterol: endogenous formation and mode of action. Hum Reprod. 2003;18:122–9.

    Article  PubMed  Google Scholar 

  30. Wiersma A, Hirsch B, Tsafriri A, Hanssen RG, Van de Kant M, Kloosterboer HJ, Conti M, Hsueh AJ. Phosphodiesterase 3 inhibitors suppress oocyte maturation and consequent pregnancy without affecting ovulation and cyclicity in rodents. J Clin Investig. 1998;102:532–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Eppig JJ, Ward-Bailey PF, Coleman DL. Hypoxanthine and adenosine in murine ovarian follicular fluid: concentrations and activity in maintaining oocyte meiotic arrest. Biol Reprod. 1985;33:1041–9.

    Article  CAS  PubMed  Google Scholar 

  32. Mehlmann LM. Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction. 2005;130:791–9.

    Article  CAS  PubMed  Google Scholar 

  33. Tripathi A, Kumar KV, Chaube SK. Meiotic cell cycle arrest in mammalian oocytes. J Cell Physiol. 2010;223:592–600.

    CAS  PubMed  Google Scholar 

  34. Su YQ, Sugiura K, Sun F, Pendola JK, Cox GA, Handel MA, Schimenti JC, Eppig JJ. MARF1 regulates essential oogenic processes in mice. Science. 2012;335:1496–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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.

    Article  CAS  PubMed  Google Scholar 

  36. Bornslaeger EA, Schultz RM. Regulation of mouse oocyte maturation: effect of elevating cumulus cell cAMP on oocyte cAMP levels. Biol Reprod. 1985;33:698–704.

    Article  CAS  PubMed  Google Scholar 

  37. Webb RJ, Marshall F, Swann K, Carroll J. Follicle-stimulating hormone induces a gap junction-dependent dynamic change in [cAMP] and protein kinase a in mammalian oocytes. Dev Biol. 2002;246:441–54.

    Article  CAS  PubMed  Google Scholar 

  38. Mehlmann LM, Jones TL, Jaffe LA. Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science. 2002;297:1343–5.

    Article  CAS  PubMed  Google Scholar 

  39. DiLuigi A, Weitzman VN, Pace MC, Siano LJ, Maier D, Mehlmann LM. Meiotic arrest in human oocytes is maintained by a Gs signaling pathway. Biol Reprod. 2008;78:667–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Vaccari S, Horner K, Mehlmann LM, Conti M. Generation of mouse oocytes defective in cAMP synthesis and degradation: endogenous cyclic AMP is essential for meiotic arrest. Dev Biol. 2008;316:124–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Joost P, Methner A. Phylogenetic analysis of 277 human G-protein-coupled receptors as a tool for the prediction of orphan receptor ligands. Genome Biol. 2002;3, RESEARCH0063.

    Google Scholar 

  42. Shitsukawa K, Andersen CB, Richard FJ, Horner AK, Wiersma A, van Duin M, Conti M. Cloning and characterization of the cyclic guanosine monophosphate-inhibited phosphodiesterase PDE3A expressed in mouse oocyte. Biol Reprod. 2001;65:188–96.

    Article  CAS  PubMed  Google Scholar 

  43. Thomas RE, Armstrong DT, Gilchrist RB. Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Dev Biol. 2002;244:215–25.

    Article  CAS  PubMed  Google Scholar 

  44. Mayes MA, Sirard MA. Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol Reprod. 2002;66:180–4.

    Article  CAS  PubMed  Google Scholar 

  45. 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.

    Article  CAS  PubMed  Google Scholar 

  46. Downs SM, Eppig JJ. The role of purines in the maintenance of meiotic arrest in mouse oocytes. Tokai J Exp Clin Med. 1986;11:463–9.

    CAS  PubMed  Google Scholar 

  47. Masciarelli S, Horner K, Liu C, Park SH, Hinckley M, Hockman S, Nedachi T, Jin C, Conti M, Manganiello V. Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest. 2004;114:196–205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sasseville M, Cote N, Guillemette C, Richard FJ. New insight into the role of phosphodiesterase 3A in porcine oocyte maturation. BMC Dev Biol. 2006;6:47.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Richard FJ, Tsafriri A, Conti M. Role of phosphodiesterase type 3A in rat oocyte maturation. Biol Reprod. 2001;65:1444–51.

    Article  CAS  PubMed  Google Scholar 

  50. Hubbard CJ. Ovarian cAMP and cGMP fluctuations in the hamster during the oestrous cycle. J Reprod Fertil. 1980;59:351–5.

    Article  CAS  PubMed  Google Scholar 

  51. Downs SM, Eppig JJ. Induction of mouse oocyte maturation in vivo by perturbants of purine metabolism. Biol Reprod. 1987;36:431–7.

    Article  CAS  PubMed  Google Scholar 

  52. Eppig JJ. Maintenance of meiotic arrest and the induction of oocyte maturation in mouse oocyte-granulosa cell complexes developed in vitro from preantral follicles. Biol Reprod. 1991;45:824–30.

    Article  CAS  PubMed  Google Scholar 

  53. Wang S, Ning G, Chen X, Yang J, Ouyang H, Zhang H, Tai P, Mu X, Zhou B, Zhang M, et al. PDE5 modulates oocyte spontaneous maturation via cGMP-cAMP but not cGMP-PKG signaling. Front Biosci: J Virtual Libr. 2008;13:7087–95.

    Article  CAS  Google Scholar 

  54. Zhang W, Colman RW. Conserved amino acids in metal-binding motifs of PDE3A are involved in substrate and inhibitor binding. Blood. 2000;95:3380–6.

    CAS  PubMed  Google Scholar 

  55. Sheth SB, Brennan KJ, Biradavolu R, Colman RW. Isolation and regulation of the cGMP-inhibited cAMP phosphodiesterase in human erythroleukemia cells. Thromb Haemost. 1997;77:155–62.

    CAS  PubMed  Google Scholar 

  56. Bu S, Xie H, Tao Y, Wang J, Xia G. Nitric oxide influences the maturation of cumulus cell-enclosed mouse oocytes cultured in spontaneous maturation medium and hypoxanthine-supplemented medium through different signaling pathways. Mol Cell Endocrinol. 2004;223:85–93.

    Article  CAS  PubMed  Google Scholar 

  57. Rosenzweig A, Seidman CE. Atrial natriuretic factor and related peptide hormones. Annu Rev Biochem. 1991;60:229–55.

    Article  CAS  PubMed  Google Scholar 

  58. Hanafy KA, Krumenacker JS, Murad F. NO, nitrotyrosine, and cyclic GMP in signal transduction. Med Sci Monit: Int Med J Exp Clin Res. 2001;7:801–19.

    CAS  Google Scholar 

  59. LaPolt PS, Leung K, Ishimaru R, Tafoya MA, You-hsin Chen J. Roles of cyclic GMP in modulating ovarian functions. Reprod Biomed Online. 2003;6:15–23.

    Article  PubMed  Google Scholar 

  60. Steegers EA, Hollanders JM, Jongsma HW, Hein PR. Atrial natriuretic peptide and progesterone in ovarian follicular fluid. Gynecol Obstet Invest. 1990;29:185–7.

    Article  CAS  PubMed  Google Scholar 

  61. Bu S, Xia G, Tao Y, Lei L, Zhou B. Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol Cell Endocrinol. 2003;207:21–30.

    Article  CAS  PubMed  Google Scholar 

  62. Klein SL, Carnovale D, Burnett AL, Wallach EE, Zacur HA, Crone JK, Dawson VL, Nelson RJ, Dawson TM. Impaired ovulation in mice with targeted deletion of the neuronal isoform of nitric oxide synthase. Mol Med. 1998;4:658–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Yang JZ, Ajonuma LC, Rowlands DK, Tsang LL, Ho LS, Lam SY, Chen WY, Zhou CX, Chung YW, Cho CY, et al. The role of inducible nitric oxide synthase in gamete interaction and fertilization: a comparative study on knockout mice of three NOS isoforms. Cell Biol Int. 2005;29:785–91.

    Article  CAS  PubMed  Google Scholar 

  64. Pallares P, Garcia-Fernandez RA, Criado LM, Letelier CA, Esteban D, Fernandez-Toro JM, Flores JM, Gonzalez-Bulnes A. Disruption of the endothelial nitric oxide synthase gene affects ovulation, fertilization and early embryo survival in a knockout mouse model. Reproduction. 2008;136:573–9.

    Article  CAS  PubMed  Google Scholar 

  65. Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y, Shirakami G, Arai H, Saito Y, Kambayashi Y, Inouye K, et al. Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natriuretic peptide. Endocrinology. 1992;130:229–39.

    Article  CAS  PubMed  Google Scholar 

  66. Zhang Y, Hao X, Xiang X, Wei K, Xia G, Zhang M. Porcine natriuretic peptide type B (pNPPB) maintains mouse oocyte meiotic arrest via natriuretic peptide receptor 2 (NPR2) in cumulus cells. Mol Reprod Dev. 2014;81:462–9.

    Article  CAS  PubMed  Google Scholar 

  67. Huang H, Acuff CG, Steinhelper ME. Isolation, mapping, and regulated expression of the gene encoding mouse C-type natriuretic peptide. Am J Physiol. 1996;271:H1565–75.

    CAS  PubMed  Google Scholar 

  68. Koller KJ, Lowe DG, Bennett GL, Minamino N, Kangawa K, Matsuo H, Goeddel DV. Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science. 1991;252:120–3.

    Article  CAS  PubMed  Google Scholar 

  69. Jankowski M, Reis AM, Mukaddam-Daher S, Dam TV, Farookhi R, Gutkowska J. C-type natriuretic peptide and the guanylyl cyclase receptors in the rat ovary are modulated by the estrous cycle. Biol Reprod. 1997;56:59–66.

    Article  CAS  PubMed  Google Scholar 

  70. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  72. Richard S, Baltz JM. 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. 2014;90:137.

    Article  PubMed  CAS  Google Scholar 

  73. Norris RP, Freudzon L, Freudzon M, Hand AR, Mehlmann LM, Jaffe LA. A G(s)-linked receptor maintains meiotic arrest in mouse oocytes, but luteinizing hormone does not cause meiotic resumption by terminating receptor-G(s) signaling. Dev Biol. 2007;310:240–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul DL, Lampe PD, Jaffe LA. 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. 2008;135:3229–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kiyosu C, Tsuji T, Yamada K, Kajita S, Kunieda T. NPPC/NPR2 signaling is essential for oocyte meiotic arrest and cumulus oophorus formation during follicular development in the mouse ovary. Reproduction. 2012;144:187–93.

    Article  CAS  PubMed  Google Scholar 

  76. Franciosi F, Coticchio G, Lodde V, Tessaro I, Modina SC, Fadini R, Dal Canto M, Renzini MM, Albertini DF, Luciano AM. Natriuretic Peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol Reprod. 2014;91:61.

    Article  PubMed  CAS  Google Scholar 

  77. Ogawa Y, Itoh H, Yoshitake Y, Inoue M, Yoshimasa T, Serikawa T, Nakao K. Molecular cloning and chromosomal assignment of the mouse C-type natriuretic peptide (CNP) gene (Nppc): comparison with the human CNP gene (NPPC). Genomics. 1994;24:383–7.

    Article  CAS  PubMed  Google Scholar 

  78. Zhang W, Yang Y, Liu W, Chen Q, Wang H, Wang X, Zhang Y, Zhang M, Xia G. Brain natriuretic peptide and C-type natriuretic peptide maintain porcine oocyte meiotic arrest. J Cell Physiol. 2014.

    Google Scholar 

  79. Hiradate Y, Hoshino Y, Tanemura K, Sato E. C-type natriuretic peptide inhibits porcine oocyte meiotic resumption. Zygote. 2014;22:372–7.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Chang MS, Lowe DG, Lewis M, Hellmiss R, Chen E, Goeddel DV. Differential activation by atrial and brain natriuretic peptides of two different receptor guanylate cyclases. Nature. 1989;341:68–72.

    Article  CAS  PubMed  Google Scholar 

  82. Ponderato N, Crotti G, Turini P, Duchi R, Galli C, Lazzari G. Embryonic and foetal development of bovine oocytes treated with a combination of butyrolactone I and roscovitine in an enriched medium prior to IVM and IVF. Mol Reprod Dev. 2002;62:513–8.

    Article  CAS  PubMed  Google Scholar 

  83. Coy P, Romar R, Payton RR, McCann L, Saxton AM, Edwards JL. Maintenance of meiotic arrest in bovine oocytes using the S-enantiomer of roscovitine: effects on maturation, fertilization and subsequent embryo development in vitro. Reproduction. 2005;129:19–26.

    Article  CAS  PubMed  Google Scholar 

  84. Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev. 1996;17:121–55.

    Article  CAS  PubMed  Google Scholar 

  85. Zeleznik AJ. Dynamics of primate follicular growth: a physiological perspective. In: Leung PCK, Adashi EY, editors. The ovary. 2nd ed. Amsterdam: Elsevier Academic Press; 2004. p. 45–53, 71.

    Google Scholar 

  86. Kawamura K, Cheng Y, Kawamura N, Takae S, Okada A, Kawagoe Y, Mulders S, Terada Y, Hsueh AJ. 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.

    Article  CAS  PubMed  Google Scholar 

  87. Zhang M, Su YQ, Sugiura K, Wigglesworth K, Xia G, Eppig JJ. Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology. 2011;152:4377–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Lee KB, Zhang M, Sugiura K, Wigglesworth K, Uliasz T, Jaffe LA, Eppig JJ. Hormonal coordination of natriuretic peptide type C and natriuretic peptide receptor 3 expression in mouse granulosa cells. Biol Reprod. 2013;88:42.

    PubMed  Google Scholar 

  89. Richards JS. Perspective: the ovarian follicle—a perspective in 2001. Endocrinology. 2001;142:2184–93.

    Article  CAS  Google Scholar 

  90. Chen X, Zhou B, Yan J, Xu B, Tai P, Li J, Peng S, Zhang M, Xia G. 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.

    Article  CAS  PubMed  Google Scholar 

  91. Sato Y, Cheng Y, Kawamura K, Takae S, Hsueh AJ. C-type natriuretic peptide stimulates ovarian follicle development. Mol Endocrinol. 2012;26:1158–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Yu C, Zhang YL, Fan HY. Selective Smad4 knockout in ovarian preovulatory follicles results in multiple defects in ovulation. Mol Endocrinol. 2013;27:966–78.

    Article  CAS  PubMed  Google Scholar 

  93. Bar-Ami S, Nimrod A, Brodie AM, Tsafriri A. Role of FSH and oestradiol-17 beta in the development of meiotic competence in rat oocytes. J Steroid Biochem. 1983;19:965–71.

    Article  CAS  PubMed  Google Scholar 

  94. Davis SR, Burger HG, Robertson DM, Farnworth PG, Carson RS, Krozowski Z. Pregnant mare’s serum gonadotropin stimulates inhibin subunit gene expression in the immature rat ovary: dose response characteristics and relationships to serum gonadotropins, inhibin, and ovarian steroid content. Endocrinology. 1988;123:2399–407.

    Article  CAS  PubMed  Google Scholar 

  95. Leveille MC, Armstrong DT. Preimplantation embryo development and serum steroid levels in immature rats induced to ovulate or superovulate with pregnant mares’ serum gonadotropin injection or follicle-stimulating hormone infusions. Gamete Res. 1989;23:127–38.

    Article  CAS  PubMed  Google Scholar 

  96. Noubani A, Farookhi R, Gutkowska J. B-type natriuretic peptide receptor expression and activity are hormonally regulated in rat ovarian cells. Endocrinology. 2000;141:551–9.

    Article  CAS  Google Scholar 

  97. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A. 1998;95:15677–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Schomberg DW, Couse JF, Mukherjee A, Lubahn DB, Sar M, Mayo KE, Korach KS. Targeted disruption of the estrogen receptor-alpha gene in female mice: characterization of ovarian responses and phenotype in the adult. Endocrinology. 1999;140:2733–44.

    Article  CAS  PubMed  Google Scholar 

  99. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development. 2000;127:4277–91.

    CAS  PubMed  Google Scholar 

  100. Britt KL, Drummond AE, Dyson M, Wreford NG, Jones ME, Simpson ER, Findlay JK. The ovarian phenotype of the aromatase knockout (ArKO) mouse. J Steroid Biochem Mol Biol. 2001;79:181–5.

    Article  CAS  PubMed  Google Scholar 

  101. Huynh K, Jones G, Thouas G, Britt KL, Simpson ER, Jones ME. Estrogen is not directly required for oocyte developmental competence. Biol Reprod. 2004;70:1263–9.

    Article  CAS  PubMed  Google Scholar 

  102. Diaz FJ, Wigglesworth K, Eppig JJ. Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci. 2007;120:1330–40.

    Article  CAS  PubMed  Google Scholar 

  103. Su YQ, Sugiura K, Eppig JJ. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med. 2009;27:32–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Vanderhyden BC, Cohen JN, Morley P. Mouse oocytes regulate granulosa cell steroidogenesis. Endocrinology. 1993;133:423–6.

    Article  CAS  PubMed  Google Scholar 

  105. Vanderhyden BC, Macdonald EA. Mouse oocytes regulate granulosa cell steroidogenesis throughout follicular development. Biol Reprod. 1998;59:1296–301.

    Article  CAS  PubMed  Google Scholar 

  106. Dragovic RA, Ritter LJ, Schulz SJ, Amato F, Thompson JG, Armstrong DT, Gilchrist RB. Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod. 2007;76:848–57.

    Article  CAS  PubMed  Google Scholar 

  107. Wigglesworth K, Lee KB, O’Brien MJ, Peng J, Matzuk MM, Eppig JJ. Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. Proc Natl Acad Sci U S A. 2013;110:E3723–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Jaffe LANR. Initiation of the meiotic prophase-to-metaphase transition in mammalian oocytes. Chichester: Wiley; 2010.

    Google Scholar 

  109. Hunzicker-Dunn M, Mayo K. Gonadotropin signaling in the ovary. In: Neill JD, editor. Knobil and Neill’s physiology of reproduction. 3rd ed. San Diego: Elsevier/Academic Press; 2006. p. 547–92.

    Chapter  Google Scholar 

  110. Schultz RM, Montgomery RR, Belanoff JR. Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol. 1983;97:264–73.

    Article  CAS  PubMed  Google Scholar 

  111. Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW, Conti M. Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol. 2007;27:1914–24.

    Article  CAS  PubMed  Google Scholar 

  112. Eppig JJ, Downs SM. Chemical signals that regulate mammalian oocyte maturation. Biol Reprod. 1984;30:1–11.

    Article  CAS  PubMed  Google Scholar 

  113. Sela-Abramovich S, Edry I, Galiani D, Nevo N, Dekel N. Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation. Endocrinology. 2006;147:2280–6.

    Article  CAS  PubMed  Google Scholar 

  114. Mehlmann LM, Kalinowski RR, Ross LF, Parlow AF, Hewlett EL, Jaffe LA. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Beyer EC, Kistler J, Paul DL, Goodenough DA. Antisera directed against connexin43 peptides react with a 43-kD protein localized to gap junctions in myocardium and other tissues. J Cell Biol. 1989;108:595–605.

    Article  CAS  PubMed  Google Scholar 

  116. Simon AM, Goodenough DA, Li E, Paul DL. Female infertility in mice lacking connexin 37. Nature. 1997;385:525–9.

    Article  CAS  PubMed  Google Scholar 

  117. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Andric N, Thomas M, Ascoli M. Transactivation of the epidermal growth factor receptor is involved in the lutropin receptor-mediated down-regulation of ovarian aromatase expression in vivo. Mol Endocrinol. 2010;24:552–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Motlik J, Fulka J, Flechon JE. Changes in intercellular coupling between pig oocytes and cumulus cells during maturation in vivo and in vitro. J Reprod Fertil. 1986;76:31–7.

    Article  CAS  PubMed  Google Scholar 

  120. Patwardhan VV, Lanthier A. Cyclic GMP phosphodiesterase and guanylate cyclase activities in rabbit ovaries and the effect of in-vivo stimulation with LH. J Endocrinol. 1984;101:305–10.

    Article  CAS  PubMed  Google Scholar 

  121. Conti M, Kasson BG, Hsueh AJ. Hormonal regulation of 3’,5’-adenosine monophosphate phosphodiesterases in cultured rat granulosa cells. Endocrinology. 1984;114:2361–8.

    Article  CAS  PubMed  Google Scholar 

  122. Liu X, Xie F, Zamah AM, Cao B, Conti M. CORRECTION: multiple pathways mediate luteinizing hormone regulation of cGMP signaling in the mouse ovarian follicle. Biol Reprod. 2014.

    Google Scholar 

  123. McRae RS, Johnston HM, Mihm M, O’Shaughnessy PJ. Changes in mouse granulosa cell gene expression during early luteinization. Endocrinology. 2005;146:309–17.

    Article  CAS  PubMed  Google Scholar 

  124. Andric N, Ascoli M. A delayed gonadotropin-dependent and growth factor-mediated activation of the extracellular signal-regulated kinase 1/2 cascade negatively regulates aromatase expression in granulosa cells. Mol Endocrinol. 2006;20:3308–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Su YQ, Nyegaard M, Overgaard MT, Qiao J, Giudice LC. Participation of mitogen-activated protein kinase in luteinizing hormone-induced differential regulation of steroidogenesis and steroidogenic gene expression in mural and cumulus granulosa cells of mouse preovulatory follicles. Biol Reprod. 2006;75:859–67.

    Article  CAS  PubMed  Google Scholar 

  126. Su YQ, Wigglesworth K, Pendola FL, O’Brien MJ, Eppig JJ. Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology. 2002;143:2221–32.

    Article  CAS  PubMed  Google Scholar 

  127. Hunt PJ, Richards AM, Espiner EA, Nicholls MG, Yandle TG. Bioactivity and metabolism of C-type natriuretic peptide in normal man. J Clin Endocrinol Metab. 1994;78:1428–35.

    CAS  PubMed  Google Scholar 

  128. Potter LR. Regulation and therapeutic targeting of peptide-activated receptor guanylyl cyclases. Pharmacol Ther. 2011;130:71–82.

    Article  CAS  PubMed  Google Scholar 

  129. Santiquet N, Papillon-Dion E, Djender N, Guillemette C, Richard FJ. New elements in the C-type natriuretic peptide signaling pathway inhibiting swine in vitro oocyte meiotic resumption. Biol Reprod. 2014;91:16.

    PubMed  Google Scholar 

  130. Abbey SE, Potter LR. Lysophosphatidic acid inhibits C-type natriuretic peptide activation of guanylyl cyclase-B. Endocrinology. 2003;144:240–6.

    Article  CAS  PubMed  Google Scholar 

  131. Abbey-Hosch SE, Cody AN, Potter LR. Sphingosine-1-phosphate inhibits C-type natriuretic peptide activation of guanylyl cyclase B (GC-B/NPR-B). Hypertension. 2004;43:1103–9.

    Article  CAS  PubMed  Google Scholar 

  132. Abbey-Hosch SE, Smirnov D, Potter LR. Differential regulation of NPR-B/GC-B by protein kinase c and calcium. Biochem Pharmacol. 2005;70:686–94.

    Article  CAS  PubMed  Google Scholar 

  133. Wang Y, Kong N, Li N, Hao X, Wei K, Xiang X, Xia G, Zhang M. Epidermal growth factor receptor signaling-dependent calcium elevation in cumulus cells is required for NPR2 inhibition and meiotic resumption in mouse oocytes. Endocrinology. 2013;154:3401–9.

    Article  CAS  PubMed  Google Scholar 

  134. Peng XR, Hsueh AJ, LaPolt PS, Bjersing L, Ny T. Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology. 1991;129:3200–7.

    Article  CAS  PubMed  Google Scholar 

  135. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science. 2004;303:682–4.

    Article  CAS  PubMed  Google Scholar 

  136. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Fan HY, Liu Z, Shimada M, Sterneck E, Johnson PF, Hedrick SM, Richards JS. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science. 2009;324:938–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Conti M, Hsieh M, Park JY, Su YQ. Role of the epidermal growth factor network in ovarian follicles. Mol Endocrinol. 2006;20:715–23.

    Article  CAS  PubMed  Google Scholar 

  140. Liu L, Kong N, Xia G, Zhang M. Molecular control of oocyte meiotic arrest and resumption. Reprod Fertil Dev. 2013;25:463–71.

    CAS  PubMed  Google Scholar 

  141. Farin CE, Rodriguez KF, Alexander JE, Hockney JE, Herrick JR, Kennedy-Stoskopf S. The role of transcription in EGF- and FSH-mediated oocyte maturation in vitro. Anim Reprod Sci. 2007;98:97–112.

    Article  CAS  PubMed  Google Scholar 

  142. Ning G, Ouyang H, Wang S, Chen X, Xu B, Yang J, Zhang H, Zhang M, Xia G. 3’,5’-cyclic adenosine monophosphate response element binding protein up-regulated cytochrome P450 lanosterol 14alpha-demethylase expression involved in follicle-stimulating hormone-induced mouse oocyte maturation. Mol Endocrinol. 2008;22:1682–94.

    Article  CAS  PubMed  Google Scholar 

  143. Chen J, Torcia S, Xie F, Lin CJ, Cakmak H, Franciosi F, Horner K, Onodera C, Song JS, Cedars MI, et al. Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nat Cell Biol. 2013;15:1415–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Li M, Liang CG, Xiong B, Xu BZ, Lin SL, Hou Y, Chen DY, Schatten H, Sun QY. PI3-kinase and mitogen-activated protein kinase in cumulus cells mediate EGF-induced meiotic resumption of porcine oocyte. Domest Anim Endocrinol. 2008;34:360–71.

    Article  CAS  PubMed  Google Scholar 

  145. Su YQ, Denegre JM, Wigglesworth K, Pendola FL, O’Brien MJ, Eppig JJ. 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. 2003;263:126–38.

    Article  CAS  PubMed  Google Scholar 

  146. Sun QY, Miao YL, Schatten H. Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle. 2009;8:2741–7.

    Article  CAS  PubMed  Google Scholar 

  147. Veldhuis JD. Mechanisms subserving hormone action in the ovary: role of calcium ions as assessed by steady state calcium exchange in cultured swine granulosa cells. Endocrinology. 1987;120:445–9.

    Article  CAS  PubMed  Google Scholar 

  148. Su YQ, Xia GL, Byskov AG, Fu GD, Yang CR. Protein kinase C and intracellular calcium are involved in follicle-stimulating hormone-mediated meiotic resumption of cumulus cell-enclosed porcine oocytes in hypoxanthine-supplemented medium. Mol Reprod Dev. 1999;53:51–8.

    Article  CAS  PubMed  Google Scholar 

  149. Chattopadhyay A, Vecchi M, Ji Q, Mernaugh R, Carpenter G. The role of individual SH2 domains in mediating association of phospholipase C-gamma1 with the activated EGF receptor. J Biol Chem. 1999;274:26091–7.

    Article  CAS  PubMed  Google Scholar 

  150. Abbey SE, Potter LR. Vasopressin-dependent inhibition of the C-type natriuretic peptide receptor, NPR-B/GC-B, requires elevated intracellular calcium concentrations. J Biol Chem. 2002;277:42423–30.

    Article  CAS  PubMed  Google Scholar 

  151. Salvador LM, Maizels E, Hales DB, Miyamoto E, Yamamoto H, Hunzicker-Dunn M. Acute signaling by the LH receptor is independent of protein kinase C activation. Endocrinology. 2002;143:2986–94.

    Article  CAS  PubMed  Google Scholar 

  152. Yamashita Y, Kawashima I, Yanai Y, Nishibori M, Richards JS, Shimada M. Hormone-induced expression of tumor necrosis factor alpha-converting enzyme/A disintegrin and metalloprotease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor. Endocrinology. 2007;148:6164–75.

    Article  CAS  PubMed  Google Scholar 

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Zhang, M. (2017). A New Understanding on the Regulation of Oocyte Meiotic Prophase Arrest and Resumption. In: Chian, RC., Nargund, G., Huang, J. (eds) Development of In Vitro Maturation for Human Oocytes. Springer, Cham. https://doi.org/10.1007/978-3-319-53454-1_3

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