1932

Abstract

Meiotic progression in mammalian preovulatory follicles is controlled by the granulosa cells around the oocyte. Cyclic GMP (cGMP) generated in the granulosa cells diffuses through gap junctions into the oocyte, maintaining meiotic prophase arrest. Luteinizing hormone then acts on receptors in outer granulosa cells to rapidly decrease cGMP. This occurs by two complementary pathways: cGMP production is decreased by dephosphorylation and inactivation of the NPR2 guanylyl cyclase, and cGMP hydrolysis is increased by activation of the PDE5 phosphodiesterase. The cGMP decrease in the granulosa cells results in rapid cGMP diffusion out of the oocyte, initiating meiotic resumption. Additional, more slowly developing mechanisms involving paracrine signaling by extracellular peptides (C-type natriuretic peptide and EGF receptor ligands) maintain the low level of cGMP in the oocyte. These coordinated signaling pathways ensure a fail-safe system to prepare the oocyte for fertilization and reproductive success.

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2017-02-10
2024-06-19
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Literature Cited

  1. Eppig JJ, Viveiros MM, Marin-Bivens C, De La Fuente R. 1.  2004. Regulation of mammalian oocyte maturation. The Ovary PCK Leung, EY Adashi 113–29 San Diego, CA: Elsevier/Academic, 2nd ed.. [Google Scholar]
  2. Conti M, Hsieh M, Zamah AM, Oh JS. 2.  2012. Novel signaling mechanisms during oocyte maturation and ovulation. Mol. Cell. Endocrinol. 356:65–73 [Google Scholar]
  3. Clift D, Schuh M. 3.  2013. Restarting life: fertilization and the transition from meiosis to mitosis. Nat. Rev. Mol. Cell Biol. 14:549–62 [Google Scholar]
  4. Holt JE, Lane SIR, Jones KT. 4.  2013. The control of meiotic maturation in mammalian oocytes. Curr. Top. Dev. Biol. 102:207–26 [Google Scholar]
  5. Adhikari D, Liu K. 5.  2014. The regulation of maturation promoting factor during prophase I arrest and meiotic entry in mammalian oocytes. Mol. Cell. Endocrinol. 382:480–87 [Google Scholar]
  6. Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM. 6.  et al. 2008. Luteinizing hormone causes MAPK-dependent phosphorylation and closure of Cx43 gap junctions in mouse ovarian follicles: one of two paths to meiotic resumption. Development 135:3229–38 [Google Scholar]
  7. Anderson E, Wilkinson RF, Lee G, Meller S. 7.  1978. A correlative microscopical analysis of differentiating ovarian follicles of mammals. J. Morphol. 156:339–66 [Google Scholar]
  8. Anderson E, Albertini DF. 8.  1976. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J. Cell Biol. 71:680–86 [Google Scholar]
  9. Simon AM, Goodenough DA, Li E, Paul DL. 9.  1997. Female infertility in mice lacking connexin 37. Nature 385:525–29 [Google Scholar]
  10. Li TY, Colley D, Barr KJ, Yee S-P, Kidder GM. 10.  2007. Rescue of oogenesis in Cx37-null mutant mice by oocyte-specific replacement with Cx43. J. Cell Sci. 120:4117–25 [Google Scholar]
  11. Gittens JE, Kidder GM. 11.  2005. Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries. J. Cell Sci. 118:5071–78 [Google Scholar]
  12. Simon AM, Chen H, Jackson CL. 12.  2006. Cx37 and Cx43 localize to zona pellucida in mouse ovarian follicles. Cell Commun. Adhes. 13:61–77 [Google Scholar]
  13. Lipner H, Cross NL. 13.  1968. Morphology of the membrana granulosa of the ovarian follicle. Endocrinology 82:638–41 [Google Scholar]
  14. Amsterdam A, Koch Y, Lieberman ME, Linder HR. 14.  1975. Distribution of binding sites for human chorionic gonadotropin in the preovulatory follicle of the rat. J. Cell. Biol. 67:894–900 [Google Scholar]
  15. Bächler M, Menshykau D, De Geyter C, Iber D. 15.  2014. Species-specific differences in follicular antral sizes result from diffusion-based limitations on the thickness of the granulosa cell layer. Mol. Hum. Reprod. 20:208–21 [Google Scholar]
  16. Griffin J, Emery BR, Huang I, Peterson CM, Carrell DT. 16.  2006. Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human). J. Exp. Clin. Assist. Reprod. 3:2 [Google Scholar]
  17. Edwards RG, Gates AH. 17.  1959. Timing of the stages of the maturation divisions, ovulation, fertilization and the first cleavage of eggs of adult mice treated with gonadotrophins. J. Endocrinol. 18:292–304 [Google Scholar]
  18. Motlík J, Fulka J. 18.  1976. Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. J. Exp. Zool. 198:155–62 [Google Scholar]
  19. Seibel MM, Smith DM, Levesque L, Borten M, Taymor ML. 19.  1982. The temporal relationship between the luteinizing hormone surge and human oocyte maturation. Am. J. Obstet. Gynecol. 142:568–72 [Google Scholar]
  20. Chesnel F, Eppig JJ. 20.  1995. Synthesis and accumulation of p34cdc2 and cyclin B in mouse oocytes during acquisition of competence to resume meiosis. Mol. Reprod. Dev. 40:503–8 [Google Scholar]
  21. de Vantéry C, Stutz A, Vassalli JD, Schorderet-Slatkine S. 21.  1997. Acquisition of meiotic competence in growing mouse oocytes is controlled at both translational and posttranslational levels. Dev. Biol. 187:43–54 [Google Scholar]
  22. Nishimura T, Shimaoka T, Kano K, Naito K. 22.  2009. Insufficient amount of Cdc2 and continuous activation of Wee1 B are the cause of meiotic failure in porcine growing oocytes. J. Reprod. Dev. 55:553–57 [Google Scholar]
  23. Adhikari D, Zheng W, Shen Y, Gorre N, Ning Y. 23.  et al. 2012. Cdk1, but not Cdk2, is the sole Cdk that is essential and sufficient to drive resumption of meiosis in mouse oocytes. Hum. Mol. Genet. 21:2476–84 [Google Scholar]
  24. Lénárt P, Rabut G, Daigle N, Hand AR, Terasaki M, Ellenberg J. 24.  2003. Nuclear envelope breakdown in starfish oocytes proceeds by partial NPC disassembly followed by a rapidly spreading fenestration of nuclear membranes. J. Cell Biol. 160:1055–68 [Google Scholar]
  25. Abe S, Nagasaka K, Hirayama Y, Kozuka-Hata H, Oyama M. 25.  et al. 2011. The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II. Genes Dev 25:863–74 [Google Scholar]
  26. Pincus G, Enzmann EV. 26.  1935. The comparative behavior of mammalian eggs in vivo and in vitro. J. Exp. Med. 62:665–75 [Google Scholar]
  27. Edwards RG. 27.  1965. Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208:349–51 [Google Scholar]
  28. Erickson GF, Sorensen RA. 28.  1974. In vitro maturation of mouse oocytes isolated from late, middle, and pre-antral Graafian follicles. J. Exp. Zool. 190:123–27 [Google Scholar]
  29. Piontkewitz Y, Dekel N. 29.  1993. Heptanol, an alkanol that blocks gap junctions, induces oocyte maturation. Endocr. J. 1:365–72 [Google Scholar]
  30. Sela-Abramovich S, Edry I, Galiani D, Nevo N, Dekel N. 30.  2006. Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation. Endocrinology 147:2280–86 [Google Scholar]
  31. Richard S, Baltz JM. 31.  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. 90:6137 [Google Scholar]
  32. Tsafriri A, Pomerantz SH, Channing CP. 32.  1976. Inhibition of oocyte maturation by porcine follicular fluid: partial characterization of the inhibitor. Biol. Reprod. 14:511–16 [Google Scholar]
  33. Cho WK, Stern S, Biggers JD. 33.  1974. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J. Exp. Zool. 187:383–86 [Google Scholar]
  34. Magnusson C, Hillensjö T. 34.  1977. Inhibition of maturation and metabolism in rat oocytes by cyclic AMP. J. Exp. Zool. 201:139–47 [Google Scholar]
  35. Bornslaeger EA, Schultz RM. 35.  1985. Adenylate cyclase in zona-free mouse oocytes. Exp. Cell Res. 156:277–81 [Google Scholar]
  36. Mehlmann LM, Jones TLZ, Jaffe LA. 36.  2002. Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science 297:1343–45 [Google Scholar]
  37. Kalinowski RR, Berlot CH, Jones TLZ, Ross LF, Jaffe LA, Mehlmann LM. 37.  2004. Maintenance of meiotic prophase arrest in vertebrate oocytes by a Gs protein-mediated pathway. Dev. Biol. 267:1–13 [Google Scholar]
  38. Gallo CJ, Hand AR, Jones TLZ, Jaffe LA. 38.  1995. Stimulation of Xenopus oocyte maturation by inhibition of the G-protein alpha S subunit, a component of the plasma membrane and yolk platelet membranes. J. Cell Biol. 130:275–84 [Google Scholar]
  39. DiLuigi A, Weitzman VN, Pace MC, Siano LJ, Maier D, Mehlmann LM. 39.  2008. Meiotic arrest in human oocytes is maintained by a Gs signaling pathway. Biol. Reprod. 78:667–72 [Google Scholar]
  40. Mehlmann LM, Saeki Y, Tanaka S, Brennan TJ, Evsikov AV. 40.  et al. 2004. The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306:1947–50 [Google Scholar]
  41. Eggerickx D, Denef J-F, Labbe O, Hayashi Y, Refetoff S. 41.  et al. 1995. Molecular cloning of an orphan G-protein-coupled receptor that constitutively activates adenylate cyclase. Biochem. J. 309:837–43 [Google Scholar]
  42. Freudzon L, Norris RP, Hand AR, Tanaka S, Saeki Y. 42.  et al. 2005. Regulation of meiotic prophase arrest in mouse oocytes by GPR3, a constitutive activator of the Gs G protein. J. Cell Biol. 171:255–65 [Google Scholar]
  43. Ledent C, Demeestere I, Blum D, Petermans J, Hamalainen T. 43.  et al. 2005. Premature ovarian aging in mice deficient for Gpr3. PNAS 102:8922–26 [Google Scholar]
  44. Mehlmann LM. 44.  2005. Oocyte-specific expression of Gpr3 is required for the maintenance of meiotic arrest in mouse oocytes. Dev. Biol. 288:397–404 [Google Scholar]
  45. Yang C-R, Wei Y, Qi S-T, Chen L, Zhang Q-H. 45.  et al. 2012. The G protein coupled receptor 3 is involved in cAMP and cGMP signaling and maintenance of meiotic arrest in porcine oocytes. PLOS ONE 7:e38807 [Google Scholar]
  46. Hinckley M, Vaccari S, Horner K, Chen R, Conti M. 46.  2005. The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Dev. Biol. 287:249–61 [Google Scholar]
  47. Horner K, Livera G, Hinckley M, Trinh K, Storm D, Conti M. 47.  2003. Rodent oocytes express an active adenylyl cyclase required for meiotic arrest. Dev. Biol. 258:385–96 [Google Scholar]
  48. Bornslaeger EA, Mattei P, Schultz RM. 48.  1986. Involvement of cAMP-dependent protein kinase and protein phosphorylation in regulation of mouse oocyte maturation. Dev. Biol. 114:453–62 [Google Scholar]
  49. Han SJ, Chen R, Paronetto MP, Conti M. 49.  2005. Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr. Biol. 15:1670–76 [Google Scholar]
  50. Duckworth BC, Weaver JS, Ruderman JV. 50.  2002. G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. PNAS 99:16794–99 [Google Scholar]
  51. Pirino G, Wescott MP, Donovan PJ. 51.  2009. Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle 8:665–70 [Google Scholar]
  52. Dupré A, Daldello EM, Nairn AC, Jessus C, Haccard O. 52.  2014. Phosphorylation of ARPP19 by protein kinase A prevents meiosis resumption in Xenopus oocytes. Nat. Commun. 5:3318 [Google Scholar]
  53. Schuh M, Ellenberg J. 53.  2007. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130:484–98 [Google Scholar]
  54. Mehlmann LM, Kline D. 54.  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. 51:1088–98 [Google Scholar]
  55. Kryzak CA, Moraine MM, Kyle DD, Lee HJ, Cubenas-Potts C. 55.  et al. 2013. Prophase I mouse oocytes are deficient in the ability to respond to fertilization by decreasing membrane receptivity to sperm and establishing a membrane block to polyspermy. Biol. Reprod. 89:44 [Google Scholar]
  56. Schultz RM, Montgomery RR, Belanoff JR. 56.  1983. Regulation of mouse oocyte meiotic maturation: Implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev. Biol. 97:264–73 [Google Scholar]
  57. Vivarelli E, Conti M, DeFelici M, Siracusa G. 57.  1983. Meiotic resumption and intracellular cAMP levels in mouse oocytes treated with compounds which act on cAMP metabolism. Cell Differ 12:271–76 [Google Scholar]
  58. Törnell J, Billig H, Hillensjö T. 58.  1990. 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. 139:511–17 [Google Scholar]
  59. Bornslaeger EA, Mattei P, Schultz RM. 59.  1984. Regulation of mouse oocyte maturation: involvement of cyclic AMP phosphodiesterase and calmodulin. Dev. Biol. 105:488–99 [Google Scholar]
  60. Törnell J, Billig H, Hillensjö T. 60.  1991. Regulation of oocyte maturation by changes in ovarian levels of cyclic nucleotides. Human. Reprod. 6:411–22 [Google Scholar]
  61. Tsafriri A, Chun S-Y, Zhang R, Hsueh AJW, Conti M. 61.  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 [Google Scholar]
  62. Masciarelli S, Horner K, Liu C, Park SH, Hinckley M. 62.  et al. 2004. Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J. Clin. Investig. 114:196–205 [Google Scholar]
  63. Vaccari S, Weeks JL, Hsieh M, Menniti FS, Conti M. 63.  2009. Cyclic GMP signaling is involved in the LH-dependent meiotic maturation of mouse oocytes. Biol. Reprod. 81:595–604 [Google Scholar]
  64. Bender AT, Beavo JA. 64.  2006. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol. Rev. 58:488–520 [Google Scholar]
  65. Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J. 65.  et al. 2009. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136:1869–78 [Google Scholar]
  66. Zhang M, Su Y-Q, Sugiura K, Xia G, Eppig JJ. 66.  2010. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330:366–69 [Google Scholar]
  67. Jankowski M, Reis AM, Mukaddam-Daher S, Dam T-V, Farookhi R, Gutkowska J. 67.  1997. C-type natriuretic peptide and the guanylyl cyclase receptors in the rat ovary are modulated by the estrous cycle. Biol. Reprod. 56:59–66 [Google Scholar]
  68. Zhang M, Su Y-Q, Sugiura K, Wigglesworth K, Xia G, Eppig JJ. 68.  2011. Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology 152:4377–85 [Google Scholar]
  69. Tsuji T, Kiyosu C, Akiyama K, Kunieda T. 69.  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 [Google Scholar]
  70. Shuhaibar LC, Egbert JR, Edmund AB, Uliasz TF, Dickey DM. 70.  et al. 2016. Dephosphorylation of juxtamembrane serines and threonines of the NPR2 guanylyl cyclase is required for rapid resumption of oocyte meiosis in response to luteinizing hormone. Dev. Biol. 409:194–201 [Google Scholar]
  71. Shuhaibar LC, Egbert JR, Norris RP, Lampe PD, Nikolaev VO. 71.  et al. 2015. Intercellular signaling via cyclic GMP diffusion through gap junctions in the mouse ovarian follicle. PNAS 112:5527–32 [Google Scholar]
  72. Geister KA, Brinkmeier ML, Hsieh M, Faust SM, Karolyi IJ. 72.  et al. 2013. A novel loss-of-function mutation in Npr2 clarifies primary role in female reproduction and reveals a potential therapy for acro-mesomelic dysplasia, Maroteaux type. Hum. Mol. Genet. 22:345–57 [Google Scholar]
  73. Khan S, Ali RH, Abbasi S, Nawaz M, Muhammad N, Ahmad W. 73.  2012. Novel mutations in natriuretic peptide receptor-2 gene underlie acromesomelic dysplasia, type maroteaux. BMC Med. Genet. 13:44 [Google Scholar]
  74. Kawamura K, Cheng Y, Kawamura N, Takae S, Okada A. 74.  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. 26:3094–101 [Google Scholar]
  75. Hiradate Y, Hoshino Y, Tanemura K, Sato E. 75.  2014. C-type natriuretic peptide inhibits porcine oocyte meiotic resumption. Zygote 22:372–77 [Google Scholar]
  76. Zhang W, Yang Y, Liu W, Chen Q, Wang H. 76.  et al. 2015. Brain natriuretic peptide and C-type natriuretic peptide maintain porcine oocyte meiotic arrest. J. Cell. Physiol. 230:71–81 [Google Scholar]
  77. Franciosi F, Coticchio G, Lodde V, Tessaro I, Modina SC. 77.  et al. 2014. Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol. Reprod. 91:3611–9 [Google Scholar]
  78. Zhong Y, Lin J, Liu X, Hou J, Zhang Y, Zhao X. 78.  2016. C-type natriuretic peptide maintains domestic cat oocytes in meiotic arrest. Reprod. Fert. Develop. 28:1553–59 [Google Scholar]
  79. Potter LR. 79.  2011. Regulation and therapeutic targeting of peptide-activated receptor guanylyl cyclases. Pharmacol. Ther. 130:71–82 [Google Scholar]
  80. Racowsky C, Baldwin KV. 80.  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 [Google Scholar]
  81. Downs SM, Eppig JJ. 81.  1987. Induction of mouse oocyte maturation in vivo by perturbants of purine metabolism. Biol. Reprod. 36:431–37 [Google Scholar]
  82. Wigglesworth K, Lee K-B, O'Brien MJ, Peng J, Matzuk MM, Eppig JJ. 82.  2013. Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. PNAS 110:E3723–29 [Google Scholar]
  83. Kozhemyakina E, Lassar AB, Zelzer E. 83.  2015. A pathway to bone: signaling molecules and transcription factors involved in chondrocyte development and maturation. Development 142:817–31 [Google Scholar]
  84. Bortolussi M, Marini G, Dal Lago A. 84.  1977. Autoradiographic study of the distribution of LH(HCG) receptors in the ovary of untreated and gonadotrophin-primed immature rats. Cell Tissue Res 183:329–42 [Google Scholar]
  85. Bortolussi M, Marini G, Reolon ML. 85.  1979. A histochemical study of binding of 125I-HCG to the rat ovary throughout the estrus cycle. Cell Tissue Res 197:213–26 [Google Scholar]
  86. Channing CP, Bae I-H, Stone SL, Anderson LD, Edelson S, Fowler SC. 86.  1981. Porcine granulosa and cumulus cell properties. LH/hCG receptors, ability to secrete progesterone and ability to respond to LH. Mol. Cell. Endocrinol. 22:359–70 [Google Scholar]
  87. Wang X, Greenwald GS. 87.  1993. Hypophysectomy of the cyclic mouse. II. Effects of follicle-stimulating hormone (FSH) and luteinizing hormone on folliculogenesis, FSH and human chorionic gonadotropin receptors, and steroidogenesis. Biol. Reprod. 48:595–605 [Google Scholar]
  88. Eppig JJ, Wigglesworth K, Pendola F, Hirao Y. 88.  1997. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol. Reprod. 56:976–84 [Google Scholar]
  89. Eppig JJ, Wigglesworth K, Pendola F. 89.  2002. The mammalian oocyte orchestrates the rate of ovarian follicular development. PNAS 99:2890–94 [Google Scholar]
  90. Jeppesen JV, Kristensen SG, Nielsen ME, Humaidan P, Dal Canto M. 90.  et al. 2012. LH-receptor gene expression in human granulosa and cumulus cells from antral and preovulatory follicles. J. Clin. Endocrinol. Metab. 97:E1524–31 [Google Scholar]
  91. Richards JS, Midgley AR. 91.  1976. Protein hormone action: a key to understanding ovarian follicular and luteal cell development. Biol. Reprod. 14:82–94 [Google Scholar]
  92. Eppig JJ. 92.  1991. Maintenance of meiotic arrest and the induction of oocyte maturation in mouse oocyte-granulosa cell complexes developed in vitro from preantral follicles. Biol. Reprod. 45:824–30 [Google Scholar]
  93. Nagahama Y, Yamashita M. 93.  2008. Regulation of oocyte maturation in fish. Dev. Growth Differ. 50:Suppl. 1S195–219 [Google Scholar]
  94. Haccard O, Dupré A, Liere P, Pianos A, Eychenne B. 94.  et al. 2012. Naturally occurring steroids in Xenopus oocyte during meiotic maturation. Unexpected presence and role of steroid sulfates. Mol. Cell. Endocrinol. 362:110–19 [Google Scholar]
  95. Tsafriri A, Motola S. 95.  2007. Are steroids dispensable for meiotic resumption in mammals?. Trends Endocrinol. Metab. 18:321–27 [Google Scholar]
  96. Norris RP, Freudzon L, Freudzon M, Hand AR, Mehlmann LM, Jaffe LA. 96.  2007. A Gs-linked receptor maintains meiotic arrest in mouse oocytes, but luteinizing hormone does not cause meiotic resumption by terminating receptor-Gs signaling. Dev. Biol. 310:240–49 [Google Scholar]
  97. Mehlmann LM, Kalinowski RR, Ross LF, Parlow AF, Hewlett EL, Jaffe LA. 97.  2006. Meiotic resumption in response to luteinizing hormone is independent of a Gi family G protein or calcium in the mouse oocyte. Dev. Biol. 299:345–55 [Google Scholar]
  98. Shilling F, Chiba K, Hoshi M, Kishimoto T, Jaffe LA. 98.  1989. Pertussis toxin inhibits 1-methyladenine-induced maturation in starfish oocytes. Dev. Biol. 133:605–8 [Google Scholar]
  99. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. 99.  2004. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682–84 [Google Scholar]
  100. Hunzicker-Dunn M, Mayo K. 100.  2015. Gonadotropin signaling in the ovary. Knobil and Neill's Physiology of Reproduction TM Plant, AJ Zeleznik 895–945 San Diego, CA: Academic, 4th ed.. [Google Scholar]
  101. Hubbard CJ. 101.  1986. Cyclic AMP changes in the component cells of Graafian follicles: possible influences on maturation in the follicle-enclosed oocytes of hamsters. Dev. Biol. 118:343–51 [Google Scholar]
  102. Ratner A. 102.  1976. Effects of follicle stimulating hormone and luteinizing hormone upon cyclic AMP and cyclic GMP levels in rat ovaries in vitro. Endocrinology 99:1496–500 [Google Scholar]
  103. Egbert JR, Shuhaibar LC, Edmund AB, Van Helden DA, Robinson JW. 103.  et al. 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 141:3594–604 [Google Scholar]
  104. Liu X, Xie F, Zamah AM, Cao B, Conti M. 104.  2014. Multiple pathways mediate luteinizing hormone regulation of cGMP signaling in the mouse ovarian follicle. Biol. Reprod. 91:191–11 [Google Scholar]
  105. Norris RP, Freudzon M, Nikolaev VO, Jaffe LA. 105.  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 140:655–62 [Google Scholar]
  106. Patwardhan VV, Lanthier A. 106.  1984. Cyclic GMP phosphodiesterase and guanylate cyclase activities in rabbit ovaries and the effect of in-vivo stimulation with LH. J. Endocrinol. 101:305–10 [Google Scholar]
  107. Patwardhan VV, Lanthier A. 107.  1987. Ovarian cyclic GMP concentration and guanylate cyclase and cyclic GMP phosphodiesterase activities in proestrous rat after treatment with LH. Horm. Metabol. Res. 19:136–37 [Google Scholar]
  108. Robinson JW, Zhang M, Shuhaibar LC, Norris RP, Geerts A. 108.  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. 366:308–16 [Google Scholar]
  109. Egbert JR, Uliasz TF, Shuhaibar LC, Geerts A, Wunder F. 109.  et al. 2016. Luteinizing hormone causes phosphorylation and activation of the cyclic GMP phosphodiesterase PDE5 in rat ovarian follicles, contributing, together with PDE1 activity, to the resumption of meiosis. Biol. Reprod. 94:1101–11 [Google Scholar]
  110. Gilula NB, Epstein ML, Beers WH. 110.  1978. Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J. Cell Biol. 78:58–75 [Google Scholar]
  111. Eppig JJ. 111.  1982. The relationship between cumulus cell-oocyte coupling, oocyte meiotic maturation, and cumulus expansion. Dev. Biol. 89:268–72 [Google Scholar]
  112. Flynn MP, Maizels ET, Karlsson AB, McAvoy T, Ahn J-H. 112.  et al. 2008. Luteinizing hormone receptor activation in ovarian granulosa cells promotes protein kinase A-dependent dephosphorylation of microtubule-associated protein 2D. Mol. Endocrinol. 22:1695–710 [Google Scholar]
  113. Corbin JD, Turko IV, Beasley A, Francis SH. 113.  2000. Phosphorylation of phosphodiesterase-5 by cyclic nucleotide-dependent protein kinase alters its catalytic and allosteric cGMP-binding activities. Eur. J. Biochem. 267:2760–67 [Google Scholar]
  114. Rybalkin SD, Rybalkina IG, Feil R, Hofmann F, Beavo JA. 114.  2002. Regulation of cGMP-specific phosphodiesterase (PDE5) phosphorylation in smooth muscle cells. J. Biol. Chem. 277:3310–17 [Google Scholar]
  115. Hunzicker-Dunn M. 115.  1981. Selective activation of rabbit ovarian protein kinase isozymes in rabbit ovarian follicles and corpora lutea. J. Biol. Chem. 256:12185–93 [Google Scholar]
  116. Flores JA, Aguirre C, Sharma OP, Veldhuis JD. 116.  1998. Luteinizing hormone (LH) stimulates both intracellular calcium ion ([Ca2+]i) mobilization and transmembrane cation influx in single ovarian (granulosa) cells: Recruitment as a cellular mechanism of LH-[Ca2+]i dose response. Endocrinology 139:3606–12 [Google Scholar]
  117. Wang Y, Kong N, Li N, Hao X, Wei K. 117.  et al. 2013. Epidermal growth factor receptor signaling-dependent calcium elevation in cumulus cells is required for NPR2 inhibition and meiotic resumption in mouse oocytes. Endocrinology 154:3401–9 [Google Scholar]
  118. Lee K-B, Zhang M, Sugiura K, Wigglesworth K, Uliasz T. 118.  et al. 2013. Hormonal coordination of natriuretic peptide type C and natriuretic peptide receptor 3 expression in mouse granulosa cells. Biol. Reprod. 88:421–9 [Google Scholar]
  119. Sekiguchi T, Mizutani T, Yamada K, Kajitani T, Yazawa T. 119.  et al. 2004. Expression of epiregulin and amphiregulin in the rat ovary. J. Mol. Endocrinol. 33:281–91 [Google Scholar]
  120. Ashkenazi H, Cao X, Motola S, Popliker M, Conti M, Tsafriri A. 120.  2005. Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146:77–84 [Google Scholar]
  121. Zhang W, Chen Q, Yang Y, Liu W, Zhang M. 121.  et al. 2014. Epidermal growth factor-network signaling mediates luteinizing hormone regulation of BNP and CNP and their receptor NPR2 during porcine oocyte meiotic resumption. Mol. Reprod. Dev. 81:1030–41 [Google Scholar]
  122. Zamah AM, Hsieh M, Chen J, Vigne JL, Rosen MP. 122.  et al. 2010. Human oocyte maturation is dependent on LH-stimulated accumulation of the epidermal growth factor-like growth factor, amphiregulin. Hum. Reprod. 25:2569–78 [Google Scholar]
  123. Kovacs E, Zorn JA, Huang Y, Barros T, Kuriyan J. 123.  2015. A structural perspective on the regulation of the epidermal growth factor receptor. Annu. Rev. Biochem. 84:739–64 [Google Scholar]
  124. Panigone S, Hsieh M, Fu M, Persani L, Conti M. 124.  2008. LH signaling in preovulatory follicles involves early activation of the EGFR pathway. Mol. Endocrinol. 22:924–36 [Google Scholar]
  125. Hsieh M, Thao K, Conti M. 125.  2011. Genetic dissection of epidermal growth factor receptor signaling during luteinizing hormone-induced oocyte maturation. PLOS ONE 6:e21574 [Google Scholar]
  126. Dekel N, Sherizly I. 126.  1985. Epidermal growth factor induces maturation of rat follicle-enclosed oocytes. Endocrinology 116:406–9 [Google Scholar]
  127. Reizel Y, Elbaz J, Dekel N. 127.  2010. Sustained activity of the EGF receptor is an absolute requisite for LH-induced oocyte maturation and cumulus expansion. Mol. Endocrinol. 24:402–11 [Google Scholar]
  128. Hsieh M, Lee D, Panigone S, Horner K, Chen R. 128.  et al. 2007. Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol. Cell. Biol. 27:1914–24 [Google Scholar]
  129. Du X, Tabeta K, Hoebe K, Liu H, Mann N. 129.  et al. 2004. Velvet, a dominant Egfr mutation that causes wavy hair and defective eyelid development in mice. Genetics 166:331–40 [Google Scholar]
  130. Andric N, Thomas M, Ascoli M. 130.  2010. Transactivation of the epidermal growth factor receptor is involved in the lutropin receptor-mediated down-regulation of ovarian aromatase expression in vivo. Mol. Endocrinol. 24:552–60 [Google Scholar]
  131. Salvador LM, Maizels E, Hales DB, Miyamoto E, Yamamoto H, Hunzicker-Dunn M. 131.  2002. Acute signaling by the LH receptor is independent of protein kinase C activation. Endocrinology 143:2986–94 [Google Scholar]
  132. Fan H-Y, Liu Z, Shimada M, Sterneck E, Johnson PF. 132.  et al. 2009. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324:938–41 [Google Scholar]
  133. Larsen WJ, Wert SE, Brunner GD. 133.  1986. A dramatic loss of cumulus cell gap junctions is correlated with germinal vesicle breakdown in rat oocytes. Dev. Biol. 113:517–21 [Google Scholar]
  134. Larsen WJ, Wert SE, Brunner GD. 134.  1987. Differential modulation of rat follicle cell gap junction populations at ovulation. Dev. Biol. 122:61–71 [Google Scholar]
  135. Sela-Abramovich S, Chorev E, Galiani D, Dekel N. 135.  2005. Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocyte maturation in rat ovarian follicles. Endocrinology 146:1236–44 [Google Scholar]
  136. Lyga S, Volpe S, Werthmann RC, Götz K, Sungkaworn T. 136.  et al. 2016. Persistent cAMP signaling by internalized LH receptors in ovarian follicles. Endocrinology 157:1613–21 [Google Scholar]
  137. Herrlich A, Kühn B, Grosse R, Schmid A, Schultz G, Gudermann T. 137.  1996. Involvement of Gs and Gi proteins in dual coupling of the luteinizing hormone receptor to adenylyl cyclase and phospholipase C. J. Biol. Chem. 271:16764–72 [Google Scholar]
  138. Rajagopalan-Gupta RM, Lamm MLG, Mukherjee S, Rasenick MM, Hunzicker-Dunn M. 138.  1998. Luteinizing hormone/choriogonadotropin receptor-mediated activation of heterotrimeric guanine nucleotide binding proteins in ovarian follicular membranes. Endocrinology 139:4547–55 [Google Scholar]
  139. Tsafriri A, Lindner HR, Zor U, Lamprecht SA. 139.  1972. In-vitro induction of meiotic division in follicle-enclosed rat oocytes by LH, cyclic AMP and prostaglandin E2. J. Reprod. Fert. 31:39–50 [Google Scholar]
  140. Hunzicker-Dunn M. 140.  1981. Rabbit follicular adenylyl cyclase activity. I. Conditions of assay and gonadotropin sensitivity in granulosa cells and follicle shells. Biol. Reprod. 24:267–78 [Google Scholar]
  141. Hashimoto N, Kishimoto T, Nagahama Y. 141.  1985. Induction and inhibition of meiotic maturation in follicle-enclosed mouse oocytes by forskolin. Develop. Growth Differ. 27:709–16 [Google Scholar]
  142. Rodriguez KF, Couse JF, Jayes FL, Hamilton KJ, Burns KA. 142.  et al. 2010. Insufficient luteinizing hormone-induced intracellular signaling disrupts ovulation in preovulatory follicles lacking estrogen receptor-β. Endocrinology 151:2826–34 [Google Scholar]
  143. Bevans CG, Kordel M, Rhee SK, Harris AL. 143.  1998. Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J. Biol. Chem. 273:2808–16 [Google Scholar]
  144. Ponsioen B, van Zeijl L, Moolenaar WH, Jalink K. 144.  2007. Direct measurement of cyclic AMP diffusion and signaling through connexin43 gap junctional channels. Exp. Cell. Res. 313:415–23 [Google Scholar]
  145. Kanaporis G, Mese G, Valiuniene L, White TW, Brink PR, Valiunas V. 145.  2008. Gap junction channels exhibit connexin-specific permeability to cyclic nucleotides. J. Gen. Physiol. 131:293–305 [Google Scholar]
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