Hormonal control of mammalian oocyte meiosis at diplotene stage

Cellular and Molecular Life Sciences

Volumn 69, Issue 8, 2012, Pages 1279-1288

  Zhang, Meijia ^a   Xia, Guoliang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Cyclic nucleotides; Gonadotropin; Meiosis; Signal transduction

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC GMP; ESTRADIOL; FOLLITROPIN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 12; G PROTEIN COUPLED RECEPTOR 3; GONADOTROPIN; GUANINE NUCLEOTIDE BINDING PROTEIN; HORMONE; LUTEINIZING HORMONE; MESSENGER RNA; NATRIURETIC PEPTIDE RECEPTOR 2; NATRIURETIC PEPTIDE TYPE C; OOCYTE DERIVED PARACRINE FACTOR; PHOSPHODIESTERASE; PHOSPHODIESTERASE 3A; PROTEIN PRECURSOR; RECEPTOR; UNCLASSIFIED DRUG;

CELL GROWTH; CELL LEVEL; CELL MATURATION; CELL STIMULATION; CUMULUS CELL; DEVELOPMENTAL STAGE; DIPLOTENE STAGE; ENZYME ACTIVITY; ENZYME INHIBITION; GAP JUNCTION; GRANULOSA CELL; GROWTH INHIBITION; GROWTH REGULATION; HORMONE ACTION; HUMAN; HYDROLYSIS; MAMMAL CELL; MEIOSIS; NONHUMAN; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; PEPTIDE SYNTHESIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; ANIMAL; CYTOLOGY; FEMALE; MEIOTIC PROPHASE I; METABOLISM; OOCYTE;

MAMMALIA;

ANIMALS; CYCLIC AMP; CYCLIC GMP; FEMALE; HORMONES; HUMANS; MEIOTIC PROPHASE I; OOCYTES;

EID: 84860875584     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0867-3     Document Type: Review

References (109)

1. Eppig JJ, Vivieros MM, Marin-Bivens C, De La Fuente R (2004) Regulation of mammalian oocyte maturation. In: Leung PCK, Adashi EY (eds) The ovary. Elsevier Academic Press, Amsterdam, pp 113-129
2. Solc P, Schultz RM, Motlik J (2010) 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 16:654-664
3. Szybek K (1972) In vitro maturation of oocytes from sexually immature mice. J Endocrinol 54:527-528
4. Erickson GF, Sorensen RA (1974) In vitro maturation ofmouse oocytes isolated from late, middle, and pre-antral Graafian fol-licles. J Exp Zool 190:123-127
5. Sorensen RA, Wassarman PM (1976) Relationship between growth and meiotic maturation of mouse oocyte. Dev Biol 50:531-536
6. Ducibella T (1996) The cortical reaction and development of activation competence in mammalian oocytes. Hum Reprod Update 2:29-42 (Pubitemid 26135090)
7. 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 (Pubitemid 27037357)
8. Ducibella T (1998) Biochemical and cellular insights into the temporal window of normal fertilization. Theriogenology 49:53-65 (Pubitemid 28135783)
9. Dekel N (1995) Molecular control of meiosis. Trends Endocrin Met 6:165-169
10. 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
11. Edwards RG (1965) Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208:349-351
12. 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 (Pubitemid 41830089)
13. Tsafriri A, Pomerantz SH (1986) Oocyte maturation inhibitor. Clin Endocrinol Meta 15:157-170 (Pubitemid 16188949)
14. 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 (Pubitemid 19201050)
15. 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 (Pubitemid 39627861)
16. 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 (Pubitemid 41636762)
17. Richard FJ, Tsafriri A, Conti M (2001) Role of phosphodies-terase type 3Ain rat oocyte maturation. Biol Reprod 65:1444-1451 (Pubitemid 33031502)
18. 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
19. Vaccari S, Weeks JL 2nd, Hsieh M, Menniti FS, Conti M (2009) Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod 81:595-604
20. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ (2010) Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330:366-369
21. Cho WK, Stern S, Biggers JD (1974) Inhibitory effect of di-butyryl camp on mouse oocyte maturation in vitro. J Exp Zool 187:383-386
22. Hambleton R, Krall J, Tikishvili E, Honeggar M, Ahmad F, Manganiello VC, Movsesian MA (2005) Isoforms of cyclic nucleotide phosphodiesterase PDE3 and their contribution to cAMP hydrolytic activity in subcellular fractions of human myocardium. J Biol Chem 280:39168-39174 (Pubitemid 41713868)
23. Törnell J, Billig H, Hillensjo T (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 139:511-517 (Pubitemid 20249323)
24. Törnell J, Carlsson B, Billig H (1990) Atrial natriuretic peptide inhibits spontaneous rat oocyte maturation. Endocrinology 126:1504-1508 (Pubitemid 20095756)
25. Grøndahl C, Breinholt J, Wahl P, Murray A, Hansen TH, Faerge I, Stidsen CE, Raun K, Hegele-Hartung C (2003) Physiology of meiosis-activating sterol: endogenous formation and mode of action. Hum Reprod 18:122-129 (Pubitemid 36138862)
26. Schultz RM, Montgomery RR, Belanoff JR (1983) Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol 97:264-273
27. Eppig JJ, Ward-Bailey PF, Coleman DL (1985) Hypoxanthine and adenosine in murine ovarian follicular fluid: concentrations and activity in maintaining oocyte meiotic arrest. Biol Reprod 33:1041-1049 (Pubitemid 16184702)
28. Zhang M, Ouyang H, Xia G (2009) The signal pathway of gonadotrophins-induced mammalian oocyte meiotic resumption. Mol Hum Reprod 15:399-409
29. Tripathi A, Kumar KV, Chaube SK (2010) Meiotic cell cycle arrest in mammalian oocytes. J Cell Physiol 223:592-600
30. Anderson E, Albertini DF (1976) Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol 71:680
31. Bornslaeger EA, Schultz RM (1985) Regulation of mouse oocyte maturation: effect of elevating cumulus cell cAMP on oocyte cAMP levels. Biol Reprod 33:698-704 (Pubitemid 15247600)
32. Webb RJ, Marshall F, Swann K, Carroll J (2002) Follicle-stimulating hormone induces a gap junction-dependent dynamic change in [cAMP] and protein kinase A in mammalian oocytes. Dev Biol 246:441-454 (Pubitemid 34775359)
33. 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 (Pubitemid 34913171)
34. 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 (Pubitemid 36683137)
35. Mehlmann LM (2005) Oocyte-specific expression of Gpr3 is required for the maintenance of meiotic arrest in mouse oocytes. Dev Biol 288:397-404 (Pubitemid 41790751)
36. Freudzon L, Norris RP, Hand AR, Tanaka S, Saeki Y, Jones TL, Rasenick MM, Berlot CH, Mehlmann LM, Jaffe LA (2005) Regulation of meiotic prophase arrest in mouse oocytes by GPR3, a constitutive activator of the Gs G protein. J Cell Biol 171:255-265 (Pubitemid 41540018)
37. Ledent C, Demeestere I, Blum D, Petermans J, Hamalainen T, Smits G, Vassart G (2005) Premature ovarian aging in mice deficient for Gpr3. Proc Natl Acad Sci USA 102:8922-8926 (Pubitemid 40881054)
38. DiLuigi A, Weitzman VN, Pace MC, Siano LJ, Maier D, Me-hlmann LM (2008) Meiotic arrest in human oocytes is maintained by a Gs signaling pathway. Biol Reprod 78:667
39. Vaccari S, Horner K, Mehlmann LM, Conti M (2008) Genera-tion of mouse oocytes defective in cAMP synthesis and degradation: endogenous cyclic AMP is essential for meiotic arrest. Dev Biol 316:124-134
40. Tsafriri A, Chun SY, Zhang R, Hsueh AJW, Conti M (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 (Pubitemid 26365046)
41. Thomas RE, Armstrong DT, Gilchrist RB (2002) Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Dev Biol 244:215-225 (Pubitemid 34450638)
42. Masciarelli S, Horner K, Liu C, Park SH, Hinckley M, Hockman S, Nedachi T, Jin C, Conti M, Manganiello V (2004) Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest 114:196-205 (Pubitemid 39071624)
43. Downs SM, Eppig JJ (1986) The role of purines in the main-tenance of meiotic arrest in mouse oocytes. Tokai J Exp Clin Med 11:463-469 (Pubitemid 18074454)
44. Reinhardt RR, Chin E, Zhou J, Taira M, Murata T, Manganiello VC, Bondy CA (1995) Distinctive anatomical patterns of gene expression for cGMP-inhibited cyclic nucleotide phosphodies-terases. J Clin Invest 95:1528-1538
45. Wiersma A, Hirsch B, Tsafriri A, Hanssen RG, Van de Kant M, Kloosterboer HJ, Conti M, Hsueh AJ (1998) Phosphodiesterase 3 inhibitors suppress oocyte maturation and consequent preg-nancy without affecting ovulation and cyclicity in rodents. J Clin Invest 102:532-537 (Pubitemid 28376156)
46. Mayes MA, Sirard MA (2002) Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol Reprod 66:180-184 (Pubitemid 34020601)
47. Sasseville M, Côté N, Guillemette C, Richard FJ (2006) New insight into the role of phosphodiesterase 3A in porcine oocyte maturation. BMC Dev Biol 6:47
48. Hubbard CJ (1980) Ovarian cAMP and cGMP fluctuations in the hamster during the oestrous cycle. J Reprod Fertil 59:351-355 (Pubitemid 10012866)
49. Downs SM, Eppig JJ (1987) Induction of mouse oocyte matu-ration in vivo by perturbants of purine metabolism. Biol Reprod 36:431-437 (Pubitemid 17062217)
50. Eppig JJ (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 45:824-830
51. Wang S, Ning G, Chen X, Yang J, Ouyang H, Zhang H, Tai P, Mu X, Zhou B, Zhang M, Xia G (2008) PDE5 modulates oocyte spontaneous maturation via cGMP-cAMP but not cGMP-PKG signaling. Front Biosci 13:7087-7095
52. Zhang W, Colman RW (2000) Conserved amino acids in metal-binding motifs of PDE3A are involved in substrate and inhibitor binding. Blood 95:3380-3386 (Pubitemid 30428467)
53. Bu S, Xie H, Tao Y, Wang J, Xia G (2004) Nitric oxide influ-ences the maturation of cumulus cell-enclosed mouse oocytes cultured in spontaneous maturation medium and hypoxanthine-supplemented medium through different signaling pathways. Mol Cell Endocrinol 223:85-93 (Pubitemid 38992913)
54. Hanafy KA, Krumenacker JS, Murad F (2001) NO, nitrotyro-sine, and cyclic GMP in signal transduction. Med Sci Monit 7:801-819 (Pubitemid 32691766)
55. Rosenzweig A, Seidman CE (1991) Atrial natriuretic factor and related peptide hormones. Annu Rev Biochem 60:229-255
56. Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y, Shira-kami G, Arai H, Saito Y, Kambayashi Y, Inouye K, Imura H (1992) Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natri-uretic peptide. Endocrinology 130:229-239
57. Koller KJ, Lowe DG, Bennett GL, Minamino N, Kangawa K, Matsuo H, Goeddel DV (1991) Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science 252:120-123 (Pubitemid 21916951)
58. Jankowski M, Reis AM, MukaddamDaher S, Dam TV, Farookhi R, Gutkowska J (1997) C-type natriuretic peptide and the gua-nylyl cyclase receptors in the rat ovary are modulated by the estrous cycle. Biol Reprod 56:59-66 (Pubitemid 27024162)
59. Norris RP, Freudzon L, Freudzon M, Hand AR, Mehlmann LM, Jaffe LA (2007) 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 310:240-249 (Pubitemid 47483672)
60. Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul DL, Lampe PD, Jaffe LA (2008) Luteinizing hor-mone 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
61. Tsafriri A, Dekel N, Barami S (1982) The role of oocyte mat-uration inhibitor in follicular regulation of oocyte maturation. J Reprod Fertil 64:541-551 (Pubitemid 12129850)
62. Ogawa Y, Itoh H, Yoshitake Y, Inoue M, Yoshimasa T, Serik-awa T, Nakao K (1994) Molecular cloning and chromosomal assignment of the mouse C-type natriuretic peptide (CNP) gene (Nppc): comparison with the human CNP gene (NPPC). Genomics 24:383-387
63. Downs SM, Coleman DL, Wardbailey PF, Eppig JJ (1985) Hypoxanthine is the principal inhibitor of murine oocyte mat-uration in a low-molecular weight fraction of porcine follicular-fluid. Proc Natl Acad Sci USA 82:454-458 (Pubitemid 15128285)
64. Ponderato N, Crotti G, Turini P, Duchi R, Galli C, Lazzari G (2002) 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 62:513-518 (Pubitemid 34745998)
65. Coy P, Romar R, Payton RR, McCann L, Saxton AM, Edwards JL (2005) Maintenance of meiotic arrest in bovine oocytes using the S-enantiomer of roscovitine: effects on maturation, fertil-ization and subsequent embryo development in vitro. Reproduction 129:19-26
66. Gougeon A (1996) Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev 17:121-155 (Pubitemid 26119956)
67. Zeleznik AJ (2004) Dynamics of primate follicular growth: a physiological perspective. In: Leung PCK, Adashi EY (eds) The ovary, 2nd edn. Elsevier Academic Press, Amsterdam, pp 45-53
68. Terranova PF, Rice VM (1997) Review: cytokine involvement in ovarian processes. Am J Reprod Immunol 37:50-63 (Pubitemid 27075968)
69. Demeestere I, Centner J, Gervy C, Englert Y, Delbaere A (2005) Impact of various endocrine and paracrine factors on in vitro culture ofpreantral follicles in rodents. Reproduction 130:147-156 (Pubitemid 41149802)
70. Noubani A, Farookhi R, Gutkowska J (2000) B-type natriuretic peptide receptor expression and activity are hormonally regu-lated in rat ovarian cells. Endocrinology 141:551-559 (Pubitemid 32250478)
71. Zhang M, Su YQ, Sugiura K, Wigglesworth K, Xia G, Eppig JJ (2011) Estradiol promotes and maintains cumulus cell expres-sion of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology (Epub ahead of print)
72. Licht P, Gallo AB, Aggarwal BB, Farmer SW, Castelino JB, Papkoff H (1979) Biological and binding activities of equine pituitary gonadotrophins and pregnant mare serum gonadotro-phin. J Endocrinol 83:311-322 (Pubitemid 10207523)
73. LaPolt PS, Leung K, Ishimaru R, Tafoya MA, You-hsin Chen J (2003) Roles of cyclic GMP in modulating ovarian functions. Reprod Biomed Online 6:15-23 (Pubitemid 36857114)
74. Gill A, Jamnongjit M, Hammes SR (2004) Androgens promote maturation and signaling in mouse oocytes independent of transcription: a release of inhibition model for mammalian oocyte meiosis. Mol Endocrinol 18:97-104 (Pubitemid 38073157)
75. Jamnongjit M, Gill A, Hammes SR (2005) Epidermal growth factor receptor signaling is required for normal ovarian steroi-dogenesis and oocyte maturation. Proc Natl Acad Sci USA 102:16257-16262 (Pubitemid 41688901)
76. Li M, Ai JS, Xu BZ, Xiong B, Yin S, Lin SL, Hou Y, Chen DY, Schatten H, Sun QY (2008) Testosterone potentially triggers meiotic resumption by activation of intra-oocyte SRC and MAPK in porcine oocytes. Biol Reprod 79:897-905
77. Motola S, Popliker M, Tsafriri A (2007) Are steroids obligatory mediators of luteinizing hormone/human chorionic gonadotro-pin-triggered resumption of meiosis in mammals? Endocrinology 148:4458-4465 (Pubitemid 47295709)
78. Tsafriri A, Motola S (2007) Are steroids dispensable for meiotic resumption in mammals? Trends Endocrinol Metab 18:321-327 (Pubitemid 47531958)
79. Diaz FJ, Wigglesworth K, Eppig JJ (2007) Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 120:1330-1340 (Pubitemid 46780026)
80. Su YQ, Sugiura K, Eppig JJ (2009) Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med 27:32-42
81. Richards JS, Russell DL, Ochsner S, Espey LL (2002) Ovula-tion: new dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol 64:69-92 (Pubitemid 34259226)
82. Hunzicker-Dunn M, Mayo K (2006) Gonadotropin signaling in the ovary. In: Neill JD (ed) Knobil and Neill's physiology of reproduction, 3rd edn. Elsevier/Academic Press, San Diego, pp 547-592
83. Hashimoto N, Kishimoto T, Nagahama Y (1985) Induction and inhibition of meiotic maturation in follicle-enclosed mouse oocytes by forskolin. Dev Growth Differ 27:709-716 (Pubitemid 16170666)
84. Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW, Conti M (2007) Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 27:1914-1924
85. Hunzicker-Dunn M (1981) Selective activation of rabbit ovarian protein kinase isozymes in rabbit ovarian follicles and corpora lutea. J Biol Chem 256:12185-12193 (Pubitemid 12140008)
86. 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 path-way. Mol Endocrinol 22:924-936 (Pubitemid 351482828)
87. Eppig JJ, Downs SM (1984) Chemical signals that regulate mammalian oocyte maturation. Biol Reprod 30:1-11 (Pubitemid 14153642)
88. 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
89. Mehlmann LM, Kalinowski RR, Ross LF, Hewlett EL, Jaffe LA (2006) Meiotic resumption in response to luteinizing hormone is independent of a Gi family G protein or calcium in the mouse oocyte. Dev Biol 299:345-355 (Pubitemid 44635444)
90. Hubbard CJ (1986) Cyclic AMP changes in the component cells of Graafian follicles: possible influences on maturation in the follicle-enclosed oocytes ofhamsters. Dev Biol 118:343-351 (Pubitemid 17212388)
91. Han SJ, Vaccari S, Nedachi T, Andersen CA, Kovacina KS, Roth RA, Conti M (2006) Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation. EMBO J 25:5716-5725 (Pubitemid 44967755)
92. Eppig JJ, Downs SM (1987) The effect of hypoxanthine on mouse oocyte growth and development in vitro: maintenance of meiotic arrest and gonadotropin-induced oocyte maturation. Dev Biol 119:313-321 (Pubitemid 17026440)
93. Kawamura K, Ye Y, Liang CG, Kawamura N, Gelpke MS, Rauch R, Tanaka T, Hsueh AJW (2009) Paracrine regulation of the resumption of oocyte meiosis by endothelin-1. Dev Biol 327:62-70
94. Park JY, Su YQ, 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 (Pubitemid 38141636)
95. Conti M, Hsieh M, Park JY, Su YQ (2006) Role of the epi-dermal growth factor network in ovarian follicles. Mol Endocrinol 20:715-723
96. Dekel N, Lawrence TS, Gilula NB, Beers WH (1981) Modu-lation of cell-to-cell communication in the cumulus-oocyte complex and the regulation of oocyte maturation by LH. Dev Biol 86:356-362
97. Salustri A, Siracusa G (1983) Metabolic coupling, cumulus expansion and meiotic resumption in mouse cumuli oophori cultured in vitro in the presence of FSH or dcAMP, or stimulated in vivo by hCG. J Reprod Fertil 68:335-341 (Pubitemid 13070391)
98. Sherizly I, Galiani D, Dekel N (1988) Regulation of oocyte maturation: communication in the rat cumulus-oocyte complex. Hum Reprod 3:761-766
99. Motlik J, Fulka J, Flechon JE (1986) Changes in intercellular coupling between pig oocytes and cumulus cells during matu-ration in vivo and in vitro. J Reprod Fertil 76:31-37 (Pubitemid 16149560)
100. Norris RP, Freudzon M, Nikolaev VO, Jaffe LA (2010) Epi-dermal 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
101. Patwardhan VV, Lanthier A (1984) Cyclic GMP phosphodies-terase and guanylate cyclase activities in rabbit ovaries and the effect of in vivo stimulation with LH. J Endocrinol 101:305-310 (Pubitemid 14149333)
102. Conti M, Kasson BG, Hsueh AJW (1984) Hormonal regulation of 3', 5'-adenosine monophosphate phosphodiesterases in cul-tured rat granulosa cells. Endocrinology 114:2361-2368 (Pubitemid 14120298)
103. 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 (Epub ahead of print)
104. Peng XR, Hsueh AJ, LaPolt PS, Bjersing L, Ny T (1991) Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology 129:3200-3207
105. Su YQ, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ (2002) Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 143:2221-2232 (Pubitemid 34521568)
106. Potter LR, Hunter T (1998) Identification and characterization of the major phosphorylation sites of the B-type natriuretic peptide receptor. J Biol Chem 273:15533-15539 (Pubitemid 28298164)
107. Pandey AN, Tripathi A, Premkumar KV, Shrivastav TG, Cha-ube SK (2010) Reactive oxygen and nitrogen species during meiotic resumption from diplotene arrest in mammalian oocytes. J Cell Biochem 111:521-528
108. Conti M, Andersen CB, Richard F, Mehats C, Chun SY, Horner K, Jin C, Tsafriri A (2002) Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrin 187:153-159 (Pubitemid 34436944)
109. Andersen CB, Roth RA, Conti M (1998) Protein kinase B/Akt induces resumption of meiosis in Xenopus oocytes. J Biol Chem 273:18705-18708 (Pubitemid 28366252)