Inhibition of germinal vesicle breakdown by antioxidants and the roles of signaling pathways related to nitric oxide and cGMP during meiotic resumption in oocytes of a marine worm

Reproduction

Volumn 143, Issue 3, 2012, Pages 261-270

  Stricker, Stephen A ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; ANTIOXIDANT; CYCLIC AMP; CYCLIC GMP; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; SEA WATER;

ANIMAL EXPERIMENT; ARTICLE; CELL DAMAGE; CEREBRATULUS; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FOLLICLE CYST; GERMINAL VESICLE; GERMINAL VESICLE BREAKDOWN; IMMUNOBLOTTING; MEIOSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; UPREGULATION; WORM;

ANIMALS; ANNELIDA; ANTIOXIDANTS; AQUATIC ORGANISMS; BLASTODISC; CYCLIC GMP; DOWN-REGULATION; FEMALE; MEIOSIS; NITRIC OXIDE; OOCYTES; OOGENESIS; RATS; SEAWATER; SIGNAL TRANSDUCTION;

INVERTEBRATA; MAMMALIA; NEMERTEA; RATTUS; SIPUNCULUS NUDUS;

EID: 84858959328     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-11-0358     Document Type: Article

References (88)

1. Abbasi M, Akbari M, Amidi F, Ragerdi Kashani I, Mahmoudi R, Sobhani A, Takzare N, Pasbaksh P, Barbarestani M, Abolhassani F et al. 2009 Nitric oxide acts through different signaling pathways in maturation of cumulus-enclosed mouse oocytes. DARU Journal of Pharmaceutical Sciences 17 48-52.
2. Ahn HS, Crim W, Romano M, Sybertz E & Pitts B 1989 Effects of selective inhibitors on cyclic nucleotide phosphodiesterases of rabbit aorta. Biochemical Pharmacology 38 3331-3339. (doi:10.1016/0006-2952(89)90631-X)
3. Akaike T, Yoshida M, Miyamoto Y, Sato K, Kohno M, Sasamoto K, Miyazaki K, Ueda S & Maeda H 1993 Antagonistic action of imidazolineoxyl N-oxides against endothelium-derived relaxing factor/ NO through a radical reaction. Biochemistry 32 827-832. (doi:10. 1021/bi00054a013)
4. Ali AA, Bilodeau JF & Sirard MA 2003 Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology 59 939-949. (doi:10.1016/S0093-691X(02)01125-1)
5. Amale MH, Shahne AZ, Abavisani A & Nasrollahi S 2011 Effects of inhibiting nitric oxide synthase on cumulus expansion and nuclear maturation of sheep oocytes. Czech Journal of Animal Science 56 284-291.
6. Bergamini S, Rota C, Canali R, Staffieri M, Daneri F, Bini A, Giovannini F, Tomasi A & Iannone A 2001 N-acetylcysteine inhibits in vivo nitric oxide production by inducible nitric oxide synthase. Nitric Oxide: Biology and Chemistry 5 349-360. (doi:10.1006/niox.2001.0356)
7. Bilodeau-Goeseels S 2007 Effects of manipulating the nitric oxide/cyclic GMP pathway on bovine oocyte meiotic resumption in vitro. Theriogenology 68 693-701. (doi:10.1016/j.theriogenology.2007.05.063)
8. Bishop CD, Pires A, Norby S-W, Boudko D, Moroz LL & Hadfield MG 2008 Analysis of nitric oxide-cyclic guanosine monophosphate signaling during metamorphosis of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). Evolution & Development 10 288-299. (doi:10.1111/j.1525- 142X.2008.00238.x)
9. Bu S, Xia G, Tao Y, Lei L & Zhou B 2003 Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Molecular and Cellular Endocrinology 207 21-30. (doi:10.1016/S0303-7207(03) 00213-2)
10. Bu S, Xie H, Tao Y, Wang J & Xia G 2004 Nitric oxide influences the maturation of cumulus cell-enclosed mouse oocytes cultured in spontaneous maturation medium and hypoxanthine-supplemented medium through different pathways. Molecular and Cellular Endocrinology 223 85-93. (doi:10.1016/j.mce. 2004.04.015)
11. Carling D 2005 AMP-activated protein kinase: balancing the scales. Biochimie 87 87-91. (doi:10.1016/j.biochi.2004.10.017)
12. Chen J & Downs SM 2008 AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Developmental Biology 313 47-57. (doi:10.1016/j.ydbio.2007.09.043)
13. Chen J, Hudson E, Chi MM, Chang AS, Moley KH, Hardie DG & Downs SM 2006 AMPK regulation of mouse oocyte meiotic resumption in vitro. Developmental Biology 291 227-238. (doi:10.1016/j.ydbio.2005.11. 039)
14. Chmelikova E, Jeseta M, SemikovaM, Petr J, Tumova L, Kott T, Lipovova P &Jflek F 2010 Nitric oxide synthase isoforms and the effect of their inhibition on meiotic maturation of porcine oocytes. Zygote 18 235-244. (doi:10.1017/S0967199409990268)
15. Choi SH, Choi DH, Song KS, Shin KH & Chun BG 2002 Zaprinast, an inhibitor of cGMP-selective phosphodiesterases, enhances the secretion of TNF-alpha and IL-1 beta and the expression of iNOS and MHC class II molecules in rat microglial cells. Journal of Neuroscience 67 411-421.
16. Deguchi R, Takeda N & Stricker SA 2011 Comparative biology of cAMPinduced germinal vesicle breakdown in marine invertebrate oocytes. Molecular Reproduction and Development 78 708-725. (doi:10.1002/ mrd.21346)
17. Denninger JW & Marletta MA 1999 Guanylate cyclase and the NO/cGMP signaling pathway. Biochimica et Biophysica Acta 1411 334-350. (doi:10.1016/S0005-2728(99) 00024-9)
18. Downs SM 2010 Regulation of the G2/M transition in rodent oocytes. Molecular Reproduction and Development 77 566-585. (doi:10.1002/ mrd.21175)
19. Downs SM, Hudson ER & Hardie DG 2002 A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Developmental Biology 245 200-212. (doi:10.1006/dbio.2002.0613)
20. Duckworth BC, Weaver JS & Ruderman JV 2002 G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. PNAS 99 16794-16799. (doi:10.1073/pnas.222661299)
21. Dumollard R, Ward Z, Carroll J & Duchen MR 2007 Regulation of redox metabolism in the mouse oocyte and embryo. Development 134 455-465. (doi:10.1242/dev.02744)
22. Evgenov OV, Pacher P, Schmidt PM, Haskó G, Schmidt HHHW & Stasch J-P 2006 NO-independent, stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential. Nature Reviews. Drug Discovery 5 755-768. (doi:10.1038/nrd2038)
23. Faerge I, Terry B, Kalous J, Wahl P, Lessl M, Ottesen JL, Hyttel P &Grøndahl C 2001 Resumption of meiosis induced by meiosis-activating sterol has a different signal transduction pathway than spontaneous resumption of meiosis in denuded mouse oocytes cultured in vitro. Biology of Reproduction 65 1751-1758. (doi:10.1095/biolreprod65.6. 1751)
24. Gonzalez-Domenech CM & Munoz-Chapuli R 2010 Molecular evolution of nitric oxide synthases in metazoans. Comparative Biochemistry and Physiology. Part D, Genomics & Proteomics 5 295-301. (doi:10.1016/j.cbd.2010.08.004)
25. Harput US, Genc Y, Khan N & Saracoglu I 2011 Radical scavenging effects of different Veronica species. Records of Natural Products 5 100-107.
26. Hubbard CJ & Price J 1988 The effects of follicle-stimulating hormone and cyclic guanosine 3′,5′ monophosphate on cyclic adenosine 3′,5′ monophosphate phosphodiesterase and resumption of meiosis in hamster cumulus-oocyte complexes. Biology of Reproduction 39 829-838. (doi:10.1095/biolreprod39.4.829)
27. Huo L-J, Liang C-G, Yu L-Z, Zhong Z-S, Yang Z-M, Fan H-Y, Chen D-Y &Sun Q-Y 2005 Inducible nitric oxide synthase-derized nitric oxide regulates germinal vesicle breakdown and first polar body emission in the mouse oocyte. Reproduction 129 403-409. (doi:10.1530/rep.1. 0542)
28. Hwang TL, Wu CC & Teng CM 1998 Comparison of two soluble guanylyl cyclase inhibitors, methylene blue and ODQ, on sodium nitroprusside-induced relaxation in guinea pig trachea. British Journal of Pharmacology 125 1158-1163. (doi:10.1038/sj.bjp.0702181)
29. Jablonka-Shariff A & Olson LM 2000 Nitric oxide is essential for optimal meiotic maturation of murine cumulus-oocyte complexes in vitro. Molecular Reproduction and Development 55 412-421. (doi:10.1002/(SICI) 1098-2795(200004)55:4〈412::AID-MRD9〉3.0.CO;2-W)
30. Jaffe LA & Norris RP 2010 Initiation of the meiotic prophase-to-metaphase transition in mammalian oocytes. In Oogenesis: The Universal Process, pp 181-198. Eds M-H Verlhac & A Villeneuve. New York: John Wiley &Sons.
31. Karaseva EM & Khotimchenko YS 1995 Effect of compounds elevating cyclic nucleotide levels on dithiothreitol-induced oocyte maturation in the holothurian Stichopus japonicus. Comparative Biochemistry and Physiology. Part C: Pharmacology, Toxicology and Endocrinology 111 441-444. (doi:10.1016/0742- 8413(95)00030-5)
32. Kim MS, Park SB, Suk K, Kim IK, Kin SY, Kim JA, Lee SH & Kim SH 2009 Gallotannin isolated from Euphorbia species, 1,2,6-tri-O-galloyl-beta-D-allose, decreases nitric oxide production through inhibition of nuclear factor kappa B and downstream inducible nitric oxide synthase expression in macrophages. Biological & Pharmaceutical Bulletin 32 1052-1056.
33. Kishimoto T 2003 Cell-cycle control during meiotic maturation. Current Opinion in Cell Biology 15 654-663. (doi:10.1016/j.ceb.2003.10.010)
34. 2+ increase induces post-fertilization events via MAP kinase dephosphorylation in eggs of the hydrozoan jellyfish Cladonema pacificum. Developmental Biology 293 228-241. (doi:10.1016/j.ydbio.2006.02.005)
35. LaPolt PS 2002 Roles of cyclic GMP in modulating ovarian functions. Reproductive Biomedicine Online 6 15-23. (doi:10.1016/S1472-6483(10) 62051-2)
36. Lei B, Matsuo K, Labinskyy V, Sharma N, Changler MP, Ahn A, Hintze TH, Stanley WC & Recchia FA 2005 Exogenous nitric oxide reduces glucose transporters translocation and lactate production in ischemic myocardium in vivo. PNAS 102 6966-6971. (doi:10.1073/pnas. 0500768102)
37. Linares E, Giorgio S & Augusto O 2008 Inhibition of in vivo leishmanicidal mechanisms by tempol: nitrix oxide downregulation and oxidant scavenging. Free Radical Biology & Medicine 44 1668-1676. (doi:10. 1016/j.freeradbiomed.2008.01.027)
38. Meijer L, Dostmann W, Genieser HG, Butt E & Jastorff B 1989 Starfish oocyte maturation: evidence for a cyclic AMP-dependent inhibitory pathway. Developmental Biology 133 58-66. (doi:10.1016/0012-1606(89)90296-0)
39. Moroz LL, Chen D, Gillette MU & Gillette R 1996 Nitric oxide synthase activity in the molluscan CNS. Journal of Neurochemistry 66 873-876. (doi:10.1046/j.1471-4159.1996.66020873.x)
40. Nadri B, Zeinoaldini S & Kohram H 2009 Ascorbic acid effects on in vitro maturation of mouse oocyte with or without cumulus cell. African Journal of Biotechnology 8 5627-5631.
41. Nakagawa S, Arai Y, Mazda O, Kishida T, Takahashi KA, Sakao K, Saito M, Honjo K, Imanishi J & Kubo T 2010 N-acetylcysteine prevents nitric oxide-induced chondrocyte apoptosis and cartilage degeneration in an experimental model of osteoarthritis. Journal of Orthopaedic Research 28 156-163.
42. Nakamura Y, Yamagata Y, Sugino N, Takayama H & Kato H 2002 Nitric oxide inhibits oocyte meiotic maturation. Biology of Reproduction 67 1588-1592. (doi:10.1095/biolreprod.102.005264)
43. Nemoto S-I & Ishida K 1983 Changes in cGMP levels on meiosis reinitiation of starfish oocytes. Experimental Cell Research 145 226-230. (doi:10. 1016/S0014-4827(83)80025-1)
44. 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 AMPand meiosis in the mouse oocyte. Development 136 1869-1878. (doi:10.1242/dev.035238)
45. Olesen S-P, Drejer J, Axelsson O, Moldt P, Bang L, Nielsen-Kudxk JE, Busse R & Mulsch A 1998 Characterization of NS 2028 as a specific inhibitor of soluble guanylyl cyclase. British Journal of Pharmacology 123 299-309. (doi:10.1038/sj.bjp.0701603)
46. Palumbo A 2005 Nitric oxide in marine invertebrates: a comparative perspective. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 142 241-248. (doi:10.1016/j.cbpb.2005.05. 043)
47. Pandey AN, Tripathi A, PremKumar K, Shrivastav TG & Chaube SK 2010 Reactive oxygen and nitrogen species during meiotic resumption from diplotene arrest in mammalian oocytes. Journal of Cellular Biochemistry 111 521-528. (doi:10.1002/jcb.22736)
48. Petr J, Rajmon R, Lanska V, Sedmikova M & Jilek F 2005 Nitric oxide dependent activation of pig oocytes: role of calcium. Molecular and Cellular Endocrinology 242 16-22. (doi:10.1016/j.mce.2005.05.004)
49. Pilon G, Dallaire P & Marette M 2004 Inhibition of inducible nitric oxide sythase by activators of AMP-activated protein kinase. A new mechanism of action of insulin-sensitizing drugs. Journal of Biological Chemistry 279 20767-20774. (doi:10.1074/jbc.M401390200)
50. Sandberg K, Bor M, Hong JI, Carvallo PM & Catt KJ 1993 Atrial natriuretic factor activates cyclic adenosine 3′,5′-monophosphate phosphodiesterase in Xenopus laevis oocytes and potentiates progesterone-induced maturation via cyclic guanosine 5′-monophosphate accumulation. Biology of Reproduction 49 1074-1082. (doi:10.1095/biolreprod49.5.1074)
51. Sato E, Wood HN, Lynn DG, Sahni MK & Koide SS 1985 Meiotic arrest in oocytes regulated by a Spisula factor. Biological Bulletin 169 334-341. (doi:10.2307/1541486)
52. Schroeder TE & Stricker SA 1983 Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Developmental Biology 98 373-384. (doi:10.1016/0012-1606(83)90366-4)
53. Sela-Abramovich S, Galiani D, Nevo N & Dekel N 2008 Inhibition of rat oocyte maturation and ovulation by nitric oxide: mechanism of action. Biology of Reproduction 78 1111-1118. (doi:10.1095/biolreprod.107. 065490)
54. Sengoku K, Takuma N, Horikawa M, Tsuchiya K, Komori H, Sharifa D, Tamate K & Ishikawa M 2001 Requirement of nitric oxide for murine oocyte maturation, embryo development, and trophoblast outgrowth in vitro. Molecular Reproduction and Development 58 262-268. (doi:10. 1002/1098-2795(200103)58: 3〈262::AID-MRD3〉3.0.CO;2-8)
55. Stricker SA 2009a Roles of protein kinase C isotypes during seawater-versus cAMP-induced oocyte maturation in a marine worm. Molecular Reproduction and Development 76 693-707. (doi:10.1002/mrd.20993)
56. Stricker SA 2009b Interactions between mitogen-activated protein kinase and protein kinase C signaling during oocyte maturation and fertilization in a marine worm. Molecular Reproduction and Development 76 708-721. (doi:10.1002/mrd.21032)
57. Stricker SA 2011 Potential upstream regulators and downstream targets of AMP-activated kinase (AMPK)during oocyte maturation in a marine worm. Reproduction 142 29-39. (doi:10.1530/REP-10-0509)
58. Stricker SA & Schatten G 1989 Nuclear disassembly and nuclear lamina depolymerization during germinal vesicle breakdown in starfish. Developmental Biology 135 87-98. (doi:10.1016/0012-1606(89)90160-7)
59. Stricker SA & Smythe TL 2001 5-HT causes an increase in cAMP that stimulates, rather than inhibits, oocyte maturation in marine nemertean worms. Development 128 1415-1427. (Pubitemid 32409661)
60. 2+ signaling in maturing and fertilized oocytes of marine protostome worms: the roles of MAPKs and MPF. Development 130 2867-2879. (doi:10.1242/dev.00508)
61. Stricker SA & Smythe TL 2006a Differing mechanisms of cAMP-versus seawater-induced oocyte maturation in marine nemertean worms I. The roles of serine/threonine kinases and phosphatases. Molecular Reproduction and Development 73 1578-1590. (doi:10.1002/mrd.20597)
62. Stricker SA & Smythe TL 2006b Differing mechanisms of cAMP-versus seawater-induced oocyte maturation in marine nemertean worms II. The roles of tyrosine kinases and phosphatases. Molecular Reproduction and Development 73 1564-1577. (doi:10.1002/mrd.20596)
63. Stricker SA, Smythe TL, Miller L & Norenburg JL 2001 Comparative biology of oogenesis in nemertean worms. Acta Zoologica 82 213-230. (Pubitemid 33669475)
64. Stricker SA, Swiderek L & Nguyen T 2010a Stimulators of AMP-activated kinase inhibit seawater - but not cAMP-induced oocyte maturation in a marine worm: implications for interactions between cAMP and AMPK signaling. Molecular Reproduction and Development 77 497-510. (doi:10.1002/mrd.21177)
65. Stricker SA, Escalona JR, Abernathy S & Marquardt A 2010b Pharmacological analyses of protein kinases regulating egg maturation in marine nemertean worms: a review and comparison with mammalian eggs. Marine Drugs 8 2417-2434. (doi:10.3390/md8082417)
66. Sun QY, Lai L, Prather RS & Schatten H 2000 Antioxidants stimulate meiosis resumption, but inhibit mitogen-activated protein kinase phosphorylation and further cell cycle progression in porcine oocytes. Reproduction, Fertility, and Development 12 383-389. (doi:10.1071/RD00104)
67. Sun QY, Miao YL & Schatten H 2009 Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 8 2741-2747. (doi:10.4161/cc.8.17.9471)
68. Takami M, Preston SL, Toyloy VA & Behrman HR 1999 Antioxidants reversibly inhibit the spontaneous resumption of meiosis. American Journal of Physiology 276 E684-E688. (Pubitemid 29211340)
69. Takeda N, Kyozuka K & Deguchi R 2006 Increase in intracellular cAMP is a prerequisite signal for initiation of physiological oocyte meiotic maturation in the hydrozoan Cytaeis uchidae. Developmental Biology 298 248-258. (doi:10.1016/j.ydbio.2006.06.034)
70. Tao Y, Zhou B, Xia G, Wang F, Wu Z & Fu M 2004a Exposure to L-ascorbic acid or a-tocopherol facilitates the development of porcine denuded oocytes from metaphase I to metaphase II and prevents cumulus cells from fragmentation. Reproduction in Domestic Animals 39 52-57. (doi:10.1046/j.1439- 0531.2003.00478.x)
71. Tao Y, Fu Z, Zhang M, Xia G, Yang J & Xie H 2004b Immunohistochemical localization of inducible and endothelial nitric oxide synthase in porcine ovaries and effects of NO on antrum formation and oocyte meiotic maturation. Molecular and Cellular Endocrinology 222 93-103. (doi:10. 1016/j.mce.2004.04. 014)
72. Tao JY, Fu Z, Zhang ML, Xia G, Lei L &Wu ZL 2005 Nitric oxide influences the meiotic maturation of porcine oocytes cultured in hypoxanthinesupplemented medium. Journal of Animal Physiology and Animal Nutrition 89 38-44. (doi:10.1111/j.1439-0396.2004.00508.x)
73. Tao Y, Chen H, Tian NN, Huo DT, Zhang YH, Liu Y, Fang FG, Ding JP &Z hang XR 2010 Effects of L-ascorbic acid, a-tocopherol and co-culture on in vitro developmental potential of porcine cumulus cells free oocytes. Reproduction in Domestic Animals 45 19-25. (doi:10.1111/j.1439-0531.2008.01129.x)
74. Thaler CD & Epel D 2003 Nitric oxide in oocyte maturation, ovulation, fertilization, cleavage and implantation: a little dab'll do ya. Current Pharmaceutical Design 9 399-409. (doi:10.2174/1381612033391748)
75. Törnell J, Billig H & Hillensjö 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 Physiologica Scandinavia 139 511-517. (doi:10.1111/j.1748-1716.1990.tb08953.x)
76. Tripathi A, Khatun S, Pandey AN, Mishra SK, Chaube R, Shrivastav TG &Chaube SK 2009 Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis. Free Radical Research 43 287-294. (doi:10.1080/1071576080269 5985)
77. Tsafriri A & Dekel N 2010. Intra- and intercellular molecular mechanisms in regulation of meiosis in murid rodents. In Oocyte Maturation and Fertilization: A Long History for a Short Event, pp 38-63. Eds E Tosti &R Boni. Bentham Science Publishers: Brussum, The Netherlands.
78. Vaccari S, Weeks JL, Hsieh M, Menniti FS & Conti M 2009 Cyclic GMP signaling is involved in the LH-dependent meiotic maturation of mouse oocytes. Biology of Reproduction 81 595-604. (doi:10.1095/biolreprod. 109.077768)
79. Viana KS, Caldas-Bussiere MC, Matta SGC, Faes MR, Paes de Carvalho CS & Quirino CR 2007 Effect of sodium nitroprusside, a nitric oxide donor, on the in vitro maturation of bovine oocytes. Animal Reproduction Science 102 217-227. (doi:10.1016/j.anireprosci. 2006.11.004)
80. Voronina E & Wessel GM 2003 The regulation of oocyte maturation. Current Topics in Developmental Biology 58 53-110. (Pubitemid 137639497)
81. Wang S, Ning G, Chen X, Yang J, Ouyang H, Zhang H, Tai P, Mu X, Zhou B, Zhang M et al. 2008 PDE5 modulates oocyte spontaneous maturation via cGMP-cAMP but not cGMP-PKG signaling. Frontiers in Bioscience 13 7087-7095. (doi:10.2741/3212)
82. Yamagata Y, Nakamura Y, Sugino N, Harad A, Takayama H, Kashida S &Kato H 2002 Alterations in nitrate/nitrite and nitric oxide synthase in preovulatory follicules of gonadotropin-primed immature rat. Endocrinology Journal 49 219-226. (Pubitemid 34496341)
83. Yamashita M 1988 Involvement of cAMP in initiating maturation of the brittle-star Amphipholis kochii oocytes: induction of oocyte maturation by inhibitors of cyclic nucleotide phosphodiesterase and activators of adenylate cyclase. Developmental Biology 125 109-114. (doi:10.1016/ 0012-1606(88)90063-2))
84. Zhang M, Tao Y, Zhou B, Xie H, Wang F, Lei L, Huo L, Sun Q & Xia G 2005 Atrial natriuretic peptide inhibits the actions of FSH and forskolin inmeiotic maturation of pig oocytes via different signaling pathways. Journal of Molecular Endocrinology 34 459-472. (doi:10.1677/jme.1.01673)
85. Zhang M, Xia G, Zhou B & Wang C 2007 Gonadotropin-controlled mammal oocyte meiotic resumption. Frontiers in Bioscience 12 282-296. (doi:10.2741/2064)
86. Zhang Y, Zhang Z, Xu X-Y, Li X-S, Yu M, Yu A-M, Zong Z-H & Yu B-Z 2008 Protein kinase A modulates Cdc25B activity during meiotic resumption of mouse oocytes. Developmental Dynamics 237 3777-3786. (doi:10. 1002/dvdy.21799)
87. Zhang M, Ouyang H & Xia G 2009 The signal pathway of gonadotrophinsinduced mammalian oocyte meiotic resumption. Molecular Human Reproduction 15 399-409. (doi:10.1093/molehr/gap031)
88. Zhang M, Su Y-Q, Sugiura K, Xia G & Eppig J 2010 Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330 366-369. (doi:10.1126/science.1193573)