New elements in the C-type natriuretic peptide signaling pathway inhibiting swine in vitro oocyte meiotic resumption

Biology of Reproduction

Volumn 91, Issue 1, 2014, Pages

  Santiquet, Nicolas ^a   Papillon Dion, Émilie ^a   Djender, Nadjib ^a   Guillemette, Christine ^a   Richard, François J ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

cumulus cells; in vitro maturation; meiotic arrest; meiotic maturation; meiotic resumption; natriuretic peptide; oocyte maturation

Indexed keywords

ATRIAL NATRIURETIC FACTOR; CYCLIC GMP; ENZYME INHIBITOR; FOLLITROPIN; NATRIURETIC PEPTIDE TYPE C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE ARREST; CELL LEVEL; CONTROLLED STUDY; CUMULUS OOPHORUS; FEMALE; GAP JUNCTION; IN VITRO OOCYTE MATURATION; IN VITRO STUDY; MEIOSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SWINE; ANIMAL; CUMULUS CELL; DRUG EFFECTS; METABOLISM; OOCYTE DEVELOPMENT; PHYSIOLOGY;

ANIMALS; CUMULUS CELLS; CYCLIC GMP; FEMALE; MEIOSIS; NATRIURETIC PEPTIDE, C-TYPE; OOCYTES; OOGENESIS; SIGNAL TRANSDUCTION; SWINE;

EID: 84906267042     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.114132     Document Type: Article

References (48)

1. Hiradate Y, Hoshino Y, Tanemura K, Sato E. C-type natriuretic peptide inhibits porcine oocyte meiotic resumption. Zygote (in press). Published online ahead of print 18 January 2013; DOI 10.1017/ S0967199412000615.
2. 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; 330:366-369.
3. 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.
4. Potter L, Yoder A, Flora D, Antos L, Dickey D. Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. In: Schmidt HHW, Hofmann F, Stasch J-P (eds.), CGMP: Generators, Effectors and Therapeutic Implications, vol. 191. Berlin/Heidelberg: Springer; 2009:341-366.
5. Schweitz H, Vigne P, Moinier D, Frelin C, Lazdunski M. A new member of the natriuretic peptide family is present in the venom of the green mamba (Dendroaspis angusticeps). J Biol Chem 1992; 267:13928-13932.
6. Schirger JA, Heublein DM, Chen HH, Lisy O, Jougasaki M, Wennberg PW, Burnett JC, Jr. Presence of Dendroaspis natriuretic peptide-like immunoreactivity in human plasma and its increase during human heart failure. Mayo Clinic Proc 1999; 74:126-130.
7. Schulz-Knappe P, Forssmann K, Herbst F, Hock D, Pipkorn R, Forssmann WG. Isolation and structural analysis of "urodilatin", a new peptide of the cardiodilatin-(ANP)-family, extracted from human urine. Klin Wochenschr 1988; 66:752-759.
8. Fry BG, Wickramaratana JC, Lemme S, Beuve A, Garbers D, Hodgson WC, Alewood P. Novel natriuretic peptides from the venom of the inland taipan (Oxyuranus microlepidotus): isolation, chemical and biological characterisation. Biochem Biophys Res Commun 2005; 327:1011-1015.
9. Zhang Y, Wu J, Yu G, Chen Z, Zhou X, Zhu S, Li R, Lu Q. A novel natriuretic peptide from the cobra venom. Toxicon 2011; 57:134-140.
10. Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y, Shirakami G, Arai H, Saito Y, Kambayashi Y, Inouye K. Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and Ctype natriuretic peptide. Endocrinology 1992; 130:229-239.
11. 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; 366:308-316.
12. 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; 152:4377-4385.
13. Sato Y, Cheng Y, Kawamura K, Takae S, Hsueh AJ. C-type natriuretic peptide stimulates ovarian follicle development. Mol Endocrinol 2012; 26: 1158-1166.
14. Potter LR. Natriuretic peptide metabolism, clearance and degradation. FEBS J 2011; 278:1808-1817.
15. Rose RA, Giles WR. Natriuretic peptide C receptor signalling in the heart and vasculature. J Physiol 2008; 586:353-366.
16. Anand-Srivastava MB. Natriuretic peptide receptor-C signaling and regulation. Peptides 2005; 26:1044-1059.
17. Berl T, Mansour J, Teitelbaum I. ANP stimulates phospholipase C in cultured RIMCT cells: roles of protein kinases and G protein. Am J Physiol 1991; 260:F590-595.
18. Resink TJ, Scott-Burden T, Baur U, Jones CR, Buhler FR. Atrial natriuretic peptide induces breakdown of phosphatidylinositol phosphates in cultured vascular smooth-muscle cells. Eur J Biochem 1988; 172: 499-505.
19. Murthy KS, Teng BQ, Zhou H, Jin JG, Grider JR, Makhlouf GM. G(i-1)/ G(i-2)-dependent signaling by single-transmembrane natriuretic peptide clearance receptor. Am J Physiol Gastrointest Liver Physiol 2000; 278: G974-G980.
20. Costa MA, Elesgaray R, Balaszczuk AM, Arranz C. Role of NPR-C natriuretic receptor in nitric oxide system activation induced by atrial natriuretic peptide. Regul Pept 2006; 135:63-68.
21. Costa MA, Elesgaray R, Caniffi C, Fellet A, Arranz C. Role of cardiovascular nitric oxide system in C-type natriuretic peptide effects. Biochem Biophys Res Commun 2007; 359:180-186.
22. 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.
23. Piao FL, Park SH, Han JH, Cao C, Kim SZ, Kim SH. Dendroaspis natriuretic peptide and its functions in pig ovarian granulosa cells. Regul Pept 2004; 118:193-198.
24. Leitman DC, Andresen JW, Kuno T, Kamisaki Y, Chang JK, Murad F. Identification of multiple binding sites for atrial natriuretic factor by affinity cross-linking in cultured endothelial cells. J Biol Chem 1986; 261: 11650-11655.
25. Hubbard CJ, Terranova PF. Inhibitory action of cyclic guanosine 50-phosphoric acid (GMP) on oocyte maturation: dependence on an intact cumulus. Biol Reprod 1982; 26:628-632.
26. Tornell J, Billig H, Hillensjo T. Resumption of rat oocyte meiosis is paralleled by a decrease in guanosine 30,50-cyclic monophosphate (cGMP) and is inhibited by microinjection of cGMP. Acta Physiol Scand 1990; 139:511-517.
27. Zhang M, Tao Y, Zhou B, Xie H, Wang F, Lei L, Huo L, Sun Q, Xia G. Atrial natriuretic peptide inhibits the actions of FSH and forskolin in meiotic maturation of pig oocytes via different signalling pathways. J Mol Endocrinol 2005; 34:459-472.
28. Zhang M, Tao Y, Xia G, Xie H, Hong H, Wang F, Lei L. Atrial natriuretic peptide negatively regulates follicle-stimulating hormone-induced porcine oocyte maturation and cumulus expansion via cGMP-dependent protein kinase pathway. Theriogenology 2005; 64:902-916.
29. 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.
30. Degerman E, Belfrage P, Manganiello VC. Structure, localization, and regulation of cGMP-inhibited phosphodiesterase (PDE3). J Biol Chem 1997; 272:6823-6826.
31. 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; 140:655-662.
32. 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; 136:1869-1878.
33. Sela-Abramovich S, Galiani D, Nevo N, Dekel N. Inhibition of rat oocyte maturation and ovulation by nitric oxide: mechanism of action. Biol Reprod 2008; 78:1111-1118.
34. Sherizly I, Galiani D, Dekel N. Regulation of oocyte maturation: communication in the rat cumulus-oocyte complex. Hum Reprod 1988; 3:761-766.
35. Thomas RE, Armstrong DT, Gilchrist RB. Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 30,50-monophosophate levels. Biol Reprod 2004; 70:548-556.
36. Shu YM, Zeng HT, Ren Z, Zhuang GL, Liang XY, Shen HW, Yao SZ, Ke PQ, Wang NN. Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum Reprod 2008; 23:504-513.
37. 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.
38. Petters RM, Wells KD. Culture of pig embryos. J Reprod Fertil Suppl 1993; 48:61-73.
39. Laforest MF, Pouliot E, Gueguen L, Richard FJ. Fundamental significance of specific phosphodiesterases in the control of spontaneous meiotic resumption in porcine oocytes. Mol Reprod Dev 2005; 70:361-372.
40. Santiquet NW, Develle Y, Laroche A, Robert C, Richard FJ. Regulation of gap-junctional communication between cumulus cells during in vitro maturation in swine, a Gap-FRAP study. Biol Reprod 2012; 87:46.
41. Salmon ED, Leslie RJ, Saxton WM, Karow ML, McIntosh JR. Spindle microtubule dynamics in sea urchin embryos: analysis using a fluoresceinlabeled tubulin and measurements of fluorescence redistribution after laser photobleaching. J Cell Biol 1984; 99:2165-2174.
42. Bovy PR, O'Neal JM, Olins GM, Patton DR. Identification of structural requirements for analogues of atrial natriuretic peptide (ANP) to discriminate between ANP receptor subtypes. J Med Chem 1989; 32: 869-874.
43. Wang S, Ning G, Chen X, Yang J, Ouyang H, Zhang H, Tai P, Mu X, Zhou B, Zhang M, Xia G. PDE5 modulates oocyte spontaneous maturation via cGMP-cAMP but not cGMP-PKG signaling. Front Biosci 2008; 13:7087-7095.
44. 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.
45. Sasseville M, Cote N, Gagnon MC, Richard FJ. Up-regulation of 3050-cyclic guanosine monophosphate-specific phosphodiesterase in the porcine cumulus-oocyte complex affects steroidogenesis during in vitro maturation. Endocrinology 2008; 149:5568-5576.
46. Wei JY, Cohen ED, Genieser HG, Barnstable CJ. Substituted cGMP analogs can act as selective agonists of the rod photoreceptor cGMP-gated cation channel. J Mol Neurosci 1998; 10:53-64.
47. Savoie P, de Champlain J, Anand-Srivastava MB. C-type natriuretic peptide and brain natriuretic peptide inhibit adenylyl cyclase activity: interaction with ANF-R2/ANP-C receptors. FEBS Lett 1995; 370:6-10.
48. Bennett BD, Bennett GL, Vitangcol RV, Jewett JR, Burnier J, Henzel W, Lowe DG. Extracellular domain-IgG fusion proteins for three human natriuretic peptide receptors: hormone pharmacology and application to solid phase screening of synthetic peptide antisera. J Biol Chem 1991; 266:23060-23067.