Hostname: page-component-76fb5796d-25wd4 Total loading time: 0 Render date: 2024-04-25T21:19:36.364Z Has data issue: false hasContentIssue false

C-type natriuretic peptide inhibits porcine oocyte meiotic resumption

Published online by Cambridge University Press:  18 January 2013

Yuki Hiradate*
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Aobaku, Sendai 981–8555, Japan.
Yumi Hoshino
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Tsutsumidori-Amamiyamachi, Aobaku, Sendai 981–8555, Japan.
Kentaro Tanemura
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Tsutsumidori-Amamiyamachi, Aobaku, Sendai 981–8555, Japan.
Eimei Sato
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Tsutsumidori-Amamiyamachi, Aobaku, Sendai 981–8555, Japan.
*
All correspondence to Yuki Hiradate. Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Aobaku, Sendai 981–8555, Japan. Tel:/Fax: +81 22 717 8687. E-mail: hiradate@bios.tohoku.ac.jp

Summary

C-type natriuretic peptide (CNP) is a recently identified meiotic inhibitor in mice. However, it has not been investigated in porcine oocytes to date. This study aimed to demonstrate the inhibitory effect of CNP against germinal vesicle breakdown (GVBD) in porcine oocyte meiotic resumption. Immunohistochemical analysis revealed intense natriuretic peptide receptor 2 (NPR2) immunoreactivity in the oocyte surrounded cumulus cells in the follicles. Furthermore, reverse transcription polymerase chain reaction (RT-PCR) analysis showed the expression of npr2 mRNA only in cumulus cells but not in oocytes, suggesting that cumulus cells are the targets of CNP. When cumulus–oocyte complexes (COCs) or denuded oocytes (DOs) were cultured with various concentrations of CNP (10, 50, 100, 500, and 1,000 nM), inhibitory effect was observed in the COC group, but not in the DO group, confirming that CNP indirectly inhibits GVBD via cumulus cells. This evidence is the first indication that the CNP-NPR2 pathway is involved in meiotic arrest in porcine oocytes. Furthermore, we investigated the effect of oocyte-derived paracrine factor (ODPF) on npr2 mRNA expression level in cumulus cells by evaluating changes in mRNA expression in oocytectomised COCs (OXCs) by real-time PCR. A significant decrease in npr2 mRNA expression level was observed in OXCs, whereas mRNA expression level was restored in OXCs with DOs, indicating that ODPF participates in the regulation of npr2 expression in porcine cumulus cells.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ballermann, B.J. & Brenner, B.J (1987). Atrial natriuretic peptide and kidney. Am. J. Kidney Dis. 10, 712.Google Scholar
Downs, S.M., Coleman, D.L., Ward-Bailey, P.F. & Eppig, J.J. (1985). Hypoxanthine is the principal inhibitor of murine oocyte maturation in a low molecular weight fraction of porcine follicular fluid. Proc. Natl. Acad. Sci. USA 82, 454–8.Google Scholar
Eppig, J.J. & Downs, S.M. (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, 313–21.Google Scholar
Fan, H.Y., Huo, L.J., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2004). Protein kinase C and mitogen-activated protein kinase cascade in mouse cumulus cells: cross talk and effect on meiotic resumption of oocyte. Biol. Reprod. 70, 1178–87.Google Scholar
Gotze, M., Kauffold, P., Schuffenhauer, A., Torner, H. & Spitschak, M. (1990). [The inhibition of meiosis of bovine oocytes using biologic of synthetic inhibitors.] Arch. Exp. Veterinarmed. 44, 1927.Google Scholar
Jankowski, M., Reis, A.M., Mukkadam-Daher, S., Dam, T.V., Farookhi, R. & Gutkowska, J. (1997). C-type natriuretic peptide and the guanylyl cyclase receptors in the rat ovary modulated by the estrous cycle. Biol. Reprod. 56, 5966.CrossRefGoogle ScholarPubMed
Kadam, A.L. & Koide, S.S. (1990). Identification of hypoxanthine in bovine follicular fluid. J. Pharm. Sci. 79, 1077–82.Google Scholar
Kimura, N., Konno, Y., Miyoshi, K., Matsumoto, H. & Sato, E. (2002). Expression of hyaluronan synthases and CD44 messenger RNAs in porcine cumulus–oocyte complexes during in vitro maturation. Biol. Reprod. 66, 707–17.CrossRefGoogle ScholarPubMed
Kiyosu, C., Tsuji, T., Yamada, K., Kajita, S. & Kunieda, T. (2012). NPPC/NPR2 signaling is essential for oocyte meiotic arrest and cumulus oophorus formation during follicular development in the mouse ovary. Reproduction 144, 187–93.CrossRefGoogle ScholarPubMed
Norris, R.P., Ratzan, W.J., Freudzon, M., Mehlmann, L.M., Krall, J., Movsesian, M.A., Wang, H., Ke, H., Nikolaev, V.O. & Jaffe, L.A. (2009). Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136, 1869–78.Google Scholar
Petr, J., Rajmon, R., Chmelíková, E., Tománek, M., Lánská, V., Pribánová, M. & Jílek, F. (2006). Nitric-oxide-dependent activation of pig oocytes: the role of the cGMP-signalling pathway. Zygote 14, 916.Google Scholar
Petters, R.M. & Wells, K.D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 6173.Google Scholar
Pincus, G. & Enzmann, E.V. (1935). The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. J. Exp. Med. 62, 665–75.CrossRefGoogle ScholarPubMed
Potter, L.R., Abbey-Hosch, S. & Dickey, D.M (2006). Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr. Rev. 27, 4772.CrossRefGoogle ScholarPubMed
Rahmutula, D. & Gardner, D.G. (2005). C-type natriuretic peptide down-regulates expression of its cognate receptor in rat aortic smooth muscle cells. Endocrinology 146, 4968–74.CrossRefGoogle ScholarPubMed
Roh, S.G., Song, S.H., Cho, K.C., Katoh, K., Wittamer, V., Parmentier, M. & Sasaki, S. (2007). Chemerin—a new adipokine that modulates adipogenesis via its own receptor. Biochem. Biophys. Res. Commun. 362, 1013–8.Google Scholar
Sato, Y., Cheng, Y., Kawamura, K., Takae, S. & Hsueh, A.J. (2012). C-type natriuretic peptide stimulates ovarian follicle development. Mol. Endocrinol. 26, 1158–66.Google Scholar
Schmidt, H., Stonkute, A., Jüttner, R., Schäffer, S., Buttgereit, J., Feil, R., Hofmann, F. & Rathjen, F.G. (2007 ). The receptor guanylyl cyclase Npr2 is essential for sensory axon bifurcation within the spinal cord. J. Cell. Biol. 179, 331–40.CrossRefGoogle ScholarPubMed
Schulz, S. (2005). C-type natriuretic peptide and guanylyl cyclase B receptor. Peptides 26, 1024–34.CrossRefGoogle ScholarPubMed
Törnell, J., Carlsson, B. & Billing, H. (1990). Atrial natriuretic peptide inhibits spontaneous rat oocyte maturation. Endocrinology 126, 1504–8.CrossRefGoogle ScholarPubMed
Warikoo, P.K. & Bavister, B.D. (1989). Hypoxanthine and cyclic adenosine 5′-monophosphate maintain meiotic arrest of rhesus monkey oocytes in vitro. Fertil. Steril. 51, 886–9.Google Scholar
Webb, R.J., 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, 441–54.Google Scholar
Woodard, G.E. & Rosado, J.A. (2008). Natriuretic peptides in vascular physiology and pathology. Int. Rev. Cell. Mol. Biol. 268, 5993.CrossRefGoogle ScholarPubMed
Zhang, M., Su, Y.Q., Sugiura, K., Xia, G. & Eppig, J.J. (2010). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–9.CrossRefGoogle ScholarPubMed