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Nitric oxide synthase isoforms and the effect of their inhibition on meiotic maturation of porcine oocytes

Published online by Cambridge University Press:  29 January 2010

Eva Chmelíková ,
Michal Ješeta ,
Markéta Sedmíková ,
Jaroslav Petr ,
Lenka Tůmová ,
Tomáš Kott ,
Petra Lipovová  and
František Jílek
Eva Chmelíková
Affiliation:
Czech University of Life Sciences in Prague, Department of Veterinary Sciences, Kamýcká 129, 165 21 Prague 6 – Suchdol, Czech Republic.
Michal Ješeta
Affiliation:
Veterinary Research Institute, Hudcova 70, Brno, 621 00, Czech Republic.
Markéta Sedmíková*
Affiliation:
Department of Veterinary Sciences, Czech University of Life Sciences in Prague, Kamýcká 129, 165 21 Prague 6 – Suchdol, Czech Republic.
Jaroslav Petr
Affiliation:
Research Institute of Animal Production, Přátelství 815, 104 01 Prague 10 – Uhříněves, Czech Republic.
Lenka Tůmová
Affiliation:
Czech University of Life Sciences in Prague, Department of Veterinary Sciences, Kamýcká 129, 165 21 Prague 6 – Suchdol, Czech Republic.
Tomáš Kott
Affiliation:
Research Institute of Animal Production, Přátelství 815, 104 01 Prague 10 – Uhříněves, Czech Republic.
Petra Lipovová
Affiliation:
Institute of Chemical Technology, Department of Biochemistry and Microbiology, Technická 5, 166 28 Praha 6 Prague, Czech Republic.
František Jílek
Affiliation:
Czech University of Life Sciences in Prague, Department of Veterinary Sciences, Kamýcká 129, 165 21 Prague 6 – Suchdol, Czech Republic.
*
All correspondence to: Markéta Sedmíková. Department of Veterinary Sciences, Czech University of Life Sciences in Prague, Kamýcká 129, 165 21 Prague 6 – Suchdol, Czech Republic. Tel: +420 224382933. Fax: +420 234381841. e-mail: sedmikova@af.czu.cz
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Summary

In this paper we assessed: (i) the change in nitric oxide synthase (NOS) isoforms' expression and intracellular localization and in NOS mRNA in porcine oocytes during meiotic maturation; (ii) the effect of NOS inhibition by Nω-nitro-l-arginine methyl ester (l-NAME) and aminoguanidine (AG) on meiotic maturation of cumulus–oocyte complexes (COC) as well as denuded oocytes (DO); and (iii) nitric oxide (NO) formation in COC. All three NOS isoforms (eNOS, iNOS and nNOS) and NOS mRNA (eNOS mRNA, iNOS mRNA and nNOS mRNA) were found in both porcine oocytes and their cumulus cells except for nNOS mRNA, which was not detected in the cumulus cells. NOS isoforms differed in their intracellular localization in the oocyte: while iNOS protein was dispersed in the oocyte cytoplasm, nNOS was localized in the oocyte cytoplasm and in germinal vesicles (GV) and eNOS was present in dots in the cytoplasm, GV and was associated with meiotic spindles. l-NAME inhibitor significantly suppressed metaphase (M)I to MII transition (5.0 mM experimental group: 34.9% MI, control group: 9.5% MI) and at the highest concentration (10.0 mM) also affected GV breakdown (GVBD); in contrast also AG inhibited primarily GVBD. The majority of the oocytes (10.0 mM experimental group: 60.8%, control group: 1.2%) was not able to resume meiosis. AG significantly inhibited GVBD in DO, but l-NAME had no significant effect on the GVBD of these cells. During meiotic maturation, NO is formed in COC and the NO formed by cumulus cells is necessary for the process of GVBD.

Keywords

Cumulus cellsMeiotic maturationNOSOocytePig
Type
Research Article
Information
Zygote , Volume 18 , Issue 3 , August 2010 , pp. 235 - 244
Copyright
Copyright © Cambridge University Press 2010

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References

Abe, K., Matsuoka, K., Inoue, N., Taga, M. & Kato, T. (1999). Messenger RNA of neuronal nitric oxide synthase is expressed and possibly function in mouse oocytes and embryos during preimplantation development. Biomed. Res. 20, 61–5.CrossRefGoogle Scholar
Alderton, W.K., Cooper, C.E. & Knowles, R.G. (2001). Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357, 593–615.CrossRefGoogle ScholarPubMed
Bilodeau-Goeseels, S. (2007). Effects of manipulating the nitric oxide/cyclic GMP pathway on bovine oocyte meiotic resumption in vitro. Theriogenology 68, 693–701.CrossRefGoogle ScholarPubMed
Bredt, D.S., Hwang, P.M., Glatt, C.E., Lowenstein, C., Reed, R.R. & Snyder, S.H. (1991). Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351, 714–8.CrossRefGoogle ScholarPubMed
Brenman, J.E., Xia, H., Chao, D.S., Black, S.M. & Bredt, D.S. (1997). Regulation of neuronal nitric oxide synthase through alternative transcripts. Dev. Neurosci. 19, 224–31.CrossRefGoogle ScholarPubMed
Bu, S.M., Xia, G.L., Tao, Y., Lei, L. & Zhou, B. (2003). Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol. Cell. Endocrinol. 207, 21–30.CrossRefGoogle ScholarPubMed
Gonzalez-Cadavid, N.F., Burnett, A.L., Magee, T.R., Zeller, C.B., Vernet, D., Smith, N., Gitter, J. & Rajfer, J. (2000). Expression of penile neuronal nitric oxide synthase variants in the rat and mouse penile nerves. Biol. Reprod. 63, 704–14.CrossRefGoogle ScholarPubMed
Graselli, F., Ponderato, N., Basini, G. & Tamanini, C. (2001). Nitric oxide synthase expression and nitric oxide/cyclic GMP pathway in swine granulose cells. Domest. Anim. Endocrinol. 20, 241–52.CrossRefGoogle Scholar
Gregg, A.R. (2003). Mouse models and the role of nitric oxide in reproduction. Curr. Pharm. Design. 9, 391–8.CrossRefGoogle ScholarPubMed
Hattori, M., Nishida, N., Takesue, K., Kato, Y. & Fujihara, N. (2000). FSH suppression of nitric oxide synthesis in porcine oocytes. J. Mol. Endocrinol. 24, 65–73.CrossRefGoogle ScholarPubMed
Hattori, M., Arai, M., Saruwatari, K. & Kato, Y. (2004). Estrogen regulation of nitric oxide synthesis in the porcine oocyte. Mol. Cell. Biochem. 260, 13–9.CrossRefGoogle ScholarPubMed
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-derived nitric oxide regulates germinal vesicle breakdown and first polar body emission in the mouse oocyte. Reproduction 129, 403–9.CrossRefGoogle ScholarPubMed
Jablonka-Shariff, A. & Olson, L.M. (1997). Hormonal regulation of nitric oxide synthases and their cell-specific expression during follicular development in the rat ovary. Endocrinology 138, 460–80.CrossRefGoogle ScholarPubMed
Jablonka-Shariff, A. & Olson, L.M. (1998). The role of nitric oxide in meiotic maturation and ovulation: meiotic abnormalities of endothelial nitric oxide synthase knock-out mouse oocytes. Endocrinology 139, 2944–54.CrossRefGoogle ScholarPubMed
Jablonka-Shariff, A. & Olson, L.M. (2000). Nitric oxide is essential for optimal meiotic maturation of murine cumulus–oocyte complexes in vitro. Mol. Reprod. Dev. 55, 412–21.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Kuo, R.C., Baxter, G.T., Thompson, S.H., Stricker, S.A., Patton, C., Bonaventura, J. & Epel, D. (2000). NO is necessary and sufficient for egg activation at fertilization. Nature 406, 633–6.CrossRefGoogle ScholarPubMed
Kwon, N.S., Nathan, C.F., Gilker, C., Griffith, O.W., Matthews, D.E. & Stuehr, D.J. (1990). l-Citrulline production from l-arginine by macrophage nitric-oxide synthase – the ureido oxygen derives from dioxygen. J. Biol. Chem. 265, 13442–5.CrossRefGoogle ScholarPubMed
Lamas, S., Marsden, P.A., Li, G.K., Tempst, P. & Michel, T. (1992). Endothelial nitric-oxide synthase-molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc. Natl. Acad. Sci. USA 89, 6348–52.CrossRefGoogle Scholar
Matta, S.G., Caldas-Bussiere, M.C., Viana, K.S., Faes, M.R., Paes de Carvalho, C.S., Dias, B.L. & Quirino, C.R. (2009). Effect of inhibition of synthesis of inducible nitric oxide synthase-derived nitric oxide by aminoguanidine on the in vitro maturation of oocyte–cumulus complexes of cattle. Anim. Reprod. Sci. 111, 189–201.CrossRefGoogle ScholarPubMed
Meinecke, B. & Krischek, C. (2003). MAPK/ERK kinase (MEK) signalling is required for resumption of meiosis in cultured cumulus-enclosed pig oocytes. Zygote 11, 7–16.CrossRefGoogle ScholarPubMed
Mitchell, L.M., Kennedy, C.R. & Hartshorne, G.M. (2004). Expression of nitric oxide synthase and effect of substrate manipulation of the nitric oxide pathway in mouse ovarian follicles Hum. Reprod. 19, 30–40.CrossRefGoogle ScholarPubMed
Moncada, S., Palmer, R.M.J. & Higgs, E.A. (1991). Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol. Rev. 43, 109–42.Google ScholarPubMed
Nathan, C. (1992). Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 3051–64.CrossRefGoogle ScholarPubMed
Palmer, A., Gavin, A.C. & Nebreda, A.R. (1998). A link between MAP kinase and p(34cdc2) cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1. EMBO J. 17, 5037–47.CrossRefGoogle Scholar
Schwarz, K.R.L., Pires, P.R.L., Adona, P.R., de Bem, T.H.C. & Leal, C.L.V. (2008). Influence of nitric oxide during maturation on bovine oocyte meiosis and embryo development in vitro. Eprod. Fertil. Dev. 20, 529–36.CrossRefGoogle ScholarPubMed
Sela-Abramovich, S., Galiani, D., Nevo, N. & Dekel, N. (2008). Inhibition of rat oocyte maturation and ovulation by nitric oxide: mechanism of action. Biol. Reprod. 78, 1111–8.CrossRefGoogle ScholarPubMed
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. Mol. Reprod. Dev. 58, 262–8.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
Su, Y., Kondrikov, D. & Block, E.R. (2005). Cytoskeletal regulation of nitric oxide synthase. Cell Biochem. Biophys. 43, 439–49.CrossRefGoogle ScholarPubMed
Takesue, K., Tabata, S., Sato, F. & Hattori, M. (2003). Expression of nitric oxide synthase-3 in porcine oocytes obtained at different follicular development. J. Reprod. Dev. 49, 135–40.CrossRefGoogle ScholarPubMed
Tao, Y., Fu, Z., Zhang, M.J., Xia, G.L., Yang, J. & Xie, H.R. (2004). Immunohistochemical localization of inducible and endothelial nitric oxide synthase in porcine ovaries and effects of NO on antrum formation and oocyte meiotic maturation. Mol. Cell. Endocrinol. 222, 93–103.CrossRefGoogle ScholarPubMed
Tao, Y., Xie, H.R., Hong, H.Y., Chen, X.F., Jang, J. & Xia, G.L. (2005). Effects of nitric oxide synthase inhibitors on porcine oocyte meiotic maturation. Zygote 13, 1–9.CrossRefGoogle ScholarPubMed
Tesfaye, D., Kadanga, A., Rings, F., Bauch, K., Jennen, D., Nganvongpanit, K., Holker, M., Tholen, E., Ponsuksili, S., Wimmers, K., Montag, M., Gilles, M., Kirfel, G., Herzog, V. & Schellander, K. (2006). The effect of nitric oxide inhibition and temporal expression patterns of the mRNA and protein products of nitric oxide synthase genes during in vitro development of bovine pre-implantation embryos. Reprod. Dom. Anim. 41, 501–9.CrossRefGoogle ScholarPubMed
Van Voorhis, B.J., Moore, K., Strijbos, P.J.L., Nelson, S., Baylis, S.A., Grzybicki, D. & Weiner, C.P. (1995). Expression and localization of inducible and endothelial nitric oxide synthase in the rat ovary. J. Clin. Invest. 96, 2719–26.CrossRefGoogle ScholarPubMed
Viana, K.S., Caldas-Bussiere, M.C., S.G.C., Faes, M.R., de Carvalho, C.S.P. & Quirino, C.R. (2007). Effect of sodium nitroprusside, a nitric oxide donor, on the in vitro maturation of bovine oocytes. Anim. Reprod. Sci. 102, 217–27.CrossRefGoogle ScholarPubMed
Wassarman, P.M. (1988). The mammalian ovum. In The Physiology of Reproduction, (eds Knobil, E. & Neill, J.), pp. 69–102. New York: Raven Press.Google Scholar
Wongsrikeao, P., Kaneshige, Y., Ooki, R., Taniguchi, M., Agung, B., Nii, M. & Otoi, T. (2005). Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod. Domest. Anim. 40, 166–70.CrossRefGoogle ScholarPubMed
Zini, A., O'Bryan, M.S. & Schlegel, P.N. (1996). Immunohistochemical localization of endothelial nitric oxide synthase in human testis, epididymis and vas deferens suggests a possible role for nitric oxide in spermatogenesis, sperm maturation and programmed cell death. Biol. Reprod. 55, 935–41.CrossRefGoogle ScholarPubMed