Czech J. Anim. Sci., 2011, 56(6):284-291 | DOI: 10.17221/1284-CJAS

Effects of inhibiting nitric oxide synthase on cumulus expansion and nuclear maturation of sheep oocytes

M. Heidari Amale1, A. Zare Shahne1, A. Abavisani2,3, S. Nasrollahi1
1 Department of Animal Science, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
2 Physiology Section, Department of Basic Sciences, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran
3 Embryonic and Stem Cell Biology and Biotechnology Research Group, Institute of Biotechnology, Ferdowsi University of Mashhad, Mashhad, Iran

Nitric oxide (NO) is a biological signaling molecule that plays a crucial role in oocyte maturation of mammalians. It is generated by the nitric oxide synthase (NOS) enzyme from l-arginine. Although the effect of NO has been shown in oocyte maturation of some species, there is no report about its effect on the in vitro maturation of sheep oocyte. So, this study aimed to investigate the importance of NO/NOS system in the in vitro maturation of ovine oocytes. Different concentrations of L-NAME (a NOS inhibitor) (0.1, 1 and 10mM) were added to maturation medium to evaluate the effect of inhibiting NOS on cumulus expansion and meiotic resumption of sheep oocytes. After 26 h culture, low and medium concentrations of L-NAME (0.1 and 1mM) had no significant effect on cumulus expansion, however, its higher concentration (10mM) decreased percentage of oocytes with total cumulus expansion as compared to control (P < 0.05). The extrusion of the first polar body was also suppressed in a dose-dependent manner, so that the addition of 10mM L-NAME to maturation medium significantly stopped oocytes in GV stage (P < 0.05). Moreover, to confirm the results and to evaluate if this effect is reversible, 0.1mM sodium nitroprusside (SNP, a NO donor) was added only to the maturation medium which had the highest concentration of L-NAME (10mM). The concomitant addition of NOS inhibitor with NO donor reversed the inhibitory effect of L-NAME on cumulus expansion and meiotic maturation. These results indicated that NO/NOS system is involved in the maturation of sheep oocytes.

Keywords: sheep; oocyte maturation; nitric oxide; L-NAME

Published: June 30, 2011  Show citation

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Heidari Amale M, Zare Shahne A, Abavisani A, Nasrollahi S. Effects of inhibiting nitric oxide synthase on cumulus expansion and nuclear maturation of sheep oocytes. Czech J. Anim. Sci.. 2011;56(6):284-291. doi: 10.17221/1284-CJAS.
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    References

    1. Albertini D.F. (1992): Regulation of meiotic maturation in the mammalian oocyte: interplay between exogenous cues and the microtubule cytoskeleton. Bioessays, 14, 97-103. Go to original source... Go to PubMed...
    2. Albertini D.F., Overstrom E.W., Ebert K.M. (1987): Changes in the organization of the actin cytoskeleton during preimplantation development of the pig embryo. Biology of Reproduction, 37, 441-451. Go to original source... Go to PubMed...
    3. 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. Go to original source... Go to PubMed...
    4. 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 signaling pathways. Molecular and Cellular Endocrinology, 223, 85-93. Go to original source... Go to PubMed...
    5. Chmelíková E., Sedmíková M., Petr J., Kott T., Lánská V., Tůmová L., Tichovská H., Ješeta M.: (2009): Expression and localization of nitric oxide synthase isoforms during porcine oocyte growth and acquisition of meiotic competence. Czech Journal of Animal Science, 54, 137-149. Go to original source...
    6. Chmelíková E., Jeseta M., Sedmíková M., Petr J., Tůmová L., Kott T., Lipovová P., Jílek F. (2010): Nitric oxide synthase isoforms and the effect of their inhibition on meiotic maturation of porcine oocytes. Zygote, 18, 235-244. Go to original source... Go to PubMed...
    7. Dixit V.,D., Parvizi N. (2001): Nitric oxide and the control of reproduction. Animal Reproduction Science, 65, 1-16. Go to original source... Go to PubMed...
    8. Eppig J.J. (1981): Prostaglandin E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice. Biology of Reproduction, 25, 191-195. Go to original source... Go to PubMed...
    9. Eppig J.J., Downs S.M. (1984): Chemical signals that regulate mammalian oocyte maturation. Biology of Reproduction, 30, 1-11. Go to original source... Go to PubMed...
    10. Gordo A.C., He C.L., Smith S., Fissore R.A. (2001): Mitogen activated protein kinase plays a significant role in metaphase II arrest, spindle morphology, and maintenance of maturation promoting factor activity in bovine oocytes. Molecular Reproduction and Development, 59, 106-114. Go to original source... Go to PubMed...
    11. 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, 403-409. Go to original source... Go to PubMed...
    12. Hurk R.V.D., Zhao J. (2005): Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology, 63, 1717-1751. Go to original source... Go to PubMed...
    13. Jablonka-Shariff A., Olson L.M. (1998): The role of nitric oxide in oocyte meiotic maturation and ovulation: meiotic abnormalities of endothelial nitric oxide synthase knock-out mouse oocytes. Endocrinology, 139, 2944-2954. Go to original source... Go to PubMed...
    14. Jablonka-Shariff A., Basuray R., Olson L.M. (1999): Inhibitors of nitric oxide synthase influence oocyte maturation in rats. Journal of the Society for Gynecologic Investigation, 6, 95-101. Go to original source... Go to PubMed...
    15. Jablonka-Shariff A., Olson L.M. (2000): Nitric oxide is essential for optimal meiotic maturation of murine cumulus-oocyte complexes in vitro. Molecular Reproduction and Development, 55, 412-421. Go to original source... Go to PubMed...
    16. Kenner J., Harel S., Granit R. (1991): Nitric oxide as an antioxidant. Archives of Biochemistry and Biophysics, 289, 130-136. Go to original source... Go to PubMed...
    17. 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. Biology of Reproduction, 66, 707-717. Go to original source... Go to PubMed...
    18. Klein S.L., Carnovale D., Burnett A.L., Wallach E.E., Zacur H.A., Crone J.K., Dawson V.L., Nelson R.J., Dawson T.M. (1998): Impaired ovulation in mice with targeted deletion of the neuronal isoform of nitric oxide synthase. Molecular Medicine, 4, 658-64. Go to original source...
    19. Lander H.M., Jacovina A.T., Davis R.J., Tauras J.M. (1996): Differential activation of mitogen-activated protein kinases by nitric oxide-related species. Journal of Biological Chemistry, 271, 19705-19709. Go to original source... Go to PubMed...
    20. Longo F.J., Chen D.Y. (1985): Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. Developmental Biology, 107, 382-394. Go to original source... Go to PubMed...
    21. Lu Q., Dunn R.L., Angeles R., Smith G.D. (2002): Regulation of spindle formation by active mitogen-activated protein kinase and protein phosphatase 2A during mouse oocyte meiosis. Biology of Reproduction, 66, 29-37. Go to original source... Go to PubMed...
    22. Matta S.G., Bussiere M.C.C., Viana K.S., Quirino C.R. (2002): Effect of different concentrations of the inhibitor of nitric oxide synthesis on the in vitro nuclear maturation of bovine oocytes. Revista Brasileira de Reproducao Animal, 26, 149-151. (in Portugese)
    23. 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 maturation of oocyte-cumulus complexes of cattle. Animal Reproduction Science, 111, 189-201. Go to original source... Go to PubMed...
    24. Mehlmann L.M. (2005): Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction, 130, 791-799. Go to original source... Go to PubMed...
    25. Messmer U.K., Lapetina E.G., Brune B. (1995): Nitric oxide-induced apoptosis in RAW 264.7 macrophages is antagonized by protein kinase C- and protein kinase A-activating compounds. Molecular Pharmacology, 47, 757-765.
    26. Moncada S., Palmer R.M., Higgs E.A. (1991): Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacological Reviews, 43, 109-142. Go to PubMed...
    27. Moor R.M., Heslop J.P. (1981): Cyclic AMP in mammalian follicle cells and oocytes during maturation. Journal of Experimental Zoology, 216, 205-209. Go to original source... Go to PubMed...
    28. Nakamura Y., Yamagata Y., Sugino N., Takayama H., Kato H. (2002): Nitric oxide inhibits oocyte meiotic maturation. Biology of Reproduction, 67, 1588-1592. Go to original source... Go to PubMed...
    29. Nathan C. (1992): Nitric oxide as a secretory product of mammalian cells. FASEB Journal, 6, 3051-3064. Go to original source...
    30. Rosselli M., Keller P.J., Dubey R.K. (1998): Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Human Reproduction Update, 4, 3-24. Go to original source... Go to PubMed...
    31. Schwarz K.R., Pires P.R., de Bem T.H., Adona P.R., Leal C.L. (2008): Consequences of nitric oxide synthase inhibition during bovine oocyte maturation on meiosis and embryo development. Reproduction in Domestic Animal, 45, 75-80. Go to original source... Go to PubMed...
    32. 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. Go to original source... Go to PubMed...
    33. 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. Go to original source... Go to PubMed...
    34. Sirard M.A., Coenen K., Bilodeau-Goeseels S. (1992): Effect of fresh or cutured follicular fraction on meiotic resumtion in bovine oocytes. Theriogenology, 37, 39-57. Go to original source...
    35. Tao Y., Fu Z., Zhang M., Xia G., Yang J., Xie H. (2004): 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. Go to original source... Go to PubMed...
    36. Tao J.Y., Fu Z., Zhang M.L., Xia G., Lei L., Wu Z.L. (2005a): Nitric oxide influences the meiotic maturation of porcine oocytes cultured in hypoxanthine-supplemented medium. Journal of Animal Physiology and Animal Nutrition (Berl), 89, 38-44. Go to original source... Go to PubMed...
    37. Tao Y., Xie H., Hong H., Chen X., Jang J., Xia G. (2005b): Effects of nitric oxide synthase inhibitors on porcine oocyte meiotic maturation. Zygote, 13, 1-9. Go to original source... Go to PubMed...
    38. 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. Reproduction in Domestic Animal, 41, 501-509. Go to original source... Go to PubMed...
    39. Thaler C.D., 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. Go to original source... Go to PubMed...
    40. Tosti E. (2006): Calcium ion currents mediating oocyte maturation events. Reproductive Biology and Endocrinology, 4, 26. Go to original source... Go to PubMed...
    41. Tranguch S., Steuerwald N., Huet-Hudson Y.M. (2003): Nitric oxide synthase production and nitric oxide regulation of preimplantation embryo development. Biology of Reproduction, 63, 1538-1544. Go to original source... Go to PubMed...
    42. Tripathi A., Kumar K.V., Chaube S.K. (2010): Meiotic cell cycle arrest in mammalian oocytes. Journal of Cellular Physiology, 223, 592-600. Go to original source... Go to PubMed...
    43. Van Voorhis B.J., Moore K., Strijbos P.J., 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. Effects of gonadotropin stimulation in vivo. Journal of Clinical Investigation, 96, 2719-2726. Go to original source... Go to PubMed...
    44. Viana K.S., Caldas-Bussiere M.C., Matta S.G., Faes M.R., de Carvalho C.S., Quirino C.R. (2007): Effect of sodium nitroprusside, a nitric oxide donor, on the in vitro maturation of bovine oocytes. Animal Reproduction Science, 102, 217-227. Go to original source... Go to PubMed...
    45. Yamauchi J., Miyazaki T., Iwasaki S., Kishi I., Kuroshima M., Tei C., Yoshimura Y. (1997): Effects of nitric oxide on ovulation and ovarian steroidogenesis and prostaglandin production in the rabbit. Endocrinology, 138, 3630-3637. Go to original source... Go to PubMed...

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