Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-25T21:04:12.443Z Has data issue: false hasContentIssue false

Influence of nitric oxide and phosphodiesterases during in vitro maturation of bovine oocytes on meiotic resumption and embryo production

Published online by Cambridge University Press:  27 June 2017

Ramon Cesar Botigelli*
Affiliation:
Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil. Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil. Departamento de Farmacologia, Instituto de Biociências de Botucatu, Universidade do Estado de São Paulo, Distrito de Rubião Junior, Botucatu - SP, CEP 18618–691, Brasil.
Katia Lancellotti Schwarz
Affiliation:
Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil.
Fabiane Gilli Zaffalon
Affiliation:
Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil.
Maite Del Collado
Affiliation:
Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil.
Fernanda Cavallari Castro
Affiliation:
Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil.
Hugo Fernandes
Affiliation:
Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil.
Claudia Lima Verde Leal
Affiliation:
Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil.
*
All correspondence to: Ramon Cesar Botigelli. Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga-SP, CEP 13635–900, Brasil. Tel:/Fax: +55 14 3880 0238. E-mail: [email protected]

Summary

This study aimed to examine the effects of nitric oxide (NO) and different phosphodiesterase (PDE) families on meiosis resumption, nucleotides levels and embryo production. Experiment I, COCs were matured in vitro with the NO donor S-nitroso-N-acetylpenicillamine (SNAP) associated or not with the soluble guanylate cyclase (sGC) inhibitor 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ), meiotic resumption and nucleotides levels were assessed. SNAP delayed germinal vesicle breakdown (GVBD) (53.4 ± 1.2 versus 78.4 ± 2.4% for controls, P < 0.05) and ODQ reversed its effect (73.4 ± 6.3%, P > 0.05). Cyclic GMP levels were higher in SNAP (3.94 ± 0.18, P < 0.05) and ODQ abolished the effect (2.48 ± 0.13 pmol/COC, P < 0.05), while cAMP levels were decreased in both treatments. Experiment II, COCs were cultured with SNAP alone or with PDEs inhibitors. SNAP alone or with PDEs inhibitors delayed GVBD (24.7 ± 2.8 to 56.9 ± 8.7%, P < 0.05) compared with the control (77.1 ± 1.8%), and SNAP and SNAP + cilostamide had lowest rates (34.9 ± 9.2% and 24.7 ± 2.8%). Experiment III, COCs were cultured (24–28 h) with SNAP and SNAP + cilostamide to assess metaphase II (MII) rates and embryo production. SNAP + cilostamide (50.0 ± 2.0%, P < 0.05) had lower MII rates at 24 h in vitro maturation (IVM), but at 28 h all groups were similar (66.6 to 71.4%, P > 0.05). Embryo development did not differ from the control for SNAP and cilostamide groups (38.7 ± 5.8, 37.9 ± 6.2 and 40.5 ± 5.8%, P > 0.05), but SNAP + cilostamide decreased embryo production (25.7 ± 6.9%, P < 0.05). In conclusion, SNAP was confirmed to delay meiosis resumption by the NO/sGC/cGMP pathway, by increasing cGMP, but not cAMP. Inhibiting different PDEs to further increase nucleotides in association with SNAP did not show any additive effects on meiosis resumption, indicating that other pathways are involved. Moreover, SNAP + cilostamide affected the meiosis progression and decreased embryo development.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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

Albuz, F.K., Sasseville, M., Lane, M., Armstrong, D.T., Thompson, J.G. & Gilchrist, R.B. (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod. 25, 29993011.CrossRefGoogle ScholarPubMed
Basini, G. & Grasselli, F. (2015). Nitric oxide in follicle development and oocyte competence. Reproduction 150, R1–9.CrossRefGoogle ScholarPubMed
Bilodeau-Goeseels, S. (2007). Effects of manipulating the nitric oxide/cyclic GMP pathway on bovine oocyte meiotic resumption in vitro . Theriogenology 68, 693701.CrossRefGoogle ScholarPubMed
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 . Mol. Cell. Endocrinol. 207, 2130.CrossRefGoogle ScholarPubMed
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. Mol. Cell. Endocrinol. 223, 8593.CrossRefGoogle ScholarPubMed
de Loos, F., Kastrop, P., Van Maurik, P., Van Beneden, T.H. & Kruip, T. A. (1991). Heterologous cell contacts and metabolic coupling in bovine cumulus oocyte complexes. Mol. Reprod. Dev. 28, 255–9.CrossRefGoogle ScholarPubMed
Denninger, J.W. & Marletta, M. A. (1999). Guanylate cyclase and the.NO/cGMP signaling pathway. Biochim. Biophys. Acta 1411, 334–50.CrossRefGoogle ScholarPubMed
Dieci, C., Lodde, V., Franciosi, F., Lagutina, I., Tessaro, I., Modina, S.C., Albertini, D.F., Lazzari, G., Galli, C. & Luciano, A. M. (2013). The effect of cilostamide on gap junction communication dynamics, chromatin remodeling, and competence acquisition in pig oocytes following parthenogenetic activation and nuclear transfer. Mol. Reprod. Dev. 89, 111.Google ScholarPubMed
Dubeibe, D.F., Caldas-Bussiere, M.C., Maciel, V.L. Jr, Sampaio, W.V., Quirino, C.R., Gonçalves, P.B.D., De Cesaro, M.P. & Faes, M.R. & Paes de Carvalho, C.S. (2017). l-Arginine affects the IVM of cattle cumulus–oocyte complexes. Theriogenology 88, 134–44.CrossRefGoogle ScholarPubMed
Eppig, J.J. & Downs, S. M. (1984). Chemical signals that regulate mammalian oocyte maturation. Mol. Reprod. Dev. 30, 111.Google ScholarPubMed
Francis, S.H., Busch, L.J. & Corbin, D.J. (2010). cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol. Rev. 62, 525–63.CrossRefGoogle ScholarPubMed
Francis, S.H., Blount, M.A. & Corbin, J. D. (2011). Mammalian cyclic nucleotide phosphodiesterases: molecular mechanisms and physiological functions. Physiol. Rev. 91, 651–90.CrossRefGoogle ScholarPubMed
Gharibi, S., Hajian, M., Ostadhosseini, S., Hosseini, S.M., Forouzanfar, M. & Nasr-Esfahani, M.H. (2013). Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes. Theriogenology 80, 302–12.CrossRefGoogle ScholarPubMed
Hanna, C.B., Yao, S., Wu, X. & Jensen, J.T. (2012). Identification of phosphodiesterase 9A as a cyclic guanosine monophosphate-specific phosphodiesterase in germinal vesicle oocytes: a proposed role in the resumption of meiosis. Fertil. Steril. 98, 48795.e1.CrossRefGoogle ScholarPubMed
Holm, P., Booth, P.J., Schmidt, M.H., Greve, T. & Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683700.CrossRefGoogle ScholarPubMed
Ignarro, L.J., Buga, G.M., Wood, K.S., Byrns, R.E. & Chaudhuri, G. (1987). Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. USA 84, 9265–9.CrossRefGoogle ScholarPubMed
Ignarro, L.J., Cirino, G., Casini, A. & Napoli, C. (1999). Nitric oxide as a signaling molecule in the vascular system: an overview. J. Cardiovasc. Pharmacol. 34, 879–86.CrossRefGoogle ScholarPubMed
Izadyar, F., Zeinstra, E. & Bevers, M.M. (1998). Follicle-stimulating hormone and growth hormone act differently on nuclear maturation while both enhance developmental competence of in vitro matured bovine oocytes. Mol. Reprod. Dev. 51, 339–45.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Jablonka-Shariff, A., Basuray, R. & Olson, L.M. (1999). Inhibitors of nitric oxide synthase influence oocyte maturation in rats. J. Soc. Gynecol. Investig. 6, 95101.CrossRefGoogle ScholarPubMed
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, 2944–54.CrossRefGoogle ScholarPubMed
Lodde, V, Modina, S, Galbusera, C, Franciosi, F & Luciano, A.M. (2007). Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol. Reprod. Dev. 74, 740–9.CrossRefGoogle ScholarPubMed
Luciano, A.M., Pocar, P., Milanesi, E., Modina, S., Rieger, D., Lauria, A. & Gandolfi, F. (1999). Effect of different levels of intracellular cAMP on the in vitro maturation of cattle oocytes and their subsequent development following in vitro fertilization. Mol. Reprod. Dev. 54, 8691.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Masciarelli, S., Horner, K., Liu, C., Park, S.H., Hinckley, M., Hockman, S., Nedachi, T., Jin, C., Conti, M. & Manganiello, V. (2004). Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J. Clin. Invest. 114, 196205.CrossRefGoogle Scholar
Mayes, M.A. & Sirard, M. A. (2002). Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol. Reprod. 66, 180–4.CrossRefGoogle ScholarPubMed
Murthy, K. S. (2001). Activation of phosphodiesterase 5 and inhibition of guanylate cyclase by cGMP-dependent protein kinase in smooth muscle. Biochem. J. 15, 199208.CrossRefGoogle Scholar
Nakamura, Y. (2002). Nitric oxide inhibits oocyte meiotic maturation. Mol. Reprod. Dev. 67, 1588–92.Google ScholarPubMed
Nogueira, D., Cortvrindt, R., De Matos, D.G., Vanhoutte, L. & Smitz, J. (2003). Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro . Mol. Reprod. Dev. 69, 2045–52.Google ScholarPubMed
Norris, R.P., Ratza, 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.CrossRefGoogle ScholarPubMed
Parrish, J. J. (2014). Bovine in vitro fertilization: in vitro oocyte maturation and sperm capacitation with heparin. Theriogenology 81, 6773.CrossRefGoogle ScholarPubMed
Pires, P.R., Santos, N.P., Adona, P.R., Natori, M.M., Schwarz, K.R.L., De Bem, T.H. & Leal, C.L.V. (2009). Endothelial and inducible nitric oxide synthases in oocytes of cattle. Anim. Reprod. Sci. 116, 233–43.CrossRefGoogle ScholarPubMed
Potter, L.R. (2011). Guanylyl cyclase structure, function and regulation. Cell Signal. 23, 1921–6.CrossRefGoogle ScholarPubMed
Sadler, S.E. & Maller, J.L. (1989). A similar pool of cyclic AMP phosphodiesterase in Xenopus oocytes is stimulated by insulin, insulin-like growth factor 1, and [Val12,Thr59]Ha-ras protein. J. Biol. Chem. 264, 856–61.CrossRefGoogle ScholarPubMed
Sasseville, M., Albuz, F.K., Côté, N., Guillemette, C., Gilchrist, R.B. & Richard, F.J. (2009). Characterization of novel phosphodiesterases in the bovine ovarian follicle. Mol. Reprod. Dev. 81, 415–25.Google ScholarPubMed
Sasseville, M., Côté, N., Gagnon, M.-C. & Richard, F.J. (2008). Up-regulation of 3’5’-cyclic guanosine monophosphate-specific phosphodiesterase in the porcine cumulus–oocyte complex affects steroidogenesis during in vitro maturation. Endocrinology 149, 5568–76.CrossRefGoogle Scholar
Schwarz, K.R., Pires, P.R., Adona, P.R., Camara de Bem, T.H. & Leal, C.L. (2008). Influence of nitric oxide during maturation on bovine oocyte meiosis and embryo development in vitro . Reprod. Fertil. Dev. 20, 529–36.CrossRefGoogle ScholarPubMed
Schwarz, K.R.L., Pires, P.R.L., de Bem, T.H.C., Adona, P.R. & Leal, C.L. (2010). Consequences of nitric oxide synthase inhibition during bovine oocyte maturation on meiosis and embryo development. Reprod. Domest. Anim. 45, 7580.CrossRefGoogle ScholarPubMed
Schwarz, K.R.L., Pires, P.R.L., Mesquita, L.G., Chiaratti, M.R. & Leal, C.L. (2014). Effect of nitric oxide on the cyclic guanosine monophosphate (cGMP) pathway during meiosis resumption in bovine oocytes. Theriogenology 81, 556–64.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. Mol. Reprod. Dev. 78, 1111–8.Google ScholarPubMed
Shu, Y., Zeng, H., Ren, Z., Zhuang, G., Liang, X.-Y., Shen, H., Yao, S., Ke, P. & Wang, N. (2008). Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum. Reprod. 23, 504–13.CrossRefGoogle ScholarPubMed
Sriraman, V., Rudd, M.D., Lohmann, S.M., Mulders, S.M. & Richards, J.S. (2006). Cyclic guanosine 5´-monophosphate-dependent protein kinase II is induced by luteinizing hormone and progesterone receptor-dependent mechanisms in granulosa cells and cumulus oocyte complexes of ovulating follicles. Mol. Endocrinol. 20, 348–61.CrossRefGoogle Scholar
Sudano, M.J., Paschoal, D.M., da Silva Rascado, T., Magalhães, L.C.O., Crocomo, L.F., de Lima-Neto, J.F. & da Cruz Landim-Alvarenga, F. (2011). Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology 75, 1211–20.CrossRefGoogle ScholarPubMed
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. Mol. Cell. Endocrinol. 222, 93103.CrossRefGoogle ScholarPubMed
Tesfaye, D.A., Kadanga, F. & Bauch, K. (2006). The effect of nitric oxide inhibition and temporal expression patterns of them RNA and protein products of nitric oxide synthase genes during in vitro development of bovine pre-implantation embryos. Reprod. Domest. Anim. 41, 501–9.CrossRefGoogle ScholarPubMed
Thomas, R.E., Armstrong, D.T. & Gilchrist, R.B. (2002). Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Dev. Biol. 244, 215–25.CrossRefGoogle ScholarPubMed
Thomas, R.E., Thompson, J.G., Armstrong, D.T. & Gilchrist, R.B. (2004a). Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol. Reprod. 71, 1142–9.CrossRefGoogle ScholarPubMed
Thomas, R.E., Armstrong, D.T. & Gilchrist, R. B. (2004b). Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels. Biol. Reprod. 70, 548–56.CrossRefGoogle ScholarPubMed
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 Physiol. Scand. 139, 511–7.CrossRefGoogle Scholar
Tsafriri, A., Chun, S.Y., Zhang, R., Hsueh, A.J. & Conti, M. (1996). Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 178, 393402.CrossRefGoogle ScholarPubMed
Vanhoutte, L., De Sutter, P., Nogueira, D., Gerris, J., Dhont, M. & Van der Elst, J. (2007). Nuclear and cytoplasmic maturation of in vitro matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor. Hum. Reprod. 22, 1239–46.CrossRefGoogle ScholarPubMed
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. Anim. Reprod. Sci. 102, 217–27.CrossRefGoogle ScholarPubMed
Wang, S., Ning, G., Chen, X., Yang, J., Ouyang, H., Zhang, H. & Tai, P., Mu, X., Zhou, B., Zhang, M. & Xia, G. (2008). PDE5 modulates oocyte spontaneous maturation via cGMP-cAMP but not cGMP-PKG signaling. Front. Biosci. 13, 7087–95.CrossRefGoogle Scholar