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A specific adenylyl cyclase inhibitor (DDA) and a cyclic AMP-dependent protein kinase inhibitor (H-89) block the action of equine growth hormone on in vitro maturation of equine oocytes

Published online by Cambridge University Press:  26 September 2014

Gabriel Ribas Pereira ,
Pedro Luis Lorenzo ,
Gustavo Ferrer Carneiro ,
Sylvie Bilodeau-Goeseels ,
John Kastelic  and
Irwin K. M. Liu
Gabriel Ribas Pereira*
Affiliation:
Animal Science Department, School of Agronomy, Federal University of Rio Grande do Sul, Campus Agronomia, Ave. Bento Gonçalves 7712, Porto Alegre, 91540–000, RS, Brasil. Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA, USA.
Pedro Luis Lorenzo
Affiliation:
Animal Physiology Department, Veterinary School, Universidad Complutense de Madrid, Madrid, Spain.
Gustavo Ferrer Carneiro
Affiliation:
Animal Reproduction Department, Garanhuns Academic Unity, Federal Rural University of Pernambuco, Garanhuns, PE, Brazil.
Sylvie Bilodeau-Goeseels
Affiliation:
Agriculture and Agri-Food Canada Research Centre, Lethbridge, Canada.
John Kastelic
Affiliation:
Agriculture and Agri-Food Canada Research Centre, Lethbridge, Canada.
Irwin K. M. Liu
Affiliation:
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA, USA.
*
All correspondence to: Gabriel Ribas Pereira. Animal Science Department, School of Agronomy, Federal University of Rio Grande do Sul, Campus Agronomia, Ave. Bento Gonçalves 7712, Porto Alegre, 91540–000, RS, Brasil. Tel.: +55 55 99972240 or +55 51.33086958. e-mail: gabriel.pereira@ufrgs.br or gpereira@ucdavis.edu
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Summary

The objectives of this study were firstly to determine whether the stimulatory function of equine growth hormone (eGH) on equine oocyte maturation in vitro is mediated via cyclic adenosine monophosphate (cAMP); and secondly if the addition of eGH in vitro influences oocyte nuclear maturation and if this effect is removed when GH inhibitors are added to the culture. Cumulus–oocyte complexes (COCs) were recovered from follicles <25 mm in diameter and randomly allocated as follows: (i) control (no additives); and (ii) 400 ng/ml of eGH. A specific inhibitor against cyclic AMP-dependent protein kinase (H-89; 10−9, 10−11 or 10−15 M concentration) and a specific adenylate cyclase inhibitor, 2′,3′-dideoxyadenosine (DDA; 10−8, 10−10 or 10−14 M concentration) were used to observe whether they could block the eGH effect. After 30 h of in vitro maturation at 38.5°C with 5% CO2 in air, oocytes were stained with 10 μg/ml of Hoechst to evaluate nuclear status. More mature oocytes (P < 0.05) were detected when COCs were incubated with eGH (29 of 84; 34.5%) than in the control group (18 of 82; 21.9%). The H-89 inhibitor used at a concentration of 10−9 M (4 of 29; 13.8%) decreased (P < 0.05) the number of oocytes reaching nuclear maturation when compared with eGH (11 of 29; 38%). The DDA inhibitor at a concentration of 10−8 M (2 of 27; 7.4%) also reduced (P < 0.05) the number of oocytes reaching maturity when compared with the eGH group (9 of 30; 30%). Results from the present study show that H-89 and DDA can be used in vitro to block the eGH effect on equine oocyte maturation.

Keywords

Equine growth hormoneInhibitorsMeiosis resumptionOocyte maturation
Type
Research Article
Information
Zygote , Volume 23 , Issue 6 , December 2015 , pp. 795 - 801
Copyright
Copyright © Cambridge University Press 2014 

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References

Bevers, M.M. & Izadyar, F. (2002). Role of growth hormone and growth hormone receptor in oocyte maturation. Mol. Cell. Endocrinol. 197, 173–8.CrossRefGoogle ScholarPubMed
Chijiwa, T., Mishima, A., Hagiwara, M., Sano, M., Hayashi, K., Inoue, T., Naito, K., Toshioka, T. & Hidaka, H. (1990). Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 265, 5267–72.Google Scholar
Del Campo, M.R., Donoso, M.X., Parrish, J.J. & Ginther, O.J. (1990). In vitro fertilization of in vitro-matured equine oocytes. Equine Vet. Sci. 10, 18–22.Google Scholar
Dell’Aquila, M.E., Fusco, S., Lacandra, G.M. & Mariato, F. (1997). Intracytoplasmic sperm injection (ICSI) versus conventional IVF on abattoir-derived and in vitro-matured oocytes. Theriogenology 47, 1139–56.Google Scholar
Downs, S.M. & Hunzicker-Dunn, M. (1995). Differential regulation of oocyte maturation and cumulus expansion in the mouse oocyte–cumulus cell complex by site-selective analogs of cyclic adenosine monophosphate. Dev. Biol. 172, 72–85.Google Scholar
Eppig, J.J. & Downs, S.M. (1984). Chemical signals that regulate mammalian oocyte maturation. Biol. Reprod. 30, 1–11.Google Scholar
Guixue, Z., Luciano, A.M., Coenen, K., Gandolfi, F. & Sirard, M.A. (2001). The influence of cAMP before or during bovine oocyte maturation on embryonic developmental competence. Theriogenology 55, 1733–43.CrossRefGoogle ScholarPubMed
Hassan, H.A., Azab, H., Rahman, A.A. & Nafee, T.M. (2001). Effects of growth hormone on in vitro maturation of germinal vesicle of human oocytes retrieved from small antral follicles. J. Assist. Reprod. Genet. 18, 417–20.Google Scholar
Hinrichs, K. & Williams, K.A. (1997). Relationships among oocyte-cumulus morphology, follicular atresia, initial chromatin configuration, and oocyte meiotic competence in the horse. Biol. Reprod. 57, 377–84.Google Scholar
Hinrichs, K. & Schmidt, A.L. (2000). Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season. Biol. Reprod. 62, 1402–8.Google Scholar
Hinrichs, K. (2010). The equine oocyte: factors affecting meiotic and developmental competence. Mol. Reprod. Dev. 77, 651–61.Google Scholar
Izadyar, F., Colenbrander, B. & Bevers, M.M. (1996). In vitro maturation of bovine oocytes in the presence of growth hormone accelerates nuclear maturation and promotes subsequent embryonic development. Mol. Reprod. Dev. 45, 372–7.Google Scholar
Izadyar, F., Colenbrander, B. & Bevers, M.M. (1997a). Stimulatory effect of growth hormone on in vitro maturation of bovine oocytes is exerted through the cyclic adenosine 3′,5′-monophosphate signaling pathway. Biol. Reprod. 57, 1484–89.Google Scholar
Izadyar, F., Van Tol, H.T., Colenbrander, B. & Bevers, M.M. (1997b). Stimulatory effect of growth hormone on in vitro maturation of bovine oocytes is exerted through cumulus cells and not mediated by IGF-I. Mol. Reprod. Dev. 47, 175–80.Google Scholar
Izadyar, F., Hage, W.J., Colenbrander, B. & Bevers, M.M. (1998). The promotory effect of growth hormone on the developmental competence of in vitro matured bovine oocytes is due to improved cytoplasmic maturation. Mol. Reprod. Dev. 49, 444–53.Google Scholar
Izadyar, F., Van Tol, H.T., Hage, W.G. & Bevers, M.M. (2000). Preimplantation bovine embryos express mRNA of growth hormone receptor and respond to growth hormone addition during in vitro development. Mol. Reprod. Dev. 57, 247–55.Google Scholar
Kolle, S., Stojkovic, M., Prelle, K., Waters, M., Wolf, E. & Sinowatz, F. (2001). Growth hormone (GH)/GH receptor expression and GH-mediated effects during early bovine embryogenesis. Biol. Reprod. 64, 1826–34.Google Scholar
Kolle, S., Stojkovic, M., Reese, S., Reichenbach, H.D., Wolf, E. & Sinowatz, F. (2004). Effects of growth hormone on the ultrastructure of bovine preimplantation embryos. Cell Tissue Res. 317, 101–8.CrossRefGoogle ScholarPubMed
Liu, J.L. & LeRoith, D. (1999). Insulin-like growth factor I is essential for postnatal growth in response to growth hormone. Endocrinology. 140, 5178–84.Google Scholar
Liu, L., Kong, N., Xia, G. & Zhang, M. (2013). Molecular control of oocyte meiotic arrest and resumption. Reprod. Fertil. Dev. 25, 463–71.Google Scholar
Lupu, F., Terwilliger, J.D., Lee, K., Segre, G.V. & Efstratiadis, A. (2001). Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev. Biol. 229, 141–62.Google Scholar
Marchal, R., Caillaud, M., Martoriati, A., Gerard, N., Mermillod, P. & Goudet, G. (2003). Effect of growth hormone (GH) on in vitro nuclear and cytoplasmic oocyte maturation, cumulus expansion, hyaluronan synthases, and connexins 32 and 43 expression, and GH receptor messenger RNA expression in equine and porcine species. Biol. Reprod. 69, 1013–22.Google Scholar
Mehlmann, L.M., Jones, T.L.Z. & Jaffe, L.A. (2002). Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science 297, 1343–5.Google Scholar
Mermillod, P., Tomanek, M., Marchal, R. & Meijer, L. (2000). High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity. Mol. Reprod. Dev. 55, 89–95.Google Scholar
Moreira, F., Paula-Lopes, F.F., Hansen, P.J., Badinga, L. & Thatcher, W.W. (2002). Effects of growth hormone and insulin-like growth factor-I on development of in vitro derived bovine embryos. Theriogenology 57, 895–907.Google Scholar
Pereira, G.R., Lorenzo, P.L., Carneiro, G.F., Ball, B.A., Bilodeau-Goeseels, S., Kastelic, J., Pegoraro, L.M., Pimentel, C.A., Esteller-Vico, A., Illera, J.C., Granado, G.S., Casey, P. & Liu, I.K.M. (2013a). The involvement of growth hormone in equine oocyte maturation, receptor localization and steroid production by cumulus–oocyte complexes in vitro . Res. Vet. Sci. 95, 667–74.Google Scholar
Pereira, G.R., Lorenzo, P.L., Carneiro, G.F., Ball, B.A., Pegoraro, L.M.C., Pimentel, C.A. & Liu, I.K.M. (2013b). Influence of equine growth hormone, insulin-like growth factor-I and its interaction with gonadotropins on in vitro maturation and cytoskeleton morphology in equine oocytes. Animal 7, 1–7.Google Scholar
Pereira, G.R., Lorenzo, P.L., Carneiro, G.F., Ball, B.A., Goncalves, P.B., Pegoraro, L.M., Bilodeau-Goeseels, S., Kastelic, J.P., Casey, P.J. & Liu, I.K. (2012). The effect of growth hormone (GH) and insulin-like growth factor-I (IGF-I) on in vitro maturation of equine oocytes. Zygote 20, 353–60.Google Scholar
Raper, S., Kothary, P., Ishoo, E., Dikin, M., Kokudo, N., Hashimoto, M. & DeMatteo, R.P. (1995). Divergent mechanisms of insulin-like growth factor I and II on rat hepatocyte proliferation. Regul. Pept. 58, 55–62.Google Scholar
Rotwein, P., Gronowski, A.M. & Thomas, M.J. (1994). Rapid nuclear actions of growth hormone. Horm. Res. 42, 170–5.Google Scholar
Smit, L.S., Meyer, D.J., Billestrup, N., Norstedt, G., Schwartz, J. & Carter-Su, C. (1996). The role of the growth hormone (GH) receptor and JAK1 and JAK2 kinases in the activation of Stats 1, 3, and 5 by GH. Mol. Endocrinol. 10, 519–33.Google Scholar
Torner, H., Alm, H., Kanitz, W., Goellnitz, K., Becker, F., Poehland, R., Bruessow, K.P. & Tuchscherer, A. (2007). Effect of initial cumulus morphology on meiotic dynamic and status of mitochondria in horse oocytes during IVM. Reprod. Domest. Anim. 42, 176–83.Google Scholar
Yoshimura, Y., Iwashita, M., Karube, M., Oda, T., Akiba, M., Shiokawa, S., Ando, M., Yoshinaga, A. & Nakamura, Y. (1994). Growth hormone stimulates follicular development by stimulating ovarian production of insulin-like growth factor-I. Endocrinology 135, 887–94.Google Scholar
Zhang, J.J., Muzs, L.Z. & Boyle, M.S. (1990). In vitro fertilization of horse follicular oocytes matured in vitro . Mol. Reprod. Dev. 26, 361–5.Google Scholar
Zhao, J., Taverne, M.A., Van Der Weijden, G.C., Bevers, M.M. & Van Den Hurk, R. (2001). Insulin-like growth factor-I (IGF-I) stimulates the development of cultured rat pre-antral follicles. Mol. Reprod. Dev. 58, 287–96.Google Scholar