Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T06:32:35.172Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of growth hormone (GH) and insulin-like growth factor-I (IGF-I) on in vitro maturation of equine oocytes

Published online by Cambridge University Press:  28 July 2011

Gabriel Ribas Pereira ,
Pedro Luis Lorenzo ,
Gustavo Ferrer Carneiro ,
Barry Allen Ball ,
Paulo Bayard Dias Gonçalves ,
Lígia Maria Cantarelli Pegoraro ,
Sylvie Bilodeau-Goeseels ,
John P. Kastelic ,
Patrick J. Casey  and
Irwin K. M. Liu
Gabriel Ribas Pereira*
Affiliation:
Laboratory of Biotechnology and Animal Reproduction–BioRep, Federal University of Santa Maria, Ave. Roraima #1000, CEP: 97105–900, Santa Maria, RS, Brazil. Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, USA.
Pedro Luis Lorenzo
Affiliation:
Departamento de Fisiología Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, Madrid, Spain.
Gustavo Ferrer Carneiro
Affiliation:
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, USA.
Barry Allen Ball
Affiliation:
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, USA.
Paulo Bayard Dias Gonçalves
Affiliation:
Laboratory of Biotechnology and Animal Reproduction - BioRep, Federal University of Santa Maria, Santa Maria, Brazil.
Lígia Maria Cantarelli Pegoraro
Affiliation:
Animal Reproduction Laboratory, EMBRAPA Temperate Climate Research Corporation, Pelotas, Brazil.
Sylvie Bilodeau-Goeseels
Affiliation:
Agriculture and Agri-Food Canada Research Centre, Lethbridge, Canada.
John P. Kastelic
Affiliation:
Agriculture and Agri-Food Canada Research Centre, Lethbridge, Canada.
Patrick J. Casey
Affiliation:
Research Centre in Reproductive Medicine, University of Auckland, Auckland, New Zealand.
Irwin K. M. Liu
Affiliation:
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, USA.
*
All correspondence to: Gabriel Ribas Pereira. Laboratory of Biotechnology and Animal Reproduction–BioRep, Federal University of Santa Maria, Ave. Roraima #1000, CEP: 97105–900, Santa Maria, RS, Brazil. Tel: +55 55 3220–8752. Fax: +55 55 3220 8484. E-mail: gabrielrp@biorep.ufsm.br or grpereira@vmth.ucdavis.edu
Get access Rights & Permissions [Opens in a new window]

Summary

The objective of this study was to test the hypothesis that equine growth hormone (eGH), in combination with insulin growth factor-I (IGF-I), influences positively in vitro nuclear and cytoplasmic maturation of equine oocytes. Cumulus–oocyte complexes were recovered from follicles that were < 25 mm in diameter, characterized by morphology and were allocated randomly as follow: (a) control (no additives); (b) 400 ng/ml eGH; (c) 200 ng/ml IGF-I; (d) eGH + IGF-I; and (e) eGH + IGF-I + 400 ng/ml anti-IGF-I antibody. Oocytes were matured for 30 h at 38.5°C in air with 5% CO2 and then stained with 10 μg/ml propidium iodide (PI) to evaluate nuclear status and 10 μg/ml Lens culinaris agglutinin-fluorescein complex (FITC-LCA) to assess cortical granule migration by confocal microscopy. The proportion of immature oocytes that developed to the metaphase II (MII) stage in the eGH + IGF-I group (15 of 45) was greater than in the groups that were treated only with IGF-I (7 of 36, p = 0.03). Oocytes that reached MII in the control group (20 of 56; 35.7%) showed a tendency to be different when compared with eGH + IGF-I group (15 of 45; 33.3%, p = 0.08). The treated group that contained anti-IGF-I (15 of 33; 45.4%) decreased the number of oocytes reaching any stage of development when compared with eGH (47 of 72; 65.3%) and eGH + IGF-I (33 of 45; 73.3%) groups (p = 0.05) when data from MI and MII were combined. We concluded that the addition of eGH to in vitro maturation (IVM) medium influenced the in vitro nuclear and cytoplasmic maturation of equine oocytes. The use of GH and IGF-I in vitro may represent a potential alternative for IVM of equine oocytes.

Keywords

Cortical granuleseGHEquine oocyteIGF-INuclear and cytoplasmic maturation
Type
Research Article
Information
Zygote , Volume 20 , Issue 4 , November 2012 , pp. 353 - 360
Copyright
Copyright © Cambridge University Press 2011

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

Adashi, E. Y., Resnick, C. E., Hurwitz, A., Ricciarelli, E., Hernandez, E. R., Roberts, C. T., Leroith, D. & Rosenfeld, R. (1991). Insulin-like growth factors: the ovarian connection. Hum. Reprod. 6, 1213–9.CrossRefGoogle ScholarPubMed
Apa, R., Lanzone, A., Miceli, F., Mastrandrea, M., Caruso, A., Mancuso, S. & Canipari, R. (1994). Growth hormone induces in vitro maturation of follicle- and cumulus-enclosed rat oocytes. Mol. Cell. Endocrinol. 106, 207–12.CrossRefGoogle ScholarPubMed
Bevers, M. M. & Izadyar, F. (2002). Role of growth hormone and growth hormone receptor in oocyte maturation. Mol. Cell. Endocrinol. 197, 173–178.CrossRefGoogle ScholarPubMed
Carneiro, G., Lorenzo, P., Pimentel, C., Pegoraro, L., Bertolini, M., Ball, B., Anderson, G. & Liu, I. (2001). Influence of insulin-like growth factor-I and its interaction with gonadotropins, estradiol, and fetal calf serum on in vitro maturation and pathenogenic development in equine oocytes. Biol. Reprod. 65, 899–905.CrossRefGoogle Scholar
Carneiro, G. F., Liu, I. K., Hyde, D., Anderson, G. B., Lorenzo, P. L. & Ball, B. A. (2002). Quantification and distribution of equine oocyte CG during meiotic maturation and after activation. Mol. Reprod. Dev. 63, 451–8.CrossRefGoogle ScholarPubMed
Damiani, P., Fissore, R. A., Cibelli, J. B., Long, C. R., Balise, J. J., Robl, J. M. & Duby, R. T. (1996). Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Mol. Reprod. Dev. 45, 521–34.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Ducibella, T., Anderson, E., Albertini, D. F., Aalberg, J. & Rangarajan, S. (1988). Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation. Dev. Biol. 130, 184–97.CrossRefGoogle ScholarPubMed
Ducibella, T., Kurasawa, S., Duffy, P., Kopf, G. S. & Schultz, R. M. (1993). Regulation of the polyspermy block in the mouse egg: maturation-dependent differences in cortical granule exocytosis & zona pellucida modifications induced by inositol 1,4,5-trisphosphate and an activator of protein kinase C. Biol. Reprod. 48, 1251–7.CrossRefGoogle Scholar
Ducibella, T., Duffy, P. & Buetow, J. (1994). Quantification and localization of cortical granules during oogenesis in the mouse. Biol. Reprod. 50, 467–73.CrossRefGoogle ScholarPubMed
Eppig, J. J. (1996). Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 8, 485–489.CrossRefGoogle ScholarPubMed
Erickson, G. F., Garzo, V. G. & Magoffin, D. A. (1989). Insulin-like growth factor-I regulates aromatase activity in human granulosa and granulosa luteal cells. J. Clin. Endocrinol. Metab. 69, 716–24.CrossRefGoogle ScholarPubMed
Fernandez, L., Flores-Morales, A., Lahuna, O., Sliva, D., Norstedt, G., Haldosen, L. A., Mode, A. & Gustafsson, J. A. (1998). Desensitization of the growth hormone-induced Janus kinase 2 (Jak 2) signal transducer and activator of transcription 5 (Stat5)-signaling pathway requires protein synthesis and phospholipase C. Endocrinology 139, 1815–24.CrossRefGoogle ScholarPubMed
Ferreira, E. M., Vireque, A. A., Adona, P. R., Meirelles, F. V., Ferriani, R. A. & Navarro, P. A. A. S. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.CrossRefGoogle ScholarPubMed
Gluckman, P. D. (1986). The role of pituitary hormones, growth factors and insulin in the regulation of fetal growth. Oxf. Rev. Reprod. Biol. 8, 1–60.Google ScholarPubMed
Goudet, G., Bezard, J., Duchamp, G., Gerard, N. & Palmer, E. (1997). Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment. Biol. Reprod. 57, 232–45.CrossRefGoogle ScholarPubMed
Guler, A., Poulin, N., Mermillod, P., Terqui, M. & Cognie, Y. (2000). Effect of growth factors, EGF and IGF-I, and estradiol on in vitro maturation of sheep oocytes. Theriogenology 54, 209–18.CrossRefGoogle ScholarPubMed
Herrler, A., Lucas-Hahn, A. & Niemann, H. (1992). Effects of insulin-like growth factor-I on in-vitro production of bovine embryos. Theriogenology 37, 1213–24.CrossRefGoogle Scholar
Herrler, A., Krusche, C. A. & Beier, H. M. (1998). Insulin and insulin-like growth factor-I promote rabbit blastocyst development and prevent apoptosis. Biol. Reprod. 59, 1302–10.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Huang, Y., Kim, S. O., Jiang, J. & Frank, S. J. (2003). Growth hormone-induced phosphorylation of epidermal growth factor (EGF) receptor in 3T3-F442A cells. Modulation of EGF-induced trafficking and signaling. J. Biol. Chem. 278, 18902–13.CrossRefGoogle ScholarPubMed
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, 372–7.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
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, 1484–9.CrossRefGoogle ScholarPubMed
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, 175–80.3.0.CO;2-J>CrossRefGoogle 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, 444–53.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
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, 247–55.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Le Roith, D., Bondy, C., Yakar, S., Liu, J. L. & Butler, A. (2001). The somatomedin hypothesis: 2001. Endocr. Rev. 22, 53–74.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.CrossRefGoogle ScholarPubMed
Liu, M., Sims, D., Calarco, P. & Talbot, P. (2003). Biochemical heterogeneity, migration, and pre-fertilization release of mouse oocyte cortical granules. Reprod Biol Endocrinol. 1, 77.CrossRefGoogle ScholarPubMed
Liu, X. Y., Mal, S. F., Miao, D. Q., Liu, D. J., Bao, S. G. & Tan, J. H. (2005). Cortical granules behave differently in mouse oocytes matured under different conditions. Hum. Reprod. 20, 3402–13.CrossRefGoogle ScholarPubMed
Lobie, P. E., Breipohl, W., Aragon, J. G. & Waters, M. J. (1990). Cellular localization of the growth hormone receptor/binding protein in the male and female reproductive systems. Endocrinology 126, 2214–21.CrossRefGoogle ScholarPubMed
Lorenzo, P. L., Rebollar, P. G., Illera, M. J., Illera, J. C., Illera, M. & Alvarino, J. M. (1996). Stimulatory effect of insulin-like growth factor I and epidermal growth factor on the maturation of rabbit oocytes in vitro. J. Reprod. Fertil. 107, 109–17.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Magier, S., van der Ven, H. H., Diedrich, K. & Krebs, D. (1990). Significance of cumulus oophorus in in-vitro fertilization and oocyte viability and fertility. Hum. Reprod. 5, 847–52.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Ogushi, S., Palmieri, C., Fulka, H., Saitou, M., Miyano, T. & Fulka, J. (2008). The maternal nucleolus is essential for early embryonic development in mammals. Science 319, 613–6.CrossRefGoogle ScholarPubMed
Pereira, G. R., Lorenzo, P. L., Carneiro, G. F., Bilodeau-Goeseels, S., Kastelic, J. P., Pegoraro, L., Pimentel, C. A., Esteller-Vico, A., Illera, J. C., Silvan, G., Casey, P. & Liu, I. K. M. (2006). Effect of equine growth hormone (eGH) on in vitro maturation of equine oocytes and on steroidogenesis by their cumulus-oocyte complexes. Anim. Reprod. Sci. 94, 364–5.Google Scholar
Rieger, D., Luciano, A. M., Modina, S., Pocar, P., Lauria, A. & Gandolfi, F. (1998). The effects of epidermal growth factor and insulin-like growth factor I on the metabolic activity, nuclear maturation and subsequent development of cattle oocytes in vitro.J. Reprod. Fertil. 112, 123–30.CrossRefGoogle ScholarPubMed
Rotwein, P., Thomas, M.J., Gronowski, A.M., Bichell, D.P. & Kikuchi, K. (1994). The somatomedin hypothesis revisited: early events in growth hormone action. In Insulin-like Growth Factors and their Regulatory Proteins (eds Baxter, R.C., Gluckman, P.C. & Rosenfeld, R.G.) pp. 13–21. Amsterdam: Elsevier Science.Google Scholar
Shirazi, A., Shams-Esfandabadi, N., Ahmadi, E. & Heidari, B. (2008). Effects of growth hormone on nuclear maturation of ovine oocytes and subsequent embryo development. Reprod Domest Anim. 45, 530–6.CrossRefGoogle ScholarPubMed
Silva, J. R., Figueiredo, J. R. & van den Hurk, R. (2009). Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 71, 1193–208.CrossRefGoogle ScholarPubMed
Sirard, M. A. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–54.CrossRefGoogle ScholarPubMed
Wang, W. H., Sun, Q. Y., Hosoe, M., Shioya, Y. & Day, B. N. (1997). Quantified analysis of cortical granule distribution and exocytosis of porcine oocytes during meiotic maturation and activation. Biol. Reprod. 56, 1376–82.CrossRefGoogle ScholarPubMed
Waters, M. J. & Kaye, P. L. (2002). The role of growth hormone in fetal development. Growth Horm. IGF Res. 12, 137–46.CrossRefGoogle ScholarPubMed
Zapf, J. & Hunziker, E. (1994). The somatomedin hypothesis revisited: Differential effects of growth hormone and IGF-I on skeletal growth of the rat in vivo. In The Insulin-Like Growth Factors and Their Regulatory Proteins (eds Baxter, R., Gluckman, P. & Rosenfeld, R.) pp. 381–391. Amsterdam: Elsevier Science.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, 361–65.CrossRefGoogle ScholarPubMed