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Real-time qRT-PCR analysis of EGF receptor in cumulus-oocyte complexes recovered by laparoscopy in hormonally treated goats

Published online by Cambridge University Press:  27 July 2010

K.C. Almeida ,
A.F. Pereira ,
A.S. Alcântara Neto ,
S.R.G. Avelar ,
L.R. Bertolini ,
M. Bertolini ,
V.J.F. Freitas  and
L.M. Melo
K.C. Almeida
Affiliation:
Laboratório de Fisiologia e Controle da Reprodução, Universidade Estadual do Ceará, Faculdade de Veterinária, Av. Dedé Brasil 1700, Fortaleza-CE, Brazil.
A.F. Pereira
Affiliation:
Laboratório de Fisiologia e Controle da Reprodução, Universidade Estadual do Ceará, Faculdade de Veterinária, Av. Dedé Brasil 1700, Fortaleza-CE, Brazil.
A.S. Alcântara Neto
Affiliation:
Laboratório de Fisiologia e Controle da Reprodução, Universidade Estadual do Ceará, Faculdade de Veterinária, Av. Dedé Brasil 1700, Fortaleza-CE, Brazil.
S.R.G. Avelar
Affiliation:
Laboratório de Fisiologia e Controle da Reprodução, Universidade Estadual do Ceará, Faculdade de Veterinária, Av. Dedé Brasil 1700, Fortaleza-CE, Brazil.
L.R. Bertolini
Affiliation:
Centro de Ciências da Saúde, Universidade de Fortaleza, Av. Washington Soares 1321, Fortaleza-CE, Brazil.
M. Bertolini
Affiliation:
Centro de Ciências da Saúde, Universidade de Fortaleza, Av. Washington Soares 1321, Fortaleza-CE, Brazil.
V.J.F. Freitas
Affiliation:
Laboratório de Fisiologia e Controle da Reprodução, Universidade Estadual do Ceará, Faculdade de Veterinária, Av. Dedé Brasil 1700, Fortaleza-CE, Brazil.
L.M. Melo*
Affiliation:
Laboratório de Fisiologia e Controle da Reprodução, Universidade Estadual do Ceará/Faculdade de Veterinária, Av. Dedé Brasil 1700, Fortaleza-CE, Brazil.
*
All correspondence to: Luciana Magalhães Melo. Laboratório de Fisiologia e Controle da Reprodução, Universidade Estadual do Ceará/Faculdade de Veterinária, Av. Dedé Brasil 1700, Fortaleza-CE, Brazil. Tel: +55 85 31019861. Fax: +55 85 31019840. e-mail: [email protected]
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Summary

Ovarian stimulation with exogenous follicle stimulating hormone (FSH) has been used to increase the number of viable oocytes for laparoscopic oocyte recovery (LOR) in goats. The aim of this study was to evaluate the effect of two FSH protocols for ovarian stimulation in goats on the expression pattern of epidermal growth factor (EGF) receptor (EGFR) in cumulus–oocyte complexes (COCs) recovered by LOR. After real-time qRT-PCR analysis, expression profiles of morphologically graded COCs were compared prior to and after in vitro maturation (IVM) on a FSH protocol basis. The use of a protocol with higher number of FSH injections at a shorter interval resulted in GI/GII COCs with a higher level of EGFR expression in cumulus cells, but not in the oocyte, which was correlated with an elevated meiotic competence following IVM. Based on the maturation profile and EGFR expression patterns observed between groups, the morphological selection of COCs prior to IVM was not a good predictor of oocyte meiotic competence. Therefore, EGFR may be a good candidate marker for indirect prediction of goat oocyte quality. The IVM process of goat COCs increased the EGFR expression in oocytes and cumulus cells, which seemed to be strongly associated with the resumption of meiosis. In summary, differential EGFR expression in goat cumulus cells was associated with the in vivo prematuration process, and in turn, the upregulation in the entire COC was associated with IVM. Cause-and-effect relationships between such increased expression levels, particularly in the oocyte, and oocyte competence itself still need to be further investigated.

Keywords

Cumulus cellsEGF receptorGoatOocyteReal-time qRT-PCR
Type
Research Article
Information
Zygote , Volume 19 , Issue 2 , May 2011 , pp. 127 - 136
Copyright
Copyright © Cambridge University Press 2010

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References

Assidi, M., Dufort, I., Ali, A., Hamel, M., Algriany, O., Dielemann, S. & Sirard, M.A. (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol. Reprod. 79, 209–222.CrossRefGoogle ScholarPubMed
Atef, A., François, P., Christian, V. & Marc-Andre, S. (2005). The potential role of gap junction communication between cumulus cells and bovine oocytes during in vitro maturation. Mol. Reprod. Dev. 71, 358–67.CrossRefGoogle ScholarPubMed
Baldassarre, H., Keefer, C., Wang, B., Lazaris, A. & Karatzas, C.N. (2003a). Nuclear transfer in goats using in vitro matured oocytes recovered by laparoscopic ovum pick-up. Cloning Stem Cells 5, 279–85.CrossRefGoogle ScholarPubMed
Baldassarre, H., Wang, B., Kafidi, N., Guathier, M., Neveu, N., Lapoint, J., Sneek, L., Leduc, M., Duguay, F., Zhou, J.F., Lazaris, A. & Karatzas, C.N. (2003b). Production of transgenic goats by pronuclear microinjection of in vitro produced zygotes derived from oocytes recovered by laparoscopy. Theriogenology 59, 831–9.CrossRefGoogle ScholarPubMed
Baldassarre, H. & Karatzas, C.N. (2004). Advanced assisted reproduction technologies (ART) in goats. Anim. Reprod. Sci. 82–83, 255–66.CrossRefGoogle ScholarPubMed
Chabot, J.G., St-Arnaud, R., Walker, P. & Pelletier, G. (1986). Distribution of epidermal growth factor receptors in the rat ovary. Mol. Cell Endocrinol. 44, 99–108.CrossRefGoogle ScholarPubMed
Chia, C.M., Winston, R.M.L. & Handyside, A.H. (1995). EGF, TGF-α and EGF-R expression in human preimplantation embryos. Development 121, 299–307.CrossRefGoogle Scholar
Choi, J.H., Choi, K.C., Auersperg, N. & Leung, P.C. (2005). Gonadotropins upregulate the epidermal growth factor receptor through activation of mitogen activated protein kinases and phosphatidyl-inositol-3-kinase in human ovarian surface epithelial cells. Endocr. Relat. Cancer 12, 407–21.CrossRefGoogle ScholarPubMed
Cognié, Y. & Baril, G. (2002). Le point sur la production et le transfert d'embryons obtenus in vivo e in vitro chez bebris e la chèvre. INRA Prod. Anim. 15, 199–207.CrossRefGoogle Scholar
Cognié, Y., Baril, G., Poulin, N. & Mermillod, P. (2003). Current status of embryo technologies in sheep and goat. Theriogenology 9, 171–188.CrossRefGoogle Scholar
Das, K., Stout, L.E., Hensleigh, H.C., Tagatz, G.E., Phipps, W.R. & Leung, B.S. (1991). Direct positive effect of epidermal growth factor on the cytoplasmic maturation of mouse and human oocytes. Fertil. Steril. 55, 1000–4.CrossRefGoogle ScholarPubMed
Dedieu, T., Gall, L., Crozet, N., Sevellec, C. & Ruffini, S. (1996). Mitogen activated protein kinase activity during goat oocyte maturation and the acquisition of meiotic competence. Mol. Reprod. Dev. 45, 351–8.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Dekel, N. & Sherizly, I. (1985). Epidermal growth factor induces maturation of rat follicle-enclosed oocytes. Endocrinology 116, 406–9.CrossRefGoogle ScholarPubMed
Dieleman, S.J., Hendriksen, P.J., Viuff, D., Thomsen, P.D., Hyttel, P., Knijn, H.M., Wrenzycki, C., Kruip, T.A., Niemann, H., Gadella, B.M., Bevers, M.M. & Vos, P.L. (2002). Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of preimplantation embryos. Theriogenology 57, 5–20.CrossRefGoogle Scholar
Downs, S.M. & Chen, J. (2008). EGF-like peptides mediate FSH-induced maturation of cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 75, 105–14.CrossRefGoogle ScholarPubMed
Dussault, A.A. & Pouliot, M. (2006). Rapid and simple comparison of messenger RNA levels using real-time PCR. Biol. Proc. Online 8, 1–10.CrossRefGoogle ScholarPubMed
Evans, A.C.O. (2003). Ovarian follicle growth and consequences for fertility in sheep. Anim. Reprod. Sci. 78, 289–306.CrossRefGoogle ScholarPubMed
Feuerstein, P., Cadoret, V., Dalbies-Tran, R., Guerif, F., Bidault, R. & Royere, D. (2007). Gene expression in human cumulus cells: one approach to oocyte competence. Hum. Reprod. 22, 3069–77.CrossRefGoogle ScholarPubMed
Gall, L., Chene, N., Dahirel, M., Ruffini, S. & Boulesteix, C. (2004). Expression of epidermal growth factor receptor in the goat cumulus–oocyte complex. Mol. Reprod. Dev. 67, 439–45.CrossRefGoogle ScholarPubMed
Gall, L., Boulesteix, C., Ruffini, S. & Germain, G. (2005). EGF-induced EGF-receptor and MAP kinase phosphorylation in goat cumulus cells during in vitro maturation. Mol. Reprod. Dev. 71, 489–94.CrossRefGoogle ScholarPubMed
Garnett, K., Wang, J. & Roy, S.K. (2002). Spatiotemporal expression of epidermal growth factor receptor messenger RNA and protein in the hamster ovary: follicle stage-specific differential modulation by follicle-stimulating hormones, luteinizing hormone, estradiol and progesterone. Biol. Reprod. 67, 1593–604.CrossRefGoogle ScholarPubMed
Gibbons, A., Bonnet, F.P., Cueto, M.I., Catala, M., Salamone, D.F. & Gonzalez-Bulnes, A. (2007). Procedure for maximizing oocyte harvest for in vitro embryo production in small ruminants. Reprod. Domest. Anim. 42, 423–6.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Ritter, L.J. & Armstrong, D.T. (2004). Oocyte-somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82–83, 431–46.CrossRefGoogle ScholarPubMed
Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A. & Peelman, L.J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev. Biol. 5, 27.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
Hashimoto, S., Saeki, K., Nagao, Y., Minami, N., Yamada, M. & Utsumi, K. (1998). Effects of cumulus cell density during in vitro maturation of the developmental competence of bovine oocytes. Theriogenology 49, 1451–63.CrossRefGoogle ScholarPubMed
Hatoya, S., Sugiyama, Y., Nishida, H., Okuno, T., Torii, R., Sugiura, K., Kida, K., Kawate, N., Tamada, H. & Inaba, T. (2009). Canine oocyte maturation in culture: significance of estrogen and EGF receptor gene expression in cumulus cells. Theriogenology 71, 560–7.CrossRefGoogle ScholarPubMed
Hill, J.L., Hammar, K., Smith, P.J.S. & Gross, D.J. (1999). Stage-dependent effects of epidermal growth factor on Ca2+ efflux in mouse oocytes. Mol. Reprod. Dev. 53, 244–53.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Hsu, C.J., Holmes, S.D. & Hammond, J.M. (1987). Ovarian epidermal growth factor-like activity. Concentrations in porcine follicular fluid during follicular enlargement. Biochem. Biophys. Res. Commun. 147, 242–7.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real time quantitative PCR and the 2−Δ ΔCT method. Methods 25, 402–8.CrossRefGoogle Scholar
Lonergan, P., Carolan, C., Van Langendonckt, A., Donnay, I., Khatir, H. & Mermillod, P. (1996). Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro. Biol. Reprod. 54, 1420–9.CrossRefGoogle ScholarPubMed
Mariante, A.S. & Egito, A.A. (2002). Animal genetic resources in Brazil: result of five centuries of natural selection. Theriogenology 57, 223–235.CrossRefGoogle ScholarPubMed
Monniaux, D., Chupin, D. & Saumande, J. (1983). Superovulatory response of cattle. Theriogenology, 19, 55–81.CrossRefGoogle Scholar
Pierson, J., Wang, B., Neveu, N., Sneek, L., Cote, F., Karatzas, C.N. & Baldassarre, H. (2004). Effects of repetition, interval between treatments and season on the results from laparoscopic ovum pick-up in goats. Reprod. Fertil. Dev. 16, 795–9.CrossRefGoogle ScholarPubMed
Prochazka, R., Srsen, V., Nagyova, E., Miyano, T. & Flechon, J.E. (2000). Developmental regulation of effect of epidermal growth factor on porcine oocyte–cumulus cell complexes: nuclear maturation, expansion, and F-actin remodeling. Mol. Reprod. Dev. 56, 63–73.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Qu, J.M.D., Nisolle, M.D. & Donnez, J.M.D. (2000). Expression of transforming growth factor-alpha, epidermal growth factor and epidermal growth factor receptor in follicles of human ovarian tissue before and after cryopreservation. Fertil. Steril. 74, 113–21.CrossRefGoogle ScholarPubMed
Sekiguchi, T., Mizutani, T., Yamada, K., Yazawa, T., Kawata, H., Yoshino, M., Kajitani, T., Kameda, T., Minegishi, T. & Miyamoto, K. (2002). Transcriptional regulation of the epiregulin gene in the rat ovary. Endocrinology 143, 4718–29.CrossRefGoogle ScholarPubMed
Shimada, M., Hernandez-Gonzalez, I., Gonzalez-Robayna, I. & Richards, J.S. (2006). Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol. Endocrinol. 20, 1352–65.CrossRefGoogle ScholarPubMed
Singh, B., Rutledge, J.M. & Armstrong, D.T. (1995). Epidermal growth factor and its receptor gene expression and peptide localization in porcine ovarian follicles. Mol. Reprod. Dev. 40, 391–99.CrossRefGoogle ScholarPubMed
Sirard, M.A., Dufort, I., Coenen, K., Tremblay, K., Massicotte, L. & Robert, C. (2003). The use of genomics and proteomics to understand oocyte and early embryo functions in farm animals. Reprod. Suppl. 61, 117–129.Google ScholarPubMed
Van Den Hurk, R. & Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–51.CrossRefGoogle ScholarPubMed
Van Zutphen, L.F.M. & Balls, M. (1997). Animal Alternatives, Welfare and Ethics. Amsterdam: Elsevier. 1260 pp.Google Scholar
Webb, R., Garnsworthy, P.C., Campbell, B.K. & Hunter, M.G. (2007). Intra-ovarian regulation of follicular development and oocyte competence in farm animals. Theriogenology 68S, S22–S29.CrossRefGoogle Scholar
Westergaard, L.G. & Andersen, C.Y. (1989). Epidermal growth factor (EGF) in human preovulatory follicles. Hum. Reprod. 4, 257–60.CrossRefGoogle ScholarPubMed
Wiley, L.M., Wu, J.X., Harari, I. & Adamson, E.D. (1992). Epidermal growth factor receptor mRNA and protein increase after the four-cell preimplantation stage in murine development. Dev. Biol. 149, 247–60.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D. & Niemann, H. (2007). Messenger RNA in oocytes and embryos in relation to embryo viability. Theriogenology 68S, S77–S83.CrossRefGoogle Scholar
Zhang, M., Ouyang, H. & Xia, G. (2009). The signal pathway of gonadotrophins-induced mammalian oocyte meiotic resumption. Mol. Hum. Reprod. 15, 399–409.CrossRefGoogle ScholarPubMed