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Expression of mRNA and protein localization of epidermal growth factor and its receptor in goat ovaries

Published online by Cambridge University Press:  01 May 2006

José R.V. Silva ,
Robert van den Hurk  and
José R. Figueiredo
José R.V. Silva*
Affiliation:
Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands. Faculty of Veterinary Medicine, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
Robert van den Hurk
Affiliation:
Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
José R. Figueiredo
Affiliation:
Faculty of Veterinary Medicine, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
*
All correspondence to: J.R.V. Silva, Universidade Estadual do Ceará, Faculdade de Medicina Veterinária, PPGCV, Av. Paranjana, 1700, CEP 60740-000, Fortaleza, CE, Brazil. Tel: +55 85 31019852. Fax: +55 85 31019859. e-mail: [email protected]
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Summary

To examine the possibility that epidermal growth factor (EGF) and its receptor (EGF-R) are expressed throughout folliculogenesis, we studied the presence and distribution of EGF and EGF-R in goat ovaries. Ovaries of goats were collected and either fixed in paraformaldehyde for immunohistochemical localization of proteins, or used for the isolation of follicles, luteal cells and ovarian surface epithelium to study mRNA expression for EGF and EGF-R, using the reverse transcriptase polymerase chain reaction. EGF protein and mRNA were found in primordial, primary and secondary follicles as well as in small and large antral follicles and in surface epithelium, but in corpora lutea only the protein could be detected. Antral follicles expressed EGF mRNA in oocyte, cumulus, mural granulosa and theca cells. For EGF-R, both protein and mRNA were present at all stages of follicular development and in all antral follicular compartments. EGF-R protein and mRNA were also found in corpora lutea and surface epithelium. It is concluded that EGF and its receptor are expressed in goat ovarian follicles at all stages of follicle development, in corpora lutea, and in ovarian surface epithelium.

Keywords

EGFEGF receptorFolliclesGoatOocyteOvary
Type
Research Article
Information
Zygote , Volume 14 , Issue 2 , May 2006 , pp. 107 - 117
Copyright
Copyright © Cambridge University Press 2006

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References

Auersperg, N., Wong, A.S., Choi, K.C., Kang, S.K. & Leung, P.C. (2001). Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr. Rev. 22, 255–88.Google ScholarPubMed
Behl, R. & Pandey, R.S. (2001). Effect of epidermal growth factor on steroidogenesis by caprine granulosa cells in culture: interaction with FSH. Small Rum. Res. 40, 57–62.CrossRefGoogle ScholarPubMed
Bennett, R.A., Osathanondh, R. & Yeh, J. (1996). Immunohistochemical localization of transforming growth factor-α, epidermal growth factor (EGF), and EGF receptor in the human fetal ovary. J. Clin. Endocrinol. Metab. 81, 3073–6.Google ScholarPubMed
Bolamba, D., Floyd, A.A., McGlone, J.J. & Lee, V.H. (2002). Epidermal growth factor enhances expression of connexin 43 protein in cultured porcine preantral follicles. Biol. Reprod. 67, 154–60.CrossRefGoogle ScholarPubMed
Boland, N.I. & Gosden, R.G. (1994). Effects of epidermal growth factor on the growth and differentiation of cultured mouse ovarian follicles. J. Reprod. Fertil. 101, 369–74.CrossRefGoogle ScholarPubMed
Carpenter, G. (1999). Employment of the epidermal growth factor receptor in growth factor-independent signaling pathways. J. Cell Biol. 146, 697–702.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
De La Fuente, R., O'Brien, M.J. & Eppig, J.J. (1999). Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum. Reprod. 14, 3060–8.CrossRefGoogle ScholarPubMed
Eppig, J.J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–38.CrossRefGoogle ScholarPubMed
Feng, P., Knecht, M. & Catt, K. (1987). Hormonal control of epidermal growth factor receptors by gonadotropins during granulosa cell differentiation. Endocrinology 120, 1121–6.CrossRefGoogle ScholarPubMed
Fortune, J.E. (2003). The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim. Reprod. Sci. 78, 135–63.CrossRefGoogle ScholarPubMed
Gall, L., Chene, N., Dahirel, M., Ruffini, S. & Boulesteix, C. (2004). Expression of epidermal growth factor receptor in the goat cumulusoocyte complex. Mol. Reprod. Dev. 67, 439–45.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 hormone, luteinizing hormone, estradiol, and progesterone. Biol. Reprod. 67, 1593–604.CrossRefGoogle ScholarPubMed
Goud, P.T., Goud, A.P., Qian, C., Laverge, H., Van der Elst, J., De Sutter, P. & Dhont, M. (1998). In vitro maturation of human germinal vesicle stage oocytes: role of cumulus cells and epidermal growth factor in the culture medium. Hum. Reprod. 13, 1638–44.CrossRefGoogle ScholarPubMed
Gupta, P.S., Nandi, S., Ravindranatha, B.M. & Sarma, P.V. (2002). In vitro culture of buffalo (Bubalus bubalis) preantral follicles. Theriogenology 57, 1839–54.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
Gutierrez, C.G., Ralph, J.H., Telfer, E.E., Wilmut, I. & Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod. 62, 1322–8.CrossRefGoogle ScholarPubMed
Hattori, M.A., Yoshino, E., Shinohara, Y., Horiuchi, R. & Kojima, I. (1995). A novel action of epidermal growth factor in rat granulosa cells: its potentiation of gonadotrophin action. J. Mol. Endocrinol. 15, 283–91.CrossRefGoogle ScholarPubMed
Hemamalini, N.C., Rao, B.S., Tamilmani, G., Amarnath, D., Vagdevi, R., Naidu, K.S., Reddy, K.K. & Rao, V.H. (2003). Influence of transforming growth factor-α, insulin-like growth factor-II, epidermal growth factor or follicle stimulating hormone on in vitro development of preantral follicles in sheep. Small Rum. Res. 50, 11–22.CrossRefGoogle Scholar
Hill, J.L., Hammar, K., Smith, P.J. & 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
Hirshfield, A. (1983). Compensatory ovarian hypertrophy in the long-term hemicastrate rat: size distribution of growing and atretic follicles. Biol. Reprod. 28, 271–8.CrossRefGoogle ScholarPubMed
Juneja, S.C., Barr, K.J., Enders, G.C. & Kidder, G.M. (1999). Defects in the germ line and gonads of mice lacking connexin 43. Biol. Reprod. 60, 1263–70.CrossRefGoogle Scholar
Kennedy, T.G., Brown, K.D. & Vaughan, T.J. (1993). Expression of the genes for the epidermal growth factor receptor and its ligands in porcine corpora lutea. Endocrinology 132, 1857–9.CrossRefGoogle ScholarPubMed
Kennedy, K.L., Floyd, A.A., Clarkson, A.M. & Lee, V.H. (2003). Epidermal growth factor regulation of connexin 43 in cultured granulosa cells from preantral rabbit follicles. Mol. Reprod. Dev. 64, 61–9.CrossRefGoogle ScholarPubMed
Li, Y.H., Liu, R.H., Jiao, L.H. & Wang, W.H. (2002). Synergetic effects of epidermal growth factor and estradiol on cytoplasmic maturation of porcine oocytes. Zygote 10, 349–54.CrossRefGoogle ScholarPubMed
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
Lucci, C.M., Amorim, C.A., Bao, S.N., Figueiredo, J.R., Rodrigues, A.P.R., Silva, J.R.V. & Gonçalves, P.B.D. (1999). Effect of the interval of serial sections of ovarian tissue in the tissue chopper on the number of isolated caprine preantral follicles. Anim. Reprod. Sci. 56, 39–49.CrossRefGoogle ScholarPubMed
Luciano, A.M., Pappalardo, A., Ray, C. & Peluso, J.J. (1994). Epidermal growth factor inhibits large granulosa cell apoptosis by stimulating progesterone synthesis and regulating the distribution of intracellular free calcium. Biol. Reprod. 51, 646–54.CrossRefGoogle ScholarPubMed
McClellan, M., Kievit, P., Auersperg, N. & Rodland, K. (1999). Regulation of proliferation and apoptosis by epidermal growth factor and protein kinase C in human ovarian surface epithelial cells. Exp. Cell Res. 246, 471–9.CrossRefGoogle ScholarPubMed
Maruo, T., Ladines-Llave, C.A., Samoto, T., Matsuo, H., Manalo, A.S., Ito, H. & Mochizuki, M. (1993). Expression of epidermal growth factor and its receptor in the human ovary during follicular growth and regression. Endocrinology 132, 924–31.CrossRefGoogle Scholar
May, J.V., Buck, P.A. & Schomberg, D.W. (1987). Epidermal growth factor enhances [125I]iodo-follicle-stimulating hormone binding by cultured porcine granulosa cells. Endocrinology 120, 2413–20.CrossRefGoogle ScholarPubMed
May, J.V., Bridge, A.J., Gotcher, E.D. & Gangrade, B.K. (1992). The regulation of porcine theca cell proliferation in vitro: synergistic actions of epidermal growth factor and platelet-derived growth factor. Endocrinology 131, 689–97.Google ScholarPubMed
Merriman, J.A., Whittingham, D.G. & Carroll, J. (1998). The effect of follicle stimulating hormone and epidermal growth factor on the developmental capacity of in vitro matured mouse oocytes. Hum. Reprod. 13, 690–5.CrossRefGoogle ScholarPubMed
Misajon, A., Hutchinson, P., Lolatgis, N., Trounson, A.O. & Almahbobi, G. (1999). The mechanism of action of epidermal growth factor and transforming growth factor alpha on aromatase activity in granulosa cells from polycystic ovaries. Mol. Hum. Reprod. 5, 96–103.CrossRefGoogle ScholarPubMed
Morbeck, D.E., Flowers, W.L. & Britt, J.H. (1993). Response of porcine granulosa cells isolated from primary and secondary follicles to FSH, 8-bromo-cAMP and epidermal growth factor in vitro. J. Reprod. Fertil. 99, 577–84.CrossRefGoogle ScholarPubMed
O'Donnell, J.B. Jr, Hill, J.L. & Gross, D.J. (2004). Epidermal growth factor activates cytosolic [Ca2+] elevations and subsequent membrane permeabilization in mouse cumulus–oocyte complexes. Reproduction 127, 207–20.CrossRefGoogle ScholarPubMed
Park, J.Y., Su, Y.Q., Ariga, M., Law, E., Jin, S.L. & Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–4.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
Prochazka, R., Kalab, P. & Nagyova, E. (2003). Epidermal growth factor-receptor tyrosine kinase activity regulates expansion of porcine oocyte–cumulus cell complexes in vitro. Biol. Reprod. 68, 797–803.CrossRefGoogle ScholarPubMed
Qu, J.P., Godin, P.A., Nisolle, M. & Donnez, J. (2000). Distribution of epidermal growth factor receptor expression of primordial follicles in human ovarian tissue before and after cryopreservation. Hum. Reprod. 15, 302–10.CrossRefGoogle ScholarPubMed
Reggio, B.C., James, A.N., Green, H.L., Gavin, W.G., Behboodi, E., Echelard, Y. & Godke, R.A. (2001). Cloned transgenic offspring resulting from somatic cell nuclear transfer in the goat: oocytes derived from both follicle-stimulating hormone-stimulated and nonstimulated abattoir-derived ovaries. Biol. Reprod. 65, 1528–33.CrossRefGoogle ScholarPubMed
Riese, D.J. II & Stern, D.F. (1998). Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20, 41–8.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Roy, S.K. (1993). Epidermal growth factor and transforming growth factor-beta modulation of follicle-stimulating hormone-induced deoxyribonucleic acid synthesis in hamster preantral and early antral follicles. Biol. Reprod. 48, 552–7.CrossRefGoogle ScholarPubMed
Roy, S.K. & Greenwald, G.S. (1990). Immunohistochemical localisation of epidermal growth factor-like activity in the hamster ovary with a polyclonal antibody. Endocrinology 126, 1309–17.CrossRefGoogle ScholarPubMed
Roy, S.K. & Kole, A.R. (1998). Ovarian transforming growth factor-beta (TGF-beta) receptors: in vitro effects of follicle stimulating hormone, epidermal growth factor and TGF-beta on receptor expression in human preantral follicles. Mol. Hum. Reprod. 4, 207–14.CrossRefGoogle ScholarPubMed
Saha, S., Shimizu, M., Geshi, M. & Izaike, Y. (2000). In vitro culture of bovine preantral follicles. Anim. Reprod. Sci. 63, 27–39.CrossRefGoogle ScholarPubMed
Sakaguchi, M., Dominko, T., Yamauchi, N., Leibfried-Rutledge, M.L., Nagai, T. & First, N.L. (2002). Possible mechanism for acceleration of meiotic progression of bovine follicular oocytes by growth factors in vitro. Reproduction 123, 135–42.CrossRefGoogle ScholarPubMed
Serta, R.T. & Seibel, M.M. (1993). The influence of epidermal growth factor on progesterone production by human granulosa-luteal cells in culture. Hum. Reprod. 8, 1005–10.CrossRefGoogle ScholarPubMed
Silva, J.R.V., Van den Hurk, R., Matos, M.H.T., Santos, R.R., Pessoa, C., Moraes, M.O. & Figueiredo, J.R. (2004 a). Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology 61, 1691–704.CrossRefGoogle ScholarPubMed
Silva, J.R.V., Van den Hurk, R., van Tol, H.T.A., Roelen, B.A.J. & Figueiredo, J.R. (2004 b). Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in goat ovaries. Mol. Reprod. Dev. 70, 11–19.CrossRefGoogle Scholar
Silva, J.R.V., Van den Hurk, R. & Figueiredo, J.R. (2004 c). Expression of kit ligand and c-kit receptor in goat ovaries. Reproduction (Abstract series) 31, 9–10.Google Scholar
Singh, B., Rutledge, J.M. & Armstrong, D.T. (1995 a). Epidermal growth factor and its receptor gene expression and peptide localisation in porcine ovarian follicles. Mol. Reprod. Dev. 40, 391–9.CrossRefGoogle ScholarPubMed
Singh, B., Kennedy, T.G., Tekpetey, F.R. & Armstrong, D.T. (1995 b). Gene expression and peptide localisation for epidermal growth factor receptor and its ligands in porcine luteal cells. Mol. Cell. Endocrinol. 113, 137–43.CrossRefGoogle ScholarPubMed
Singh, B., Meng, L., Rutledge, J.M. & Armstrong, D.T. (1997). Effects of epidermal growth factor and follicle-stimulating hormone during in vitro maturation on cytoplasmic maturation of porcine oocytes. Mol. Reprod. Dev. 46, 401–7.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Smitz, J., Cortvrindt, R. & Hu, Y. (1998). Epidermal growth factor combined with recombinant human chorionic gonadotrophin improves meiotic progression in mouse follicle-enclosed oocyte culture. Hum. Reprod. 13, 664–9.CrossRefGoogle ScholarPubMed
Tekpetey, F.R., Singh, B., Barbe, G. & Armstrong, D.T. (1995). Localisation of epidermal growth factor (EGF) receptor in the rat corpus luteum, and EGF and transforming growth factor-alpha stimulation of luteal cell steroidogenesis in vitro. Mol. Cell. Endocrinol. 110, 95–102.CrossRefGoogle ScholarPubMed
Van den Hurk, R. & Zhao, J. (2005). Formation of ovarian follicles and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–51.CrossRefGoogle ScholarPubMed
Van den Hurk, R., Dijkstra, G., Hulshof, S.C.J. & Vos, P.L.A.M. (1994). Micromorphology of antral follicles in cattle after prostaglandin-induced luteolysis, with particular reference to atypical granulosa cells. J. Reprod. Fertil. 100, 137–42.CrossRefGoogle ScholarPubMed
Van der Burg, M.E., Henzen-Logmans, S.C., Foekens, J.A., Berns, E.M., Rodenburg, C.J., van Putten, W.L. & Klijn, J.G. (1993). The prognostic value of epidermal growth factor receptors, determined by both immunohistochemistry and ligand binding assays, in primary epithelial ovarian cancer: a pilot study. Eur. J. Cancer 29, 1951–7.CrossRefGoogle Scholar
Van Haaften-Day, C., Russell, P., Boyer, C.M., Kerns, B.J., Wiener, J.R., Jensen, D.N., Bast, R.C. Jr & Hacker, N.F. (1996). Expression of cell regulatory proteins in ovarian borderline tumors. Cancer 77, 2092–8.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Van Tol, H.T. & Bevers, M.M. (1998). Theca cells and thecacell conditioned medium inhibit the progression of FSH-induced meiosis of bovine oocytes surrounded by cumulus cells connected to membrana granulosa. Mol. Reprod. Dev. 51, 315–21.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Wandji, S.-A., Eppig, J.J. & Fortune, J.E. (1996). FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology 45, 817–32.CrossRefGoogle ScholarPubMed
Yang, P. & Roy, S.K. (2001). Epidermal growth factor modulates transforming growth factor receptor messenger RNA and protein levels in hamster preantral follicles in vitro. Biol. Reprod. 65, 847–54.CrossRefGoogle ScholarPubMed