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Role of follicle stimulating hormone and epidermal growth factor in the development of porcine preantral follicle in vitro

Published online by Cambridge University Press:  01 August 2007

Ji Wu  and
Qi Tian
Ji Wu*
Affiliation:
School of Life Science and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China.
Qi Tian
Affiliation:
Temple University School of Medicine, Philadelphia, 19140, USA.
*
All correspondence to: Ji Wu, School of Life Science and Biotechnology, Shanghai Jiao Tong University, No. 800. Dongchuan Road, Minhang District, Shanghai, 200240, China. Tel: +86 21 34204933. Fax: +86 21 34204051. e-mail: [email protected]
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Summary

The aim of the present study was to assess the role of follicle stimulating hormone (FSH), epidermal growth factor (EGF) or a combination of EGF and FSH on the in vitro growth of porcine preantral follicles, estradiol secretion, antrum formation, oocyte maturation and subsequent embryonic development. Porcine preantral follicles were cultured for 3 days in the absence or in the presence of FSH or EGF. Oocytes from these follicles were then matured, fertilized in vitro and embryos were cultured. Estradiol secretion and histological analysis of cultured follicles were also carried out. The results showed that when FSH, or a combination of EGF and FSH, was added to the culture medium, most of preantral follicles grew to antral follicles with high estradiol secretion and the oocytes from these antral follicles could mature, fertilize and develop to the blastocyst stage. Without FSH, or a combination of EGF and FSH, preantral follicles were unable to develop to the antral stage. Histology demonstrated that the resulting follicles were nonantral, estradiol production was reduced and none of their oocytes matured after in vitro maturation. The results indicate the essential role of FSH in promoting in vitro growth of porcine preantral follicle, estradiol secretion, antrum formation, oocyte maturation and subsequent embryonic development. EGF with FSH treatment of porcine preantral follicles improves the quality of oocytes, shown by a higher frequency of embryonic development.

Keywords

EGFEmbryonic developmentFSHOocyte maturationPorcine preantral follicle
Type
Research Article
Information
Zygote , Volume 15 , Issue 3 , August 2007 , pp. 233 - 240
Copyright
Copyright © Cambridge University Press 2007

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References

Abeydeera, L.R., Wang, W.H., Cantley, T.C., Rieke, A. & Day, B.N. (1998). Cocuture with follicular shell pieces can enhance the developmental competence of porcine oocytes after in vitro fertilization: relevance to intracellular glutathione. Biol. Reprod. 58, 213–8.CrossRefGoogle Scholar
Anderiesz, A, Ferraretti, AP, Magli, C, Fiorentino, A, Fortini, D, Gianaroli, L, Jones, GM & Trounson, AO. (2000). Effect of recombinant human gonadotrophins on human, bovine and murine oocyte meiosis, fertilization and embryonic development in vitro. Human Reprod. 15, 1140–8.CrossRefGoogle ScholarPubMed
Boland, N.I., Humpherson, P.G., Leese, H. & Gosden, R.G. (1993). Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro. Biol. Reprod. 48, 798–806.CrossRefGoogle ScholarPubMed
Cain, L., Chatterjee, S. & Collins, T.J. (1995). In vitro folliculogenesis of rat preantral follicles. Endocrinol. 136, 3369–77.CrossRefGoogle ScholarPubMed
Cook, S.J. & McCormick, F. (1993). Inhibition by cAMP of Ras-dependent activation of Raf. Science 262, 1069–72.CrossRefGoogle ScholarPubMed
Cortvrindt, R., Smitz, J. & Van Steirteghem, A.C. (1997). Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Human Reprod. 12, 759–68.CrossRefGoogle ScholarPubMed
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
Downs, S.M., Daniel, S.A.J. & Eppig, J.J. (1998). Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. J. Exp. Zool. 245, 86–96.CrossRefGoogle Scholar
Eppig, J.J., Schultz, R.M., O'Brien, M. & Chesnel, F. (1994). Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev. Biol. 164, 1–9.CrossRefGoogle ScholarPubMed
Eppig, J.J, O'Brien, M.. & Wigglesworth, K. (1996). Mammalian oocyte growth and development in vitro. Mol. Reprod. Dev. 44, 260–73.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Eppig, J.J., O'Brien, M.J., Pendola, F.L. & Watanabe, S. (1998). Factors affecting the developmental competence of mouse oocytes grown in vitro: follicle-stimulating hormone and insulin. Biol. Reprod. 59, 1445–53.CrossRefGoogle ScholarPubMed
Goldenberg, R.L., Reiter, E.O. & Ross, G.T. (1973). Follicle response to exogenous gonadotropins: an estrogen-mediated phenomenon. Fertil. Steril. 24, 121–5.CrossRefGoogle ScholarPubMed
Gougeon, A. (1982). Rate of follicular growth in the human ovary. In: Van Hall EVGoogle Scholar
Gore-Langton, R.E. & Daniel, S. A.J. (1990). Follicle-stimulating hormone and estradiol regulate antrum-like reorganization of granulosa cells in rat preantral follicle cultures. Biol. Reprod. 43, 65–72.CrossRefGoogle ScholarPubMed
Gulyas, B.J., Hodgen, G.D., Tullner, W.W. & Ross, G.T. (1977). Effects of fetal or maternal hypophysectomy on endocrine organs and body weight in infant rhesus monkeys (Macaca mulatta): with particular emphasis on oogenesis. Biol. Reprod. 16, 216–27.CrossRefGoogle ScholarPubMed
Halpin, D.M., Jones, A., Fink, G. & Charlton, H.M. (1986). Postnatal ovarian follicle development in hypogonadal (hpg) and normal mice and associated changes in the hypothalamic-pituitary ovarian axis.J. Reprod. Fertil. 77, 287–96.CrossRefGoogle ScholarPubMed
Hillier, S.G. (1994). Current concepts of the roles of follicle stimulating hormone and luteinizing hormone in folliculogenesis. Human Reprod. 9, 188–91.CrossRefGoogle ScholarPubMed
Hillier, S.G., McNatty, K.P., Schoemaker, J. (eds) (1996). Follicular Maturation and Ovulation, pp. 155–169, Amsterdam, North Holland: Elsevier.Google Scholar
Hirao, Y., Nagai, T., Kubo, M., Miyano, T., Miyake, M. & Kato, S. (1994). In vitro growth and maturation of porcine oocytes.J. Reprod. Fertil. 100, 333–9.CrossRefGoogle Scholar
Johnson, G.L. & Dhanasedaran, N. (1989). The G protein family and their interactions with receptors. Endocrine Reviews 10, 317–31.CrossRefGoogle Scholar
Kobayashi, K., Yamashita, S. & Hoshi, H. (1994). Influence of epidermal growth factor and transforming growth factor-α on in vitro maturation of cumulus cell-enclosed bovine oocytes in a defined medium. J. Reprod. Fertil. 100, 439–46.CrossRefGoogle Scholar
Li, R., Phillips, D.M. & Mather, J.P. (1995). Activin promotes ovarian follicle development in vitro. Endocrinol. 136, 849–56.CrossRefGoogle ScholarPubMed
Liu, J., Aronow, B.J., Witte, D.P., Pope, W.F. & La Barbera, A.R. (1998). Cyclic and maturation-dependent regulation of follicle-stimulating hormone receptor and luteinizing hormone receptor messenger ribonucleic acid expression in the porcine ovary. Biol. Reprod. 58, 648–58.CrossRefGoogle ScholarPubMed
Maizels, E.T., Cottom, J., Jones, J.C. & Hunzicker-Dunn, M. (1998). Follicle stimulating hormone (FSH) activates the p38 mitogen-activated protein kinase pathway, inducing small heat shock protein phosphorylation and cell rounding in immature rat ovarian granulose cells. Endocrinology 139, 3353–6.CrossRefGoogle Scholar
McGee, E.A., Perlas, E., Lapolt, P.S., Tsafriri, A. & Hsueh, A.J.W. (1997a). Follicle-stimulating hormone enhances the development of preantral follicles in juvenile rats. Biol. Reprod. 57, 990–8.CrossRefGoogle ScholarPubMed
McGee, E., Spears, N., Minami, S., Hsu, S.Y., Chun, S.Y., Billig, H. & Hsueh, A.J.W. (1997b). Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3′,5′-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone. Endocrinol. 138, 2417–24.CrossRefGoogle ScholarPubMed
Meijs-Roelofs, H.M., Van Cappellen, W.A., Van Leeuwen, W. & Kramer, P. (1990). Short-and long-term effects of an LHRH antagonist given during the prepubertal period on follicle dynamics in the rat. J. Endocrinol. 124, 247–53.CrossRefGoogle ScholarPubMed
Nayudu, P.L. & Osborn, S.M. (1992). Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J. Reprod. Fertil. 95, 349–62.CrossRefGoogle ScholarPubMed
Oktay, K., Newton, H., Mullan, J. & Gosden, R.G. (1998). Development of human primordial follicles to antral stages in SCID/hpg mice stimulated with follicle stimulating hormone. Hum. Reprod. 13, 1133–8.CrossRefGoogle ScholarPubMed
Packer, A.I., Hsu, Y.C., Besmer, P. & Bachvarova, R.F. (1994). The ligand of the c-kit receptor promotes oocyte growth. Dev. Biol. 161, 194–205.CrossRefGoogle ScholarPubMed
Parrott, J.A. & Skinner, M.K. (1997). Direct actions of KL on theca cell growth and differentiation during follicle development. Endocrinol. 138, 3819–27.CrossRefGoogle ScholarPubMed
Parrott, J.A. & Skinner, M.K. (1998). Thecal cell–granulosa cell interactions involve a positive feedback loop among keratinocyte growth factor, hepatocyte growth factor, and kit ligand during ovarian follicular development. Endocrinol. 139, 2240–5.CrossRefGoogle ScholarPubMed
Richards, J.S., Jahnsen, T., Hedlin, L., Lifka, J., Ratoosh, S., Durica, J.M. & Goldring, N.B. (1986). Ovarian follicle development: from physiology to molecular biology. Recent Progress in Hormone Research 43, 231–76.Google Scholar
Roy, S.K. & Greenwald, G.S. (1989). Hormonal requirements for the growth and differentiation of hamster preantral follicles in long-term culture. J. Reprod. Fertil. 87, 103–114.CrossRefGoogle ScholarPubMed
Roy, S.K. & Greenwald, G.S. (1990). Immunohistochemical localization of epidermal growth factor-like activity in the hamster ovary with a polyclonal antibody. Endocrinology 126, 1309–17.CrossRefGoogle ScholarPubMed
Roy, S.K. & Harris, S.G. (1994). Antisense epidermal growth factor oligodeoxynucleotides inhibit follicle-stimulating hormone-induced in vitro DNA and progesterone synthesis in hamster preantral follicles. Mol Endocrinol 8, 1175–81.Google ScholarPubMed
Singh, B., Barbe, G.J. & Armstrong, D.T. (1993). Factors influencing resumption of meiotic maturation and cumulus expansion of porcine oocyte–cumulus cell complexes in vitro.Mol. Reprod. Dev. 36, 113–9.CrossRefGoogle ScholarPubMed
Spears, N., Murray, A.A., Allison, V., Boland, N.I. & Gosden, R.G. (1998). Role of gonadotrophins and ovarian steroids in the development of mouse follicles in vitro. J. Reprod. Fertil. 113, 19–26.CrossRefGoogle ScholarPubMed
Wu, J, Dent, P, Jelinek, T., Wolfman, A., Weber, M.J. & Sturgill,, T.W. (1993). Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3′,5′-monophosphate. Science 262, 1065–9.CrossRefGoogle ScholarPubMed
Wu, J., Nayuyu, P.L., Kiesel, P.S. & Michelmann, H.W. (2000). Luteinizing hormone has a stage-limited effect on preantral follicle development in vitro. Biol. Reprod. 63, 320–327.CrossRefGoogle Scholar
Wu, J., Emery, B.R. & Carrell, D.T. (2001). In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles. Biol. Reprod. 64, 375–81.CrossRefGoogle ScholarPubMed
Wu, J., Chen, Y. & Li, T. (2002). Expression of Fas, p53 and AFP in development of human fetal germ cells in vitro. Zygote 10, 333–40.CrossRefGoogle ScholarPubMed
Yang, J.G., Chen, W.Y. & Li, P.S. (1999). Effects of glucocorticoids on maturation of porcine oocytes and their subsequent fertilizing capacity in vitro. Biol. Reprod. 60, 929–36.CrossRefGoogle ScholarPubMed
Yuan, W., Lucy, M.C. & Smith, M.F. (1996). Messenger Ribonucleic Acid for insulin-like growth factors-I and -II, insulin-like growth factor-binding protein-2, gonadotropin receptors, and steroidogenic enzymes in porcine follicles. Biol. Reprod. 55, 1045–54.CrossRefGoogle ScholarPubMed