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Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro

  • M.H.T. Matos (a1), I.B. Lima-Verde (a2), M.C.A. Luque (a3), J.E. Maia Jr (a1), J.R.V. Silva (a1), J.J.H. Celestino (a1), F.S. Martins (a1), S.N. Báo (a3), C.M. Lucci (a4) and J.R. Figueiredo (a1)...

Summary

The aims of the present study were to investigate the effects of follicle-stimulating hormone (FSH) on survival, activation and growth of caprine primordial follicles using histological and ultrastructural studies. Pieces of caprine ovarian cortex were cultured for 1 or 7 days in minimum essential medium (MEM – control medium) supplemented with different concentrations of FSH (0, 10, 50 or 100 ng/ml). Small fragments from non-cultured ovarian tissue and from those cultured for 1 or 7 days in a specific medium were processed for classical histology and transmission electron microscopy (TEM). Additionally, effects of FSH on oocyte and follicle diameter of cultured follicles were evaluated. The results showed that the lowest percentage of normal follicles was observed after 7 days of culture in control medium. After 1 day of culture, a higher percentage of growing follicles was observed in the medium supplemented with 50 ng/ml of FSH. In the presence of 10 and 50 ng/ml of FSH, an increase in diameter of both oocyte and follicle on day 7 of culture was observed. TEM showed ultrastructural integrity of follicles after 1 day of culture in MEM and after 7 days in MEM plus 50 ng/ml FSH, but did not confirm the integrity of those follicles cultured for 7 days in MEM. In conclusion, this study demonstrated that FSH at concentration of 50 ng/ml not only maintains the morphological integrity of 7 days cultured caprine preantral follicles, but also stimulate the activation of primordial follicles and the growth of activated follicles.

Copyright

Corresponding author

All correspondence to: Maria Helena T. Matos, Programa de Pós-Graduação em Ciências Veterinárias (PPGCV), Laboratório de Manipulação de Oócitos e Folículos Pré-Antrais (LAMOFOPA), Universidade Estadual do Ceará (UECE), Av. Paranjana, 1700, Campus do Itaperi, Fortaleza–CE–Brasil. CEP: 60740–000. Tel: +55 85 3101 9852. Fax: +55 85 3101 9840. e-mail: htmatos@yahoo.com

References

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Abel, M.H., Wootton, A.N., Wilkins, V., Huhtaniemi, I., Knight, P.G. & Charlton, H.M. (2000). The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 141, 17951803.
Abir, R., Franks, S., Mobberley, M.A., Moore, P.A., Margara, R.A. & Winston, R.M.L. (1997). Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fert. Steril. 68, 682–8.
Adriaens, I., Cortvrindt, R. & Smitz, J. (2004). Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Human Reprod. 19, 398408.
Amsterdam, A. & Rotmensch, S. (1987). Structure–function relationships during granulosa cell differentiation. Endocr. Rev. 8, 309–37.
Assey, R.J., Hyttel, P., Roche, J.F. & Boland, M.P. (1994). Infrequent structures in cattle oocytes. Anat. Embryol. 190, 263–71.
Baker, S.J. & Spears, N. (1997). Follicle stimulating hormone inhibits apoptosis in pre- and early-antral murine follicles in vitro. J. Reprod. Fertil Abstr. Ser. 19, 21.
Beau, I., Touraine, P., Meduri, G., Gougeon, A., Desroches, A., Matuchansky, C., Milgrom, E., Kuttenn, F. & Misrahi, M. (1998). A novel phenotype related to partial loss of function mutations of the follicle stimulating hormone receptor. J. Clin. Invest. 102, 1352–9.
Boland, N.I., Humpherson, P.G., Leese, H.J. & Gosden, R.G. (1993). Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro. Biol. Reprod. 48, 798806.
Braw-Tal, R. & Yossefi, S. (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fert. 109, 165–71.
Cecconi, S., Barboni, B., Coccia, M. & Mattioli, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594601.
Chun, S.Y., Billig, H., Tilly, J.L., Furuta, I., Tsafriri, A. & Hsueh, A.J. (1994). Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor I. Endocrinology 135, 1845–53.
Cortvrindt, R., Smitz, J. & Van Steirteghem, A.C. (1996). In vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepubertal mice in a simplified culture system. Human Reprod. 11, 2656–66.
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.
Cortvrindt, R., Hu, Y. & Smitz, J. (1998). Recombinant luteinizing hormone as a survival and differentiation factor increases oocyte maturation in recombinant follicle stimulating hormone-supplemented mouse preantral follicle culture. Human Reprod. 13, 12921302.
Derrar, N., Price, C.A. & Sirard, M.-A. (2000). Effect of growth factors and co-culture with ovarian medulla on the activation of primordial follicles in explants of bovine ovarian cortex. Theriogenology 54, 587–98.
Dierich, A., Sairam, M.R., Monaco, L., Fimia, G.M., Gansmuller, A., LeMeur, M. & Sassone-Corsi, P. (1998). Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci USA 95, 13612–7.
Dong, J., Albertine, D.F., Nishimori, K., Kumar, T.R., Lu, N. & Matzuk, M.M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–5.
Dorrington, J.H., Moon, Y.S. & Armstrong, D.T. (1975). Estradiol-17beta biosynthesis in cultured granulosa cells from hypophysectomized immature rats; stimulation by follicle-stimulating hormone. Endocrinology 97, 1328–31.
Eppig, J.J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–38.
Fauser, B.C. & Van Heusden, A.M. (1997). Manipulation of human ovarian function: physiological concepts and clinical consequences. Endocr. Rev. 18, 71106.
Fortune, J.E., Kito, S., Wandji, S.-A. & Srsen, V. (1998). Activation of bovine and baboon primordial follicles in vitro. Theriogenology 49, 441–9.
Fuku, E., Xia, L. & Downey, B.R (1995). Ultrastructural changes in bovine oocytes cryopreserved by vitrification. Cryobiology 32, 139–56.
Galloway, S.M., McNatty, K.P., Cambridge, L.M., Laitinen, M.P., Juengel, J.L., Jokiranta, T.S., McLaren, R.J., Luiro, K., Dodds, K.G., Montgomery, G.W., Beattie, A.E., Davis, G.H. & Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279–83.
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.
Hay, M.F., Cran, D.G. & Moor, R.M. (1976). Structural changes occuring during atresia in sheep ovarian follicles. Cell Tissue Res. 169, 515–29.
Hsueh, A.J., Billig, H. & Tsafriri, A. (1994). Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr. Rev. 15, 707–24.
Hulshof, S.C.J., Figueiredo, J.R., Beckers, J.F., Bevers, M.M. & Van Den Hurk, R. (1994). Isolation and characterization of preantral follicles from foetal bovine ovaries. Vet Q. 18, 7880.
Itoh, T., Kacchi, M., Abe, H., Sendai, Y. & Hoshi, H. (2002). Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biol. Reprod. 67, 1099–105.
Joyce, I.M., Pendola, F.L., Wigglesworth, K. & Eppig, J.J. (1999). Oocyte regulation of Kit ligand expression in mouse ovarian follicles. Dev. Biol. 214, 342–53.
Kreeger, P.K., Fernandes, N.N., Woodruff, T.K. & Shea, L.D. (2005). Regulation of mouse follicle development by follicle stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose. Biol. Reprod. 73, 942–50.
Kumar, T.R., Wang, Y., Lu, N. & Matzuk, M.M. (1997). Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 15, 201–4.
Mao, J., Wu, G., Smith, M.F., McCauley, T.C., Cantley, T.C., Prather, R.S., Didion, B.A. & Day, B.N. (2002). Effects of culture medium, serum type, and various concentrations of follicle-stimulating hormone on porcine preantral follicular development and antrum formation in vitro. Biol. Reprod. 67, 1197–203.
McGee, E., Spears, N., Minami, S., Hsu, S.-Y., Chun, S.-Y., Billig, H. & Hsueh, A.J.W. (1997). 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. Endocrinology 138, 2417–24.
Méduri, G., Charnaux, N., Driancourt, M.-A., Combettes, L., Granet, P., Vannier, B., Loosfelt, H. & Migrom, E. (2002). Follicle-stimulating hormone receptors in oocytes? J. Clin. Endocrinol. Metab. 87, 2266–76.
Mitchell, L.M., Kennedy, C.R. & Hartshorne, G.M. (2002). Effects of varying gonadotrophin dose and timing on antrum formation and ovulation efficiency of mouse follicles in vitro. Human Reprod. 17, 1181–8.
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.
Nilsson, E.E. & Skinner, M.K. (2001). Cellular interactions that control primordial follicle development and folliculogenesis. J. Soc. Gynecol. Investig. 8, 1720.
Oktay, K., Briggs, D. & Gosden, R.G. (1997). Ontogeny of follicle-stimulating hormone receptor gene expression in solated human ovarian follicles. J. Clin. Endocrinol. Metab. 82, 3748–51.
O'Shaughnessy, P.J., Dudley, K. & Rajapaksha, W.R. (1996). Expression of follicle stimulating hormone-receptor mRNA during gonadal development. Mol. Cell. Endocrinol. 125, 169–75.
Parrott, J.A. & Skinner, M.K. (1998). Thecal cell–granulosa cell interactions involve a positive freedback loop among keratinocyte growth factor, hepatocyte growth factor, and kit ligand during ovarian follicular development. Endocrinology 139, 2240–5.
Parrot, J.A. & Skinner, M.K. (1999). Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140, 4262–71.
Ralph, J.H., Wilmut, I. & Telfer, E.E. (1995). In vitro growth of bovine preantral follicles and the influence of FSH on follicular and oocyte diameters. J. Reprod. Fertil. 15, Abstr. Series., 6 abstr.
Ralph, J.H., Wilmut, I. & Telfer, E.E. (1996). The effect of FSH on bovine preantral to early antral ovarian follicle growth in vitro. Biol. Reprod. 54 (Suppl 1.), 5 abstract.
Roy, S.K. & Treacy, B.J. (1993). Isolation and long-term culture of human preantral follicles. Fert. Steril. 59, 783–91.
Roy, S.K. & Albee, L. (2000). Requirement for follicle-stimulating hormone action in the formation of primordial follicles during perinatal ovarian development in the hamster. Endocrinology 141, 4449–56.
Saha, S., Shimizu, M., Geshi, M. & Izaike, Y. (2000). In vitro culture of bovine preantral follicles. Anim. Reprod. Sci. 63, 2739.
Salehnia, M., Moghadam, E.A. & Velojerdi, M.R. (2002). Ultrastructure of follicles after vitrification of mouse ovarian tissue. Fert. Steril. 78, 644–5.
Silva, J.R.V., Lucci, C.M., Carvalho, F.C.A., Báo, S.N., Costa, S.H.F., Santos, R.R. & Figueiredo, J.R. (2000). Effect of coconut water and Braun-Collins solutions at different temperatures and incubation times on the morphology of goat preantral follicles preserved in vitro. Theriogenology 54, 809–22.
Silva, J.R.V., Báo, S.N., Lucci, C.M., Carvalho, F.C.A., Andrade, E.R., Ferreira, M.A.L. & Figueiredo, J.R. (2001). Morphological and ultrastructural changes occurring during degeneration of goat preantral follicles preserved in vitro. Animal Reprod. Sci. 66, 209–23.
Silva, J.R.V., Van Den Hurk, R., Matos, M.H.T., Santos, R.R., Pessoa, C., Moraed, M.O. & Figueiredo, J.R. (2004). Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology 61, 1691–704.
Spears, N., Murray, A.A., Alisson, V., Boland, N.I. & Gosden, R.G. (1998). Role of gonadotrofins and ovarian steroids in the development of mouse follicles in vitro. J. Reprod. Fertil. 113, 1926.
Tassel, R. & Kennedy, J.P. (1980). Early follicular development and atretic changes in the ovary of the lamb–fine structure and histochemistry. Aust. J. Biol. Sci. 33, 675–87.
Thomas, F.H., Ethier, J.-F., Shimasaki, S. & Vanderhyden, B.C. (2005). Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors. Endocrinology 146, 941–9.
Touraine, P., Beau, I., Gougeon, A., Meduri, G., Desroches, A., Pichard, C., Detoeuf, M., Paniel, B., Prieur, M., Zorn, J.R., Milgrom, E., Kuttenn, F. & Misrahi, M. (1999). New natural inactivating mutations of the follicle-stimulating hormone receptor: correlations between receptor function and phenotype. Mol. Endocrinol. 13, 1844–54.
Ulloa-Aguirre, A., Midgley, A.R. Jr., Beitins, I.Z. & Padmanabhan, V. (1995). Follicle-stimulating isohormones: characterization and physiological relevance. Endocr. Rev. 16, 765–87.
Van Den Hurk, R. & Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–51.
Van den Hurk, R., Spek, E.R., Hage, W.J., Fair, T., Ralph, J.H. & Schotanus, K. (1998). Ultrastructure and viability of isolated bovine preantral follicles. Human Reprod. 4, 833–41.
Wandji, S.-A., Srsen, V., Voss, A.K., Eppig, J.J. & Fortune, J.E. (1996). Initiation in vitro of growth of bovine primordial follicles. Biol. Reprod. 55, 942–8.
Wright, C.S., Hovatta, O., Margara, R., Trew, G., Winston, R.M.L., Franks, S. & Hardy, K. (1999). Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles. Human Reprod. 14, 1555–62.
Wu, J., Nayudu, P.L., Kiesel, P.S. & Michelmann, H.W. (2000). Luteinizing hormone has a stage-limited effect on preantral follicles development in vitro. Biol. Reprod. 63, 320–7.
Zhao, J., Dorland, M., Taverne, M.A.M., Van Der Weijden, G.C., Bevers, M.M. & Van Den Hurk, R. (2000). In vitro culture of rat pre-antral follicles with emphasis on follicular interactions. Mol. Reprod. Develop. 55, 6574.
Zhou, H. & Zhang, Y. (2005). Regulation of in vitro growth of preantral follicles by growth factors in goats. Domest. Anim. Endoc. 28, 235–42.

Keywords

Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro

  • M.H.T. Matos (a1), I.B. Lima-Verde (a2), M.C.A. Luque (a3), J.E. Maia Jr (a1), J.R.V. Silva (a1), J.J.H. Celestino (a1), F.S. Martins (a1), S.N. Báo (a3), C.M. Lucci (a4) and J.R. Figueiredo (a1)...

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