Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-29T12:59:27.289Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  01 May 2007

M.H.T. Matos*
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
I.B. Lima-Verde
Affiliation:
Faculty of Veterinary Medicine, PPGCV, Federal Rural University of Pernambuco, Recife, PE, Brazil.
M.C.A. Luque
Affiliation:
Laboratory of Electron Microscopy, Department of Cell Biology, University of Brasilia, Brasilia, DF, Brazil.
J.E. Maia Jr
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
J.R.V. Silva
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
J.J.H. Celestino
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
F.S. Martins
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
S.N. Báo
Affiliation:
Laboratory of Electron Microscopy, Department of Cell Biology, University of Brasilia, Brasilia, DF, Brazil.
C.M. Lucci
Affiliation:
Faculty of Veterinary Medicine, University of Brasilia, Brasilia, DF, Brazil.
J.R. Figueiredo
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
*
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: [email protected]

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.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2007

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

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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Amsterdam, A. & Rotmensch, S. (1987). Structure–function relationships during granulosa cell differentiation. Endocr. Rev. 8, 309–37.CrossRefGoogle ScholarPubMed
Assey, R.J., Hyttel, P., Roche, J.F. & Boland, M.P. (1994). Infrequent structures in cattle oocytes. Anat. Embryol. 190, 263–71.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Cecconi, S., Barboni, B., Coccia, M. & Mattioli, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594601.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Eppig, J.J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–38.CrossRefGoogle ScholarPubMed
Fauser, B.C. & Van Heusden, A.M. (1997). Manipulation of human ovarian function: physiological concepts and clinical consequences. Endocr. Rev. 18, 71106.Google ScholarPubMed
Fortune, J.E., Kito, S., Wandji, S.-A. & Srsen, V. (1998). Activation of bovine and baboon primordial follicles in vitro. Theriogenology 49, 441–9.CrossRefGoogle ScholarPubMed
Fuku, E., Xia, L. & Downey, B.R (1995). Ultrastructural changes in bovine oocytes cryopreserved by vitrification. Cryobiology 32, 139–56.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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
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.CrossRefGoogle ScholarPubMed
Hsueh, A.J., Billig, H. & Tsafriri, A. (1994). Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr. Rev. 15, 707–24.Google ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.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
Nilsson, E.E. & Skinner, M.K. (2001). Cellular interactions that control primordial follicle development and folliculogenesis. J. Soc. Gynecol. Investig. 8, 1720.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Parrot, J.A. & Skinner, M.K. (1999). Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140, 4262–71.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
Roy, S.K. & Treacy, B.J. (1993). Isolation and long-term culture of human preantral follicles. Fert. Steril. 59, 783–91.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Saha, S., Shimizu, M., Geshi, M. & Izaike, Y. (2000). In vitro culture of bovine preantral follicles. Anim. Reprod. Sci. 63, 2739.CrossRefGoogle ScholarPubMed
Salehnia, M., Moghadam, E.A. & Velojerdi, M.R. (2002). Ultrastructure of follicles after vitrification of mouse ovarian tissue. Fert. Steril. 78, 644–5.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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 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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 6574.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Zhou, H. & Zhang, Y. (2005). Regulation of in vitro growth of preantral follicles by growth factors in goats. Domest. Anim. Endoc. 28, 235–42.CrossRefGoogle ScholarPubMed