Follicle stimulating hormone and fibroblast growth factor-2 interact and promote goat primordial follicle development in vitro
M. H. T. Matos A C , I. B. Lima-Verde A , J. B. Bruno A , C. A. P. Lopes A , F. S. Martins A , K. D. B. Santos A , R. M. P. Rocha A , J. R. V. Silva A , S. N. Báo B and J. R. Figueiredo A
+ Author Affiliations
- Author Affiliations
A Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
B Laboratory of Electron Microscopy, Department of Cell Biology, University of Brasilia, Brasilia, DF, Brazil.
C Corresponding author. Email: htmatos@yahoo.com
Reproduction, Fertility and Development 19(5) 677-684 https://doi.org/10.1071/RD07021
Submitted: 31 January 2007 Accepted: 4 May 2007 Published: 2 July 2007
Abstract
The aims of the present study were to investigate the effects of the interaction between follicle stimulating hormone (FSH) and fibroblast growth factor-2 (FGF-2) on survival, follicular growth initiation and further growth of caprine preantral follicles. Pieces of caprine ovarian cortex were cultured for 1 or 7 days in minimum essential medium (MEM) supplemented with FSH, FGF-2 or FSH + FGF-2. Small fragments from non-cultured ovarian tissue and from those cultured for 1 or 7 days were processed for classical histology and transmission electron microscopy (TEM) to verify follicular morphology and growth. The results showed that, after 7 days culture, the highest percentages of normal follicles were observed in medium supplemented with FSH. After 7 days culture, the interaction between FSH and FGF-2 was most effective to promote the initiation of primordial follicles growth and oocyte growth. TEM showed ultrastructural integrity of follicles after 1 day of culture in MEM and after 7 days in all treatments, except in those follicles cultured for 7 days in MEM. In conclusion, this study demonstrated that the interaction between FSH and FGF-2 stimulates the initiation of primordial follicles growth and the subsequent growth of developing follicles. Furthermore, these data showed that FSH is important to maintain follicular integrity after 7 days culture.
Additional keywords: caprine, culture, FGF-2, FSH, primordial follicles.
Acknowledgements
This work was supported by CNPq, FINEP and Fundação Cearense de Apoio à Pesquisa (FUNCAP). Maria Helena Tavares de Matos is a recipient of a grant from CNPq (Brazil). We would like to acknowledge the generous donation of pFSH by Dr Jean-François Beckers of the University of Liège, Belgium.
References
Amsterdam, A. , and Rotmensch, S. (1987). Structure-function relationships during granulosa cell differentiation. Endocr. Rev. 8, 309–337.
| PubMed |
Anderson, E. , and Lee, G. Y. (1993). The participation of growth factors in stimulating the quiescent, proliferative, and differentiative stages of rat granulosa cells grown in a serum-free medium. Tissue Cell 25, 49–72.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Asakai, R. , Tamura, K. , Eishi, Y. , Iwamoto, M. , Kato, Y. , and Okamo, R. (1993). Basic fibroblast growth factor (bFGF) receptors decrease with luteal age in rat ovarian luteal cells: colocalization of bFGF receptors and bFGF in luteal cells. Endocrinology 133, 1074–1084.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Assey, R. J. , Hyttel, P. , Roche, J. F. , and Boland, M. P. (1994). Infrequent structures in cattle oocytes. Anat. Embryol. (Berl.) 190, 263–271.
| PubMed |
Baker, S. J. , and Spears, N. (1997). Follicle stimulating hormone inhibits apoptosis in pre- and early-antral murine follicles in vitro. J. Reprod. Fertil. Abstr. Ser. 19, 21.
Ben-Haroush, A. , Abir, R. , Ao, A. , Jin, S. , Kessler-Icekson, G. , Feldberg, D. , and Fisch, B. (2005). Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses. Fertil. Steril. 84, 1257–1268.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cortvrindt, R. , Smitz, J. , and Van Steirteghem, A. C. (1997). Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Hum. Reprod. 12, 759–768.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Derrar, N. , Price, C. A. , and 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, 587–598.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dierich, A. , Sairam, M. R. , Monaco, L. , Fimia, G. M. , Gansmuller, A. , LeMeur, M. , and 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, 13612–13617.
| Crossref | GoogleScholarGoogle Scholar |
Dong, J. , Albertine, D. F. , Nishimori, K. , Kumar, T. R. , Lu, N. , and Matzuk, M. M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–535.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eppig, J. J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–838.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fortune, J. E. (2003). The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim. Reprod. Sci. 78, 135–163.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Galloway, S. M. , McNatty, K. P. , Cambridge, L. M. , Laitinen, M. P. , and Juengel, J. L. , et al. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279–283.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hay, M. F. , Cran, D. G. , and Moor, R. M. (1976). Structural changes occuring during atresia in sheep ovarian follicles. Cell Tissue Res. 169, 515–529.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hsueh, A. J. , Billig, H. , and Tsafriri, A. (1994). Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr. Rev. 15, 707–724.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jewgenow, K. (1996). Impact of peptide growth factors on the culture of small preantral follicles of domestic cats. Theriogenology 45, 889–895.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Joyce, I. M. , Pendola, F. L. , Wigglesworth, K. , and Eppig, J. J. (1999). Oocyte regulation of Kit ligand expression in mouse ovarian follicles. Dev. Biol. 214, 342–353.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kumar, T. R. , Wang, Y. , Lu, N. , and Matzuk, M. M. (1997). Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 15, 201–204.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mao, J. , Wu, G. , Smith, M. F. , McCauley, T. C. , Cantley, T. C. , Prather, R. S. , Didion, B. A. , and 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, 1197–1203.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Matos, M. H. T. , Lima-Verde, I. B. , Luque, M. C. A. , Maia, J. E. , Silva, J. R. V. , Celestino, J. J. H. , Martins, F. S. , Báo, S. N. , Lucci, C. M. , and Figueiredo, J. R. (2007a). Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro. Zygote ,In press.
Matos, M. H. T. , van den Hurk, R. , Lima-Verde, I. B. , Luque, M. C. A. , Santos, K. D. B. , Martins, F. S. , Báo, S. N. , Lucci, C. M. , and Figueiredo, J. R. (2007b). Effects of fibroblast growth factor-2 on the in vitro culture of caprine preantral follicles. Cells Tissues Organs ,In press.
McGee, E. , Spears, N. , Minami, S. , Hsu, S.-Y. , Chun, S.-Y. , Billig, H. , and 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, 2417–2424.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Méduri, G. , Charnaux, N. , Driancourt, M.-A. , Combettes, L. , Granet, P. , Vannier, B. , Loosfelt, H. , and Milgrom, E. (2002). Follicle-stimulating hormone receptors in oocytes? J. Clin. Endocrinol. Metab. 87, 2266–2276.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nilsson, E. , Parrott, J. A. , and Skinner, M. K. (2001). Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol. Cell. Endocrinol. 175, 123–130.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ojeda, S. R. , and Dissen, G. A. (1994). Developmental regulation of the ovary via growth factor tyrosine kinase recptors. Trends Endocrin. Met. 5, 317–323.
| Crossref | GoogleScholarGoogle Scholar |
O’Shaughnessy, P. J. , Dudley, K. , and Rajapaksha, W. R. (1996). Expression of follicle stimulating hormone-receptor mRNA during gonadal development. Mol. Cell. Endocrinol. 125, 169–175.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Parrott, J. A. , and Skinner, M. K. (1999). Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140, 4262–4271.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roberts, R. D. , and Ellis, R. C. L. (1999). Mitogenic effects of fibroblast growth factors on chicken granulosa and theca cells in vitro. Biol. Reprod. 61, 1387–1392.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roy, S. K. , and Greenwald, G. S. (1991). In vitro effects of epidermal growth factor, insulin-like growth factor-I, fibroblast growth factor, and follicle-stimulating hormone on hamster follicular deoxyribonucleic acid synthesis and steroidogenesis. Biol. Reprod. 44, 889–896.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sadeu, J. C. , Cortvrindt, R. , Ron-El, R. , Kasterstein, E. , and Smitz, J. (2006). Morphological and ultrastructural evaluation of cultured frozen-thawed human fetal ovarian tissue. Fertil. Steril. 85, 1130–1141.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Saha, S. , Shimizu, M. , Geshi, M. , and Izaike, Y. (2000). In vitro culture of bovine preantral follicles. Anim. Reprod. Sci. 63, 27–39.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Silva, J. R. V. , Lucci, C. M. , Carvalho, F. C. A. , Báo, S. N. , Costa, S. H. F. , Santos, R. R. , and 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, 809–822.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Silva, J. R. V. , Báo, S. N. , Lucci, C. M. , Carvalho, F. C. A. , Andrade, E. R. , Ferreira, M. A. L. , and Figueiredo, J. R. (2001). Morphological and ultrastructural changes occurring during degeneration of goat preantral follicles preserved in vitro. Anim. Reprod. Sci. 66, 209–223.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Silva, J. R. V. , Van den Hurk, R. , Matos, M. H. T. , Santos, R. R. , Pessoa, C. , Moraed, M. O. , and Figueiredo, J. R. (2004). Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology 61, 1691–1704.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shikone, T. , Yamoto, M. , and Nakano, R. (1992). Follicle-stimulating hormone induces functional receptors for basic fibroblast growth factor in rat granulosa cells. Endocrinology 131, 1063–1068.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thomas, F. H. , Ethier, J.-F. , Shimasaki, S. , and Vanderhyden, B. C. (2005). Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors. Endocrinology 146, 941–949.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tilly, J. L. , Billig, H. , Kowalski, K. I. , and Hsueh, A. J. (1992). Epidermal growth factor and basic fibroblast growth factor supress the spontaneous onset of apoptosis in cultured rat ovarian granulosa cells and follicles by a tyrosine-kinase-depedent mechanism. Mol. Endocrinol. 6, 1942–1950.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Trolice, M. P. , Pappalardo, A. , and Peluso, J. J. (1997). Basic fibroblast growth factor and N-Cadherin maintain rat granulosa cell and ovarian surface epithelial cell viability by stimulating the tyrosine phosphorylation of the fibroblast growth factor receptors. Endocrinology 138, 107–113.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Van den Hurk, R. , and Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–1751.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Van den Hurk, R. , Spek, E. R. , Hage, W. J. , Fair, T. , Ralph, J. H. , and Schotanus, K. (1998). Ultrastructure and viability of isolated bovine preantral follicles. Hum. Reprod. 4, 833–841.
| Crossref | GoogleScholarGoogle Scholar |
Vernon, R. K. , and Spicer, L. J. (1994). Effects of basic fibroblast growth factor and heparin on follicle-stimulating hormone-induced streroidogenesis by bovine granulosa cells. J. Anim. Sci. 72, 2696–2702.
| PubMed |
Wandji, S. , Fortier, M. A. , and Sirard, M. (1992). Differential response to gonadotrophins and prostaglandin E2 in ovarian tissue during prenatal and postnatal development in cattle. Biol. Reprod. 46, 1034–1041.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wandji, S.-A. , Eppig, J. J. , and Fortune, J. E. (1996a). FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology 45, 817–832.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wandji, S.-A. , Srsen, V. , Voss, A. K. , Eppig, J. J. , and Fortune, J. E. (1996b). Initiation in vitro of growth of bovine primordial follicles. Biol. Reprod. 55, 942–948.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhou, H. , and Zhang, Y. (2005). Regulation of in vitro growth of preantral follicles by growth factors in goats. Domest. Anim. Endocrin. 28, 235–242.
| Crossref | GoogleScholarGoogle Scholar |
