Growth and differentiation factor-9 stimulates activation of goat primordial follicles in vitro and their progression to secondary follicles
F. S. Martins A D , J. J. H. Celestino A , M. V. A. Saraiva A , M. H. T. Matos A , J. B. Bruno A , C. M. C. Rocha-Junior B , I. B. Lima-Verde A , C. M. Lucci B , S. N. Báo C and J. R. Figueiredo AA Laboratory of Manipulation of Oocytes Enclosed in Preantral Follicles (LAMOFOPA), Veterinary Faculty, State University of Ceará, Av. Paranjana, 1700, Campus do Itaperi, Fortaleza 60740-000, CE, Brazil.
B Faculty of Veterinary Medicine, University of Brasilia, Av. Asa Norte, Campus Darcy Ribeiro, Brasilia 70910-900, DF, Brazil.
C Laboratory of Electron Microscopy, Department of Cell Biology, University of Brasilia, Av. Asa Norte, Campus Darcy Ribeiro, Brasilia 70910-900, DF, Brazil.
D Corresponding author. Email: fabriciosm@fortalnet.com.br
Reproduction, Fertility and Development 20(8) 916-924 https://doi.org/10.1071/RD08108
Submitted: 19 May 2008 Accepted: 4 August 2008 Published: 10 October 2008
Abstract
The aim of the present study was to investigate the effects of growth and differentiation factor-9 (GDF-9) on the survival and activation of preantral follicles, as well as their subsequent progression to secondary follicles, using goat ovarian cortical culture in vitro. Pieces of ovarian cortex were cultured for 1 and 7 days in minimum essential medium (MEM) with or without different concentrations of GDF-9 (1–200 ng mL–1). On Day 0 and after 1 and 7 days of culture, cortical pieces were fixed for histological and transmission electron microscopy evaluation. Preantral follicles were classified according to their development stage (primordial, intermediate, primary and secondary) and on the basis of morphological features (normal or degenerated). In addition, follicular and oocyte diameters were determined before and after culture. The results showed that, compared with non-cultured cortical tissue (Day 0), the culture of ovarian tissue significantly reduced (P < 0.05) the percentage of normal follicles in all media tested, except for tissue cultured in the presence of 200 ng mL–1 GDF-9. Furthermore, in all media tested, the percentage of primordial follicles was significantly reduced (P < 0.05), with a concomitant increase in the percentage of developing follicles. The highest percentage of secondary follicles was observed after 7 days of culture in MEM plus 200 ng mL–1 GDF-9. At all concentrations of GDF-9 tested, follicular diameter increased significantly after 7 days of culture compared with non-cultured cortical tissue. In conclusion, the results of the present study indicate that 200 ng mL–1 GDF-9 maintains the survival of preantral follicles and promotes activation of primordial follicles. Furthermore, GDF-9 stimulates the transition from primary to secondary follicles, maintaining ultrastructural integrity of the follicles.
Additional keywords: culture, GDF-9, preantral follicles.
Acknowledgements
The authors thank CAPES, CNPq, RENORBIO and all the members of our laboratory, especially undergraduate students Sarah Bezerra Honório and José Erisvaldo Maia Júnior, whose help and enthusiasm made this study possible.
Aaltonen, J. , Laitinen, M. P. , Vuojolainen, K. , Jaatinen, R. , and Horelli-Kuitunen, N. , et al. (1999). Human growth differentiation factor 9 (GDF-9) and its novel novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J. Clin. Endocrinol. Metab. 84, 2744–2750.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Bodensteiner, K. J. , Clay, C. M. , Moeller, C. L. , and Sawer, H. R. (1999). Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol. Reprod. 60, 381–386.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Braw-tal, R. , and Yossefi, S. (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fertil. 109, 165–171.
| PubMed | CAS |
Dong, J. , Albertini, 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 | CAS |
Elvin, J. A. , Clark, A. T. , Wang, P. , Wolfman, N. M. , and Matzuk, M. M. (1999). Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 13, 1035–1048.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Elvin, J. A. , Yan, C. , and Matzuk, M. M. (2000). Oocyte-expressed TGF-beta superfamily members in female fertility. Mol. Cell. Endocrinol. 159, 1–5.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Eppig, J. J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–838.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Fortune, J. E. , Kito, S. , Wandji, S. A. , and Srsen, V. (1998). Activation of bovine and baboon primordial follicles in vitro. Theriogenology 49, 441–449.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Hanrahan, J. P. , Gregan, S. M. , Mulsant, P. , Mullen, M. , Davis, G. H. , Powell, R. , and Galloway, S. M. (2004). Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol. Reprod. 70, 900–909.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Hayashi, M. , McGee, E. A. , Min, G. , Klein, C. , Rose, U. M. , van Duin, M. , and Hsueh, A. J. W. (1999). Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140, 1236–1244.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Hreinsson, J. G. , Scott, J. E. , Rasmussen, C. , Swahn, M. L. , Hsueh, A. J. , and Hovatta, O. (2002). Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J. Clin. Endocrinol. Metab. 87, 316–321.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Jaatinen, R. , Latinen, M. P. , Vuojolainen, K. , Aaltonen, J. , Louhio, H. , Heikinhemio, K. , Lehtonen, E. , and Ritvos, O. (1999). Localization of growth differentiation factor-9 (GDF-9) mRNA and protein in rat ovaries and cDNA cloning of rat GDF-9 and its novel homologue GDF-9B. Mol. Cell. Endocrinol. 156, 189–193.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Juengel, J. L. , Hudson, N. L. , Heath, D. A. , Smith, P. , and Reader, K. L. , et al. (2002). Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 67, 1777–1789.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lucci, C. M. , Silva, J. R. V. , Carvalho, C. A. , Figueiredo, J. R. , and Báo, S. N. (2001). Light microscopical and ultrastructural characterization of goat preantral follicles. Small Rumin. Res. 41, 61–69.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Martins, F. S. , Van den Hurk, R. , Santos, R. R. , Silva, J. R. V. , Matos, M. H. T. , Celestino, J. J. H. , Rodrigues, A. P. R. , Pessoa, C. , Ferreira, F. V. A. , and Figueiredo, J. R. (2005). Development of goat primordial follicles after in vitro culture of ovarian tissue in minimal essential medium supplemented with coconut water. Anim. Reprod. 2, 106–113.
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. (2007). Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro. Zygote 15, 173–182.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McGee, E. A. , and Hsueh, A. J. (2000). Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 21, 200–214.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McGrath, S. A. , Esquela, A. F. , and Lee, S. J. (1995). Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 9, 131–136.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McNatty, K. P. , Juengel, J. L. , Wilson, T. , Galloway, S. M. , and Davis, G. H. (2001). Genetic mutations influencing ovulation rate in sheep. Reprod. Fertil. Dev. 13, 549–555.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Nilsson, E. E. , and Skinner, M. K. (2002). Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol. Reprod. 67, 1018–1024.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Nilsson, E. E. , and Skinner, M. K. (2003). Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol. Reprod. 69, 1265–1272.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Orisaka, M. , Orisaka, S. J. , Jin-Yi, C. J. , Wang, Y. , Kotsuji, F. , and Tsang, B. K. (2006). Growth differentiation factor-9 is anti-apoptotic during follicular development from preantral to early antral stage. Mol. Endocrinol. 20, 2456–2468.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Perkins, G. A. , and Frey, T. G. (2000). Recent structural insight into mitochondria gained by microscopy. Micron 31, 97–111.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Salehnia, M. , Moghadan, E. A. , and Velojerdi, M. R. (2002). Ultrastructure of follicles after vitrification of mouse ovarian tissue. Fertil. Steril. 78, 644–645.
| 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 situ. Theriogenology 54, 809–822.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Silva, J. R. V. , Van Den Hurk, R. , Van Tol, H. T. A. , Roelen, B. A. J. , and Figueiredo, J. R. (2005). Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15) and BMP receptors in the ovaries of goats. Mol. Reprod. Dev. 70, 11–19.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Silva, J. R. V. , Tharasanit, T. , Taverne, M. A. M. , Van der Weijden, G. C. , Santos, R. R. , Figueiredo, J. R. , and Van den Hurk, R. (2006). The activin–follistatin system and in vitro early development in goats. J. Endocrinol. 189, 113–125.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
van den Hurk, R. , Spek, E. R. , Hage, W. J. , Fair, T. , Ralph, J. H. , and Schotanus, K. (1998). Ultrastructure and viability of isolate preantral follicles. Hum. Reprod. Update 4, 833–841.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Vitt, U. A. , Hayashi, M. , Klein, C. , and Hsueh, A. J. (2000). Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol. Reprod. 62, 370–377.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wandji, S.-A. , Eppig, J. J. , and 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, 817–832.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wang, J. , and Roy, S. K. (2004). Growth differentiation factor-9 and stem cell factor promote primordial follicle formation in the hamster: modulation by follicle-stimulating hormone. Biol. Reprod. 70, 577–585.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zhao, J. , Dorland, M. , Taverne, M. A. M. , Van Der Weijden, G. C. , Bevers, M. M. , and Van Den Hurk, R. (2000). In vitro culture of rat pre-antral follicles with emphasis on follicular interactions. Mol. Reprod. Dev. 55, 65–74.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
