Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-27T18:27:51.117Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression of follicle-stimulating hormone receptor (FSHR) in goat ovarian follicles and the impact of sequential culture medium on in vitro development of caprine preantral follicles

Published online by Cambridge University Press:  21 December 2010

M.V.A. Saraiva ,
J.J.H. Celestino ,
V.R. Araújo ,
R.N. Chaves ,
A.P. Almeida ,
I.B. Lima-Verde ,
A.B.G. Duarte ,
G.M. Silva ,
F.S. Martins  and
J.B. Bruno
...Show all authors
M.V.A. Saraiva*
Affiliation:
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.
J.J.H. Celestino
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
V.R. Araújo
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
R.N. Chaves
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
A.P. Almeida
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
I.B. Lima-Verde
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
A.B.G. Duarte
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
G.M. Silva
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.
J.B. Bruno
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
M.H.T. Matos
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
C.C. Campello
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
J.R.V. Silva
Affiliation:
Biotecnology Nucleus of Sobral (NUBIS), Federal University of Ceara, Sobral-CE, Brazil.
J.R. Figueiredo
Affiliation:
Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceara, Fortaleza-CE, Brazil.
*
All correspondence to: M.V.A. Saraiva. 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 address: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study evaluated the expression of FSH receptors (FSHR) in the different stages of goat follicle development and investigated whether the addition of increasing concentrations of FSH throughout the culture period influences the survival, growth and antral formation of in vitro-cultured caprine preantral follicles. The expression of FSHR was analysed before and after culturing follicles using real-time RT-PCR. For the culture, preantral follicles (≥150 μm) were isolated from ovarian fragments and cultured for 18 days in α-MEM+ alone or associated with recombinant FSH (rFSH: 100 or 1000 ng/ml), or in α-MEM+ supplemented with increasing concentrations of FSH throughout culture periods as follows: (a) sequential medium 1: FSH 100 ng/ml (from day 0 to 6), FSH 500 ng/ml (from day 6 to 12) and FSH 1000 ng/ml (from day 12 to 18); and (b) sequential medium 2: FSH 500 ng/ml (from day 0 to 9) and 1000 ng/ml (from day 9 to 18). Follicle development was evaluated on the basis of antral cavity formation, follicular and oocyte growth, and cumulus–oocyte complex health. The expression of FSHR in isolated caprine follicles increased from the preantral to antral phase. Regarding the culture, after 18 days, sequential medium 1 promoted follicular survival, antrum formation and a reduction in oocyte extrusion. Both sequential media promoted a higher rate of meiotic resumption compared with the other treatments. In conclusion, the addition of increased concentrations of FSH (sequential medium) has a significant impact on the in vitro development of caprine preantral follicles.

Keywords

CultureFSH receptorGoatOvarian follicleSequential FSH
Type
Research Article
Information
Zygote , Volume 19 , Issue 3 , August 2011 , pp. 205 - 214
Copyright
Copyright © Cambridge University Press 2010

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

Adriaens, I., Cortvrindt, R. & Smitz, J. (2004). Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Hum. Reprod. 19, 398–408.CrossRefGoogle ScholarPubMed
Braw, R.H. & Tsafriri, A. (1980). Follicles explanted from pentobarbitone treated rats provide a model for atresia. J. Reprod. Fertil. 59, 259–65.CrossRefGoogle Scholar
Byskov, A.G., Andersen, Y., Hossaini, C. & Guoliang, X.A. (1997). Cumulus cells of oocyte–cumulus complexes secrete a meiosis-activating substance when stimulated with FSH. Mol. Reprod. Dev. 46, 296–305.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Chappel, S.C. & Howles, C. (1991). Reevaluation of the roles of luteinizing hormone and follicle-stimulating hormone in the ovulatory process. Hum. Reprod. 6, 1206–12.CrossRefGoogle ScholarPubMed
Chaves, R.N., Martins, F.S., Saraiva, M.V., Celestino, J.J.H., Lopes, C.A., Correia, J.C., Verde, I.B., Matos, M.H., Báo, S.N., Name, K.P. et al. (2008). Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro. Reprod. Fertil. Dev. 20, 640–7.CrossRefGoogle ScholarPubMed
Chun, S.Y., Eisenhauer, K.M., Minami, S., Billig, H., Perlas, E. & Hsueh, A.J. (1996). Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor. Endocrinology 137, 1447–56.CrossRefGoogle ScholarPubMed
Cortvrindt, R., Smitz, J. & van Steirteghem, A.C. (1997). Assesment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Hum. Reprod. 12, 759–68.CrossRefGoogle Scholar
Cortvrindt, R.G., Hu, Y., Liu, J. & Smitz, J.E. (1998a). Timed analysis of the nuclear maturation of oocytes in early preantral mouse follicle culture supplemented with recombinant gonadotrophin. Fertil. Steril. 70, 1114–25.CrossRefGoogle Scholar
Cortvrindt, R., Hu, Y. & Smitz, J. (1998b). Recombinant luteinizing hormone as a survival and differentiation factor increases oocyte maturation in recombinant follicle stimulating hormone-supplemented mouse preantral follicle culture. Hum. Reprod. 13, 1292–302.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
Dufour, J., Cahill, L. & Mauleon, P. (1979). Short and long-term effects of hypophysectomy and unilateral ovariectomy on ovarian follicular populations in sheep. J. Reprod. Fertil. 57, 301–9.CrossRefGoogle Scholar
Eppig, J.J. & O'Brian, M.J. (1998). Comparison of preimplantation developmental competence after mouse oocyte growth and development in vitro and in vivo. Theriogenology 49, 415–22.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Ritter, L.J. & Armstrong, D.T. (2004). Oocyte-somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82/83, 431–46.CrossRefGoogle ScholarPubMed
Gudermann, T., Nürnberg, B. & Schultz, G. (1995). Receptors and G proteins as primary components of transmembrane signal transduction. I. G-protein-coupled receptors: structure and function. J. Mol. Med. 73, 51–63.CrossRefGoogle Scholar
Gupta, P.S.P., Ramesh, H.S., Manjunatha, B.M., Nandi, S. & Ravindra, J.P. (2008). Production of buffalo embryos using oocytes from in vitro grown preantral follicles. Zygote 16, 57–63.CrossRefGoogle ScholarPubMed
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
Hirshfield, A.N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43–101.CrossRefGoogle ScholarPubMed
Hsueh, A.J.W. & LaPolt, P.S. (1992). Molecular basis of gonadotropin receptor regulation. Trends Endocrinol. Metab. 3, 164–70.CrossRefGoogle ScholarPubMed
Hunzicker-Dunn, M. & Maizels, E.T. (2006). FSH signaling pathways in immature granulosa cells that regulate target gene expression: branching out from protein kinase A. Cell Signal 18, 1351–9.CrossRefGoogle ScholarPubMed
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
Knight, P.G. & Glister, C. (2006). TGF-β superfamily members and ovarian follicle development. Reproduction 132, 191–206.CrossRefGoogle ScholarPubMed
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
LaPolt, P.S., Tilly, J.L., Aihara, T., Nishimori, K. & Hsueh, A.J.W. (1992). Gonadotropin-induced up- and down-regulation of ovarian follicle-stimulating hormone (FSH) receptor gene expression in immature rats: effects of pregnant mare's serum gonadotropin, human chorionic gonadotropin, and recombinant FSH. Endocrinology 130, 1289–95.Google ScholarPubMed
Lucci, C.M., Amorim, C.A., Báo, S.N., Figueiredo, J.R., Rodrigues, A.P.R., Silva, J.R. & Gonçalves, P.B.D. (1999). Effect of the interval of serial sections of ovarian in the tissue chopper on the number of isolated caprine preantral follicles. Anim. Reprod. Sci. 56, 39–49.CrossRefGoogle ScholarPubMed
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
Mao, J., Smith, M.F., Rucker, E.B., Wu, G.M., McCauley, T.C., Cantley, T.C., Prather, R.S., Didion, B.A. & Day, B.N. (2004). Effect of epidermal growth factor and insulin-like growth factor I on porcine preantral follicular growth, antrum formation, and stimulation of granulosal cell proliferation and suppression of apoptosis in vitro. J. Anim. Sci. 82, 1967–75.CrossRefGoogle ScholarPubMed
Markstrom, E., Svensson, E.Ch., Shao, R., Svanberg, B. & Billig, H. (2002). Survival factors regulating ovarian apoptosis—dependence on follicle differentiation. Reproduction 123, 23–30.CrossRefGoogle ScholarPubMed
Matos, M.H.T., Lima-Verde, I.B., Luque, M.C.A., Maia, J.E. Jr, Silva, J.R., Celestino, J.J.H., Martins, F.S., Báo, S.N., Lucci, A.M. & Figueiredo, J.R. (2007). Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro. Zygote 15, 173–82.CrossRefGoogle ScholarPubMed
McGee, E.A., Perlas, E., LaPolt, P.S., Tsafriri, A. & Hsueh, A.J. (1997). Follicle-stimulating hormone enhances the development of preantral follicles in juvenile rats. Biol. Reprod. 57, 990–8.CrossRefGoogle ScholarPubMed
McNatty, K., Fidler, A., Juengel, J., Quirke, L.D., Smith, P.R., Heath, D.A., Lundy, T., O'Connell, A. & Tisdall, D.J. (2000). Growth and paracrine factors regulating follicular formation and cellular function. J. Mol. Endocrinol. 163, 11–20.CrossRefGoogle ScholarPubMed
Méduri, G., Charnaux, N., Driancourt, M.A., Combettes, L., Granet Vannier, B., Loosfelt, H. & Migrom, E. (2002). Follicle-stimulating hormone receptors in oocytes? J. Clin. Endocrinol. Metab. 87, 2266–76.CrossRefGoogle ScholarPubMed
Moor, R. & Dai, Y. (2001). Maturation of pig oocytes in vivo and in vitro. Reproduction 58, 91–104.Google ScholarPubMed
O'Shaughnessy, P.J., McLelland, D. & McBride, M.W. (1997). Regulation of luteinizing hormone-receptor and follicle stimulating hormone-receptor messenger ribonucleic acid levels during development in the neonatal mouse ovary. Biol. Reprod. 57, 602–8.CrossRefGoogle ScholarPubMed
Roy, S. & Greenwald, G. (1996). Follicular development through preantral stages: signalling via growth factors. J. Reprod. Fertil. 50, 83–94.Google ScholarPubMed
Roy, S.K. & Terada, D.M. (1999). Activities of glucose metabolic enzymes in human preantral follicles: in vitro modulation by follicle-stimulating hormone, luteinizing hormone, epidermal growth factor, insulin-like growth factor I, and transforming growth factor. Biol. Reprod. 60, 763–8.CrossRefGoogle ScholarPubMed
Saraiva, M.V.A., Celestino, J.J.H., Chaves, R.N., Martins, F.S., Bruno, J.B., Lima-Verde, I.B., Matos, M.H.T., Silva, G.M., Porfirio, E.P., Báo, S.N. et al. (2008). Influence of different concentrations of LH and FSH on in vitro caprine primordial ovarian follicle development. Small Rum. Res. 78, 87–95.CrossRefGoogle Scholar
Sasson, R., Rimon, E., Dantes, A., Cohen, T., Shinder, V., Land-Bracha, A. & Amsterdam, A. (2004). Gonadotrophin-induced gene regulation in human granulosa cells obtained from IVF patients. Modulation of steroidogenic genes, cytoskeletal genes and genes coding for apoptotic signalling and protein kinases. Mol. Hum. Reprod. 10, 299–311.CrossRefGoogle ScholarPubMed
Silva, J.M., Hamel, M., Sahmi, M. & Price, C.A. (2006). Control of oestradiol secretion and of cytochrome P450 aromatase messenger ribonucleic acid accumulation by FSH involves different intracellular pathways in oestrogenic bovine granulosa cells in vitro. Reproduction 132, 909–17.CrossRefGoogle ScholarPubMed
Simoni, M. & Nieschlag, E. (1995). FSH in therapy: physiological basis, new preparations and clinical use. Reprod. Med. Rev. 4, 163–77.CrossRefGoogle Scholar
Tilly, J.L., Kowalski, K.I., Schomberg, D.W. & Hsueh, A.J.W. (1992). Apoptosis in atretic ovarian follicles is associated with selective decreases in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase. Endocrinology 131, 1670–6.CrossRefGoogle ScholarPubMed
Tisdall, D.J., Watanabe, K., Hudson, N.L., Smith, P. & McNatty, K.P. (1995). FSH receptor gene expression during ovarian follicle development in sheep. J. Endocrinol. 15, 273–81.Google ScholarPubMed
Urban, R.J., Garmey, J.C., Shupnik, M.A. & Veldhuis, J.D. (1991). Follicle-stimulating hormone increases concentrations of messenger ribonucleic acid encoding cytochrome P450 cholesterol side-chain cleavage enzyme in primary cultures of porcine granulosa cells. Endocrinology 128, 2000–7.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., Dijkstra, G., Hulshof, S.C.J. & Vos, P.L.A.M. (1994). Micromorphology of antral follicles in cattle after prostaglandin-induced luteolysis, with particular reference to atypical granulosa cells. J. Reprod. Fertil. 100, 137–42.CrossRefGoogle ScholarPubMed
van Tol, H.T. & Bevers, M.M. (1998). Theca cells and theca-cell conditioned medium inhibit the progression of FSH-induced meiosis of bovine oocytes surrounded by cumulus cells connected to membrana granulosa. Mol. Reprod. Dev. 51, 315–21.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
van Tol, H.T., van Eijk, M.J., Mummery, C.L., van den Hurk, R. & Bevers, M.M. (1996). Influence of FSH and hCG on the resumption of meiosis of bovine oocytes surrounded by cumulus cells connected to membrane granulosa. Mol. Reprod. Dev. 45, 218–24.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Wang, Y., Rippstein, P.U. & Tsang, B.K. (2003). Role and gonadotrophic regulation of X-linked inhibitor of apoptosis protein expression during rat ovarian follicular development in vitro. Biol. Reprod. 68, 610–9.CrossRefGoogle ScholarPubMed
Webb, R., Campbell, B., Garverick, H., Gong, J., Gutierrez, C. & Armstrong, D. (1999). Molecular mechanisms regulating follicular recruitment and selection. J. Reprod. Fertil. Suppl. 53, 33–48.Google Scholar
Wu, J., Nayudu, 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, 320–7.CrossRefGoogle Scholar
Xu, Z., Garverick, H.A., Smith, G.W., Smith, M.F., Hamilton, S.A. & Youngquist, R.S. (1995). Expression of follicle-stimulating hormone and luteinizing hormone receptor messenger ribonucleic acids in bovine follicles during the first follicular wave. Biol. Reprod. 53, 951–7.CrossRefGoogle ScholarPubMed