Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-20T15:31:49.946Z Has data issue: false hasContentIssue false
  • English
  • Français

Stability of housekeeping genes and expression of locally produced growth factors and hormone receptors in goat preantral follicles

Published online by Cambridge University Press:  30 June 2010

Isana M. A. Frota ,
Cintia C. F. Leitão ,
José J. N. Costa ,
Ivina R. Brito ,
Robert van den Hurk  and
José R. V. Silva
Isana M. A. Frota
Affiliation:
Biotechnology Nucleus of Sobral – NUBIS, Federal University of Ceara, Av. Geraldo Rangel 100, CEP 62041-040, Sobral, CE, Brazil.
Cintia C. F. Leitão
Affiliation:
Biotechnology Nucleus of Sobral – NUBIS, Federal University of Ceara, Av. Geraldo Rangel 100, CEP 62041-040, Sobral, CE, Brazil.
José J. N. Costa
Affiliation:
Biotechnology Nucleus of Sobral – NUBIS, Federal University of Ceara, Av. Geraldo Rangel 100, CEP 62041-040, Sobral, CE, Brazil.
Ivina R. Brito
Affiliation:
Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, CE, Brazil.
Robert van den Hurk
Affiliation:
Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
José R. V. Silva*
Affiliation:
Biotechnology Nucleus of Sobral – NUBIS, Federal University of Ceara, Av. Geraldo Rangel 100, CEP 62041-040, Sobral, CE, Brazil.
*
All correspondence to J.R.V. Silva. Biotechnology Nucleus of Sobral – NUBIS, Federal University of Ceara, Av. Geraldo Rangel 100, CEP 62041-040, Sobral, CE, Brazil. Tel:/Fax: +55 88 36132603. e-mail: jrvsilva@ufc.br
Get access Rights & Permissions [Opens in a new window]

Summary

The aim of the present study was to investigate the stability of six housekeeping genes, and the relative expression of growth factors (EGF, GDF-9, BMP-15, VEGF, FGF-2, BMP-6, IGF-1 and KL) and hormone receptors (FSH, LH and GH) in goat preantral follicles. To evaluate to stability of housekeeping genes micro-dissected fresh follicles (150–200 μm) as well as follicles that have been in vitro cultured for 12 days were used. In addition, isolated fresh follicles were used to compare expression of various growth factors and hormone receptors before culture. Both fresh and cultured follicles were subjected to total RNA extraction and synthesis of cDNA. After amplification of cDNA by real-time PCR, the geNorm software program was used to evaluate the stability of glyceraldehyde-2-phosphate dehydrogenase (GAPDH), β-tubulin, β-actin, phosphoglycerokinase (PGK), 18S rRNA, ubiquitin (UBQ) and ribosomal protein 19 (RPL-19). In addition, follicular steady-state levels of mRNA from the various growth factors under study were compared. Results demonstrated that, in goat preantral follicles, UBQ and β-actin were the most suitable reference genes and thus could be used as parameters to normalize data from future in vitro studies. In contrast, 18S RNA appeared the least stable gene among the tested housekeeping genes. Analysis of mRNA for several hypophyseal hormone receptors in fresh preantral follicles showed significantly higher FSH-R mRNA levels than those of LH-R and GH-R, and no difference between GH-R and LH-R mRNA levels. In regard growth factor mRNA expression in goat preantral follicles, EGF mRNA levels appeared significantly lower than those of the other studied growth factors. Increasingly higher relative mRNA levels were observed for GDF-9, BMP-15, BMP-6, FGF-2, VEGF, Kl and IGF-1, successively. In conclusion, UBQ and β-actin are the most stable housekeeping genes in fresh and 12-days cultured caprine preantral follicles. Furthermore, in fresh follicles, high levels of FSH-R mRNA are detected while among eight growth factors, IGF-1 is the most highly expressed and EGF the weakest expressed compound.

Keywords

GoatGrowth factorsHousekeeping genesHypophyseal hormone receptorsmRNAOvarian follicles
Type
Research Article
Information
Zygote , Volume 19 , Issue 1 , February 2011 , pp. 71 - 83
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

Abir, R., Franks, S., Mobberley, M.A., Moore, P.A., Margara, R.A. & Winston, R.M.Mechanical isolation and in vitro growth of preantral and small antral human follicles. (1997). Fertil. Steril. 68, 682–8.CrossRefGoogle ScholarPubMed
Abir, R., Garor, R., Felz, C., Nitke, S., Krissi, H. & Fisch, B. (2008). Growth hormone and its receptor in human ovaries from fetuses and adults. Fertil. Steril. 90, 1333–39.CrossRefGoogle ScholarPubMed
Banda, M., Bommineni, A., Thomas, R.A., Luckinbill, L.S. & Tucker, J.D. (2008). Evaluation and validation of housekeeping genes in response to ionizing radiation and chemical exposure for normalizing RNA expression in real-time PCR. Mutat. Res. 649, 126–34.CrossRefGoogle ScholarPubMed
Ben-Haroush, A., Abir, R., Ao, A., Jin, S., Kesler-Icekson, G., Feldberg, D. & Fisch, B. (2005). Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses. Fertil. Steril. 84, 1257–68.CrossRefGoogle ScholarPubMed
Berisha, B., Sinowatz, F. & Schams, D. (2004). Expression and localization of fibroblast growth factor (FGF) family members during the final growth of bovine ovarian follicles. Mol. Reprod. Dev. 67, 162–71.CrossRefGoogle ScholarPubMed
Braw-Tal, R. & Roth, Z. (2005). Gene expression for LH receptor, 17 alpha-hydroxylase and StAR in the theca interna of preantral and early antral follicles in the bovine ovary. Reproduction 129, 453–61.CrossRefGoogle ScholarPubMed
Bruno, J.B., Celestino, J.J., Lima-Verde, I.B., Lima, L.F., Matos, M.H., Araújo, V.R., Saraiva, M.V., Martins, F.S., Name, K.P., Campello, C.C., Báo, S.N., Silva, J.R. & Figueiredo, J.R. (2009). Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF. Reprod. Fertil. Dev. 21, 679–87.CrossRefGoogle ScholarPubMed
Carlsson, B., Nilsson, A., Isaksson, O.G. & Billig, H. (1993). Growth hormone-receptor messenger RNA in the rat ovary: regulation and localization. Mol. Cell. Endocrinol. 95, 59–66.CrossRefGoogle ScholarPubMed
Cecconi, S., Barboni, B., Coccia, M. & Mattioli, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594–601.CrossRefGoogle ScholarPubMed
Chang, H., Brown, C.W. & Matzuk, M.M. (2002). Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocrinology Rev. 23, 787–823.CrossRefGoogle ScholarPubMed
Cortvrindt, R., Smitz, J. & Van Steirteghem, A. C. (1996). Ovary and ovulation: In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Hum. 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. Hum. Reprod. 12, 759–68.CrossRefGoogle ScholarPubMed
Cortvrindt, R.G., Hu, Y., Liu, J. & Smitz, J.E. (1998). Timed analysis of the nuclear maturation of oocytes in early preantral mouse follicle culture supplemented with recombinant gonadotropin. Fertil. Steril. 70, 1114–25.CrossRefGoogle ScholarPubMed
Danforth, D.R., Arbogast, L.K., Ghosh, S., Dickerman, A., Rofagha, R. & Friedman, C.I. (2001).Vascular endothelial growth factor stimulates preantral follicle growth in the rat ovary. Biol. Reprod. 68, 1736–41.CrossRefGoogle Scholar
Danilovich, N.A., Bartke, A. & Winters, T.A. (2000). Ovarian follicle apoptosis in bovine growth hormone transgenic mice. Biol. Reprod. 62, 103.CrossRefGoogle ScholarPubMed
Eckery, D.C., Moeller, C.L., Nett, T.M. & Sawyer, H.R. (1997). Localization and quantification of binding sites for follicle-stimulating hormone, luteinizing hormone, growth hormone, and insulin-like growth factor I in sheep ovarian follicles. Biol. Reprod. 57, 507–13.CrossRefGoogle ScholarPubMed
Elvin, J.A. & Matzuk, M.M. (1998). Mouse models of ovarian failure. Reproduction 3, 183–95.Google ScholarPubMed
Erickson, G.F. & Shimasaki, S. (2003). The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod. Biol. Endocrinol. 1, 9.CrossRefGoogle ScholarPubMed
Fortune, J.E. (2003). The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim. Reprod. Sci. 78, 135–63.CrossRefGoogle ScholarPubMed
Fortune, J.E., Rivera, G.M. & Yang, M.Y. (2004). Follicular development: the role of the follicular microenvironment in selection of the dominant follicle. Anim. Reprod. Sci. 82–83, 109–26.CrossRefGoogle Scholar
Garcia-Vallejo, J.J., Van het Hof, B., Robben, J., Van Wijk, J.A.E., Van Die, I., Joziasse, D.H. & Van Dijk, K. (2004). Approach for defining endogenous reference genes in gene expression experiments. Anal. Biochem. 329, 293–99.CrossRefGoogle ScholarPubMed
Garnett, K., Wang, J. & Roy, S.K. (2002). Spatiotemporal expression of EGF receptor messenger RNA and protein in the hamster ovary, p. follicle stage specific differential modulation by follicle-stimulating hormone, luteinizing hormone, estradiol, and progesterone. Biol. Reprod. 67, 1593–604.CrossRefGoogle ScholarPubMed
Glister, C., Kemp, C.F. & Knight, P.G. (2004). Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin. Reproduction 127, 239–54.CrossRefGoogle ScholarPubMed
Gong, J.G., Bramley, T. & Webb, R. (1991). The effect of recombinant bovine somatotropin on ovarian function in heifers, p. follicular population and peripheral hormones. Biol. Reprod. 45, 941–49.CrossRefGoogle ScholarPubMed
Gong, J.G., Baxter, G., Bramley, T.A. & Webb, R. (1997).Enhancement of ovarian follicle development in heifers by treatment with recombinant bovine somatotrophin, p. a dose–response study. J. Reprod. Fertil. 110, 91–97.CrossRefGoogle Scholar
Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A. & Peelman, L.J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. Dev. Biol. 5, 27.Google ScholarPubMed
Guthridge, M., Bertolini, J., Cowling, J. & Hearn, M.T. (1992). Localization of bFGF mRNA in cyclic rat ovary, diethylstilbesterol primed rat ovary, and cultured rat granulosa cells. Growth Factors 7, 15–25.Google 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
Hattori, M.A., Yoshino, E., Shinohara, Y., Horiuchi, R. & Kojima, I. (1995). A novel action of epidermal growth factor in rat granulosa cells: its potentiation of gonadotrophin action. J. Mol. Endocrinol. 15, 283–91.CrossRefGoogle ScholarPubMed
Hayashi, M., Mcgee, E.A., Min, G., Klein, C., Rose, U.M., Van Duin, M. & Hsueh, A.J.W. (1999). Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early follicles. Endocrinology 140, 1236–44.CrossRefGoogle Scholar
Kishi, H. & Greenwald, G. S. (1999a). Autoradiographic analysis of follicle-stimulating hormone and human chorionic gonadotropin receptors in the ovary of immature rats treated with equine chorionic gonadotropin. Biol. Reprod. 61, 1171–76.CrossRefGoogle ScholarPubMed
Kishi, H. & Greenwald, G. S. (1999b). In vitro steroidogenesis by dissociated rat follicles, primary to antral, before and after injection of equine chorionic gonadotropin. Biol. Reprod. 61, 1177–83.CrossRefGoogle ScholarPubMed
Hreinsson, J.G., Scott, J.E., Rasmussen, C., Swahn, M.L., Hsueh, A.L.W. & 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, 316–21.CrossRefGoogle ScholarPubMed
Hsieh, M., Zamah, A.M. & Conti, M. (2009).Epidermal growth factor-like growth factors in the follicular fluid: role in oocyte development and maturation. Semin. Reprod. Endocrinol. 27. 52–61.CrossRefGoogle ScholarPubMed
Huanmin, Z. & Yong, Z. (2000). In vitro development of caprine ovarian preantral follicles. Theriogenology 54, 641–50.CrossRefGoogle ScholarPubMed
Huggett, J., Dheda, K., Bustin, S. & Zumla, A. (2005). Real-time PCR normalisation; strategies and considerations. Gene Immun. 6, 279–84.CrossRefGoogle ScholarPubMed
Hulshof, S.C., Figueiredo, J.R., Beckers, J.F., Bevers, M.M., Van der Donk, J.A. & Van den Hurk, R. (1995). Effects of fetal bovine serum, FSH and 17beta-estradiol on the culture of bovine preantral follicles. Theriogenology 44, 217–26.CrossRefGoogle ScholarPubMed
Hutt, K.J., Mclaughlin, E.A. & Holland, M.K. (2006). KIT/KIT ligand in mammalian oogenesis and folliculogenesis: roles in rabbit and murine ovarian follicle activation and oocyte growth. Biol. Reprod. 75, 421–33.CrossRefGoogle ScholarPubMed
Joyce, I.M., Pendola, F.L., Wigglesworth, K. & Eppig, J.J. (1999). Oocyte regulation of Kit ligand expression in mouse ovarian follicles. Dev. Biol. l214, 342–53.CrossRefGoogle Scholar
Joyce, I.M., Clark, A.T., Pendola, F.L. & Eppig, J.J. (2000). Comparison of recombinant growth differentiation factor-9 and oocyte regulation of Kit ligand messenger ribonucleic acid expression in mouse ovarian follicles. Biol. Reprod. 63, 11669–75.CrossRefGoogle ScholarPubMed
Juengel, J.L. & McNatty, K.P. (2005). The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Human Hum. Reprod. Update. 11, 143–60.Google ScholarPubMed
Juengel, J.L., Heath, D.A., Quirke, L.D. & McNatty, K.P. (2006). Oestrogen receptor α and ß, androgen receptor and progesterone receptor mRNA and protein localisation within the developing ovary and in small growing follicles of sheep. Reprod. Fertil. 131, 81–92.CrossRefGoogle Scholar
Kamat, B.R., Brown, L.F., Manseau, E.J., Senger, D.R. & Dvorak, H.F. (1995). Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Role in corpus luteum development Am. J. Pathol. 146, 157–65.Google ScholarPubMed
Kezele, P.R., Ague, J.M., Nilsson, E. & Skinner, M.K. (2005). Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol. Reprod. 72, 241–55.CrossRefGoogle ScholarPubMed
Kikuchi, N., Andoh, K., Abe, Y., Yamada, K., Mizunuma, H. & Ibuki, Y. (2001). Inhibitory action of leptin on early follicular growth differs in immature and adult female mice. Biol. Reprod. 65, 66–71.CrossRefGoogle ScholarPubMed
Knight, P.G. & Glister, C. (2006). TGF-beta superfamily members and ovarian follicle development. Reproduction 132, 191–206.CrossRefGoogle ScholarPubMed
Kobayashi, J., Mizunuma, H., Kikuchi, N., Liu, X., Andoh, K., Abe, Y., Yokota, H., Yamada, K., Ibuki, Y. & Hagiwara, H. (2000). Morphological assessment of the effect of growth hormone on preantral follicles from 11-day-old mice in an in vitro culture system. Biochem. Biophys. Res. Commun. 268, 36–41.CrossRefGoogle Scholar
Kolle, S., Sinowatz, F., Boie, G., & Lincoln, D. (1998). Developmental changes in the expression of the growth hormone receptor messenger ribonucleic acid and protein in the bovine ovary. Biol. Reprod. 59, 836–42.CrossRefGoogle ScholarPubMed
Koos, R.D. (1995). Increased expression of vascular endothelial growth/permeability factor in the rat ovary following an ovulatory gonadotropin stimulus, potential roles in follicle rupture. Biol. Reprod. 52, 1426–35.CrossRefGoogle ScholarPubMed
Kouadjo, K.E., Nishida, Y., Cadrm-Girard, J.F., Yoshioka, M. & St Amand, J. (2007). Housekeeping and tissue-specific genes in mouse tissue. BMC Genomics 8, 67.CrossRefGoogle Scholar
Kuyk, E.W., du Puy, L., van Tol, H.T., Haagsman, H.P., Colenbrander, B. & Roelen, B.A. (2007). Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev. Biol. 7, 58.Google Scholar
Langhout, D.J., Spicer, L.J. & Geisert, R.D. (1991). Development of a culture system for bovine granulose cells, p. effects of growth hormone, estradiol, and gonadotropins on cell proliferation, steroidogenesis, and protein synthesis. J. Anim. Sci. 69, 3321–34.CrossRefGoogle Scholar
Lin, C., Spikings, E.Zhang, T. & Rawson, D. (2009). Housekeeping genes for cryopreservation studies on zebrafish embryos and blastomeres. Theriogenology 71, 1147–1155.CrossRefGoogle ScholarPubMed
Liu, X., Andoh, K., Yokota, H., Kobayashi, J., Abe, Y., Yamada, K., Mizunuma, H. & Ibuki, Y. (1998). Effects of growth hormone, activin, and follistatin on the development of preantral follicle from immature female mice. Endocrinology 139, 2342–7.CrossRefGoogle ScholarPubMed
Luciano, A.M., Pappalardo, A., Ray, C. & Peluso, J.J. (1994). Epidermal growth factor inhibits large granulosa cell apoptosis by stimulating progesterone synthesis and regulating the distribution of intracellular free calcium. Biol. Reprod. 51, 646–54.CrossRefGoogle ScholarPubMed
Mamo, S., Gal, A.B., Bodo, S. & Dmnyes, A. (2007) Quantitative evaluation and selection of reference genes in mouse oocyte and embryos cultured in vivo and in vitro. BMC. Dev. Biol. 7, 14.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 EGF and IGF-1 on porcine preantral follicular growth, antrum formation, and stimulation of granulosa cell proliferation and suppression of apoptosis in vitro. J Anim Sci. 82, 1967–75.CrossRefGoogle ScholarPubMed
Markström, E., Svensson, E.C., 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., 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. & Figueiredo, J.R. (2006). Effects of fibroblast growth factor-2 on the in vitro culture of caprine preantral follicles. In Resumos da XX Reunião Anual da SBTE (Araxá, Brasil). p. 265.Google Scholar
Monget, P., Monniaux, D. & Durand, P. (1989). Localization, characterization and quantification of insulin-like growth factor-I-binding sites in the ewe ovary. Endocrinology 125, 2486–93.CrossRefGoogle ScholarPubMed
Monniaux, D. & Reviers, M. M. (1989).Quantitative autoradiographic study of FSH binding sites in prepubertal ovaries of three strains of rats. J. Reprod. Fertil. 85, 151–62.CrossRefGoogle ScholarPubMed
Morbeck, D.E., Flowers, W.L. & Britt, J.H. (1993). Response of porcine granulosa cells isolated from primary and secondary follicles to FSH, 8-bromo-cAMP and epidermal growth factor in vitro. J. Reprod. Fertil. 99, 577–84.CrossRefGoogle ScholarPubMed
Newton, H., Picton, H., & Gosden, R.G. (1999). In vitro growth of oocyte–granulosa cell complexes isolated from cryopreserved ovine tissue. J. Reprod. Fertil. 115, 141–50.CrossRefGoogle ScholarPubMed
Nilsson, E., Parrot, J.A. & Skinner, M.K. (2001). Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol. Cell. Endocrinol. 175, 123–30.CrossRefGoogle ScholarPubMed
Nygard, A.B., Jorgensen, C.B., Cirera, S. & Fredholm, M. (2007). Selection of reference genes for gene expression studies in pig tissue using SYBR green qPCR. BMC Mol. Biol. 8, 67.CrossRefGoogle ScholarPubMed
Oliver, J.E., Aitman, T.J., Powell, J.F., Wilson, C.A. & Clayton, R.N. (1989). Insulin-like growth factor I gene expression in the rat ovary is confined to the granulosa cells of developing follicles. Endocrinology 124, 2671–79.CrossRefGoogle Scholar
Ortega, H.H., Salvetti, N.R., Amable, P., Dallard, B.E., Baravalle, C., Barbeito, C.G. & Gimeno, E.J. (2007). Intraovarian localization of growth factors in induced cystic ovaries in rats. Anat. Histol. Embryol. 36, 94–102.CrossRefGoogle ScholarPubMed
Otsuka, F. & Shimasaki, S. (2002). A negative feedback system between oocyte bone morphogenetic protein15 and granulose cell Kit ligand: its role in regulating granulose cell mitosis. Proc. Natl. Acad. Sci. USA 99, 8060–65.CrossRefGoogle Scholar
Otsuka, F., Yamamoto, S., Erickson, G.F. & Shimasaki, S. (2001). Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression. J. Biol. Chem. 276, 11387–92.CrossRefGoogle ScholarPubMed
Parrot, J.A. & Skinner, M.K. (1999). Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140, 262–71.Google Scholar
Qu, J., Godin, P. A., Nisolle, M. & Donnez, J. (2000). Distribution and epidermal growth factor receptor expression of primordial follicles in human ovarian tissue before and after cryopreservation. Hum. Reprod. 15, 302–10.CrossRefGoogle ScholarPubMed
Quennell, J.H., Stanton, J.A. & Hurst, P.R. (2004). Basic fibroblast growth factor expression in isolated small human ovarian follicles. Mol. Hum. Reprod. 10, 623–28.CrossRefGoogle ScholarPubMed
Quintana, R., Kopcow, L., Sueldo, C., Marconi, G., Rueda, N.G. & Barañao, R.I. (2004). Direct injection of vascular endothelial growth factor into the ovary of mice promotes follicular development. Fertil. Steril. 82 Suppl. 3, 1101–15.CrossRefGoogle ScholarPubMed
Radonic, A., Thulke, S., Mackay, I.M., Landt, O., Siegert, W. & Nitsche, A. (2004). Guideline to reference gene selection for quantitative real-time PCR. Biochem. Biophys. Res. Commun. 313, 856–62.CrossRefGoogle ScholarPubMed
Redmer, D. & Reynolds, L. (1996). Angiogenesis in the ovary. Biol. Reprod. 1, 182–92.Google ScholarPubMed
Reeka, N., Berg, F.D. & Brucker, C. (1998). Presence of transforming growth factor alpha and epidermal growth factor in human ovarian tissue and follicular fluid. Hum. Reprod. 13, 2199–205.CrossRefGoogle ScholarPubMed
Reynolds, L.P. & Redmer, D.A. (1998). Expression of the angiogenic factors, basic fibroblast growth factor and vascular endothelial growth factor, in the ovary. J. Anim. Sci. 76, 1671–81.CrossRefGoogle ScholarPubMed
Roberts, R.D. & Ellis, R.C.L. (1999). Mitogenic effects of fibroblast growth factors on chicken granulosa and theca cells in vitro. Biol. Reprod. 61, 1387–92.CrossRefGoogle ScholarPubMed
Roy, S.K. & Treacy, B.J. (1993). Isolation and long-term culture of human preantral follicles. Fertil. Steril. 59, 783–90.CrossRefGoogle ScholarPubMed
Schmid, H., Cohen, C.D., Henger, A., Irrgang, S., Schlondorff, D. & Kretzler, M. (2003). Validation of endogenous controls for gene expression analysis in microdissected human renal biopsies. Kidney Int. 64, 356–60.CrossRefGoogle ScholarPubMed
Schmittgen, T.D. & Zakrajsek, B.A. (2000), Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J. Biochem. Biophys. Methods 46, 69–81.CrossRefGoogle ScholarPubMed
Shimasaki, S., Moore, R.K., Erickson, G.F. & Otsuka, F. (2003). The role of bone morphogenetic proteins in ovarian function. Reproduction 61, 323–37.Google ScholarPubMed
Shimasaki, S., Kelly Moore, R., Otsuka, F., & Erickson, G.F. (2004). The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25: 72–101.CrossRefGoogle ScholarPubMed
Silva, J.R.V., Ferreira, M. A. L., Costa, S. H. F., Santos, R. R., Carvalho, F. C. A., Rodrigues, A. P. R., Lucci, C. M., Báo, S. N. & Figueiredo, J. R. (2002). Degeneration rate of preantral follicles in the ovaries of goats. Small Rum. Res. 43, 203–9.CrossRefGoogle Scholar
Silva, J.R.V., van den Hurk, R., Matos, M.H.T., Santos, R.R., Pessoa, C., Moraes, M.O. & Figueiredo, J.R. (2004a). Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology 61, 1691–704.CrossRefGoogle ScholarPubMed
Silva, J.R.V., van den Hurk, R., Van Tol, H.T.A., Roelen, B.A.J. & Figueiredo, J.R. (2004b). 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.CrossRefGoogle Scholar
Silva, J.R.V., van den Hurk, R. & Figueiredo, J. R. (2006a) Expression of mRNA and protein localisation for epidermal growth factor and its receptor in goat ovaries. Zygote 14, 107–117.CrossRefGoogle ScholarPubMed
Silva, J.R.V., van den Hurk, R., Van Tol, H.T., Roelen, B.A. & Figueiredo, J.R. (2006b). The Kit ligand/c-Kit receptor system in goat ovaries: gene expression and protein localization. Zygote 14, 317–28.CrossRefGoogle ScholarPubMed
Silva, J.R.V., Brito, I.R., Leitão, C.C.F., Silva, A.W.B., Passos, M.J., Fernandes, L.A., Vasconcelos, G.L. & Figueiredo, J.R. (2007). Expression of bone morphogenetic protein-6 (BMP-6) in goat ovarian follicles. In Resumos da XXI Reunião Anual da SBTE (Costa do Sauípe, BA, Brasil). p. 1044.Google Scholar
Silva, J.R., Figueiredo, J.R. & van den Hurk, R. (2009). Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 8, 1193–208.CrossRefGoogle Scholar
Spears, N., Murray, A.A., Allison, V., Boland, N.I. & Gosden, R.G. (1998). Role of gonadotrophins and ovarian steroids in the development of mouse follicles in vitro. J. Reprod Fertil. 113, 19–26.CrossRefGoogle ScholarPubMed
Spicer, L.J., Aad, P.Y., Allen, D., Mazerbourg, S. & Hsueh, A.J. 2006. Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells. J. Endocrinol. 189, 329–39.CrossRefGoogle ScholarPubMed
Spicer, L.J., Aad, P.Y., Allen, D.T., Mazerbourg, S., Payne, A.H. & Hsueh, A.J. (2008). Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9. Biol. Reprod. 78, 243–53.CrossRefGoogle ScholarPubMed
Tajima, K., Yoshii, K., Fukuda, S., Orisaka, M., Miyamoto, K., Amsterdam, A. & Kotsuji, F. (2005). Luteinizing hormone-induced extracellular-signal regulated kinase activation differently modulates progesterone and androstenedione production in bovine theca cells. Endocrinology. 146, 2903–10.CrossRefGoogle ScholarPubMed
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, 941–49.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. Hum. Reprod. 4, 833–41.Google 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
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N. & De Paepe, A. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, 34.CrossRefGoogle ScholarPubMed
Van Tol, H.T.A., van Eerdenburg, F.J.C.M., Colenbrander, B. & Roelen, B.A.J. (2007). Enhancement of bovine oocyte maturation by leptin is accompanied by an upregulation in mRNA expression of leptin receptor isoforms in cumulus cells. Mol. Reprod. Dev. 75, 578–87.CrossRefGoogle Scholar
Van Wezel, I.L., Umapathysivam, K., Tilley, W.D. & Rodgers, R.J. (1995). Immunohistochemical localization of basic fibroblast growth factor in bovine ovarian follicles. Mol. Cell. Endocrinol. 115, 133–40.CrossRefGoogle ScholarPubMed
Wandji, S., Fortier, M.A. & Sirard, M. (1992). Differential response to gonadotrophins and prostaglandin E2 in ovarian tissue during prenatal and postnatal development in cattle. Biol. Reprod. 46, 1034–41.CrossRefGoogle ScholarPubMed
Wandji, S.A., Eppig, J.J. & 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, 817–32.CrossRefGoogle ScholarPubMed
Wang, J. & 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, 577–85.CrossRefGoogle ScholarPubMed
Wright, C., Hovatta, O., Margara, R., Trowe, G., Winston, R.M.L., Franks, S. & Hardy, K. (1999). Effect of follicle stimulating hormone and serum substitution on the development and growth of early human follicles. Hum. Reprod. 14, 1555–62.CrossRefGoogle 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, 320–27.CrossRefGoogle Scholar
Yamamoto, S., Konishi, I., Tsuruta, Y., Nanbu, K., Kuroda, H., Matsushita, K., Hamid, A., Yura, Y. & Mori, I. (1997). Expression of vascular endothelial growth factor (VEGF) during folliculogenesis and corpus luteum formation in the human ovary. Gynec. Endocrinol. 11, 371–81.CrossRefGoogle ScholarPubMed
Zhou, H. & Zhang, Y. (2005a). Regulation of in vitro growth of preantral follicles by growth factors in goats. Dom. Anim. Endocrinol. 28, 235–42.CrossRefGoogle ScholarPubMed
Zhou, H. & Zhang, Y. (2005b). Effect of growth factors on in vitro development of caprine preantral follicle oocytes. Anim. Reprod. Sci. 90, 265–72.CrossRefGoogle ScholarPubMed
Zhao, J., Dorland, M., Taverne, M.A., 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. Dev. 55, 65–74.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Zhao, J., Taverne, M.A.M., Van Der Weijden, B.C., Bevers, M.M. & Van den Hurk, R. (2001). Effect of activin A on in vitro development of rat preantral follicles and localization of activin A and activin receptor II. Biol. Reprod. 65, 967–77.CrossRefGoogle ScholarPubMed
Zhao, J., Taverne, M.A., van der Weijden, G.C., Bevers, M.M. & van den Hurk, R. (2002). Immunohistochemical localisation of growth hormone (GH), GH receptor (GHR), insulin-like growth factor I (IGF-I) and type I IGF-I receptor, and gene expression of GH and GHR in rat pre-antral follicles. Zygote 10, 85–94.CrossRefGoogle ScholarPubMed