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Expression levels of mRNA for insulin-like growth factors 1 and 2, IGF receptors and IGF binding proteins in in vivo and in vitro grown bovine follicles

Published online by Cambridge University Press:  09 May 2013

Emanuela L. Rebouças ,
José J.N. Costa ,
Maria J. Passos ,
Anderson W.B. Silva ,
Rodrigo O.D.S. Rossi ,
Robert van den Hurk  and
José R.V. Silva
Emanuela L. Rebouças
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil
José J.N. Costa
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil
Maria J. Passos
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil
Anderson W.B. Silva
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil
Rodrigo O.D.S. Rossi
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, 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, Rua Comandante Maurocélio Rocha Pontes 100, CEP 62042–280, Sobral, CE, Brazil.
*
All correspondence to: José R.V. Silva. Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, Rua Comandante Maurocélio Rocha Pontes 100, CEP 62042–280, Sobral, CE, Brazil. Tel:/Fax: +55 88 36132603. e-mail: [email protected]
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Summary

This study investigated mRNA levels for insulin-like growth factors (IGFs) IGF1 (IGF-I) and IGF2 (IGF-II), IGF receptors (IGF1R and IGF2R), and binding proteins (IGFBP-1, IGFBP-2. IGFBP-3, IGFBP-4, IGFBP-5 and IGFBP-6) in bovine follicles of 0.2, 0.5 or 1.0 mm in diameter. mRNA expression levels in in vitro cultured follicles that reached approximately 0.5 mm were compared with that of in vivo grown follicles. IGF1R and IGF2R expression levels in 0.5 mm in vivo follicles were higher than in 1.0 or 0.2 mm follicles, respectively. IGFBP-1, IGFBP-2. IGFBP-3, IGFBP-4, IGFBP-5 and IGFBP-6 showed variable expression in the follicular size classes analyzed. In vitro grown follicles had significantly reduced expression levels for IGF1, IGF1R, IGFBP-3, IGFBP-5 and IGFBP-6 mRNA when compared with 0.2 mm follicles, but, when compared with in vivo grown follicles (0.5 mm), only IGFBP-1, IGFBP-2, IGFBP-3 and IGFBP-6 showed a reduction in their expression. In conclusion, IGFs, their receptors and IGFBPs showed variable expression of mRNA levels in the follicular size classes analyzed.

Keywords

BovineHousekeeping genesIGFmRNAOvarian follicles
Type
Research Article
Information
Zygote , Volume 22 , Issue 4 , November 2014 , pp. 521 - 532
Copyright
Copyright © Cambridge University Press 2013 

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References

Armstrong, D.G., Baxter, G., Gutierrez, C.G., Hogg, C.O., Glazyrin, A.L., Campbell, B.K., Bramley, T.A. & Webb, R. (1998). Insulin-like growth factor binding protein -2 and -4 messenger ribonucleic acid expression in bovine ovarian follicles: effect of gonadotropins and developmental status. Endocrinology 139, 2146–54.Google Scholar
Armstrong, D.G., Baxter, G., Hogg, C.O. & Woad, K.J. (2002). Insulin-like growth factor (IGF) system in the oocyte and somatic cells of bovine preantral follicles. Reproduction 123, 789–97.Google Scholar
Arraztoa, J.A., Monget, P., Bondy, C. & Zhou, J. (2002). Expression patterns of insulin-like growth factor-binding proteins 1, 2, 3, 5, and 6 in the mid-cycle monkey ovary. J. Clin. Endocrinol. Metab. 87, 5220–8.Google Scholar
Arunakumari, G., Shanmugasundaram, N. & Rao, V.H. (2010). Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884–94.Google Scholar
Baxter, R.C. (2000). Insulin-like growth factor (IGF)-binding proteins: interactions with IGFs and intrinsic bioactivities. Am. J. Physiol. Endocrinol. Metab. 278, 967–76.Google Scholar
Beg, M.A. & Ginther, O.J. (2006). Follicle selection in cattle and horse: role of intrafollicular factors. Soc. Reprod. Fertil. 132, 365–77.Google Scholar
Besnard, N., Pisselet, C., Monniaux, D., Locatelli, A., Benne, F., Gasser, F., Hatey, F. & Monget, P. (1996). Expression of messenger ribonucleic acids of insulin-like growth factor binding protein -2, -4, and -5 in the ovine ovary: localization and changes during growth and atresia of antral follicles. Biol. Reprod. 55, 1356–67.Google Scholar
Besnard, N., Pisselet, C., Monniaux, D. & Monget, P. (1997). Proteolytic activity degrading insulin-like growth factor-binding protein -2, -3, -4, and -5 in healthy growing and atretic follicles in the pig ovary. Biol. Reprod. 56, 1050–8.Google Scholar
Bonnet, A., Dalbiès-Tran, R. & Sirard, M.A. (2008). Opportunities and challenges in applying genomics to the study of oogenesis and folliculogenesis in farm animals. Reproduction 135, 119–28.CrossRefGoogle Scholar
Cecconi, S., Barboni, B., Coccia, M. & Mattiol, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594–601.Google Scholar
Chen, A.Q., Yu, S.D., Wang, Z.G., Xu, Z.R. & Yang, Z.G. (2009). Stage-specific expression of bone morphogenetic protein type I and type II receptor genes: effects of follicle-stimulating hormone on ovine antral follicles. Anim. Reprod. Sci. 111, 391–9.Google Scholar
Giudice, L.C. (1992). Insulin-like growth factors and ovarian follicular development. Endocr. Rev. 13, 641–69.Google Scholar
Grimes, R.W., Guthrie, H.D. & Hammond, J.M. (1994). Insulin-like growth factor binding protein-2 and -3 are correlated with atresia and preovulatory maturation in the porcine ovary. Endocrinology 135, 1996–2000.Google 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.Google Scholar
Hastie, P.M. & Haresign, W. (2006). Expression of mRNAs encoding insulin-like growth factor (IGF) ligands, IGF receptors and IGF binding proteins during follicular growth and atresia in the ovine ovary throughout the oestrous cycle. Anim. Reprod. Sci. 92, 284–99.Google Scholar
Kawashima, I., Okazaki, T., Noma, N., Nishibori, M., Yamashita, Y. & Shimada, M. (2008). Sequential exposure of porcine cumulus cells to FSH and/or LH is critical for appropriate expression of steroidogenic and ovulation-related genes that impact oocyte maturation in vivo and in vitro. Reproduction 136, 9–21.Google Scholar
Le Roith, D., Bondy, C., Yakar, S., Jun-Li, L. & Butler, A. (2001). The somatomedin hypothesis. Endocr. Rev. 22, 53–74.Google Scholar
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT. Method 25, 402–8.Google Scholar
Llewellyn, S., Fitzpatrick, R., Kenny, D.A., Murphy, J.J., Scaramuzzi, R.J. & Wathes, D.C. (2007). Effect of negative energy balance on the insulin-like growth factor system in pre-recruitment ovarian follicles of post partum dairy cows. Reproduction 133, 627–39.Google Scholar
Magalhães, D.M., Duarte, A.B., Araújo, V.R., Brito, I.R., Soares, T.G., Lima, I.M., Lopes, C.A., Campello, C.C., Rodrigues, A.P.R. & Figueiredo, J.R. (2010). In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology 75, 182–8.Google Scholar
McLaughlin, M., Bromfield, J.J., Albertini, D.F. & Telfer, E.E. (2010). Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Mol. Hum. Reprod. 16, 644–53.Google Scholar
Monget, P., Monniaux, D., Pisselet, C. & Durand, P. (1993). Changes in insulin-like growth factor-I (IGFI), IGFII, and their binding proteins during growth and atresia of ovine ovarian follicles. Endocrinology 132, 1438–46.Google Scholar
Monget, P., Fabre, S., Mulsant, P., Lecerf, F., Elsen, J.M., Mazerbourg, S., Pisselet, C. & Monniaux, D. (2002). Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals. Domest. Anim. Endocrinol. 23, 139–54.Google Scholar
Muñoz-Gutiérrez, M., Findlay, P.A., Adam, C.L., Wax, G., Campbell, B.K., Kendall, N.R., Khalid, M., Forsberg, M. & Scaramuzzi, R.J. (2005). The ovarian expression of mRNAs for aromatase, IGFI receptor, IGF-binding protein -2, -4 and -5, leptin and leptin receptor in cycling ewes after three days of leptin infusion. Reproduction 130, 869–81.Google Scholar
Parrott, J.A. & Skinner, M.K. (2000). Kit ligand on ovarian stromal cells: effects on theca cell recruitment and steroid production. Mol. Reprod. Dev. 55, 55–64.Google Scholar
Perks, C.M., Peters, A.R. & Wathes, D.C. (1999). Follicular and luteal expression of insulin-like growth factors I and II and the type 1 IGF receptor in the bovine ovary. J. Reprod. Fertil. 116, 157–65.Google Scholar
Saraiva, M.V.A., Rossetto, R., Brito, I.R., Celestino, J.J.H., Silva, C.M.G., Faustino, L.R., Almeida, A.P., Bruno, J.B., Magalhães, D.M., Matos, M.H.T., Campello, C.C. & Figueiredo, J.R. (2010). Dynamic medium produces caprine embryo from preantral follicles grown in vitro. Reprod. Sci. 17, 1135–43.Google Scholar
Schams, D., Berisha, B., Kosmann, M., Einspanier, R. & Amselgruber, W.M. (1999). Possible role of growth hormone, IGFs, and IGF-binding proteins in the regulation of ovarian function in large farm animals. Domest. Anim. Endocrinol. 17, 279–85.Google Scholar
Schams, D., Berisha, B., Kosmann, M. & Amselgruber, W.M. (2002). Expression and localization of IGF family members in bovine antral follicles during final growth and in luteal tissue during different stages of estrous cycle and pregnancy. Domest. Anim. Endocrinol. 22, 51–72.Google Scholar
Silva, J.R.V., Figueiredo, J.R. & Van den Hurk, R. (2009). Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 71, 1193–208.Google Scholar
Spicer, L.J. & Echternkamp, S.E. (1995). The ovarian insulin and insulin-like growth factor system with an emphasis on domestic animals. Domest. Anim. Endocrinol. 12, 223–45.Google Scholar
Spicer, L.J., Voge, J.L. & Allen, D.T. (2004). Insulin-like growth factor-II stimulates steroidogenesis in cultured bovine thecal cells. Mol. Cell. Endocrinol. 227, 1–7.Google Scholar
Stewart, R.E., Spicer, L.J., Hamilton, T.D., Keefer, B.E., Dawson, L.J., Morgan, G.L. & Echternkamp, S.E. (1996). Levels of insulin-like growth factor (IGF) binding proteins, luteinizing hormone and IGFI receptors, and steroids in dominant follicles during the first follicular wave in cattle exhibiting regular estrous cycles. Endocrinology 137, 2842–50.Google Scholar
Van den Hurk, R. & Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicle. Theriogenology 63, 1717–57.Google Scholar
Vandesonpele, J., De Preter, K., Pattyn, F., Poppe, B., Van Rou, N., De Paepe, A. & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Gen. Biol. 3, 34.1–11.Google Scholar
Vendola, K., Zhou, J., Wang, J., Famuyiwa, O.A., Bievre, M. & Bondy, C.A. (1999). Androgens promote oocyte insulin-like growth factor I expression and initiation of follicle development in the primate ovary. Biol. Reprod. 61, 353–7.Google Scholar
Vergani, G., Bartke, A. & Mayerhofer, A. (1997). Visualizing the expression of a human growth hormone (hGH) transgene in the liver: intrahepatic regional and intracellular differences of expression are associated with morphological alterations and hepatocellular proliferation. Tissue Cell 29, 611–6.Google Scholar
Wandji, S.A., Gadsby, J.E., Simmen, F.A., Barber, J.A. & Hammond, J.M. (2000). Porcine ovarian cells express messenger ribonucleic acids for the acid-labile subunit and insulin-like growth factor binding protein-3 during follicular and luteal phases of the estrous cycle. Endocrinology 141, 2638–47.Google Scholar