Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-27T14:19:31.622Z Has data issue: false hasContentIssue false
  • English
  • Français

Growth factor receptor-bound protein 14: a potential new gene associated with oocyte competence

Published online by Cambridge University Press:  17 May 2013

Paulo Roberto Antunes Rosa ,
Rodrigo Camponogara Bohrer ,
Matheus Pedrotti De Cesaro ,
Karina Gutierrez ,
Rogério Ferreira ,
Gabriel Ribas Pereira ,
João Francisco Coelho Oliveira  and
Paulo Bayard Dias Gonçalves
Paulo Roberto Antunes Rosa
Affiliation:
Laboratory of Biotechnology and Animal Reproduction - BioRep, Federal University of Santa Maria, Santa Maria, RS 97105–900, Brazil.
Rodrigo Camponogara Bohrer
Affiliation:
Laboratory of Biotechnology and Animal Reproduction - BioRep, Federal University of Santa Maria, Santa Maria, RS 97105–900, Brazil.
Matheus Pedrotti De Cesaro
Affiliation:
Laboratory of Biotechnology and Animal Reproduction - BioRep, Federal University of Santa Maria, Santa Maria, RS 97105–900, Brazil.
Karina Gutierrez
Affiliation:
Laboratory of Biotechnology and Animal Reproduction - BioRep, Federal University of Santa Maria, Santa Maria, RS 97105–900, Brazil.
Rogério Ferreira
Affiliation:
Department of Animal Science, Santa Catarina State University, Chapecó, SC, 89802–200, Brazil.
Gabriel Ribas Pereira
Affiliation:
Laboratory of Biotechnology and Animal Reproduction - BioRep, Federal University of Santa Maria, Santa Maria, RS 97105–900, Brazil.
João Francisco Coelho Oliveira
Affiliation:
Laboratory of Biotechnology and Animal Reproduction - BioRep, Federal University of Santa Maria, Santa Maria, RS 97105–900, Brazil.
Paulo Bayard Dias Gonçalves*
Affiliation:
Laboratory of Biotechnology and Animal Reproduction- BioRep, Federal University of Santa Maria, Av. Roraima #1000, CEP 97105–900, Santa Maria, RS 97105–900, Brazil. Laboratory of Biotechnology and Animal Reproduction - BioRep, Federal University of Santa Maria, Santa Maria, RS 97105–900, Brazil.
*
All correspondence to: Paulo Bayard Dias Gonçalves. Laboratory of Biotechnology and Animal Reproduction- BioRep, Federal University of Santa Maria, Av. Roraima #1000, CEP 97105–900, Santa Maria, RS 97105–900, Brazil. Tel: +55 55 3220 8752. Fax: +55 55 3220 8484. E-mail: bayard@ufsm.br
Get access Rights & Permissions [Opens in a new window]

Summary

The Grb14 protein is a member of the Grb7 protein family. This protein family acts by binding to tyrosine kinase receptors, promoting cell proliferation and differentiation. There is evidence of the involvement of tyrosine kinase factors in the bovine oocyte maturation process. However, Grb14 has not been studied for bovine cumulus–oocyte complexes (COCs). The aim of the present study was to characterize Grb14 mRNA expression in bovine COCs during follicular development. Furthermore, we demonstrated that the expression of Grb14 mRNA is not regulated by estradiol. mRNA expression of Grb14 was assessed in 480 COCs from follicles of different sizes (1–3, 4–6, 6–8 or >8 mm) by quantitative reverse transcription polymerase chain reaction (qRT-PCR). Grb14 mRNA expression decreased in COCs throughout follicular growth (P < 0.05). The role of estradiol in the expression of Grb14 mRNA in COCs was studied. Grb14 mRNA abundance did not differ in COCs cultured in the presence or absence of 17β-estradiol or fulvestrant. In conclusion, we showed that Grb14 mRNA is downregulated in COCs during antral follicle development, a finding that suggests a role for Grb14 in oocyte competence.

Keywords

CattleFollicle developmentGrb14OocyteOocyte maturation
Type
Research Article
Information
Zygote , Volume 22 , Issue 2 , May 2014 , pp. 103 - 109
Copyright
Copyright © Cambridge University Press 2013 

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

Ali, A. & Sirard, M.A. (2002). The effects of 17beta-estradiol and protein supplement on the response to purified and recombinant follicle stimulating hormone in bovine oocytes. Zygote 10, 65–71.Google Scholar
Arlotto, T., Schwartz, J.L., First, N.L. & Leibfried-Rutledge, M.L. (1996). Aspects of follicle and oocyte stage that affect in vitro maturation and development of bovine oocytes. Theriogenology 45, 943–56.Google Scholar
Assey, R.J., Hyttel, P., Greve, T. & Purwantara, B. (1994). Oocyte morphology in dominant and subordinate follicles. Mol. Reprod. Dev. 37, 335–44.Google Scholar
Barreta, M.H., Oliveira, J.F., Ferreira, R., Antoniazzi, A.Q., Gasperin, B.G., Sandri, L.R. & Goncalves, P.B. (2008). Evidence that the effect of angiotensin II on bovine oocyte nuclear maturation is mediated by prostaglandins E2 and F2alpha. Reproduction 136, 733–40.Google Scholar
Browaeys-Poly, E., Blanquart, C., Perdereau, D., Antoine, A.F., Goenaga, D., Luzy, J.P., Chen, H., Garbay, C., Issad, T., Cailliau, K. & Burnol, A.F. (2010). Grb14 inhibits FGF receptor signaling through the regulation of PLCgamma recruitment and activation. FEBS Lett. 584, 4383–8.Google Scholar
Cailliau, K., Le Marcis, V., Béréziat, V., Perdereau, D., Cariou, B., Vilain, J.P., Burnol, A.-F. & Browaeys-Poly, E. (2003). Inhibition of FGF receptor signalling in Xenopus oocytes: differential effect of Grb7, Grb10 and Grb14. FEBS Lett. 548, 43–8.Google Scholar
Campbell, B.K. & McNeilly, A.S. (1996). Follicular dominance and oocyte maturation. Zygote 4, 327–34.Google Scholar
Charalambous, M., Smith, F.M., Bennett, W.R., Crew, T.E., Mackenzie, F. & Ward, A. (2003). Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc. Natl. Acad. Sci. USA 100, 8292–7.Google Scholar
Fair, T., Hyttel, P. & Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437–42.Google Scholar
Fissore, R.A., He, C.L. & Vande Woude, G.F. (1996). Potential role of mitogen-activated protein kinase during meiosis resumption in bovine oocytes. Biol. Reprod. 55, 1261–70.Google Scholar
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. 82–3, 109–126.Google Scholar
Giometti, I.C., Bertagnolli, A.C., Ornes, R.C., da Costa, L.F., Carambula, S.F., Reis, A.M., de Oliveira, J.F., Emanuelli, I.P. & Goncalves, P.B. (2005). Angiotensin II reverses the inhibitory action produced by theca cells on bovine oocyte nuclear maturation. Theriogenology 63, 1014–25.Google Scholar
Goenaga, D., Hampe, C., Carre, N., Cailliau, K., Browaeys-Poly, E., Perdereau, D., Holt, L.J., Daly, R.J., Girard, J., Broutin, I., Issad, T. & Burnol, A.F. (2009). Molecular determinants of Grb14-mediated inhibition of insulin signaling. Mol. Endocrinol. 23, 1043–51.Google Scholar
Han, D.C., Shen, T.L. & Guan, J.L. (2001). The Grb7 family proteins: structure, interactions with other signaling molecules and potential cellular functions. Oncogene 20, 6315–21.Google Scholar
Holt, L.J. & Siddle, K. (2005). Grb10 and Grb14: enigmatic regulators of insulin action—and more? Biochem. J. 388, 393–406.Google Scholar
Holt, L.J., Lyons, R.J., Ryan, A.S., Beale, S.M., Ward, A., Cooney, G.J. & Daly, R.J. (2009). Dual ablation of Grb10 and Grb14 in mice reveals their combined role in regulation of insulin signaling and glucose homeostasis. Mol. Endocrinol. 23, 1406–14.Google Scholar
Kairouz, R., Parmar, J., Lyons, R.J., Swarbrick, A., Musgrove, E.A. & Daly, R.J. (2005). Hormonal regulation of the Grb14 signal modulator and its role in cell cycle progression of MCF-7 human breast cancer cells. J. Cell. Physiol. 203, 85–93.Google Scholar
Leibfried, L. & First, N.L. (1979). Characterization of bovine follicular oocytes and their ability to mature in vitro. J. Anim. Sci. 48, 76–86.Google Scholar
Lequarre, A.S., Vigneron, C., Ribaucour, F., Holm, P., Donnay, I., Dalbies-Tran, R., Callesen, H. & Mermillod, P. (2005). Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. Theriogenology 63, 841–59.CrossRefGoogle ScholarPubMed
Li, X., Dai, Y. & Allen, W.R. (2004). Influence of insulin-like growth factor-I on cytoplasmic maturation of horse oocytes in vitro and organization of the first cell cycle following nuclear transfer and parthenogenesis. Biol. Reprod. 71, 1391–6.Google Scholar
Lim, M.A., Riedel, H. & Liu, F. (2004). Grb10: more than a simple adaptor protein. Front. Biosci. 9, 387–403.Google Scholar
Lonergan, P., Monaghan, P., Rizos, D., Boland, M.P. & Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol. Reprod. Dev. 37, 48–53.CrossRefGoogle ScholarPubMed
Lucas-Fernandez, E., Garcia-Palmero, I. & Villalobo, A. (2008). Genomic organization and control of the grb7 gene family. Curr. Genomics 9, 60–8.Google Scholar
Luo, W. & Wiltbank, M.C. (2006). Distinct regulation by steroids of messenger RNAs for FSHR and CYP19A1 in bovine granulosa cells. Biol. Reprod. 75, 217–25.Google Scholar
McCann, J.A., Zheng, H., Islam, A., Goodyer, C.G. & Polychronakos, C. (2001). Evidence against GRB10 as the gene responsible for Silver-Russell syndrome. Biochem. Biophys. Res. Comm. 286, 943–8.Google Scholar
Meidan, R., Wolfenson, D., Thatcher, W.W., Gilad, E., Aflalo, L., Greber, Y., Shoshani, E. & Girsh, E. (1993). Oxytocin and estradiol concentrations in follicular fluid as a means for the classification of large bovine follicles. Theriogenology 39, 421–32.CrossRefGoogle ScholarPubMed
Nurse, P. (1990). Universal control mechanism regulating onset of M-phase. Nature 344, 503–8.Google Scholar
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.Google Scholar
Purohit, G.N., Brady, M.S. & Sharma, S.S. (2005). Influence of epidermal growth factor and insulin-like growth factor 1 on nuclear maturation and fertilization of buffalo cumulus oocyte complexes in serum free media and their subsequent development in vitro. Anim. Reprod. Sci. 87, 229–39.Google Scholar
Reizel, Y., Elbaz, J. & Dekel, N. (2010). Sustained activity of the EGF receptor is an absolute requisite for LH-induced oocyte maturation and cumulus expansion. Mol. Endocrinol. 24, 402–11.Google Scholar
Richard, F.J. & Sirard, M.A. (1996). Effects of follicular cells on oocyte maturation. II: theca cell inhibition of bovine oocyte maturation in vitro. Biol. Reprod. 54, 22–8.Google Scholar
Rivera, G.M. & Fortune, J.E. (2003). Selection of the dominant follicle and insulin-like growth factor (IGF)-binding proteins: evidence that pregnancy-associated plasma protein A contributes to proteolysis of IGF-binding protein 5 in bovine follicular fluid. Endocrinology 144, 437–46.Google Scholar
Sakaguchi, M., Dominko, T., Yamauchi, N., Leibfried-Rutledge, M.L., Nagai, T. & First, N.L. (2002). Possible mechanism for acceleration of meiotic progression of bovine follicular oocytes by growth factors in vitro. Reproduction 123, 135–42.Google Scholar
Sirard, M.A., Florman, H.M., Leibfried-Rutledge, M.L., Barnes, F.L., Sims, M.L. & First, N.L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–63.Google Scholar
Stefanello, J.R., Barreta, M.H., Porciuncula, P.M., Arruda, J.N., Oliveira, J.F., Oliveira, M.A. & Goncalves, P.B. (2006). Effect of angiotensin II with follicle cells and insulin-like growth factor-I or insulin on bovine oocyte maturation and embryo development. Theriogenology 66, 2068–76.Google Scholar
Sugiura, K., Su, Y.Q., Li, Q., Wigglesworth, K., Matzuk, M.M. & Eppig, J.J. (2010). Estrogen promotes the development of mouse cumulus cells in coordination with oocyte-derived GDF9 and BMP15. Mol. Endocrinol. 24, 2303–14.Google Scholar
Sun, Q.Y., Miao, Y.L. & Schatten, H. (2009). Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 8, 2741–7.Google Scholar
Svensson, J., Movérare-Skrtic, S., Windahl, S., Swanson, C. & Sjögren, K. (2010). Stimulation of both estrogen and androgen receptors maintains skeletal muscle mass in gonadectomized male mice but mainly via different pathways. J. Mol. Endocrinol. 45, 45–57.Google Scholar
Wang, H., Isobe, N., Kumamoto, K., Yamashiro, H., Yamashita, Y. & Terada, T. (2006). Studies of the role of steroid hormone in the regulation of oocyte maturation in cattle. Reprod. Biol. Endocrinol. 4, 4.Google Scholar
Wang, L.M., Feng, H.L., Ma, Y.Z., Cang, M., Li, H.J., Zh, Y., Zhou, P., Wen, J.X., Shorgan, B. & Liu, D.J. (2009). Expression of IGF receptors and its ligands in bovine oocytes and preimplantation embryos. Anim. Reprod. Sci. 114, 99–108.Google Scholar
Wu, B., Ignotz, G., Currie, W.B. & Yang, X. (1997). Dynamics of maturation-promoting factor and its constituent proteins during in vitro maturation of bovine oocytes. Biol. Reprod. 56, 253–9.Google Scholar
Yang, X., Kubota, C., Suzuki, H., Taneja, M., Bols, P.E.J. & Presicce, G.A. (1998). Control of oocyte maturation in cows—biological factors. Theriogenology 49, 471–82.Google Scholar
Zhang, K., Hansen, P. & Ealy, A.D. (2010). Fibroblast growth factor-10 enhances bovine oocyte maturation and developmental competence in vitro. Reproduction 140, 815–26.CrossRefGoogle ScholarPubMed