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Effects of bone morphogenetic protein 4 (BMP4) on in vitro development and survival of bovine preantral follicles enclosed in fragments ovarian tissue

Published online by Cambridge University Press:  16 March 2017

Ellen de Vasconcelos da Cunha ,
Glaucinete Borges de Souza ,
José Renato de Sousa Passos ,
Anderson Weiny Barbalho Silva ,
Andressa Minussi Dau ,
Márcia Viviane Alves Saraiva ,
Raimundo Nonato Braga Lobo  and
José Roberto Viana Silva
Ellen de Vasconcelos da Cunha
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil.
Glaucinete Borges de Souza
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil.
José Renato de Sousa Passos
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil.
Anderson Weiny Barbalho Silva
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil.
Andressa Minussi Dau
Affiliation:
Laboratory of Biotechnology and Animal Reproduction (BioRep), Federal University of Santa Maria (UFSM) Santa Maria, RS, Brazil.
Márcia Viviane Alves Saraiva
Affiliation:
Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Sobral, CE, Brazil.
Raimundo Nonato Braga Lobo
Affiliation:
Brazilian Agricultural Research Corporation (EMBRAPA) Goats and Sheep, Sobral, CE, Brazil.
José Roberto Viana Silva*
Affiliation:
Biotechnology Nucleus of Sobral − NUBIS, Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041–040, Sobral, CE, Brazil.
*
All correspondence to José Roberto Viana Silva. Biotechnology Nucleus of Sobral − NUBIS, Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041–040, Sobral, CE, Brazil. Tel:/Fax: +55 88 36118000. E-mail: jrvsilva@ufc.br
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Summary

The aim of this study was to evaluate the effects of different concentrations of BMP4 on activation, development and mRNA expression of GDF9, BMP15, PCNA, Bax and Bcl2 in cultured bovine follicles enclosed in ovarian tissues. Ovarian tissue fragments were cultured for 6 days in α-MEM+ alone or supplemented with different concentrations of BMP4 (10, 50 or 100 ng/ml). Classical histology was performed to analyze follicle growth and morphology, while real-time PCR was used to analyze mRNA levels in fresh and cultured tissues. After 6 days, the culture of ovarian tissue in α-MEM+ alone or supplemented with 10, 50 or 100 ng/ml BMP4 promoted follicular activation. The different concentrations of BMP4 maintained the percentage of normal follicles similar to results of the control. The presence of 100 ng/ml BMP-4 in culture medium increased oocyte and follicular diameters of primary and secondary follicles when compared with those follicles from uncultured control or cultured in α-MEM+ alone (P < 0.05). The tissues cultured in the presence of increasing concentrations of BMP4 had an increase in mRNA expression of the tested genes, but despite this the differences were not statistically significant. In conclusion, 100 ng/ml BMP4 promotes an increase in diameters of follicles and oocytes of primary and secondary follicles after 6 days of in vitro culture.

Keywords

ActivationCowCultureOvaryPrimordial follicle
Type
Research Article
Information
Zygote , Volume 25 , Issue 3 , June 2017 , pp. 256 - 264
Copyright
Copyright © Cambridge University Press 2017 

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References

Bertoldo, M.J., Duffard, N., Bernard, J., Frapsauce, C., Calais, L., Rico, C., Mermillod, P. & Locatelli, Y. (2014). Effects of bone morphogenetic protein 4 (BMP4) supplementation during culture of the sheep ovarian cortex. Anim. Reprod. Sci. 149, 3–4, 124–34.Google Scholar
Bodensteiner, K.J., Clay, C.M., Moeller, C.L. & Sawyer, 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, 381–6.Google Scholar
Campbell, B.K., Souza, C.J., Skinner, A.J., Webb, R. & Baird, D.T. (2006). Enhanced response of granulose and theca cells from sheep carriers of the FecB mutation in vitro to gonadotropins and bone morphogenic protein-2, -4, and -6. Endocrinology 147, 1608–20.Google Scholar
Carabatsos, M.J., Elvin, J., Matzuk, M.M. & Albertini, D.F. (1998). Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev. Biol. 204, 373–84.CrossRefGoogle ScholarPubMed
Celestino, J.J., Bruno, J.B., Saraiva, M.V., Rocha, R.M., Brito, I.R., Duarte, A.B., Araújo, V.R., Silva, C.M., Matos, M.H., Campello, C.C., Silva, J.R. & Figueiredo, J.R. (2011). Steady-state level of epidermal growth factor (EGF) mRNA and effect of EGF on in vitro culture of caprine preantral follicles. Cell Tissue 344, 539–50.Google Scholar
Chen, D., Zhao, M. & Mundy, G.R. (2004). Bone morphogenetic proteins. Growth Factors 22, 233–41.CrossRefGoogle ScholarPubMed
Childs, A.J., Kinnell, H.L., Collins, C.S., Hogg, K., Bayne, R.A., Green, S.J., Mcneilly, A.S. & Anderson, R.A. (2010). BMP signaling in the human fetal ovary is developmentally regulated and promotes primordial germ cell apoptosis. Stem Cells 28, 1368–78.Google Scholar
Choi, D., Hwang, S., Lee, E., Yoon, S., Yoon, B. & Bae, D. (2004). Expression of mitochondria dependent apoptosis genes (p53, Bax, Bcl-2) in rat granulosa cells during follicular development. J. Soc. Gynecol. Investig. 11, 311–7.Google Scholar
Cortvrindt, R. & Smitz, J. (2001). In vitro follicle growth: achievements in mammalian species. Reprod. Domest. Anim. 36, 3–9.Google Scholar
Costa, J.J., Passos, M.J., Leitão, C.C., Vasconcelos, G.L., Saraiva, M.V., Figueiredo, J.R., van den Hurk, R. & Silva, J.R. (2012). Levels of mRNA for bone morphogenetic proteins, their receptors and SMADs in goat ovarian follicles grown in vivo and in vitro . Reprod. Fertil. Dev. 24, 723–32.CrossRefGoogle ScholarPubMed
Cushman, R.A., Wahl, C.M. & Fortune, J.E. (2002). Bovine ovarian cortical pieces grafted to chick embryonic membranes: a model for studies on the activation of primordial follicles. Hum. Reprod. 17, 48–54.Google Scholar
Ding, X., Zhang, X., Mu, Y., Li, Y. & Hao, J. (2013). Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via up-regulation of Sohlh2 and c-kit. Mol. Reprod. Dev. 80, 70–8.Google Scholar
Fabre, S., Pierre, A., Pisselet, C., Mulsant, P., Lecerf, F., Pohl, J., Monget, P. & Monniaux, D. (2003). The Booroola mutation in sheep is associated with an alteration of the bone morphogenetic protein receptor-IB functionality. J. Endocrinol. 177, 435–44.Google Scholar
Fatehi, A.N., Van Den Hurk, R., Colenbrander, B., Daemen, A.J., Van Tol H, T., Monteiro, R.M., Roelen, B.A. & Bevers, M.M. (2005). Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 63, 872–89.CrossRefGoogle ScholarPubMed
Glister, C., Richards, S.L. & Knight, P.G. (2004). Bone morphogenetic proteins (BMP) -4, -6, and -7 potently suppress basal and luteinizing hormone-induced androgen production by bovine theca interna cells in primary culture: could ovarian hyperandrogenic dysfunction be caused by a defect in thecal BMP signaling. Endocrinology 146, 1883–92.CrossRefGoogle ScholarPubMed
Hayashi, M., Mcgee, E.A., Min, G., Klein, C., Rose, U.M., Van Duin, M. & Hsueh, A.J. (1999). Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140, 1236–44.Google Scholar
Hsueh, A.J.W., Kawamura, K., Cheng, Y. & Fauser, B.C.J.M. (2015). Intraovarian control of early folliculogenesis. Endocr. Rev. 36, 1–24.CrossRefGoogle ScholarPubMed
Hussein, M.R. (2005). Apoptosis in the ovary: molecular mechanisms. Hum. Reprod. Update 11, 162–78.Google Scholar
Hussein, M.R., Bedaiwy, M.A. & Falcon, E.T. (2006). Analysis of apoptotic cell death, Bcl-2, and p53 protein expression in freshly fixed and cryopreserved ovarian tissue after exposure to warm ischemia. Fertil. Steril. 85, 1082–92.Google Scholar
Juengel, J.L., Hudson, N.L., Whitinig, L. & Mcnatty, K.P. (2004). Effects of immunization against bone morphogenetic protein 15 and growth differentiation factor 9 on ovulation rate, fertilization, and pregnancy in ewes. Biol. Reprod. 70, 557–61.Google Scholar
Juengel, J.L., Reader, K.L., Bibby, A.H., Lun, S., Ross, I., Haydon, L.J. & McNatty, K.P. (2006). The role of bone morphogenetic proteins 2, 4, 6 and 7 during ovarian follicular development in sheep: contrast to rat. Reproduction 131, 501–13.Google Scholar
Juengel, J.L., Hudson, N.L., Heath, D.A., Smith, P., Reader, K.L., Lawrence, S.B., O'Connell, A.R., Laitinen, M.P., Cranfield, M., Groome, N.P., Ritvos, O. & Mcnatty, K.P. (2002). Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 67, 1777–89.Google Scholar
Kawamura, K., Cheng, Y., Suzuki, N., Deguchi, M., Sato, Y., Takae, S., Ho, C.H., Kawamura, N., Tamura, M., Hashimoto, S., Sugishita, Y., Morimoto, Y., Hosoi, Y., Yoshioka, N., Ishizuka, B. & Hsueh, A.J. (2013). Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc. Natl. Acad. Sci. USA 43, 17474–9.Google Scholar
Kerr, J.B., Myers, M. & Anderson, R.A. (2013). The dynamics of the primordial follicle reserve. Reproduction 146, 205–15.Google Scholar
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔC t method. Methods 25, 402–8.Google Scholar
Maga, G. & Hubscher, U. (2003). Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J. Cell Sci. 116, 3051–60.Google Scholar
Martins, F.F.S., Celestino, J.J.H., Saraiva, M.V.A., Matos, M.H.T., Bruno, J.B., Rocha-Junior, C.M.C., Lima-Verde, I.B., Lucci, C.M., Báo, S.N. & Figueiredo, J.R. (2008). Growth and differentiation factor-9 stimulates goat primordial follicles activation in vitro and the progression to secondary follicles reproduction. Reprod. Fertil. Dev. 20, 916–24.CrossRefGoogle Scholar
Muskhelishvili, L., Wingard, S.K. & Latendresse, J.R. (2005). Proliferating cell nuclear antigen − a marker for ovarian follicle counts. Toxicol. Pathol. 33, 365–8.Google Scholar
Nilsson, E.E. & Skinner, M.K. (2003). Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol. Reprod. 69, 1265–72.Google Scholar
Otsuka, S., Suda, S., Li, R., Matsumoto, S. & Watanabe, M.M. (2000). Morphological variability of colonies of Microcystis morphospecies in culture. J. Gen. Appl. Microbiol. 46, 39–50.Google Scholar
Park, E.S., Woods, D.C & Tilly, J.L. (2013). Bone morphogenetic protein 4 promotes mammalian oogonial stem cell differentiation via Smad1/5/8 signaling. Fertil. Steril. 100, 1468–75.Google Scholar
Pfaffl, M.W., Lange, I.G., Daxenberger, A. & Meyer, H.H. (2001). Tissue-specific expression pattern of estrogen receptors (ER): quantification of ER alpha and ER beta mRNA with real-time RT-PCR. APMIS 109, 345–55.CrossRefGoogle ScholarPubMed
Pierre, A., Pisselet, C., Dupont, J., Mandon-Pépin, B., Monniaux, D., Monget, P. & Fabre, S. (2004). Molecular basis of bone morphogenetic protein-4 inhibitory action on progesterone secretion by ovine granulosa cells. J. Mol. Endocrinol. 33, 805–17.Google Scholar
Rebouças, E.L., Costa, J.J.N., Passos, M.J., Passos, J.R.S., van den Hurk, R. & Silva, J.R.V. (2013) Real time PCR and importance of housekeepings genes for normalization and quantification of mRNA expression in different tissues. Braz. Arch. Biol. Technol. 56, 1.Google Scholar
Rossi, R.O.D.S., Portela, A.M.L.R., Passos, J.R.S., Cunha, E.V., Silva, A.W.B., Costa, J.J.N., Saraiva, M.V.A., Donato, M.A.M., Peixoto, C.A., Van Der Huck, R. & Silva, J.R.V. (2015). Effects of BMP-4 and FSH on growth, morphology and mRNA expression of oocyte-secreted factors in cultured bovine secondary follicles. Anim. Reprod. 12, 910–919.Google Scholar
Sadeu, J.C. & Smitz, J. (2008). Growth differentiation factor-9 and anti-Mullerian hormone expression in cultured follicles from frozen-thawed ovarian tissue. Reprod. Biomed. Online 17, 537–48.Google Scholar
Shah, S.M., Saini, N., Ashraf, S., Singh, M.K., Manik, R., Singla, S.K., Palta, P. & Chauhan, M.S. (2015). Development of buffalo (Bubalus bubalis) embryonic stem cell lines from somatic cell nuclear transferred blastocysts. Stem Cell Res. 15, 633–9.Google Scholar
Shimasaki, S., Zachow, R.J., Li, D., Kim, H., Iemura, S., Ueno, N., Sampath, K., Chang, R.J. & Erickson, G.F. (1999). A functional bone morphogenetic protein system in the ovary. Proc. Natl. Acad. Sci. USA 96, 7282–7.Google Scholar
Shimizu, T., Kayamori, T., Murayama, C. & Miyamoto, A. (2012). Bone morphogenetic protein (BMP)-4 and BMP-7 suppress granulosa cell apoptosis via different pathways: BMP-4 via PI3K/PDK-1/Akt and BMP-7 via PI3K/PDK-1/PKC. Biochem. Biophys. Res. Commun. 417, 869–73.Google Scholar
Shimizu, T., Yokoo, M., Miyake, Y., Sasada, H. & Sato, E. (2004). Differential expression of bone morphogenetic protein 4–6 (BMP-4,-5, and -6) and growth differentiation factor-9 (GDF-9) during ovarian development in neonatal pigs. Domest. Anim. Endocrinol. 27, 397–405.CrossRefGoogle ScholarPubMed
Singhal, D.K., Singhal, R., Malik, H.N., Singh, S., Kumar, S., Kaushik, J.K., Mohanty, A.K. & Malakar, D. (2015). Generation of germ cell-like cells and oocyte-like cells from goat induced pluripotent stem cells. J. Stem Cell Res. 5, 5.Google Scholar
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.Google Scholar
Tanwar, P.S. & McFarlane, J.R. (2011). Dynamic expression of bone morphogenetic protein 4 in reproductive organs of female mice. Reproduction 142, 573–9.Google Scholar
Tanwar, P.S., O'Shea, T. & McFarlane, J.R. (2008). In vivo evidence of role of bone morphogenetic protein-4 in the mouse ovary. Anim. Reprod. Sci. 106, 232–40.Google Scholar
Tilly, J.L., Tilly, K., Kenton, M. & Johnson, A. (1995). Expression of members of the Bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-x long messenger ribonucleic acid levels. Endocrinology 136, 232–41.Google Scholar
Van Den Hurk, R. & Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–51.Google Scholar
Vitt, U.A., Mcgee, E.A., Hayashi, M. & Hsueh, A.J. (2000). In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 141, 3814–20.Google Scholar
Wandji, S.A., Srsen, V., Voss, A.K., Eppig, J.J. & Fortune, J.E. (1996). Initiation in vitro of growth of bovine primordial follicles. Biol. Reprod. 55, 942–8.Google Scholar
Young, J.M. & McNeilly, A.S. (2010). Theca: the forgotten cell of the ovarian follicle. Reproduction 140, 489–504.CrossRefGoogle ScholarPubMed