Hostname: page-component-7dd5485656-bt4hw Total loading time: 0 Render date: 2025-10-31T03:52:54.884Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of exogenous transforming growth factor β1 (TGF-β1) on early bovine embryo development

Published online by Cambridge University Press:  08 June 2018

Antonio D. Barrera Open the ORCID record for Antonio D. Barrera [Opens in a new window] ,
Elina V. García  and
Dora C. Miceli
Antonio D. Barrera*
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, and Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, UNT. Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, Argentina
Elina V. García
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, and Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, UNT. Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, Argentina.
Dora C. Miceli
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, and Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, UNT. Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, Argentina.
*
All correspondence to: Antonio Daniel Barrera. Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, and Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, UNT. Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, Argentina. Telephone: +54 381 4247752, ext. 7099. Fax: +54 381 4248921. E-mail: abarrera@fbqf.unt.edu.ar
Get access Rights & Permissions [Opens in a new window]

Summary

During preimplantation development, embryos are exposed and have the capacity to respond to different growth factors present in the maternal environment. Among these factors, transforming growth factor β1 (TGF-β1) is a well known modulator of embryonic growth and development. However, its action during the first stages of development, when the embryo transits through the oviduct, has not been yet elucidated. The objective of the present study was to examine the effect of early exposure to exogenous TGF-β1 on embryo development and expression of pluripotency (OCT4, NANOG) and DNA methylation (DNMT1, DNMT3A, DNMT3B) genes in bovine embryos produced in vitro. First, gene expression analysis of TGF-β receptors confirmed a stage-specific expression pattern, showing greater mRNA abundance of TGFBR1 and TGFBR2 from the 2- to the 8-cell stage, before embryonic genome activation. Second, embryo culture for the first 48 h in serum-free CR1aa medium supplemented with 50 or 100 ng/ml recombinant TGF-β1 did not affect the cleavage and blastocyst rate (days 7 and 8). However, RT-qPCR analysis showed a significant increase in the relative abundance of NANOG and DNMT3A in the 8-cell stage embryos and expanded blastocysts (day 8) derived from TGF-β1 treated embryos. These results suggest an early action of exogenous TGF-β1 on the bovine embryo, highlighting the importance to provide a more comprehensive understanding of the role of TGF-β signalling during early embryogenesis.

Keywords

Early developmentDNA methylationGrowth factorsOviductPluripotency

Information

Type
Research Article
Information
Zygote , Volume 26 , Issue 3 , June 2018 , pp. 232 - 241
Copyright
Copyright © Cambridge University Press 2018 

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.)

Article purchase

Temporarily unavailable

References

Aviles, M., Gutierrez-Adan, A. & Coy, P. (2010). Oviductal secretions: will they be key factors for the future ARTs? Mol. Hum. Reprod. 16, 896–906.CrossRefGoogle ScholarPubMed
Bai, J. & Xi, Q. (2018). Crosstalk between TGF-beta signaling and epigenome. Acta Biochim. Biophys. Sin (Shanghai) 50, 60–7.Google Scholar
Beyer, T.A., Narimatsu, M., Weiss, A., David, L. & Wrana, J.L. (2013). The TGFbeta superfamily in stem cell biology and early mammalian embryonic development. Biochim. Biophys. Acta 1830, 2268–79.Google Scholar
Brons, I.G., Smithers, L.E., Trotter, M.W., Rugg-Gunn, P., Sun, B., Chuva de Sousa Lopes, S.M., Howlett, S.K., Clarkson, A., Ahrlund-Richter, L., Pedersen, R.A. & Vallier, L. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191–5.Google Scholar
Buhi, W.C., Alvarez, I.M. & Kouba, A.J. (2000). Secreted proteins of the oviduct. Cells Tissues Organs 166, 165–79.CrossRefGoogle ScholarPubMed
Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J. & Wittwer, C.T. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–22.Google Scholar
Cardenas, H., Vieth, E., Lee, J., Segar, M., Liu, Y., Nephew, K.P. & Matei, D. (2014). TGF-beta induces global changes in DNA methylation during the epithelial-to-mesenchymal transition in ovarian cancer cells. Epigenetics 9, 1461–72.CrossRefGoogle ScholarPubMed
Cometti, B.P. S., Dubey, R.K., Imthurn, B. & Rosselli, M. (2018). Natural and environmental oestrogens induce TGFB1 synthesis in oviduct cells. Reproduction 155, 233–44.Google Scholar
Dobbs, K.B., Rodriguez, M., Sudano, M.J., Ortega, M.S. & Hansen, P.J. (2013). Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PLoS One 8, e66230.Google Scholar
Duranthon, V., Watson, A.J. & Lonergan, P. (2008). Preimplantation embryo programming: transcription, epigenetics, and culture environment. Reproduction 135, 141–50.Google Scholar
Edwards, J.R., Yarychkivska, O., Boulard, M. & Bestor, T.H. (2017). DNA methylation and DNA methyltransferases. Epigenetics Chromatin 10, 23.CrossRefGoogle ScholarPubMed
García, E.V., Miceli, D.C., Rizo, G., Valdecantos, P.A. & Barrera, A.D. (2015). Effect of early addition of bone morphogenetic protein 5 (BMP5) to embryo culture medium on in vitro development and expression of developmentally important genes in bovine preimplantation embryos. Theriogenology 84, 589–99.CrossRefGoogle ScholarPubMed
Graf, A., Krebs, S., Zakhartchenko, V., Schwalb, B., Blum, H. & Wolf, E. (2014). Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc. Natl. Acad. Sci. USA 111, 4139–44.Google Scholar
Hajian, M., Hosseini, S.M., Ostadhosseini, S. & Nasr-Esfahani, M.H. (2016). Targeting the transforming growth factor-beta signaling during pre-implantation development in embryos of cattle, sheep and goats. Growth Factors 34, 141–8.Google Scholar
HosseinNia, P., Tahmoorespur, M., Hosseini, S.M., Hajian, M., Ostadhosseini, S., Nasiri, M.R. & Nasr-Esfahani, M.H. (2016). Stage-specific profiling of transforming growth factor-beta, fibroblast growth factor and Wingless-int signaling pathways during early embryo development in the goat. Cell J. 17, 648–58.Google Scholar
Ingman, W.V. & Jones, R.L. (2008). Cytokine knockouts in reproduction: the use of gene ablation to dissect roles of cytokines in reproductive biology. Hum. Reprod. Update 14, 179–92.CrossRefGoogle ScholarPubMed
Ingman, W.V. & Robertson, S.A. (2009). The essential roles of TGFB1 in reproduction. Cytokine Growth Factor Rev. 20, 233–9.Google Scholar
Itoh, F., Watabe, T. & Miyazono, K. (2014). Roles of TGF-beta family signals in the fate determination of pluripotent stem cells. Semin. Cell. Dev. Biol. 32, 98–106.Google Scholar
Jones, R.L., Stoikos, C., Findlay, J.K. & Salamonsen, L.A. (2006). TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132, 217–32.Google Scholar
Keefer, C.L., Stice, S.L., Paprocki, A.M. & Golueke, P. (1994). In vitro culture of bovine IVM-IVF embryos: cooperative interaction among embryos and the role of growth factors. Theriogenology 41, 1323–31.Google Scholar
Khan, D.R., Dube, D., Gall, L., Peynot, N., Ruffini, S., Laffont, L., Le Bourhis, D., Degrelle, S., Jouneau, A. & Duranthon, V. (2012). Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS One 7, e34110.CrossRefGoogle ScholarPubMed
Knight, P.G. & Glister, C. (2006). TGF-beta superfamily members and ovarian follicle development. Reproduction 132, 191–206.Google Scholar
Kues, W.A., Sudheer, S., Herrmann, D., Carnwath, J.W., Havlicek, V., Besenfelder, U., Lehrach, H., Adjaye, J. & Niemann, H. (2008). Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. Proc. Natl. Acad. Sci. USA 105, 19768–73.CrossRefGoogle ScholarPubMed
Larson, R.C., Ignotz, G.G. & Currie, W.B. (1992). Transforming growth factor-beta and basic fibroblast growth factor synergistically promote early bovine embryo development during the fourth cell cycle. Mol. Reprod. Dev. 33, 432–5.Google Scholar
Lee, K.F. & Yeung, W.S. (2006). Gamete/embryo - oviduct interactions: implications on in vitro culture. Hum. Fertil. (Camb.) 9, 137–43.CrossRefGoogle ScholarPubMed
Li, Q. (2014). Transforming growth factor-beta signaling in uterine development and function. J. Anim. Sci. Biotechnol. 5, 52.Google Scholar
Lim, J., Bongso, A. & Ratnam, S. (1993). Mitogenic and cytogenetic evaluation of transforming growth factor-beta on murine preimplantation embryonic development in vitro. Mol. Reprod. Dev. 36, 482–7.Google Scholar
Loh, Y.H., Wu, Q., Chew, J.L., Vega, V.B., Zhang, W., Chen, X., Bourque, G., George, J., Leong, B., Liu, J., Wong, K.Y., Sung, K.W., Lee, C.W., Zhao, X.D., Chiu, K.P., Lipovich, L., Kuznetsov, V.A., Robson, P., Stanton, L.W., Wei, C.L., Ruan, Y., Lim, B. & Ng, H.H. (2006). The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 38, 431–40.Google Scholar
Maillo, V., Lopera-Vasquez, R., Hamdi, M., Gutierrez-Adan, A., Lonergan, P. & Rizos, D. (2016). Maternal-embryo interaction in the bovine oviduct: evidence from in vivo and in vitro studies. Theriogenology 86, 443–50.CrossRefGoogle ScholarPubMed
Monsivais, D., Matzuk, M.M. & Pangas, S.A. (2017). The TGF-beta family in the reproductive tract. Cold Spring Harb. Perspect. Biol. 9, pii: a022251.Google Scholar
Moreno, D., Neira, A., Dubreil, L., Liegeois, L., Destrumelle, S., Michaud, S., Thorin, C., Briand-Amirat, L., Bencharif, D. & Tainturier, D. (2015). In vitro bovine embryo production in a synthetic medium: embryo development, cryosurvival, and establishment of pregnancy. Theriogenology 84, 1053–60.CrossRefGoogle Scholar
Neira, J.A., Tainturier, D., Pena, M.A. & Martal, J. (2010). Effect of the association of IGF-I, IGF-II, bFGF, TGF-beta1, GM-CSF, and LIF on the development of bovine embryos produced in vitro. Theriogenology 73, 595–604.Google Scholar
Palmer, N. & Kaldis, P. (2016). Regulation of the embryonic cell cycle during mammalian preimplantation development. Curr. Top. Dev. Biol. 120, 1–53.Google Scholar
Pan, X., Chen, Z., Huang, R., Yao, Y. & Ma, G. (2013). Transforming growth factor beta1 induces the expression of collagen type I by DNA methylation in cardiac fibroblasts. PLoS One 8, e60335.Google Scholar
Pillai, V.V., Weber, D.M., Phinney, B.S. & Selvaraj, V. (2017). Profiling of proteins secreted in the bovine oviduct reveals diverse functions of this luminal microenvironment. PLoS One 12, e0188105.Google Scholar
Rizos, D., Maillo, V., Sanchez-Calabuig, M.J. & Lonergan, P. (2017). The consequences of maternal-embryonic cross talk during the periconception period on subsequent embryonic development. Adv. Exp. Med. Biol. 1014, 69–86.Google Scholar
Robertson, S.A., Chin, P.Y., Schjenken, J.E. & Thompson, J.G. (2015). Female tract cytokines and developmental programming in embryos. Adv. Exp. Med. Biol. 843, 173–213.CrossRefGoogle ScholarPubMed
Sudheer, S. & Adjaye, J. (2007). Functional genomics of human pre-implantation development. Brief Funct. Genomic Proteomic 6, 120–32.Google Scholar
Tribulo, P., Siqueira, L.G. B., Oliveira, L.J., Scheffler, T. & Hansen, P.J. (2018). Identification of potential embryokines in the bovine reproductive tract. J. Dairy Sci. 101, 690–704.CrossRefGoogle ScholarPubMed
Weiss, A. & Attisano, L. (2013). The TGFbeta superfamily signaling pathway. Wiley Interdiscip. Rev. Dev. Biol. 2, 47–63.Google Scholar
Xu, R.H., Sampsell-Barron, T.L., Gu, F., Root, S., Peck, R.M., Pan, G., Yu, J., Antosiewicz-Bourget, J., Tian, S., Stewart, R. & Thomson, J.A. (2008). NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 3, 196–206.Google Scholar
Zhang, K., Rajput, S.K., Lee, K.B., Wang, D., Huang, J., Folger, J.K., Knott, J.G., Zhang, J. & Smith, G.W. (2015). Evidence supporting a role for SMAD2/3 in bovine early embryonic development: potential implications for embryotropic actions of follistatin. Biol. Reprod. 93, 86.Google Scholar
Zhang, Q., Chen, L., Helfand, B.T., Jang, T.L., Sharma, V., Kozlowski, J., Kuzel, T.M., Zhu, L.J., Yang, X.J., Javonovic, B., Guo, Y., Lonning, S., Harper, J., Teicher, B.A., Brendler, C., Yu, N., Catalona, W.J. & Lee, C. (2011). TGF-beta regulates DNA methyltransferase expression in prostate cancer, correlates with aggressive capabilities, and predicts disease recurrence. PLoS One 6, e25168.Google Scholar
Zhang, Y.E. (2017). Non-Smad signaling pathways of the TGF-beta family. Cold Spring Harb. Perspect. Biol. 9, pii: a022129.Google Scholar
Zuo, Y., Su, G., Wang, S., Yang, L., Liao, M., Wei, Z., Bai, C. & Li, G. (2016). Exploring timing activation of functional pathway based on differential co-expression analysis in preimplantation embryogenesis. Oncotarget 7, 74120–31.CrossRefGoogle ScholarPubMed