Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-13T04:26:52.579Z Has data issue: false hasContentIssue false

Paternal breed effects on expression of IGF-II, BAK1 and BCL2-L1 in bovine preimplantation embryos

Published online by Cambridge University Press:  02 September 2014

Mehdi Vafaye Valleh*
Affiliation:
Department of Animal Science, Faculty of Agriculture, University of Zabol, P.O. Box 98615–538, Zabol, Iran.
Mojtaba Tahmoorespur
Affiliation:
Department of Animal Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, I.R. Iran.
Morteza Daliri Joupari
Affiliation:
National Institutes for Genetic Engineering and Biotechnology, Karaj, Iran.
Hesam Dehghani
Affiliation:
Embryonic and Stem Cell Biology and Biotechnology Research Group, Research Institute of Biotechnology, Ferdowsi University of Mashhad, Mashhad, Iran.
Mikkel Aabech Rasmussen
Affiliation:
Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Groennegardsvej, 7,1870 Frederiksberg C, Denmark.
Poul Hyttel
Affiliation:
Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Groennegardsvej, 7,1870 Frederiksberg C, Denmark.
Lotte Strøbech
Affiliation:
Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Groennegardsvej, 7,1870 Frederiksberg C, Denmark.
*
All correspondence to: Mehdi Vafaye Valleh. Department of Animal Science, Faculty of Agriculture, University of Zabol, P.O. Box 98615-538, Zabol, Iran. e-mail: mehdi.valleh@uoz.ac.ir

Summary

The effects of the paternal breed on early embryo and later pre- and postnatal development are well documented. Several recent studies have suggested that such paternal effects may be mediated by the paternally induced epigenetic modifications during early embryogenesis. The objective of this study was to investigate the effects of the paternal breed on the early embryonic development and relative expression of the maternally imprinted gene, IGF-II, and the apoptosis-related genes BAK1 and BCL2-L1 in in vitro produced (IVP) bovine embryos derived from two unrelated paternal breeds (Holstein and Brown Swiss). The degree of correlation of IGF-II expression pattern with embryo developmental competence and apoptosis-related genes was also investigated. The relative abundance of IGF-II, BCL2-L1 and BAK1 transcripts in day 8 embryos was measured by quantitative reverse-transcription polymerase chain reaction using the comparative Cp method. Our data revealed that the paternal breed did not influence cleavage rate, blastocyst rate and relative abundance of IGF-II, BAK1 and BCL2-L1 in day 8 blastocysts (P > 0.05). Nevertheless, IGF-II expression levels were highly correlated with embryonic developmental competence (r = 0.66, P < 0.1), relative expression of BCL2-L1 (r = 0.72, P < 0.05) and ratio of BCL2-L1/BAK1 (r = 0.78, P < 0.05). In conclusion, our data show that IGF-II, BCL2-L1 and BAK1 expression is not related to the chosen combination of paternal breed, but that IGF-II expression is correlated with embryonic viability and apoptosis-related gene expression.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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

Barros, C.M., Pegorer, M.F., Vasconcelos, J.L., Eberhardt, B.G. & Monteiro, F.M. (2006). Importance of sperm genotype (indicus versus taurus) for fertility and embryonic development at elevated temperatures. Theriogenology 65, 210–8.CrossRefGoogle ScholarPubMed
Bilodeau-Goeseels, S. & Kastelic, J.P. (2003). Factors affecting embryo survival and strategies to reduce embryonic mortality in cattle. Can. J. Anim. Sci. 83, 659–67.CrossRefGoogle Scholar
Byrne, A.T., Southgate, J., Brison, D.R. & Leese, H.J. (2002). Regulation of apoptosis in the bovine blastocyst by insulin and the insulin-like growth factor (IGF) superfamily. Mol. Reprod. Dev. 62, 489–95.CrossRefGoogle ScholarPubMed
Casas, E., Thallman, R.M. & Cundiff, L.V. (2011). Birth and weaning traits in crossbred cattle from Hereford, Angus, Brahman, Boran, Tuli, and Belgian Blue sires. J. Anim. Sci. 89, 979–87.CrossRefGoogle ScholarPubMed
Chason, R.J., Csokmay, J., Segars, J.H., DeCherney, A.H. & Armant, D.R. (2011). Environmental and epigenetic effects upon preimplantation embryo metabolism and development. Trends Endocrinol. Metab. 22, 412–20.CrossRefGoogle ScholarPubMed
Chen, J.J., Delongchamp, R.R., Tsai, C.A., Hsueh, H.M., Sistare, F., Thompson, K.L., Desai, V.G. & Fuscoe, J.C. (2004). Analysis of variance components in gene expression data. Bioinformatics 20, 1436–46.CrossRefGoogle ScholarPubMed
Constancia, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C. & Reik, W. (2002). Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417, 945–8.CrossRefGoogle Scholar
Dean, W., Bowden, L., Aitchison, A., Klose, J., Moore, T., Meneses, J.J., Reik, W. & Feil, R. (1998). Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes. Development 125, 2273–82.CrossRefGoogle ScholarPubMed
Eberhardt, B.G., Satrapa, R.A., Capinzaiki, C.R., Trinca, L.A. & Barros, C.M. (2009). Influence of the breed of bull (Bos taurus indicus vs. Bos taurus taurus) and the breed of cow (Bos taurus indicus, Bos taurus taurus and crossbred) on the resistance of bovine embryos to heat. Anim. Reprod. Sci. 114, 5461.CrossRefGoogle ScholarPubMed
Feinberg, A.P. & Irizarry, R.A. (2010). Evolution in health and medicine Sackler colloquium: Stochastic epigenetic variation as a driving force of development evolutionary adaptation, and disease. Proc. Natl. Acad. Sci. USA 107 (Suppl. 1), 1757–64.CrossRefGoogle ScholarPubMed
Fischer, A.E., Bernal, D.P., Gutierrez-Robayo, C. & Rutledge, J.J. (2000). Estimates of heterosis for in vitro embryo production using reciprocal crosses in cattle. Theriogenology, 54, 1433–42.CrossRefGoogle ScholarPubMed
Fryer, H.C., Marion, G.B. & Farmer, J.L. (1958). nonreturn rate of artificially inseminated dairy cows as affected by age of semen, breed of bull, and season. J. Dairy Sci. 41, 987–93.CrossRefGoogle Scholar
Fu, H., Subramanian, R.R. & Masters, S.C. (2000). 14–3–3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 40, 617–47.CrossRefGoogle Scholar
Gebert, C., Wrenzycki, C., Herrmann, D., Groger, D., Reinhardt, R., Hajkova, P., Lucas-Hahn, A., Carnwath, J., Lehrach, H. & Niemann, H. (2006). The bovine IGF2 gene is differentially methylated in oocyte and sperm DNA. Genomics 88, 222–9.CrossRefGoogle ScholarPubMed
Gebert, C., Wrenzycki, C., Herrmann, D., Groger, D., Thiel, J., Reinhardt, R., Lehrach, H., Hajkova, P., Lucas-Hahn, A., Carnwath, J.W. & Niemann, H. (2009). DNA methylation in the IGF2 intragenic DMR is re-established in a sex-specific manner in bovine blastocysts after somatic cloning. Genomics 94, 63–9.CrossRefGoogle Scholar
Glabowski, W., Kurzawa, R., Wiszniewska, B., Baczkowski, T., Marchlewicz, M. & Brelik, P. (2005). Growth factors effects on preimplantation development of mouse embryos exposed to tumor necrosis factor alpha. Reprod. Biol. 5, 8399.Google ScholarPubMed
Goodall, J.J. & Schmutz, S.M. (2003). Linkage mapping of IGF2 on cattle chromosome 29. Anim. Genet. 34, 313.CrossRefGoogle ScholarPubMed
Gyu-Jin, Rho, Balasubramanian, S, Dong-Sik, Kim, Woo-Jin, Son, Sang-Rae, Cho, Jung-Gon, Kim, Mohana kumar, B & Sang-Young, Cho. (2007). Influence of in vitro oxygen concentrations on preimplantation embryo development gene expression and production of Hanwoo calves following embryo transfer. Mol. Reprod. Dev. 74, 486–96.Google Scholar
Han, L., Lee, D.H. & Szabo, P.E. (2008a). CTCF is the master organizer of domain-wide allele-specific chromatin at the H19/Igf2 imprinted region. Mol. Cell. Biol. 28, 1124–35.CrossRefGoogle ScholarPubMed
Han, Z.M., Mtango, N.R., Patel, B.G., Sapienza, C. & Latham, K.E. (2008b). Hybrid vigor and transgenerational epigenetic effects on early mouse embryo phenotype. Biol. Reprod. 79, 638648.CrossRefGoogle ScholarPubMed
Hansen, P.J. (2007). Embryonic mortality in cattle from the embryo's perspective. J. Anim. Sci. 80, e33–44.CrossRefGoogle Scholar
Harvey, A.J. (2007). The role of oxygen in ruminant preimplantation embryo development and metabolism. Anim. Reprod. Sci. 98, 113–28.CrossRefGoogle ScholarPubMed
Hwang, I.S., Park, M.R., Moon, H.J., Shim, J.H., Kim, D.H., Yang, B.C., Ko, Y.G., Yang, B.S., Cheong, H.T. & Im, G.S. (2008). Osmolarity at early culture stage affects development and expression of apoptosis related genes (Bax-alpha and Bcl-xl) in pre-implantation porcine NT embryos. Mol. Reprod. Dev. 75, 464–71.CrossRefGoogle ScholarPubMed
Jenkins, T.G. & Carrell, D.T. (2011). The paternal epigenome and embryogenesis: poising mechanisms for development. Asian J. Androl. 13, 7680.CrossRefGoogle ScholarPubMed
Jenkins, T.G. & Carrell, D.T. (2012). The sperm epigenome and potential implications for the developing embryo. Reproduction 143, 727–34.CrossRefGoogle ScholarPubMed
Jeong, Y.J., Cui, X.S., Kim, B.K., Kim, I.H., Kim, T., Chung, Y.B. & Kim, N.H. (2005). Haploidy influences Bak and Bcl-xL mRNA expression and increases incidence of apoptosis in porcine embryos. Zygote 13, 1721.CrossRefGoogle ScholarPubMed
Jin, Y.X., Lee, J.Y., Choi, S.H., Kim, T., Cui, X.S. & Kim, N.H. (2007). Heat shock induces apoptosis related gene expression and apoptosis in porcine parthenotes developing in vitro. Anim. Reprod. Sci. 100, 118–27.CrossRefGoogle ScholarPubMed
Khatib, H., Huang, W., Wang, X., Tran, A.H., Bindrim, A.B., Schutzkus, V., Monson, R.L. & Yandell, B.S. (2009). Single gene and gene interaction effects on fertilization and embryonic survival rates in cattle. J. Dairy Sci. 92, 2238–47.CrossRefGoogle ScholarPubMed
Khosla, S., Dean, W., Reik, W. & Feil, R. (2001). Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Hum. Reprod. Update 7, 419–27.CrossRefGoogle ScholarPubMed
Kim, J., Song, G., Gao, H., Farmer, J.L., Satterfield, M.C., Burghardt, R.C., Wu, G., Johnson, G.A., Spencer, T.E. & Bazer, F.W. (2008). Insulin-like growth factor II activates phosphatidylinositol 3-kinase-protooncogenic protein kinase 1 and mitogen-activated protein kinase cell signaling pathways, and stimulates migration of ovine trophectoderm cells. Endocrinology 149, 3085–94.CrossRefGoogle ScholarPubMed
Kurzawa, R., Glabowski, W., Baczkowski, T., Wiszniewska, B. & Marchlewicz, M. (2004). Growth factors protect in vitro cultured embryos from the consequences of oxidative stress. Zygote 12, 231240.CrossRefGoogle ScholarPubMed
Kwong, W.Y., Miller, D.J., Ursell, E., Wild, A.E., Wilkins, A.P., Osmond, C., Anthony, F.W. & Fleming, T.P. (2006). Imprinted gene expression in the rat embryo-fetal axis is altered in response to periconceptional maternal low protein diet. Reproduction 132, 265–77.CrossRefGoogle ScholarPubMed
Lazzari, G., Colleoni, S., Duchi, R., Galli, A., Houghton, F.D. & Galli, C. (2011). Embryonic genotype and inbreeding affect preimplantation development in cattle. Reproduction 141, 625–32.CrossRefGoogle ScholarPubMed
Lloyd, R.E., Romar, R., Matas, C., Gutierrez-Adan, A., Holt, W.V. & Coy, P. (2009). Effects of oviductal fluid on the development quality, and gene expression of porcine blastocysts produced in vitro. Reproduction 137, 679–87.CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Moreira, P.M., Pintado, B., de la Fuente, J. & Boland, M.P. (2003a). Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol Reprod. 69, 1424–31.CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Kanka, J., Nemcova, L., Mbaye, A.M., Kingston, M., Wade, M., Duffy, P. & Boland, M.P. (2003b). Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction 126, 337–46.CrossRefGoogle ScholarPubMed
Natale, D.R., De Sousa, P.A., Westhusin, M.E. & Watson, A.J. (2001). Sensitivity of bovine blastocyst gene expression patterns to culture environments assessed by differential display RT-PCR. Reproduction 122, 687–93.CrossRefGoogle ScholarPubMed
Niemann, H., Tian, X.C., King, W.A. & Lee, R.S. (2008). Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning. Reproduction 135, 151–63.CrossRefGoogle ScholarPubMed
Nussbaum, T., Samarin, J., Ehemann, V., Bissinger, M., Ryschich, E., Khamidjanov, A., Yu, X., Gretz, N., Schirmacher, P. & Breuhahn, K. (2008). Autocrine insulin-like growth factor-II stimulation of tumor cell migration is a progression step in human hepatocarcinogenesis. Hepatology 48, 146–56.CrossRefGoogle ScholarPubMed
Perecin, F., Meo, S.C., Yamazaki, W., Ferreira, C.R., Merighe, G.K., Meirelles, F.V. & Garcia, J.M. (2009). Imprinted gene expression in in vivo- and in vitro-produced bovine embryos and chorio-allantoic membranes. Genet. Mol. Res. 8, 7685.CrossRefGoogle ScholarPubMed
Peruzzi, F., Prisco, M., Dews, M., Salomoni, P., Grassilli, E., Romano, G., Calabretta, B. & Baserga, R. (1999). Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol. Cell. Biol. 19, 7203–15.CrossRefGoogle ScholarPubMed
Pfaffl, M.W., Horgan, G.W. & Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.CrossRefGoogle Scholar
Rappolee, D.A., Sturm, K.S., Behrendtsen, O., Schultz, G.A., Pedersen, R.A. & Werb, Z. (1992). Insulin-like growth factor-Ii acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. Genes Dev. 6, 939–52.CrossRefGoogle ScholarPubMed
Robert, C., McGraw, S., Massicotte, L., Pravetoni, M., Gandolfi, F. & Sirard, M.A. (2002). Quantification of housekeeping transcript levels during the development of bovine preimplantation embryos. Biol. Reprod. 67, 1465–72.CrossRefGoogle ScholarPubMed
Shao, W.J., Tao, L.Y., Gao, C., Xie, J.Y. & Zhao, R.Q. (2008). Alterations in methylation and expression levels of imprinted genes H19 and Igf2 in the fetuses of diabetic mice. Comp. Med. 58, 341–6.Google ScholarPubMed
Sibley, C.P., Coan, P.M., Ferguson-Smith, A.C., Dean, W., Hughes, J., Smith, P., Reik, W., Burton, G.J., Fowden, A.L. & Constancia, M. (2004). Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc. Natl. Acad. Sci. USA 101, 8204–8.CrossRefGoogle ScholarPubMed
Su, J.M., Yang, B., Wang, Y.S., Li, Y.Y., Xiong, X.R., Wang, L.J., Guo, Z.K. & Zhang, Y. (2011). Expression and methylation status of imprinted genes in placentas of deceased and live cloned transgenic calves. Theriogenology 75, 1346–59.CrossRefGoogle ScholarPubMed
Vigneault, C., Gilbert, I., Sirard, M.A. & Robert, C. (2007). Using the histone H2a transcript as an endogenous standard to study relative transcript abundance during bovine early development. Mol. Reprod. Dev. 74, 703–15.CrossRefGoogle ScholarPubMed
Vincent, A.M. & Feldman, E.L. (2002). Control of cell survival by IGF signaling pathways. Growth Horm. IGF Res. 12, 193–7.CrossRefGoogle ScholarPubMed
Wang, L.M., Feng, H.L., Ma, Y., Cang, M., Li, H.J., Yan, Z., Zhou, P., Wen, J.X., Bou, S. & Liu, D.J. (2009). Expression of IGF receptors and its ligands in bovine oocytes and preimplantation embryos. Anim. Reprod. Sci. 114, 99108.CrossRefGoogle ScholarPubMed
Warzych, E., Wrenzycki, C., Peippo, J. & Lechniak, D. (2007). Maturation medium supplements affect transcript level of apoptosis and cell survival related genes in bovine blastocysts produced in vitro. Mol. Reprod. Dev. 74, 280–9.CrossRefGoogle ScholarPubMed
Willis, S.N., Chen, L., Dewson, G., Wei, A., Naik, E., Fletcher, J.I., Adams, J.M. & Huang, D.C. (2005). Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 19, 1294–305.CrossRefGoogle Scholar
Wu, Q., Ohsako, S., Ishimura, R., Suzuki, J.S. & Tohyama, C. (2004). Exposure of mouse preimplantation embryos to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol. Reprod. 70, 1790–7.CrossRefGoogle ScholarPubMed
Yadav, A., Singh, K.P., Singh, M.K., Saini, N., Palta, P., Manik, R.S., Singla, S.K., Upadhyay, R.C. & Chauhan, M.S. (2013). Effect of physiologically relevant heat shock on development apoptosis and expression of some genes in buffalo (Bubalus bubalis) embryos produced in vitro. Reprod. Domest. Anim. 48, 858–65.CrossRefGoogle ScholarPubMed
Yaseen, M.A., Wrenzycki, C., Herrmann, D., Carnwath, J.W. & Niemann, H. (2001). Changes in the relative abundance of mRNA transcripts for insulin-like growth factor (IGF-I and IGF-II) ligands and their receptors (IGF-IR/IGF-IIR) in preimplantation bovine embryos derived from different in vitro systems. Reproduction 122, 601–10.CrossRefGoogle ScholarPubMed
Zi, X.D., Yin, R.H., Chen, S.W., Liang, G.N., Zhang, D.W. & Guo, C.H. (2009). Developmental competence of embryos derived from reciprocal in vitro fertilization between yak (Bos grunniens) and cattle (Bos taurus). J. Reprod. Dev. 55, 480–83.CrossRefGoogle ScholarPubMed