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

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.

[1]  K. Kikuchi,et al.  Developmental Competence of Early Stage Porcine Embryos Cultured in Medium with Different Energy Substrate in vitro , 2015 .

[2]  R. Bashir,et al.  Growth Factors , 1996 .

[3]  C. Ricordi,et al.  Influence of In Vitro and In Vivo Oxygen Modulation on β Cell Differentiation From Human Embryonic Stem Cells , 2014, Stem cells translational medicine.

[4]  M. K. Singh,et al.  Effect of physiologically relevant heat shock on development, apoptosis and expression of some genes in buffalo (Bubalus bubalis) embryos produced in vitro. , 2013, Reproduction in domestic animals = Zuchthygiene.

[5]  Zhou Lin-ya.  Expression and methylation of ABCG2 gene in gastric carcinoma , 2013 .

[6]  D. Carrell,et al.  The sperm epigenome and potential implications for the developing embryo. , 2012, Reproduction.

[7]  J. Segars,et al.  Environmental and epigenetic effects upon preimplantation embryo metabolism and development , 2011, Trends in Endocrinology & Metabolism.

[8]  R. Duchi,et al.  Embryonic genotype and inbreeding affect preimplantation development in cattle. , 2011, Reproduction.

[9]  Zekun Guo,et al.  Expression and methylation status of imprinted genes in placentas of deceased and live cloned transgenic calves. , 2011, Theriogenology.

[10]  R. Thallman,et al.  Birth and weaning traits in crossbred cattle from Hereford, Angus, Brahman, Boran, Tuli, and Belgian Blue sires. , 2011, Journal of animal science.

[11]  D. Carrell,et al.  The paternal epigenome and embryogenesis: poising mechanisms for development. , 2011, Asian journal of andrology.

[12]  A. Feinberg,et al.  Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease , 2010, Proceedings of the National Academy of Sciences.

[13]  H. Lehrach,et al.  DNA methylation in the IGF2 intragenic DMR is re-established in a sex-specific manner in bovine blastocysts after somatic cloning. , 2009, Genomics.

[14]  X. Zi,et al.  Developmental competence of embryos derived from reciprocal in vitro fertilization between Yak (Bos grunniens) and cattle (Bos taurus). , 2009, The Journal of reproduction and development.

[15]  L. Trinca,et al.  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. , 2009, Animal reproduction science.

[16]  Dongjun Liu,et al.  Expression of IGF receptors and its ligands in bovine oocytes and preimplantation embryos. , 2009, Animal reproduction science.

[17]  C. Ferreira,et al.  Imprinted gene expression in in vivo- and in vitro-produced bovine embryos and chorio-allantoic membranes. , 2009, Genetics and molecular research : GMR.

[18]  B. Yandell,et al.  Single gene and gene interaction effects on fertilization and embryonic survival rates in cattle. , 2009, Journal of dairy science.

[19]  A. Gutiérrez-Adán,et al.  Effects of oviductal fluid on the development, quality, and gene expression of porcine blastocysts produced in vitro. , 2009, Reproduction.

[20]  C. Sapienza,et al.  Hybrid Vigor and Transgenerational Epigenetic Effects on Early Mouse Embryo Phenotype1 , 2008, Biology of reproduction.

[21]  Wei-Juan Shao,et al.  Alterations in methylation and expression levels of imprinted genes H19 and Igf2 in the fetuses of diabetic mice. , 2008, Comparative medicine.

[22]  P. Schirmacher,et al.  Autocrine insulin‐like growth factor‐II stimulation of tumor cell migration is a progression step in human hepatocarcinogenesis , 2008, Hepatology.

[23]  Jennifer L. Farmer,et al.  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. , 2008, Endocrinology.

[24]  I. Hwang,et al.  Osmolarity at early culture stage affects development and expression of apoptosis related genes (bax‐α and bcl‐xl) in pre‐implantation porcine NT embryos , 2008, Molecular reproduction and development.

[25]  H. Niemann,et al.  Focus on Mammalian Embryogenomics Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning , 2008 .

[26]  P. Szabó,et al.  CTCF Is the Master Organizer of Domain-Wide Allele-Specific Chromatin at the H19/Igf2 Imprinted Region , 2007, Molecular and Cellular Biology.

[27]  X. Cui,et al.  Heat shock induces apoptosis related gene expression and apoptosis in porcine parthenotes developing in vitro. , 2007, Animal reproduction science.

[28]  C. Robert,et al.  Using the histone H2a transcript as an endogenous standard to study relative transcript abundance during bovine early development , 2007, Molecular reproduction and development.

[29]  G. Rho,et al.  Influence of in vitro oxygen concentrations on preimplantation embryo development, gene expression and production of hanwoo calves following embryo transfer , 2007, Molecular reproduction and development.

[30]  C. Wrenzycki,et al.  Maturation medium supplements affect transcript level of apoptosis and cell survival related genes in bovine blastocysts produced in vitro , 2007, Molecular reproduction and development.

[31]  A. Harvey,et al.  The role of oxygen in ruminant preimplantation embryo development and metabolism. , 2007, Animal reproduction science.

[32]  H. Lehrach,et al.  The bovine IGF2 gene is differentially methylated in oocyte and sperm DNA. , 2006, Genomics.

[33]  C. Osmond,et al.  Imprinted gene expression in the rat embryo-fetal axis is altered in response to periconceptional maternal low protein diet. , 2006, Reproduction.

[34]  J. Vasconcelos,et al.  Importance of sperm genotype (indicus versus taurus) for fertility and embryonic development at elevated temperatures. , 2006, Theriogenology.

[35]  Lin Chen,et al.  Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. , 2005, Genes & development.

[36]  R. Kurzawa,et al.  Growth factors effects on preimplantation development of mouse embryos exposed to tumor necrosis factor alpha. , 2005, Reproductive biology.

[37]  X. Cui,et al.  Haploidy influences Bak and Bcl-xL mRNA expression and increases incidence of apoptosis in porcine embryos , 2005, Zygote.

[38]  R. Kurzawa,et al.  Growth factors protect in vitro cultured embryos from the consequences of oxidative stress , 2004, Zygote.

[39]  James J. Chen,et al.  Analysis of variance components in gene expression data , 2004, Bioinform..

[40]  C. Tohyama,et al.  Exposure of Mouse Preimplantation Embryos to 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) Alters the Methylation Status of Imprinted Genes H19 and Igf21 , 2004, Biology of reproduction.

[41]  W. Reik,et al.  Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  S. Bilodeau-Goeseels,et al.  Factors affecting embryo survival and strategies to reduce embryonic mortality in cattle , 2003 .

[43]  A. Gutiérrez-Adán,et al.  Temporal Divergence in the Pattern of Messenger RNA Expression in Bovine Embryos Cultured from the Zygote to Blastocyst Stage In Vitro or In Vivo1 , 2003, Biology of reproduction.

[44]  P. Lonergan,et al.  Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. , 2003, Reproduction.

[45]  S. Schmutz,et al.  Linkage mapping of IGF2 on cattle chromosome 29. , 2003, Animal genetics.

[46]  S. McGraw,et al.  Quantification of Housekeeping Transcript Levels During the Development of Bovine Preimplantation Embryos1 , 2002, Biology of reproduction.

[47]  Eva L Feldman,et al.  Control of cell survival by IGF signaling pathways. , 2002, Growth hormone & IGF research : official journal of the Growth Hormone Research Society and the International IGF Research Society.

[48]  J. Southgate,et al.  Regulation of apoptosis in the bovine blastocyst by insulin and the insulin‐like growth factor (IGF) superfamily , 2002, Molecular Reproduction and Development.

[49]  W. Reik,et al.  Placental-specific IGF-II is a major modulator of placental and fetal growth , 2002, Nature.

[50]  G. Horgan,et al.  Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR , 2002 .

[51]  P. Hansen.  Embryonic mortality in cattle from the embryo's perspective , 2002 .

[52]  P. D. De Sousa,et al.  Sensitivity of bovine blastocyst gene expression patterns to culture environments assessed by differential display RT-PCR. , 2001, Reproduction.

[53]  C. Wrenzycki,et al.  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. , 2001, Reproduction.

[54]  W. Reik,et al.  Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. , 2001, Human reproduction update.

[55]  J. Rutledge,et al.  Estimates of heterosis for in vitro embryo production using reciprocal crosses in cattle. , 2000, Theriogenology.

[56]  S. Masters,et al.  14-3-3 proteins: structure, function, and regulation. , 2000, Annual review of pharmacology and toxicology.

[57]  B. Calabretta,et al.  Multiple Signaling Pathways of the Insulin-Like Growth Factor 1 Receptor in Protection from Apoptosis , 1999, Molecular and Cellular Biology.

[58]  T. Moore,et al.  Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes. , 1998, Development.

[59]  T. Ogihara,et al.  [Linkage mapping]. , 1996, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[60]  J. Macfarlane.  Embryonic mortality in cattle , 1994, Veterinary Record.

[61]  D. Rappolee,et al.  Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. , 1992, Genes & development.

[62]  N. Ayalon.  Embryonic mortality in cattle , 1981 .

[63]  H. C. Fryer,et al.  Nonreturn Rate of Artificially Inseminated Dairy Cows as Affected by Age of Semen, Breed of Bull, and Season , 1958 .