Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
REVIEW

Molecular and cellular programs underlying the development of bovine pre-implantation embryos

Zongliang Jiang https://orcid.org/0000-0002-3040-7771 A *
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences, Genetics Institute, University of Florida, Gainesville, FL 32610, USA.

* Correspondence to: z.jiang1@ufl.edu

Reproduction, Fertility and Development 36(2) 34-42 https://doi.org/10.1071/RD23146

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the IETS

Abstract

Early embryonic mortality is a major cause of infertility in cattle, yet the underlying molecular causes remain a mystery. Over the past half century, assisted reproductive technologies such as in vitro fertilisation and somatic cell nuclear transfer have been used to improve cattle reproductive efficiency; however, reduced embryo developmental potential is seen compared to their in vivo counterparts. Recent years have seen exciting progress across bovine embryo research, including genomic profiling of embryogenesis, new methods for improving embryo competence, and experimenting on building bovine embryos from stem cell cultures. These advances are beginning to define bovine embryo molecular and cellular programs and could potentially lead to improved embryo health. Here, I highlight the current status of molecular determinants and cellular programs of bovine embryo development and new opportunities to improve the bovine embryo health.

Keywords: blastoid, bovine, embryonic stem cells, epigenetic modification, gene expression, pre-implantation embryo, trophoblast stem cells.

References

Acosta DAV, Denicol AC, Tribulo P, Rivelli MI, Skenandore C, Zhou Z, Luchini D, Correa MN, Hansen PJ, Cardoso FC (2016) Effects of rumen-protected methionine and choline supplementation on the preimplantation embryo in Holstein cows. Theriogenology 85, 1669-1679 PMID:.
| Crossref | Google Scholar | PubMed |

Ashworth CJ, Toma LM, Hunter MG (2009) Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 3351-3361 PMID:.
| Crossref | Google Scholar | PubMed |

Banliat C, Mahe C, Lavigne R, Com E, Pineau C, Labas V, Guyonnet B, Mermillod P, Saint-Dizier M (2022a) Dynamic changes in the proteome of early bovine embryos developed in vivo. Frontiers in Cell and Developmental Biology 10, 863700 PMID:.
| Crossref | Google Scholar | PubMed |

Banliat C, Mahe C, Lavigne R, Com E, Pineau C, Labas V, Guyonnet B, Mermillod P, Saint-Dizier M (2022b) The proteomic analysis of bovine embryos developed in vivo or in vitro reveals the contribution of the maternal environment to early embryo. BMC Genomics 23, 839 PMID:.
| Crossref | Google Scholar | PubMed |

Bogliotti YS, Wu J, Vilarino M, Okamura D, Soto DA, Zhong C, Sakurai M, Sampaio RV, Suzuki K, Izpisua Belmonte JC, Ross PJ (2018) Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts. Proceedings of the National Academy of Sciences of the United States of America 115, 2090-2095 PMID:.
| Crossref | Google Scholar | PubMed |

Bourc’his D, Le Bourhis D, Patin D, Niveleau A, Comizzoli P, Renard J-P, Viegas-Pequignot E (2001) Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos. Current Biology 11, 1542-1546 PMID:.
| Crossref | Google Scholar | PubMed |

Canovas S, Cibelli JB, Ross PJ (2012) Jumonji domain-containing protein 3 regulates histone 3 lysine 27 methylation during bovine preimplantation development. Proceedings of the National Academy of Sciences of the United States of America 109, 2400-2405 PMID:.
| Crossref | Google Scholar | PubMed |

Chen JC, Alvarez MJ, Talos F, Dhruv H, Rieckhof GE, Iyer A, Diefes KL, Aldape K, Berens M, Shen MM, Califano A (2014) Identification of causal genetic drivers of human disease through systems-level analysis of regulatory networks. Cell 159, 402-414 PMID:.
| Crossref | Google Scholar | PubMed |

Chung N, Bogliotti YS, Ding W, Vilarino M, Takahashi K, Chitwood JL, Schultz RM, Ross PJ (2017) Active H3K27me3 demethylation by KDM6B is required for normal development of bovine preimplantation embryos. Epigenetics 12, 1048-1056 PMID:.
| Crossref | Google Scholar | PubMed |

Cuthbert JM, Russell SJ, White KL, Benninghoff AD (2019) The maternal-to-zygotic transition in bovine in vitro-fertilized embryos is associated with marked changes in small non-coding RNAs. Biology of Reproduction 100, 331-350 PMID:.
| Crossref | Google Scholar | PubMed |

Cuthbert JM, Russell SJ, Polejaeva IA, Meng Q, White KL, Benninghoff AD (2021a) Dynamics of small non-coding RNAs in bovine scNT embryos through the maternal-to-embryonic transition. Biology of Reproduction 105, 918-933 PMID:.
| Crossref | Google Scholar | PubMed |

Cuthbert JM, Russell SJ, Polejaeva IA, Meng Q, White KL, Benninghoff AD (2021b) Comparing mRNA and sncRNA profiles during the maternal-to-embryonic transition in bovine IVF and scNT embryos. Biology of Reproduction 105, 1401-1415 PMID:.
| Crossref | Google Scholar | PubMed |

Daigneault BW (2021) Dynamics of paternal contributions to early embryo development in large animals. Biology of Reproduction 104, 274-281 PMID:.
| Crossref | Google Scholar | PubMed |

Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf E, Reik W (2001) Conservation of methylation reprogramming in mammalian development: Aberrant reprogramming in cloned embryos. Proceedings of the National Academy of Sciences of the United States of America 98, 13734-13738 PMID:.
| Crossref | Google Scholar | PubMed |

De Iaco A, Planet E, Coluccio A, Verp S, Duc J, Trono D (2017) DUX-family transcription factors regulate zygotic genome activation in placental mammals. Nature Genetics 49, 941-945 PMID:.
| Crossref | Google Scholar | PubMed |

Demant M, Deutsch DR, Frohlich T, Wolf E, Arnold GJ (2015) Proteome analysis of early lineage specification in bovine embryos. Proteomics 15, 688-701 PMID:.
| Crossref | Google Scholar | PubMed |

Deutsch DR, Frohlich T, Otte KA, Beck A, Habermann FA, Wolf E, Arnold GJ (2014) Stage-specific proteome signatures in early bovine embryo development. Journal of Proteome Research 13, 4363-4376 PMID:.
| Crossref | Google Scholar | PubMed |

Driver AM, Penagaricano F, Huang W, Ahmad KR, Hackbart KS, Wiltbank MC, Khatib H (2012) RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo- and in vitro-derived bovine blastocysts. BMC Genomics 13, 118 PMID:.
| Crossref | Google Scholar | PubMed |

Duan JE, Jiang ZC, Alqahtani F, Mandoiu I, Dong H, Zheng X, Marjani SL, Chen J, Tian XC (2019) Methylome dynamics of bovine gametes and in vivo early embryos. Frontiers in Genetics 10, 512 PMID:.
| Crossref | Google Scholar | PubMed |

Estrada-Cortes E, Negron-Perez VM, Tribulo P, Zenobi MG, Staples CR, Hansen PJ (2020) Effects of choline on the phenotype of the cultured bovine preimplantation embryo. Journal of Dairy Science 103, 10784-10796 PMID:.
| Crossref | Google Scholar | PubMed |

Estrada-Cortes E, Ortiz W, Rabaglino MB, Block J, Rae O, Jannaman EA, Xiao Y, Hansen PJ (2021) Choline acts during preimplantation development of the bovine embryo to program postnatal growth and alter muscle DNA methylation. The FASEB Journal 35, e21926 PMID:.
| Crossref | Google Scholar | PubMed |

Goel P, Malpotra S, Shyam S, Kumar D, Singh MK, Palta P (2022) Global microRNA expression profiling of buffalo (Bubalus bubalis) embryos at different developmental stages produced by somatic cell nuclear transfer and in-vitro fertilization using RNA sequencing. Genes 13, 453.
| Crossref | Google Scholar |

Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E (2014) Fine mapping of genome activation in bovine embryos by RNA sequencing. Proceedings of the National Academy of Sciences of the United States of America 111, 4139-4144 PMID:.
| Crossref | Google Scholar | PubMed |

Gutiérrez-adán A, Rizos D, Fair T, Moreira PN, Pintado B, de la Fuente J, Boland MP, Lonergan P (2004) Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro. Molecular Reproduction and Development 68, 441-448 PMID:.
| Crossref | Google Scholar | PubMed |

Gutierrez-Castillo E, Ming H, Foster B, Gatenby L, Mak CK, Pinto C, Bondioli K, Jiang Z (2021) Effect of vitrification on global gene expression dynamics of bovine elongating embryos. Reproduction, Fertility and Development 33, 338-348 PMID:.
| Crossref | Google Scholar | PubMed |

Halstead MM, Ma X, Zhou C, Schultz RM, Ross PJ (2020) Chromatin remodeling in bovine embryos indicates species-specific regulation of genome activation. Nature Communications 11, 4654 PMID:.
| Crossref | Google Scholar | PubMed |

Han YM, Kang YK, Koo DB, Lee KK (2003) Nuclear reprogramming of cloned embryos produced in vitro. Theriogenology 59, 33-44 PMID:.
| Crossref | Google Scholar | PubMed |

Hansen PJ, Dobbs KB, Denicol AC, Siqueira LGB (2016) Sex and the preimplantation embryo: implications of sexual dimorphism in the preimplantation period for maternal programming of embryonic development. Cell and Tissue Research 363, 237-247 PMID:.
| Crossref | Google Scholar | PubMed |

Herrmann D, Dahl JA, Lucas-Hahn A, Collas P, Niemann H (2013) Histone modifications and mRNA expression in the inner cell mass and trophectoderm of bovine blastocysts. Epigenetics 8, 281-289 PMID:.
| Crossref | Google Scholar | PubMed |

Jiang Z, Sun J, Dong H, Luo O, Zheng X, Obergfell C, Tang Y, Bi J, O’Neill R, Ruan Y, Chen J, Tian XC (2014) Transcriptional profiles of bovine in vivo pre-implantation development. BMC Genomics 15, 756 PMID:.
| Crossref | Google Scholar | PubMed |

Jiang Z, Harrington P, Zhang M, Marjani SL, Park J, Kuo L, Pribenszky C, Tian XC (2016) Effects of high hydrostatic pressure on expression profiles of in vitro produced vitrified bovine blastocysts. Scientific Reports 6, 21215 PMID:.
| Crossref | Google Scholar | PubMed |

Jiang Z, Lin J, Dong H, Zheng X, Marjani SL, Duan J, Ouyang Z, Chen J, Tian XC (2018) DNA methylomes of bovine gametes and in vivo produced preimplantation embryos. Biology of Reproduction 99, 949-959 PMID:.
| Crossref | Google Scholar | PubMed |

Jin L, Guo Q, Zhu H-Y, Xing X-X, Zhang G-L, Xuan M-F, Luo Q-R, Luo Z-B, Wang J-X, Yin X-J, Kang J-D (2017) Quisinostat treatment improves histone acetylation and developmental competence of porcine somatic cell nuclear transfer embryos. Molecular Reproduction and Development 84, 340-346 PMID:.
| Crossref | Google Scholar | PubMed |

Kang Y-K, Park JS, Koo D-B, Choi Y-H, Kim S-U, Lee K-K, Han Y-M (2002) Limited demethylation leaves mosaic-type methylation states in cloned bovine pre-implantation embryos. The EMBO Journal 21, 1092-1100 PMID:.
| Crossref | Google Scholar | PubMed |

Kannampuzha-Francis J, Denicol AC, Loureiro B, Kaniyamattam K, Ortega MS, Hansen PJ (2015) Exposure to colony stimulating factor 2 during preimplantation development increases postnatal growth in cattle. Molecular Reproduction and Development 82, 892-897 PMID:.
| Crossref | Google Scholar | PubMed |

Kues WA, Sudheer S, Herrmann D, Carnwath JW, 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. Proceedings of the National Academy of Sciences of the United States of America 105, 19768-19773 PMID:.
| Crossref | Google Scholar | PubMed |

Lan X, Cretney EC, Kropp J, Khateeb K, Berg MA, Penagaricano F, Magness R, Radunz AE, Khatib H (2013) Maternal diet during pregnancy induces gene expression and DNA methylation changes in fetal tissues in sheep. Frontiers in Genetics 4, 49 PMID:.
| Crossref | Google Scholar | PubMed |

Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559 PMID:.
| Crossref | Google Scholar | PubMed |

Lavagi I, Krebs S, Simmet K, Beck A, Zakhartchenko V, Wolf E, Blum H (2018) Single-cell RNA sequencing reveals developmental heterogeneity of blastomeres during major genome activation in bovine embryos. Scientific Reports 8, 4071 PMID:.
| Crossref | Google Scholar | PubMed |

Lee MT, Bonneau AR, Takacs CM, Bazzini AA, DiVito KR, Fleming ES, Giraldez AJ (2013) Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. Nature 503, 360-364 PMID:.
| Crossref | Google Scholar | PubMed |

Lepikhov K, Zakhartchenko V, Hao R, Yang F, Wrenzycki C, Niemann H, Wolf E, Walter J (2008) Evidence for conserved DNA and histone H3 methylation reprogramming in mouse, bovine and rabbit zygotes. Epigenetics & Chromatin 1, 8 PMID:.
| Crossref | Google Scholar | PubMed |

Liang H-L, Nien C-Y, Liu H-Y, Metzstein MM, Kirov N, Rushlow C (2008) The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456, 400-403 PMID:.
| Crossref | Google Scholar | PubMed |

Liu X, Wang Y, Gao Y, Su J, Zhang J, Xing X, Zhou C, Yao K, An Q, Zhang Y (2018) H3K9 demethylase KDM4E is an epigenetic regulator for bovine embryonic development and a defective factor for nuclear reprogramming. Development (Cambridge, England) 145, dev158261.
| Crossref | Google Scholar |

Lonergan P, Rizos D, Gutierrez-Adan A, Moreira PM, Pintado B, de la Fuente J, Boland MP (2003) Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biology of Reproduction 69, 1424-1431 PMID:.
| Crossref | Google Scholar | PubMed |

Lu X, Zhang Y, Wang L, Wang L, Wang H, Xu Q, Xiang Y, Chen C, Kong F, Xia W, Lin Z, Ma S, Liu L, Wang X, Ni H, Li W, Guo Y, Xie W (2021) Evolutionary epigenomic analyses in mammalian early embryos reveal species-specific innovations and conserved principles of imprinting. Science Advances 7, eabi6178.
| Crossref | Google Scholar |

Memili E, First NL (1998) Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of α-amanitin on embryo development. Molecular Reproduction and Development 51, 381-389 PMID:.
| Crossref | Google Scholar | PubMed |

Ming H, Sun J, Pasquariello R, Gatenby L, Herrick JR, Yuan Y, Pinto CR, Bondioli KR, Krisher RL, Jiang Z (2021) The landscape of accessible chromatin in bovine oocytes and early embryos. Epigenetics 16, 300-312 PMID:.
| Crossref | Google Scholar | PubMed |

Misirlioglu M, Page GP, Sagirkaya H, Kaya A, Parrish JJ, First NL, Memili E (2006) Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proceedings of the National Academy of Sciences of the United States of America 103, 18905-18910 PMID:.
| Crossref | Google Scholar | PubMed |

Morgan HL, Eid N, Khoshkerdar A, Watkins AJ (2020) Defining the male contribution to embryo quality and offspring health in assisted reproduction in farm animals. Animal Reproduction 17, e20200018 PMID:.
| Crossref | Google Scholar | PubMed |

Niemann H, Carnwath JW, Herrmann D, Wieczorek G, Lemme E, Lucas-Hahn A, Olek S (2010) DNA methylation patterns reflect epigenetic reprogramming in bovine embryos. Cellular Reprogramming 12, 33-42 PMID:.
| Crossref | Google Scholar | PubMed |

Org T, Hensen K, Kreevan R, Mark E, Sarv O, Andreson R, Jaakma U, Salumets A, Kurg A (2019) Genome-wide histone modification profiling of inner cell mass and trophectoderm of bovine blastocysts by RAT-ChIP. PLoS ONE 14, e0225801 PMID:.
| Crossref | Google Scholar | PubMed |

Paulson EE, Fishman EL, Schultz RM, Ross PJ (2022) Embryonic microRNAs are essential for bovine preimplantation embryo development. Proceedings of the National Academy of Sciences of the United States of America 119, e2212942119 PMID:.
| Crossref | Google Scholar | PubMed |

Peat JR, Reik W (2012) Incomplete methylation reprogramming in SCNT embryos. Nature Genetics 44, 965-966 PMID:.
| Crossref | Google Scholar | PubMed |

Pillai VV, Siqueira LG, Das M, Kei TG, Tu LN, Herren AW, Phinney BS, Cheong SH, Hansen PJ, Selvaraj V (2019) Physiological profile of undifferentiated bovine blastocyst-derived trophoblasts. Biology Open 8, bio037937.
| Crossref | Google Scholar |

Pinzon-Arteaga CA, Wang Y, Wei Y, Ribeiro Orsi AE, Li L, Scatolin G, Liu L, Sakurai M, Ye J, Hao M, Yu L, Li B, Jiang Z, Wu J (2023) Bovine blastocyst-like structures derived from stem cell cultures. Cell Stem Cell 30, 611-616.e7 PMID:.
| Crossref | Google Scholar | PubMed |

Rabaglino MB, Salilew-Wondim D, Zolini A, Tesfaye D, Hoelker M, Lonergan P, Hansen PJ (2023) Machine-learning methods applied to integrated transcriptomic data from bovine blastocysts and elongating conceptuses to identify genes predictive of embryonic competence. The FASEB Journal 37, e22809 PMID:.
| Crossref | Google Scholar | PubMed |

Reis e Silva AR, Bruno C, Fleurot R, Daniel N, Archilla C, Peynot N, Lucci CM, Beaujean N, Duranthon V (2012) Alteration of DNA demethylation dynamics by in vitro culture conditions in rabbit pre-implantation embryos. Epigenetics 7, 440-446.
| Crossref | Google Scholar |

Reynolds LP, Diniz WJS, Crouse MS, Caton JS, Dahlen CR, Borowicz PP, Ward AK (2023) Maternal nutrition and developmental programming of offspring. Reproduction, Fertility and Development 35, 19-26.
| Crossref | Google Scholar |

Ross PJ, Ragina NP, Rodriguez RM, Iager AE, Siripattarapravat K, Lopez-Corrales N, Cibelli JB (2008) Polycomb gene expression and histone H3 lysine 27 trimethylation changes during bovine preimplantation development. Reproduction 136, 777-785 PMID:.
| Crossref | Google Scholar | PubMed |

Salilew-Wondim D, Fournier E, Hoelker M, Saeed-Zidane M, Tholen E, Looft C, Neuhoff C, Besenfelder U, Havlicek V, Rings F, Gagne D, Sirard M-A, Robert C, Shojaei Saadi HA, Gad A, Schellander K, Tesfaye D (2015) Genome-wide DNA methylation patterns of bovine blastocysts developed in vivo from embryos completed different stages of development in vitro. PLoS ONE 10, e0140467 PMID:.
| Crossref | Google Scholar | PubMed |

Salilew-Wondim D, Saeed-Zidane M, Hoelker M, Gebremedhn S, Poirier M, Pandey HO, Tholen E, Neuhoff C, Held E, Besenfelder U, Havlicek V, Rings F, Fournier E, Gagne D, Sirard M-A, Robert C, Gad A, Schellander K, Tesfaye D (2018) Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation. BMC Genomics 19, 424 PMID:.
| Crossref | Google Scholar | PubMed |

Santos F, Zakhartchenko V, Stojkovic M, Peters A, Jenuwein T, Wolf E, Reik W, Dean W (2003) Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Current Biology 13, 1116-1121 PMID:.
| Crossref | Google Scholar | PubMed |

Sawai K, Takahashi M, Moriyasu S, Hirayama H, Minamihashi A, Hashizume T, Onoe S (2010) Changes in the DNA methylation status of bovine embryos from the blastocyst to elongated stage derived from somatic cell nuclear transfer. Cellular Reprogramming 12, 15-22 PMID:.
| Crossref | Google Scholar | PubMed |

Schulz KN, Bondra ER, Moshe A, Villalta JE, Lieb JD, Kaplan T, McKay DJ, Harrison MM (2015) Zelda is differentially required for chromatin accessibility, transcription factor binding, and gene expression in the early Drosophila embryo. Genome Research 25, 1715-1726 PMID:.
| Crossref | Google Scholar | PubMed |

Shimada A, Nakano H, Takahashi T, Imai K, Hashizume K (2001) Isolation and characterization of a bovine blastocyst-derived trophoblastic cell line, BT-1: development of a culture system in the absence of feeder cell. Placenta 22, 652-662 PMID:.
| Crossref | Google Scholar | PubMed |

Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, Thurston A, Huntley JF, Rees WD, Maloney CA, Lea RG, Craigon J, McEvoy TG, Young LE (2007) DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proceedings of the National Academy of Sciences of the United States of America 104, 19351-19356 PMID:.
| Crossref | Google Scholar | PubMed |

Sinclair KD, Rutherford KMD, Wallace JM, Brameld JM, Stoger R, Alberio R, Sweetman D, Gardner DS, Perry VEA, Adam CL, Ashworth CJ, Robinson JE, Dwyer CM (2016) Epigenetics and developmental programming of welfare and production traits in farm animals. Reproduction, Fertility and Development 28(10), 1443-1478.
| Crossref | Google Scholar |

Siqueira LG, Tribulo P, Chen Z, Denicol AC, Ortega MS, Negron-Perez VM, Kannampuzha-Francis J, Pohler KG, Rivera RM, Hansen PJ (2017) Colony-stimulating factor 2 acts from days 5 to 7 of development to modify programming of the bovine conceptus at day 86 of gestationdagger. Biology of Reproduction 96, 743-757 PMID:.
| Crossref | Google Scholar | PubMed |

Sirard M-A (2017) The influence of in vitro fertilization and embryo culture on the embryo epigenetic constituents and the possible consequences in the bovine model. Journal of Developmental Origins of Health and Disease 8, 411-417 PMID:.
| Crossref | Google Scholar | PubMed |

Sirard M-A (2021) How the environment affects early embryonic development. Reproduction, Fertility and Development 34, 203-213 PMID:.
| Crossref | Google Scholar | PubMed |

Smallwood SA, Lee HJ, Angermueller C, Krueger F, Saadeh H, Peat J, Andrews SR, Stegle O, Reik W, Kelsey G (2014) Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nature Methods 11, 817-820 PMID:.
| Crossref | Google Scholar | PubMed |

Smith SL, Everts RE, Tian XC, Du F, Sung L-Y, Rodriguez-Zas SL, Jeong B-S, Renard J-P, Lewin HA, Yang X (2005) Global gene expression profiles reveal significant nuclear reprogramming by the blastocyst stage after cloning. Proceedings of the National Academy of Sciences of the United States of America 102, 17582-17587 PMID:.
| Crossref | Google Scholar | PubMed |

Smith LC, Therrien J, Filion F, Bressan F, Meirelles FV (2015) Epigenetic consequences of artificial reproductive technologies to the bovine imprinted genes SNRPN, H19/IGF2, and IGF2R. Frontiers in Genetics 6, 58 PMID:.
| Crossref | Google Scholar | PubMed |

Sun J, Jiang Z, Tian X, Bi J (2016) A cross-species bi-clustering approach to identifying conserved co-regulated genes. Bioinformatics 32, i137-i146 PMID:.
| Crossref | Google Scholar | PubMed |

Talbot NC, Caperna TJ, Edwards JL, Garrett W, Wells KD, Ealy AD (2000) Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon tau and transferrin expression as respective in vitro markers. Biology of Reproduction 62, 235-247 PMID:.
| Crossref | Google Scholar | PubMed |

Telford NA, Watson AJ, Schultz GA (1990) Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Molecular Reproduction and Development 26, 90-100 PMID:.
| Crossref | Google Scholar | PubMed |

The Bovine Genome Sequencing and Analysis Consortium, Analysis C, Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, Weinstock GM, Adelson DL, Eichler EE, Elnitski L, Guigo R, Hamernik DL, Kappes SM, Lewin HA, Lynn DJ, Nicholas FW, Reymond A, Rijnkels M, Skow LC, Zdobnov EM, Schook L, Womack J, Alioto T, Antonarakis SE, Astashyn A, Chapple CE, Chen H-C, Chrast J, Camara F, Ermolaeva O, Henrichsen CN, Hlavina W, Kapustin Y, Kiryutin B, Kitts P, Kokocinski F, Landrum M, Maglott D, Pruitt K, Sapojnikov V, Searle SM, Solovyev V, Souvorov A, Ucla C, Wyss C, Anzola JM, Gerlach D, Elhaik E, Graur D, Reese JT, Edgar RC, Mcewan JC, Payne GM, Raison JM, Junier T, Kriventseva EV, Eyras E, Plass M, Donthu R, Larkin DM, Reecy J, Yang MQ, Chen L, Cheng Z, Chitko-McKown CG, Liu GE, Matukumalli LK, Song J, Zhu B, Bradley DG, Brinkman FSL, Lau LPL, Whiteside MD, Walker A, Wheeler TT, Casey T, German JB, Lemay DG, Maqbool NJ, Molenaar AJ, Seo S, Stothard P, Baldwin CL, Baxter R, Brinkmeyer-Langford CL, Brown WC, Childers CP, Connelley T, Ellis SA, Fritz K, Glass EJ, Herzig CTA, Iivanainen A, Lahmers KK, Bennett AK, Dickens CM, Gilbert JGR, Hagen DE, Salih H, et al. (2009) The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324, 522-528.
| Crossref | Google Scholar |

Tribulo P, Leao BCdS, Lehloenya KC, Mingoti GZ, Hansen PJ (2017) Consequences of endogenous and exogenous WNT signaling for development of the preimplantation bovine embryo. Biology of Reproduction 96, 1129-1141 PMID:.
| Crossref | Google Scholar | PubMed |

Tribulo P, Rabaglino MB, Bo MB, Carvalheira LdR, Bishop JV, Hansen TR, Hansen PJ (2019) Dickkopf-related protein 1 is a progestomedin acting on the bovine embryo during the morula-to-blastocyst transition to program trophoblast elongation. Scientific Reports 9, 11816 PMID:.
| Crossref | Google Scholar | PubMed |

Viana J (2023) 2021 Statistics of embryo production and transfer in domestic farm animals. Embryo Technology Newsletter 40(4), 2022.
| Google Scholar |

Wang Y, Ming H, Yu L, Li J, Zhu L, Sun H-X, Pinzon-Arteaga CA, Wu J, Jiang Z (2023) Establishment of bovine trophoblast stem cells. Cell Reports 42, 112439.
| Crossref | Google Scholar |

Wrenzycki C, Herrmann D, Lucas-Hahn A, Korsawe K, Lemme E, Niemann H (2005) Messenger RNA expression patterns in bovine embryos derived from in vitro procedures and their implications for development. Reproduction, Fertility and Development 17, 23-35 PMID:.
| Crossref | Google Scholar | PubMed |

Wu C, Sirard M-A (2020) Parental effects on epigenetic programming in gametes and embryos of dairy cows. Frontiers in Genetics 11, 557846 PMID:.
| Crossref | Google Scholar | PubMed |

Wu X, Li Y, Xue L, Wang L, Yue Y, Li K, Bou S, Li G-P, Yu H (2011) Multiple histone site epigenetic modifications in nuclear transfer and in vitro fertilized bovine embryos. Zygote 19, 31-45 PMID:.
| Crossref | Google Scholar | PubMed |

Zhang S, Chen X, Wang F, An X, Tang B, Zhang X, Sun L, Li Z (2016) Aberrant DNA methylation reprogramming in bovine SCNT preimplantation embryos. Scientific Reports 6, 30345 PMID:.
| Crossref | Google Scholar | PubMed |

Zhang J, Qu P, Zhou C, Liu X, Ma X, Wang M, Wang Y, Su J, Liu J, Zhang Y (2017) MicroRNA-125b is a key epigenetic regulatory factor that promotes nuclear transfer reprogramming. Journal of Biological Chemistry 292, 15916-15926 PMID:.
| Crossref | Google Scholar | PubMed |

Zhao Y-H, Wang J-J, Zhang P-P, Hao H-S, Pang Y-W, Wang H-Y, Du W-H, Zhao S-J, Ruan W-M, Zou H-Y, Hao T, Zhu H-B, Zhao X-M (2020) Oocyte IVM or vitrification significantly impairs DNA methylation patterns in blastocysts as analysed by single-cell whole-genome methylation sequencing. Reproduction, Fertility and Development 32, 676-689.
| Crossref | Google Scholar |

Zhao L, Gao X, Zheng Y, Wang Z, Zhao G, Ren J, Zhang J, Wu J, Wu B, Chen Y, Sun W, Li Y, Su J, Ding Y, Gao Y, Liu M, Bai X, Sun L, Cao G, Tang F, Bao S, Liu P, Li X (2021) Establishment of bovine expanded potential stem cells. Proceedings of the National Academy of Sciences of the United States of America 118, e2018505118.
| Crossref | Google Scholar |

Zhou C, Halstead MM, Bonnet-Garnier A, Schultz RM, Ross PJ (2023) Histone remodeling reflects conserved mechanisms of bovine and human preimplantation development. EMBO Reports 24, e55726 PMID:.
| Crossref | Google Scholar | PubMed |

Zhu L, Marjani SL, Jiang Z (2021) The epigenetics of gametes and early embryos and potential long-range consequences in livestock species – filling in the picture with epigenomic analyses. Frontiers in Genetics 12, 557934 PMID:.
| Crossref | Google Scholar | PubMed |

Zhu L, Zhou T, Iyyappan R, Ming H, Dvoran M, Wang Y, Chen Q, Roberts RM, Susor A, Jiang Z (2022) High-resolution ribosome profiling reveals translational selectivity for transcripts in bovine preimplantation embryo development. Development (Cambridge, England) 149, dev200819.
| Crossref | Google Scholar |