Abstract
Investigation of the role of epigenetics in cattle breeding is gaining importance. DNA methylation represents an epigenetic modification which is essential for genomic stability and maintenance of development. Recently, DNA methylation research in cattle has intensified. The studies focus on the definition of methylomes in various organs and tissues in relation to the expression of genes underlying economically important traits, and explore methylome changes under developmental, environmental, disease, and diet influences. The investigations further characterize the methylation patterns of gametes in connection with their quality, and study methylome alterations in the developing naturally or assisted produced zygotes, embryos, and fetuses, considering their viability. A wide array of technologies developed for accurate and precise analysis of DNA methylation patterns is employed for both single-gene and genome-wide studies. Overall, the research is directed towards the identification of single methylation markers or their combinations which may be useful in the selection and breeding of animals to ensure cattle improvement.
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Change history
02 March 2021
A Correction to this paper has been published: https://doi.org/10.1007/s13353-021-00622-7
References
Ahlawat S, Sharma R, Arora R et al (2019) Promoter methylation and expression analysis of Bvh gene in bulls with varying semen motility parameters. Theriogenology 125:152–156. https://doi.org/10.1016/j.theriogenology.2018.11.001
Akey DT, Akey JM, Zhang K, Jin L (2002) Assaying DNA methylation based on high-throughput melting curve approaches. Genomics 80(4):376e384
Alonso-González L, Couldrey C, Meinhardt MW et al (2012) Primary transgenic bovine cells and their rejuvenated cloned equivalents show transgene-specific epigenetic differences. PLoS ONE 7(4):e35619. https://doi.org/10.1371/journal.pone.0035619
Alves BRC, Cardoso RC, Doan R (2017) Nutritional programming of accelerated puberty in heifers: alterations in DNA methylation in the arcuate nucleus. Biol Reprod 96(1):174–184. https://doi.org/10.1095/biolreprod.116.144741
Bach A, Aris A, Guasch I (2017) Consequences of supplying methyl donors during pregnancy on the methylome of the offspring from lactating and non-lactating dairy cattle. PLoS ONE 12(12):e0189581. https://doi.org/10.1371/journal.pone.0189581
Baik M, Vu TTT, Piao MY et al (2014) Association of DNA methylation levels with tissue-specific expression of adipogenic and lipogenic genes in longissimus dorsi muscle of Korean cattle. Asian Austral J Anim 27(10):1493–1498. https://doi.org/10.5713/ajas.2014.14283
Barlow DP, Bartolomei MS (2014) Genomic imprinting in mammals. Cold Spring Harb Perspect Biol 6:a018382. https://doi.org/10.1101/cshperspect.a018382
Barrera AD, García EV, Hamdi M et al (2017) Embryo culture in presence of oviductal fluid induces DNA methylation changes in bovine blastocysts. Reproduction 154:1–12. https://doi.org/10.1530/REP-16-0651
Barrera AD, García EV, Miceli DC (2018) Effect of exogenous transforming growth factor β1 (TGF-β1) on early bovine embryo development. Zygote. 26(3):232–241. https://doi.org/10.1017/S096719941800014X
Bennemann J, Grothmann H, Wrenzycki C (2018) Reduced oxygen concentration during in vitro oocyte maturation alters global DNA methylation in the maternal pronucleus of subsequent zygotes in cattle. Mol Reprod Dev 85:849–857. https://doi.org/10.1002/mrd.23073
Bernstein BE, Meissner A, Lander ES (2007) The mammalian epigenome. Cell 128:669–681. https://doi.org/10.1016/j.cell.2007.01.033
Bird AP, Southern EM (1978) Use of restriction enzymes to study eukaryotic DNA methylation: I. The methylation pattern in ribosomal DNA from Xenopus laevis. J Mol Biol 118(1):27e47
Bomfim MM, Andrade GM, del Collado M et al (2017) Antioxidant responses and deregulation of epigenetic writers and erasers link oxidative stress and DNA methylation in bovine blastocysts. Mol Reprod Dev 84(12):1296–1305. https://doi.org/10.1002/mrd.22929
Boulougouris X, Rogiers C, Van Poucke M et al (2019) Methylation of selected CpG islands involved in the transcription of myeloperoxidase and superoxide dismutase 2 in neutrophils of periparturient and mid-lactation cows. J Dairy Sci 102(8):7421–7434. https://doi.org/10.3168/jds.2018-16027
Burri N, Chaubert P (1999) Complex methylation patterns analyzed by single-strand conformation polymorphism. Biotechniques 26(2):232e234
Carvalho JO, Michalczechen-Lacerda VA, Sartori R et al (2012) The methylation patterns of the IGF2 and IGF2R genes in bovine spermatozoa are not affected by flow-cytometric sex sorting. Mol Reprod Dev 79:77–84. https://doi.org/10.1002/mrd.21410
Chen Z, Chu S, Xu X et al (2019) Analysis of longissimus muscle quality characteristics and associations with DNA methylation status in cattle. Genes Genomics 41(10):1147–1163. https://doi.org/10.1007/s13258-019-00844-4
Cheow LF, Quake SR, Burkholder WF, Messerschmidt DM (2015) Multiplexed locus-specific analysis of DNA methylation in single cells. Nat Protoc 10(4):619e631
Choi S-W, Friso S (2010) Epigenetics: a new bridge between nutrition and health. Adv Nutr 1:8–16. https://doi.org/10.3945/an.110.1004
Clark SJ, Harrison J, Paul CL, Frommer M (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Res 22(15):2990e2997
Cottrell SE, Distler J, Goodman NS, Mooney SH, Kluth A, Olek A, Schwope I, Tetzner R, Ziebarth H, Berlin K (2004) A real-time PCR assay for DNA-methylation using methylation specific blockers. Nucleic Acids Res 32(1):e10
Couldrey C, Lee RSF (2010) DNA methylation patterns in tissues from mid-gestation bovine foetuses produced by somatic cell nuclear transfer show subtle abnormalities in nuclear reprogramming. BMC Dev Biol 10:27
Couldrey C, Brauning R, Retzel EF, McEwan JC (2012) Development of epigenomic pipelines for use in agricultural animals. P New Zealand Soc Anim Prod 72:163–165
Couldrey C, Wells DN (2013) DNA methylation at a bovine alpha satellite I repeat CpG site during development following fertilization and somatic cell nuclear transfer. PLoS One 8(2):e55153. https://doi.org/10.1371/journal.pone.0055153
Couldrey C, Cave V (2014) Assessing DNA methylation levels in animals: choosing the right tool for the job. Stichting Int Found Animal Genet 45(1):15–24. https://doi.org/10.1111/age.12186
Curchoe CL, Zhang S, Yang L et al (2009) Hypomethylation trends in the intergenic region of the imprinted IGF2 and H19 genes in cloned cattle. Anim Reprod Sci 116:213–225. https://doi.org/10.1016/j.anireprosci.2009.02.008
Davidović RS, Božović AM, Mandušić VLJ, Krajnović MM (2014) Methylation-specific PCR: four steps in primer design. Cent Eur J Biol 9(12):1127–1139. https://doi.org/10.2478/s11535-014-0324-z
Dechow CH, Liu W-S (2018) DNA methylation patterns in peripheral blood mononuclear cells from Holstein cattle with variable milk yield. Genomics 19:744. https://doi.org/10.1186/s12864-018-5124-9
Deng D, Deng G, Smith MF, Zhou J, Xin H, Powell SM, Lu Y (2002) Simultaneous detection of CpG methylation and single nucleotide polymorphism by denaturing high performance liquid chromatography. Nucleic Acids Res 30(3):e13
Diederich M, Hansmann T, Heinzmann J et al (2012) DNA methylation and mRNA expression profiles in bovine oocytes derived from prepubertal and adult donors. Reproduction 144:319–330. https://doi.org/10.1530/REP-12-0134
Dobbs KB, Rodriguez M, Sudano MJ et al (2013) Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PLoS One 8(6):e66230. https://doi.org/10.1371/journal.pone.0066230
Doherty R, Couldrey C (2014) Exploring genome wide bisulphite sequencing for DNA methylation analysis in livestock: a technical assessment. Front Genet 5:126. https://doi.org/10.3389/fgene.2014.00126
Dong G, Qiu M, Ao C et al (2014) Feeding a high-concentrate corn straw diet induced epigenetic alterations in the mammary tissue of dairy cows. PLoS One 9(9):e107659. https://doi.org/10.1371/journal.pone.0107659
Eads CA, Danenberg KD, Kawakami K, Saltz LB, Blake C, Shibata D, Danenberg PV, Laird PW (2000) MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res 28(8):e32
Fagundes NS, Michalczechen-Lacerda VA, Caixeta ES et al (2011) Methylation status in the intragenic differentially methylated region of the IGF2 locus in Bos taurus indicus oocytes with different developmental competencies. Mol Hum Reprod 17(2):85–91. https://doi.org/10.1093/molehr/gaq075
Fang L, Zhou Y, Liu S et al (2019) Comparative analyses of sperm DNA methylomes among human, mouse and cattle provide insights into epigenomic evolution and complex traits. Epigenetics 14(3):260–276. https://doi.org/10.1080/15592294.2019.1582217
Fang X, Zhao Z, Yu H et al (2017) Comparative genome-wide methylation analysis of longissimus dorsi muscles between Japanese black (Wagyu) and Chinese Red Steppes cattle. PLoS One 12(8):e0182492. https://doi.org/10.1371/journal.pone.0182492
Gebert C, Wrenzycki C, Herrmann D et al (2006) The bovine IGF2 gene is differentially methylated in oocyte and sperm DNA. Genomics 88:222–229. https://doi.org/10.1016/j.ygeno.2006.03.011
Goddard ME, Whitelaw E (2014) The use of epigenetic phenomena for the improvement of sheep and cattle. Front Genet 5:247. https://doi.org/10.3389/fgene.2014.00247
Gouil Q, Keniry A (2019) Latest techniques to study DNA methylation. Essays Biochem 63:639–648. https://doi.org/10.1042/EBC20190027
Gravina S, Ganapathi S, Vijg J (2015) Single-cell, locus-specific bisulfite sequencing (SLBS) for direct detection of epimutations in DNA methylation patterns. Nucleic Acids Res 43(14):e93
Gu Y, Li Q, Pan Z et al (2013) Molecular cloning, gene expression and methylation status analysis of PIWIL1 in cattle-yaks and the parental generation. Anim Reprod Sci 140:131–137. https://doi.org/10.1016/j.anireprosci.2013.05.010
Guo H, Zhu P, Guo F, Li X, Wu X, Fan X, Wen L, Tang F (2015) Profiling DNA methylome landscapes of mammalian cells with single-cell reduced-representation bisulfite sequencing. Nat Protoc 10(5):645e659
Guo H, Zhu P, Wu X, Li X, Wen L, Tang F (2013) Single-cell methylome landscapes of mouse embryonic stem cells and early embryos analyzed using reduced representation bisulfite sequencing. Genome Res 23(12):2126e2135
Heras S, Smits K, de Schauwer K et al (2017) Dynamics of 5-methylcytosine and 5-hydroxymethylcytosine during pronuclear development in equine zygotes produced by ICSI. Epigenetics Chromatin 10(13). https://doi.org/10.1186/s13072-017-0120-x
Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB (1996) Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 93(18):9821e9826
Holland PM, Abramson RD, Watson R, Gelfand DH (1991) Detection of specific polymerase chain reaction product by utilizing the 50-30 exonuclease activity of Thermus aquaticus DNA polymerase. Proc Natl Acad Sci U S A 88(16):7276e7280
Hori N, Nagai M, Hirayama M et al (2010) Aberrant CpG methylation of the imprinting control region KvDMR1 detected in assisted reproductive technology produced calves and pathogenesis of large offspring syndrome. Anim Reprod Sci 122:303–312. https://doi.org/10.1016/j.anireprosci.2010.09.008
Hsu H-K, Weng D, Hsu P-Y, Huang T, Huang Y-W (2020) Detection of DNA methylation by MeDIP and MBDCap assays: an overview of techniques. Methods in molecular biology (Clifton, NJ) in book: molecular toxicology protocols. 2102:225-234. https://doi.org/10.1007/978-1-0716-0223-2_12
Huang J, Zhang S, Mo F, Su S, Chen X, Li Y, Fang L, Huang H, Deng J, Liu H, Yang X, Zheng J (2019) An electrochemical DNA biosensor analytic technique for identifying DNA methylation specific sites and quantify DNA methylation level. Biosens Bioelectron 127:155–160. https://doi.org/10.1016/j.bios.2018.12.022
Huang TH, Perry MR, Laux DE (1999) Methylation profiling of CpG islands in human breast cancer cells. Hum Mol Genet 8(3):459e470
Huang Y-Z, Sun J-J, Zhang L-Z et al (2014a) Genome-wide DNA methylation profiles and their relationships with mRNA and the microRNA transcriptome in bovine muscle tissue (Bos taurine). Sci Rep 4:6546. https://doi.org/10.1038/srep06546
Huang Y-Z, Zhan Z-Y, Sun Y-J et al (2014b) Intragenic DNA methylation status down-regulates bovine IGF2 gene expression in different developmental stages. Gene 534(2):356–361. https://doi.org/10.1016/j.gene.2013.09.111
Ibeagha-Awemu EM, Zhao X (2015) Epigenetic marks: regulators of livestock phenotypes and conceivable sources of missing variation in livestock improvement programs. Front Genet 6:302. https://doi.org/10.3389/fgene.2015.00302
Ispada J, Bruna de Lima C, Sirard M-A et al (2018) Genome-wide screening of DNA methylation in bovine blastocysts with different kinetics of development. Epigenetics Chromatin 11:1. https://doi.org/10.1186/s13072-017-0171-z
Jang H, Serra C (2014) Nutrition, epigenetics, and diseases. Clin Nutr Res 3:1–8. https://doi.org/10.7762/cnr.2014.3.1.1
Jiang Z, Lin J, Dong H et al (2018) DNA methylomes of bovine gametes and in vivo produced preimplantation embryos. Biol Reprod 99(5):949–959
Kaneda M, Takahashi M, Yamanaka K-I et al (2017) Epigenetic analysis of bovine parthenogenetic embryonic fibroblasts. J Reprod Develop 63:365–375
Kiefer H, Jouneau L, Campion É et al (2016) Altered DNA methylation associated with an abnormal liver phenotype in a cattle model with a high incidence of perinatal pathologies. Sci Rep 6:38869. https://doi.org/10.1038/srep38869
Kohda T (2013) Effects of embryonic manipulation and epigenetics. J Hum Genet 58:416–420. https://doi.org/10.1038/jhg.2013.61
Korkmaz FT, Kerr DE (2017) Genome-wide methylation analysis reveals differentially methylated loci that are associated with an age-dependent increase in bovine fibroblast response to LPS. BMC Genomics 18:405. https://doi.org/10.1186/s12864-017-3796-1
Koufariotis LT, Chen Y-PP, Stothard P (2018) Variance explained by whole genome sequence variants in coding and regulatory genome annotations for six dairy traits. BMC Genomics 19:237. https://doi.org/10.1186/s12864-018-4617-x
Kropp J, Carrillo JA, Namous H et al (2017) Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genomics 18:280. https://doi.org/10.1186/s12864-017-3673-y
Lambert S, Blondin P, Vigneault C et al (2018) Spermatozoa DNA methylation patterns differ due to peripubertal age in bulls. Theriogenology 106:21–29. https://doi.org/10.1016/j.theriogenology.2017.10.006
Langevin SM, Kelsey KT (2013) The fate is not always written in the genes: epigenomics in epidemiologic studies. Environ Mol Mutagen 54:533–541. https://doi.org/10.1002/em.21762
Laskowski D, Humblot P, Sirard M-A et al (2018) DNA methylation pattern of bovine blastocysts associated with hyperinsulinemia in vitro. Mol Reprod Dev 85:599–611. https://doi.org/10.1002/mrd.22995
Lee EJ, Luo J, Wilson JM, Shi H (2012) Analyzing the cancer methylome through targeted bisulfite sequencing. Cancer Lett 340:171–178
Li Y, Carrillo JA, Ding Y et al (2019) DNA methylation, microRNA expression profiles and their relationships with transcriptome in grass-fed and grain-fed Angus cattle rumen tissue. PLoS One 14(10):e0214559. https://doi.org/10.1371/journal.pone.0214559
Littlejohn BP, Price DM, Neuendorff DA et al (2018) Prenatal transportation stress alters genome-wide DNA methylation in suckling Brahman bull calves. J Anim Sci 96:5075–5099. https://doi.org/10.1093/jas/sky350
Liu S, Fang L, Zhou Y et al (2019) Analyses of inter-individual variations of sperm DNA methylation and their potential implications in cattle. BMC Genomics 20:888. https://doi.org/10.1186/s12864-019-6228-6
Liu X, Yang J, Zhang Q et al (2017) Regulation of DNA methylation on EEF1D and RPL8 expression in cattle. Genetica 145:387–395. https://doi.org/10.1007/s10709-017-9974-x
Liu Z, Li Q, Pan Z et al (2011) Comparative analysis on mRNA expression level and methylation status of DAZL gene between cattle-yaks and their parents. Anim Reprod Sci 126:258–264. https://doi.org/10.1016/j.anireprosci.2011.05.013
Lorthongpanich C, Cheow LF, Balu S, Quake SR, Knowles BB, Burkholder WF, Solter D, Messerschmidt DM (2013) Single-cell DNA-methylation analysis reveals epigenetic chimerism in preimplantation embryos. Science 341(6150):1110e1112
Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D’Souza C, Fouse SD, Johnson BE, Hong C, Nielsen C, Zhao Y, Turecki G, Delaney A, Varhol R, Thiessen N, Shchors K, Heine VM, Rowitch DH, Xing X, Fiore C, Schillebeeckx M, Jones SJ, Haussler D, Marra MA, Hirst M, Wang T, Costello JF (2010) Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466(7303):253e257
Meissner A, Gnirke A, Bell GW, Ramsahoye B, Lander ES, Jaenisch R (2005) Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res 33(18):5868e5877
Mendonça ADS, Silveira MM, Rios ÁFL et al (2019a) DNA methylation and functional characterization of the XIST gene during in vitro early embryo development in cattle. Epigenetics. 14(6):568–588. https://doi.org/10.1080/15592294.2019.1600828
Mendonça ADS, Franco MM, de Oliveira CJ et al (2019b) DNA methylation of the insulin-like growth factor 2-imprinted gene in trophoblast cells of elongated bovine embryo: effects of the in vitro culture. Cell Rep 21(5):260–269. https://doi.org/10.1089/cell.2019.0041
Niemann H (2016) Epigenetic reprogramming in mammalian species after SCNT-based cloning. Theriogenology 86:80–90. https://doi.org/10.1016/j.theriogenology.2016.04.021
Nygren AO, Ameziane N, Duarte HM, Vijzelaar RN, Waisfisz Q, Hess CJ, Schouten JP, Errami A (2005) Methylation-specific MLPA (MS-MLPA): simultaneous detection of CpG methylation and copy number changes of up to 40 sequences. Nucleic Acids Res 33(14):e128
O’Doherty AM, O’Shea LC, Fair T (2012) Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biol Reprod 86(3):67,1–10. https://doi.org/10.1095/biolreprod.111.094946
O’Doherty AM, MacHugh DE, Spillane C, Magee DA (2015) Genomic imprinting effects on complex traits in domesticated animal species. Front Genet 6:156. https://doi.org/10.3389/fgene.2015.00156
O’Doherty AM, McGettigan P, Irwin RE et al (2018) Intragenic sequences in the trophectoderm harbour the greatest proportion of methylation errors in day 17 bovine conceptuses generated using assisted reproductive technologies. Genomics 19:438. https://doi.org/10.1186/s12864-018-4818-3
O’Doherty AM, Rue-Albrecht KC, Magee DA et al (2019) The bovine alveolar macrophage DNA methylome is resilient to infection with Mycobacterium bovis. Sci Rep 9:1510. https://doi.org/10.1038/s41598-018-37618-z
Paibomesai M, Hussey B, Nino-Soto M et al (2013) Effects of parturition and dexamethasone on DNA methylation patterns of IFN-g and IL-4 promoters in CD4+ T-lymphocytes of Holstein dairy cows. Can J Vet Res 77:54–62
Pallotta MM, Barbato V, Pinton A et al (2019) In vitro exposure to CPF affects bovine sperm epigenetic gene methylation pattern and the ability of sperm to support fertilization and embryo development. Environ Mol Mutagen 60:85–95. https://doi.org/10.1002/em.22242
Paradis F, Wood KM, Swanson KC et al (2017) Maternal nutrient restriction in mid-to-late gestation influences fetal mRNA expression in muscle tissues in beef cattle. BMC Genomics 18:632. https://doi.org/10.1186/s12864-017-4051-5
Park JS, Jeong YS, Shin ST et al (2007) Dynamic DNA methylation reprogramming: active demethylation and immediate remethylation in the male pronucleus of bovine zygotes. Dev Dyn 236:2523–2533. https://doi.org/10.1002/dvdy.21278
Penteado JCT, Borduchi RJ, Maldonado MBC et al (2017) Expression of tissue-specific imprinted gene tumor suppressing subtransferable candidate 4 (TSSC4) is altered in placentae produced by nuclear transfer in cattle. Anim Reprod Sci 187:174–180. https://doi.org/10.1016/j.anireprosci.2017.11.003
Perrier J-P, Sellem E, Prézelin A et al (2018) A multi-scale analysis of bull sperm methylome revealed both species peculiarities and conserved tissue-specific features. Genomics 19:404. https://doi.org/10.1186/s12864-018-4764-0
Rakyan VK, Down TA, Balding DJ et al (2011) Epigenome-wide association studies for common human diseases. Nat Rev Genet 12:529–541
Rao Y, Sun X, Yang N et al (2018) Neonatal respiratory distress syndrome and underlying mechanisms in cloned cattle. Mol Reprod Dev 85:227–235. https://doi.org/10.1002/mrd.22956
Rekawiecki R, Kisielewska K, Kowalik MK et al (2018) Methylation of progesterone receptor isoform A and B promoters in the reproductive system of cows. Reprod Fertil Dev 30(12):1634–1642. https://doi.org/10.1071/RD17518
Rutkowska K, Xu H, Flisikowski K (2019) Differentially methylated region in bovine MIMT1 detected by-small scale whole-genome methylation sequencing. J Appl Genet 60:401–404. https://doi.org/10.1007/s13353-019-00519-6
Sadri R, Hornsby PJ (1996) Rapid analysis of DNA methylation using new restriction enzyme sites created by bisulfite modification. Nucleic Acids Res 24(24):5058e5059
Salilew-Wondim D, Saeed-Zidane M, Hoelker M et al (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. https://doi.org/10.1186/s12864-018-4826-3
Sarova N, Ahlawat S, Grewal A et al (2018) Differential promoter methylation of DAZL gene in bulls with varying seminal parameters. Reprod Domest Anim 53:914–920. https://doi.org/10.1111/rda.13187
Sevane N, Martínez R, Bruford MW (2019) Genome-wide differential DNA methylation in tropically adapted creole cattle and their Iberian ancestors. Anim Genet 50(1):15–26. https://doi.org/10.1111/age.12731
Shi B, Thomas AJ, Benninghoff AD et al (2018) Genetic and epigenetic regulation of major histocompatibility complex class I gene expression in bovine trophoblast cells. Am J Reprod Immunol 79:e12779. https://doi.org/10.1111/aji.12779
Silveira MM, Salgado Bayão HX, dos Santos MA et al (2018) DNA methylation profile at a satellite region is associated with aberrant placentation in cloned calves. Placenta 70:25–33. https://doi.org/10.1016/j.placenta.2018.08.007
Singer-Sam J, LeBon JM, Tanguay RL, Riggs AD (1990) A quantitative HpaII-PCR assay to measure methylation of DNA from a small number of cells. Nucleic Acids Res 18(3):687
Skibiel AL, Peñagaricano F, Amorín R et al (2018) In utero heat stress alters the ofspring epigenome. Sci Rep 8:14609. https://doi.org/10.1038/s41598-018-32975-1
Su J, Yang B, Wang Y et al (2011) Expression and methylation status of imprinted genes in placentas of deceased and live cloned transgenic calves. Theriogenology 75:1346–1359. https://doi.org/10.1016/j.theriogenology.2010.11.045
Su J, Wang Y, Xing X et al (2014) Genome-wide analysis of DNA methylation in bovine placentas. BMC Genomics 15:12 http://www.biomedcentral.com/1471-2164/15/12
Sun HL, Meng LN, Zhao X et al (2016) Effects of DNA methyltransferase inhibitor RG108 on methylation in buffalo adult fibroblasts and subsequent embryonic development following somatic cell nuclear transfer. Genet Mol Res 15(3):gmr.15038455. https://doi.org/10.4238/gmr.15038455
Takeda K, Kobayashi E, Akagi S et al (2017) Differentially methylated CpG sites in bull spermatozoa revealed by human DNA methylation arrays and bisulfite analysis. J Reprod Develop 63:279–287. https://doi.org/10.1093/gigascience/giy039
Takeda K, Kobayashi E, Nishino K et al (2019) Age-related changes in DNA methylation levels at CpG sites in bull spermatozoa and in vitro fertilization-derived blastocyst-stage embryos revealed by combined bisulfite restriction analysis. J Reprod Dev 65:305–312
Tost J, Gut IG (2017) Molecular techniques for DNA methylation studies. Mol Diagnost. George P. Patrinos Ed. Elsevier Ltd. ISDN 978–0–12-802971-8. https://doi.org/10.1016/B978-0-12-802971-8.00007-9
Tremblay R, Dufort I, Sirard M-A (2018) Metabolic stress induces modifications in the epigenetic program of preimplantation bovine embryos. Mol Reprod Dev 85:117–127. https://doi.org/10.1002/mrd.22941
Triantaphyllopoulos KA, Ikonomopoulos I, Bannister AJ (2016) Epigenetics and inheritance of phenotype variation in livestock. Epigenetics Chromatin 9:31. https://doi.org/10.1186/s13072-016-0081-5
Urrego R, Rodriguez-Osorio N, Niemann H (2014) Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle. Epigenetics 9(6):803–815. https://doi.org/10.4161/epi.28711
Vanselow J, Yang W, Herrmann J et al (2007) DNA-remethylation around a STAT5-binding enhancer in the alphaS1-casein promoter is associated with abrupt shutdown of alphaS1 casein synthesis during acute mastitis. J Mol Endocrinol 37(3):463–477. https://doi.org/10.1677/jme.1.02131
Verma A, Rajput S, De S et al (2014) Genome-wide profiling of sperm DNA methylation in relation to buffalo (Bubalus bubalis) bull fertility. Theriogenology 82:750–759. https://doi.org/10.1016/j.theriogenology.2014.06.012
Wang G-N, Yang W-Z, Xu D et al (2017) Aberrant expression of MICO1 and MICO1OS in deceased somatic cell nuclear transfer calves. Mol Reprod Dev 84:517–524. https://doi.org/10.1002/mrd.22807
Wang J, Xiaoxiao Y, Nesengani LT et al (2018) LPS-induces IL-6 and IL-8 gene expression in bovine endometrial cells “through DNA methylation”. Gene. 30(677):266–272. https://doi.org/10.1016/j.gene.2018.07.074
Wang L, Sun HZ, Guan LL et al (2019a) Short communication: relationship of blood DNA methylation rate and milk performance in dairy cows. J Dairy Sci 102(6):5208–5211. https://doi.org/10.3168/jds.2018-15869
Wang L, Hand JM, Fu L et al (2019b) DNA methylation and miRNA-1296 act in concert to mediate spatiotemporal expression of KPNA7 during bovine oocyte and early embryonic development. Dev Biol 19:23. https://doi.org/10.1186/s12861-019-0204-x
Wang XS, Zhang Y, He YH et al (2013) Aberrant promoter methylation of the CD4 gene in peripheral blood cells of mastitic dairy cows. Genet Mol Res 12(4):6228–6239. https://doi.org/10.4238/2013.December.4.10
Wei D, Li A, Zhao C et al (2018) Transcriptional regulation by CpG sites methylation in the core promoter region of the bovine SIX1 gene: roles of histone H4 and E2F2. Int J Mol Sci 19:213. https://doi.org/10.3390/ijms19010213
Worm J, Aggerholm A, Guldberg P (2001) In-tube DNA methylation profiling by fluorescence melting curve analysis. Clin Chem 47(7):1183e1189
Wyck S, Herrera C, Requena CE et al (2018) Oxidative stress in sperm affects the epigenetic reprogramming in early embryonic development. Epigenetics Chromatin 11:60. https://doi.org/10.1186/s13072-018-0224-y
Xiong Z, Laird PW (1997) COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 25(12):2532e2534
Xu D, Zhang C, Li J et al (2018) Polymorphic imprinting of SLC38A4 gene in bovine placenta. Biochem Genet 56:639–649. https://doi.org/10.1007/s10528-018-9866-5
Xu D, Wang G, Li J et al (2019) Tissue-specific monoallelic expression of bovine AXL is associated with DNA methylation of promoter DMR. Biochem Genet 57:801–812. https://doi.org/10.1007/s10528-019-09925-1
Yakovlev AF (2018) Epigenetic effects in livestock breeding. Russ J Genet 54(8):897–909. https://doi.org/10.1134/S1022795418080148
Yamada Y, Watanabe H, Miura F, Soejima H, Uchiyama M, Iwasaka T, Mukai T, Sakaki Y, Ito T (2004) A comprehensive analysis of allelic methylation status of CpG islands on human chromosome 21q. Genome Res 14(2):247e266
Yamanaka K-I, Yamashita K, Khatun H et al (2018) Normal DNA methylation status in sperm from a somatic cell cloned bull and their fertilized embryos. Anim Sci J:1–9. https://doi.org/10.1111/asj.13086
Zeschnigk M, Bohringer S, Price EA, Onadim Z, Masshofer L, Lohmann DR (2004) A novel real-time PCR assay for quantitative analysis of methylated alleles (QAMA): analysis of the retinoblastoma locus. Nucleic Acids Res 32(16):e125
Zhang G-M, Song C-C, Li L-J et al (2018a) DNA methylation status of CRABP2 promoter down-regulates its expression. Gene. 676:243–248. https://doi.org/10.1016/j.gene.2018.07.049
Zhang Y, Wang X, Jiang Q et al (2018b) DNA methylation rather than single nucleotide polymorphisms regulates the production of an aberrant splice variant of IL6R in mastitic cows. Cell Stress Chaperones 23:617–628. https://doi.org/10.1007/s12192-017-0871-0
Zhang J, Zhang S, Wang Y et al (2017) Effect of TET inhibitor on bovine parthenogenetic embryo development. PLoS One 12(12):e0189542. https://doi.org/10.1371/journal.pone.0189542
Zhou X-Y, Liu L-L, Jia W-C et al (2016a) Methylation profile of bovine Oct4 gene coding region in relation to three germ layers. J Integr Agric 15(3):618–628. https://doi.org/10.1016/S2095-3119(15)61100-5
Zhou Y, Xu L, Bickhart DM et al (2016b) Reduced representation bisulphite sequencing of ten bovine somatic tissues reveals DNA methylation patterns and their impacts on gene expression. BMC Genomics 17:779. https://doi.org/10.1186/s12864-016-3116-1
Zhou Y, Connor EE, Bickhart DM et al (2018) Comparative whole genome DNA methylation profiling of cattle sperm and somatic tissues reveals striking hypomethylated patterns in sperm. GigaScience 7:1–13. https://doi.org/10.1093/gigascience/giy039
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This work was supported by the Scientific Grant Agency of Slovak Republik under grant number 1/0242/19.
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Communicated by: Maciej Szydlowski
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The original online version of this article was revised: The author would like to add Funding in the back matter of the originally published article. Funding This work was supported by the Scientific Grant Agency of Slovak Republik under grant number 1/0242/19.
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Halušková, J., Holečková, B. & Staničová, J. DNA methylation studies in cattle. J Appl Genetics 62, 121–136 (2021). https://doi.org/10.1007/s13353-020-00604-1
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DOI: https://doi.org/10.1007/s13353-020-00604-1