{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T22:11:08Z","timestamp":1790806268661,"version":"4.1.0"},"reference-count":77,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2018,5,29]],"date-time":"2018-05-29T00:00:00Z","timestamp":1527552000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-13-LAB3-0008-01"],"award-info":[{"award-number":["ANR-13-LAB3-0008-01"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-11-INBS -0003"],"award-info":[{"award-number":["ANR-11-INBS -0003"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Genomics"],"published-print":{"date-parts":[[2018,12]]},"DOI":"10.1186\/s12864-018-4764-0","type":"journal-article","created":{"date-parts":[[2018,5,29]],"date-time":"2018-05-29T08:13:06Z","timestamp":1527581586000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":45,"title":["A multi-scale analysis of bull sperm methylome revealed both species peculiarities and conserved tissue-specific features"],"prefix":"10.1186","volume":"19","author":[{"given":"Jean-Philippe","family":"Perrier","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eli","family":"Sellem","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Audrey","family":"Pr\u00e9zelin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maxime","family":"Gasselin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luc","family":"Jouneau","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fran\u00e7ois","family":"Piumi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hala","family":"Al Adhami","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Micha\u00ebl","family":"Weber","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S\u00e9bastien","family":"Fritz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Didier","family":"Boichard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chrystelle","family":"Le Danvic","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurent","family":"Schibler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H\u00e9l\u00e8ne","family":"Jammes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6631-741X","authenticated-orcid":false,"given":"H\u00e9l\u00e8ne","family":"Kiefer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2018,5,29]]},"reference":[{"issue":"2","key":"4764_CR1","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.fertnstert.2011.12.036","volume":"97","author":"DT Carrell","year":"2012","unstructured":"Carrell DT. Epigenetics of the male gamete. Fertil Steril. 2012;97(2):267\u201374.","journal-title":"Fertil Steril"},{"issue":"10","key":"4764_CR2","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1038\/nrg.2016.88","volume":"17","author":"WW Tang","year":"2016","unstructured":"Tang WW, Kobayashi T, Irie N, Dietmann S, Surani MA. Specification and epigenetic programming of the human germ line. Nat Rev Genet. 2016;17(10):585\u2013600.","journal-title":"Nat Rev Genet"},{"issue":"1","key":"4764_CR3","doi-asserted-by":"publisher","first-page":"R25","DOI":"10.1530\/REP-14-0643","volume":"150","author":"C Yao","year":"2015","unstructured":"Yao C, Liu Y, Sun M, Niu M, Yuan Q, Hai Y, Guo Y, Chen Z, Hou J, Liu Y, et al. MicroRNAs and DNA methylation as epigenetic regulators of mitosis, meiosis and spermiogenesis. Reprod. 2015;150(1):R25\u201334.","journal-title":"Reprod"},{"issue":"5","key":"4764_CR4","doi-asserted-by":"publisher","first-page":"R55","DOI":"10.1530\/REP-15-0562","volume":"151","author":"J Bao","year":"2016","unstructured":"Bao J, Bedford MT. Epigenetic regulation of the histone-to-protamine transition during spermiogenesis. Reprod. 2016;151(5):R55\u201370.","journal-title":"Reprod"},{"key":"4764_CR5","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1007\/978-1-4614-7783-9_4","volume":"791","author":"JR Gannon","year":"2014","unstructured":"Gannon JR, Emery BR, Jenkins TG, Carrell DT. The sperm epigenome: implications for the embryo. Adv Exp Med Biol. 2014;791:53\u201366.","journal-title":"Adv Exp Med Biol"},{"issue":"3","key":"4764_CR6","doi-asserted-by":"publisher","first-page":"624","DOI":"10.1016\/j.fertnstert.2013.01.124","volume":"99","author":"CC Boissonnas","year":"2013","unstructured":"Boissonnas CC, Jouannet P, Jammes H. Epigenetic disorders and male subfertility. Fertil Steril. 2013;99(3):624\u201331.","journal-title":"Fertil Steril"},{"issue":"1","key":"4764_CR7","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1038\/ejhg.2009.117","volume":"18","author":"CC Boissonnas","year":"2010","unstructured":"Boissonnas CC, Abdalaoui HE, Haelewyn V, Fauque P, Dupont JM, Gut I, Vaiman D, Jouannet P, Tost J, Jammes H. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Human Genet : EJHG. 2010;18(1):73\u201380.","journal-title":"Eur J Human Genet : EJHG"},{"issue":"7","key":"4764_CR8","doi-asserted-by":"publisher","first-page":"2310","DOI":"10.1016\/j.fertnstert.2011.03.096","volume":"95","author":"L Nanassy","year":"2011","unstructured":"Nanassy L, Carrell DT. Abnormal methylation of the promoter of CREM is broadly associated with male factor infertility and poor sperm quality but is improved in sperm selected by density gradient centrifugation. Fertil Steril. 2011;95(7):2310\u20134.","journal-title":"Fertil Steril"},{"key":"4764_CR9","doi-asserted-by":"publisher","first-page":"2889","DOI":"10.1038\/ncomms3889","volume":"4","author":"R Lambrot","year":"2013","unstructured":"Lambrot R, Xu C, Saint-Phar S, Chountalos G, Cohen T, Paquet M, Suderman M, Hallett M, Kimmins S. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun. 2013;4:2889.","journal-title":"Nat Commun"},{"issue":"6","key":"4764_CR10","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1016\/j.cmet.2014.03.026","volume":"19","author":"D Martinez","year":"2014","unstructured":"Martinez D, Pentinat T, Ribo S, Daviaud C, Bloks VW, Cebria J, Villalmanzo N, Kalko SG, Ramon-Krauel M, Diaz R, et al. In utero undernutrition in male mice programs liver lipid metabolism in the second-generation offspring involving altered Lxra DNA methylation. Cell Metab. 2014;19(6):941\u201351.","journal-title":"Cell Metab"},{"issue":"6198","key":"4764_CR11","doi-asserted-by":"publisher","first-page":"1255903","DOI":"10.1126\/science.1255903","volume":"345","author":"EJ Radford","year":"2014","unstructured":"Radford EJ, Ito M, Shi H, Corish JA, Yamazawa K, Isganaitis E, Seisenberger S, Hore TA, Reik W, Erkek S, et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Sci. 2014;345(6198):1255903.","journal-title":"Sci"},{"key":"4764_CR12","doi-asserted-by":"publisher","unstructured":"Aston KI, Uren PJ, Jenkins TG, Horsager A, Cairns BR, Smith AD, Carrell DT. Aberrant sperm DNA methylation predicts male fertility status and embryo quality. Fertil Steril. 2015; \n                    https:\/\/doi.org\/10.1016\/j.fertnstert.2015.08.019\n                    \n                  .","DOI":"10.1016\/j.fertnstert.2015.08.019"},{"issue":"3","key":"4764_CR13","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1016\/j.fertnstert.2015.06.015","volume":"104","author":"A Salas-Huetos","year":"2015","unstructured":"Salas-Huetos A, Blanco J, Vidal F, Godo A, Grossmann M, Pons MC, Fernandez SF, Garrido N, Anton E. Spermatozoa from patients with seminal alterations exhibit a differential micro-ribonucleic acid profile. Fertil Steril. 2015;104(3):591\u2013601.","journal-title":"Fertil Steril"},{"issue":"5","key":"4764_CR14","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1111\/andr.12216","volume":"4","author":"K Ni","year":"2016","unstructured":"Ni K, Spiess AN, Schuppe HC, Steger K. The impact of sperm protamine deficiency and sperm DNA damage on human male fertility: a systematic review and meta-analysis. Androl. 2016;4(5):789\u201399.","journal-title":"Androl"},{"issue":"3","key":"4764_CR15","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1016\/j.molmet.2015.12.002","volume":"5","author":"T de Castro Barbosa","year":"2016","unstructured":"de Castro Barbosa T, Ingerslev LR, Alm PS, Versteyhe S, Massart J, Rasmussen M, Donkin I, Sjogren R, Mudry JM, Vetterli L, et al. High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Mol Metab. 2016;5(3):184\u201397.","journal-title":"Mol Metab"},{"issue":"6271","key":"4764_CR16","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1126\/science.aad6780","volume":"351","author":"U Sharma","year":"2016","unstructured":"Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY, Belleannee C, Kucukural A, Serra RW, Sun F, et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Sci. 2016;351(6271):391\u20136.","journal-title":"Sci"},{"key":"4764_CR17","doi-asserted-by":"publisher","first-page":"42336","DOI":"10.1038\/srep42336","volume":"7","author":"N Kobayashi","year":"2017","unstructured":"Kobayashi N, Miyauchi N, Tatsuta N, Kitamura A, Okae H, Hiura H, Sato A, Utsunomiya T, Yaegashi N, Nakai K, et al. Factors associated with aberrant imprint methylation and oligozoospermia. Sci Rep. 2017;7:42336.","journal-title":"Sci Rep"},{"key":"4764_CR18","doi-asserted-by":"publisher","unstructured":"Jenkins TG, Aston KI, Meyer TD, Hotaling JM, Shamsi MB, Johnstone EB, Cox KJ, Stanford JB, Porucznik CA, Carrell DT. Decreased fecundity and sperm DNA methylation patterns. Fertil Steril. 2016; \n                    https:\/\/doi.org\/10.1016\/j.fertnstert.2015.09.013\n                    \n                  .","DOI":"10.1016\/j.fertnstert.2015.09.013"},{"issue":"5","key":"4764_CR19","doi-asserted-by":"publisher","first-page":"1014","DOI":"10.1093\/humrep\/dev053","volume":"30","author":"RG Urdinguio","year":"2015","unstructured":"Urdinguio RG, Bayon GF, Dmitrijeva M, Torano EG, Bravo C, Fraga MF, Bassas L, Larriba S, Fernandez AF, Aberrant DNA. Methylation patterns of spermatozoa in men with unexplained infertility. Hum Reprod. 2015;30(5):1014\u201328.","journal-title":"Hum Reprod"},{"issue":"7004","key":"4764_CR20","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1038\/nature02886","volume":"431","author":"D Bourc'his","year":"2004","unstructured":"Bourc'his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nat. 2004;431(7004):96\u20139.","journal-title":"Nat"},{"key":"4764_CR21","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.tox.2016.07.005","volume":"361-362","author":"N Song","year":"2016","unstructured":"Song N, Endo D, Song B, Shibata Y, Koji T. 5-aza-2\u2032-deoxycytidine impairs mouse spermatogenesis at multiple stages through different usage of DNA methyltransferases. Toxicol. 2016;361-362:62\u201372.","journal-title":"Toxicol"},{"issue":"6314","key":"4764_CR22","doi-asserted-by":"publisher","first-page":"909","DOI":"10.1126\/science.aah5143","volume":"354","author":"J Barau","year":"2016","unstructured":"Barau J, Teissandier A, Zamudio N, Roy S, Nalesso V, Herault Y, Guillou F, Bourc'his D. The DNA methyltransferase DNMT3C protects male germ cells from transposon activity. Sci. 2016;354(6314):909\u201312.","journal-title":"Sci"},{"issue":"2","key":"4764_CR23","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1530\/REP-13-0343","volume":"147","author":"F Guo","year":"2014","unstructured":"Guo F, Yang B, Ju ZH, Wang XG, Qi C, Zhang Y, Wang CF, Liu HD, Feng MY, Chen Y, et al. Alternative splicing, promoter methylation, and functional SNPs of sperm flagella 2 gene in testis and mature spermatozoa of Holstein bulls. Reprod. 2014;147(2):241\u201352.","journal-title":"Reprod"},{"issue":"4","key":"4764_CR24","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1002\/mrd.22303","volume":"81","author":"SC Jena","year":"2014","unstructured":"Jena SC, Kumar S, Rajput S, Roy B, Verma A, Kumaresan A, Mohanty TK, De S, Kumar R, Datta TK. Differential methylation status of IGF2-H19 locus does not affect the fertility of crossbred bulls but some of the CTCF binding sites could be potentially important. Mol Reprod Dev. 2014;81(4):350\u201362.","journal-title":"Mol Reprod Dev"},{"issue":"6","key":"4764_CR25","doi-asserted-by":"publisher","first-page":"e0128250","DOI":"10.1371\/journal.pone.0128250","volume":"10","author":"W Yao","year":"2015","unstructured":"Yao W, Li Y, Li B, Luo H, Xu H, Pan Z, Xie Z, Li Q. Epigenetic regulation of bovine spermatogenic cell-specific gene boule. PLoS One. 2015;10(6):e0128250.","journal-title":"PLoS One"},{"issue":"5","key":"4764_CR26","doi-asserted-by":"publisher","first-page":"750","DOI":"10.1016\/j.theriogenology.2014.06.012","volume":"82","author":"A Verma","year":"2014","unstructured":"Verma A, Rajput S, De S, Kumar R, Chakravarty AK, Datta TK. Genome-wide profiling of sperm DNA methylation in relation to buffalo (Bubalus bubalis) bull fertility. Theriogenology. 2014;82(5):750\u20139. e751","journal-title":"Theriogenology"},{"issue":"1","key":"4764_CR27","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1186\/s12864-017-3673-y","volume":"18","author":"J Kropp","year":"2017","unstructured":"Kropp J, Carrillo JA, Namous H, Daniels A, Salih SM, Song J, Khatib H. Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genomics. 2017;18(1):280.","journal-title":"BMC Genomics"},{"key":"4764_CR28","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1186\/1471-2164-15-451","volume":"15","author":"HA Shojaei Saadi","year":"2014","unstructured":"Shojaei Saadi HA, O'Doherty AM, Gagne D, Fournier E, Grant JR, Sirard MA, Robert C. An integrated platform for bovine DNA methylome analysis suitable for small samples. BMC Genomics. 2014;15:451.","journal-title":"BMC Genomics"},{"issue":"5926","key":"4764_CR29","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1126\/science.1169588","volume":"324","author":"S Bovine Genome","year":"2009","unstructured":"Bovine Genome S, Analysis C, Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, Weinstock GM, Adelson DL, Eichler EE, et al. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science. 2009;324(5926):522\u20138.","journal-title":"Science"},{"issue":"1","key":"4764_CR30","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1007\/s00438-016-1264-2","volume":"292","author":"F Kader","year":"2017","unstructured":"Kader F, Ghai M. DNA methylation-based variation between human populations. Mol Genet Genomics : MGG. 2017;292(1):5\u201335.","journal-title":"Mol Genet Genomics : MGG"},{"issue":"2","key":"4764_CR31","doi-asserted-by":"publisher","first-page":"308","DOI":"10.1017\/S1751731113002097","volume":"8","author":"I Ortiz","year":"2014","unstructured":"Ortiz I, Dorado J, Ramirez L, Morrell JM, Acha D, Urbano M, Galvez MJ, Carrasco JJ, Gomez-Arrones V, Calero-Carretero R, et al. Effect of single layer centrifugation using Androcoll-E-large on the sperm quality parameters of cooled-stored donkey semen doses. Animal. 2014;8(2):308\u201315.","journal-title":"Animal"},{"key":"4764_CR32","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1007\/978-1-4939-1594-1_20","volume":"1222","author":"H Kiefer","year":"2015","unstructured":"Kiefer H. Genome-wide analysis of methylation in bovine clones by methylated DNA immunoprecipitation (MeDIP). Methods Mol Biol. 2015;1222:267\u201380.","journal-title":"Methods Mol Biol"},{"issue":"11","key":"4764_CR33","doi-asserted-by":"publisher","first-page":"1989","DOI":"10.1016\/j.yexcr.2006.03.006","volume":"312","author":"M Karimi","year":"2006","unstructured":"Karimi M, Johansson S, Stach D, Corcoran M, Grander D, Schalling M, Bakalkin G, Lyko F, Larsson C, Ekstrom TJ. LUMA (LUminometric methylation assay)--a high throughput method to the analysis of genomic DNA methylation. Exp Cell Res. 2006;312(11):1989\u201395.","journal-title":"Exp Cell Res"},{"issue":"6","key":"4764_CR34","doi-asserted-by":"publisher","first-page":"e66816","DOI":"10.1371\/journal.pone.0066816","volume":"8","author":"L Attig","year":"2013","unstructured":"Attig L, Vige A, Gabory A, Karimi M, Beauger A, Gross MS, Athias A, Gallou-Kabani C, Gambert P, Ekstrom TJ, et al. Dietary alleviation of maternal obesity and diabetes: increased resistance to diet-induced obesity transcriptional and epigenetic signatures. PLoS One. 2013;8(6):e66816.","journal-title":"PLoS One"},{"key":"4764_CR35","doi-asserted-by":"publisher","first-page":"38869","DOI":"10.1038\/srep38869","volume":"6","author":"H Kiefer","year":"2016","unstructured":"Kiefer H, Jouneau L, Campion E, Rousseau-Ralliard D, Larcher T, Martin-Magniette ML, Balzergue S, Ledevin M, Prezelin A, Chavatte-Palmer P, et al. Altered DNA methylation associated with an abnormal liver phenotype in a cattle model with a high incidence of perinatal pathologies. Sci Rep. 2016;6:38869.","journal-title":"Sci Rep"},{"issue":"1","key":"4764_CR36","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1038\/nprot.2008.211","volume":"4","author":"d W Huang","year":"2009","unstructured":"Huang d W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44\u201357.","journal-title":"Nat Protoc"},{"issue":"4","key":"4764_CR37","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1038\/nprot.2010.190","volume":"6","author":"H Gu","year":"2011","unstructured":"Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat Protoc. 2011;6(4):468\u201381.","journal-title":"Nat Protoc"},{"issue":"12","key":"4764_CR38","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1186\/s13059-014-0545-5","volume":"15","author":"G Auclair","year":"2014","unstructured":"Auclair G, Guibert S, Bender A, Weber M. Ontogeny of CpG island methylation and specificity of DNMT3 methyltransferases during embryonic development in the mouse. Genome Biol. 2014;15(12):545.","journal-title":"Genome Biol"},{"key":"4764_CR39","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1186\/s13100-015-0041-9","volume":"6","author":"W Bao","year":"2015","unstructured":"Bao W, Kojima KK, Kohany O. Repbase update, a database of repetitive elements in eukaryotic genomes. Mob DNA. 2015;6:11.","journal-title":"Mob DNA"},{"issue":"1","key":"4764_CR40","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1016\/j.ab.2004.05.007","volume":"333","author":"JM Dupont","year":"2004","unstructured":"Dupont JM, Tost J, Jammes H, Gut IG. De novo quantitative bisulfite sequencing using the pyrosequencing technology. Anal Biochem. 2004;333(1):119\u201327.","journal-title":"Anal Biochem"},{"issue":"11","key":"4764_CR41","doi-asserted-by":"publisher","first-page":"1427","DOI":"10.1093\/bioinformatics\/18.11.1427","volume":"18","author":"LC Li","year":"2002","unstructured":"Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics. 2002;18(11):1427\u201331.","journal-title":"Bioinformatics"},{"key":"4764_CR42","first-page":"11","volume":"13","author":"A Weyrich","year":"2012","unstructured":"Weyrich A. Preparation of genomic DNA from mammalian sperm. Curr Protoc Mo Biol. 2012, Chapter 2:Unit 2;13:11\u20133.","journal-title":"Curr Protoc Mo Biol"},{"issue":"3","key":"4764_CR43","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1111\/eci.12403","volume":"45","author":"D Schubeler","year":"2015","unstructured":"Schubeler D. ESCI award lecture: regulation, function and biomarker potential of DNA methylation. Eur J Clin Investig. 2015;45(3):288\u201393.","journal-title":"Eur J Clin Investig"},{"issue":"8","key":"4764_CR44","doi-asserted-by":"publisher","first-page":"853","DOI":"10.1038\/ng1598","volume":"37","author":"M Weber","year":"2005","unstructured":"Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schubeler D. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet. 2005;37(8):853\u201362.","journal-title":"Nat Genet"},{"issue":"17","key":"4764_CR45","doi-asserted-by":"publisher","first-page":"2226","DOI":"10.1128\/MCB.01102-15","volume":"36","author":"M Arribas-Layton","year":"2016","unstructured":"Arribas-Layton M, Dennis J, Bennett EJ, Damgaard CK, Lykke-Andersen J. The C-terminal RGG domain of human Lsm4 promotes processing body formation stimulated by arginine Dimethylation. Mol Cell Biol. 2016;36(17):2226\u201335.","journal-title":"Mol Cell Biol"},{"issue":"10","key":"4764_CR46","doi-asserted-by":"publisher","first-page":"1501","DOI":"10.1111\/jog.12765","volume":"41","author":"T Miyamoto","year":"2015","unstructured":"Miyamoto T, Minase G, Okabe K, Ueda H, Sengoku K. Male infertility and its genetic causes. J Obstet Gynaecol Res. 2015;41(10):1501\u20135.","journal-title":"J Obstet Gynaecol Res"},{"key":"4764_CR47","doi-asserted-by":"publisher","unstructured":"Cheng YS, Lu CW, Lin TY, Lin PY, Lin YM. Causes and clinical features of infertile men with nonobstructive azoospermia and histopathologic diagnosis of Hypospermatogenesis. Urol. 2017; \n                    https:\/\/doi.org\/10.1016\/j.urology.2017.03.026\n                    \n                  .","DOI":"10.1016\/j.urology.2017.03.026"},{"issue":"6","key":"4764_CR48","doi-asserted-by":"publisher","first-page":"1029","DOI":"10.1016\/j.cell.2011.08.016","volume":"146","author":"A Molaro","year":"2011","unstructured":"Molaro A, Hodges E, Fang F, Song Q, McCombie WR, Hannon GJ, Smith AD. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell. 2011;146(6):1029\u201341.","journal-title":"Cell"},{"issue":"10","key":"4764_CR49","doi-asserted-by":"publisher","first-page":"e44479","DOI":"10.1371\/journal.pone.0044479","volume":"7","author":"C Krausz","year":"2012","unstructured":"Krausz C, Sandoval J, Sayols S, Chianese C, Giachini C, Heyn H, Esteller M. Novel insights into DNA methylation features in spermatozoa: stability and peculiarities. PLoS One. 2012;7(10):e44479.","journal-title":"PLoS One"},{"issue":"21","key":"4764_CR50","doi-asserted-by":"publisher","first-page":"2312","DOI":"10.1101\/gad.261925.115","volume":"29","author":"SS Hammoud","year":"2015","unstructured":"Hammoud SS, Low DH, Yi C, Lee CL, Oatley JM, Payne CJ, Carrell DT, Guccione E, Cairns BR. Transcription and imprinting dynamics in developing postnatal male germline stem cells. Genes Dev. 2015;29(21):2312\u201324.","journal-title":"Genes Dev"},{"issue":"10","key":"4764_CR51","doi-asserted-by":"publisher","first-page":"e47892","DOI":"10.1371\/journal.pone.0047892","volume":"7","author":"H Heyn","year":"2012","unstructured":"Heyn H, Ferreira HJ, Bassas L, Bonache S, Sayols S, Sandoval J, Esteller M, Larriba S. Epigenetic disruption of the PIWI pathway in human spermatogenic disorders. PLoS One. 2012;7(10):e47892.","journal-title":"PLoS One"},{"issue":"1","key":"4764_CR52","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.devcel.2016.03.010","volume":"37","author":"H Royo","year":"2016","unstructured":"Royo H, Stadler MB, Peters AH. Alternative computational analysis shows no evidence for nucleosome enrichment at repetitive sequences in mammalian spermatozoa. Dev Cell. 2016;37(1):98\u2013104.","journal-title":"Dev Cell"},{"issue":"1","key":"4764_CR53","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/j.devcel.2016.03.020","volume":"37","author":"T Dansranjavin","year":"2016","unstructured":"Dansranjavin T, Schagdarsurengin U. The rationale of the inevitable, or why is the consideration of repetitive DNA elements indispensable in studies of sperm nucleosomes. Dev Cell. 2016;37(1):13\u20134.","journal-title":"Dev Cell"},{"issue":"2","key":"4764_CR54","doi-asserted-by":"publisher","first-page":"695","DOI":"10.1016\/0006-291X(83)91782-5","volume":"113","author":"RL Adams","year":"1983","unstructured":"Adams RL, Burdon RH, Fulton J. Methylation of satellite DNA. Biochem Biophys Res Commun. 1983;113(2):695\u2013702.","journal-title":"Biochem Biophys Res Commun"},{"issue":"11","key":"4764_CR55","doi-asserted-by":"publisher","first-page":"3969","DOI":"10.1093\/nar\/13.11.3969","volume":"13","author":"SI Feinstein","year":"1985","unstructured":"Feinstein SI, Racaniello VR, Ehrlich M, Gehrke CW, Miller DA, Miller OJ. Pattern of undermethylation of the major satellite DNA of mouse sperm. Nucleic Acids Res. 1985;13(11):3969\u201378.","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"4764_CR56","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1016\/j.ydbio.2007.09.041","volume":"312","author":"K Yamagata","year":"2007","unstructured":"Yamagata K, Yamazaki T, Miki H, Ogonuki N, Inoue K, Ogura A, Baba T. Centromeric DNA hypomethylation as an epigenetic signature discriminates between germ and somatic cell lineages. Dev Biol. 2007;312(1):419\u201326.","journal-title":"Dev Biol"},{"issue":"1","key":"4764_CR57","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1007\/s10577-016-9547-3","volume":"25","author":"G Nishibuchi","year":"2017","unstructured":"Nishibuchi G, Dejardin J. The molecular basis of the organization of repetitive DNA-containing constitutive heterochromatin in mammals. Chromosom Res. 2017;25(1):77\u201387.","journal-title":"Chromosom Res"},{"issue":"3","key":"4764_CR58","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1007\/s10577-015-9499-z","volume":"23","author":"MA Biscotti","year":"2015","unstructured":"Biscotti MA, Olmo E, Heslop-Harrison JS. Repetitive DNA in eukaryotic genomes. Chromosom Res. 2015;23(3):415\u201320.","journal-title":"Chromosom Res"},{"issue":"4","key":"4764_CR59","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1016\/j.devcel.2010.09.002","volume":"19","author":"AV Probst","year":"2010","unstructured":"Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, Almouzni G. A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell. 2010;19(4):625\u201338.","journal-title":"Dev Cell"},{"issue":"Suppl 4","key":"4764_CR60","doi-asserted-by":"publisher","first-page":"S3","DOI":"10.1186\/1753-6561-5-S4-S3","volume":"5","author":"M Kaneda","year":"2011","unstructured":"Kaneda M, Akagi S, Watanabe S, Nagai T. Comparison of DNA methylation levels of repetitive loci during bovine development. BMC Proc. 2011;5(Suppl 4):S3.","journal-title":"BMC Proc"},{"issue":"1","key":"4764_CR61","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1002\/mrd.20249","volume":"71","author":"YK Kang","year":"2005","unstructured":"Kang YK, Lee HJ, Shim JJ, Yeo S, Kim SH, Koo DB, Lee KK, Beyhan Z, First NL, Han YM. Varied patterns of DNA methylation change between different satellite regions in bovine preimplantation development. Mol Reprod Dev. 2005;71(1):29\u201335.","journal-title":"Mol Reprod Dev"},{"issue":"4","key":"4764_CR62","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1111\/j.1740-0929.2011.00881.x","volume":"82","author":"K Yamanaka","year":"2011","unstructured":"Yamanaka K, Kaneda M, Inaba Y, Saito K, Kubota K, Sakatani M, Sugimura S, Imai K, Watanabe S, Takahashi M. DNA methylation analysis on satellite I region in blastocysts obtained from somatic cell cloned cattle. Anim Sci J. 2011;82(4):523\u201330.","journal-title":"Anim Sci J"},{"issue":"3","key":"4764_CR63","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1262\/jrd.10-181A","volume":"57","author":"K Yamanaka","year":"2011","unstructured":"Yamanaka K, Sakatani M, Kubota K, Balboula AZ, Sawai K, Takahashi M. Effects of downregulating DNA methyltransferase 1 transcript by RNA interference on DNA methylation status of the satellite I region and in vitro development of bovine somatic cell nuclear transfer embryos. J Reprod Dev. 2011;57(3):393\u2013402.","journal-title":"J Reprod Dev"},{"issue":"2","key":"4764_CR64","doi-asserted-by":"publisher","first-page":"e55153","DOI":"10.1371\/journal.pone.0055153","volume":"8","author":"C Couldrey","year":"2013","unstructured":"Couldrey C, Wells DN. DNA methylation at a bovine alpha satellite I repeat CpG site during development following fertilization and somatic cell nuclear transfer. PLoS One. 2013;8(2):e55153.","journal-title":"PLoS One"},{"issue":"19","key":"4764_CR65","doi-asserted-by":"publisher","first-page":"2272","DOI":"10.1093\/hmg\/ddm179","volume":"16","author":"Y Kato","year":"2007","unstructured":"Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M, Kohara Y, Okano M, Li E, Nozaki M, Sasaki H. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum Mol Genet. 2007;16(19):2272\u201380.","journal-title":"Hum Mol Genet"},{"issue":"3","key":"4764_CR66","doi-asserted-by":"publisher","first-page":"578","DOI":"10.3390\/biology3030578","volume":"3","author":"EL Walton","year":"2014","unstructured":"Walton EL, Francastel C, Velasco G. Dnmt3b prefers germ line genes and Centromeric regions: lessons from the ICF syndrome and Cancer and implications for diseases. Biol. 2014;3(3):578\u2013605.","journal-title":"Biol"},{"issue":"1","key":"4764_CR67","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.devcel.2014.05.023","volume":"30","author":"B Samans","year":"2014","unstructured":"Samans B, Yang Y, Krebs S, Sarode GV, Blum H, Reichenbach M, Wolf E, Steger K, Dansranjavin T, Schagdarsurengin U. Uniformity of nucleosome preservation pattern in mammalian sperm and its connection to repetitive DNA elements. Dev Cell. 2014;30(1):23\u201335.","journal-title":"Dev Cell"},{"issue":"3","key":"4764_CR68","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1530\/REP-16-0441","volume":"153","author":"G Sillaste","year":"2017","unstructured":"Sillaste G, Kaplinski L, Meier R, Jaakma U, Eriste E, Salumets A. A novel hypothesis for histone-to-protamine transition in Bos taurus spermatozoa. Reprod. 2017;153(3):241\u201351.","journal-title":"Reprod"},{"issue":"7","key":"4764_CR69","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1038\/nsmb.2599","volume":"20","author":"S Erkek","year":"2013","unstructured":"Erkek S, Hisano M, Liang CY, Gill M, Murr R, Dieker J, Schubeler D, van der Vlag J, Stadler MB, Peters AH. Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat Struct Mol Biol. 2013;20(7):868\u201375.","journal-title":"Nat Struct Mol Biol"},{"issue":"1","key":"4764_CR70","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1111\/j.1432-1033.1978.tb12155.x","volume":"84","author":"G Macaya","year":"1978","unstructured":"Macaya G, Cortadas J, Bernardi G. An analysis of the bovine genome by density-gradient centrifugation. Preparation of the dG+dC-rich DNA components. Eur J Biochem. 1978;84(1):179\u201388.","journal-title":"Eur J Biochem"},{"issue":"1","key":"4764_CR71","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1159\/000350444","volume":"140","author":"M Vozdova","year":"2013","unstructured":"Vozdova M, Sebestova H, Kubickova S, Cernohorska H, Vahala J, Rubes J. A comparative study of meiotic recombination in cattle (Bos taurus) and three wildebeest species (Connochaetes gnou, C. Taurinus taurinus and C. t. Albojubatus). Cytogenet Genome Res. 2013;140(1):36\u201345.","journal-title":"Cytogenet Genome Res"},{"issue":"11","key":"4764_CR72","doi-asserted-by":"publisher","first-page":"e1005387","DOI":"10.1371\/journal.pgen.1005387","volume":"11","author":"L Ma","year":"2015","unstructured":"Ma L, O'Connell JR, VanRaden PM, Shen B, Padhi A, Sun C, Bickhart DM, Cole JB, Null DJ, Liu GE, et al. Cattle sex-specific recombination and genetic control from a large pedigree analysis. PLoS Genet. 2015;11(11):e1005387.","journal-title":"PLoS Genet"},{"issue":"10","key":"4764_CR73","doi-asserted-by":"publisher","first-page":"1323","DOI":"10.1101\/gr.204214.116","volume":"26","author":"NK Kadri","year":"2016","unstructured":"Kadri NK, Harland C, Faux P, Cambisano N, Karim L, Coppieters W, Fritz S, Mullaart E, Baurain D, Boichard D, et al. Coding and noncoding variants in HFM1, MLH3, MSH4, MSH5, RNF212, and RNF212B affect recombination rate in cattle. Genome Res. 2016;26(10):1323\u201332.","journal-title":"Genome Res"},{"issue":"2","key":"4764_CR74","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1007\/s00412-016-0574-9","volume":"125","author":"P Termolino","year":"2016","unstructured":"Termolino P, Cremona G, Consiglio MF, Conicella C. Insights into epigenetic landscape of recombination-free regions. Chromosoma. 2016;125(2):301\u20138.","journal-title":"Chromosoma"},{"key":"4764_CR75","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1186\/1471-2164-10-571","volume":"10","author":"GE Liu","year":"2009","unstructured":"Liu GE, Ventura M, Cellamare A, Chen L, Cheng Z, Zhu B, Li C, Song J, Eichler EE. Analysis of recent segmental duplications in the bovine genome. BMC Genomics. 2009;10:571.","journal-title":"BMC Genomics"},{"key":"4764_CR76","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1186\/1471-2164-11-284","volume":"11","author":"J Fadista","year":"2010","unstructured":"Fadista J, Thomsen B, Holm LE, Bendixen C. Copy number variation in the bovine genome. BMC Genomics. 2010;11:284.","journal-title":"BMC Genomics"},{"issue":"5","key":"4764_CR77","doi-asserted-by":"publisher","first-page":"e1002692","DOI":"10.1371\/journal.pgen.1002692","volume":"8","author":"J Li","year":"2012","unstructured":"Li J, Harris RA, Cheung SW, Coarfa C, Jeong M, Goodell MA, White LD, Patel A, Kang SH, Shaw C, et al. Genomic hypomethylation in the human germline associates with selective structural mutability in the human genome. PLoS Genet. 2012;8(5):e1002692.","journal-title":"PLoS Genet"}],"container-title":["BMC Genomics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-018-4764-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12864-018-4764-0\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-018-4764-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,5,28]],"date-time":"2019-05-28T19:06:11Z","timestamp":1559070371000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcgenomics.biomedcentral.com\/articles\/10.1186\/s12864-018-4764-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,5,29]]},"references-count":77,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2018,12]]}},"alternative-id":["4764"],"URL":"https:\/\/doi.org\/10.1186\/s12864-018-4764-0","relation":{},"ISSN":["1471-2164"],"issn-type":[{"value":"1471-2164","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,5,29]]},"assertion":[{"value":"12 September 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 May 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 May 2018","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"All study methods were implemented in accordance with EU guidelines and regulations (Directive 2010\/63\/UE). For animals maintained in INRA facilities, the experimental protocols were approved by the INRA local Ethics Committee (COMETHEA, authorization numbers 12\/160 and M\u00e9jusseaumes Animal Care committee 0162503). Mice semen samples were collected from 7-week-old male C57Bl\/6JOlaHsd mice supplied by Harlan Laboratory (Venray, Netherlands) and euthanized by cervical dislocation. The bull samples were provided by commercial companies: Montb\u00e9liarde breed by GEN\u2019IATEST (Roulans, France) and UMOTEST (Ceyzeriat, France), Holstein and Normande breeds by EVOLUTION (Rennes, France) and Belgian White Blue Breed by AWE (Ciney, Belgium); the ram, goat and boar semen were also supplied by commercial companies, Oson (France), CAPGENES (France) and Laboratoire National de Contr\u00f4le des Reproducteurs (LNCR, France), respectively. Stallion semen was supplied by Dr. M. Magistrini (UMR INRA 0085 PRC, Nouzilly, France). Human sperm samples from patients included in a PHRC METASPERME study, coordinated by Dr. R. Levy (Laboratoire d\u2019Histologie Embryologie Cytog\u00e9n\u00e9tique CECOS, H\u00f4pital Jean Verdier, Bondy, France); this study received the approval from French ethics board (Conseil d\u2019\u00e9valuation \u00e9thique pour les recherches en sant\u00e9, CERES) and all the patients gave their informed written consent to participate.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"The authors declare that they have no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Publisher\u2019s Note"}}],"article-number":"404"}}