{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,20]],"date-time":"2026-06-20T03:52:42Z","timestamp":1781927562317,"version":"3.54.5"},"reference-count":89,"publisher":"Japanese Society of Animal Reproduction","issue":"3","funder":[{"name":"JSPS KAKENHI","award":["22HP2009"],"award-info":[{"award-number":["22HP2009"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J. Reprod. Dev.","Journal of Reproduction and Development"],"published-print":{"date-parts":[[2026]]},"DOI":"10.1262\/jrd.2025-134","type":"journal-article","created":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T22:10:50Z","timestamp":1781734250000},"page":"267-273","source":"Crossref","is-referenced-by-count":0,"title":["The bull sperm epigenome: role in male fertility and transmission to the offspring"],"prefix":"10.1262","volume":"72","author":[{"given":"Inass","family":"BOURASSI","sequence":"first","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, UVSQ, INRAE, BREED, 78350, Jouy-en-Josas, France"},{"name":"Ecole Nationale V\u00e9t\u00e9rinaire d\u2019Alfort, BREED, 94700, Maisons-Alfort, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amrita","family":"RAJA-RAVI-SHANKAR","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, UVSQ, INRAE, BREED, 78350, Jouy-en-Josas, France"},{"name":"Ecole Nationale V\u00e9t\u00e9rinaire d\u2019Alfort, BREED, 94700, Maisons-Alfort, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eliaou","family":"SELLEM","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, UVSQ, INRAE, BREED, 78350, Jouy-en-Josas, France"},{"name":"Ecole Nationale V\u00e9t\u00e9rinaire d\u2019Alfort, BREED, 94700, Maisons-Alfort, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H\u00e9l\u00e8ne","family":"KIEFER","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, UVSQ, INRAE, BREED, 78350, Jouy-en-Josas, France"},{"name":"Ecole Nationale V\u00e9t\u00e9rinaire d\u2019Alfort, BREED, 94700, Maisons-Alfort, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"349","reference":[{"key":"1","doi-asserted-by":"crossref","unstructured":"1. Smith ZD, Hetzel S, Meissner A. DNA methylation in mammalian development and disease. Nat Rev Genet<\/i> 2025; 26: 7\u201330.","DOI":"10.1038\/s41576-024-00760-8"},{"key":"2","doi-asserted-by":"crossref","unstructured":"2. Mill\u00e1n-Zambrano G, Burton A, Bannister AJ, Schneider R. Histone post-translational modifications - cause and consequence of genome function. Nat Rev Genet<\/i> 2022; 23: 563\u2013580.","DOI":"10.1038\/s41576-022-00468-7"},{"key":"3","doi-asserted-by":"crossref","unstructured":"3. Jonas S, Izaurralde E. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet<\/i> 2015; 16: 421\u2013433.","DOI":"10.1038\/nrg3965"},{"key":"4","doi-asserted-by":"crossref","unstructured":"4. Carrell DT. Epigenetics of the male gamete. Fertil Steril<\/i> 2012; 97: 267\u2013274.","DOI":"10.1016\/j.fertnstert.2011.12.036"},{"key":"5","doi-asserted-by":"crossref","unstructured":"5. Champroux A, Torres-Carreira J, Gharagozloo P, Drevet JR, Kocer A. Mammalian sperm nuclear organization: resiliencies and vulnerabilities. Basic Clin Androl<\/i> 2016; 26: 17.","DOI":"10.1186\/s12610-016-0044-5"},{"key":"6","doi-asserted-by":"crossref","unstructured":"6. Rivera RM. Consequences of assisted reproductive techniques on the embryonic epigenome in cattle. Reprod Fertil Dev<\/i> 2019; 32: 65\u201381.","DOI":"10.1071\/RD19276"},{"key":"7","doi-asserted-by":"crossref","unstructured":"7. Wu C, Sirard MA. Parental effects on epigenetic programming in gametes and embryos of dairy cows. Front Genet<\/i> 2020; 11: 557846.","DOI":"10.3389\/fgene.2020.557846"},{"key":"8","doi-asserted-by":"crossref","unstructured":"8. Tang WW, Kobayashi T, Irie N, Dietmann S, Surani MA. Specification and epigenetic programming of the human germ line. Nat Rev Genet<\/i> 2016; 17: 585\u2013600.","DOI":"10.1038\/nrg.2016.88"},{"key":"9","doi-asserted-by":"crossref","unstructured":"9. Hill PWS, Leitch HG, Requena CE, Sun Z, Amouroux R, Roman-Trufero M, Borkowska M, Terragni J, Vaisvila R, Linnett S, Bagci H, Dharmalingham G, Haberle V, Lenhard B, Zheng Y, Pradhan S, Hajkova P. Epigenetic reprogramming enables the transition from primordial germ cell to gonocyte. Nature<\/i> 2018; 555: 392\u2013396.","DOI":"10.1038\/nature25964"},{"key":"10","doi-asserted-by":"crossref","unstructured":"10. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature<\/i> 2004; 429: 900\u2013903.","DOI":"10.1038\/nature02633"},{"key":"11","doi-asserted-by":"crossref","unstructured":"11. Dura M, Teissandier A, Armand M, Barau J, Lapoujade C, Fouchet P, Bonneville L, Schulz M, Weber M, Baudrin LG, Lameiras S, Bourc\u2019his D. DNMT3A-dependent DNA methylation is required for spermatogonial stem cells to commit to spermatogenesis. Nat Genet<\/i> 2022; 54: 469\u2013480.","DOI":"10.1038\/s41588-022-01040-z"},{"key":"12","doi-asserted-by":"crossref","unstructured":"12. Bourc\u2019his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature<\/i> 2004; 431: 96\u201399.","DOI":"10.1038\/nature02886"},{"key":"13","doi-asserted-by":"crossref","unstructured":"13. Barau J, Teissandier A, Zamudio N, Roy S, Nalesso V, H\u00e9rault Y, Guillou F, Bourc\u2019his D. The DNA methyltransferase DNMT3C protects male germ cells from transposon activity. Science<\/i> 2016; 354: 909\u2013912.","DOI":"10.1126\/science.aah5143"},{"key":"14","doi-asserted-by":"crossref","unstructured":"14. Tang Q, Chen Y, Wu W, Ding H, Xia Y, Chen D, Wang X. Idiopathic male infertility and polymorphisms in the DNA methyltransferase genes involved in epigenetic marking. Sci Rep<\/i> 2017; 7: 11219.","DOI":"10.1038\/s41598-017-11636-9"},{"key":"15","doi-asserted-by":"crossref","unstructured":"15. Wang C, Lin H. Roles of piRNAs in transposon and pseudogene regulation of germline mRNAs and lncRNAs. Genome Biol<\/i> 2021; 22: 27.","DOI":"10.1186\/s13059-020-02221-x"},{"key":"16","doi-asserted-by":"crossref","unstructured":"16. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev Biol<\/i> 2007; 307: 368\u2013379.","DOI":"10.1016\/j.ydbio.2007.05.002"},{"key":"17","doi-asserted-by":"crossref","unstructured":"17. Ben Maamar M, Beck D, Nilsson E, McCarrey JR, Skinner MK. Developmental alterations in DNA methylation during gametogenesis from primordial germ cells to sperm. iScience<\/i> 2022; 25: 103786.","DOI":"10.1016\/j.isci.2022.103786"},{"key":"18","doi-asserted-by":"crossref","unstructured":"18. Siebert-Kuss LM, Dietrich V, Di Persio S, Bhaskaran J, Stehling M, Cremers JF, Sandmann S, Varghese J, Kliesch S, Schlatt S, Vaquerizas JM, Neuhaus N, Laurentino S. Genome-wide DNA methylation changes in human spermatogenesis. Am J Hum Genet<\/i> 2024; 111: 1125\u20131139.","DOI":"10.1016\/j.ajhg.2024.04.017"},{"key":"19","doi-asserted-by":"crossref","unstructured":"19. Huang Y, Li L, An G, Yang X, Cui M, Song X, Lin J, Zhang X, Yao Z, Wan C, Zhou C, Zhao J, Song K, Ren S, Xia X, Fu X, Lan Y, Hu X, Wang W, Wang M, Zheng Y, Miao K, Bai X, Hutchins AP, Chang G, Gao S, Zhao XY. Single-cell multi-omics sequencing of human spermatogenesis reveals a DNA demethylation event associated with male meiotic recombination. Nat Cell Biol<\/i> 2023; 25: 1520\u20131534.","DOI":"10.1038\/s41556-023-01232-7"},{"key":"20","doi-asserted-by":"crossref","unstructured":"20. Gaysinskaya V, Miller BF, De Luca C, van der Heijden GW, Hansen KD, Bortvin A. Transient reduction of DNA methylation at the onset of meiosis in male mice. Epigenetics Chromatin<\/i> 2018; 11: 15.","DOI":"10.1186\/s13072-018-0186-0"},{"key":"21","doi-asserted-by":"crossref","unstructured":"21. Capra E, Turri F, Lazzari B, Biffani S, Lange Consiglio A, Ajmone Marsan P, Stella A, Pizzi F. CpG DNA methylation changes during epididymal sperm maturation in bulls. Epigenetics Chromatin<\/i> 2023; 16: 20.","DOI":"10.1186\/s13072-023-00495-6"},{"key":"22","doi-asserted-by":"crossref","unstructured":"22. Galan C, Serra RW, Sun F, Rinaldi VD, Conine CC, Rando OJ. Stability of the cytosine methylome during post-testicular sperm maturation in mouse. PLoS Genet<\/i> 2021; 17: e1009416.","DOI":"10.1371\/journal.pgen.1009416"},{"key":"23","doi-asserted-by":"crossref","unstructured":"23. Chen H, Scott-Boyer MP, Droit A, Robert C, Belleann\u00e9e C. Sperm heterogeneity accounts for sperm DNA methylation variations observed in the caput epididymis, independently from DNMT\/TET activities. Front Cell Dev Biol<\/i> 2022; 10: 834519.","DOI":"10.3389\/fcell.2022.834519"},{"key":"24","doi-asserted-by":"crossref","unstructured":"24. 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<\/i> 2013; 4: 2889.","DOI":"10.1038\/ncomms3889"},{"key":"25","doi-asserted-by":"crossref","unstructured":"25. Mart\u00ednez D, Pentinat T, Rib\u00f3 S, Daviaud C, Bloks VW, Cebri\u00e0 J, Villalmanzo N, Kalko SG, Ram\u00f3n-Krauel M, D\u00edaz R, Pl\u00f6sch T, Tost J, Jim\u00e9nez-Chillar\u00f3n JC. In utero undernutrition in male mice programs liver lipid metabolism in the second-generation offspring involving altered Lxra DNA methylation. Cell Metab<\/i> 2014; 19: 941\u2013951.","DOI":"10.1016\/j.cmet.2014.03.026"},{"key":"26","doi-asserted-by":"crossref","unstructured":"26. Toschi P, Capra E, Anzalone DA, Lazzari B, Turri F, Pizzi F, Scapolo PA, Stella A, Williams JL, Ajmone Marsan P, Loi P. Maternal peri-conceptional undernourishment perturbs offspring sperm methylome. Reproduction<\/i> 2020; 159: 513\u2013523.","DOI":"10.1530\/REP-19-0549"},{"key":"27","doi-asserted-by":"crossref","unstructured":"27. Perrier JP, Kenny DA, Chaulot-Talmon A, Byrne CJ, Sellem E, Jouneau L, Aubert-Frambourg A, Schibler L, Jammes H, Lonergan P, Fair S, Kiefer H. Accelerating onset of puberty through modification of early life nutrition induces modest but persistent changes in bull sperm DNA methylation profiles post-puberty. Front Genet<\/i> 2020; 11: 945.","DOI":"10.3389\/fgene.2020.00945"},{"key":"28","doi-asserted-by":"crossref","unstructured":"28. Johnson C, Kiefer H, Chaulot-Talmon A, Dance A, Sellem E, Jouneau L, Jammes H, Kastelic J, Thundathil J. Prepubertal nutritional modulation in the bull and its impact on sperm DNA methylation. Cell Tissue Res<\/i> 2022; 389: 587\u2013601.","DOI":"10.1007\/s00441-022-03659-0"},{"key":"29","doi-asserted-by":"crossref","unstructured":"29. Marcho C, Oluwayiose OA, Pilsner JR. The preconception environment and sperm epigenetics. Andrology<\/i> 2020; 8: 924\u2013942.","DOI":"10.1111\/andr.12753"},{"key":"30","doi-asserted-by":"crossref","unstructured":"30. Korhonen HM, Meikar O, Yadav RP, Papaioannou MD, Romero Y, Da Ros M, Herrera PL, Toppari J, Nef S, Kotaja N. Dicer is required for haploid male germ cell differentiation in mice. PLoS One<\/i> 2011; 6: e24821.","DOI":"10.1371\/journal.pone.0024821"},{"key":"31","doi-asserted-by":"crossref","unstructured":"31. Comazzetto S, Di Giacomo M, Rasmussen KD, Much C, Azzi C, Perlas E, Morgan M, O\u2019Carroll D. Oligoasthenoteratozoospermia and infertility in mice deficient for miR-34b\/c and miR-449 loci. PLoS Genet<\/i> 2014; 10: e1004597.","DOI":"10.1371\/journal.pgen.1004597"},{"key":"32","doi-asserted-by":"crossref","unstructured":"32. Niu Z, Goodyear SM, Rao S, Wu X, Tobias JW, Avarbock MR, Brinster RL. MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proc Natl Acad Sci USA<\/i> 2011; 108: 12740\u201312745.","DOI":"10.1073\/pnas.1109987108"},{"key":"33","doi-asserted-by":"crossref","unstructured":"33. He Z, Jiang J, Kokkinaki M, Tang L, Zeng W, Gallicano I, Dobrinski I, Dym M. MiRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1. Stem Cells<\/i> 2013; 31: 2205\u20132217.","DOI":"10.1002\/stem.1474"},{"key":"34","doi-asserted-by":"crossref","unstructured":"34. Huang YL, Huang GY, Lv J, Pan LN, Luo X, Shen J. miR-100 promotes the proliferation of spermatogonial stem cells via regulating Stat3. Mol Reprod Dev<\/i> 2017; 84: 693\u2013701.","DOI":"10.1002\/mrd.22843"},{"key":"35","doi-asserted-by":"crossref","unstructured":"35. de Mateo S, Sassone-Corsi P. Regulation of spermatogenesis by small non-coding RNAs: role of the germ granule. Semin Cell Dev Biol<\/i> 2014; 29: 84\u201392.","DOI":"10.1016\/j.semcdb.2014.04.021"},{"key":"36","doi-asserted-by":"crossref","unstructured":"36. Aravin AA, Sachidanandam R, Bourc\u2019his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell<\/i> 2008; 31: 785\u2013799.","DOI":"10.1016\/j.molcel.2008.09.003"},{"key":"37","doi-asserted-by":"crossref","unstructured":"37. Pillai RS, Chuma S. piRNAs and their involvement in male germline development in mice. Dev Growth Differ<\/i> 2012; 54: 78\u201392.","DOI":"10.1111\/j.1440-169X.2011.01320.x"},{"key":"38","doi-asserted-by":"crossref","unstructured":"38. Chuma S, Nakano T. piRNA and spermatogenesis in mice. Philos Trans R Soc Lond B Biol Sci<\/i> 2013; 368: 20110338.","DOI":"10.1098\/rstb.2011.0338"},{"key":"39","doi-asserted-by":"crossref","unstructured":"39. Sellem E, Marthey S, Rau A, Jouneau L, Bonnet A, Perrier JP, Fritz S, Le Danvic C, Boussaha M, Kiefer H, Jammes H, Schibler L. A comprehensive overview of bull sperm-borne small non-coding RNAs and their diversity across breeds. Epigenetics Chromatin<\/i> 2020; 13: 19.","DOI":"10.1186\/s13072-020-00340-0"},{"key":"40","doi-asserted-by":"crossref","unstructured":"40. Capra E, Turri F, Lazzari B, Cremonesi P, Gliozzi TM, Fojadelli I, Stella A, Pizzi F. Small RNA sequencing of cryopreserved semen from single bull revealed altered miRNAs and piRNAs expression between High- and Low-motile sperm populations. BMC Genomics<\/i> 2017; 18: 14.","DOI":"10.1186\/s12864-016-3394-7"},{"key":"41","doi-asserted-by":"crossref","unstructured":"41. Stowe HM, Calcatera SM, Dimmick MA, Andrae JG, Duckett SK, Pratt SL. The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression. PLoS One<\/i> 2014; 9: e113163.","DOI":"10.1371\/journal.pone.0113163"},{"key":"42","doi-asserted-by":"crossref","unstructured":"42. Zhang Y, Labrecque R, Tremblay P, Plessis C, Dufour P, Martin H, Sirard MA. Sperm-borne tsRNAs and miRNAs analysis in relation to dairy cattle fertility. Theriogenology<\/i> 2024; 215: 241\u2013248.","DOI":"10.1016\/j.theriogenology.2023.11.029"},{"key":"43","doi-asserted-by":"crossref","unstructured":"43. Sellem E, Marthey S, Rau A, Jouneau L, Bonnet A, Le Danvic C, Guyonnet B, Kiefer H, Jammes H, Schibler L. Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm. Epigenetics Chromatin<\/i> 2021; 14: 24.","DOI":"10.1186\/s13072-021-00397-5"},{"key":"44","doi-asserted-by":"crossref","unstructured":"44. Chu C, Zhang YL, Yu L, Sharma S, Fei ZL, Drevet JR. Epididymal small non-coding RNA studies: progress over the past decade. Andrology<\/i> 2019; 7: 681\u2013689.","DOI":"10.1111\/andr.12639"},{"key":"45","doi-asserted-by":"crossref","unstructured":"45. Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY, Belleannee C, Kucukural A, Serra RW, Sun F, Song L, Carone BR, Ricci EP, Li XZ, Fauquier L, Moore MJ, Sullivan R, Mello CC, Garber M, Rando OJ. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science<\/i> 2016; 351: 391\u2013396.","DOI":"10.1126\/science.aad6780"},{"key":"46","doi-asserted-by":"crossref","unstructured":"46. Zhang Y, Bruna de Lima C, Labrecque R, Sirard MA. Whole-genome DNA methylation analysis of the sperm in relation to bull fertility. Reproduction<\/i> 2023; 165: 557\u2013568.","DOI":"10.1530\/REP-22-0283"},{"key":"47","doi-asserted-by":"crossref","unstructured":"47. 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<\/i> 2017; 18: 280.","DOI":"10.1186\/s12864-017-3673-y"},{"key":"48","doi-asserted-by":"crossref","unstructured":"48. Gross N, Pe\u00f1agaricano F, Khatib H. Integration of whole-genome DNA methylation data with RNA sequencing data to identify markers for bull fertility. Anim Genet<\/i> 2020; 51: 502\u2013510.","DOI":"10.1111\/age.12941"},{"key":"49","doi-asserted-by":"crossref","unstructured":"49. Narud B, Khezri A, Zeremichael TT, Stenseth EB, Heringstad B, Johannisson A, Morrell JM, Collas P, Myromslien FD, Kommisrud E. Sperm chromatin integrity and DNA methylation in Norwegian Red bulls of contrasting fertility. Mol Reprod Dev<\/i> 2021; 88: 187\u2013200.","DOI":"10.1002\/mrd.23461"},{"key":"50","doi-asserted-by":"crossref","unstructured":"50. Takeda K, Kobayashi E, Ogata K, Imai A, Sato S, Adachi H, Hoshino Y, Nishino K, Inoue M, Kaneda M, Watanabe S. Differentially methylated CpG sites related to fertility in Japanese Black bull spermatozoa: epigenetic biomarker candidates to predict sire conception rate. J Reprod Dev<\/i> 2021; 67: 99\u2013107.","DOI":"10.1262\/jrd.2020-137"},{"key":"51","doi-asserted-by":"crossref","unstructured":"51. \u0160tiavnick\u00e1 M, Chaulot-Talmon A, Perrier JP, Ho\u0161ek P, Kenny DA, Lonergan P, Kiefer H, Fair S. Sperm DNA methylation patterns at discrete CpGs and genes involved in embryonic development are related to bull fertility. BMC Genomics<\/i> 2022; 23: 379.","DOI":"10.1186\/s12864-022-08614-5"},{"key":"52","doi-asserted-by":"crossref","unstructured":"52. \u00c5senius F, Danson AF, Marzi SJ. DNA methylation in human sperm: a systematic review. Hum Reprod Update<\/i> 2020; 26: 841\u2013873.","DOI":"10.1093\/humupd\/dmaa025"},{"key":"53","doi-asserted-by":"crossref","unstructured":"53. 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<\/i> 2015; 104: 1388\u20131397.e5.","DOI":"10.1016\/j.fertnstert.2015.08.019"},{"key":"54","doi-asserted-by":"crossref","unstructured":"54. Costes V, Chaulot-Talmon A, Sellem E, Perrier JP, Aubert-Frambourg A, Jouneau L, Pontlevoy C, Hoz\u00e9 C, Fritz S, Boussaha M, Le Danvic C, Sanchez MP, Boichard D, Schibler L, Jammes H, Jaffr\u00e9zic F, Kiefer H. Predicting male fertility from the sperm methylome: application to 120 bulls with hundreds of artificial insemination records. Clin Epigenetics<\/i> 2022; 14: 54.","DOI":"10.1186\/s13148-022-01275-x"},{"key":"55","doi-asserted-by":"crossref","unstructured":"55. Hua M, Liu W, Chen Y, Zhang F, Xu B, Liu S, Chen G, Shi H, Wu L. Identification of small non-coding RNAs as sperm quality biomarkers for in vitro fertilization. Cell Discov<\/i> 2019; 5: 20.","DOI":"10.1038\/s41421-019-0087-9"},{"key":"56","doi-asserted-by":"crossref","unstructured":"56. Alves MBR, Celeghini ECC, Belleann\u00e9e C. From sperm motility to sperm-borne microRNA signatures: new approaches to predict male fertility potential. Front Cell Dev Biol<\/i> 2020; 8: 791.","DOI":"10.3389\/fcell.2020.00791"},{"key":"57","doi-asserted-by":"crossref","unstructured":"57. Mehta P, Singh R. The composition of human sperm sncRNAome: a cross-country small RNA profiling. Reprod Biol Endocrinol<\/i> 2025; 23: 36.","DOI":"10.1186\/s12958-025-01358-3"},{"key":"58","doi-asserted-by":"crossref","unstructured":"58. Fagerlind M, St\u00e5lhammar H, Olsson B, Klinga-Levan K. Expression of miRNAs in Bull Spermatozoa Correlates with Fertility Rates. Reprod Domest Anim<\/i> 2015; 50: 587\u2013594.","DOI":"10.1111\/rda.12531"},{"key":"59","doi-asserted-by":"crossref","unstructured":"59. Keles E, Malama E, Bozukova S, Siuda M, Wyck S, Witschi U, Bauersachs S, Bollwein H. The micro-RNA content of unsorted cryopreserved bovine sperm and its relation to the fertility of sperm after sex-sorting. BMC Genomics<\/i> 2021; 22: 30.","DOI":"10.1186\/s12864-020-07280-9"},{"key":"60","doi-asserted-by":"crossref","unstructured":"60. Donnellan EM, Perrier JP, Keogh K, \u0160tiavnick\u00e1 M, Collins CM, Dunleavy EM, Sellem E, Bernecic NC, Lonergan P, Kenny DA, Fair S. Identification of differentially expressed mRNAs and miRNAs in spermatozoa of bulls of varying fertility. Front Vet Sci<\/i> 2022; 9: 993561.","DOI":"10.3389\/fvets.2022.993561"},{"key":"61","doi-asserted-by":"crossref","unstructured":"61. Bodu M, Hitit M, Donmez H, Kaya A, Ugur MR, Memili E. Exploration of small non-coding RNAs as molecular markers of ram sperm fertility. Int J Mol Sci<\/i> 2025; 26: 2690.","DOI":"10.3390\/ijms26062690"},{"key":"62","doi-asserted-by":"crossref","unstructured":"62. Grosso JB, Zoff L, Calvo KL, Maraval MB, Perez M, Carbonaro M, Brignardello C, Morente C, Spinelli SV. Levels of seminal tRNA-derived fragments from normozoospermic men correlate with the success rate of ART. Mol Hum Reprod<\/i> 2021; 27: gaab017.","DOI":"10.1093\/molehr\/gaab017"},{"key":"63","doi-asserted-by":"crossref","unstructured":"63. Hekim N, Gunes S, Ayas B, Alkan EN. Seminal 5'tRF-Glu-CTC as a biomarker for oligozoospermia and ART outcome prediction. Basic Clin Androl<\/i> 2025; 35: 33.","DOI":"10.1186\/s12610-025-00283-0"},{"key":"64","doi-asserted-by":"crossref","unstructured":"64. Costes V, Sellem E, Marthey S, Hoze C, Bonnet A, Schibler L, Kiefer H, Jaffrezic F. Multi-omics data integration for the identification of biomarkers for bull fertility. PLoS One<\/i> 2024; 19: e0298623.","DOI":"10.1371\/journal.pone.0298623"},{"key":"65","doi-asserted-by":"crossref","unstructured":"65. Bakhtari A, Ross PJ. DPPA3 prevents cytosine hydroxymethylation of the maternal pronucleus and is required for normal development in bovine embryos. Epigenetics<\/i> 2014; 9: 1271\u20131279.","DOI":"10.4161\/epi.32087"},{"key":"66","doi-asserted-by":"crossref","unstructured":"66. Dobbs KB, Rodriguez M, Sudano MJ, Ortega MS, Hansen PJ. Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PLoS One<\/i> 2013; 8: e66230.","DOI":"10.1371\/journal.pone.0066230"},{"key":"67","doi-asserted-by":"crossref","unstructured":"67. Lepikhov K, Zakhartchenko V, Hao R, Yang F, Wrenzycki C, Niemann H, Wolf E, Walter J. Evidence for conserved DNA and histone H3 methylation reprogramming in mouse, bovine and rabbit zygotes. Epigenetics Chromatin<\/i> 2008; 1: 8.","DOI":"10.1186\/1756-8935-1-8"},{"key":"68","doi-asserted-by":"crossref","unstructured":"68. Duan JE, Jiang ZC, Alqahtani F, Mandoiu I, Dong H, Zheng X, Marjani SL, Chen J, Tian XC. Methylome dynamics of bovine gametes and in vivo<\/i> early embryos. Front Genet<\/i> 2019; 10: 512.","DOI":"10.3389\/fgene.2019.00512"},{"key":"69","doi-asserted-by":"crossref","unstructured":"69. Jiang Z, Lin J, Dong H, Zheng X, Marjani SL, Duan J, Ouyang Z, Chen J, Tian XC. DNA methylomes of bovine gametes and in vivo produced preimplantation embryos. Biol Reprod<\/i> 2018; 99: 949\u2013959.","DOI":"10.1093\/biolre\/ioy138"},{"key":"70","doi-asserted-by":"crossref","unstructured":"70. Halstead MM, Ma X, Zhou C, Schultz RM, Ross PJ. Chromatin remodeling in bovine embryos indicates species-specific regulation of genome activation. Nat Commun<\/i> 2020; 11: 4654.","DOI":"10.1038\/s41467-020-18508-3"},{"key":"71","doi-asserted-by":"crossref","unstructured":"71. Liu S, Holmes AD, Gupta A, Katzman S, Sharma U. Epididymal dynamics and preimplantation roles of a sperm-enriched 5\u2032 fragment of tRNA-valine. Cell Rep<\/i> 2025; 44: 116366.","DOI":"10.1016\/j.celrep.2025.116366"},{"key":"72","doi-asserted-by":"crossref","unstructured":"72. Conine CC, Sun F, Song L, Rivera-P\u00e9rez JA, Rando OJ. Small RNAs gained during epididymal transit of sperm are essential for embryonic development in mice. Dev Cell<\/i> 2018; 46: 470\u2013480.e3.","DOI":"10.1016\/j.devcel.2018.06.024"},{"key":"73","doi-asserted-by":"crossref","unstructured":"73. Trigg NA, Conine CC. Epididymal acquired sperm microRNAs modify post-fertilization embryonic gene expression. Cell Rep<\/i> 2024; 43: 114698.","DOI":"10.1016\/j.celrep.2024.114698"},{"key":"74","doi-asserted-by":"crossref","unstructured":"74. Donkin I, Barr\u00e8s R. Sperm epigenetics and influence of environmental factors. Mol Metab<\/i> 2018; 14: 1\u201311.","DOI":"10.1016\/j.molmet.2018.02.006"},{"key":"75","doi-asserted-by":"crossref","unstructured":"75. Champroux A, Cocquet J, Henry-Berger J, Drevet JR, Kocer A. A Decade of Exploring the Mammalian Sperm Epigenome: Paternal Epigenetic and Transgenerational Inheritance. Front Cell Dev Biol<\/i> 2018; 6: 50.","DOI":"10.3389\/fcell.2018.00050"},{"key":"76","doi-asserted-by":"crossref","unstructured":"76. Horii T, Morita S, Hino S, Hino Y, Fukushima HS, Kobayashi R, Kimura M, Nakao M, Mizukami Y, Inoue A, Hatada I. Germline epigenome editing identifies H3K9me3 as a mediator of intergenerational DNA methylation recovery in mice. Nat Commun<\/i> 2025; 16: 11200.","DOI":"10.1038\/s41467-025-67488-9"},{"key":"77","doi-asserted-by":"crossref","unstructured":"77. Seah MKY, Messerschmidt DM. From germline to soma: epigenetic dynamics in the mouse preimplantation embryo. Curr Top Dev Biol<\/i> 2018; 128: 203\u2013235.","DOI":"10.1016\/bs.ctdb.2017.10.011"},{"key":"78","doi-asserted-by":"crossref","unstructured":"78. Takahashi Y, Morales Valencia M, Yu Y, Ouchi Y, Takahashi K, Shokhirev MN, Lande K, Williams AE, Fresia C, Kurita M, Hishida T, Shojima K, Hatanaka F, Nu\u00f1ez-Delicado E, Esteban CR, Izpisua Belmonte JC. Transgenerational inheritance of acquired epigenetic signatures at CpG islands in mice. Cell<\/i> 2023; 186: 715\u2013731.e19.","DOI":"10.1016\/j.cell.2022.12.047"},{"key":"79","doi-asserted-by":"crossref","unstructured":"79. Kremsky I, Corces VG. Protection from DNA re-methylation by transcription factors in primordial germ cells and pre-implantation embryos can explain trans-generational epigenetic inheritance. Genome Biol<\/i> 2020; 21: 118.","DOI":"10.1186\/s13059-020-02036-w"},{"key":"80","doi-asserted-by":"crossref","unstructured":"80. Braz CU, Taylor T, Namous H, Townsend J, Crenshaw T, Khatib H. Paternal diet induces transgenerational epigenetic inheritance of DNA methylation signatures and phenotypes in sheep model. PNAS Nexus<\/i> 2022; 1: pgac040.","DOI":"10.1093\/pnasnexus\/pgac040"},{"key":"81","doi-asserted-by":"crossref","unstructured":"81. Fou\u00e9r\u00e9 C, Costes V, Hoz\u00e9 C, Raja Ravi Shankar A, Besnard F, Costa Monteiro Moreira G, Sorin V, Le Danvic C, Chaulot-Talmon A, Ali F, Deloche MC, Bonnet A, Sellem E, Jammes H, Fritz S, Boussaha M, Boichard D, Kiefer H, Sanchez MP. Genetic regulation of sperm DNA methylation in cattle through meQTL mapping. BMC Genomics<\/i> 2025; 26: 771.","DOI":"10.1186\/s12864-025-11934-x"},{"key":"82","doi-asserted-by":"crossref","unstructured":"82. Dahlen CR, Amat S, Caton JS, Crouse MS, Diniz WJDS, Reynolds LP. Paternal effects on fetal programming. Anim Reprod<\/i> 2023; 20: e20230076.","DOI":"10.1590\/1984-3143-ar2023-0076"},{"key":"83","doi-asserted-by":"crossref","unstructured":"83. Soubry A. POHaD: why we should study future fathers. Environ Epigenet<\/i> 2018; 4: dvy007.","DOI":"10.1093\/eep\/dvy007"},{"key":"84","doi-asserted-by":"crossref","unstructured":"84. Fanourgakis G, Gaspa-Toneu L, Komarov PA, Papasaikas P, Ozonov EA, Smallwood SA, Peters AHFM. DNA methylation modulates nucleosome retention in sperm and H3K4 methylation deposition in early mouse embryos. Nat Commun<\/i> 2025; 16: 465.","DOI":"10.1038\/s41467-024-55441-1"},{"key":"85","doi-asserted-by":"crossref","unstructured":"85. Wu C, Blondin P, Vigneault C, Labrecque R, Sirard MA. The age of the bull influences the transcriptome and epigenome of blastocysts produced by IVF. Theriogenology<\/i> 2020; 144: 122\u2013131.","DOI":"10.1016\/j.theriogenology.2019.12.020"},{"key":"86","doi-asserted-by":"crossref","unstructured":"86. da Silva DF, Rodrigues TA, da Silveira JC, Gonella-Diaza AM, Binelli M, Lopes JV, Moura MT, Feitosa WB, Paula-Lopes FF. Cellular responses and microRNA profiling in bovine spermatozoa under heat shock. Reproduction<\/i> 2022; 164: 155\u2013168.","DOI":"10.1530\/REP-21-0507"},{"key":"87","doi-asserted-by":"crossref","unstructured":"87. Chen Q, Yan W, Duan E. Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications. Nat Rev Genet<\/i> 2016; 17: 733\u2013743.","DOI":"10.1038\/nrg.2016.106"},{"key":"88","doi-asserted-by":"crossref","unstructured":"88. Rodgers AB, Morgan CP, Leu NA, Bale TL. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci USA<\/i> 2015; 112: 13699\u201313704.","DOI":"10.1073\/pnas.1508347112"},{"key":"89","doi-asserted-by":"crossref","unstructured":"89. Costes V., et alThe RUMIGEN EpiChip: a versatile, medium density DNA methylation Beadchip for large scale population studies in cattle.<\/i>bioRxiv<\/i> , 2025.","DOI":"10.64898\/2025.12.19.695474"}],"container-title":["Journal of Reproduction and Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/jrd\/72\/3\/72_2025-134\/_pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,20]],"date-time":"2026-06-20T03:25:59Z","timestamp":1781925959000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/jrd\/72\/3\/72_2025-134\/_article"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026]]},"references-count":89,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2026]]}},"URL":"https:\/\/doi.org\/10.1262\/jrd.2025-134","relation":{},"ISSN":["0916-8818","1348-4400"],"issn-type":[{"value":"0916-8818","type":"print"},{"value":"1348-4400","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026]]},"article-number":"2025-134"}}