{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T19:28:51Z","timestamp":1777577331538,"version":"3.51.4"},"reference-count":67,"publisher":"Springer Science and Business Media LLC","issue":"6","license":[{"start":{"date-parts":[[2025,1,3]],"date-time":"2025-01-03T00:00:00Z","timestamp":1735862400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,1,3]],"date-time":"2025-01-03T00:00:00Z","timestamp":1735862400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100006306","name":"Sigrid Jus\u00e9liuksen S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100006306","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004756","name":"Emil Aaltosen S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004756","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008723","name":"Suomen L\u00e4\u00e4ketieteen S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008723","id-type":"DOI","asserted-by":"publisher"}]},{"name":"State Research Grant"},{"DOI":"10.13039\/501100011747","name":"Novo Nordisk Foundation Center for Basic Metabolic Research","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100011747","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004325","name":"Signe ja Ane Gyllenbergin S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004325","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005609","name":"Turun Yliopisto","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100005609","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002341","name":"Academy of Finland","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002341","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009708","name":"Novo Nordisk Fonden","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100009708","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010125","name":"Jalmari ja Rauha Ahokkaan S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100010125","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004012","name":"Jane ja Aatos Erkon S\u00e4\u00e4ti\u00f6","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004012","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Mol Psychiatry"],"published-print":{"date-parts":[[2025,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:p>Childhood maltreatment exposure (CME) increases the risk of adverse long-term health consequences for the exposed individual. Animal studies suggest that CME may also influence the health and behaviour in the next generation offspring through CME-driven epigenetic changes in the germ line. Here we investigated the associated between early life stress on the epigenome of sperm in humans with history of CME. We measured paternal CME using the Trauma and Distress Scale (TADS) questionnaire and mapped sperm-borne sncRNAs expression by small RNA sequencing (small RNA-seq) and DNA methylation (DNAme) in spermatozoa by reduced-representation bisulfite sequencing (RRBS-seq) in males from the FinnBrain Birth Cohort Study. The study design was a (nested) case-control study, high-TADS (TADS\u2009\u2265\u200939, <jats:italic>n<\/jats:italic>\u2009=\u200925 for DNAme and <jats:italic>n<\/jats:italic>\u2009=\u200914 for small RNA-seq) and low-TADS (TADS\u2009\u2264\u200910, <jats:italic>n<\/jats:italic>\u2009=\u200930 for DNAme and <jats:italic>n<\/jats:italic>\u2009=\u200916 for small RNA-seq). We identified 3 genomic regions with differential methylation between low and high-TADS and 68 tRNA-derived small RNAs (tsRNAs) and miRNAs with different levels in males with high CME (False discovery rate, FDR corrected <jats:italic>p<\/jats:italic>\u2009&lt;\u20090.05). Of potential interest, we identified differential expression of miRNA hsa-mir-34c-5p and differential methylation levels near the <jats:italic>CRTC1<\/jats:italic> and <jats:italic>GBX2<\/jats:italic> genes, which are documented to control brain development. Our results provide further evidence that early life stress influences the paternal germline epigenome and supports a possible effect in modulating the development of the central nervous system of the next generation.<\/jats:p>","DOI":"10.1038\/s41380-024-02872-3","type":"journal-article","created":{"date-parts":[[2025,1,3]],"date-time":"2025-01-03T12:40:29Z","timestamp":1735908029000},"page":"2635-2644","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Exposure to childhood maltreatment is associated with specific epigenetic patterns in sperm"],"prefix":"10.1038","volume":"30","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1797-8000","authenticated-orcid":false,"given":"Jetro J.","family":"Tuulari","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9156-2807","authenticated-orcid":false,"given":"Matthieu","family":"Bourgery","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-2158-4597","authenticated-orcid":false,"given":"Jo","family":"Iversen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thomas Gade","family":"Koefoed","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Annukka","family":"Ahonen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ammar","family":"Ahmedani","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eeva-Leena","family":"Kataja","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4725-0176","authenticated-orcid":false,"given":"Linnea","family":"Karlsson","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Romain","family":"Barr\u00e8s","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hasse","family":"Karlsson","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Noora","family":"Kotaja","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2025,1,3]]},"reference":[{"key":"2872_CR1","doi-asserted-by":"publisher","first-page":"e848","DOI":"10.1016\/S2468-2667(21)00232-2","volume":"6","author":"K Hughes","year":"2021","unstructured":"Hughes K, Ford K, Bellis MA, Glendinning F, Harrison E, Passmore J. Health and financial costs of adverse childhood experiences in 28 European countries: a systematic review and meta-analysis. Lancet Public Health. 2021;6:e848\u201357.","journal-title":"Lancet Public Health"},{"key":"2872_CR2","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1002\/car.2353","volume":"24","author":"M Stoltenborgh","year":"2015","unstructured":"Stoltenborgh M, Bakermans\u2010Kranenburg MJ, Alink LRA, IJzendoorn MH. The prevalence of child maltreatment across the globe: review of a series of meta\u2010analyses. Child Abuse Rev. 2015;24:37\u201350.","journal-title":"Child Abuse Rev"},{"key":"2872_CR3","doi-asserted-by":"publisher","first-page":"649825","DOI":"10.3389\/fpubh.2021.649825","volume":"9","author":"S Soares","year":"2021","unstructured":"Soares S, Rocha V, Kelly-Irving M, Stringhini S, Fraga S. Adverse childhood events and health biomarkers: a systematic review. Front Public Health. 2021;9:649825.","journal-title":"Front Public Health"},{"key":"2872_CR4","doi-asserted-by":"publisher","first-page":"e300","DOI":"10.1016\/S2468-2667(17)30104-4","volume":"2","author":"G Sara","year":"2017","unstructured":"Sara G, Lappin J. Childhood trauma: psychiatry\u2019s greatest public health challenge? Lancet Public Health. 2017;2:e300\u20131.","journal-title":"Lancet Public Health"},{"key":"2872_CR5","doi-asserted-by":"publisher","first-page":"e0226134","DOI":"10.1371\/journal.pone.0226134","volume":"15","author":"GM Waehrer","year":"2020","unstructured":"Waehrer GM, Miller TR, Marques SCS, Oh DL, Harris NB. Disease burden of adverse childhood experiences across 14 states. Plos One. 2020;15:e0226134.","journal-title":"Plos One"},{"key":"2872_CR6","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1038\/s41398-018-0146-2","volume":"8","author":"DA Dickson","year":"2018","unstructured":"Dickson DA, Paulus JK, Mensah V, Lem J, Saavedra-Rodriguez L, Gentry A, et al. Reduced levels of miRNAs 449 and 34 in sperm of mice and men exposed to early life stress. Transl Psychiat. 2018;8:101.","journal-title":"Transl Psychiat"},{"key":"2872_CR7","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1016\/j.biopsych.2017.07.009","volume":"83","author":"NK Moog","year":"2018","unstructured":"Moog NK, Entringer S, Rasmussen JM, Styner M, Gilmore JH, Kathmann N, et al. Intergenerational effect of maternal exposure to childhood maltreatment on newborn brain anatomy. Biol Psychiat. 2018;83:120\u20137.","journal-title":"Biol Psychiat"},{"key":"2872_CR8","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1038\/s41398-018-0252-1","volume":"8","author":"AL Roberts","year":"2018","unstructured":"Roberts AL, Gladish N, Gatev E, Jones MJ, Chen Y, MacIsaac JL, et al. Exposure to childhood abuse is associated with human sperm DNA methylation. Transl Psychiat. 2018;8:194.","journal-title":"Transl Psychiat"},{"key":"2872_CR9","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1111\/jcpp.12877","volume":"60","author":"P Scorza","year":"2019","unstructured":"Scorza P, Duarte CS, Hipwell AE, Posner J, Ortin A, Canino G, et al. Research Review: Intergenerational transmission of disadvantage: epigenetics and parents\u2019 childhoods as the first exposure. J Child Psychol Psyc. 2019;60:119\u201332.","journal-title":"J Child Psychol Psyc"},{"key":"2872_CR10","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1002\/wps.20568","volume":"17","author":"R Yehuda","year":"2018","unstructured":"Yehuda R, Lehrner A. Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms. World Psychiatry. 2018;17:243\u201357.","journal-title":"World Psychiatry"},{"key":"2872_CR11","doi-asserted-by":"publisher","first-page":"621","DOI":"10.1038\/mp.2014.80","volume":"20","author":"J Bohacek","year":"2015","unstructured":"Bohacek J, Farinelli M, Mirante O, Steiner G, Gapp K, Coiret G, et al. Pathological brain plasticity and cognition in the offspring of males subjected to postnatal traumatic stress. Mol Psychiatr. 2015;20:621\u201331.","journal-title":"Mol Psychiatr"},{"key":"2872_CR12","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.semcdb.2019.07.005","volume":"97","author":"J Bohacek","year":"2019","unstructured":"Bohacek J, Rassoulzadegan M. Sperm RNA: Quo vadis? Semin Cell Dev Biol. 2019;97:123\u201330.","journal-title":"Semin Cell Dev Biol"},{"key":"2872_CR13","doi-asserted-by":"publisher","first-page":"2162","DOI":"10.1038\/s41380-018-0271-6","volume":"25","author":"K Gapp","year":"2020","unstructured":"Gapp K, van Steenwyk G, Germain PL, Matsushima W, Rudolph KLM, Manuella F, et al. Alterations in sperm long RNA contribute to the epigenetic inheritance of the effects of postnatal trauma. Mol Psychiatr. 2020;25:2162\u201374.","journal-title":"Mol Psychiatr"},{"key":"2872_CR14","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1038\/nn.3695","volume":"17","author":"K Gapp","year":"2014","unstructured":"Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci. 2014;17:667\u20139.","journal-title":"Nat Neurosci"},{"key":"2872_CR15","doi-asserted-by":"publisher","first-page":"dvac011","DOI":"10.1093\/eep\/dvac011","volume":"8","author":"M Kretschmer","year":"2022","unstructured":"Kretschmer M, Gapp K. Deciphering the RNA universe in sperm in its role as a vertical information carrier. Environ Epigenetics. 2022;8:dvac011.","journal-title":"Environ Epigenetics"},{"key":"2872_CR16","doi-asserted-by":"publisher","first-page":"1107","DOI":"10.1007\/s10528-021-10155-7","volume":"60","author":"M Ghai","year":"2022","unstructured":"Ghai M, Kader F. A review on epigenetic inheritance of experiences in humans. Biochem Genet. 2022;60:1107\u201340.","journal-title":"Biochem Genet"},{"key":"2872_CR17","doi-asserted-by":"publisher","first-page":"103786","DOI":"10.1016\/j.isci.2022.103786","volume":"25","author":"MB Maamar","year":"2022","unstructured":"Maamar MB, Beck D, Nilsson E, McCarrey JR, Skinner MK. Developmental alterations in DNA methylation during gametogenesis from primordial germ cells to sperm. Iscience. 2022;25:103786.","journal-title":"Iscience"},{"key":"2872_CR18","doi-asserted-by":"publisher","first-page":"e1002426","DOI":"10.1371\/journal.pbio.1002426","volume":"14","author":"EJ Nestler","year":"2016","unstructured":"Nestler EJ. Transgenerational epigenetic contributions to stress responses: fact or fiction? Plos Biol. 2016;14:e1002426.","journal-title":"Plos Biol"},{"key":"2872_CR19","doi-asserted-by":"publisher","first-page":"2084","DOI":"10.1111\/brv.12322","volume":"92","author":"Y Wang","year":"2017","unstructured":"Wang Y, Liu H, Sun Z. Lamarck rises from his grave: parental environment\u2010induced epigenetic inheritance in model organisms and humans. Biol Rev. 2017;92:2084\u2013111.","journal-title":"Biol Rev"},{"key":"2872_CR20","doi-asserted-by":"publisher","DOI":"10.1186\/s13148-020-00929-y","volume":"12","author":"L Senaldi","year":"2020","unstructured":"Senaldi L, Smith-Raska M. Evidence for germline non-genetic inheritance of human phenotypes and diseases. Clin Epigenetics. 2020;12:136.","journal-title":"Clin Epigenetics"},{"key":"2872_CR21","doi-asserted-by":"crossref","unstructured":"Jawaid A, Kunzi M, Mansoor M, Khan ZY, Abid A, Taha M, et al. Distinct microRNA signature in human serum and germline after childhood trauma. Medrxiv. 2020;2020.08.11.20168393.","DOI":"10.1101\/2020.08.11.20168393"},{"key":"2872_CR22","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1093\/ije\/dyx173","volume":"47","author":"L Karlsson","year":"2018","unstructured":"Karlsson L, Tolvanen M, Scheinin NM, Uusitupa HM, Korja R, Ekholm E, et al. Cohort Profile: The FinnBrain Birth Cohort Study (FinnBrain). Int J Epidemiol. 2018;47:15\u201316j.","journal-title":"Int J Epidemiol"},{"key":"2872_CR23","doi-asserted-by":"publisher","first-page":"30062","DOI":"10.3402\/ejpt.v7.30062","volume":"7","author":"RKR Salokangas","year":"2016","unstructured":"Salokangas RKR, Schultze-Lutter F, Patterson P, von Reventlow HG, Heinimaa M, From T, et al. Psychometric properties of the Trauma and Distress Scale, TADS, in an adult community sample in Finland. Eur J Psychotraumato. 2016;7:30062.","journal-title":"Eur J Psychotraumato"},{"key":"2872_CR24","doi-asserted-by":"publisher","first-page":"e2024832","DOI":"10.1001\/jamanetworkopen.2020.24832","volume":"3","author":"H Karlsson","year":"2020","unstructured":"Karlsson H, Merisaari H, Karlsson L, Scheinin NM, Parkkola R, Saunavaara J, et al. Association of cumulative paternal early life stress with white matter maturation in newborns. JAMA Netw Open. 2020;3:e2024832.","journal-title":"JAMA Netw Open"},{"key":"2872_CR25","doi-asserted-by":"publisher","first-page":"782","DOI":"10.1192\/bjp.150.6.782","volume":"150","author":"JL Cox","year":"1987","unstructured":"Cox JL, Holden JM, Sagovsky R. Detection of postnatal depression. Brit J Psychiat. 1987;150:782\u20136.","journal-title":"Brit J Psychiat"},{"key":"2872_CR26","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1111\/j.1600-0447.1998.tb09961.x","volume":"97","author":"MM Holi","year":"1998","unstructured":"Holi MM, Sammallahti PR, Aalberg VA. A Finnish validation study of the SCL\u201090. Acta Psychiat Scand. 1998;97:42\u20136.","journal-title":"Acta Psychiat Scand"},{"key":"2872_CR27","doi-asserted-by":"crossref","unstructured":"Danielsson O, Nano J, Pahkala K, Rospleszcz S, Lehtim\u00e4ki T, Schlett CL, et al. Validity of fatty liver disease indices in the presence of alcohol consumption. Scand J Gastroenterol. 2022;57:1349\u201360.","DOI":"10.1080\/00365521.2022.2085060"},{"key":"2872_CR28","doi-asserted-by":"publisher","first-page":"10","DOI":"10.14806\/ej.17.1.200","volume":"17","author":"M Martin","year":"2011","unstructured":"Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J. 2011;17:10\u20132.","journal-title":"Embnet J."},{"key":"2872_CR29","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1016\/j.gpb.2018.04.004","volume":"16","author":"J Shi","year":"2018","unstructured":"Shi J, Ko EA, Sanders KM, Chen Q, Zhou T. SPORTS1.0: A tool for annotating and profiling non-coding RNAs optimized for rRNA- and tRNA-derived small RNAs. Genom Proteom Bioinform. 2018;16:144\u201351.","journal-title":"Genom Proteom Bioinform"},{"key":"2872_CR30","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-15-545","volume":"15","author":"H Ha","year":"2014","unstructured":"Ha H, Song J, Wang S, Kapusta A, Feschotte C, Chen KC, et al. A comprehensive analysis of piRNAs from adult human testis and their relationship with genes and mobile elements. Bmc Genomics. 2014;15:545.","journal-title":"Bmc Genomics"},{"key":"2872_CR31","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","volume":"37","author":"D Kim","year":"2019","unstructured":"Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37:907\u201315.","journal-title":"Nat Biotechnol"},{"key":"2872_CR32","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","volume":"30","author":"Y Liao","year":"2014","unstructured":"Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923\u201330.","journal-title":"Bioinformatics."},{"key":"2872_CR33","doi-asserted-by":"publisher","first-page":"726","DOI":"10.1038\/nbt.3605","volume":"34","author":"C Bock","year":"2016","unstructured":"Bock C, Halbritter F, Carmona FJ, Tierling S, Datlinger P, Assenov Y, et al. Quantitative comparison of DNA methylation assays for biomarker development and clinical applications. Nat Biotechnol. 2016;34:726\u201337.","journal-title":"Nat Biotechnol"},{"key":"2872_CR34","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.ymeth.2020.06.021","volume":"187","author":"MJ Pajares","year":"2021","unstructured":"Pajares MJ, Palanca-Ballester C, Urtasun R, Alemany-Cosme E, Lahoz A, Sandoval J. Methods for analysis of specific DNA methylation status. Methods. 2021;187:3\u201312.","journal-title":"Methods."},{"key":"2872_CR35","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.","journal-title":"Genome Biol"},{"key":"2872_CR36","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","volume":"57","author":"Y Benjamini","year":"1995","unstructured":"Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B (Methodol). 1995;57:289\u2013300.","journal-title":"J Royal Stat Soc Ser B (Methodol)"},{"key":"2872_CR37","doi-asserted-by":"publisher","first-page":"e517","DOI":"10.1016\/S2468-2667(19)30145-8","volume":"4","author":"MA Bellis","year":"2019","unstructured":"Bellis MA, Hughes K, Ford K, Rodriguez GR, Sethi D, Passmore J. Life course health consequences and associated annual costs of adverse childhood experiences across Europe and North America: a systematic review and meta-analysis. Lancet Public Health. 2019;4:e517\u201328.","journal-title":"Lancet Public Health"},{"key":"2872_CR38","doi-asserted-by":"publisher","first-page":"e356","DOI":"10.1016\/S2468-2667(17)30118-4","volume":"2","author":"K Hughes","year":"2017","unstructured":"Hughes K, Bellis MA, Hardcastle KA, Sethi D, Butchart A, Mikton C, et al. The effect of multiple adverse childhood experiences on health: a systematic review and meta-analysis. Lancet Public Health. 2017;2:e356\u201366.","journal-title":"Lancet Public Health"},{"key":"2872_CR39","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1159\/000330002","volume":"32","author":"H Thabrew","year":"2011","unstructured":"Thabrew H, Sylva S, de, Romans S. Evaluating childhood adversity. Adv Psychosom Med. 2011;32:35\u201357.","journal-title":"Adv Psychosom Med"},{"key":"2872_CR40","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1038\/429154a","volume":"429","author":"GC Ostermeier","year":"2004","unstructured":"Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA. Delivering spermatozoan RNA to the oocyte. Nature. 2004;429:154\u2013154.","journal-title":"Nature."},{"key":"2872_CR41","doi-asserted-by":"publisher","first-page":"4104","DOI":"10.1093\/nar\/gkt132","volume":"41","author":"E Sendler","year":"2013","unstructured":"Sendler E, Johnson GD, Mao S, Goodrich RJ, Diamond MP, Hauser R, et al. Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res. 2013;41:4104\u201317.","journal-title":"Nucleic Acids Res"},{"key":"2872_CR42","doi-asserted-by":"publisher","first-page":"10851","DOI":"10.3390\/ijms231810851","volume":"23","author":"J Luo","year":"2022","unstructured":"Luo J, Tan X, Li H, Ding X. sncRNAs in Epididymosomes: The contribution to embryonic development and offspring health. Int J Mol Sci. 2022;23:10851.","journal-title":"Int J Mol Sci"},{"key":"2872_CR43","doi-asserted-by":"publisher","first-page":"13699","DOI":"10.1073\/pnas.1508347112","volume":"112","author":"AB Rodgers","year":"2015","unstructured":"Rodgers AB, Morgan CP, Leu NA, Bale TL. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci. 2015;112:13699\u2013704.","journal-title":"Proc Natl Acad Sci"},{"key":"2872_CR44","first-page":"635","volume":"143","author":"S Yuan","year":"2015","unstructured":"Yuan S, Schuster A, Tang C, Yu T, Ortogero N, Bao J, et al. Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development. Development. 2015;143:635\u201347.","journal-title":"Development."},{"key":"2872_CR45","doi-asserted-by":"publisher","first-page":"158","DOI":"10.3390\/cells11010158","volume":"11","author":"M Grad","year":"2022","unstructured":"Grad M, Nir A, Levy G, Trangle SS, Shapira G, Shomron N, et al. Altered white matter and microRNA expression in a murine model related to Williams Syndrome suggests that miR-34b\/c Affects Brain Development via Ptpru and Dcx Modulation. Cells. 2022;11:158.","journal-title":"Cells."},{"key":"2872_CR46","doi-asserted-by":"publisher","first-page":"936","DOI":"10.1007\/s12035-016-0359-4","volume":"55","author":"A Jauhari","year":"2018","unstructured":"Jauhari A, Singh T, Singh P, Parmar D, Yadav S. Regulation of miR-34 family in neuronal development. Mol Neurobiol. 2018;55:936\u201345.","journal-title":"Mol Neurobiol"},{"key":"2872_CR47","doi-asserted-by":"publisher","first-page":"e1622","DOI":"10.1038\/cddis.2014.589","volume":"6","author":"C Mollinari","year":"2015","unstructured":"Mollinari C, Racaniello M, Berry A, Pieri M, Stefano MC, de, Cardinale A, et al. miR-34a regulates cell proliferation, morphology and function of newborn neurons resulting in improved behavioural outcomes. Cell Death Dis. 2015;6:e1622\u2013e1622.","journal-title":"Cell Death Dis"},{"key":"2872_CR48","doi-asserted-by":"publisher","first-page":"E2851","DOI":"10.1073\/pnas.1407777111","volume":"111","author":"J Wu","year":"2014","unstructured":"Wu J, Bao J, Kim M, Yuan S, Tang C, Zheng H, et al. Two miRNA clusters, miR-34b\/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis. Proc Natl Acad Sci. 2014;111:E2851\u20137.","journal-title":"Proc Natl Acad Sci"},{"key":"2872_CR49","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1093\/jnen\/nlv016","volume":"75","author":"VTS Rao","year":"2016","unstructured":"Rao VTS, Ludwin SK, Fuh SC, Sawaya R, Moore CS, Ho MK, et al. MicroRNA expression patterns in human astrocytes in relation to anatomical location and age. J Neuropathol Neurol. 2016;75:156\u201366.","journal-title":"J Neuropathol Neurol."},{"key":"2872_CR50","doi-asserted-by":"publisher","first-page":"31","DOI":"10.3389\/fnmol.2017.00031","volume":"10","author":"MT Ven\u00f8","year":"2017","unstructured":"Ven\u00f8 MT, Ven\u00f8 ST, Rehberg K, Asperen JV, van, Clausen BH, Holm IE, et al. Cortical morphogenesis during embryonic development is regulated by miR-34c and miR-204. Front Mol Neurosci. 2017;10:31.","journal-title":"Front Mol Neurosci"},{"key":"2872_CR51","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/j.semcdb.2021.04.011","volume":"118","author":"A Morgunova","year":"2021","unstructured":"Morgunova A, Flores C. MicroRNA regulation of prefrontal cortex development and psychiatric risk in adolescence. Semin Cell Dev Biol. 2021;118:83\u201391.","journal-title":"Semin Cell Dev Biol"},{"key":"2872_CR52","doi-asserted-by":"publisher","first-page":"2773","DOI":"10.3390\/cancers12102773","volume":"12","author":"J Park","year":"2020","unstructured":"Park J, Ahn SH, Shin MG, Kim HK, Chang S. tRNA-derived small RNAs: Novel epigenetic regulators. Cancers. 2020;12:2773.","journal-title":"Cancers"},{"key":"2872_CR53","doi-asserted-by":"crossref","unstructured":"Tuulari JJ, Kataja EL, Karlsson L, Karlsson H. Associations of cumulative paternal and maternal childhood maltreament exposure with neonate brain anatomy. bioRxiv. 2022;2022.10.16.512276.","DOI":"10.1101\/2022.10.16.512276"},{"key":"2872_CR54","doi-asserted-by":"crossref","unstructured":"Tuulari JJ, Pulli EP, Kataja EL, Perasto L, Lewis JD, Karlsson L, et al. Parental childhood maltreatment associates with offspring left amygdala volume at early infancy. Biorxiv. 2023;2023.02.23.529799.","DOI":"10.1101\/2023.02.23.529799"},{"key":"2872_CR55","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1016\/j.cmet.2015.11.004","volume":"23","author":"I Donkin","year":"2016","unstructured":"Donkin I, Versteyhe S, Ingerslev LR, Qian K, Mechta M, Nordkap L, et al. Obesity and bariatric surgery drive epigenetic variation of Spermatozoa in humans. Cell Metab. 2016;23:369\u201378.","journal-title":"Cell Metab"},{"key":"2872_CR56","doi-asserted-by":"publisher","DOI":"10.1186\/s13148-018-0446-7","volume":"10","author":"LR Ingerslev","year":"2018","unstructured":"Ingerslev LR, Donkin I, Fabre O, Versteyhe S, Mechta M, Pattamaprapanont P, et al. Endurance training remodels sperm-borne small RNA expression and methylation at neurological gene hotspots. Clin Epigenetics. 2018;10:12.","journal-title":"Clin Epigenetics"},{"key":"2872_CR57","doi-asserted-by":"publisher","first-page":"4485","DOI":"10.1038\/s41380-022-01791-5","volume":"27","author":"A Cherix","year":"2022","unstructured":"Cherix A, Poitry-Yamate C, Lanz B, Zanoletti O, Grosse J, Sandi C, et al. Deletion of Crtc1 leads to hippocampal neuroenergetic impairments associated with depressive-like behavior. Mol Psychiatry. 2022;27:4485\u2013501.","journal-title":"Mol Psychiatry"},{"key":"2872_CR58","doi-asserted-by":"publisher","first-page":"4405","DOI":"10.1007\/s12035-022-02787-6","volume":"59","author":"D Li","year":"2022","unstructured":"Li D, Liao Q, Tao Y, Ni S, Wang C, Xu D, et al. Downregulation of CRTC1 Is Involved in CUMS-Induced Depression-Like Behavior in the Hippocampus and Its RNA Sequencing Analysis. Mol Neurobiol. 2022;59:4405\u201318.","journal-title":"Mol Neurobiol"},{"key":"2872_CR59","doi-asserted-by":"publisher","first-page":"180131","DOI":"10.1098\/rsob.180131","volume":"8","author":"R Luo","year":"2018","unstructured":"Luo R, Bai C, Yang L, Zheng Z, Su G, Gao G, et al. DNA methylation subpatterns at distinct regulatory regions in human early embryos. Open Biology. 2018;8:180131.","journal-title":"Open Biology"},{"key":"2872_CR60","doi-asserted-by":"crossref","unstructured":"M\u00e9ndez-Maldonado K, Vega-L\u00f3pez GA, Aybar MJ, Velasco I Neurogenesis from neural crest cells: molecular mechanisms in the formation of cranial nerves and Ganglia. Front Cell Dev Biol. 2020 [cited 2024 Sep 30];8. Available from: https:\/\/www.frontiersin.org\/journals\/cell-and-developmental-biology\/articles\/10.3389\/fcell.2020.00635\/full","DOI":"10.3389\/fcell.2020.00635"},{"key":"2872_CR61","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-023-43471-0","volume":"14","author":"M Maimaitili","year":"2023","unstructured":"Maimaitili M, Chen M, Febbraro F, Ucuncu E, Kelly R, Niclis JC, et al. Enhanced production of mesencephalic dopaminergic neurons from lineage-restricted human undifferentiated stem cells. Nat Commun. 2023;14:7871.","journal-title":"Nat Commun"},{"key":"2872_CR62","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/j.cytogfr.2016.06.003","volume":"32","author":"O Monestier","year":"2016","unstructured":"Monestier O, Blanquet V. WFIKKN1 and WFIKKN2: \u201cCompanion\u201d proteins regulating TGFB activity. Cytokine Growth Factor Rev. 2016;32:75\u201384.","journal-title":"Cytokine Growth Factor Rev"},{"key":"2872_CR63","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1038\/s41562-022-01482-9","volume":"7","author":"JR Baldwin","year":"2023","unstructured":"Baldwin JR, Sallis HM, Schoeler T, Taylor MJ, Kwong ASF, Tielbeek JJ, et al. A genetically informed Registered Report on adverse childhood experiences and mental health. Nat Hum Behav. 2023;7:269\u201390.","journal-title":"Nat Hum Behav"},{"key":"2872_CR64","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s42003-021-02316-6","volume":"4","author":"CV Breton","year":"2021","unstructured":"Breton CV, Landon R, Kahn LG, Enlow MB, Peterson AK, Bastain T, et al. Exploring the evidence for epigenetic regulation of environmental influences on child health across generations. Commun Biol. 2021;4:1\u201315.","journal-title":"Commun Biol"},{"key":"2872_CR65","doi-asserted-by":"publisher","DOI":"10.1186\/s40246-024-00626-4","volume":"18","author":"M Hosseini","year":"2024","unstructured":"Hosseini M, Khalafiyan A, Zare M, Karimzadeh H, Bahrami B, Hammami B, et al. Sperm epigenetics and male infertility: unraveling the molecular puzzle. Human Genomics. 2024;18:57.","journal-title":"Human Genomics"},{"key":"2872_CR66","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-05445-5","volume":"9","author":"B Horsthemke","year":"2018","unstructured":"Horsthemke B. A critical view on transgenerational epigenetic inheritance in humans. Nat Commun. 2018;9:2973.","journal-title":"Nat Commun"},{"key":"2872_CR67","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1016\/j.tig.2019.12.001","volume":"36","author":"L Duempelmann","year":"2020","unstructured":"Duempelmann L, Skribbe M, B\u00fchler M. Small RNAs in the transgenerational inheritance of epigenetic information. Trends Genetics. 2020;36:203\u201314.","journal-title":"Trends Genetics"}],"container-title":["Molecular Psychiatry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41380-024-02872-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41380-024-02872-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41380-024-02872-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,5,20]],"date-time":"2025-05-20T10:08:23Z","timestamp":1747735703000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41380-024-02872-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,3]]},"references-count":67,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2025,6]]}},"alternative-id":["2872"],"URL":"https:\/\/doi.org\/10.1038\/s41380-024-02872-3","relation":{},"ISSN":["1359-4184","1476-5578"],"issn-type":[{"value":"1359-4184","type":"print"},{"value":"1476-5578","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,3]]},"assertion":[{"value":"20 December 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 November 2024","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 December 2024","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 January 2025","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}