{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T19:51:18Z","timestamp":1785786678237,"version":"3.56.0"},"reference-count":66,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,8,29]],"date-time":"2025-08-29T00:00:00Z","timestamp":1756425600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell Dev. Biol."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>The histone H4 hyperacetylation (i.e., acetylation of H4 at lysines -K5, -K8, -K12, and -K16, here reported as H4tetraAc) occurs in elongating spermatids (eSPTs) during spermiogenesis. Although it is critically involved in histone displacement, the mechanistic involvement of histone -acetyltransferases (HATs) and -deacetylases (HDACs) in the pathway underlying H4 hyperacetylation is poorly defined. Here, we investigate the involvement of SIRT1 deacetylase, and its functional interaction with the histone acetyltransferase MOF, in regulating H4 hyperacetylation underlying histone-to-protamine exchange.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Exploiting the cannabinoid receptor 1 (<jats:italic>Cb1<\/jats:italic>) null mice (Cb1<jats:sup>\u2212\/\u2212<\/jats:sup>) as a model of impaired histone displacement, we assessed in eSPTs the expression and the localization of SIRT1 in combination with the enrichment of H4tetraAc and the relative monoacetylated forms (H4-K5ac, -K8ac, -K12ac and -K16ac), by Western Blot and immunohistochemistry analyses. Then, focusing on SIRT1 interaction with MOF HAT by protein immunoprecipitation experiments, we verified the H4K16ac and H4TetraAc enrichment in eSPTs in response to <jats:italic>ex vivo<\/jats:italic> SIRT1 inhibition by using the selective EX-527 inhibitor.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>We show that the hyperacetylation of histone H4 occurs progressively in steps 8\u20139 eSPTs and bursts in step 10 eSPTs, appearing inversely correlated to the expression pattern of SIRT1, being SIRT1 present in step 8, detectable in step 9 and absent in step 10 eSPTs. The abnormal SIRT1 retention in step 10 eSPTs of Cb1<jats:sup>\u2212\/\u2212<\/jats:sup> mice, despite the observed enrichment of H4-K5ac, -K8ac, and -K12ac, counteracts the H4 hyperacetylation burst by limiting the H4 acetylation at lysine K16. Mechanistically, SIRT1 directly or indirectly interacts with and negatively regulates MOF acetyltransferase, specifically affecting its acetylation status and protein content, thereby interfering with H4K16 acetylation. Counteracting the MOF\/SIRT1 interaction by SIRT1 inhibition in <jats:italic>ex vivo<\/jats:italic> Cb1<jats:sup>\u2212\/\u2212<\/jats:sup> testis, both MOF protein content and acetylation status increase, downstream promoting recovery of H4K16ac and H4tetraAc in step 10 eSPT, and full rescue of histone displacement.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>These results underscore the key involvement of SIRT1\u2013MOF axis in modulating H4K16 acetylation. Our findings provide mechanistic insights into H4K16 acetylation pathway in eSPTs and support the key role of H4K16ac in chromatin remodeling underlying histone displacement.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fcell.2025.1524919","type":"journal-article","created":{"date-parts":[[2025,8,29]],"date-time":"2025-08-29T05:43:53Z","timestamp":1756446233000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["SIRT1 retention in elongating spermatids interferes with histone displacement by counteracting MOF-dependent H4K16 acetylation"],"prefix":"10.3389","volume":"13","author":[{"given":"Veronica","family":"Porreca","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Teresa","family":"Chioccarelli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco","family":"Albano","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valeria","family":"Nittoli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giulia","family":"Ricci","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Concetta","family":"Ambrosino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rosanna","family":"Chianese","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincenza Grazia","family":"Mele","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonella","family":"Migliaccio","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariano","family":"Stornaiuolo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Suglia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gilda","family":"Cobellis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco","family":"Manfrevola","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,8,29]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"44","DOI":"10.3109\/19396360903490790","article-title":"Histone H4 acetylation is essential to proceed from a histone-to a protamine-based chromatin structure in spermatid nuclei of Drosophila melanogaster","volume":"56","author":"Awe","year":"2010","journal-title":"Syst. Biol. Reprod. Med."},{"key":"B2","doi-asserted-by":"publisher","first-page":"101087","DOI":"10.1016\/j.molmet.2020.101087","article-title":"Reversal of diet-induced hepatic steatosis by peripheral CB1 receptor blockade in mice is p53\/miRNA-22\/SIRT1\/PPAR\u03b1 dependent","volume":"42","author":"Azar","year":"2020","journal-title":"Mol. Metab."},{"key":"B3","doi-asserted-by":"publisher","first-page":"R55","DOI":"10.1530\/REP-15-0562","article-title":"Epigenetic regulation of the histone-to-protamine transition during spermiogenesis","volume":"151","author":"Bao","year":"2016","journal-title":"Reproduction"},{"key":"B4","doi-asserted-by":"publisher","first-page":"3495","DOI":"10.1242\/dev.110627","article-title":"SIRT1 is required in the male germ cell for differentiation and fecundity in mice","volume":"141","author":"Bell","year":"2014","journal-title":"Development"},{"key":"B5","doi-asserted-by":"publisher","first-page":"10264","DOI":"10.1074\/jbc.M408748200","article-title":"SIRT1 deacetylation and repression of p300 involves lysine residues 1020\/1024 within the cell cycle regulatory domain 1","volume":"280","author":"Bouras","year":"2005","journal-title":"J. Biol. Chem."},{"key":"B6","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1038\/nsmb.1821","article-title":"Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa","volume":"17","author":"Brykczynska","year":"2010","journal-title":"Nat. Struct. Mol. Biol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1095\/biolreprod.112.105726","article-title":"Low 17beta-estradiol levels in Cnr1 knock-out mice affect spermatid chromatin remodeling by interfering with chromatin reorganization","volume":"88","author":"Cacciola","year":"","journal-title":"Biol. Reprod."},{"key":"B8","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.ygcen.2013.07.018","article-title":"Nuclear size as estrogen-responsive chromatin quality parameter of mouse spermatozoa","volume":"193","author":"Cacciola","year":"","journal-title":"Gen. Comp. Endocrinol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"501350","DOI":"10.1155\/2013\/501350","article-title":"Estrogens and spermiogenesis: new insights from type 1 cannabinoid receptor knockout mice","volume":"2013","author":"Cacciola","year":"","journal-title":"Int. J. Endocrinol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"4268","DOI":"10.1074\/jbc.C109.087981","article-title":"Subunit composition and substrate specificity of a MOF-containing histone acetyltransferase distinct from the male-specific lethal (MSL) complex","volume":"285","author":"Cai","year":"2010","journal-title":"J. Biol. Chem."},{"key":"B11","doi-asserted-by":"publisher","first-page":"1048","DOI":"10.1074\/mcp.M112.019547","article-title":"Quantitative acetylome analysis reveals the roles of SIRT1 in regulating diverse substrates and cellular pathways","volume":"11","author":"Chen","year":"2012","journal-title":"Mol. Cell Proteomics"},{"key":"B12","doi-asserted-by":"publisher","first-page":"5017","DOI":"10.1210\/en.2010-0133","article-title":"Cannabinoid receptor 1 influences chromatin remodeling in mouse spermatids by affecting content of transition protein 2 mRNA and histone displacement","volume":"151","author":"Chioccarelli","year":"2010","journal-title":"Endocrinology"},{"key":"B13","doi-asserted-by":"publisher","first-page":"3117","DOI":"10.3390\/ijms21093117","article-title":"The cannabinoid receptor CB1 stabilizes sperm chromatin condensation status during epididymal transit by promoting disulphide bond Formation","volume":"21","author":"Chioccarelli","year":"","journal-title":"Int. J. Mol. Sci."},{"key":"B14","doi-asserted-by":"publisher","first-page":"E640","DOI":"10.3390\/jcm9030640","article-title":"Histone post-translational modifications and circRNAs in mouse and human spermatozoa: potential epigenetic marks to assess human sperm quality","volume":"9","author":"Chioccarelli","year":"","journal-title":"J. Clin. Med."},{"key":"B15","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1095\/biolreprod.106.051730","article-title":"Endocannabinoid system in frog and rodent testis: type-1 cannabinoid receptor and fatty acid amide hydrolase activity in male germ cells","volume":"75","author":"Cobellis","year":"2006","journal-title":"Biol. Reprod."},{"key":"B16","doi-asserted-by":"publisher","first-page":"6387","DOI":"10.1074\/jbc.M111.288167","article-title":"Insights into role of bromodomain, testis-specific (Brdt) in acetylated histone H4-dependent chromatin remodeling in mammalian spermiogenesis","volume":"287","author":"Dhar","year":"2012","journal-title":"J. Biol. Chem."},{"key":"B17","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1101\/gad.240200.114","article-title":"Structural analysis of the KANSL1\/WDR5\/KANSL2 complex reveals that WDR5 is required for efficient assembly and chromatin targeting of the NSL complex","volume":"28","author":"Dias","year":"2014","journal-title":"Genes Dev."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1476312","DOI":"10.3389\/fcell.2024.1476312","article-title":"Contribution of the paternal histone epigenome to the preimplantation embryo","volume":"12","author":"Dodd","year":"2024","journal-title":"Front. Cell Dev. Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"e00082-17","DOI":"10.1128\/MCB.00082-17","article-title":"EPC1\/TIP60-Mediated histone acetylation facilitates spermiogenesis in mice","volume":"37","author":"Dong","year":"2017","journal-title":"Mol. Cell. Biol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1884","DOI":"10.1128\/MCB.24.5.1884-1896.2004","article-title":"Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans","volume":"24","author":"Doyon","year":"2004","journal-title":"Mol. Cell Biol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1038\/nsmb.2599","article-title":"Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa","volume":"20","author":"Erkek","year":"2013","journal-title":"Nat. Struct. Mol. Biol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"102034","DOI":"10.1016\/j.gde.2023.102034","article-title":"Nucleosomes in mammalian sperm: conveying paternal epigenetic inheritance or subject to reprogramming between generations?","volume":"79","author":"Gaspa-Toneu","year":"2023","journal-title":"Curr. Opin. Genet. Dev."},{"key":"B23","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1083\/jcb.200604141","article-title":"Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis","volume":"176","author":"Govin","year":"2007","journal-title":"J. Cell. Biol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"2558","DOI":"10.1093\/humrep\/der192","article-title":"Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men","volume":"26","author":"Hammoud","year":"2011","journal-title":"Human Reprod."},{"key":"B25","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1038\/nature08162","article-title":"Distinctive chromatin in human sperm packages genes for embryo development","volume":"460","author":"Hammoud","year":"2009","journal-title":"Nature"},{"key":"B26","doi-asserted-by":"publisher","first-page":"950","DOI":"10.1078\/0171-9335-00123","article-title":"Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases","volume":"79","author":"Hazzouri","year":"2000","journal-title":"Eur. J. Cell. Biol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/978-0-387-09597-4_1","article-title":"Spermatogenesis and cycle of the seminiferous epithelium","volume":"636","author":"Hess","year":"2008","journal-title":"Adv. Exp. Med. Biol."},{"key":"B28","first-page":"539","article-title":"Spermatogenesis: an overview","volume-title":"Encyclopedia of reproduction","author":"Hess","year":"1999"},{"key":"B29","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1093\/jb\/mvx079","article-title":"Histone variants: essential actors in male genome programming","volume":"163","author":"Hoghoughi","year":"2017","journal-title":"J. Biochem."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1366","DOI":"10.1016\/j.celrep.2017.01.034","article-title":"Chromatin States in mouse sperm correlate with embryonic and adult regulatory landscapes","volume":"18","author":"Jung","year":"2017","journal-title":"Cell Rep."},{"key":"B31","doi-asserted-by":"publisher","first-page":"20121022","DOI":"10.1098\/rsif.2012.1022","article-title":"The role of the nucleosome acidic patch in modulating higher order chromatin structure","volume":"10","author":"Kalashnikova","year":"2013","journal-title":"J. R. Soc. Interface"},{"key":"B32","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1093\/biolre\/iox159","article-title":"Early histone H4 acetylation during chromatin remodeling in equine spermatogenesis","volume":"98","author":"Ketchum","year":"2018","journal-title":"Biol. Reprod."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1032","DOI":"10.1111\/rda.12632","article-title":"VASA (DDX4) is a putative marker for Spermatogonia, spermatocytes and round spermatids in stallions","volume":"50","author":"Kim","year":"2015","journal-title":"Reprod. Domest. Anim."},{"key":"B34","doi-asserted-by":"publisher","first-page":"R25","DOI":"10.1186\/gb-2009-10-3-r25","article-title":"Ultrafast and memory-efficient alignment of short DNA sequences to the human genome","volume":"10","author":"Langmead","year":"2009","journal-title":"Genome Biol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1126\/science.283.5400.401","article-title":"Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice","volume":"283","author":"Ledent","year":"1999","journal-title":"Science"},{"key":"B36","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1016\/j.molcel.2009.07.031","article-title":"Two mammalian MOF complexes regulate transcription activation by distinct mechanisms","volume":"36","author":"Li","year":"2010","journal-title":"Mol. Cell"},{"key":"B37","doi-asserted-by":"publisher","first-page":"1182","DOI":"10.1038\/cr.2011.71","article-title":"Modulations of hMOFautoacetylation by SIRT1 regulate hMOF recruitment and activities on the chromatin","volume":"21","author":"Lu","year":"2011","journal-title":"Cell Res."},{"key":"B38","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1016\/j.devcel.2010.01.010","article-title":"RNF8-dependent histone modifications regulate nucleosome removal during spermatogenesis","volume":"18","author":"Lu","year":"2010","journal-title":"Dev. Cell"},{"key":"B39","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1016\/j.devcel.2019.10.024","article-title":"Gcn5-Mediated histone acetylation governs nucleosome dynamics in spermiogenesis","volume":"51","author":"Luense","year":"2019","journal-title":"Dev. Cell"},{"key":"B40","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1186\/s13072-016-0072-6","article-title":"Comprehensive analysis of histone post-translational modifications in mouse and human male germ cells","volume":"9","author":"Luense","year":"2016","journal-title":"Epigenetics Chromatin"},{"key":"B41","doi-asserted-by":"publisher","first-page":"5136","DOI":"10.7150\/ijbs.76261","article-title":"Actin remodeling driven by circLIMA1: sperm cell as an intriguing cellular model","volume":"18","author":"Manfrevola","year":"2022","journal-title":"Int. J. Biol. Sci."},{"key":"B42","doi-asserted-by":"publisher","first-page":"10","DOI":"10.14806\/ej.17.1.200","article-title":"Cutadapt removes adapter sequences from high-throughput sequencing reads","volume":"17","author":"Martin","year":"2011","journal-title":"EMBnet. J."},{"key":"B43","doi-asserted-by":"publisher","first-page":"2234","DOI":"10.7150\/ijbs.77166","article-title":"Cytochalasin D restores nuclear size acting on F-actin and IZUMO1 localization in low-quality spermatozoa","volume":"19","author":"Martinez","year":"2023","journal-title":"Int. J. Biol. Sci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/j.sbi.2021.05.006","article-title":"Principles of nucleosome recognition by chromatin factors and enzymes","volume":"71","author":"McGinty","year":"2021","journal-title":"Curr. Opin. Struct. Biol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1007\/978-1-62703-038-0_27","article-title":"Assessment of spermatogenesis through staging of seminiferous tubules","volume":"927","author":"Meistrich","year":"2013","journal-title":"Methods Mol. Biol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"895502","DOI":"10.3389\/fendo.2022.895502","article-title":"The art of packaging the sperm genome: molecular and structural basis of the histone-to-protamine exchange","volume":"13","author":"Moritz","year":"2022","journal-title":"Front. Endocrinol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"102075","DOI":"10.1016\/j.ceb.2022.102075","article-title":"Sperm chromatin structure: insights from in vitro to in situ experiments","volume":"75","author":"Okada","year":"2022","journal-title":"Curr. Opin. Cell. Biol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1989","DOI":"10.1128\/mcb.00552-08","article-title":"hSirt1-Dependent regulation of the Pcaf-E2f1-P73 apoptotic pathway in response to DNA damage","volume":"29","author":"Pediconi","year":"2009","journal-title":"Mol. Cell Biol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"2823","DOI":"10.1128\/MCB.00496-12","article-title":"SIRT1 negatively regulates the activities, functions, and protein levels of hMOF and TIP60","volume":"32","author":"Peng","year":"2012","journal-title":"Mol. Cell. Biol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"371832","DOI":"10.1155\/2011\/371832","article-title":"Physical and functional HAT\/HDAC interplay regulates protein acetylation balance","volume":"2011","author":"Peserico","year":"2011","journal-title":"J. Biomed. Biotechnol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"166701","DOI":"10.1016\/j.jmb.2020.11.001","article-title":"Nucleosome clutches are regulated by chromatin internal parameters","volume":"433","author":"Portillo-Ledesma","year":"2021","journal-title":"J. Mol. Biol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"1012","DOI":"10.1016\/j.cell.2013.04.032","article-title":"Acetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis","volume":"153","author":"Qian","year":"2013","journal-title":"Cell"},{"key":"B53","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.bbagrm.2013.08.004","article-title":"Chromatin dynamics during spermiogenesis","volume":"1839","author":"Rathke","year":"2014","journal-title":"Biochim. Biophys. Acta."},{"key":"B54","doi-asserted-by":"publisher","first-page":"e02104","DOI":"10.7554\/eLife.02104","article-title":"Mof-associated complexes have overlapping and unique roles in regulating pluripotency in embryonic stem cells and during differentiation","volume":"3","author":"Ravens","year":"2014","journal-title":"Elife"},{"key":"B55","doi-asserted-by":"publisher","first-page":"3477","DOI":"10.1016\/j.celrep.2018.08.069","article-title":"Nut directs p300-Dependent, genome-wide H4 hyperacetylation in Male germ cells","volume":"24","author":"Shiota","year":"2018","journal-title":"Cell Rep."},{"key":"B56","doi-asserted-by":"publisher","first-page":"844","DOI":"10.1126\/science.1124000","article-title":"Histone H4-K16 acetylation controls chromatin structure and protein interactions","volume":"311","author":"Shogren-Knaak","year":"2006","journal-title":"Science"},{"key":"B57","doi-asserted-by":"publisher","first-page":"2737","DOI":"10.1101\/gad.202713.112","article-title":"RNF8 regulates active epigenetic modifications and escape gene activation from inactive sex chromosomes in post-meiotic spermatids","volume":"26","author":"Sin","year":"2012","journal-title":"Genes Dev."},{"key":"B58","doi-asserted-by":"publisher","first-page":"9175","DOI":"10.1128\/MCB.25.21.9175-9188.2005","article-title":"A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16","volume":"25","author":"Smith","year":"2005","journal-title":"Mol. Cell. Biol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"780","DOI":"10.3389\/fgene.2020.00780","article-title":"The interplay between replacement and retention of histones in the sperm genome","volume":"11","author":"Torres-Flores","year":"2020","journal-title":"Front. Genet."},{"key":"B60","doi-asserted-by":"publisher","first-page":"458","DOI":"10.1016\/j.ydbio.2006.06.051","article-title":"Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin","volume":"298","author":"van der Heijden","year":"2006","journal-title":"Dev. Biol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1016\/j.molcel.2004.08.031","article-title":"Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin","volume":"16","author":"Vaquero","year":"2004","journal-title":"Mol. Cell"},{"key":"B62","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1038\/s41392-022-01257-8","article-title":"The sirtuin family in health and disease","volume":"7","author":"Wu","year":"2022","journal-title":"Signal Transduct. Target Ther."},{"key":"B63","doi-asserted-by":"publisher","first-page":"101835","DOI":"10.1016\/j.media.2020.101835","article-title":"Computerized spermatogenesis staging (CSS) of mouse testis sections via quantitative histomorphological analysis","volume":"70","author":"Xu","year":"2021","journal-title":"Med. Image Anal."},{"key":"B64","doi-asserted-by":"publisher","first-page":"3920","DOI":"10.1016\/j.celrep.2018.05.094","article-title":"Re-evaluating the localization of sperm-retained histones revealed the modification-dependent accumulation in specific genome regions","volume":"23","author":"Yamaguchi","year":"2018","journal-title":"Cell Rep."},{"key":"B65","doi-asserted-by":"publisher","first-page":"3885","DOI":"10.1038\/s41467-018-06243-9","article-title":"Mapping of histone-binding sites in histone replacement-completed spermatozoa","volume":"9","author":"Yoshida","year":"2018","journal-title":"Nat. Commun."},{"key":"B66","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1177\/1535370218757950","article-title":"Activation of the cannabinoid receptor 1 by ACEA suppresses senescence in human primary chondrocytes through sirt1 activation","volume":"243","author":"Zhang","year":"2018","journal-title":"Exp. Biol. Med."}],"container-title":["Frontiers in Cell and Developmental Biology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2025.1524919\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,8,29]],"date-time":"2025-08-29T05:43:54Z","timestamp":1756446234000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2025.1524919\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,8,29]]},"references-count":66,"alternative-id":["10.3389\/fcell.2025.1524919"],"URL":"https:\/\/doi.org\/10.3389\/fcell.2025.1524919","relation":{},"ISSN":["2296-634X"],"issn-type":[{"value":"2296-634X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,8,29]]},"article-number":"1524919"}}