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We used recombination-independent doxycycline-inducible myonucleus-specific fluorescent labelling, tissue RNA-sequencing, myonuclear DNA methylation analysis, multi-omic integration, and single myonucleus RNA-sequencing to define the molecular characteristics of adult (6-8 month) and aged (24 month) murine skeletal muscle after acute mechanical overload (MOV). In adult and aged MOV muscles, we found that: 1) similarities in the transcriptional response to loading \u2013 specifically in metabolism genes \u2013 were partly explained by a post-transcriptional microRNA-mediated mechanism, which we corroborated using an inducible muscle fiber-specific\n                  <jats:italic>miR-1<\/jats:italic>\n                  knockout model, 2) differences in age-dependent transcriptional responses were linked to the magnitude and location of differential DNA methylation in resident myonuclei, specifically around hypertrophy-associated genes such as\n                  <jats:italic>Myc<\/jats:italic>\n                  ,\n                  <jats:italic>Runx1<\/jats:italic>\n                  ,\n                  <jats:italic>Mybph<\/jats:italic>\n                  ,\n                  <jats:italic>Ankrd1,<\/jats:italic>\n                  collagen genes, and minichromosome maintenance genes, 3) adult and aged resident myonuclear transcriptomes had differing enrichment for innervation-related transcripts as well as unique transcriptional profiles in an\n                  <jats:italic>Atf3+<\/jats:italic>\n                  \u201csarcomere assembly\u201d population after MOV, and 4) cellular deconvolution analysis supports a role for neuromuscular junction regulation in age-specific hypertrophic adaptation. These data are a roadmap for uncovering molecular targets to enhance aged muscle adaptability.\n                <\/jats:p>","DOI":"10.1101\/2025.10.29.685384","type":"posted-content","created":{"date-parts":[[2025,10,30]],"date-time":"2025-10-30T11:10:20Z","timestamp":1761822620000},"source":"Crossref","is-referenced-by-count":3,"title":["The Age-Dependent Resident Myonuclear Multi-Omic Response to a Skeletal Muscle Hypertrophic Stimulus"],"prefix":"10.64898","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4797-5265","authenticated-orcid":false,"given":"Pieter J.","family":"Koopmans","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"suffix":"III","given":"Ronald G.","family":"Jones","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9811-3585","authenticated-orcid":false,"given":"Ana 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J.","family":"McCarthy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4025-3945","authenticated-orcid":false,"given":"Ahmed","family":"Ismaeel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan","family":"Wen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin 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