Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle
Exercise training prevents age‐related decline in muscle function. Targeting epigenetic aging is a promising actionable mechanism and late‐life exercise mitigates epigenetic aging in rodent muscle. Whether exercise training can decelerate, or reverse epigenetic aging in humans is unknown. Here, we p...
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| creator | Voisin, Sarah Seale, Kirsten Jacques, Macsue Landen, Shanie Harvey, Nicholas R. Haupt, Larisa M. Griffiths, Lyn R. Ashton, Kevin J. Coffey, Vernon G. Thompson, Jamie‐Lee M. Doering, Thomas M. Lindholm, Malene E. Walsh, Colum Davison, Gareth Irwin, Rachelle McBride, Catherine Hansson, Ola Asplund, Olof Heikkinen, Aino E. Piirilä, Päivi Pietiläinen, Kirsi H. Ollikainen, Miina Blocquiaux, Sara Thomis, Martine Coletta, Dawn K. Sharples, Adam P. Eynon, Nir |
| description | Exercise training prevents age‐related decline in muscle function. Targeting epigenetic aging is a promising actionable mechanism and late‐life exercise mitigates epigenetic aging in rodent muscle. Whether exercise training can decelerate, or reverse epigenetic aging in humans is unknown. Here, we performed a powerful meta‐analysis of the methylome and transcriptome of an unprecedented number of human skeletal muscle samples (n = 3176). We show that: (1) individuals with higher baseline aerobic fitness have younger epigenetic and transcriptomic profiles, (2) exercise training leads to significant shifts of epigenetic and transcriptomic patterns toward a younger profile, and (3) muscle disuse “ages” the transcriptome. Higher fitness levels were associated with attenuated differential methylation and transcription during aging. Furthermore, both epigenetic and transcriptomic profiles shifted toward a younger state after exercise training interventions, while the transcriptome shifted toward an older state after forced muscle disuse. We demonstrate that exercise training targets many of the age‐related transcripts and DNA methylation loci to maintain younger methylome and transcriptome profiles, specifically in genes related to muscle structure, metabolism, and mitochondrial function. Our comprehensive analysis will inform future studies aiming to identify the best combination of therapeutics and exercise regimes to optimize longevity.
Higher fitness levels were associated with attenuated differential methylation and transcription during aging in human muscle. Furthermore, exercise training targets many of the age‐related transcripts and DNA methylation loci to maintain younger methylome and transcriptome profiles, specifically in genes related to muscle structure, metabolism, and mitochondrial function. Our comprehensive analysis will inform future studies aiming to identify the best exercise regimes to optimize longevity. |
| doi_str_mv | 10.1111/acel.13859 |
| format | Article |
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Higher fitness levels were associated with attenuated differential methylation and transcription during aging in human muscle. Furthermore, exercise training targets many of the age‐related transcripts and DNA methylation loci to maintain younger methylome and transcriptome profiles, specifically in genes related to muscle structure, metabolism, and mitochondrial function. Our comprehensive analysis will inform future studies aiming to identify the best exercise regimes to optimize longevity.</description><identifier>ISSN: 1474-9718</identifier><identifier>ISSN: 1474-9726</identifier><identifier>EISSN: 1474-9726</identifier><identifier>DOI: 10.1111/acel.13859</identifier><identifier>PMID: 37128843</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Age ; Aging ; Basic Medicine ; Cardiorespiratory fitness ; Datasets ; DNA methylation ; Epigenetics ; Epigenome - genetics ; Exercise ; Exercise - physiology ; exercise training ; Fitness training programs ; Fysiologi ; Gene expression ; Gene Expression Profiling ; human skeletal muscle ; Humans ; Laboratories ; Medical and Health Sciences ; Medicin och hälsovetenskap ; Medicinska och farmaceutiska grundvetenskaper ; meta‐analysis ; Mortality ; mRNA expression ; Muscle, Skeletal - metabolism ; Musculoskeletal system ; Online data bases ; Physical fitness ; Physical training ; Physiology ; Senescence ; Skeletal muscle ; Stem cells ; Strength training ; Transcriptome - genetics ; Transcriptomes ; Transcriptomics</subject><ispartof>Aging cell, 2024-01, Vol.23 (1), p.e13859-n/a</ispartof><rights>2023 The Authors. published by Anatomical Society and John Wiley & Sons Ltd.</rights><rights>2023 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd.</rights><rights>2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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Targeting epigenetic aging is a promising actionable mechanism and late‐life exercise mitigates epigenetic aging in rodent muscle. Whether exercise training can decelerate, or reverse epigenetic aging in humans is unknown. Here, we performed a powerful meta‐analysis of the methylome and transcriptome of an unprecedented number of human skeletal muscle samples (n = 3176). We show that: (1) individuals with higher baseline aerobic fitness have younger epigenetic and transcriptomic profiles, (2) exercise training leads to significant shifts of epigenetic and transcriptomic patterns toward a younger profile, and (3) muscle disuse “ages” the transcriptome. Higher fitness levels were associated with attenuated differential methylation and transcription during aging. Furthermore, both epigenetic and transcriptomic profiles shifted toward a younger state after exercise training interventions, while the transcriptome shifted toward an older state after forced muscle disuse. We demonstrate that exercise training targets many of the age‐related transcripts and DNA methylation loci to maintain younger methylome and transcriptome profiles, specifically in genes related to muscle structure, metabolism, and mitochondrial function. Our comprehensive analysis will inform future studies aiming to identify the best combination of therapeutics and exercise regimes to optimize longevity.
Higher fitness levels were associated with attenuated differential methylation and transcription during aging in human muscle. Furthermore, exercise training targets many of the age‐related transcripts and DNA methylation loci to maintain younger methylome and transcriptome profiles, specifically in genes related to muscle structure, metabolism, and mitochondrial function. Our comprehensive analysis will inform future studies aiming to identify the best exercise regimes to optimize longevity.</description><subject>Age</subject><subject>Aging</subject><subject>Basic Medicine</subject><subject>Cardiorespiratory fitness</subject><subject>Datasets</subject><subject>DNA methylation</subject><subject>Epigenetics</subject><subject>Epigenome - genetics</subject><subject>Exercise</subject><subject>Exercise - physiology</subject><subject>exercise training</subject><subject>Fitness training programs</subject><subject>Fysiologi</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>human skeletal muscle</subject><subject>Humans</subject><subject>Laboratories</subject><subject>Medical and Health Sciences</subject><subject>Medicin och hälsovetenskap</subject><subject>Medicinska och farmaceutiska grundvetenskaper</subject><subject>meta‐analysis</subject><subject>Mortality</subject><subject>mRNA expression</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Musculoskeletal system</subject><subject>Online data bases</subject><subject>Physical fitness</subject><subject>Physical training</subject><subject>Physiology</subject><subject>Senescence</subject><subject>Skeletal muscle</subject><subject>Stem cells</subject><subject>Strength training</subject><subject>Transcriptome - genetics</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><issn>1474-9718</issn><issn>1474-9726</issn><issn>1474-9726</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>D8T</sourceid><recordid>eNp9kluL1DAUgIso7kVf_AES8EUWuubSNsmTLMN4gQFf9Dkk6elOdtNmTNod59-b2nFwBQ0ccjj58hFOTlG8Ivia5PVOW_DXhIlaPinOScWrUnLaPD3lRJwVFyndYUy4xOx5ccY4oUJU7LzQ6x8QrUuAXEI6pWCdHqFFezdu0SFMwy1E1MO4PfjQA9JDi8aoh2Sj241zZRdD5zwk5Aa0nXo9oHQPHkbtUT8l6-FF8azTPsHL435ZfPuw_rr6VG6-fPy8utmUtq4bWdIad5pLrU3HDLC6Y5RgCdhoojGzYFhbc2FaIYgldUUabjnD0koqSb4F7LIoF2_aw24yahddr-NBBe3UsXSfM1BV1RBBM7_5J--nXQ6TY77AmKkl0TmhmqnKiEYJa6wiLZZCM2GFbLLu_aLLrh5aC0Puk39kfXwyuK26DQ-KYM4bQmfD26Mhhu8TpFH1LuWv9XqAMCVFBRa14FjM6Ju_0LswxSG3V-V2UMyooDxTVwtlY0gpQnd6DcFqnhw1T476NTkZfv3n-0_o71HJAFmAff7uw39U6ma13izSn2Pu0HE</recordid><startdate>202401</startdate><enddate>202401</enddate><creator>Voisin, Sarah</creator><creator>Seale, Kirsten</creator><creator>Jacques, Macsue</creator><creator>Landen, Shanie</creator><creator>Harvey, Nicholas R.</creator><creator>Haupt, Larisa M.</creator><creator>Griffiths, Lyn R.</creator><creator>Ashton, Kevin J.</creator><creator>Coffey, Vernon G.</creator><creator>Thompson, Jamie‐Lee M.</creator><creator>Doering, Thomas M.</creator><creator>Lindholm, Malene E.</creator><creator>Walsh, Colum</creator><creator>Davison, Gareth</creator><creator>Irwin, Rachelle</creator><creator>McBride, Catherine</creator><creator>Hansson, Ola</creator><creator>Asplund, Olof</creator><creator>Heikkinen, Aino E.</creator><creator>Piirilä, Päivi</creator><creator>Pietiläinen, Kirsi H.</creator><creator>Ollikainen, Miina</creator><creator>Blocquiaux, Sara</creator><creator>Thomis, Martine</creator><creator>Coletta, Dawn K.</creator><creator>Sharples, Adam P.</creator><creator>Eynon, Nir</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7TK</scope><scope>8FE</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AGCHP</scope><scope>AOWAS</scope><scope>D8T</scope><scope>D95</scope><scope>ZZAVC</scope><orcidid>https://orcid.org/0000-0002-4074-7083</orcidid></search><sort><creationdate>202401</creationdate><title>Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle</title><author>Voisin, Sarah ; Seale, Kirsten ; Jacques, Macsue ; Landen, Shanie ; Harvey, Nicholas R. ; Haupt, Larisa M. ; Griffiths, Lyn R. ; Ashton, Kevin J. ; Coffey, Vernon G. ; Thompson, Jamie‐Lee M. ; Doering, Thomas M. ; Lindholm, Malene E. ; Walsh, Colum ; Davison, Gareth ; Irwin, Rachelle ; McBride, Catherine ; Hansson, Ola ; Asplund, Olof ; Heikkinen, Aino E. ; Piirilä, Päivi ; Pietiläinen, Kirsi H. ; Ollikainen, Miina ; Blocquiaux, Sara ; Thomis, Martine ; Coletta, Dawn K. ; Sharples, Adam P. ; Eynon, Nir</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5569-250fa79aabf3be35f32109e0ba1a03ceb3d578bd881c154167c7309c92919aae3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Age</topic><topic>Aging</topic><topic>Basic Medicine</topic><topic>Cardiorespiratory fitness</topic><topic>Datasets</topic><topic>DNA methylation</topic><topic>Epigenetics</topic><topic>Epigenome - 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Targeting epigenetic aging is a promising actionable mechanism and late‐life exercise mitigates epigenetic aging in rodent muscle. Whether exercise training can decelerate, or reverse epigenetic aging in humans is unknown. Here, we performed a powerful meta‐analysis of the methylome and transcriptome of an unprecedented number of human skeletal muscle samples (n = 3176). We show that: (1) individuals with higher baseline aerobic fitness have younger epigenetic and transcriptomic profiles, (2) exercise training leads to significant shifts of epigenetic and transcriptomic patterns toward a younger profile, and (3) muscle disuse “ages” the transcriptome. Higher fitness levels were associated with attenuated differential methylation and transcription during aging. Furthermore, both epigenetic and transcriptomic profiles shifted toward a younger state after exercise training interventions, while the transcriptome shifted toward an older state after forced muscle disuse. We demonstrate that exercise training targets many of the age‐related transcripts and DNA methylation loci to maintain younger methylome and transcriptome profiles, specifically in genes related to muscle structure, metabolism, and mitochondrial function. Our comprehensive analysis will inform future studies aiming to identify the best combination of therapeutics and exercise regimes to optimize longevity.
Higher fitness levels were associated with attenuated differential methylation and transcription during aging in human muscle. Furthermore, exercise training targets many of the age‐related transcripts and DNA methylation loci to maintain younger methylome and transcriptome profiles, specifically in genes related to muscle structure, metabolism, and mitochondrial function. Our comprehensive analysis will inform future studies aiming to identify the best exercise regimes to optimize longevity.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>37128843</pmid><doi>10.1111/acel.13859</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-4074-7083</orcidid><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_swepub_primary_oai_swepub_ki_se_446182 |
| source | MEDLINE; Wiley Online Library Open Access; DOAJ Directory of Open Access Journals; Wiley Online Library Journals Frontfile Complete; EZB-FREE-00999 freely available EZB journals; PubMed Central; SWEPUB Freely available online |
| subjects | Age Aging Basic Medicine Cardiorespiratory fitness Datasets DNA methylation Epigenetics Epigenome - genetics Exercise Exercise - physiology exercise training Fitness training programs Fysiologi Gene expression Gene Expression Profiling human skeletal muscle Humans Laboratories Medical and Health Sciences Medicin och hälsovetenskap Medicinska och farmaceutiska grundvetenskaper meta‐analysis Mortality mRNA expression Muscle, Skeletal - metabolism Musculoskeletal system Online data bases Physical fitness Physical training Physiology Senescence Skeletal muscle Stem cells Strength training Transcriptome - genetics Transcriptomes Transcriptomics |
| title | Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T00%3A53%3A42IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_swepu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Exercise%20is%20associated%20with%20younger%20methylome%20and%20transcriptome%20profiles%20in%20human%20skeletal%20muscle&rft.jtitle=Aging%20cell&rft.au=Voisin,%20Sarah&rft.date=2024-01&rft.volume=23&rft.issue=1&rft.spage=e13859&rft.epage=n/a&rft.pages=e13859-n/a&rft.issn=1474-9718&rft.eissn=1474-9726&rft_id=info:doi/10.1111/acel.13859&rft_dat=%3Cproquest_swepu%3E2912032827%3C/proquest_swepu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2912032827&rft_id=info:pmid/37128843&rfr_iscdi=true |