Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle. / 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; Dawn, Coletta K.; Sharples, Adam P.; Eynon, Nir.

In: Aging Cell, Vol. 23, No. 1, e13859, 2024.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Voisin, S, Seale, K, Jacques, M, Landen, S, Harvey, NR, Haupt, LM, Griffiths, LR, Ashton, KJ, Coffey, VG, Thompson, JLM, Doering, TM, Lindholm, ME, Walsh, C, Davison, G, Irwin, R, McBride, C, Hansson, O, Asplund, O, Heikkinen, AE, Piirilä, P, Pietiläinen, KH, Ollikainen, M, Blocquiaux, S, Thomis, M, Dawn, CK, Sharples, AP & Eynon, N 2024, 'Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle', Aging Cell, vol. 23, no. 1, e13859. https://doi.org/10.1111/acel.13859

APA

Voisin, S., Seale, K., Jacques, M., Landen, S., Harvey, N. R., Haupt, L. M., Griffiths, L. R., Ashton, K. J., Coffey, V. G., Thompson, J. L. M., Doering, T. M., Lindholm, M. E., Walsh, C., Davison, G., Irwin, R., McBride, C., Hansson, O., Asplund, O., Heikkinen, A. E., ... Eynon, N. (2024). Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle. Aging Cell, 23(1), [e13859]. https://doi.org/10.1111/acel.13859

Vancouver

Voisin S, Seale K, Jacques M, Landen S, Harvey NR, Haupt LM et al. Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle. Aging Cell. 2024;23(1). e13859. https://doi.org/10.1111/acel.13859

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 ; Dawn, Coletta K. ; Sharples, Adam P. ; Eynon, Nir. / Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle. In: Aging Cell. 2024 ; Vol. 23, No. 1.

Bibtex

@article{1421b5a6d92d403aa04e259da2eaad1c,
title = "Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle",
abstract = "Exercise training prevents age-related decline in muscle function. Targeting epigenetic aging is a promising actionable mechanism and late- life exercise mitigates epi -genetic 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 aero -bic 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 struc-ture, 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.",
keywords = "aging, cardiorespiratory fitness, DNA methylation, exercise training, human skeletal muscle, meta-analysis, mRNA expression",
author = "Sarah Voisin and Kirsten Seale and Macsue Jacques and Shanie Landen and Harvey, {Nicholas R.} and Haupt, {Larisa M.} and Griffiths, {Lyn R.} and Ashton, {Kevin J.} and Coffey, {Vernon G.} and Thompson, {Jamie Lee M.} and Doering, {Thomas M.} and Lindholm, {Malene E.} and Colum Walsh and Gareth Davison and Rachelle Irwin and Catherine McBride and Ola Hansson and Olof Asplund and Heikkinen, {Aino E.} and P{\"a}ivi Piiril{\"a} and Pietil{\"a}inen, {Kirsi H.} and Miina Ollikainen and Sara Blocquiaux and Martine Thomis and Dawn, {Coletta K.} and Sharples, {Adam P.} and Nir Eynon",
note = "Publisher Copyright: {\textcopyright} 2023 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd.",
year = "2024",
doi = "10.1111/acel.13859",
language = "English",
volume = "23",
journal = "Aging Cell",
issn = "1474-9718",
publisher = "Wiley-Blackwell",
number = "1",

}

RIS

TY - JOUR

T1 - Exercise is associated with younger methylome and transcriptome profiles in human skeletal muscle

AU - Voisin, Sarah

AU - Seale, Kirsten

AU - Jacques, Macsue

AU - Landen, Shanie

AU - Harvey, Nicholas R.

AU - Haupt, Larisa M.

AU - Griffiths, Lyn R.

AU - Ashton, Kevin J.

AU - Coffey, Vernon G.

AU - Thompson, Jamie Lee M.

AU - Doering, Thomas M.

AU - Lindholm, Malene E.

AU - Walsh, Colum

AU - Davison, Gareth

AU - Irwin, Rachelle

AU - McBride, Catherine

AU - Hansson, Ola

AU - Asplund, Olof

AU - Heikkinen, Aino E.

AU - Piirilä, Päivi

AU - Pietiläinen, Kirsi H.

AU - Ollikainen, Miina

AU - Blocquiaux, Sara

AU - Thomis, Martine

AU - Dawn, Coletta K.

AU - Sharples, Adam P.

AU - Eynon, Nir

N1 - Publisher Copyright: © 2023 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd.

PY - 2024

Y1 - 2024

N2 - Exercise training prevents age-related decline in muscle function. Targeting epigenetic aging is a promising actionable mechanism and late- life exercise mitigates epi -genetic 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 aero -bic 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 struc-ture, 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.

AB - Exercise training prevents age-related decline in muscle function. Targeting epigenetic aging is a promising actionable mechanism and late- life exercise mitigates epi -genetic 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 aero -bic 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 struc-ture, 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.

KW - aging

KW - cardiorespiratory fitness

KW - DNA methylation

KW - exercise training

KW - human skeletal muscle

KW - meta-analysis

KW - mRNA expression

U2 - 10.1111/acel.13859

DO - 10.1111/acel.13859

M3 - Journal article

C2 - 37128843

AN - SCOPUS:85157977495

VL - 23

JO - Aging Cell

JF - Aging Cell

SN - 1474-9718

IS - 1

M1 - e13859

ER -

ID: 347485717