Time course-dependent changes in the transcriptome of human skeletal muscle during recovery from endurance exercise: From inflammation to adaptive remodeling

Oliver Neubauer, Surendran Sabapathy, Kevin J. Ashton, Ben Desbrow, Jonathan M. Peake, Ross Lazarus, Barbara Wessner, David Cameron-Smith, Karl Heinz Wagner, Luke J. Haseler, Andrew C. Bulmer

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25 Citations (Scopus)

Abstract

Reprogramming of gene expression is fundamental for skeletal muscle adaptations in response to endurance exercise. This study investigated the time course-dependent changes in the muscular transcriptome after an endurance exercise trial consisting of 1 h of intense cycling immediately followed by 1 h of intense running. Skeletal muscle samples were taken at baseline, 3 h, 48 h, and 96 h postexercise from eight healthy, endurance-trained men. RNA was extracted from muscle. Differential gene expression was evaluated using Illumina microarrays and validated with qPCR. Gene set enrichment analysis identified enriched molecular signatures chosen from the Molecular Signatures Database. Three hours postexercise, 102 gene sets were upregulated [family wise error rate (FWER), P < 0.05], including groups of genes related with leukocyte migration, immune and chaperone activation, and cyclic AMP responsive element binding protein (CREB) 1 signaling. Forty-eight hours postexercise, among 19 enriched gene sets (FWER, P<0.05), two gene sets related to actin cytoskeleton remodeling were upregulated. Ninety-six hours postexercise, 83 gene sets were enriched (FWER, P < 0.05), 80 of which were upregulated, including gene groups related to chemokine signaling, cell stress management, and extracellular matrix remodeling. These data provide comprehensive insights into the molecular pathways involved in acute stress, recovery, and adaptive muscular responses to endurance exercise. The novel 96 h postexercise transcriptome indicates substantial transcriptional activity potentially associated with the prolonged presence of leukocytes in the muscles. This suggests that muscular recovery, from a transcriptional perspective, is incomplete 96 h after endurance exercise involving muscle damage.

Original languageEnglish
Pages (from-to)274-287
Number of pages14
JournalJournal of Applied Physiology
Volume116
Issue number3
DOIs
Publication statusPublished - 1 Feb 2014

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Transcriptome
Skeletal Muscle
Exercise
Inflammation
Genes
Muscles
Leukocytes
Chemical Databases
Gene Expression
Actin Cytoskeleton
Chemokines
Running
Cyclic AMP
Extracellular Matrix
Carrier Proteins
RNA

Cite this

Neubauer, Oliver ; Sabapathy, Surendran ; Ashton, Kevin J. ; Desbrow, Ben ; Peake, Jonathan M. ; Lazarus, Ross ; Wessner, Barbara ; Cameron-Smith, David ; Wagner, Karl Heinz ; Haseler, Luke J. ; Bulmer, Andrew C. / Time course-dependent changes in the transcriptome of human skeletal muscle during recovery from endurance exercise : From inflammation to adaptive remodeling. In: Journal of Applied Physiology. 2014 ; Vol. 116, No. 3. pp. 274-287.
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abstract = "Reprogramming of gene expression is fundamental for skeletal muscle adaptations in response to endurance exercise. This study investigated the time course-dependent changes in the muscular transcriptome after an endurance exercise trial consisting of 1 h of intense cycling immediately followed by 1 h of intense running. Skeletal muscle samples were taken at baseline, 3 h, 48 h, and 96 h postexercise from eight healthy, endurance-trained men. RNA was extracted from muscle. Differential gene expression was evaluated using Illumina microarrays and validated with qPCR. Gene set enrichment analysis identified enriched molecular signatures chosen from the Molecular Signatures Database. Three hours postexercise, 102 gene sets were upregulated [family wise error rate (FWER), P < 0.05], including groups of genes related with leukocyte migration, immune and chaperone activation, and cyclic AMP responsive element binding protein (CREB) 1 signaling. Forty-eight hours postexercise, among 19 enriched gene sets (FWER, P<0.05), two gene sets related to actin cytoskeleton remodeling were upregulated. Ninety-six hours postexercise, 83 gene sets were enriched (FWER, P < 0.05), 80 of which were upregulated, including gene groups related to chemokine signaling, cell stress management, and extracellular matrix remodeling. These data provide comprehensive insights into the molecular pathways involved in acute stress, recovery, and adaptive muscular responses to endurance exercise. The novel 96 h postexercise transcriptome indicates substantial transcriptional activity potentially associated with the prolonged presence of leukocytes in the muscles. This suggests that muscular recovery, from a transcriptional perspective, is incomplete 96 h after endurance exercise involving muscle damage.",
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Neubauer, O, Sabapathy, S, Ashton, KJ, Desbrow, B, Peake, JM, Lazarus, R, Wessner, B, Cameron-Smith, D, Wagner, KH, Haseler, LJ & Bulmer, AC 2014, 'Time course-dependent changes in the transcriptome of human skeletal muscle during recovery from endurance exercise: From inflammation to adaptive remodeling' Journal of Applied Physiology, vol. 116, no. 3, pp. 274-287. https://doi.org/10.1152/japplphysiol.00909.2013

Time course-dependent changes in the transcriptome of human skeletal muscle during recovery from endurance exercise : From inflammation to adaptive remodeling. / Neubauer, Oliver; Sabapathy, Surendran; Ashton, Kevin J.; Desbrow, Ben; Peake, Jonathan M.; Lazarus, Ross; Wessner, Barbara; Cameron-Smith, David; Wagner, Karl Heinz; Haseler, Luke J.; Bulmer, Andrew C.

In: Journal of Applied Physiology, Vol. 116, No. 3, 01.02.2014, p. 274-287.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Peake, Jonathan M.

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