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

Author:

Neubauer Oliver12,Sabapathy Surendran2,Ashton Kevin J.3,Desbrow Ben4,Peake Jonathan M.5,Lazarus Ross67,Wessner Barbara8,Cameron-Smith David9,Wagner Karl-Heinz12,Haseler Luke J.2,Bulmer Andrew C.2

Affiliation:

1. Emerging Field Oxidative Stress and DNA Stability, Research Platform Active Aging, and Department of Nutritional Sciences, University of Vienna, Austria;

2. Heart Foundation Research Centre, Griffith Health Institute, Griffith University, Gold Coast Campus, Australia;

3. Faculty of Health Sciences and Medicine, Bond University, Robina, Australia;

4. The School of Allied Health Sciences, Griffith Health Institute, Griffith University, Gold Coast Campus, Australia;

5. School of Biomedical Sciences, Queensland University of Technology, Brisbane, Australia;

6. Genomics & Systems Biology, Baker IDI Heart and Diabetes Institute, Melbourne, Australia;

7. Harvard Medical School, Boston, Massachusetts;

8. Research Platform Active Aging, and Department of Sports and Exercise Physiology, University of Vienna, Austria; and

9. Liggins Institute, University of Auckland, New Zealand

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.

Publisher

American Physiological Society

Subject

Physiology (medical),Physiology

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