Sex-Specific Skeletal Muscle Gene Expression Responses to Exercise Reveal Novel Direct Mediators of Insulin Sensitivity Change

Authors

S Ma, Institute for Health Informatics (IHI), Academic Health Center, University of Minnesota, Minneapolis, MN 55455.
M C. Morris, Center for Clinical Systems Biology, Rochester General Hospital, Rochester, NY 14621.
M J. Hubal, Department of Kinesiology, Indiana University - Indianapolis, Indianapolis IN 46202.
L M. Ross, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
K M. Huffman, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
C G. Vann, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
N Moore, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
E R. Hauser, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
A Bareja, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
R Jiang, Department of Head and Neck Surgery & Communication Sciences, Duke University School of Medicine, Durham, NC 27701.
E Kummerfeld, Institute for Health Informatics (IHI), Academic Health Center, University of Minnesota, Minneapolis, MN 55455.
M D. Barberio, Department of Exercise and Nutrition Sciences, George Washington University, Washington DC 20052.
J A. Houmard, Department of Kinesiology, ECU, Greenville, NC 27858.
W B. Bennett, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
J L. Johnson, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
J A. Timmons, School of Medicine and Dentistry, Queen Mary University of London, UK.
G Broderick, Center for Clinical Systems Biology, Rochester General Hospital, Rochester, NY 14621.
V B. Kraus, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.
C F. Aliferis, Institute for Health Informatics (IHI), Academic Health Center, University of Minnesota, Minneapolis, MN 55455.
W E. Kraus, Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC 27701.

Document Type

Journal Article

Publication Date

9-8-2024

Journal

medRxiv : the preprint server for health sciences

DOI

10.1101/2024.09.07.24313236

Abstract

BACKGROUND: Understanding the causal pathways, systems, and mechanisms through which exercise impacts human health is complex. This study explores molecular signaling related to whole-body insulin sensitivity (Si) by examining changes in skeletal muscle gene expression. The analysis considers differences by biological sex, exercise amount, and exercise intensity to identify potential molecular targets for developing pharmacologic agents that replicate the health benefits of exercise. METHODS: The study involved 53 participants from the STRRIDE I and II trials who completed eight months of aerobic training. Skeletal muscle gene expression was measured using Affymetrix and Illumina technologies, while pre- and post-training Si was assessed via an intravenous glucose tolerance test. A novel gene discovery protocol, integrating three literature-derived and data-driven modeling strategies, was employed to identify causal pathways and direct causal factors based on differentially expressed transcripts associated with exercise intensity and amount. RESULTS: In women, the transcription factor targets identified were primarily influenced by exercise amount and were generally inhibitory. In contrast, in men, these targets were driven by exercise intensity and were generally activating. Transcription factors such as ATF1, CEBPA, BACH2, and STAT1 were commonly activating in both sexes. Specific transcriptional targets related to exercise-induced Si improvements included TACR3 and TMC7 for intensity-driven effects, and GRIN3B and EIF3B for amount-driven effects. Two key signaling pathways mediating aerobic exercise-induced Si improvements were identified: one centered on estrogen signaling and the other on phorbol ester (PKC) signaling, both converging on the epidermal growth factor receptor (EGFR) and other relevant targets. CONCLUSIONS: The signaling pathways mediating Si improvements from aerobic exercise differed by sex and were further distinguished by exercise intensity and amount. Transcriptional adaptations in skeletal muscle related to Si improvements appear to be causally linked to estrogen and PKC signaling, with EGFR and other identified targets emerging as potential skeletal muscle-specific drug targets to mimic the beneficial effects of exercise on Si.

Department

Exercise and Nutrition Sciences

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