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Molecular adaptations in response to exercise training are associated with tissue-specific transcriptomic and epigenomic signatures

2024; Elsevier BV; Volume: 4; Issue: 6 Linguagem: Inglês

10.1016/j.xgen.2023.100421

2666-979X

Venugopalan D. Nair, Hanna Pinças, Gregory R. Smith, Elena Zaslavsky, Yongchao Ge, Mary Anne S. Amper, Mital Vasoya, Maria Chikina, Yifei Sun, Archana N. Raja, Weiguang Mao, Nicole R. Gay, Karyn A. Esser, Kevin S. Smith, Bingqing Zhao, Laurens Wiel, Aditya Singh, Maléne E. Lindholm, David Amar, Stephen B. Montgomery, M Snyder, Martin J. Walsh, Stuart C. Sealfon, Joshua Adkins, José Juan Almagro Armenteros, Euan A. Ashley, Dam Bae, Marcas M. Bamman, Nasim Bararpour, Alexis H. Bennett, Bryan C. Bergman, Daniel H. Bessesen, Sue C. Bodine, Thomas W. Buford, Toby L. Chambers, Clarisa Chavez, Tiffany Cortes, Gary Cutter, Sara Espinoza, Facundo M. Fernández, Nicole Gagne, David A. Gaul, Bret H. Goodpaster, Chia-Jui Hung, Bailey E. Jackson, Catherine M. Jankowski, Christopher Jin, Wendy M. Kohrt, Kyle S. Kramer, Bridget Lester, Ana Lira, Sandy May, Nada Marjanović, Edward L. Melanson, Samuel G. Moore, Kerrie L. Moreau, Nicolas Musi, Daniel Nachum, German Nudelman, Marco Pahor, D.C. Patel, Paul Piehowski, Wei-Jun Qian, Blake B. Rasmussen, Stas Rirak, Jessica L. Rooney, James Sanford, Evan Savage, Irene E. Schauer, Monica C. Serra, Cynthia L. Stowe, Anna Thalacker‐Mercer, Todd A. Trappe, Scott Trappe, Nikolai G. Vetr, Elena Volpi, Matthew T. Wheeler, Si Wu, Navid Zebarjadi, Jimmy Zhen,

Birth, Development, and Health

Regular exercise has many physical and brain health benefits, yet the molecular mechanisms mediating exercise effects across tissues remain poorly understood. Here we analyzed 400 high-quality DNA methylation, ATAC-seq, and RNA-seq datasets from eight tissues from control and endurance exercise-trained (EET) rats. Integration of baseline datasets mapped the gene location dependence of epigenetic control features and identified differing regulatory landscapes in each tissue. The transcriptional responses to 8 weeks of EET showed little overlap across tissues and predominantly comprised tissue-type enriched genes. We identified sex differences in the transcriptomic and epigenomic changes induced by EET. However, the sex-biased gene responses were linked to shared signaling pathways. We found that many G protein-coupled receptor-encoding genes are regulated by EET, suggesting a role for these receptors in mediating the molecular adaptations to training across tissues. Our findings provide new insights into the mechanisms underlying EET-induced health benefits across organs.