Temporal dynamics of the multi-omic response to endurance exercise training

Author:

, , ,Amar DavidORCID,Gay Nicole R.ORCID,Jean-Beltran Pierre M.ORCID, ,Bae Dam,Dasari Surendra,Dennis Courtney,Evans Charles R.,Gaul David A.ORCID,Ilkayeva OlgaORCID,Ivanova Anna A.,Kachman Maureen T.ORCID,Keshishian Hasmik,Lanza Ian R.,Lira Ana C.,Muehlbauer Michael J.,Nair Venugopalan D.ORCID,Piehowski Paul D.ORCID,Rooney Jessica L.,Smith Kevin S.,Stowe Cynthia L.ORCID,Zhao Bingqing, ,Clark Natalie M.,Jimenez-Morales DavidORCID,Lindholm Malene E.ORCID,Many Gina M.ORCID,Sanford James A.ORCID,Smith Gregory R.ORCID,Vetr Nikolai G.,Zhang Tiantian,Almagro Armenteros Jose J.,Avila-Pacheco JulianORCID,Bararpour NasimORCID,Ge Yongchao,Hou ZhenxinORCID,Marwaha ShrutiORCID,Presby David M.,Natarajan Raja Archana,Savage Evan M.,Steep Alec,Sun Yifei,Wu SiORCID,Zhen Jimmy, ,Bodine Sue C.ORCID,Esser Karyn A.ORCID,Goodyear Laurie J.ORCID,Schenk SimonORCID, , ,Montgomery Stephen B.ORCID,Fernández Facundo M.ORCID,Sealfon Stuart C.ORCID,Snyder Michael P.ORCID, ,Adkins Joshua N.ORCID,Ashley EuanORCID,Burant Charles F.,Carr Steven A.ORCID,Clish Clary B.ORCID,Cutter GaryORCID,Gerszten Robert E.ORCID,Kraus William E.ORCID,Li Jun Z.,Miller Michael E.,Nair K. SreekumaranORCID,Newgard ChristopherORCID,Ortlund Eric A.ORCID,Qian Wei-JunORCID,Tracy RussellORCID,Walsh Martin J.ORCID,Wheeler Matthew T., , , ,Dalton Karen P.,Hastie TrevorORCID,Hershman Steven G.,Samdarshi Mihir,Teng Christopher,Tibshirani Rob, ,Cornell Elaine,Gagne Nicole,May Sandy, ,Bouverat Brian,Leeuwenburgh Christiaan,Lu Ching-ju,Pahor Marco, ,Hsu Fang-Chi,Rushing Scott,Walkup Michael P., ,Nicklas Barbara,Rejeski W. JackORCID, ,Williams John P.,Xia Ashley, ,Albertson Brent G.,Barton Elisabeth R.,Booth Frank W.,Caputo Tiziana,Cicha Michael,De Sousa Luis Gustavo Oliveira,Farrar Roger,Hevener Andrea L.ORCID,Hirshman Michael F.ORCID,Jackson Bailey E.,Ke Benjamin G.,Kramer Kyle S.,Lessard Sarah J.ORCID,Makarewicz Nathan S.,Marshall Andrea G.,Nigro PasqualeORCID,Powers Scott,Ramachandran Krithika,Rector R. Scott,Richards Collyn Z-T.,Thyfault JohnORCID,Yan ZhenORCID,Zang Chongzhi, ,Amper Mary Anne S.ORCID,Balci Ali Tugrul,Chavez Clarisa,Chikina Maria,Chiu Roxanne,Gritsenko Marina A.ORCID,Guevara Kristy,Hansen Joshua R.ORCID,Hennig Krista M.,Hung Chia-Jui,Hutchinson-Bunch Chelsea,Jin Christopher A.,Liu Xueyun,Maner-Smith Kristal M.ORCID,Mani D. R.ORCID,Marjanovic Nada,Monroe Matthew E.ORCID,Moore Ronald J.ORCID,Moore Samuel G.ORCID,Mundorff Charles C.ORCID,Nachun Daniel,Nestor Michael D.ORCID,Nudelman German,Pearce Cadence,Petyuk Vladislav A.ORCID,Pincas Hanna,Ramos IreneORCID,Raskind Alexander,Rirak Stas,Robbins Jeremy M.,Rubenstein Aliza B.,Ruf-Zamojski FrederiqueORCID,Sagendorf Tyler J.ORCID,Seenarine Nitish,Soni Tanu,Uppal Karan,Vangeti SindhuORCID,Vasoya Mital,Vornholt Alexandria,Yu Xuechen,Zaslavsky ElenaORCID,Zebarjadi Navid, ,Bamman Marcas,Bergman Bryan C.ORCID,Bessesen Daniel H.,Buford Thomas W.ORCID,Chambers Toby L.ORCID,Coen Paul M.ORCID,Cooper Dan,Haddad Fadia,Gadde Kishore,Goodpaster Bret H.ORCID,Harris Melissa,Huffman Kim M.,Jankowski Catherine M.,Johannsen Neil M.,Kohrt Wendy M.,Lester Bridget,Melanson Edward L.,Moreau Kerrie L.,Musi Nicolas,Newton Robert L.,Radom-Aizik Shlomit,Ramaker Megan E.,Rankinen Tuomo,Rasmussen Blake B.ORCID,Ravussin EricORCID,Schauer Irene E.,Schwartz Robert S.,Sparks Lauren M.ORCID,Thalacker-Mercer AnnaORCID,Trappe Scott,Trappe Todd A.,Volpi Elena

Abstract

AbstractRegular exercise promotes whole-body health and prevents disease, but the underlying molecular mechanisms are incompletely understood1–3. Here, the Molecular Transducers of Physical Activity Consortium4 profiled the temporal transcriptome, proteome, metabolome, lipidome, phosphoproteome, acetylproteome, ubiquitylproteome, epigenome and immunome in whole blood, plasma and 18 solid tissues in male and female Rattus norvegicus over eight weeks of endurance exercise training. The resulting data compendium encompasses 9,466 assays across 19 tissues, 25 molecular platforms and 4 training time points. Thousands of shared and tissue-specific molecular alterations were identified, with sex differences found in multiple tissues. Temporal multi-omic and multi-tissue analyses revealed expansive biological insights into the adaptive responses to endurance training, including widespread regulation of immune, metabolic, stress response and mitochondrial pathways. Many changes were relevant to human health, including non-alcoholic fatty liver disease, inflammatory bowel disease, cardiovascular health and tissue injury and recovery. The data and analyses presented in this study will serve as valuable resources for understanding and exploring the multi-tissue molecular effects of endurance training and are provided in a public repository (https://motrpac-data.org/).

Publisher

Springer Science and Business Media LLC

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