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

Manuscript Writing Group; Senior Leadership; Co-corresponding Authors; MoTrPAC Study Group; Bioinformatics Center; Biospecimens Repository; Administrative Coordinating Center; Data Management, Analysis, and Quality Control Center; Exercise Intervention Core; NIH; Preclinical Animal Study Sites; Chemical Analysis Sites; Clinical Sites; MoTrPAC Study Group; Primary authors; Lead Analysts; Lead Data Generators; Analysts; Animal Study Leadership; Manuscript Writing Group Leads

doi:10.1038/s41586-023-06877-w

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

Manuscript Writing Group
, Senior Leadership
, Co-corresponding Authors
, MoTrPAC Study Group
, Bioinformatics Center
, Biospecimens Repository
, Administrative Coordinating Center
, Data Management, Analysis, and Quality Control Center
, Exercise Intervention Core
, NIH
, Preclinical Animal Study Sites
, Chemical Analysis Sites
, Clinical Sites
, MoTrPAC Study Group
, Primary authors
, Lead Analysts
, Lead Data Generators
, Analysts
, Animal Study Leadership
, Manuscript Writing Group Leads

Stanford University
Broad Institute
University of Iowa
Mayo Clinic Rochester, MN
University of Michigan, Ann Arbor
Georgia Institute of Technology
Duke University
Emory University
Icahn School of Medicine at Mount Sinai
Pacific Northwest National Laboratory
University of Vermont
Wake Forest University
Joslin Diabetes Center
Oklahoma Medical Research Foundation
University of Florida
University of California at San Diego
University of Alabama at Birmingham
Beth Israel Deaconess Medical Center
National Institutes of Health
University of Missouri
University of Texas at Austin
University of California at Los Angeles
University of Virginia
Vanderbilt University
Stetson University
University of Kansas
Virginia Polytechnic Institute and State University
University of Pittsburgh
University of Colorado Anschutz Medical Campus
Ball State University
Translational Research Institute
University of California at Irvine
LSU Pennington Biomedical Research Center
Cedars-Sinai Medical Center
University of Texas Health Science Center at San Antonio

Research output: Contribution to journal › Article › peer-review

171 Scopus citations

Abstract

Regular exercise promotes whole-body health and prevents disease, but the underlying molecular mechanisms are incompletely understood^1–3. 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/).

Original language	English
Pages (from-to)	174-183
Number of pages	10
Journal	Nature
Volume	629
Issue number	8010
DOIs	https://doi.org/10.1038/s41586-023-06877-w
State	Published - 2 May 2024
Externally published	Yes

Funding

Funders	Funder number
F32 postdoctoral fellowship
Knut och Alice Wallenbergs Stiftelse
National Heart, Lung, and Blood Institute
National Opinion Research Center
U.S. Department of Health and Human Services
National Science Foundation Major Research Instrumentation
National Science Foundation	1726528, 1445197
National Human Genome Research Institute	5T32HG000044
Materials Research Institute, Pennsylvania State University	CHE-1726528
National Institute on Aging	P30AG003319, P30AG044271
National Institutes of Health	U24OD026629, U01AG055137, U24DK112340, U24DK112341, U24DK112342, U24DK112331, F32HL154711, U01AR071128, U01AR071158, U01AR071124, U01AR071133, U24AR071113, U01AR071130, U01AR071150, U01AR071160, U24DK112326, U24DK112348, U24DK112349, U01AG055133, U01AG055135
University of Chicago	P30DK07247

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10.1038/s41586-023-06877-w

Cite this

Manuscript Writing Group, Senior Leadership, Co-corresponding Authors, MoTrPAC Study Group, Bioinformatics Center, Biospecimens Repository, Administrative Coordinating Center, Data Management, Analysis, and Quality Control Center, Exercise Intervention Core, NIH, Preclinical Animal Study Sites, Chemical Analysis Sites, Clinical Sites, MoTrPAC Study Group, Primary authors, Lead Analysts, Lead Data Generators, Analysts, Animal Study Leadership, & Manuscript Writing Group Leads (2024). Temporal dynamics of the multi-omic response to endurance exercise training. Nature, 629(8010), 174-183. https://doi.org/10.1038/s41586-023-06877-w

@article{d44e15edb3614d9ba27ea8d3feed2cbc,

title = "Temporal dynamics of the multi-omic response to endurance exercise training",

abstract = "Regular 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/).",

author = "\{Manuscript Writing Group\} and \{Senior Leadership\} and \{Co-corresponding Authors\} and \{MoTrPAC Study Group\} and \{Bioinformatics Center\} and \{Biospecimens Repository\} and \{Administrative Coordinating Center\} and \{Data Management, Analysis, and Quality Control Center\} and \{Exercise Intervention Core\} and NIH and \{Preclinical Animal Study Sites\} and \{Chemical Analysis Sites\} and \{Clinical Sites\} and \{MoTrPAC Study Group\} and \{Primary authors\} and \{Lead Analysts\} and \{Lead Data Generators\} and Analysts and \{Animal Study Leadership\} and \{Manuscript Writing Group Leads\} and David Amar and Gay, \{Nicole R.\} and Jean-Beltran, \{Pierre M.\} and Dam Bae and Surendra Dasari and Courtney Dennis and Evans, \{Charles R.\} and Gaul, \{David A.\} and Olga Ilkayeva and Ivanova, \{Anna A.\} and Kachman, \{Maureen T.\} and Hasmik Keshishian and Lanza, \{Ian R.\} and Lira, \{Ana C.\} and Muehlbauer, \{Michael J.\} and Nair, \{Venugopalan D.\} and Piehowski, \{Paul D.\} and Rooney, \{Jessica L.\} and Smith, \{Kevin S.\} and Stowe, \{Cynthia L.\} and Bingqing Zhao and Clark, \{Natalie M.\} and David Jimenez-Morales and Lindholm, \{Malene E.\} and Many, \{Gina M.\} and Sanford, \{James A.\} and Smith, \{Gregory R.\} and Vetr, \{Nikolai G.\} and Tiantian Zhang and \{Almagro Armenteros\}, \{Jose J.\} and Julian Avila-Pacheco and Nasim Bararpour and Yongchao Ge and Zhenxin Hou and Shruti Marwaha and Presby, \{David M.\} and \{Natarajan Raja\}, Archana and Savage, \{Evan M.\} and Alec Steep and Yifei Sun and Si Wu and Jimmy Zhen and Bodine, \{Sue C.\} and Esser, \{Karyn A.\} and Goodyear, \{Laurie J.\} and Simon Schenk and Montgomery, \{Stephen B.\} and Fern{\'a}ndez, \{Facundo M.\} and Sealfon, \{Stuart C.\} and Snyder, \{Michael P.\}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = may,

day = "2",

doi = "10.1038/s41586-023-06877-w",

language = "אנגלית",

volume = "629",

pages = "174--183",

journal = "Nature",

issn = "0028-0836",

number = "8010",

}

Manuscript Writing Group, Senior Leadership, Co-corresponding Authors, MoTrPAC Study Group, Bioinformatics Center, Biospecimens Repository, Administrative Coordinating Center, Data Management, Analysis, and Quality Control Center, Exercise Intervention Core, NIH, Preclinical Animal Study Sites, Chemical Analysis Sites, Clinical Sites, MoTrPAC Study Group, Primary authors, Lead Analysts, Lead Data Generators, Analysts, Animal Study Leadership & Manuscript Writing Group Leads 2024, 'Temporal dynamics of the multi-omic response to endurance exercise training', Nature, vol. 629, no. 8010, pp. 174-183. https://doi.org/10.1038/s41586-023-06877-w

TY - JOUR

T1 - Temporal dynamics of the multi-omic response to endurance exercise training

AU - Manuscript Writing Group

AU - Senior Leadership

AU - Co-corresponding Authors

AU - MoTrPAC Study Group

AU - Bioinformatics Center

AU - Biospecimens Repository

AU - Administrative Coordinating Center

AU - Data Management, Analysis, and Quality Control Center

AU - Exercise Intervention Core

AU - NIH

AU - Preclinical Animal Study Sites

AU - Chemical Analysis Sites

AU - Clinical Sites

AU - MoTrPAC Study Group

AU - Primary authors

AU - Lead Analysts

AU - Lead Data Generators

AU - Analysts

AU - Animal Study Leadership

AU - Manuscript Writing Group Leads

AU - Amar, David

AU - Gay, Nicole R.

AU - Jean-Beltran, Pierre M.

AU - Bae, Dam

AU - Dasari, Surendra

AU - Dennis, Courtney

AU - Evans, Charles R.

AU - Gaul, David A.

AU - Ilkayeva, Olga

AU - Ivanova, Anna A.

AU - Kachman, Maureen T.

AU - Keshishian, Hasmik

AU - Lanza, Ian R.

AU - Lira, Ana C.

AU - Muehlbauer, Michael J.

AU - Nair, Venugopalan D.

AU - Piehowski, Paul D.

AU - Rooney, Jessica L.

AU - Smith, Kevin S.

AU - Stowe, Cynthia L.

AU - Zhao, Bingqing

AU - Clark, Natalie M.

AU - Jimenez-Morales, David

AU - Lindholm, Malene E.

AU - Many, Gina M.

AU - Sanford, James A.

AU - Smith, Gregory R.

AU - Vetr, Nikolai G.

AU - Zhang, Tiantian

AU - Almagro Armenteros, Jose J.

AU - Avila-Pacheco, Julian

AU - Bararpour, Nasim

AU - Ge, Yongchao

AU - Hou, Zhenxin

AU - Marwaha, Shruti

AU - Presby, David M.

AU - Natarajan Raja, Archana

AU - Savage, Evan M.

AU - Steep, Alec

AU - Sun, Yifei

AU - Wu, Si

AU - Zhen, Jimmy

AU - Bodine, Sue C.

AU - Esser, Karyn A.

AU - Goodyear, Laurie J.

AU - Schenk, Simon

AU - Montgomery, Stephen B.

AU - Fernández, Facundo M.

AU - Sealfon, Stuart C.

AU - Snyder, Michael P.

PY - 2024/5/2

Y1 - 2024/5/2

N2 - Regular 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/).

AB - Regular 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/).

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DO - 10.1038/s41586-023-06877-w

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AN - SCOPUS:85191955121

SN - 0028-0836

VL - 629

SP - 174

EP - 183

JO - Nature

JF - Nature

IS - 8010

ER -

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

Abstract

Funding

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