Molecular Choreography of Acute Exercise

Kévin Contrepois; Si Wu; Kegan J. Moneghetti; Daniel Hornburg; Sara Ahadi; Ming Shian Tsai; Ahmed A. Metwally; Eric Wei; Brittany Lee-McMullen; Jeniffer V. Quijada; Songjie Chen; Jeffrey W. Christle; Mathew Ellenberger; Brunilda Balliu; Shalina Taylor; Matthew G. Durrant; David A. Knowles; Hani Choudhry; Melanie Ashland; Amir Bahmani; Brooke Enslen; Myriam Amsallem; Yukari Kobayashi; Monika Avina; Dalia Perelman; Sophia Miryam Schüssler-Fiorenza Rose; Wenyu Zhou; Euan A. Ashley; Stephen B. Montgomery; Hassan Chaib; Francois Haddad; Michael P. Snyder

doi:10.1016/j.cell.2020.04.043

Molecular Choreography of Acute Exercise

Kévin Contrepois, Si Wu, Kegan J. Moneghetti, Daniel Hornburg, Sara Ahadi, Ming Shian Tsai, Ahmed A. Metwally, Eric Wei, Brittany Lee-McMullen, Jeniffer V. Quijada, Songjie Chen, Jeffrey W. Christle, Mathew Ellenberger, Brunilda Balliu, Shalina Taylor, Matthew G. Durrant, David A. Knowles, Hani Choudhry, Melanie Ashland, Amir BahmaniBrooke Enslen, Myriam Amsallem, Yukari Kobayashi, Monika Avina, Dalia Perelman, Sophia Miryam Schüssler-Fiorenza Rose, Wenyu Zhou, Euan A. Ashley, Stephen B. Montgomery, Hassan Chaib, Francois Haddad, Michael P. Snyder

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

276 Scopus citations

Abstract

Acute physical activity leads to several changes in metabolic, cardiovascular, and immune pathways. Although studies have examined selected changes in these pathways, the system-wide molecular response to an acute bout of exercise has not been fully characterized. We performed longitudinal multi-omic profiling of plasma and peripheral blood mononuclear cells including metabolome, lipidome, immunome, proteome, and transcriptome from 36 well-characterized volunteers, before and after a controlled bout of symptom-limited exercise. Time-series analysis revealed thousands of molecular changes and an orchestrated choreography of biological processes involving energy metabolism, oxidative stress, inflammation, tissue repair, and growth factor response, as well as regulatory pathways. Most of these processes were dampened and some were reversed in insulin-resistant participants. Finally, we discovered biological pathways involved in cardiopulmonary exercise response and developed prediction models revealing potential resting blood-based biomarkers of peak oxygen consumption.

Original language	English
Pages (from-to)	1112-1130.e16
Journal	Cell
Volume	181
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2020.04.043
State	Published - 28 May 2020
Externally published	Yes

Keywords

cardiopulmonary exercise testing
fitness
insulin resistance
multi-omics
outlier analysis
peak VO
physical activity
predictive analytics
systems biology
time-series analysis

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2020.04.043

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Contrepois, K., Wu, S., Moneghetti, K. J., Hornburg, D., Ahadi, S., Tsai, M. S., Metwally, A. A., Wei, E., Lee-McMullen, B., Quijada, J. V., Chen, S., Christle, J. W., Ellenberger, M., Balliu, B., Taylor, S., Durrant, M. G., Knowles, D. A., Choudhry, H., Ashland, M., ... Snyder, M. P. (2020). Molecular Choreography of Acute Exercise. Cell, 181(5), 1112-1130.e16. https://doi.org/10.1016/j.cell.2020.04.043

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title = "Molecular Choreography of Acute Exercise",

abstract = "Acute physical activity leads to several changes in metabolic, cardiovascular, and immune pathways. Although studies have examined selected changes in these pathways, the system-wide molecular response to an acute bout of exercise has not been fully characterized. We performed longitudinal multi-omic profiling of plasma and peripheral blood mononuclear cells including metabolome, lipidome, immunome, proteome, and transcriptome from 36 well-characterized volunteers, before and after a controlled bout of symptom-limited exercise. Time-series analysis revealed thousands of molecular changes and an orchestrated choreography of biological processes involving energy metabolism, oxidative stress, inflammation, tissue repair, and growth factor response, as well as regulatory pathways. Most of these processes were dampened and some were reversed in insulin-resistant participants. Finally, we discovered biological pathways involved in cardiopulmonary exercise response and developed prediction models revealing potential resting blood-based biomarkers of peak oxygen consumption.",

keywords = "cardiopulmonary exercise testing, fitness, insulin resistance, multi-omics, outlier analysis, peak VO, physical activity, predictive analytics, systems biology, time-series analysis",

author = "K{\'e}vin Contrepois and Si Wu and Moneghetti, {Kegan J.} and Daniel Hornburg and Sara Ahadi and Tsai, {Ming Shian} and Metwally, {Ahmed A.} and Eric Wei and Brittany Lee-McMullen and Quijada, {Jeniffer V.} and Songjie Chen and Christle, {Jeffrey W.} and Mathew Ellenberger and Brunilda Balliu and Shalina Taylor and Durrant, {Matthew G.} and Knowles, {David A.} and Hani Choudhry and Melanie Ashland and Amir Bahmani and Brooke Enslen and Myriam Amsallem and Yukari Kobayashi and Monika Avina and Dalia Perelman and {Sch{\"u}ssler-Fiorenza Rose}, {Sophia Miryam} and Wenyu Zhou and Ashley, {Euan A.} and Montgomery, {Stephen B.} and Hassan Chaib and Francois Haddad and Snyder, {Michael P.}",

note = "Publisher Copyright: {\textcopyright} 2020 Elsevier Inc.",

year = "2020",

month = may,

day = "28",

doi = "10.1016/j.cell.2020.04.043",

language = "English",

volume = "181",

pages = "1112--1130.e16",

journal = "Cell",

issn = "0092-8674",

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Contrepois, K, Wu, S, Moneghetti, KJ, Hornburg, D, Ahadi, S, Tsai, MS, Metwally, AA, Wei, E, Lee-McMullen, B, Quijada, JV, Chen, S, Christle, JW, Ellenberger, M, Balliu, B, Taylor, S, Durrant, MG, Knowles, DA, Choudhry, H, Ashland, M, Bahmani, A, Enslen, B, Amsallem, M, Kobayashi, Y, Avina, M, Perelman, D, Schüssler-Fiorenza Rose, SM, Zhou, W, Ashley, EA, Montgomery, SB, Chaib, H, Haddad, F & Snyder, MP 2020, 'Molecular Choreography of Acute Exercise', Cell, vol. 181, no. 5, pp. 1112-1130.e16. https://doi.org/10.1016/j.cell.2020.04.043

TY - JOUR

T1 - Molecular Choreography of Acute Exercise

AU - Contrepois, Kévin

AU - Wu, Si

AU - Moneghetti, Kegan J.

AU - Hornburg, Daniel

AU - Ahadi, Sara

AU - Tsai, Ming Shian

AU - Metwally, Ahmed A.

AU - Wei, Eric

AU - Lee-McMullen, Brittany

AU - Quijada, Jeniffer V.

AU - Chen, Songjie

AU - Christle, Jeffrey W.

AU - Ellenberger, Mathew

AU - Balliu, Brunilda

AU - Taylor, Shalina

AU - Durrant, Matthew G.

AU - Knowles, David A.

AU - Choudhry, Hani

AU - Ashland, Melanie

AU - Bahmani, Amir

AU - Enslen, Brooke

AU - Amsallem, Myriam

AU - Kobayashi, Yukari

AU - Avina, Monika

AU - Perelman, Dalia

AU - Schüssler-Fiorenza Rose, Sophia Miryam

AU - Zhou, Wenyu

AU - Ashley, Euan A.

AU - Montgomery, Stephen B.

AU - Chaib, Hassan

AU - Haddad, Francois

AU - Snyder, Michael P.

PY - 2020/5/28

Y1 - 2020/5/28

N2 - Acute physical activity leads to several changes in metabolic, cardiovascular, and immune pathways. Although studies have examined selected changes in these pathways, the system-wide molecular response to an acute bout of exercise has not been fully characterized. We performed longitudinal multi-omic profiling of plasma and peripheral blood mononuclear cells including metabolome, lipidome, immunome, proteome, and transcriptome from 36 well-characterized volunteers, before and after a controlled bout of symptom-limited exercise. Time-series analysis revealed thousands of molecular changes and an orchestrated choreography of biological processes involving energy metabolism, oxidative stress, inflammation, tissue repair, and growth factor response, as well as regulatory pathways. Most of these processes were dampened and some were reversed in insulin-resistant participants. Finally, we discovered biological pathways involved in cardiopulmonary exercise response and developed prediction models revealing potential resting blood-based biomarkers of peak oxygen consumption.

AB - Acute physical activity leads to several changes in metabolic, cardiovascular, and immune pathways. Although studies have examined selected changes in these pathways, the system-wide molecular response to an acute bout of exercise has not been fully characterized. We performed longitudinal multi-omic profiling of plasma and peripheral blood mononuclear cells including metabolome, lipidome, immunome, proteome, and transcriptome from 36 well-characterized volunteers, before and after a controlled bout of symptom-limited exercise. Time-series analysis revealed thousands of molecular changes and an orchestrated choreography of biological processes involving energy metabolism, oxidative stress, inflammation, tissue repair, and growth factor response, as well as regulatory pathways. Most of these processes were dampened and some were reversed in insulin-resistant participants. Finally, we discovered biological pathways involved in cardiopulmonary exercise response and developed prediction models revealing potential resting blood-based biomarkers of peak oxygen consumption.

KW - cardiopulmonary exercise testing

KW - fitness

KW - insulin resistance

KW - multi-omics

KW - outlier analysis

KW - peak VO

KW - physical activity

KW - predictive analytics

KW - systems biology

KW - time-series analysis

UR - http://www.scopus.com/inward/record.url?scp=85085345831&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2020.04.043

DO - 10.1016/j.cell.2020.04.043

M3 - Article

C2 - 32470399

AN - SCOPUS:85085345831

SN - 0092-8674

VL - 181

SP - 1112-1130.e16

JO - Cell

JF - Cell

IS - 5

ER -

Molecular Choreography of Acute Exercise

Abstract

Keywords

ASJC Scopus subject areas

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