Effects of Acute and Chronic Resistance Exercise on the Skeletal Muscle Metabolome.

beta-citrylglutamate chenodeoxycholate hypertrophy metabolomics resistance exercise skeletal muscle skeletal muscle adaptation

Journal

Metabolites
ISSN: 2218-1989
Titre abrégé: Metabolites
Pays: Switzerland
ID NLM: 101578790

Informations de publication

Date de publication:
16 May 2022
Historique:
received: 28 03 2022
revised: 05 05 2022
accepted: 11 05 2022
entrez: 28 5 2022
pubmed: 29 5 2022
medline: 29 5 2022
Statut: epublish

Résumé

Resistance training promotes metabolic health and stimulates muscle hypertrophy, but the precise routes by which resistance exercise (RE) conveys these health benefits are largely unknown. To investigate how acute RE affects human skeletal muscle metabolism. We collected vastus lateralis biopsies from six healthy male untrained volunteers at rest, before the first of 13 RE training sessions, and 45 min after the first and last bouts of RE. Biopsies were analysed using untargeted mass spectrometry-based metabolomics. We measured 617 metabolites covering a broad range of metabolic pathways. In the untrained state RE altered 33 metabolites, including increased 3-methylhistidine and N-lactoylvaline, suggesting increased protein breakdown, as well as metabolites linked to ATP (xanthosine) and NAD (N1-methyl-2-pyridone-5-carboxamide) metabolism; the bile acid chenodeoxycholate also increased in response to RE in muscle opposing previous findings in blood. Resistance training led to muscle hypertrophy, with slow type I and fast/intermediate type II muscle fibre diameter increasing by 10.7% and 10.4%, respectively. Comparison of post-exercise metabolite levels between trained and untrained state revealed alterations of 46 metabolites, including decreased N-acetylated ketogenic amino acids and increased beta-citrylglutamate which might support growth. Only five of the metabolites that changed after acute exercise in the untrained state were altered after chronic training, indicating that training induces multiple metabolic changes not directly related to the acute exercise response. The human skeletal muscle metabolome is sensitive towards acute RE in the trained and untrained states and reflects a broad range of adaptive processes in response to repeated stimulation.

Identifiants

pubmed: 35629949
pii: metabo12050445
doi: 10.3390/metabo12050445
pmc: PMC9142957
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : Bundesinstitut für Sportwissenschaft
ID : 070106/16-17
Organisme : Bundesinstitut für Sportwissenschaft
ID : 070112/13-14

Références

J Mol Evol. 1983;19(5):371-5
pubmed: 6644831
Cell Rep. 2020 Dec 29;33(13):108554
pubmed: 33378671
Nat Metab. 2020 Sep;2(9):817-828
pubmed: 32747792
Eur J Cardiovasc Prev Rehabil. 2007 Oct;14(5):630-7
pubmed: 17925621
J Appl Physiol (1985). 2007 May;102(5):1767-72
pubmed: 17234805
Nature. 1967 Aug 26;215(5104):993-4
pubmed: 6055440
Acta Physiol (Oxf). 2011 Mar;201(3):365-72
pubmed: 20874802
Exerc Sport Sci Rev. 1991;19:507-37
pubmed: 1936094
Int J Mol Sci. 2020 Sep 25;21(19):
pubmed: 32992783
Appl Physiol Nutr Metab. 2006 Dec;31(6):702-8
pubmed: 17213884
Biochim Biophys Acta. 2012 Sep;1822(9):1442-52
pubmed: 22627108
Nature. 1968 Feb 3;217(5127):452-3
pubmed: 4966706
Med Sci Sports Exerc. 1998 Jan;30(1):67-72
pubmed: 9475646
Fed Proc. 1978 Jul;37(9):2308-12
pubmed: 658470
Int J Sports Med. 1987 Mar;8 Suppl 1:66-9
pubmed: 2953691
Toxins (Basel). 2016 Nov 15;8(11):
pubmed: 27854278
Acta Physiol Scand. 1995 Feb;153(2):87-96
pubmed: 7778464
Nat Commun. 2020 Jan 24;11(1):470
pubmed: 31980607
Physiol Rev. 2008 Oct;88(4):1243-76
pubmed: 18923182
Nat Genet. 2017 Apr;49(4):568-578
pubmed: 28263315
Biochem Biophys Res Commun. 2003 Feb 7;301(2):417-23
pubmed: 12565877
Physiol Rep. 2021 Feb;9(3):e14497
pubmed: 33547753
Biochim Biophys Acta. 1978 Dec 18;544(3):656-66
pubmed: 728476
Circulation. 2006 Aug 8;114(6):597-605
pubmed: 16894049
J Biol Chem. 2021 Jan-Jun;296:100622
pubmed: 33811861
Front Physiol. 2017 Jun 07;8:390
pubmed: 28638350
Cell Metab. 2013 Feb 5;17(2):162-84
pubmed: 23395166
Nat Med. 2017 Aug;23(8):990-996
pubmed: 28650457
Diabetologia. 2014 Nov;57(11):2282-95
pubmed: 25091629
Am J Physiol Cell Physiol. 2020 Aug 1;319(2):C300-C312
pubmed: 32520607
J Physiol. 1997 Jan 1;498 ( Pt 1):239-48
pubmed: 9023782
J Physiol. 2010 Mar 15;588(Pt 6):905-6
pubmed: 20231147
Front Physiol. 2019 Feb 01;10:32
pubmed: 30774600
Genome Biol. 2019 Jun 4;20(1):118
pubmed: 31164141
Aging (Albany NY). 2020 May 5;12(10):9447-9460
pubmed: 32369778
Clin Sci (Lond). 1991 Aug;81(2):249-56
pubmed: 1716189
J Proteome Res. 2016 Feb 5;15(2):499-509
pubmed: 26732810
Nutrition. 2004 Jul-Aug;20(7-8):716-27
pubmed: 15212756
J Biol Chem. 2006 Feb 10;281(6):3057-66
pubmed: 16314416
J Biol Chem. 2011 Nov 4;286(44):38220-38230
pubmed: 21908619
Bioinformatics. 2016 Sep 15;32(18):2847-9
pubmed: 27207943
J Cell Physiol. 2021 Jan;236(1):260-272
pubmed: 32506638
Dig Dis. 2015;33(3):327-31
pubmed: 26045265
J Physiol. 2017 May 1;595(9):2857-2871
pubmed: 27861911
J Physiol. 2002 Jun 15;541(Pt 3):969-78
pubmed: 12068055
J Physiol. 2004 Aug 1;558(Pt 3):1005-12
pubmed: 15218062
Am J Physiol Endocrinol Metab. 2012 Aug 1;303(3):E308-21
pubmed: 22436696
Proc Soc Exp Biol Med. 1973 Jul;143(3):753-5
pubmed: 4719462
Autophagy. 2015;11(3):538-46
pubmed: 25714469
Cold Spring Harb Symp Quant Biol. 2011;76:325-34
pubmed: 22262476
J Physiol. 2009 Feb 15;587(Pt 4):897-904
pubmed: 19124543
Br J Sports Med. 2020 Dec;54(24):1451-1462
pubmed: 33239350
Front Aging Neurosci. 2020 Dec 16;12:609517
pubmed: 33390929
Essays Biochem. 2012;52:23-35
pubmed: 22708561
J Biol Chem. 2015 Dec 18;290(51):30429-40
pubmed: 26515061
JCI Insight. 2018 Aug 9;3(15):
pubmed: 30089729
Biol Pharm Bull. 2010;33(5):729-37
pubmed: 20460747
Med Sci Sports Exerc. 1987 Oct;19(5 Suppl):S166-71
pubmed: 3316916
Mol Nutr Food Res. 2018 May;62(9):e1701062
pubmed: 29573154
Biochim Biophys Acta. 1982 Dec 17;719(3):495-500
pubmed: 6983891
Pflugers Arch. 2015 Jun;467(6):1343-56
pubmed: 25070178
Proc Natl Acad Sci U S A. 2015 May 26;112(21):6601-6
pubmed: 25964343
J Appl Physiol (1985). 2009 Jun;106(6):2026-39
pubmed: 19164770
CNS Neurosci Ther. 2013 Apr;19(4):252-61
pubmed: 23521913
Annu Rev Gerontol Geriatr. 2016;36(1):205-228
pubmed: 27134329
JIMD Rep. 2019 May 31;48(1):67-74
pubmed: 31392115
J Appl Physiol (1985). 2017 Mar 1;122(3):541-548
pubmed: 27742803
J Biomed Sci. 2012 Oct 12;19:89
pubmed: 23061754
FEBS J. 2016 Jul;283(13):2528-45
pubmed: 27208881
Nutrients. 2019 Sep 30;11(10):
pubmed: 31575008
Cell Mol Life Sci. 2008 Aug;65(16):2461-83
pubmed: 18488143
Curr Opin Clin Nutr Metab Care. 2005 Sep;8(5):534-7
pubmed: 16079625
J Appl Physiol (1985). 2019 Jan 1;126(1):30-43
pubmed: 30335577
Am J Physiol Endocrinol Metab. 2010 May;298(5):E1011-8
pubmed: 20304764
J Appl Physiol (1985). 2019 Aug 1;127(2):581-590
pubmed: 30676865
Front Endocrinol (Lausanne). 2021 Feb 22;11:554922
pubmed: 33692750
Acta Physiol Scand. 1989 Jun;136(2):193-8
pubmed: 2782092
Diabetes Care. 2010 Nov;33(11):2327-32
pubmed: 20724647
J Appl Physiol (1985). 1992 Nov;73(5):1854-9
pubmed: 1474061
J Proteome Res. 2013 Apr 5;12(4):1956-68
pubmed: 23473242

Auteurs

Sebastian Gehlert (S)

Department for Biosciences of Sports, Institute of Sport Science, University of Hildesheim, 31139 Hildesheim, Germany.
Institute of Cardiovascular Research and Sports Medicine, German Sport University, 50933 Cologne, Germany.

Patrick Weinisch (P)

Institute of Computational Biology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany.

Werner Römisch-Margl (W)

Institute of Computational Biology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany.

Richard T Jaspers (RT)

Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Amsterdam Movement Sciences, Vrije Universiteit Amsterdam, 1081 BT Amsterdam, The Netherlands.

Anna Artati (A)

Metabolomics and Proteomics Core, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany.

Jerzy Adamski (J)

Institute of Experimental Genetics, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany.
Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117597, Singapore.
Institute of Biochemistry, Faculty of Medicine, University of Ljubljana, 1000 Ljubljana, Slovenia.

Kenneth A Dyar (KA)

Metabolic Physiology, Institute of Diabetes and Cancer, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany.
German Center for Diabetes Research (DZD), 85764 Neuherberg, Germany.

Thorben Aussieker (T)

Institute of Cardiovascular Research and Sports Medicine, German Sport University, 50933 Cologne, Germany.

Daniel Jacko (D)

Institute of Cardiovascular Research and Sports Medicine, German Sport University, 50933 Cologne, Germany.

Wilhelm Bloch (W)

Institute of Cardiovascular Research and Sports Medicine, German Sport University, 50933 Cologne, Germany.

Henning Wackerhage (H)

Department of Sport and Health Sciences, Technical University of Munich, 80809 Munich, Germany.

Gabi Kastenmüller (G)

Institute of Computational Biology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany.
German Center for Diabetes Research (DZD), 85764 Neuherberg, Germany.

Classifications MeSH