Day-night rhythm of skeletal muscle metabolism is disturbed in older, metabolically compromised individuals.


Journal

Molecular metabolism
ISSN: 2212-8778
Titre abrégé: Mol Metab
Pays: Germany
ID NLM: 101605730

Informations de publication

Date de publication:
11 2020
Historique:
received: 16 04 2020
revised: 21 06 2020
accepted: 06 07 2020
pubmed: 14 7 2020
medline: 17 8 2021
entrez: 14 7 2020
Statut: ppublish

Résumé

Skeletal muscle mitochondrial function and energy metabolism displays day-night rhythmicity in healthy, young individuals. Twenty-four-hour rhythmicity of metabolism has been implicated in the etiology of age-related metabolic disorders. Whether day-night rhythmicity in skeletal muscle mitochondrial function and energy metabolism is altered in older, metabolically comprised humans remains unknown. Twelve male overweight volunteers with impaired glucose tolerance and insulin sensitivity stayed in a metabolic research unit for 2 days under free living conditions with regular meals. Indirect calorimetry was performed at 5 time points (8 AM, 1 PM, 6 PM, 11 PM, 4 AM), followed by a muscle biopsy. Mitochondrial oxidative capacity was measured in permeabilized muscle fibers using high-resolution respirometry. Mitochondrial oxidative capacity did not display rhythmicity. The expression of circadian core clock genes BMAL1 and REV-ERBα showed a clear day-night rhythm (p < 0.001), peaking at the end of the waking period. Remarkably, the repressor clock gene PER2 did not show rhythmicity, whereas PER1 and PER3 were strongly rhythmic (p < 0.001). On the whole-body level, resting energy expenditure was highest in the late evening (p < 0.001). Respiratory exchange ratio did not decrease during the night, indicating metabolic inflexibility. Mitochondrial oxidative capacity does not show a day-night rhythm in older, overweight participants with impaired glucose tolerance and insulin sensitivity. In addition, gene expression of PER2 in skeletal muscle indicates that rhythmicity of the negative feedback loop of the molecular clock is disturbed. CLINICALTRIALS. NCT03733743.

Identifiants

pubmed: 32659272
pii: S2212-8778(20)30124-1
doi: 10.1016/j.molmet.2020.101050
pmc: PMC7415921
pii:
doi:

Substances chimiques

ARNTL Transcription Factors 0
BMAL1 protein, human 0
NR1D1 protein, human 0
Nuclear Receptor Subfamily 1, Group D, Member 1 0
Period Circadian Proteins 0
CLOCK Proteins EC 2.3.1.48

Banques de données

ClinicalTrials.gov
['NCT03733743']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

101050

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier GmbH.. All rights reserved.

Références

Genes Dev. 2018 Nov 1;32(21-22):1367-1379
pubmed: 30366905
Diabetes. 2002 Oct;51(10):2944-50
pubmed: 12351431
Proc Natl Acad Sci U S A. 2016 Mar 22;113(12):E1673-82
pubmed: 26862173
Diabetes. 2008 Nov;57(11):2943-9
pubmed: 18678616
Proc Natl Acad Sci U S A. 2018 Jun 5;115(23):E5390-E5399
pubmed: 29784788
Cell Metab. 2015 Oct 6;22(4):709-20
pubmed: 26365180
J Clin Invest. 1979 Jun;63(6):1274-83
pubmed: 221538
Sci Rep. 2016 Oct 19;6:35047
pubmed: 27756900
Science. 2003 May 16;300(5622):1140-2
pubmed: 12750520
Mol Metab. 2016 Jul 01;5(8):635-645
pubmed: 27656401
Am J Physiol Endocrinol Metab. 2010 Nov;299(5):E794-801
pubmed: 20739506
Mol Metab. 2018 Jun;12:39-47
pubmed: 29706321
Diabetes Care. 2017 Jan;40(Suppl 1):S11-S24
pubmed: 27979889
Obesity (Silver Spring). 2008 May;16(5):1025-32
pubmed: 18309299
Scand J Clin Lab Invest. 1975 Nov;35(7):609-16
pubmed: 1108172
Chronobiol Int. 2012 Aug;29(7):868-81
pubmed: 22823870
Elife. 2018 Apr 16;7:
pubmed: 29658882
Genome Biol. 2007;8(2):R19
pubmed: 17291332
Am J Physiol. 1999 Dec;277(6):E1130-41
pubmed: 10600804
Proc Natl Acad Sci U S A. 2014 Dec 2;111(48):17302-7
pubmed: 25404342
Clin Sci (Lond). 2016 Jun 1;130(11):843-52
pubmed: 27129097
Diabetologia. 2019 Apr;62(4):704-716
pubmed: 30737520
Curr Opin Genet Dev. 2017 Apr;43:120-127
pubmed: 28363112
Cell Metab. 2017 May 2;25(5):1027-1036
pubmed: 28467922
Proc Natl Acad Sci U S A. 2018 Jul 24;115(30):7789-7794
pubmed: 29987027
Proc Natl Acad Sci U S A. 2014 Feb 11;111(6):E682-91
pubmed: 24449876
J Biol Rhythms. 2002 Apr;17(2):181-93
pubmed: 12002165
J Physiol. 1949 Aug;109(1-2):1-9
pubmed: 15394301
Diabetes. 2005 Jan;54(1):8-14
pubmed: 15616005
Proc Natl Acad Sci U S A. 1918 Dec;4(12):370-3
pubmed: 16576330
J Biol Rhythms. 2010 Oct;25(5):372-80
pubmed: 20876817
Nat Med. 2013 Aug;19(8):1039-46
pubmed: 23852339
Diabetologia. 2002 Sep;45(9):1201-10
pubmed: 12242452
Diabetes Care. 2001 Mar;24(3):539-48
pubmed: 11289482
Proc Natl Acad Sci U S A. 2015 Apr 28;112(17):E2225-34
pubmed: 25870289
J Clin Endocrinol Metab. 2011 Jul;96(7):2032-4
pubmed: 21734004
Diabetes. 2010 Sep;59(9):2117-25
pubmed: 20573749
J Appl Physiol (1985). 1997 Dec;83(6):2064-72
pubmed: 9390982
Anal Biochem. 2014 Dec 15;467:1-3
pubmed: 25193447
Br Med J. 1969 May 10;2(5653):341-4
pubmed: 5768458
Diabetes Care. 2018 Apr;41(4):762-769
pubmed: 29440150

Auteurs

Jakob Wefers (J)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Niels J Connell (NJ)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Ciarán E Fealy (CE)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Charlotte Andriessen (C)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Vera de Wit (V)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Dirk van Moorsel (D)

Division of Endocrinology, Department of Internal Medicine, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Esther Moonen-Kornips (E)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Johanna A Jörgensen (JA)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Matthijs K C Hesselink (MKC)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Bas Havekes (B)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands; Division of Endocrinology, Department of Internal Medicine, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Joris Hoeks (J)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands.

Patrick Schrauwen (P)

Department of Nutrition and Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, 6200 MD Maastricht, the Netherlands. Electronic address: p.schrauwen@maastrichtuniversity.nl.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH