Exercise training modifies skeletal muscle clock gene expression but not 24-hour rhythmicity in substrate metabolism of men with insulin resistance

被引:8
作者
Harmsen, Jan-Frieder [1 ]
Kotte, Marit [1 ]
Habets, Ivo [1 ]
Bosschee, Frederieke [1 ]
Frenken, Koen [1 ]
Jorgensen, Johanna A. [1 ]
de Kam, Soraya [1 ]
Moonen-Kornips, Esther [1 ]
Cissen, Jochem [1 ]
Doligkeit, Daniel [1 ]
van de Weijer, Tineke [1 ]
Erazo-Tapia, Edmundo [1 ]
Buitinga, Mijke [1 ]
Hoeks, Joris [1 ]
Schrauwen, Patrick [1 ,2 ]
机构
[1] Maastricht Univ, Med Ctr, NUTRIM Sch Nutr & Translat Res Metab, Dept Nutr & Movement Sci, Maastricht, Netherlands
[2] Maastricht Univ, Med Ctr, Dept Nutr & Movement Sci, POB 616, NL-6200MD Maastricht, Netherlands
来源
JOURNAL OF PHYSIOLOGY-LONDON | 2024年 / 602卷 / 23期
关键词
circadian rhythm; exercise; insulin resistance; mitochondria; CIRCADIAN CLOCK; MITOCHONDRIAL RESPIRATION; GLUCOSE-METABOLISM; INTENSITY EXERCISE; CARBOHYDRATE; SENSITIVITY; DYSFUNCTION; PHYSIOLOGY; GLYCOGEN; BALANCE;
D O I
10.1113/JP285523
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Twenty-four hour rhythmicity in whole-body substrate metabolism, skeletal muscle clock gene expression and mitochondrial respiration is compromised upon insulin resistance. With exercise training known to ameliorate insulin resistance, our objective was to test if exercise training can reinforce diurnal variation in whole-body and skeletal muscle metabolism in men with insulin resistance. In a single-arm longitudinal design, 10 overweight and obese men with insulin resistance performed 12 weeks of high-intensity interval training recurrently in the afternoon (between 14.00 and 18.00 h) and were tested pre- and post-exercise training, while staying in a metabolic research unit for 2 days under free-living conditions with regular meals. On the second days, indirect calorimetry was performed at 08.00, 13.00, 18.00, 23.00 and 04.00 h, muscle biopsies were taken from the vastus lateralis at 08.30, 13.30 and 23.30 h, and blood was drawn at least bi-hourly over 24 h. Participants did not lose body weight over 12 weeks, but improved body composition and exercise capacity. Exercise training resulted in reduced 24-h plasma glucose levels, but did not modify free fatty acid and triacylglycerol levels. Diurnal variation of muscle clock gene expression was modified by exercise training with period genes showing an interaction (time x exercise) effect and reduced mRNA levels at 13.00 h. Exercise training increased mitochondrial respiration without inducing diurnal variation. Twenty-four-hour substrate metabolism and energy expenditure remained unchanged. Future studies should investigate alternative exercise strategies or types of interventions (e.g. diet or drugs aiming at improving insulin sensitivity) for their capacity to reinforce diurnal variation in substrate metabolism and mitochondrial respiration.
引用
收藏
页码:6417 / 6433
页数:17
相关论文
共 66 条
[1]   Clock proteins and training modify exercise capacity in a daytime-dependent manner [J].
Adamovich, Yaarit ;
Dandavate, Vaishnavi ;
Ezagouri, Saar ;
Manella, Gal ;
Zwighaft, Ziv ;
Sobel, Jonathan ;
Kuperman, Yael ;
Golik, Marina ;
Auerbach, Asher ;
Itkin, Maxim ;
Malitsky, Sergey ;
Asher, Gad .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2021, 118 (35)
[2]   Three weeks of time-restricted eating improves glucose homeostasis in adults with type 2 diabetes but does not improve insulin sensitivity: a randomised crossover trial [J].
Andriessen, Charlotte ;
Fealy, Ciaran E. ;
Veelen, Anna ;
van Beek, Sten M. M. ;
Roumans, Kay H. M. ;
Connell, Niels J. ;
Mevenkamp, Julian ;
Moonen-Kornips, Esther ;
Havekes, Bas ;
Schrauwen-Hinderling, Vera B. ;
Hoeks, Joris ;
Schrauwen, Patrick .
DIABETOLOGIA, 2022, 65 (10) :1710-1720
[3]   Classification and Diagnosis of Diabetes [J].
不详 .
DIABETES CARE, 2015, 38 :S8-S16
[4]   Circadian topology of metabolism [J].
Bass, Joseph .
NATURE, 2012, 491 (7424) :348-356
[5]   DIET MUSCLE GLYCOGEN AND PHYSICAL PERFORMANCE [J].
BERGSTROM, J ;
HERMANSEN, L ;
HULTMAN, E ;
SALTIN, B .
ACTA PHYSIOLOGICA SCANDINAVICA, 1967, 71 (2-3) :140-+
[6]  
BROUWER E, 1957, ACTA PHYSIOL PHARM N, V6, P795
[7]   Exercise alters the circadian rhythm of REV-ERB-α and downregulates autophagy-related genes in peripheral and central tissues [J].
da Rocha, Alisson L. ;
Pinto, Ana P. ;
Bedo, Bruno L. S. ;
Morais, Gustavo P. ;
Oliveira, Luciana C. ;
Carolino, Ruither O. G. ;
Pauli, Jose R. ;
Simabuco, Fernando M. ;
de Moura, Leandro P. ;
Ropelle, Eduardo R. ;
Cintra, Dennys E. ;
Rivas, Donato A. ;
da Silva, Adelino S. R. .
SCIENTIFIC REPORTS, 2022, 12 (01)
[8]   The nuclear receptor REV-ERBα is required for the daily balance of carbohydrate and lipid metabolism [J].
Delezie, Julien ;
Dumont, Stephanie ;
Dardente, Hugues ;
Oudart, Hugues ;
Grechez-Cassiau, Aline ;
Klosen, Paul ;
Teboul, Michele ;
Delaunay, Franck ;
Pevet, Paul ;
Challet, Etienne .
FASEB JOURNAL, 2012, 26 (08) :3321-3335
[9]   Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock [J].
Dyar, Kenneth A. ;
Ciciliot, Stefano ;
Wright, Lauren E. ;
Bienso, Rasmus S. ;
Tagliazucchi, Guidantonio M. ;
Patel, Vishal R. ;
Forcato, Mattia ;
Paz, Marcia I. P. ;
Gudiksen, Anders ;
Solagna, Francesca ;
Albiero, Mattia ;
Moretti, Irene ;
Eckel-Mahan, Kristin L. ;
Baldi, Pierre ;
Sassone-Corsi, Paolo ;
Rizzuto, Rosario ;
Bicciato, Silvio ;
Pilegaard, Henriette ;
Blaauw, Bert ;
Schiaffino, Stefano .
MOLECULAR METABOLISM, 2014, 3 (01) :29-41
[10]   METABOLISM AND THE CIRCADIAN CLOCK CONVERGE [J].
Eckel-Mahan, Kristin ;
Sassone-Corsi, Paolo .
PHYSIOLOGICAL REVIEWS, 2013, 93 (01) :107-135