Demonstration of a day-night rhythm in human skeletal muscle oxidative capacity

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Abstract

Objective

A disturbed day-night rhythm is associated with metabolic perturbations that can lead to obesity and type 2 diabetes mellitus (T2DM). In skeletal muscle, a reduced oxidative capacity is also associated with the development of T2DM. However, whether oxidative capacity in skeletal muscle displays a day-night rhythm in humans has so far not been investigated.

Methods

Lean, healthy subjects were enrolled in a standardized living protocol with regular meals, physical activity and sleep to reflect our everyday lifestyle. Mitochondrial oxidative capacity was examined in skeletal muscle biopsies taken at five time points within a 24-hour period.

Results

Core-body temperature was lower during the early night, confirming a normal day-night rhythm. Skeletal muscle oxidative capacity demonstrated a robust day-night rhythm, with a significant time effect in ADP-stimulated respiration (state 3 MO, state 3 MOG and state 3 MOGS, p < 0.05). Respiration was lowest at 1 PM and highest at 11 PM (state 3 MOGS: 80.6 ± 4.0 vs. 95.8 ± 4.7 pmol/mg/s). Interestingly, the fluctuation in mitochondrial function was also observed in whole-body energy expenditure, with peak energy expenditure at 11 PM and lowest energy expenditure at 4 AM (p < 0.001). In addition, we demonstrate rhythmicity in mRNA expression of molecular clock genes in human skeletal muscle.

Conclusions

Our results suggest that the biological clock drives robust rhythms in human skeletal muscle oxidative metabolism. It is tempting to speculate that disruption of these rhythms contribute to the deterioration of metabolic health associated with circadian misalignment.

Graphical abstract

Highlights

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Mitochondrial oxidative capacity in human skeletal muscle follows a day-night rhythm.
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Oxidative capacity peaks in the late evening and is lowest in the early afternoon.
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Energy expenditure follows a day-night rhythm and is highest in the late evening.
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Human muscle exhibits rhythmic gene expression, with a cycling core molecular clock.

Related collections

Most cited references 28

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Studies of body weight regulation have focused almost entirely on caloric intake and energy expenditure. However, a number of recent studies in animals linking energy regulation and the circadian clock at the molecular, physiological, and behavioral levels raise the possibility that the timing of food intake itself may play a significant role in weight gain. The present study focused on the role of the circadian phase of food consumption in weight gain. We provide evidence that nocturnal mice fed a high-fat diet only during the 12-h light phase gain significantly more weight than mice fed only during the 12-h dark phase. A better understanding of the role of the circadian system for weight gain could have important implications for developing new therapeutic strategies for combating the obesity epidemic facing the human population today.

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Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27,485 people.

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To explore how metabolic risk factors for cardiovascular disease (CVD) differ between shift workers and day workers in a defined population. Shift work has been associated with an increased risk of CVD. Risk factors and causal pathways for this association are only partly known. A working population of 27,485 people from the Västerbotten intervention program (VIP) has been analysed. Cross sectional data, including blood sampling and questionnaires were collected in a health survey. Obesity was more prevalent among shift workers in all age strata of women, but only in two out of four age groups in men. Increased triglycerides (>1.7 mmol/l) were more common among two age groups of shift working women but not among men. Low concentrations of high density lipoprotein (HDL) cholesterol (men<0.9 and women<1.0 mmol/l) were present in the youngest age group of shift workers in both men and women. Impaired glucose tolerance was more often found among 60 year old women shift workers. Obesity and high triglycerides persisted as risk factors in shift working men and women after adjusting for age and socioeconomic factors, with an OR of 1.4 for obesity and 1.1 for high triglyceride concentrations. The relative risks for women working shifts versus days with one, two, and three metabolic variables were 1.06, 1.20, and 1.71, respectively. The corresponding relative risks for men were 0.99, 1.30, and 1.63, respectively. In this study, obesity, high triglycerides, and low concentrations of HDL cholesterol seem to cluster together more often in shift workers than in day workers, which might indicate an association between shift work and the metabolic syndrome.

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Circadian Misalignment Augments Markers of Insulin Resistance and Inflammation, Independently of Sleep Loss

Rachel Leproult, Ulf Holmbäck, Eve Van Cauter (2014)

Shift workers, who are exposed to irregular sleep schedules resulting in sleep deprivation and misalignment of circadian rhythms, have an increased risk of diabetes relative to day workers. In healthy adults, sleep restriction without circadian misalignment promotes insulin resistance. To determine whether the misalignment of circadian rhythms that typically occurs in shift work involves intrinsic adverse metabolic effects independently of sleep loss, a parallel group design was used to study 26 healthy adults. Both interventions involved 3 inpatient days with 10-h bedtimes, followed by 8 inpatient days of sleep restriction to 5 h with fixed nocturnal bedtimes (circadian alignment) or with bedtimes delayed by 8.5 h on 4 of the 8 days (circadian misalignment). Daily total sleep time (SD) during the intervention was nearly identical in the aligned and misaligned conditions (4 h 48 min [5 min] vs. 4 h 45 min [6 min]). In both groups, insulin sensitivity (SI) significantly decreased after sleep restriction, without a compensatory increase in insulin secretion, and inflammation increased. In male participants exposed to circadian misalignment, the reduction in SI and the increase in inflammation both doubled compared with those who maintained regular nocturnal bedtimes. Circadian misalignment that occurs in shift work may increase diabetes risk and inflammation, independently of sleep loss.

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Author and article information

Contributors

Patrick Schrauwen

Journal

Journal ID (nlm-ta): Mol Metab

Journal ID (iso-abbrev): Mol Metab

Title: Molecular Metabolism

Publisher: Elsevier

ISSN (Electronic): 2212-8778

Publication date PMC-release: 01 July 2016

Publication date Collection: August 2016

Publication date (Electronic): 01 July 2016

Volume: 5

Issue: 8

Pages: 635-645

Affiliations

[1 ]Department of Human Biology and Human Movement Sciences, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, PO Box 616, 6200 MD Maastricht, The Netherlands

[2 ]Department of Internal Medicine, Division of Endocrinology, Maastricht University Medical Center, PO Box 5800, 6202 AZ Maastricht, The Netherlands

[3 ]Medical Chronobiology Program, Division of Sleep and Circadian Disorders, Brigham and Women's Hospital, Boston, MA 02115, USA

[4 ]Division of Sleep Medicine, Harvard Medical School, Boston, MA 02115, USA

[5 ]Department of Radiology, Maastricht University Medical Center, PO Box 5800, 6202 AZ Maastricht, The Netherlands

[6 ]Univ Lille, Inserm, Institut Pasteur de Lille, UMR1011-EGID, BP245, 59019 Lille, France

[7 ]CAPHRI School for Public Health and Primary Care, Maastricht University Medical Center, Maastricht, The Netherlands

Author notes

[∗ ]Corresponding author. Department of Human Biology and Human Movement Sciences, Maastricht University Medical Center, PO Box 616, 6200 MD Maastricht, The Netherlands. Tel.: +31 43 3881502.Department of Human Biology and Human Movement SciencesMaastricht University Medical CenterPO Box 616Maastricht6200 MDThe Netherlands p.schrauwen@ 123456maastrichtuniversity.nl

[8]

Dirk van Moorsel and Jan Hansen contributed equally to this work.

Article

Publisher ID: S2212-8778(16)30075-8

DOI: 10.1016/j.molmet.2016.06.012

PMC ID: 5021670

PubMed ID: 27656401

SO-VID: 4759cccf-851d-4438-82c4-11ba8c697de9

License:

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

History

Date received : 6 June 2016

Date revision received : 23 June 2016

Date accepted : 26 June 2016

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