The effect of acute sleep deprivation on skeletal muscle protein synthesis and the hormonal environment.

Séverine Lamon,Emily Arentson‐Lantz,Brad Aisbett,Douglas Paddon‐Jones,Aimee Morabito,Dominique Condo,Grace Elizabeth Vincent,Olivia Knowles,Andrew Garnham,Sarah Elizabeth Alexander

doi:10.14814/phy2.14660

Abstract

Chronic sleep loss is a potent catabolic stressor, increasing the risk of metabolic dysfunction and loss of muscle mass and function. To provide mechanistic insight into these clinical outcomes, we sought to determine if acute sleep deprivation blunts skeletal muscle protein synthesis and promotes a catabolic environment. Healthy young adults (N = 13; seven male, six female) were subjected to one night of total sleep deprivation (DEP) and normal sleep (CON) in a randomized cross‐over design. Anabolic and catabolic hormonal profiles were assessed across the following day. Postprandial muscle protein fractional synthesis rate (FSR) was assessed between 13:00 and 15:00 and gene markers of muscle protein degradation were assessed at 13:00. Acute sleep deprivation reduced muscle protein synthesis by 18% (CON: 0.072 ± 0.015% vs. DEP: 0.059 ± 0.014%·h‐1, p = .040). In addition, sleep deprivation increased plasma cortisol by 21% (p = .030) and decreased plasma testosterone by 24% (p = .029). No difference was found in the markers of protein degradation. A single night of total sleep deprivation is sufficient to induce anabolic resistance and a procatabolic environment. These acute changes may represent mechanistic precursors driving the metabolic dysfunction and body composition changes associated with chronic sleep deprivation.

Highlights

Acute and chronic sleep loss are linked with a range of negative physiological and psychological outcomes (Kecklund & Axelsson, 2016)
Chronic sleep loss is a potent catabolic stressor (Cedernaes et al, 2018; Saner et al, 2020) that increases the risk of metabolic dysfunction (Reutrakul & Van Cauter, 2018) and is associated with a loss of muscle mass and function at the population level (Lucassen et al, 2017; Piovezan et al, 2015)
We have demonstrated that a single night of sleep deprivation is sufficient to induce anabolic resistance, TABLE 3 Muscle L-[ring-13C6]- phenylalanine intracellular enrichments in muscle biopsy samples in the control trial (CON) or DEP conditions

Summary

| INTRODUCTION

Acute and chronic sleep loss are linked with a range of negative physiological and psychological outcomes (Kecklund & Axelsson, 2016). Sleep deprivation negatively impacted the pathways regulating protein synthesis and increased muscle proteolytic activity (de Sa et al, 2016) These findings were paralleled by a human study reporting a catabolic gene signature in skeletal muscle following one night of total sleep deprivation in healthy young males (Cedernaes et al, 2018). Experimental evidence suggests that acute and chronic sleep loss alter anabolic (Leproult & Van Cauter, 2011; Reynolds et al, 2012) and catabolic (Cedernaes et al, 2018; Dáttilo et al, 2020) hormone secretion patterns in humans On this basis, we hypothesized that one night of sleep deprivation would decrease muscle protein synthesis and that the hormonal environment may provide a possible mechanism for impaired muscle protein metabolism. We sought to determine if one night of complete sleep deprivation promotes a catabolic hormonal environment and compromises postprandial muscle protein synthesis and markers of muscle protein degradation in young, healthy male and female participants

| Participants

| Prestudy procedure

| RESULTS

| DISCUSSION

Findings

| Strengths and limitations