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

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.

Keywords: hormones; muscle; muscle protein synthesis; sleep deprivation.

Figure 1

Experimental Protocol. blood collection; : muscle collection; : standardized meal. IGF‐1, cortisol, and testosterone concentrations were measured at the 07:00, 10:00, 13:00, and 16:00 timepoints. Insulin concentrations were measured at the 07:00, 11:00, and 15:00 timepoints. Phe enrichment (Phe) was measured in both muscle tissue and blood samples between 10:00 and 16:00. PCRs were run on muscle tissue collected at 13:00

Figure 2

Plasma enrichment of L‐[ring‐¹³C₆]‐ phenylalanine in a subset of volunteers during the experimental protocol (N = 4). Data were analyzed using a two‐way ANOVA. Data are presented as mean ± SD (a). Postprandial mixed muscle fractional synthesis rate was measured in the control (CON) and sleep‐deprived (DEP) conditions. Red dots depict male subjects. Blue dots depict female subjects. N = 13. Data were analyzed using a single‐tailed paired t test. * significantly different from the CON condition, p < .05 (b)

Figure 3

Plasma testosterone concentrations in control (CON) and sleep‐deprived (DEP) conditions. N = 13. Data were analyzed using a two‐way ANOVA. Data are presented as mean ± SD (a). Area under the curve calculated for plasma cortisol concentrations. Red dots depict male subjects. Blue dots depict female subjects. N = 13. Data were analyzed using a single‐tailed paired t test *; significantly different from the CON condition, p < .05 (b)

Figure 4

Plasma cortisol concentrations in control (CON) and sleep‐deprived (DEP) conditions. N = 13. Data were analyzed using a two‐way ANOVA. * significantly different from the CON condition, p < .05. ^##; CON group was significantly different from the 07:00 timepoint in the CON group, p < .01. ^###; CON group was significantly different from the 07:00 timepoint in the CON group, p < .001. Data are presented as mean ± SD (a). Area under the curve calculated for plasma cortisol concentrations from 10:00 (dashed line, a) until the end of the protocol. Red dots depict male subjects. Blue dots depict female subjects. N = 13. Data were analyzed using a single‐tailed paired t test *; significantly different from the CON condition, p < .05. (b)

Figure 5

Plasma IGF‐1 concentrations in control (CON) and sleep‐deprived (DEP) conditions. N = 13. Data were analyzed using a two‐way ANOVA (a). Muscle mRNA levels of the IGF‐1 isoforms IGF1‐Ea (b) and IGF1‐Eb (c) in muscle biopsies collected at 13:00. Red dots depict male subjects. Blue dots depict female subjects. N = 13. Data were analyzed using a two‐tailed paired t test. Insulin concentrations in control (CON) and sleep‐deprived (DEP) conditions. N = 13. Data were analyzed using a two‐way ANOVA (d). All data are presented as mean ± SD

Figure 6

Muscle mRNA levels of ARNTL (a), CRY1 (b), PER1 (c), atrogin (FBOX32) (d), MURF1 (e), FOXO1 (f), and FOXO3 (g) in muscle biopsies collected at 13:00. Red dots depict male subjects. Blue dots depict female subjects. N = 13. Data were analyzed using a two‐tailed paired t test. All data are presented as mean ± SD