Acute sleep deprivation exacerbates systemic inflammation and psychiatry disorders through gut microbiota dysbiosis and disruption of circadian rhythms

Deng Fa Yang, Wen Ching Huang, Changwei W. Wu, Ching Ying Huang, Yu Chen S.H. Yang, Yu Tang Tung

Research output: Contribution to journalArticlepeer-review

27 Citations (Scopus)

Abstract

Acute sleep deprivation (ASD) is often observed in shift workers and characterized by drowsiness and unrelenting exhaustion. The physiological and psychological effects of ASD include anxiety, depression, cognitive impairment, systemic inflammation, stress responses, and disruptions of gut microbiota. However, the mechanisms involved in the ASD-associated circadian dysregulations with regard to gut dysbiosis, systemic inflammation, physiological modulation, and psychiatry disorders remain unclear. The aim of this study was to investigate whether central nervous system disorders induced by ASD are related to inflammation, barrier dysfunction, and circadian dysregulation. We also assessed impacts on microbiota succession. Male C57BL/6 mice were randomly allocated to the control and sleep deprivation (SD) groups. Mice in the SD group were subjected to 72 h of paradoxical SD using the modified multiple-platform method for ASD induction (72 h rapid eye movement-SD). The effects of ASD on dietary consumption, behaviors, cytokines, microbiota, and functional genes were determined. The appetite of the SD group was significantly higher than that of the control group, but the body weight was significantly lower than that of the control group. The anxiety-like behaviors were found in the SD group. Alpha and beta diversity of microbiota showed significant decrease after ASD induction; the relative abundance of Candidatus_Arthromitus and Enterobacter was increased, whereas that abundance of Lactobacillus, Muribaculum, Monoglobus, Parasutterella, and others was decreased in the SD group. These effects were accompanied by reduction in fecal propionic acid. In the proximal colon, the SD group exhibited significantly higher inflammation (tumor necrosis factor-α [TNF-α]) and dysregulation of the circadian rhythms (brain and muscle ARNT-like 1 [BMAL1] and cryptochrome circadian regulator 1 [CRY1]) and tight junction genes (occludin [OCLN]) than the control group. Gut barrier dysfunction slightly increased the plasma concentration of lipopolysaccharide and significantly elevated TNF-α. Inflammatory signals might be transduced through the brain via TNF receptor superfamily member 1 A (TNFRSF1A), which significantly increased the levels of microglia activation marker (ionized calcium-binding adapter molecule 1 [IBA1]) and chemokine (intercellular adhesion molecule 1 [ICAM1]) in the cerebral cortex. The serotonin receptor (5-hydroxytryptamine 1A receptor [5-HT1AR]) was significantly downregulated in the hippocampus. In summary, 72 h of rapid eye movement-SD induced physiological and psychological stress, which led to disruption of the circadian rhythms and gut microbiota dysbiosis; these effects were related to decrement of short chain fatty acids, gut inflammation, and hyperpermeability. The microbiota may be utilized as preventive and therapeutic strategies for ASD from the perspectives of medicine and nutrition.

Original languageEnglish
Article number127292
JournalMicrobiological Research
Volume268
DOIs
Publication statusPublished - Mar 2023

Keywords

  • Gut microbiota
  • Gut-brain axis
  • Inflammation
  • Psychiatry disorder
  • Sleep deprivation

ASJC Scopus subject areas

  • Microbiology

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