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Article

Melatonin Ameliorates Neuropsychiatric Behaviors, Gut Microbiome, and Microbiota-Derived Metabolites in Rats with Chronic Sleep Deprivation

by
Bingcong Li
1,†,
Yin-Ru Hsieh
1,†,
Wen-De Lai
1,
Te-Hsuan Tung
1,
Yu-Xuan Chen
1,
Chia-Hui Yang
1,
Yu-Chiao Fang
1 and
Shih-Yi Huang
1,2,3,4,*
1
School of Nutrition and Health Sciences, Taipei Medical University, Taipei 110301, Taiwan
2
Graduate Institute of Metabolism and Obesity Sciences, Taipei Medical University, Taipei 110301, Taiwan
3
Nutrition Research Center, Taipei Medical University Hospital, Taipei 110301, Taiwan
4
TMU Research Center for Digestive Medicine, Taipei Medical University, Taipei 110301, Taiwan
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2023, 24(23), 16820; https://doi.org/10.3390/ijms242316820
Submission received: 9 November 2023 / Revised: 23 November 2023 / Accepted: 24 November 2023 / Published: 27 November 2023
(This article belongs to the Special Issue Depression: From Molecular Basis to Therapy)
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Abstract

With the increasing prevalence of sleep deprivation (SD)-related disorders, the effective treatment of sleep disorders has become a critical health research topic. Thus, we hypothesized and investigated the effectiveness of a 3-week melatonin intervention on neuropsychiatric behavioral responses mediated throughout melatonin receptors, gut microbiota, and lipid metabolites in rats with chronic SD. Eighteen 6-week-old Wistar rats were used and divided into the control grup (C, n = 6), SD group (n = 6), and melatonin-supplemented group (SDM, n = 6). During weeks 0 to 6, animals were provided with the AIN-93M diet and free access to water. Four-week chronic SD was conducted from weeks 7 to 10. Exogenous melatonin administration (10 mg/kg BW) was injected intraperitoneally 1 h before the daily administration of SD for 3 weeks in the SDM group. SD rats exhibited anxiety-like behavior, depression-like behavior, and cognitive impairment. Exogenous melatonin administration ameliorated neuropsychiatric behaviors induced by chronic SD. Analysis of fecal metabolites indicated that melatonin may influence brain messaging through the microbiota–gut–brain axis by increasing the production of short-chain fatty acids (SCFA) and decreasing the production of secondary bile acids (SBA). Four-week SD reduced the cerebral cortex expression of MT1, but not in the colon. Chronic SD led to anxiety and depression-like behaviors and cognitive decline, as well as the reduced intestinal level of SCFAs and the enhanced intestinal level of SBAs in rats. In this work, we confirmed our hypothesis that a 3-week melatonin intervention on neuropsychiatric behavioral response mediated throughout melatonin receptors, gut microbiota, and lipid metabolites in rats with chronic SD.
Keywords: melatonin; sleep deprivation; depression-like behavior; cognitive; intestinal metabolites melatonin; sleep deprivation; depression-like behavior; cognitive; intestinal metabolites
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MDPI and ACS Style

Li, B.; Hsieh, Y.-R.; Lai, W.-D.; Tung, T.-H.; Chen, Y.-X.; Yang, C.-H.; Fang, Y.-C.; Huang, S.-Y. Melatonin Ameliorates Neuropsychiatric Behaviors, Gut Microbiome, and Microbiota-Derived Metabolites in Rats with Chronic Sleep Deprivation. Int. J. Mol. Sci. 2023, 24, 16820. https://doi.org/10.3390/ijms242316820

AMA Style

Li B, Hsieh Y-R, Lai W-D, Tung T-H, Chen Y-X, Yang C-H, Fang Y-C, Huang S-Y. Melatonin Ameliorates Neuropsychiatric Behaviors, Gut Microbiome, and Microbiota-Derived Metabolites in Rats with Chronic Sleep Deprivation. International Journal of Molecular Sciences. 2023; 24(23):16820. https://doi.org/10.3390/ijms242316820

Chicago/Turabian Style

Li, Bingcong, Yin-Ru Hsieh, Wen-De Lai, Te-Hsuan Tung, Yu-Xuan Chen, Chia-Hui Yang, Yu-Chiao Fang, and Shih-Yi Huang. 2023. "Melatonin Ameliorates Neuropsychiatric Behaviors, Gut Microbiome, and Microbiota-Derived Metabolites in Rats with Chronic Sleep Deprivation" International Journal of Molecular Sciences 24, no. 23: 16820. https://doi.org/10.3390/ijms242316820

APA Style

Li, B., Hsieh, Y.-R., Lai, W.-D., Tung, T.-H., Chen, Y.-X., Yang, C.-H., Fang, Y.-C., & Huang, S.-Y. (2023). Melatonin Ameliorates Neuropsychiatric Behaviors, Gut Microbiome, and Microbiota-Derived Metabolites in Rats with Chronic Sleep Deprivation. International Journal of Molecular Sciences, 24(23), 16820. https://doi.org/10.3390/ijms242316820

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