Abstract
Our study demonstrated that sleep deprivation resulted in homeostasis disorder of colon. Our study goes deeper into the positive effects of melatonin on small intestinal microbiota disorder caused by sleep deprivation. We successfully established a multiplatform 72 h sleep deprivation mouse model with or without melatonin supplementation, and analyzed the change of small intestinal microbiota using high-throughput sequencing of the 16S rRNA. We found melatonin supplementation suppressed the decrease of plasma melatonin level in sleep deprivation mice. Meanwhile, melatonin supplementation improved significantly the reduction in OTU numbers and the diversity and richness of jejunal microbiota and the abundance of Bacteroidaeae and Prevotellaceae, as well as an increase in the Firmicutes-to-Bacteroidetes ratio and the content of Moraxellaceae and Aeromonadaceae in the jejunum of sleep deprived-mice. Moreover, melatonin supplementation reversed the change of metabolic pathway in sleep deprived-mice, including metabolism, signal transduction mechanisms and transcription etc, which were related to intestinal health. Furthermore, melatonin supplementation inverted the sleep deprivation-induced a decline of anti-inflammatory cytokines (IL-22) and an increase of the ROS and proinflammatory cytokines (IL-17) in jejunum. These findings suggested that melatonin, similar to a probiotics agent, can reverse sleep deprivation-induced small intestinal microbiota disorder by suppressing oxidative stress and inflammation response.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bäckhed, F., Ding, H., Wang, T., Hooper, L.V., Koh, G. Y., Nagy, A., Semenkovich, C.F., and Gordon, J.I. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA101, 15718–15723.
Bäckhed, F., Manchester, J.K., Semenkovich, C.F., and Gordon, J.I. 2007. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl. Acad. Sci. USA104, 979–984.
Bao, Y.M., Choct, M., Iji, P., and Bruerton, K. 2010. Trace mineral interactions in broiler chicken diets. Br. Poult. Sci.51, 109–117.
Boonstra, R. 2005 Equipped for life: the adaptive role of the stress axis in male mammals. J. Mammal.86, 236–247.
Brownlee, I.A., Knight, J., Dettmar, P.W., and Pearson, J.P. 2007. Action of reactive oxygen species on colonic mucus secretions. Free Radic. Biol. Med.43, 800–808.
Brzozowski, T. and Jaworek, J. 2014. Basic and clinical aspects of melatonin in the gastrointestinal tract. New advancements and future perspectives. Curr. Pharm. Des.20, 4785–4787.
Deitch, E.A., Xu, D., Naruhn, M.B., Deitch, D.C., Lu, Q., and Marino, A.A. 1995. Elemental diet and IV-TPN-induced bacterial translocation is associated with loss of intestinal mucosal barrier function against bacteria. Ann. Surg.221, 299–307.
Fernández-Gil, B., Moneim, A.E., Ortiz, F., Shen, Y.Q., Soto-Mercado, V., Mendivil-Perez, M., Guerra-Librero, A., Acuña-Castroviejo, D., Molina-Navarro, M.M., García-Verdugo, J.M., et al. 2017. Melatonin protects rats from radiotherapy-induced small intestine toxicity. PLoS One12, e0174474.
Frank, D.N., Robertson, C.E., Hamm, C.M., Kpadeh, Z., Zhang, T., Chen, H., Zhu, W., Sartor, R.B., Boedeker, E.C., Harpaz, N., et al. 2011. Disease phenotype and genotype are associated with shifts in intestinal associated microbiota in inflammatory bowel diseases. Inflamm. Bowel Dis.17, 179–184.
Glaser, R. and Kiecolt-Glaser, J.K. 2005. Stress-induced immune dysfunction: implications for health. Nat. Rev. Immunol.5, 243–251.
Gori, A., Tincati, C., Rizzardini, G., Torti, C., Quirino, T., Haarman, M., Ben Amor, K., van Schaik, J., Vriesema, A., Knol, J., et al. 2008. Early impairment of gut function and gut flora supporting a role for alteration of gastrointestinal mucosa in human immunodeficiency virus pathogenesis. J. Clin. Microbiol.46, 757–758.
Grivennikov, S.I., Greten, F.R., and Karin, M. 2010. Immunity, inflammation, and cancer. Cell140, 883–899.
Hildebrandt, M.A., Hoffmann, C., Sherrill-Mix, S.A., Keilbaugh, S.A., Hamady, M., Chen, Y.Y., Knight, R., Ahima, R.S., Bushman, F., and Wu, G.D. 2009. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterolgy137, 1716–1724.e1-2.
Larsen, N., Vogensen, F.K., van den Berg, F.W.J., Nielsen, D.S., Andreasen, A.S., Pedersen, B.K., Al-Soud, W.A., Sørensen, S.J., Hansen, L.H., and Jakobsen, M. 2010. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One5, e9085.
Mazzon, E., Esposito, E., Crisafulli, C., Riccardi, L., Muià, C., Di Bella, P., Meli, R., and Cuzzocrea, S. 2006. Melatonin modulates signal transduction pathways and apoptosis in experimental colitis. J. Pineal Res.41, 363–373.
Mirpuri, J., Raetz, M., Sturge, C., Wilhelm, C.L., Benson, A., Savani, R.C., Hooper, L.V., and Yarovinsky, F. 2014. Proteobacteriaspecific IgA regulates maturation of the intestinal microbiota. Gut Microbes5, 28–39.
Necefli, A., Tulumoğlu, B., Giriş, M., Barbaros, U., Gündüz, M., Olgaç, V., Güloğlu, R., and Toker, G. 2006. The effect of melatonin on TNBS-induced colitis. Dig. Dis. Sci.51, 1538–1545.
Paulose, J.K., Wright, J.M., Patel, A.G., and Cassone, V.M. 2016. Human gut bacteria are sensitive to melatonin and express endogenous circadian rhythmicity. PLoS One11, e0146643.
Rajaratnam, S.M. and Arendt, J. 2001. Health in a 24-h society. Lancet358, 999–1005.
Randall-Demllo, S., Chieppa, M., and Eri, R. 2013. Intestinal epithelium and autophagy: partners in gut homeostasis. Front. Immunol.4, 301.
Raoult, D. and Henrissat, B. 2014. Are stool samples suitable for studying the link between gut microbiota and obesity? Eur. J. Epidemiol.29, 307–309.
Rezaie, A., Parker, R.D., and Abdollahi, M. 2007. Oxidative stress and pathogenesis of inflammatory bowel disease: an epiphenomenon or the cause? Dig. Dis. Sci.52, 2015–2021.
Sreevalsan, S. and Safe, S. 2013. Reactive oxygen species and colorectal cancer. Curr. Colorectal Cancer Rep.9, 350–357.
Uni, Z., Platin, R., and Sklan, D. 1998. Cell proliferation in chicken intestinal epithelium occurs both in the crypt and along the villus. J. Comp. Physiol. B168, 241–247.
Wang, Y., Jiang, L., He, J., Hu, M., Zeng, F., Li, Y., Tian, H., and Luo, X. 2018. The adverse effects of Se toxicity on inflammatory and immune responses in chicken spleens. Biol. Trace Elem. Res.185, 170–176.
Wrzosek, L., Miquel, S., Noordine, M.L., Bouet, S., Joncquel Chevalier-Curt, M., Robert, V., Philippe, C., Bridonneau, C., Cherbuy, C., Robbe-Masselot, C., et al. 2013. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol.11, 61.
Xie, Z., Chen, F., Li, W.A., Geng, X., Li, C., Meng, X., Feng, Y., Liu, W., and Yu, F. 2017. A review of sleep disorders and melatonin. Neurol. Res.39, 559–565.
Xu, P., Wang, J., Hong, F., Wang, S., Jin, X., Xue, T., Jia, L., and Zhai, Y. 2017. Melatonin prevents obesity through modulation of gut microbiota in mice. J. Pineal Res.62, e12399.
Zhang, S.L., Bai, L., Goel, N., Bailey, A., Jang, C.J., Bushman, F.D., Meerlo, P., Dinges, D.F., and Sehgal, A. 2017. Human and rat gut microbiome composition is maintained following sleep restriction. Proc. Natl. Acad. Sci. USA114, E1564–E1571.
Zhang, M., Liu, B., Zhang, Y., Wei, H., Lei, Y., and Zhao, L. 2007. Structural shifts of mucosa-associated lactobacilli and Clostridium leptum subgroup in patients with ulcerative colitis. J. Clin. Microbiol.45, 496–500.
Acknowledgments
This study was supported partially by Chinese National Natural Science Foundation (31873000 and 31672501) and the Beijing Natural Science Foundation (6182018).
Author information
Authors and Affiliations
Contributions
Y.C. and T.G. contributed to the study design; Y.C. obtained funding; T.G. performed the experiments; T.G., Z.W., J.C., and Y.D. analyzed the data; T.G. and Y.C. wrote the manuscript. All authors reviewed the final manuscript.
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest.
Additional information
Supplemental material for this article may be found at http://www.springerlink.com/content/120956
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Gao, T., Wang, Z., Cao, J. et al. Melatonin attenuates microbiota dysbiosis of jejunum in short-term sleep deprived mice. J Microbiol. 58, 588–597 (2020). https://doi.org/10.1007/s12275-020-0094-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12275-020-0094-4