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      Gut microbiota depletion by chronic antibiotic treatment alters the sleep/wake architecture and sleep EEG power spectra in mice

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          Abstract

          Dysbiosis of the gut microbiota affects physiological processes, including brain functions, by altering the intestinal metabolism. Here we examined the effects of the gut microbiota on sleep/wake regulation. C57BL/6 male mice were treated with broad-spectrum antibiotics for 4 weeks to deplete their gut microbiota. Metabolome profiling of cecal contents in antibiotic-induced microbiota-depleted (AIMD) and control mice showed significant variations in the metabolism of amino acids and vitamins related to neurotransmission, including depletion of serotonin and vitamin B6, in the AIMD mice. Sleep analysis based on electroencephalogram and electromyogram recordings revealed that AIMD mice spent significantly less time in non-rapid eye movement sleep (NREMS) during the light phase while spending more time in NREMS and rapid eye movement sleep (REMS) during the dark phase. The number of REMS episodes seen in AIMD mice increased during both light and dark phases, and this was accompanied by frequent transitions from NREMS to REMS. In addition, the theta power density during REMS was lower in AIMD mice during the light phase compared with that in the controls. Consequently, the gut microbiota is suggested to affect the sleep/wake architecture by altering the intestinal balance of neurotransmitters.

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          Most cited references 45

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          The gut microbiota as an environmental factor that regulates fat storage.

          New therapeutic targets for noncognitive reductions in energy intake, absorption, or storage are crucial given the worldwide epidemic of obesity. The gut microbial community (microbiota) is essential for processing dietary polysaccharides. We found that conventionalization of adult germ-free (GF) C57BL/6 mice with a normal microbiota harvested from the distal intestine (cecum) of conventionally raised animals produces a 60% increase in body fat content and insulin resistance within 14 days despite reduced food intake. Studies of GF and conventionalized mice revealed that the microbiota promotes absorption of monosaccharides from the gut lumen, with resulting induction of de novo hepatic lipogenesis. Fasting-induced adipocyte factor (Fiaf), a member of the angiopoietin-like family of proteins, is selectively suppressed in the intestinal epithelium of normal mice by conventionalization. Analysis of GF and conventionalized, normal and Fiaf knockout mice established that Fiaf is a circulating lipoprotein lipase inhibitor and that its suppression is essential for the microbiota-induced deposition of triglycerides in adipocytes. Studies of Rag1-/- animals indicate that these host responses do not require mature lymphocytes. Our findings suggest that the gut microbiota is an important environmental factor that affects energy harvest from the diet and energy storage in the host. Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AY 667702--AY 668946).
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            KEGG for linking genomes to life and the environment

            KEGG (http://www.genome.jp/kegg/) is a database of biological systems that integrates genomic, chemical and systemic functional information. KEGG provides a reference knowledge base for linking genomes to life through the process of PATHWAY mapping, which is to map, for example, a genomic or transcriptomic content of genes to KEGG reference pathways to infer systemic behaviors of the cell or the organism. In addition, KEGG provides a reference knowledge base for linking genomes to the environment, such as for the analysis of drug-target relationships, through the process of BRITE mapping. KEGG BRITE is an ontology database representing functional hierarchies of various biological objects, including molecules, cells, organisms, diseases and drugs, as well as relationships among them. KEGG PATHWAY is now supplemented with a new global map of metabolic pathways, which is essentially a combined map of about 120 existing pathway maps. In addition, smaller pathway modules are defined and stored in KEGG MODULE that also contains other functional units and complexes. The KEGG resource is being expanded to suit the needs for practical applications. KEGG DRUG contains all approved drugs in the US and Japan, and KEGG DISEASE is a new database linking disease genes, pathways, drugs and diagnostic markers.
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              Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease

              The gut microbiota is a crucial actor in human physiology. Many of these effects are mediated by metabolites that are either produced by the microbes or derived from the transformation of environmental or host molecules. Among the array of metabolites at the interface between these microorganisms and the host is the essential aromatic amino acid tryptophan (Trp). In the gut, the three major Trp metabolism pathways leading to serotonin (5-hydroxytryptamine), kynurenine (Kyn), and indole derivatives are under the direct or indirect control of the microbiota. In this review, we gather the most recent advances concerning the central role of Trp metabolism in microbiota-host crosstalk in health and disease. Deciphering the complex equilibrium between these pathways will facilitate a better understanding of the pathogenesis of human diseases and open therapeutic opportunities.
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                Author and article information

                Contributors
                sfukuda@sfc.keio.ac.jp
                yanagisawa.masa.fu@u.tsukuba.ac.jp
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                11 November 2020
                11 November 2020
                2020
                : 10
                Affiliations
                [1 ]GRID grid.20515.33, ISNI 0000 0001 2369 4728, International Institute for Integrative Sleep Medicine (WPI-IIIS), , University of Tsukuba, ; 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575 Japan
                [2 ]GRID grid.26091.3c, ISNI 0000 0004 1936 9959, Institute for Advanced Biosciences, , Keio University, ; 246-2 Mizukami, Kakuganji, Tsuruoka, Yamagata 997-0052 Japan
                [3 ]GRID grid.416835.d, ISNI 0000 0001 2222 0432, Food Research Institute, , National Agriculture and Food Research Organization (NARO), ; 2-1-12 Kannondai, Tsukuba, Ibaraki 305-8642 Japan
                [4 ]GRID grid.20515.33, ISNI 0000 0001 2369 4728, Transborder Medical Research Center, , University of Tsukuba, ; 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575 Japan
                [5 ]Intestinal Microbiota Project, Kanagawa Institute of Industrial Science and Technology, 3-25-13 Tonomachi, Kawasaki-ku, Kawasaki, Kanagawa 210-0821 Japan
                [6 ]Metabologenomics, Inc., 246-2 Mizukami, Kakuganji, Tsuruoka, Yamagata 997-0052 Japan
                [7 ]GRID grid.20515.33, ISNI 0000 0001 2369 4728, Life Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance (TARA), , University of Tsukuba, ; 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575 Japan
                [8 ]GRID grid.20515.33, ISNI 0000 0001 2369 4728, R&D Center for Frontiers of Mirai in Policy and Technology (F-MIRAI), , University of Tsukuba, ; 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575 Japan
                [9 ]GRID grid.267313.2, ISNI 0000 0000 9482 7121, Department of Molecular Genetics, , University of Texas Southwestern Medical Center, ; Dallas, TX 75390-8584 USA
                Article
                76562
                10.1038/s41598-020-76562-9
                7659342
                33177599
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 19K14023
                Award ID: 18H04805
                Award ID: 17H06095
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002241, Japan Science and Technology Agency;
                Award ID: JPMJER1902
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100009619, Japan Agency for Medical Research and Development;
                Award ID: JP19gm1010009
                Award Recipient :
                Funded by: the Takeda Science Foundation
                Funded by: the Food Science Institute Foundation
                Funded by: the Program for the Advancement of Research in Core Projects under Keio University’s Longevity Initiative
                Funded by: FundRef http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science and Technology;
                Award ID: A3A28043
                Award Recipient :
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                © The Author(s) 2020

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                sleep, microbiome, metabolomics

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