Intermittent Fasting Confers Protection in CNS Autoimmunity by Altering the Gut Microbiota

Multiple sclerosis (MS) is more common in western countries with diet being a potential contributing factor. Here we show that intermittent fasting (IF) ameliorated clinical course and pathology of the MS model, experimental autoimmune encephalomyelitis (EAE). IF led to increased gut bacteria richne...

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Published in	Cell metabolism Vol. 27; no. 6; pp. 1222 - 1235.e6
Main Authors	Cignarella, Francesca, Cantoni, Claudia, Ghezzi, Laura, Salter, Amber, Dorsett, Yair, Chen, Lei, Phillips, Daniel, Weinstock, George M., Fontana, Luigi, Cross, Anne H., Zhou, Yanjiao, Piccio, Laura
Format	Journal Article
Language	English
Published	United States Elsevier Inc 05.06.2018
Subjects	Adipokines - blood Adult Animals Autoimmunity Bacteroidaceae - metabolism Central Nervous System - immunology diet Encephalomyelitis, Autoimmune, Experimental - diet therapy Encephalomyelitis, Autoimmune, Experimental - immunology Encephalomyelitis, Autoimmune, Experimental - microbiology experimental autoimmune encephalomyelitis Fasting Female Gastrointestinal Microbiome gut microbiota Humans intermittent fasting Lactobacillaceae - metabolism Mice Mice, Inbred C57BL Middle Aged multiple sclerosis Multiple Sclerosis - diet therapy Multiple Sclerosis - immunology Multiple Sclerosis - microbiology Pilot Projects T-Lymphocytes, Regulatory - immunology Th17 Cells - immunology intermittent fasting experimental autoimmune encephalomyelitis diet multiple sclerosis gut microbiota
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Abstract	Multiple sclerosis (MS) is more common in western countries with diet being a potential contributing factor. Here we show that intermittent fasting (IF) ameliorated clinical course and pathology of the MS model, experimental autoimmune encephalomyelitis (EAE). IF led to increased gut bacteria richness, enrichment of the Lactobacillaceae, Bacteroidaceae, and Prevotellaceae families and enhanced antioxidative microbial metabolic pathways. IF altered T cells in the gut with a reduction of IL-17 producing T cells and an increase in regulatory T cells. Fecal microbiome transplantation from mice on IF ameliorated EAE in immunized recipient mice on a normal diet, suggesting that IF effects are at least partially mediated by the gut flora. In a pilot clinical trial in MS patients, intermittent energy restriction altered blood adipokines and the gut flora resembling protective changes observed in mice. In conclusion, IF has potent immunomodulatory effects that are at least partially mediated by the gut microbiome. [Display omitted] •IF ameliorates the clinical course and pathology of the MS mouse model (EAE)•IF increases gut microbial diversity, alters their composition and metabolic pathways•Gut microbiota transfer from mice on IF led to protection from EAE in recipient mice•Findings with IER in MS patients partially recapitulates what is observed with IF in EAE Intermittent fasting confers protection in the multiple sclerosis animal model through effects on the gut microbiota; similar changes to the gut microbiota were observed in relapsing multiple sclerosis patients undergoing intermittent energy restriction.
AbstractList	Multiple sclerosis (MS) is more common in western countries with diet being a potential contributing factor. Here we show that intermittent fasting (IF) ameliorated clinical course and pathology of the MS model, experimental autoimmune encephalomyelitis (EAE). IF led to increased gut bacteria richness, enrichment of the Lactobacillaceae, Bacteroidaceae, and Prevotellaceae families and enhanced antioxidative microbial metabolic pathways. IF altered T cells in the gut with a reduction of IL-17 producing T cells and an increase in regulatory T cells. Fecal microbiome transplantation from mice on IF ameliorated EAE in immunized recipient mice on a normal diet, suggesting that IF effects are at least partially mediated by the gut flora. In a pilot clinical trial in MS patients, intermittent energy restriction altered blood adipokines and the gut flora resembling protective changes observed in mice. In conclusion, IF has potent immunomodulatory effects that are at least partially mediated by the gut microbiome. Multiple sclerosis (MS) is more common in western countries with diet being a potential contributing factor. Here we show that intermittent fasting (IF) ameliorated clinical course and pathology of the MS model, experimental autoimmune encephalomyelitis (EAE). IF led to increased gut bacteria richness, enrichment of the Lactobacillaceae, Bacteroidaceae, and Prevotellaceae families and enhanced antioxidative microbial metabolic pathways. IF altered T cells in the gut with a reduction of IL-17 producing T cells and an increase in regulatory T cells. Fecal microbiome transplantation from mice on IF ameliorated EAE in immunized recipient mice on a normal diet, suggesting that IF effects are at least partially mediated by the gut flora. In a pilot clinical trial in MS patients, intermittent energy restriction altered blood adipokines and the gut flora resembling protective changes observed in mice. In conclusion, IF has potent immunomodulatory effects that are at least partially mediated by the gut microbiome. [Display omitted] •IF ameliorates the clinical course and pathology of the MS mouse model (EAE)•IF increases gut microbial diversity, alters their composition and metabolic pathways•Gut microbiota transfer from mice on IF led to protection from EAE in recipient mice•Findings with IER in MS patients partially recapitulates what is observed with IF in EAE Intermittent fasting confers protection in the multiple sclerosis animal model through effects on the gut microbiota; similar changes to the gut microbiota were observed in relapsing multiple sclerosis patients undergoing intermittent energy restriction. Multiple sclerosis (MS) is more common in western countries with diet being a potential contributing factor. Here we show that intermittent fasting (IF) ameliorated clinical course and pathology of the MS model, experimental autoimmune encephalomyelitis (EAE). IF led to increased gut bacteria richness, enrichment of the Lactobacillaceae, Bacteroidaceae, and Prevotellaceae families and enhanced antioxidative microbial metabolic pathways. IF altered T cells in the gut with a reduction of IL-17 producing T cells and an increase in regulatory T cells. Fecal microbiome transplantation from mice on IF ameliorated EAE in immunized recipient mice on a normal diet, suggesting that IF effects are at least partially mediated by the gut flora. In a pilot clinical trial in MS patients, intermittent energy restriction altered blood adipokines and the gut flora resembling protective changes observed in mice. In conclusion, IF has potent immunomodulatory effects that are at least partially mediated by the gut microbiome.Multiple sclerosis (MS) is more common in western countries with diet being a potential contributing factor. Here we show that intermittent fasting (IF) ameliorated clinical course and pathology of the MS model, experimental autoimmune encephalomyelitis (EAE). IF led to increased gut bacteria richness, enrichment of the Lactobacillaceae, Bacteroidaceae, and Prevotellaceae families and enhanced antioxidative microbial metabolic pathways. IF altered T cells in the gut with a reduction of IL-17 producing T cells and an increase in regulatory T cells. Fecal microbiome transplantation from mice on IF ameliorated EAE in immunized recipient mice on a normal diet, suggesting that IF effects are at least partially mediated by the gut flora. In a pilot clinical trial in MS patients, intermittent energy restriction altered blood adipokines and the gut flora resembling protective changes observed in mice. In conclusion, IF has potent immunomodulatory effects that are at least partially mediated by the gut microbiome. Multiple sclerosis (MS) is a central nervous system (CNS) inflammatory demyelinating disease impacted by the interplay of genetic and environmental factors. It is presumed to be autoimmune. MS is more common in western countries and differences in diet could contribute to its particular geographical distribution. Studies relating diet to MS have been inconclusive. A mechanism through which diet can influence immune responses is the gut microbiome, which is emerging as a critical contributor in numerous human diseases. Here we show that intermittent fasting (IF) ameliorated clinical course and pathology of the MS animal model, experimental autoimmune encephalomyelitis (EAE), leading to less inflammation, demyelination and axonal damage. IF changed the gut microbiome resulting in increased bacteria richness and enrichment of the Lactobacillaceae , Bacterioidaceae and Prevotellaceae families. Gut microbiome richness was inversely correlated with leptin levels. Microbial metabolic pathway analysis revealed that IF-induced changes to the gut microbiome increased ketone formation and glutathione metabolism, enhancing anti-oxidative pathways. Furthermore, IF had direct effects on the composition of T cells in the gut lamina propria with a reduction of IL-17 producing T cells and an increase in the number of regulatory T cells. These effects might modulate systemic immune responses. Importantly, fecal microbiome transplantation from mice on IF ameliorated EAE in immunized recipient mice on a normal diet, suggesting that IF immunomodulatory effects are at least partially mediated by the gut flora. We translated our findings to MS patients in a pilot clinical trial in MS patients undergoing relapse to test the safety, feasibility and effects of IF on clinical and laboratory measures. Potentially beneficial effects on levels of several immune inflammatory parameters as well as gut flora that resembled the protective changes observed in mice in EAE were observed. In conclusion, IF has potent immunomodulatory effects that are at least partially mediated by the gut microbiome. Intermittent fasting (IF) confers protection in the multiple sclerosis animal model through effects on the gut microbiota, with similar changes to gut microbiota observed in relapsing MS patients undergoing short-term IF.
Author	Fontana, Luigi Weinstock, George M. Cignarella, Francesca Zhou, Yanjiao Chen, Lei Ghezzi, Laura Dorsett, Yair Piccio, Laura Phillips, Daniel Cross, Anne H. Salter, Amber Cantoni, Claudia
AuthorAffiliation	1 Department of Neurology, Washington University School of Medicine, St Louis, MO, USA 5 Department of Medicine, Washington University School of Medicine St. Louis, MO 63110, USA 8 Hope Center for Neurological Disorders, Washington University School of Medicine, St Louis, MO, USA 4 Jackson Laboratory for Genomic Medicine, Farmington, CT, USA 2 Neurology Unit, Department of Pathophysiology and Transplantation, University of Milan, Fondazione Cà Granda, IRCCS Ospedale Policlinico, Milan, Italy 6 Department of Clinical and Experimental Sciences, Brescia University Medical School, Brescia, Italy 7 CEINGE Biotecnologie Avanzate, Napoli, Italy 3 Division of Biostatistics, Washington University School of Medicine St. Louis, MO 63110, USA
AuthorAffiliation_xml	– name: 2 Neurology Unit, Department of Pathophysiology and Transplantation, University of Milan, Fondazione Cà Granda, IRCCS Ospedale Policlinico, Milan, Italy – name: 4 Jackson Laboratory for Genomic Medicine, Farmington, CT, USA – name: 8 Hope Center for Neurological Disorders, Washington University School of Medicine, St Louis, MO, USA – name: 6 Department of Clinical and Experimental Sciences, Brescia University Medical School, Brescia, Italy – name: 3 Division of Biostatistics, Washington University School of Medicine St. Louis, MO 63110, USA – name: 5 Department of Medicine, Washington University School of Medicine St. Louis, MO 63110, USA – name: 7 CEINGE Biotecnologie Avanzate, Napoli, Italy – name: 1 Department of Neurology, Washington University School of Medicine, St Louis, MO, USA
Author_xml	– sequence: 1 givenname: Francesca surname: Cignarella fullname: Cignarella, Francesca organization: Department of Neurology, Washington University School of Medicine, Campus Box 8111, 660 S. Euclid Avenue, St. Louis, MO 63110, USA – sequence: 2 givenname: Claudia surname: Cantoni fullname: Cantoni, Claudia organization: Department of Neurology, Washington University School of Medicine, Campus Box 8111, 660 S. Euclid Avenue, St. Louis, MO 63110, USA – sequence: 3 givenname: Laura surname: Ghezzi fullname: Ghezzi, Laura organization: Department of Neurology, Washington University School of Medicine, Campus Box 8111, 660 S. Euclid Avenue, St. Louis, MO 63110, USA – sequence: 4 givenname: Amber surname: Salter fullname: Salter, Amber organization: Division of Biostatistics, Washington University School of Medicine, St. Louis, MO 63110, USA – sequence: 5 givenname: Yair surname: Dorsett fullname: Dorsett, Yair organization: Jackson Laboratory for Genomic Medicine, Farmington, CT, USA – sequence: 6 givenname: Lei surname: Chen fullname: Chen, Lei organization: Jackson Laboratory for Genomic Medicine, Farmington, CT, USA – sequence: 7 givenname: Daniel surname: Phillips fullname: Phillips, Daniel organization: Jackson Laboratory for Genomic Medicine, Farmington, CT, USA – sequence: 8 givenname: George M. surname: Weinstock fullname: Weinstock, George M. organization: Jackson Laboratory for Genomic Medicine, Farmington, CT, USA – sequence: 9 givenname: Luigi surname: Fontana fullname: Fontana, Luigi organization: Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA – sequence: 10 givenname: Anne H. surname: Cross fullname: Cross, Anne H. organization: Department of Neurology, Washington University School of Medicine, Campus Box 8111, 660 S. Euclid Avenue, St. Louis, MO 63110, USA – sequence: 11 givenname: Yanjiao surname: Zhou fullname: Zhou, Yanjiao email: yazhou@uchc.edu organization: Jackson Laboratory for Genomic Medicine, Farmington, CT, USA – sequence: 12 givenname: Laura surname: Piccio fullname: Piccio, Laura email: picciol@wustl.edu organization: Department of Neurology, Washington University School of Medicine, Campus Box 8111, 660 S. Euclid Avenue, St. Louis, MO 63110, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/29874567$$D View this record in MEDLINE/PubMed
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Keywords	intermittent fasting experimental autoimmune encephalomyelitis diet multiple sclerosis gut microbiota
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 ObjectType-Undefined-3 These authors contributed equally to the work AUTHORS CONTRIBUTIONS L.P., A.H.C., L.F. and Y.Z. designed and conceived the study; F.C., C.C. and L.G. planned and performed all experiments; A.S. performed statistical analyses; G.M.W facilitated sequencing and analysis of microbome data. Y.D and L.C. performed microbiome analyses; L.P., A.H.C. and Y.Z. wrote the manuscript with contributions from L.F., C.C., F.C., L.G. and G.M.W.
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Snippet	Multiple sclerosis (MS) is more common in western countries with diet being a potential contributing factor. Here we show that intermittent fasting (IF)... Multiple sclerosis (MS) is a central nervous system (CNS) inflammatory demyelinating disease impacted by the interplay of genetic and environmental factors. It...
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SubjectTerms	Adipokines - blood Adult Animals Autoimmunity Bacteroidaceae - metabolism Central Nervous System - immunology diet Encephalomyelitis, Autoimmune, Experimental - diet therapy Encephalomyelitis, Autoimmune, Experimental - immunology Encephalomyelitis, Autoimmune, Experimental - microbiology experimental autoimmune encephalomyelitis Fasting Female Gastrointestinal Microbiome gut microbiota Humans intermittent fasting Lactobacillaceae - metabolism Mice Mice, Inbred C57BL Middle Aged multiple sclerosis Multiple Sclerosis - diet therapy Multiple Sclerosis - immunology Multiple Sclerosis - microbiology Pilot Projects T-Lymphocytes, Regulatory - immunology Th17 Cells - immunology
Title	Intermittent Fasting Confers Protection in CNS Autoimmunity by Altering the Gut Microbiota
URI	https://dx.doi.org/10.1016/j.cmet.2018.05.006 https://www.ncbi.nlm.nih.gov/pubmed/29874567 https://www.proquest.com/docview/2051670805 https://pubmed.ncbi.nlm.nih.gov/PMC6460288
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