CXCR3+ T cells in multiple sclerosis correlate with reduced diversity of the gut microbiome

Journal of Translational Autoimmunity - Tập 3 - Trang 100032 - 2020
Siobhán Ní Choileáin1, Markus Kleinewietfeld1,2, Khadir Raddassi1, David A. Hafler1,3, William E. Ruff1, Erin E. Longbrake1,4
1Department of Neurology, Yale University School of Medicine, New Haven, CT, 06511, USA
2VIB Laboratory of Translational Immunomodulation, VIB Center for Inflammation Research (IRC), UHasselt, Campus Diepenbeek, Hasselt, Belgium
3Department of Immunobiology, Yale University School of Medicine, New Haven, CT, 06511, USA
4Center for Neuroepidemiology and Clinical Neurological Research, Yale School of Medicine, Yale University, New Haven, CT, USA

Tài liệu tham khảo

Lodygin, 2019, beta-Synuclein-reactive T cells induce autoimmune CNS grey matter degeneration, Nature, 566, 503, 10.1038/s41586-019-0964-2 Compston, 2008, Multiple sclerosis, Lancet, 372, 1502, 10.1016/S0140-6736(08)61620-7 Reich, 2018, Multiple sclerosis, N. Engl. J. Med., 378, 169, 10.1056/NEJMra1401483 Nylander, 2012, Multiple sclerosis, J. Clin. Investig., 122, 1180, 10.1172/JCI58649 Hafler, 2007, Risk alleles for multiple sclerosis identified by a genomewide study, N. Engl. J. Med., 357, 851, 10.1056/NEJMoa073493 Patsopoulos, 2017 International, 2018, Multiple sclerosis genetics consortium. Electronic address, C. International multiple sclerosis genetics. Low-frequency and rare-coding variation contributes to multiple sclerosis risk, Cell, 175, 1679, 10.1016/j.cell.2018.09.049 Olsson, 2017, Interactions between genetic, lifestyle and environmental risk factors for multiple sclerosis, Nat. Rev. Neurol., 13, 25, 10.1038/nrneurol.2016.187 Marson, 2015, Genetic basis of autoimmunity, J. Clin. Investig., 125, 2234, 10.1172/JCI78086 Sumida, 2018, Activated beta-catenin in Foxp3(+) regulatory T cells links inflammatory environments to autoimmunity, Nat. Immunol., 19, 1391, 10.1038/s41590-018-0236-6 Wekerle, 2017, Brain autoimmunity and intestinal microbiota: 100 trillion game changers, Trends Immunol., 38, 483, 10.1016/j.it.2017.03.008 Cao, 2015, Functional inflammatory profiles distinguish myelin-reactive T cells from patients with multiple sclerosis, Sci. Transl. Med., 7, 287ra74, 10.1126/scitranslmed.aaa8038 Ota, 1990, T-cell recognition of an immunodominant myelin basic protein epitope in multiple sclerosis, Nature, 346, 183, 10.1038/346183a0 Martin, 1990, Fine specificity and HLA restriction of myelin basic protein-specific cytotoxic T cell lines from multiple sclerosis patients and healthy individuals, J. Immunol., 145, 540, 10.4049/jimmunol.145.2.540 Pette, 1990, Myelin basic protein-specific T lymphocyte lines from MS patients and healthy individuals, Neurology, 40, 1770, 10.1212/WNL.40.11.1770 Sun, 1991, Autoreactive T and B cells responding to myelin proteolipid protein in multiple sclerosis and controls, Eur. J. Immunol., 21, 1461, 10.1002/eji.1830210620 Zhang, 1994, Increased frequency of interleukin 2-responsive T cells specific for myelin basic protein and proteolipid protein in peripheral blood and cerebrospinal fluid of patients with multiple sclerosis, J. Exp. Med., 179, 973, 10.1084/jem.179.3.973 Raddassi, 2011, Increased frequencies of myelin oligodendrocyte glycoprotein/MHC class II-binding CD4 cells in patients with multiple sclerosis, J. Immunol., 187, 1039, 10.4049/jimmunol.1001543 Cho, 2012, The human microbiome: at the interface of health and disease, Nat. Rev. Genet., 13, 260, 10.1038/nrg3182 Backhed, 2012, Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications, Cell Host Microbe, 12, 611, 10.1016/j.chom.2012.10.012 Ruff, 2015, Autoimmune host-microbiota interactions at barrier sites and beyond, Trends Mol. Med., 21, 233, 10.1016/j.molmed.2015.02.006 Miyake, 2015, Dysbiosis in the gut microbiota of patients with multiple sclerosis, with a striking depletion of species belonging to clostridia XIVa and IV clusters, PLoS One, 10, 10.1371/journal.pone.0137429 Cantarel, 2015, Gut microbiota in multiple sclerosis: possible influence of immunomodulators, J. Investig. Med., 63, 729, 10.1097/JIM.0000000000000192 Chen, 2016, Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls, Sci. Rep., 6, 28484, 10.1038/srep28484 Cekanaviciute, 2017, Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models, Proc. Natl. Acad. Sci. U. S. A., 114, 10713, 10.1073/pnas.1711235114 Berer, 2017, Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice, Proc. Natl. Acad. Sci. U. S. A., 114, 10719, 10.1073/pnas.1711233114 Jangi, 2016, Alterations of the human gut microbiome in multiple sclerosis, Nat. Commun., 7, 12015, 10.1038/ncomms12015 Reboldi, 2009, C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE, Nat. Immunol., 10, 514, 10.1038/ni.1716 Dominguez-Villar, 2011, Identification of T helper type 1-like, Foxp3+ regulatory T cells in human autoimmune disease, Nat. Med., 17, 673, 10.1038/nm.2389 Cunill, 2018, Relapsing-remitting multiple sclerosis is characterized by a T follicular cell pro-inflammatory shift, reverted by dimethyl fumarate treatment, Front. Immunol., 9, 1097, 10.3389/fimmu.2018.01097 Morita, 2011, Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion, Immunity, 34, 108, 10.1016/j.immuni.2010.12.012 Babbe, 2000, Clonal expansions of CD8(+) T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction, J. Exp. Med., 192, 393, 10.1084/jem.192.3.393 Bargatze, 1995, Distinct roles of L-selectin and integrins alpha 4 beta 7 and LFA-1 in lymphocyte homing to Peyer’s patch-HEV in situ: the multistep model confirmed and refined, Immunity, 3, 99, 10.1016/1074-7613(95)90162-0 Caporaso, 2011, Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample, Proc. Natl. Acad. Sci. U. S. A., 108, 4516, 10.1073/pnas.1000080107 Kozich, 2013, Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform, Appl. Environ. Microbiol., 79, 5112, 10.1128/AEM.01043-13 Cullen, 2015, Gut microbiota. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation, Science, 347, 170, 10.1126/science.1260580 Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data, Nat. Methods, 7, 335, 10.1038/nmeth.f.303 Segata, 2011, Metagenomic biomarker discovery and explanation, Genome Biol., 12, R60, 10.1186/gb-2011-12-6-r60 Lozupone, 2005, UniFrac: a new phylogenetic method for comparing microbial communities, Appl. Environ. Microbiol., 71, 8228, 10.1128/AEM.71.12.8228-8235.2005 Shahi, 2017, Gut microbiome in multiple sclerosis: the players involved and the roles they play, Gut Microb., 1 Sallusto, 1999, Two subsets of memory T lymphocytes with distinct homing potentials and effector functions, Nature, 401, 708, 10.1038/44385 Masopust, 2013, The integration of T cell migration, differentiation and function, Nat. Rev. Immunol., 13, 309, 10.1038/nri3442 Habtezion, 2016, Leukocyte trafficking to the small intestine and colon, Gastroenterology, 150, 340, 10.1053/j.gastro.2015.10.046 Tremlett, 2016, Gut microbiota in early pediatric multiple sclerosis: a case-control study, Eur. J. Neurol., 23, 1308, 10.1111/ene.13026 Le Chatelier, 2013, Richness of human gut microbiome correlates with metabolic markers, Nature, 500, 541, 10.1038/nature12506 Manichanh, 2006, Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach, Gut, 55, 205, 10.1136/gut.2005.073817 Lozupone, 2013, Meta-analyses of studies of the human microbiota, Genome Res., 23, 1704, 10.1101/gr.151803.112 de Goffau, 2012, Fecal microbiota composition differs between children with -cell autoimmunity and those without, Diabetes, 62, 1238, 10.2337/db12-0526 Kostic, 2015, The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes, Cell Host Microbe, 17, 260, 10.1016/j.chom.2015.01.001 Scher, 2015, Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease, Arthritis Rheum., 67, 128, 10.1002/art.38892 Turnbaugh, 2009, A core gut microbiome in obese and lean twins, Nature, 457, 480, 10.1038/nature07540 Kriss, 2018, Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery, Curr. Opin. Microbiol., 44, 34, 10.1016/j.mib.2018.07.003 Rooks, 2016, Gut microbiota, metabolites and host immunity, Nat. Rev. Immunol., 16, 341, 10.1038/nri.2016.42 Smith, 2013, The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis, Science, 341, 569, 10.1126/science.1241165 Arpaia, 2013, Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation, Nature, 504, 451, 10.1038/nature12726 Furusawa, 2013, Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells, Nature, 504, 446, 10.1038/nature12721 Braniste, 2014, The gut microbiota influences blood-brain barrier permeability in mice, Sci. Transl. Med., 6, 263ra158, 10.1126/scitranslmed.3009759 Li, 2016, Sodium butyrate exerts neuroprotective effects by restoring the blood-brain barrier in traumatic brain injury mice, Brain Res., 1642, 70, 10.1016/j.brainres.2016.03.031 Haghikia, 2015, Dietary fatty acids directly impact central nervous system Autoimmunity via the small intestine, Immunity, 43, 817, 10.1016/j.immuni.2015.09.007 Mizuno, 2017, The dual role of short fatty acid chains in the pathogenesis of autoimmune disease models, PLoS One, 12, 10.1371/journal.pone.0173032 Viglietta, 2004, Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis, J. Exp. Med., 199, 971, 10.1084/jem.20031579 Astier, 2006, Alterations in CD46-mediated Tr1 regulatory T cells in patients with multiple sclerosis, J. Clin. Investig., 116, 3252, 10.1172/JCI29251 Venken, 2008, Compromised CD4+ CD25(high) regulatory T-cell function in patients with relapsing-remitting multiple sclerosis is correlated with a reduced frequency of FOXP3-positive cells and reduced FOXP3 expression at the single-cell level, Immunology, 123, 79, 10.1111/j.1365-2567.2007.02690.x Hansen, 2011, Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins, Proc. Natl. Acad. Sci. U.S.A., 108, 4599, 10.1073/pnas.1000071108 Attaluri, 2010, Methanogenic flora is associated with altered colonic transit but not stool characteristics in constipation without IBS, Am. J. Gastroenterol., 105, 1407, 10.1038/ajg.2009.655 Balashov, 1999, CCR5(+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions, Proc. Natl. Acad. Sci. U. S. A., 96, 6873, 10.1073/pnas.96.12.6873 Sorensen, 1999, Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients, J. Clin. Investig., 103, 807, 10.1172/JCI5150 Sorensen, 2002, Multiple sclerosis: a study of CXCL10 and CXCR3 co-localization in the inflamed central nervous system, J. Neuroimmunol., 127, 59, 10.1016/S0165-5728(02)00097-8 Romme Christensen, 2013, Systemic inflammation in progressive multiple sclerosis involves follicular T-helper, Th17- and activated B-cells and correlates with progression, PLoS One, 8, 10.1371/annotation/b4e623eb-4950-48d9-8d85-8d70426d95a3 Groom, 2011, CXCR3 ligands: redundant, collaborative and antagonistic functions, Immunol. Cell Biol., 89, 207, 10.1038/icb.2010.158 von Andrian, 2000, T-cell function and migration. Two sides of the same coin, N. Engl. J. Med., 343, 1020, 10.1056/NEJM200010053431407 Kivisakk, 2006, Human cerebrospinal fluid contains CD4+ memory T cells expressing gut- or skin-specific trafficking determinants: relevance for immunotherapy, BMC Immunol., 7, 14, 10.1186/1471-2172-7-14 Mazmanian, 2005, An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system, Cell, 122, 107, 10.1016/j.cell.2005.05.007 Greiling, 2018, Commensal orthologs of the human autoantigen Ro60 as triggers of autoimmunity in lupus, Sci. Transl. Med., 10, 10.1126/scitranslmed.aan2306 Gil-Cruz, 2019, Microbiota-derived peptide mimics drive lethal inflammatory cardiomyopathy, Science, 366, 881, 10.1126/science.aav3487 Ruff, 2019, Pathogenic autoreactive T and B cells cross-react with mimotopes expressed by a common human gut commensal to trigger autoimmunity, Cell Host Microbe, 26, 100, 10.1016/j.chom.2019.05.003 Hughes, 2003, Cross-reactivity between related sequences found in Acinetobacter sp., Pseudomonas aeruginosa, myelin basic protein and myelin oligodendrocyte glycoprotein in multiple sclerosis, J. Neuroimmunol., 144, 105, 10.1016/S0165-5728(03)00274-1 Planas, 2018, GDP-l-fucose synthase is a CD4(+) T cell-specific autoantigen in DRB3*02:02 patients with multiple sclerosis, Sci. Transl. Med., 10, 10.1126/scitranslmed.aat4301 Rojas, 2019, Recirculating intestinal IgA-producing cells regulate neuroinflammation via IL-10, Cell, 177, 492, 10.1016/j.cell.2019.03.037