The intestinal microbiome in spondyloarthritis

Purpose of reviewMicrobial dysbiosis in the gut is emerging as a common component in various inflammatory disorders including spondyloarthritis (SpA). The depth of this influence has begun to be realized with next-generation sequencing of the gut microbiome providing unbiased assessment of previously uncharted bacterial populations. Recent findingsDecreased numbers of Firmicutes, a major phyla of gut commensals, especially the species Faecalibacterium prausnitzii and Clostridium leptum have been found in various inflammatory disorders including SpA and inflammatory bowel disease (IBD), and could be an important link between SpA and gut inflammation. Multiple studies in ankylosing spondylitis, psoriatic arthritis, juvenile SpA, and animal models of SpA are revealing common bacterial associations among these diseases as well as IBD. SummaryWe are beginning to appreciate the complex relationship between the gut microbiome and host immune regulation and dysregulation in health and disease. Potentially important differences have been revealed in SpA, but cause and effect relationships remain far from established. Many critical questions remain to be answered before we can apply new knowledge to improve therapeutics in SpA.

[1]  R. Misra,et al.  Low molecular weight proteins of outer membrane of Salmonella typhimurium are immunogenic in Salmonella induced reactive arthritis revealed by proteomics , 2007, Clinical and experimental immunology.

[2]  R. Knight,et al.  Microbiota restoration: natural and supplemented recovery of human microbial communities , 2011, Nature Reviews Microbiology.

[3]  K. McCoy,et al.  Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. , 2014, Immunity.

[4]  D. Aguirre de Cárcer,et al.  ZAP‐70 Genotype Disrupts the Relationship Between Microbiota and Host, Leading to Spondyloarthritis and Ileitis in SKG Mice , 2014, Arthritis & rheumatology.

[5]  E. Jones,et al.  Intrinsic multipotential mesenchymal stromal cell activity in gelatinous Heberden’s nodes in osteoarthritis at clinical presentation , 2014, Arthritis Research & Therapy.

[6]  Judith Hall,et al.  Tolerance of bacteriuria after urinary diversion is linked to antimicrobial peptide activity. , 2011, Urology.

[7]  Francisco Guarner,et al.  The gut microbiota in IBD , 2012, Nature Reviews Gastroenterology &Hepatology.

[8]  Tony J. Kenna,et al.  Intestinal Dysbiosis in Ankylosing Spondylitis , 2016 .

[9]  R. Misra,et al.  Evidence of Cellular Immune Response to Outer Membrane Protein of Salmonella typhimurium in Patients with Enthesitis-related Arthritis Subtype of Juvenile Idiopathic Arthritis , 2011, The Journal of Rheumatology.

[10]  S. Raimondo,et al.  Evidence that autophagy, but not the unfolded protein response, regulates the expression of IL-23 in the gut of patients with ankylosing spondylitis and subclinical gut inflammation , 2013, Annals of the rheumatic diseases.

[11]  Rustem F. Ismagilov,et al.  Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness , 2014, Nature.

[12]  Christophe Benoist,et al.  Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. , 2010, Immunity.

[13]  Simon C. Potter,et al.  Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants , 2007, Nature Genetics.

[14]  M. Stone,et al.  Comparative immune responses to candidate arthritogenic bacteria do not confirm a dominant role for Klebsiella pneumonia in the pathogenesis of familial ankylosing spondylitis. , 2003, Rheumatology.

[15]  R. Hammer,et al.  Inflammatory disease in HLA‐B27 transgenic rats , 1999, Immunological reviews.

[16]  Judy H. Cho,et al.  A Genome-Wide Association Study Identifies IL23R as an Inflammatory Bowel Disease Gene , 2006, Science.

[17]  H. Harmsen,et al.  Reduction of Colitis by Prebiotics in HLA‐B27 Transgenic Rats Is Associated with Microflora Changes and Immunomodulation , 2005, Inflammatory bowel diseases.

[18]  J. Rosenbaum,et al.  Time for a gut check: evidence for the hypothesis that HLA-B27 predisposes to ankylosing spondylitis by altering the microbiome. , 2011, Arthritis and rheumatism.

[19]  F. D'armiento,et al.  Microscopic inflammatory changes in colon of patients with both active psoriasis and psoriatic arthritis without bowel symptoms. , 2000, The Journal of rheumatology.

[20]  D. Laukens,et al.  CARD15 gene polymorphisms in patients with spondyloarthropathies identify a specific phenotype previously related to Crohn’s disease , 2004, Annals of the rheumatic diseases.

[21]  J. Nicholson,et al.  Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. , 2012, Cell metabolism.

[22]  J. Highton,et al.  The Immune Response to Autologous Bacteroides in Ankylosing Spondylitis Is Characterized by Reduced Interleukin 10 Production , 2009, The Journal of Rheumatology.

[23]  A. Macpherson,et al.  Interactions Between the Microbiota and the Immune System , 2012, Science.

[24]  W. R. Wikoff,et al.  Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites , 2009, Proceedings of the National Academy of Sciences.

[25]  V. De Rosa,et al.  A key role of leptin in the control of regulatory T cell proliferation. , 2007, Immunity.

[26]  F. Bäckhed,et al.  Host-Bacterial Mutualism in the Human Intestine , 2005, Science.

[27]  M. De Vos,et al.  The evolution of spondyloarthropathies in relation to gut histology. III. Relation between gut and joint. , 1995, The Journal of rheumatology.

[28]  P. Das,et al.  Antibodies to mycobacterial 65-kDa heat shock protein and other immunodominant antigens in patients with psoriasis. , 1993, The Journal of investigative dermatology.

[29]  Huidong Shi,et al.  Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. , 2014, Immunity.

[30]  Aaron Y. Lee,et al.  HLA-B27 and Human β2-Microglobulin Affect the Gut Microbiota of Transgenic Rats , 2014, PloS one.

[31]  K. Honda,et al.  Induction of Colonic Regulatory T Cells by Indigenous Clostridium Species , 2011, Science.

[32]  S. Grivennikov,et al.  Transcription factor T-bet regulates intraepithelial lymphocyte functional maturation. , 2014, Immunity.

[33]  R. Hammer,et al.  Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. , 1996, The Journal of clinical investigation.

[34]  D. Artis,et al.  Intestinal bacteria and the regulation of immune cell homeostasis. , 2010, Annual review of immunology.

[35]  Xiangqin Cui,et al.  Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis , 2014, Arthritis Research & Therapy.

[36]  V. Young,et al.  Microbial ecology of the murine gut associated with the development of dextran sodium sulfate‐induced colitis , 2011, Inflammatory bowel diseases.

[37]  K. Wilson,et al.  Differential Induction of Colitis and Gastritis in HLA-B27 Transgenic Rats Selectively Colonized with Bacteroides vulgatus or Escherichia coli , 1999, Infection and Immunity.

[38]  K. Honda,et al.  Microbiota in autoimmunity and tolerance. , 2011, Current opinion in immunology.

[39]  J. Cantero-Hinojosa,et al.  Intestinal permeability in patients with ankylosing spondylitis and their healthy relatives. , 1994, British journal of rheumatology.

[40]  Z. Filipovic,et al.  Repeated measurement of intestinal permeability as an assessment of colitis severity in HLA-B27 transgenic rats. , 1999, The Journal of pharmacology and experimental therapeutics.

[41]  Luying Peng,et al.  Effects of Butyrate on Intestinal Barrier Function in a Caco-2 Cell Monolayer Model of Intestinal Barrier , 2007, Pediatric Research.

[42]  Julia Manasson,et al.  Decreased Bacterial Diversity Characterizes the Altered Gut Microbiota in Patients With Psoriatic Arthritis, Resembling Dysbiosis in Inflammatory Bowel Disease , 2015, Arthritis & rheumatology.

[43]  L. Latulippe,et al.  [Reactive arthritis]. , 1980, L'union medicale du Canada.

[44]  V. Saudek,et al.  Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression , 2010, Proceedings of the National Academy of Sciences.

[45]  Ting Wang,et al.  The gut microbiota as an environmental factor that regulates fat storage. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[46]  A. Ebringer,et al.  Ankylosing spondylitis: klebsiella and HL-A B27. , 1977, Rheumatology and rehabilitation.

[47]  L. Sistonen,et al.  Enhanced intracellular replication of Salmonella enteritidis in HLA-B27-expressing human monocytic cells: dependency on glutamic acid at position 45 in the B pocket of HLA-B27. , 2004, Arthritis and rheumatism.

[48]  M. Leirisalo-Repo.  Reactive arthritis: [review] , 2005 .

[49]  J. Doré,et al.  Comparison of the faecal microflora of patients with ankylosing spondylitis and controls using molecular methods of analysis. , 2002, Rheumatology.

[50]  Anders F. Andersson,et al.  A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. , 2010, Gastroenterology.

[51]  I. Ivanov,et al.  Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. , 2014, Immunity.

[52]  B. Roe,et al.  A core gut microbiome in obese and lean twins , 2008, Nature.

[53]  R. Hammer,et al.  The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats , 1994, The Journal of experimental medicine.

[54]  H. Mcdevitt,et al.  Endotoxin-induced uveitis in rats as a model for human disease , 1980, Nature.

[55]  Mhairi Marshall,et al.  Brief Report: Intestinal Dysbiosis in Ankylosing Spondylitis , 2014, Arthritis & rheumatology.

[56]  J. Carter,et al.  Reactive arthritis: clinical aspects and medical management. , 2009, Rheumatic diseases clinics of North America.

[57]  Nick C Fox,et al.  Gene-Wide Analysis Detects Two New Susceptibility Genes for Alzheimer's Disease , 2014, PLoS ONE.

[58]  S. Targan,et al.  Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease. , 2005, Gastroenterology.

[59]  W. Garrett,et al.  The Microbial Metabolites, Short-Chain Fatty Acids, Regulate Colonic Treg Cell Homeostasis , 2013, Science.

[60]  W. Strober.  Impact of the gut microbiome on mucosal inflammation. , 2013, Trends in immunology.

[61]  R. Colbert,et al.  HLA-B27 misfolding and ankylosing spondylitis. , 2014, Molecular immunology.

[62]  C. Huttenhower,et al.  Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis , 2013, eLife.

[63]  N. Bernard.  Rheumatoid arthritis: Prevotella copri associated with new-onset untreated RA , 2014, Nature Reviews Rheumatology.

[64]  J. Baker,et al.  Evaluation of the safety and tolerability of a short higher-dose primaquine regimen for presumptive anti-relapse therapy in healthy subjects. , 2011, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[65]  M. Hattori,et al.  Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota , 2013, Nature.

[66]  M. Tomita,et al.  Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells , 2013, Nature.

[67]  M. Fielder,et al.  Antibodies to Klebsiella, Proteus, and HLA-B27 peptides in Japanese patients with ankylosing spondylitis and rheumatoid arthritis. , 1997, The Journal of rheumatology.