Gut microbes, immunity, and spondyloarthritis

Clinical Immunology

Volumn 159, Issue 2, 2014, Pages 134-142

  Stoll, Matthew L ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Inflammatory bowel disease; Microbiome; Microbiota; Spondyloarthritis

Indexed keywords

ANTIBIOTIC AGENT; DNA 16S; OUTER MEMBRANE PROTEIN; PROBIOTIC AGENT; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR INHIBITOR;

ANKYLOSING SPONDYLITIS; ANTIBIOTIC THERAPY; ARTICLE; CROHN DISEASE; ENTERITIS; HUMAN; HUMORAL IMMUNITY; IMMUNITY; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; JUVENILE RHEUMATOID ARTHRITIS; NONHUMAN; PRIORITY JOURNAL; PSORIATIC ARTHRITIS; REACTIVE ARTHRITIS; SPONDYLARTHRITIS; T LYMPHOCYTE; ULCERATIVE COLITIS; ANIMAL; IMMUNE SYSTEM; IMMUNOLOGY; INFLAMMATION; INTESTINE; MICROBIOLOGY; MOUSE; SPONDYLOARTHROPATHY;

ANIMALS; ARTHRITIS, JUVENILE; ARTHRITIS, PSORIATIC; ARTHRITIS, REACTIVE; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNE SYSTEM; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTESTINES; MICE; SPONDYLARTHROPATHIES; SPONDYLITIS, ANKYLOSING;

EID: 84952630346     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2015.05.001     Document Type: Article

References (91)

1. Nuki G., Simkin P.A. A concise history of gout and hyperuricemia and their treatment. Arthritis Res. Ther. 2006, 8(Suppl. 1):S1.
2. Dougados M., Baeten D. Spondyloarthritis. Lancet 2011, 377:2127-2137.
3. Burgos-Vargas R., Vazquez-Mellado J. The early clinical recognition of juvenile-onset ankylosing spondylitis and its differentiation from juvenile rheumatoid arthritis. Arthritis Rheum. 1995, 38:835-844.
4. van der Linden S., Valkenburg H.A., Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum. 1984, 27:361-368.
5. Petty R.E., Southwood T.R., Manners P., et al. International League of Associations for Rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J. Rheumatol. 2004, 31:390-392.
6. Stoll M.L., Bhore R., Dempsey-Robertson M., et al. Spondyloarthritis in a pediatric population: risk factors for sacroiliitis. J. Rheumatol. 2010, 37:2402-2408.
7. Hall M.A., Burgos Vargos R., Ansell B.M. Sacroiliitis in juvenile chronic arthritis. A 10-year follow-up. Clin. Exp. Rheumatol. 1987, 5(Suppl. 1):S65-S67.
8. Stolwijk C., van Tubergen A., Castillo-Ortiz J.D., et al. Prevalence of extra-articular manifestations in patients with ankylosing spondylitis: a systematic review and meta-analysis. Ann. Rheum. Dis. 2015, 74(1):65-73.
9. Mielants H., Veys E.M., Goemaere S., et al. Gut inflammation in the spondyloarthropathies: clinical, radiologic, biologic and genetic features in relation to the type of histology. A prospective study. J. Rheumatol. 1991, 18:1542-1551.
10. Mielants H., Veys E.M., Cuvelier C., et al. Gut inflammation in children with late onset pauciarticular juvenile chronic arthritis and evolution to adult spondyloarthropathy-a prospective study. J. Rheumatol. 1993, 20:1567-1572.
11. Stoll M.L., Punaro M., Patel A.S. Fecal calprotectin in children with the enthesitis-related arthritis subtype of juvenile idiopathic arthritis. J. Rheumatol. 2011, 38:2274-2275.
12. Van Praet L., Jans L., Carron P., et al. Degree of bone marrow oedema in sacroiliac joints of patients with axial spondyloarthritis is linked to gut inflammation and male sex: results from the GIANT cohort. Ann. Rheum. Dis. 2014, 73:1186-1189.
13. Mielants H., Veys E.M., Cuvelier C., et al. The evolution of spondyloarthropathies in relation to gut histology. III. Relation between gut and joint. J. Rheumatol. 1995, 22:2279-2284.
14. Schatteman L., Mielants H., Veys E.M., et al. Gut inflammation in psoriatic arthritis: a prospective ileocolonoscopic study. J. Rheumatol. 1995, 22:680-683.
15. Fantini M.C., Pallone F., Monteleone G. Common immunologic mechanisms in inflammatory bowel disease and spondylarthropathies. World J. Gastroenterol. 2009, 15:2472-2478.
16. Reveille J.D. Genetics of spondyloarthritis-beyond the MHC. Nat. Rev. Rheumatol. 2012, 8:296-304.
17. Naser S.A., Arce M., Khaja A., et al. Role of ATG16L, NOD2 and IL23R in Crohn's disease pathogenesis. World J. Gastroenterol. 2012, 18:412-424.
18. Sokol H., Conway K.L., Zhang M., et al. Card9 mediates intestinal epithelial cell restitution, T-helper 17 responses, and control of bacterial infection in mice. Gastroenterology 2013, 145:591-601.
19. De Cruz P., Prideaux L., Wagner J., et al. Characterization of the gastrointestinal microbiota in health and inflammatory bowel disease. Inflamm. Bowel Dis. 2012, 18:372-390.
20. Huttenhower C., Kostic A.D., Xavier R.J. Inflammatory bowel disease as a model for translating the microbiome. Immunity 2014, 40:843-854.
21. Cao Y., Shen J., Ran Z.H. Association between Faecalibacterium prausnitzii reduction and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Gastroenterol. Res. Pract. 2014, 2014:872725.
22. Taurog J.D., Richardson J.A., Croft J.T., et al. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J. Exp. Med. 1994, 180:2359-2364.
23. Dieleman L.A., Goerres M.S., Arends A., et al. Lactobacillus GG prevents recurrence of colitis in HLA-B27 transgenic rats after antibiotic treatment. Gut 2003, 52:370-376.
24. Sinkorova Z., Capkova J., Niederlova J., et al. Commensal intestinal bacterial strains trigger ankylosing enthesopathy of the ankle in inbred B10.BR (H-2(k)) male mice. Hum. Immunol. 2008, 69:845-850.
25. Rehaume L.M., Mondot S., Aguirre de Carcer D., et al. ZAP-70 genotype disrupts the relationship between microbiota and host, leading to spondyloarthritis and ileitis in SKG mice. Arthritis Rheum. 2014, 66:2780-2792.
26. Garrett W.S., Lord G.M., Punit S., et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007, 131:33-45.
27. Stebbings S., Munro K., Simon M.A., et al. Comparison of the faecal microflora of patients with ankylosing spondylitis and controls using molecular methods of analysis. Rheumatology (Oxford) 2002, 41:1395-1401.
28. Metzker M.L. Sequencing technologies - the next generation. Nat. Rev. Genet. 2010, 11:31-46.
29. Stoll M.L., Kumar R., Morrow C.D., et al. Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis. Arthritis Res. Ther. 2014, 16:486.
30. Costello M.E., Ciccia F., Willner D., et al. Intestinal dysbiosis in ankylosing spondylitis. Arthritis Rheum. 2014, (epub ahead of print).
31. Sokol H., Pigneur B., Watterlot L., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16731-16736.
32. Hold G.L., Schwiertz A., Aminov R.I., et al. Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl. Environ. Microbiol. 2003, 69:4320-4324.
33. Hamer H.M., Jonkers D., Venema K., et al. Review article: the role of butyrate on colonic function. Aliment. Pharmacol. Ther. 2008, 27:104-119.
34. Segain J.P., Raingeard de la Bletiere D., Bourreille A., et al. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 2000, 47:397-403.
35. Smith P.M., Howitt M.R., Panikov N., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013, 341:569-573.
36. Rath H.C., Herfarth H.H., Ikeda J.S., et al. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J. Clin. Invest. 1996, 98:945-953.
37. Prindiville T.P., Sheikh R.A., Cohen S.H., et al. Bacteroides fragilis enterotoxin gene sequences in patients with inflammatory bowel disease. Emerg. Infect. Dis. 2000, 6:171-174.
38. Salyers A.A., Vercellotti J.R., West S.E., et al. Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl. Environ. Microbiol. 1977, 33:319-322.
39. Derrien M., Vaughan E.E., Plugge C.M., et al. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 2004, 54:1469-1476.
40. Martinez-Gonzalez O., Cantero-Hinojosa J., Paule-Sastre P., et al. Intestinal permeability in patients with ankylosing spondylitis and their healthy relatives. Br. J. Rheumatol. 1994, 33:644-647.
41. Hollander D., Vadheim C.M., Brettholz E., et al. Increased intestinal permeability in patients with Crohn's disease and their relatives. A possible etiologic factor. Ann. Intern. Med. 1986, 105:883-885.
42. Rosenbaum J.T., Lin P., Asquith M., et al. Does the microbiome play a causal role in spondyloarthritis?. Clin. Rheumatol. 2014, 33:763-767.
43. Scher J.U., Ubeda C., Artacho A., et al. Decreased bacterial diversity characterizes an altered gut microbiota in psoriatic arthritis and resembles dysbiosis of inflammatory bowel disease. Arthritis Rheum. 2015, 67(1):128-139.
44. Castelino M., Eyre S., Upton M., et al. The bacterial skin microbiome in psoriatic arthritis, an unexplored link in pathogenesis: challenges and opportunities offered by recent technological advances. Rheumatology (Oxford) 2014, 53:777-784.
45. Caporaso J.G., Lauber C.L., Walters W.A., et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(Suppl. 1):4516-4522.
46. Hugot J.P., Chamaillard M., Zouali H., et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001, 411:599-603.
47. Biswas A., Petnicki-Ocwieja T., Kobayashi K.S. Nod2: a key regulator linking microbiota to intestinal mucosal immunity. J. Mol. Med. (Berl.) 2012, 90:15-24.
48. Strober W., Asano N., Fuss I., et al. Cellular and molecular mechanisms underlying NOD2 risk-associated polymorphisms in Crohn's disease. Immunol. Rev. 2014, 260:249-260.
49. Laukens D., Peeters H., Marichal D., et al. CARD15 gene polymorphisms in patients with spondyloarthropathies identify a specific phenotype previously related to Crohn's disease. Ann. Rheum. Dis. 2005, 64:930-935.
50. Cypers H., Van Praet L., Varkas G., et al. Relevance of the gut/joint axis for the management of spondyloarthritis in daily clinical practice. Curr. Opin. Rheumatol. 2014, 26:371-376.
51. Inman R.D., El-Gabalawy H.S. The immunology of ankylosing spondylitis and rheumatoid arthritis: a tale of similarities and dissimilarities. Clin. Exp. Rheumatol. 2009, 27:S26-S32.
52. Lodes M.J., Cong Y., Elson C.O., et al. Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Invest. 2004, 113:1296-1306.
53. Targan S.R., Landers C.J., Yang H., et al. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease. Gastroenterology 2005, 128:2020-2028.
54. Plevy S., Silverberg M.S., Lockton S., et al. Combined serological, genetic, and inflammatory markers differentiate non-IBD, Crohn's disease, and ulcerative colitis patients. Inflamm. Bowel Dis. 2013, 19:1139-1148.
55. Alexander K.L., Targan S.R., Elson C.O. Microbiota activation and regulation of innate and adaptive immunity. Immunol. Rev. 2014, 260:206-220.
56. Torok H.P., Glas J., Gruber R., et al. Inflammatory bowel disease-specific autoantibodies in HLA-B27-associated spondyloarthropathies: increased prevalence of ASCA and pANCA. Digestion 2004, 70:49-54.
57. Hoffman I.E., Demetter P., Peeters M., et al. Anti-saccharomyces cerevisiae IgA antibodies are raised in ankylosing spondylitis and undifferentiated spondyloarthropathy. Ann. Rheum. Dis. 2003, 62:455-459.
58. Aydin S.Z., Atagunduz P., Temel M., et al. Anti-Saccharomyces cerevisiae antibodies (ASCA) in spondyloarthropathies: a reassessment. Rheumatology (Oxford) 2008, 47:142-144.
59. Mundwiler M.L., Mei L., Landers C.J., et al. Inflammatory bowel disease serologies in ankylosing spondylitis patients: a pilot study. Arthritis Res. Ther. 2009, 11:R177.
60. Wallis D., Asaduzzaman A., Weisman M., et al. Elevated serum anti-flagellin antibodies implicate subclinical bowel inflammation in ankylosing spondylitis: an observational study. Arthritis Res. Ther. 2013, 15:R166.
61. Riente L., Chimenti D., Pratesi F., et al. Antibodies to tissue transglutaminase and Saccharomyces cerevisiae in ankylosing spondylitis and psoriatic arthritis. J. Rheumatol. 2004, 31:920-924.
62. Baeten D., Kruithof E., Breban M., et al. Spondylarthritis in the absence of B lymphocytes. Arthritis Rheum. 2008, 58:730-733.
63. Ng S.C., Kamm M.A., Stagg A.J., et al. Intestinal dendritic cells: their role in bacterial recognition, lymphocyte homing, and intestinal inflammation. Inflamm. Bowel Dis. 2010, 16:1787-1807.
64. Goto Y., Panea C., Nakato G., et al. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity 2014, 40:594-607.
65. Devlin S.M., Yang H., Ippoliti A., et al. NOD2 variants and antibody response to microbial antigens in Crohn's disease patients and their unaffected relatives. Gastroenterology 2007, 132:576-586.
66. Duchmann R., Kaiser I., Hermann E., et al. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin. Exp. Immunol. 1995, 102:448-455.
67. Cong Y., Weaver C.T., Lazenby A., et al. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J. Immunol. 2002, 169:6112-6119.
68. Feng T., Qin H., Wang L., et al. Th17 cells induce colitis and promote Th1 cell responses through IL-17 induction of innate IL-12 and IL-23 production. J. Immunol. 2011, 186:6313-6318.
69. Taurog J.D., Dorris M.L., Satumtira N., et al. Spondylarthritis in HLA-B27/human beta2-microglobulin-transgenic rats is not prevented by lack of CD8. Arthritis Rheum. 2009, 60:1977-1984.
70. Breban M., Fernandez-Sueiro J.L., Richardson J.A., et al. T cells, but not thymic exposure to HLA-B27, are required for the inflammatory disease of HLA-B27 transgenic rats. J. Immunol. 1996, 156:794-803.
71. Jacques P., Lambrecht S., Verheugen E., et al. Proof of concept: enthesitis and new bone formation in spondyloarthritis are driven by mechanical strain and stromal cells. Ann. Rheum. Dis. 2014, 73:437-445.
72. Saxena S., Aggarwal A., Misra R. Outer membrane protein of salmonella is the major antigenic target in patients with salmonella induced reactive arthritis. J. Rheumatol. 2005, 32:86-92.
73. Singh Y.P., Singh A.K., Aggarwal A., 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. J. Rheumatol. 2011, 38:161-166.
74. Sinha R., Aggarwal A., Prasad K., et al. Sporadic enteric reactive arthritis and undifferentiated spondyloarthropathy: evidence for involvement of Salmonella typhimurium. J. Rheumatol. 2003, 30:105-113.
75. Stebbings S.M., Taylor C., Tannock G.W., et al. The immune response to autologous bacteroides in ankylosing spondylitis is characterized by reduced interleukin 10 production. J. Rheumatol. 2009, 36:797-800.
76. Syrbe U., Scheer R., Wu P., et al. Differential synovial Th1 cell reactivity towards Escherichia coli antigens in patients with ankylosing spondylitis and rheumatoid arthritis. Ann. Rheum. Dis. 2012, 71:1573-1576.
77. Brooke B.N. Outcome of surgery for ulcerative colitis. Lancet 1956, 271:532-536.
78. Carter J.D., Espinoza L.R., Inman R.D., et al. Combination antibiotics as a treatment for chronic Chlamydia-induced reactive arthritis: a double-blind, placebo-controlled, prospective trial. Arthritis Rheum. 2010, 62:1298-1307.
79. Barber C.E., Kim J., Inman R.D., et al. Antibiotics for treatment of reactive arthritis: a systematic review and metaanalysis. J. Rheumatol. 2013, 40:916-928.
80. Jenks K., Stebbings S., Burton J., et al. Probiotic therapy for the treatment of spondyloarthritis: a randomized controlled trial. J. Rheumatol. 2010, 37:2118-2125.
81. Wu G.D., Chen J., Hoffmann C., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011, 334:105-108.
82. Soo J., Malik B.A., Turner J.M., et al. Use of exclusive enteral nutrition is just as effective as corticosteroids in newly diagnosed pediatric Crohn's disease. Dig. Dis. Sci. 2013, 58:3584-3591.
83. Sigall-Boneh R., Pfeffer-Gik T., Segal I., et al. Partial enteral nutrition with a Crohn's disease exclusion diet is effective for induction of remission in children and young adults with Crohn's disease. Inflamm. Bowel Dis. 2014, 20(8):1353-1360.
84. Cameron F.L., Gerasimidis K., Papangelou A., et al. Clinical progress in the two years following a course of exclusive enteral nutrition in 109 paediatric patients with Crohn's disease. Aliment. Pharmacol. Ther. 2013, 37:622-629.
85. Leach S.T., Mitchell H.M., Eng W.R., et al. Sustained modulation of intestinal bacteria by exclusive enteral nutrition used to treat children with Crohn's disease. Aliment. Pharmacol. Ther. 2008, 28:724-733.
86. Lionetti P., Callegari M.L., Ferrari S., et al. Enteral nutrition and microflora in pediatric Crohn's disease. JPEN J. Parenter. Enteral Nutr. 2005, 29:S173-S175. (discussion S175-178, S184-178).
87. Tjellstrom B., Hogberg L., Stenhammar L., et al. Effect of exclusive enteral nutrition on gut microflora function in children with Crohn's disease. Scand. J. Gastroenterol. 2012, 47:1454-1459.
88. Austin M., Mellow M., Tierney W.M. Fecal microbiota transplantation in the treatment of Clostridium difficile infections. Am. J. Med. 2014, 127:479-483.
89. Kosiewicz M.M., Dryden G.W., Chhabra A., et al. Relationship between gut microbiota and development of T cell associated disease. FEBS Lett. 2014, 588:4195-4206.
90. Suskind D.L., Brittnacher M.J., Wahbeh G., et al. Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn's disease. Inflamm. Bowel Dis. 2015, 21:556-563.
91. Rossen N.G., Fuentes S., van der Spek M.J., et al. Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology 2015, (epub ahead of print).