Microbiome and mucosal inflammation as extra-articular triggers for rheumatoid arthritis and autoimmunity

Current Opinion in Rheumatology

Volumn 26, Issue 1, 2014, Pages 101-107

  Brusca, Samuel B ^a   Abramson, Steven B ^a   Scher, Jose U ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

arthritis; microbiome; peridontal; Porphyromonas; rheumatoid

Indexed keywords

C REACTIVE PROTEIN; HLA B27 ANTIGEN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR;

AUTOIMMUNITY; COMPUTER ASSISTED TOMOGRAPHY; DISEASE ASSOCIATION; ENTERITIS; ERYTHROCYTE SEDIMENTATION RATE; FECES MICROFLORA; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; LACTOBACILLUS SALIVARIUS; LUNG PARENCHYMA; MICROBIAL COMMUNITY; MICROBIOME; MUCOSA INFLAMMATION; NONHUMAN; PARTICULATE MATTER; PERIODONTAL DISEASE; PERIODONTIUM; POINT MUTATION; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; REVIEW; RHEUMATOID ARTHRITIS; SMOKING; SPONDYLOARTHROPATHY; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, BACTERIAL; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; AUTOIMMUNITY; DISEASE MODELS, ANIMAL; DYSBIOSIS; HUMANS; INFLAMMATION; MICE; MICROBIOTA; MUCOUS MEMBRANE; PERIODONTAL DISEASES;

EID: 84890211295     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0000000000000008     Document Type: Review

References (63)

1. Bäckhed F, Ley RE, Sonnenburg JL, et al. Host-bacterial mutualism in the human intestine. Science 2005; 307:1915-1920.
2. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002; 22:283-307.
3. Zoetendal EG, Akkermans ADL, Vos WMD. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 1998; 64:3854-3859.
4. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464:59-65.
5. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486:207-214.
6. Scher JU, Abramson SB. The microbiome and rheumatoid arthritis. Nat Rev Rheumatol 2011; 7:569-578.
7. Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science 2005; 308:1635-1638.
8. Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature 2011; 473:174-180.
9. Koren O, Knights D, Gonzalez A, et al. A guide to enterotypes across the human body: Meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol 2013; 9:e1002863.
10. Gregersen PK, Silver J, Winchester RJ. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum 1987; 30:1205-1213.
11. Eyre S, Bowes J, Diogo D, et al. High-density genetic mapping identifies new susceptibility loci for rheumatoid arthritis. Nat Genet 2012; 44:1336-1340.
12. Nielen MMJ, van Schaardenburg D, Reesink HW, et al. Specific autoantibodies precede the symptoms of rheumatoid arthritis: A study of serial measurements in blood donors. Arthritis Rheum 2004; 50:380-386.
13. Sokolove J, Bromberg R, Deane KD, et al. Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS One 2012; 7:e35296.
14. Van de Sande MGH, de Hair MJH, van der Leij C, et al. Different stages of rheumatoid arthritis: Features of the synovium in the preclinical phase. Ann Rheum Dis 2011; 70:772-777.
15. Kohashi O, Kuwata J, Umehara K, et al. Susceptibility to adjuvant-induced arthritis among germfree, specific-pathogen-free, and conventional rats. Infect Immun 1979; 26:791-794.
16. Van den Broek MF, van Bruggen MC, Koopman JP, et al. Gut flora induces and maintains resistance against streptococcal cell wall-induced arthritis in F344 rats. Clin Exp Immunol 1992; 88:313-317.
17. Taurog JD, Richardson JA, Croft JT, 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.
18. DeLay ML, Turner MJ, Klenk EI, et al. HLA-B27 misfolding and the unfolded protein response augment IL-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum 2009; 60:2633-2643.
19. Utriainen L, Firmin D, Wright P, et al. Expression of HLA-B27 causes loss of migratory dendritic cells in a rat model of spondyloarthritis. Arthritis Rheum 2012; 64:3199-3209.
20. Abdollahi-Roodsaz S, Joosten LAB, Koenders MI, et al. Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J Clin Invest 2008; 118:205-216.
21. Wu H-J, Ivanov II, Darce J, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010; 32:815-827.
22. Yoshitomi H, Sakaguchi N, Kobayashi K, et al. A role for fungal b-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med 2005; 201:949-960.
23. Wu D, Liu X, Su H, et al. Oral antigens induce rheumatoid arthritis-like inflammation in a rat model. Inflamm Res 2013; 62:291-297.
24. Gomez A, Luckey D, Yeoman CJ, et al. Loss of sex and age driven differences in the gut microbiome characterize arthritis-susceptible -0401 mice but not arthritis-resistant -0402 mice. PLoS One 2012; 7. Available from http:// www.ncbi.nlm.nih.gov/pmc/articles/PMC3338357/. [Cited 13 April 2013].
25. Vaahtovuo J, Munukka E, Korkeamäki M, et al. Fecal microbiota in early rheumatoid arthritis. J Rheumatol 2008; 35:1500-1505.
26. Liu X, Zou Q, Zeng B, et al. Analysis of fecal lactobacillus community structure in patients with early rheumatoid arthritis. Curr Microbiol 2013; 67:170-176.
27. Elinav E, Strowig T, Kau AL, et al. NLRP6 inflammasome is a regulator of colonic microbial ecology and risk for colitis. Cell 2011; 145:745-757.
28. Koeth RA, Wang Z, Levison BS, et al. Intestinal microbiota metabolism of Lcarnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 2013; 19:576-585.
29. Kawar N, Gajendrareddy PK, Hart TC, et al. Periodontal disease for the primary care physician. Dis Mon 2011; 57:174-183.
30. Liao F, Li Z, Wang Y, et al. Porphyromonas gingivalis may play an important role in the pathogenesis of periodontitis-associated rheumatoid arthritis. Med Hypotheses 2009; 72:732-735.
31. Berthelot J-M, Le Goff B. Rheumatoid arthritis and periodontal disease. Joint Bone Spine 2010; 77:537-541.
32. De Pablo P, Dietrich T, McAlindon TE. Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol 2008; 35:70-76.
33. Potikuri D, Dannana KC, Kanchinadam S, et al. Periodontal disease is significantly higher in nonsmoking treatment-naive rheumatoid arthritis patients: Results from a case-control study. Ann Rheum Dis 2012; 71:1541-1544.
34. Pischon N, Pischon T, Krö ger J, et al. Association among rheumatoid arthritis, oral hygiene, and periodontitis. J Periodontol 2008; 79:979-986.
35. Chen H-H, Huang N, Chen Y-M, et al. Association between a history of periodontitis and the risk of rheumatoid arthritis: A nationwide, populationbased, case-control study. Ann Rheum Dis 2013; 72:1206-1211.
36. Arkema EV, Karlson EW, Costenbader KH. A prospective study of periodontal disease and risk of rheumatoid arthritis. J Rheumatol 2010; 37:1800-1804.
37. Erciyas K, Sezer U, Üstün K, et al. Effects of periodontal therapy on disease activity and systemic inflammation in rheumatoid arthritis patients. Oral Dis 2013; 19:394-400.
38. Biyikoǧ lu B, Buduneli N, Aksu K, et al. Periodontal therapy in chronic periodontitis lowers gingival crevicular fluid interleukin-1beta and DAS28 in rheumatoid arthritis patients. Rheumatol Int 2013; 33:2607-2616.
39. Savioli C, Ribeiro ACM, Fabri GMC, et al. Persistent periodontal disease hampers anti-tumor necrosis factor treatment response in rheumatoid arthritis. J Clin Rheumatol 2012; 18:180-184.
40. Dewhirst FE, Chen T, Izard J, et al. The human oral microbiome. J Bacteriol 2010; 192:5002-5017.
41. Wade WG. The oral microbiome in health and disease. Pharmacol Res 2013; 69:137-143.
42. Kumar PS, Griffen AL, Barton JA, et al. New bacterial species associated with chronic periodontitis. J Dent Res 2003; 82:338-344.
43. Bizzarro S, Loos BG, Laine ML, et al. Subgingival microbiome in smokers and nonsmokers in periodontitis: An exploratory study using traditional targeted techniques and a next-generation sequencing. J Clin Periodontol 2013; 40:483-492.
44. McGraw WT, Potempa J, Farley D, Travis J. Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidyl arginine deiminase. Infect Immun 1999; 67:3248-3256.
45. Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G. Hypothesis: The humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation 2004; 28:311-318.
46. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011; 365:2205-2219.
47. Barra L, Scinocca M, Saunders S, et al. Anti-citrullinated protein antibodies in unaffected first-degree relatives of rheumatoid arthritis patients. Arthritis Rheum 2013; 65:1439-1447.
48. Wegner N, Wait R, Sroka A, et al. Peptidyl arginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and a-enolase: Implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 2010; 62:2662- 2672.
49. Kinloch AJ, Alzabin S, Brintnell W, et al. Immunization with Porphyromonas gingivalis enolase induces autoimmunity to mammalian a-enolase and arthritis in DR4-IE-transgenic mice. Arthritis Rheum 2011; 63:3818-3823.
50. Okada M, Kobayashi T, Ito S, et al. Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol 2013; 1-12.
51. Mikuls TR, Payne JB, Reinhardt RA, et al. Antibody responses to Porphyromonas gingivalis (P. gingivalis) in subjects with rheumatoid arthritis and periodontitis. Int Immunopharmacol 2009; 9:38-42.
52. Mikuls TR, Thiele GM, Deane KD, et al. Porphyromonas gingivalis and disease-related autoantibodies in individuals at increased risk of rheumatoid arthritis. Arthritis Rheum 2012; 64:3522-3530.
53. Hitchon CA, Chandad F, Ferucci ED, et al. Antibodies to Porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol2010; 37:1105-1112.
54. Scher JU, Ubeda C, Equinda M, et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum2012; 64:3083-3094.
55. Morris A, Beck JM, Schloss PD, et al. Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am J Respir Crit Care Med 2013; 187:1067-1075.
56. Erb-Downward JR, Thompson DL, Han MK, et al. Analysis of the lung microbiome in the 'Healthy' smoker and in COPD. PLoS One 2011; 6:e16384.
57. Hilty M, Burke C, Pedro H, et al. Disordered microbial communities in asthmatic airways. PLoS One 2010; 5:e8578.
58. Segal LN, Alekseyenko AV, Clemente JC, et al. Enrichment of lung microbiome with supraglottic taxa is associated with increased pulmonary inflammation. Microbiome 2013; 1:19.
59. Makrygiannakis D, Hermansson M, Ulfgren A-K, et al. Smoking increases peptidyl arginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann Rheum Dis 2008; 67:1488-1492.
60. Kochi Y, Thabet MM, Suzuki A, et al. PADI4 polymorphism predisposes male smokers to rheumatoid arthritis. Ann Rheum Dis 2011; 70:512-515.
61. Gan RW, Deane KD, Zerbe GO, et al. Relationship between air pollution and positivity of RA-related autoantibodies in individuals without established RA: A report on SERA. Ann Rheum Dis 2013; 72:2002-2005.
62. Demoruelle MK, Weisman MH, Simonian PL, et al. Brief report: Airways abnormalities and rheumatoid arthritis-related autoantibodies in subjects without arthritis: Early injury or initiating site of autoimmunity? Arthritis Rheum 2012; 64:1756-1761.
63. Willis VC, Demoruelle MK, Derber LA, et al. Sputa autoantibodies in patients with established rheumatoid arthritis and subjects at-risk for future clinically apparent disease. Arthritis Rheum 2013; 65:2545-2554.