Toll-like receptor mediated modulation of T cell response by commensal intestinal microbiota as a trigger for autoimmune arthritis

Journal of Immunology Research

Volumn 2015, Issue , 2015, Pages

  Rogier, Rebecca ^a   Koenders, Marije I ^a   Abdollahi Roodsaz, Shahla ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

TOLL LIKE RECEPTOR; BACTERIAL ANTIGEN; PROTEIN BINDING;

AUTOIMMUNE ARTHRITIS; AUTOIMMUNE DISEASE; COMMENSAL; ENVIRONMENTAL FACTOR; GENETIC PREDISPOSITION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INTESTINE FLORA; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL; ANIMAL; ARTHRITIS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, BACTERIAL; ARTHRITIS; ARTHRITIS, RHEUMATOID; AUTOIMMUNE DISEASES; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNOMODULATION; INTESTINAL MUCOSA; PROTEIN BINDING; T-LYMPHOCYTE SUBSETS; TH17 CELLS; TOLL-LIKE RECEPTORS;

EID: 84924529833     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2015/527696     Document Type: Review

References (186)

1. G. S. Firestein, "Evolving concepts of rheumatoid arthritis," Nature, Vol. 423, no. 6937, pp. 356-361, 2003.
2. D. van der Woude and T. W. J. Huizinga, "Translating basic research into clinical rheumatology," Best Practice and Research: Clinical Rheumatology, Vol. 22, no. 2, pp. 299-310, 2008.
3. E. Lubberts, "Th17 cytokines and arthritis," Seminars in Immunopathology, Vol. 32, no. 1, pp. 43-53, 2010.
4. S. K. Lundy, S. Sarkar, L. A. Tesmer, and D. A. Fox, "Cells of the synovium in rheumatoid arthritis. T lymphocytes," Arthritis Research and Therapy, Vol. 9, no. 1, article 202, 2007.
5. S. L. Gafen, "The role of interleukin-17 in the pathogenesis of rheumatoid arthritis," Current Rheumatology Reports, Vol. 11, no. 5, pp. 365-370, 2009.
6. W. B. van den Berg and P. Miossec, "IL-17 as a future therapeutic target for rheumatoid arthritis," Nature Reviews Rheumatology, Vol. 5, no. 10, pp. 549-553, 2009.
7. L. Klareskog, L. Padyukov, J. Rönnelid, and L. Alfredsson, "Genes, environment and immunity in the development of rheumatoid arthritis," Current Opinion in Immunology, Vol. 18, no. 6, pp. 650-655, 2006.
8. A. K. Andersson, C. Li, and F. M. Brennan, "Recent developments in the immunobiology of rheumatoid arthritis," Arthritis Research and Therapy, Vol. 10, no. 2, article 204, 2008.
9. D. Sugiyama, K. Nishimura, K. Tamaki et al., "Impact of smoking as a risk factor for developing rheumatoid arthritis: a meta-analysis of observational studies," Annals of the Rheumatic Diseases, Vol. 69, no. 1, pp. 70-81, 2010.
10. J. U. Scher, C. Ubeda, M. Equinda et al., "Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis," Arthritis and Rheumatism, Vol. 64, no. 10, pp. 3083-3094, 2012.
11. S. G. de Aquino, S. Abdollahi-Roodsaz, M. I. Koenders et al., "Periodontal pathogens directly promote autoimmune experimental arthritis by inducing a TLR2- and IL-1-Driven Th17 Response," Journal of Immunology, Vol. 192, no. 9, pp. 4103-4111, 2014.
12. J. U. Scher and S. B. Abramson, "The microbiome and rheumatoid arthritis," Nature Reviews Rheumatology, Vol. 7, no. 10, pp. 569-578, 2011.
13. S. Abdollahi-Roodsaz, L. A. B. Joosten, M. I. Koenders et al., "Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis," The Journal of Clinical Investigation, Vol. 118, no. 1, pp. 205-216, 2008.
14. S. Abdollahi-Roodsaz, M. I. Koenders, B. Walgreen et al., "Tolllike receptor 2 controls acute immune complex-driven arthritis in mice by regulating the inhibitory Fcγ receptor IIB," Arthritis and Rheumatism, Vol. 65, no. 10, pp. 2583-2593, 2013.
15. S. Abdollahi-Roodsaz, F. A. J. van de Loo, and W. B. van den Berg, "Trapped in a vicious loop: toll-like receptors sustain the spontaneous cytokine production by rheumatoid synovium," Arthritis Research and Therapy, Vol. 13, no. 2, article 105, 2011.
16. A. Ruyssen-Witrand, A. Constantin, A. Cambon-Thomsen, and M. Thomsen, "New insights into the genetics of immune responses in rheumatoid arthritis," Tissue Antigens, Vol. 80, no. 2, pp. 105-118, 2012.
17. D. Matusevicius, P. Kivisäkk, B. He et al., "Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis," Multiple Sclerosis, Vol. 5, no. 2, pp. 101-104, 1999.
18. V. Hölttä, P. Klemetti, H. M. Salo et al., "Interleukin-17 immunity in pediatric crohn disease and ulcerative colitis," Journal of Pediatric Gastroenterology and Nutrition, Vol. 57, no. 3, pp. 287-292, 2013.
19. S. Fujino, A. Andoh, S. Bamba et al., "Increased expression of interleukin 17 in inflammatory bowel disease," Gut, Vol. 52, no. 1, pp. 65-70, 2003.
20. M. Veny, M. Esteller, E. Ricart, J. M. Pique, J. Panes, and A. Salas, "Late crohn's disease patients present an increase in peripheral Th17 cells and cytokine production compared with early patients," Alimentary Pharmacology & Therapeutics, Vol. 31, no. 5, pp. 561-572, 2010.
21. M. Merle Elloso, M. Gomez-Angelats, and A. M. Fourie, "Targeting the th17 pathway in psoriasis," Journal of Leukocyte Biology, Vol. 92, no. 6, pp. 1187-1197, 2012.
22. J. P. van Hamburg, P. S. Asmawidjaja, N. Davelaar et al., "Th17 cells, but not Th1 cells, from patients with early rheumatoid arthritis are potent inducers of matrix metalloproteinases and proinflammatory cytokines upon synovial fibroblast interaction, including autocrine interleukin-17A production," Arthritis and Rheumatism, Vol. 63, no. 1, pp. 73-83, 2011.
23. P. Miossec, T. Korn, and V. K. Kuchroo, "Interleukin-17 and type 17 helper T cells," The New England Journal of Medicine, Vol. 361, no. 9, pp. 888-898, 2009.
24. M. Samson, S. Audia, N. Janikashvili et al., "Brief report: inhibition of interleukin-6 function corrects Th17/Treg cell imbalance in patients with rheumatoid arthritis," Arthritis and Rheumatism, Vol. 64, no. 8, pp. 2499-2503, 2012.
25. W. Wang, S. Shao, Z. Jiao, M. Guo, H. Xu, and S. Wang, "The Th17/Treg imbalance and cytokine environment in peripheral blood of patients with rheumatoid arthritis," Rheumatology International, Vol. 32, no. 4, pp. 887-893, 2012.
26. A. Zanin-Zhorov, Y. Ding, S. Kumari et al., "Protein kinase C-θ mediates negative feedback on regulatory T cell function," Science, Vol. 328, no. 5976, pp. 372-376, 2010.
27. + regulatory T cells," Immunological Reviews, Vol. 212, pp. 60-73, 2006.
28. T. Korn, E. Bettelli, W. Gao et al., "IL-21 initiates an alternative pathway to induce proinflammatory T H17 cells," Nature, Vol. 448, no. 7152, pp. 484-487, 2007.
29. D. M. Roeleveld, A. E. M. van Nieuwenhuijze, W. B. van den Berg, and M. I. Koenders, "The Th17 pathway as a therapeutic target in rheumatoid arthritis and other autoimmune and inflammatory disorders," BioDrugs, Vol. 27, no. 5, pp. 439-452, 2013.
30. A. J. Macpherson and N. L. Harris, "Interactions between commensal intestinal bacteria and the immune system," Nature Reviews Immunology, Vol. 4, no. 6, pp. 478-485, 2004.
31. A. J. Macpherson, M. B. Geuking, and K. D. McCoy, "Immune responses that adapt the intestinal mucosa to commensal intestinal bacteria," Immunology, Vol. 115, no. 2, pp. 153-162, 2005.
32. S. K. Mazmanian, H. L. Cui, A. O. Tzianabos, and D. L. Kasper, "An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system," Cell, Vol. 122, no. 1, pp. 107-118, 2005.
33. I. I. Ivanov, K. Atarashi, N. Manel et al., "Induction of intestinal Th17 cells by segmented filamentous bacteria," Cell, Vol. 139, no. 3, pp. 485-498, 2009.
34. Y. K. Lee, J. S. Menezes, Y. Umesaki, and S. K. Mazmanian, "Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis," Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, supplement 1, pp. 4615-4622, 2011.
35. + T cells," inflammatory Bowel Diseases, Vol. 13, no. 10, pp. 1202-1211, 2007.
36. H. J. Wu, I. I. Ivanov, J. Darce et al., "Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells," Immunity, Vol. 32, no. 6, pp. 815-827, 2010.
37. J. L. Round and S. K. Mazmanian, "Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota," Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, no. 27, pp. 12204-12209, 2010.
38. J. Ochoa-Repáraz, D. W. Mielcarz, Y. Wang et al., "A polysaccha-ride from the human commensal Bacteroides fragilis protects against CNS demyelinating disease," Mucosal Immunology, Vol. 3, no. 5, pp. 487-495, 2010.
39. K. Atarashi, T. Tanoue, T. Shima et al., "Induction of colonic regulatory T cells by indigenous Clostridium species," Science, Vol. 331, no. 6015, pp. 337-341, 2011.
40. A. M. Morton, E. Sefik, R. Upadhyay, R. Weissleder, C. Benoist, and D. Mathis, "Endoscopic photoconversion reveals unexpectedly broad leukocyte traficking to and from the gut," Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, no. 18, pp. 6696-6701, 2014.
41. N. Cerf-Bensussan and V. Gaboriau-Routhiau, "The immune system and the gut microbiota: friends or foes?" Nature Reviews Immunology, Vol. 10, no. 10, pp. 735-744, 2010.
42. M. Stone, P. R. Fortin, C. Pacheco-Tena, and R. D. Inman, "Should tetracycline treatment be used more extensively for rheumatoid arthritis? Metaanalysis demonstrates clinical ben-efit with reduction in disease activity," Journal of Rheumatology, Vol. 30, no. 10, pp. 2112-2122, 2003.
43. P. Hannonen, T. Mottonen, M. Hakola, and M. Oka, "Sul-fasalazine in early rheumatoid arthritis: a 48-week doubleblind, prospective, placebo-controlled study," Arthritis and Rheumatism, Vol. 36, no. 11, pp. 1501-1509, 1993.
44. J. Vaahtovuo, E. Munukka, M. Korkeamäki, R. Luukkainen, and P. Toivanen, "Fecal microbiota in early rheumatoid arthritis," Journal of Rheumatology, Vol. 35, no. 8, pp. 1500-1505, 2008.
45. J. U. Scher, A. Sczesnak, R. S. Longman et al., "Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis," eLife, Vol. 2013, no. 2, Article ID e01202, 2013.
46. X. Liu, Q. Zou, B. Zeng, Y. Fang, and H. Wei, "Analysis of fecal lactobacillus community structure in patients with early rheumatoid arthritis," Current Microbiology, Vol. 67, no. 2, pp. 170-176, 2013.
47. S. Hida, N. N. Miura, Y. Adachi, and N. Ohno, "Cell wall β-glucan derived from Candida albicans acts as a trigger for autoimmune arthritis in SKG mice," Biological and Pharmaceutical Bulletin, Vol. 30, no. 8, pp. 1589-1592, 2007.
48. I. Dorozyńska, M. Majewska-Szczepanik, and K. Marcińska, "Partial depletion of natural gut flora by antibiotic aggravates collagen induced arthritis (CIA) in mice," Pharmacological Reports, Vol. 66, no. 2, pp. 250-255, 2014.
49. R. Horai, S. Saijo, H. Tanioka et al., "Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin I receptor antagonist-deficient mice," Journal of Experimental Medicine, Vol. 191, no. 2, pp. 313-320, 2000.
50. N. Sakaguchi, T. Takahashi, H. Hata et al., "Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice," Nature, Vol. 426, no. 6965, pp. 454-460, 2003.
51. A. Didierlaurent, M. Simonet, and J.-C. Sirard, "Innate and acquired plasticity of the intestinal immune system," Cellular and Molecular Life Sciences, Vol. 62, no. 12, pp. 1285-1287, 2005.
52. H. Kumar, T. Kawai, and S. Akira, "Pathogen recognition by the innate immune system," International Reviews of Immunology, Vol. 30, no. 1, pp. 16-34, 2011.
53. P. A. Hopkins and S. Sriskandan, "Mammalian toll-like receptors: to immunity and beyond," Clinical and Experimental Immunology, Vol. 140, no. 3, pp. 395-407, 2005.
54. C. Pasare and R. Medzhitov, "Toll-like receptors and acquired immunity," Seminars in Immunology, Vol. 16, no. 1, pp. 23-26, 2004.
55. A. M. Krieg, "CpG motifs in bacterial DNA and their immune effects," Annual Review of Immunology, Vol. 20, pp. 709-760, 2002.
56. F. Re and J. L. Strominger, "Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells," The Journal of Biological Chemistry, Vol. 276, no. 40, pp. 37692-37699, 2001.
57. C. Reis E Sousa, S. Hieny, T. Scharton-Kersten et al., "In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas," Journal of Experimental Medicine, Vol. 186, no. 11, pp. 1819-1829, 1997.
58. G. Trinchieri, "Interleukin-12 and the regulation of innate resistance and adaptive immunity," Nature Reviews Immunology, Vol. 3, no. 2, pp. 133-146, 2003.
59. S. Agrawal, A. Agrawal, B. Doughty et al., "Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct T responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos," The Journal of Immunology, Vol. 171, no. 10, pp. 4984-4989, 2003.
60. S. Dillon, A. Agrawal, T. Van Dyke et al., "A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells," Journal of Immunology, Vol. 172, no. 8, pp. 4733-4743, 2004.
61. V. Redecke, H. Häcker, S. K. Datta et al., "Cutting edge: activation of Toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma," Journal of Immunology, Vol. 172, no. 5, pp. 2739-2743, 2004.
62. M. G. Kattah, M. T. Wong, M. D. Yocum, and P. J. Utz, "Cytokines secreted in response to toll-like receptor ligand stimulation modulate differentiation of human Th17 cells," Arthritis and Rheumatism, Vol. 58, no. 6, pp. 1619-1629, 2008.
63. M. Veldhoen, R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger, "TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells," Immunity, Vol. 24, no. 2, pp. 179-189, 2006.
64. D. A. Piggott, S. C. Eisenbarth, L. Xu et al., "MyD88-dependent induction of allergic Th2 responses to intranasal antigen," The Journal of Clinical Investigation, Vol. 115, no. 2, pp. 459-467, 2005.
65. G. Caron, D. Duluc, I. Frémaux et al., "Direct stimulation of human T cells via TLR5 and TLR7/8: Flagellin and R-848 up-regulate proliferation and IFN-γ production by memory CD4+ T cells," Journal of Immunology, Vol. 175, no. 3, pp. 1551-1557, 2005.
66. D. Kabelitz, "Expression and function of Toll-like receptors in T lymphocytes," Current Opinion in Immunology, Vol. 19, no. 1, pp. 39-45, 2007
67. M. Komai-Koma, L. Jones, G. S. Ogg, D. Xu, and F. Y. Liew, "TLR2 is expressed activated T cells as a costimulatory receptor," Proceedings of the National Academy of Sciences of the United States of America, Vol. 101, no. 9, pp. 3029-3034, 2004.
68. + T cell survival," The Journal of Immunology, Vol. 172, no. 10, pp. 6065-6073, 2004.
69. F. Hu, Y L. Li, L. Zheng et al., "Toll-like receptors expressed by synovial fbroblasts perpetuate Th1 and th17 cell responses in rheumatoid arthritis," PLoS ONE, Vol. 9, no. 6, Article ID e100266, 2014.
70. J. H. Niess, S. Brand, X. Gu et al., "CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance," Science, Vol. 307, no. 5707, pp. 254-258, 2005.
71. C. C. Bain, C. L. Scott, H. Uronen-Hansson et al., "Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6C hi monocyte precursors," Mucosal Immunology, Vol. 6, no. 3, pp. 498-510, 2013.
72. +, antigen sampling cells migrate in lymph and serve classical dendritic cell functions," Journal of Experimental Medicine, Vol. 206, no. 13, pp. 3101-3114, 2009.
73. -dendritic cells migrate in lymph and prime effector T cells," Mucosal Immunology, Vol. 6, no. 1, pp. 104-113, 2013.
74. hi cells," Nature, Vol. 494, no. 7435, pp. 116-120, 2013.
75. A. T. Satpathy, C. G Briseno, J. S. Lee et al., "Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens," Nature Immunology, Vol. 14, no. 9, pp. 937-948, 2013.
76. + dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense," Immunity, Vol. 36, no. 2, pp. 276-287, 2012.
77. C. L. Scott, C. C. Bain, P. B. Wright et al., "CCR2CD103 intestinal dendritic cells develop from DC-committed precursors and induce interleukin-17 production by T cells," Mucosal Immunology. In press.
78. J. Farache, I. Koren, I. Milo et al., "Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation," Immunity, Vol. 38, no. 3, pp. 581-595, 2013.
79. T. Feng, Y Cong, K. Alexander, and C. O. Elson, "Regulation of Toll-like receptor 5 gene expression and function on mucosal dendritic cells," PLoS ONE, Vol. 7, no. 4, Article ID e35918, 2012.
80. + lamina propria dendritic cells in enterobacterial infection," Journal of Gastroenterology, Vol. 44, no. 8, pp. 803-811, 2009.
81. J. A. Hall, N. Bouladoux, C. M. Sun et al., "Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses," Immunity, Vol. 29, no. 4, pp. 637-649, 2008.
82. M. T. Abreu, "Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function," Nature Reviews Immunology, Vol. 10, no. 2, pp. 131-143, 2010.
83. A. Lundin, C. M. Bok, L. Aronsson et al., "Gut flora, Toll-like receptors and nuclear receptors: a tripartite communication that tunes innate immunity in large intestine," Cellular Microbiology, Vol. 10, no. 5, pp. 1093-1103, 2008.
84. h1-polarized regulatory or inflammatory type effector response in vitro," Immunobiology, Vol. 216, no. 4, pp. 518-527, 2011.
85. S. de Kivit, A. D. Kraneveld, L. M. J. Knippels, Y. van Kooyk, J. Garssen, and L. E. M. Willemsen, "Intestinal epithelium-derived galectin-9 is involved in the immunomodulating effects of nondigestible oligosaccharides," Journal of Innate Immunity, Vol. 5, no. 6, pp. 625-638, 2013.
86. X. Li, C. Wang, J. Nie, D. Lv, T. Wang, and Y. Xu, "Toll-like receptor 4 increases intestinal permeability through up-regulation of membrane PKC activity in alcoholic steatohepatitis," Alcohol, Vol. 47, no. 6, pp. 459-465, 2013.
87. E. Cario, G. Gerken, and D. K. Podolsky, "Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C," Gastroenterology, Vol. 127, no. 1, pp. 224-238, 2004.
88. A. Fasano, "Zonulin and its regulation of intestinal barrier function: The biological door to inflammation, autoimmunity, and cancer," Physiological Reviews, Vol. 91, no. 1, pp. 151-175, 2011.
89. A. Fasano, "Leaky gut and autoimmune diseases," Clinical Reviews in Allergy and Immunology, Vol. 42, no. 1, pp. 71-78, 2012.
90. J. L. Round, S. M. Lee, J. Li et al., "The toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota," Science, Vol. 332, no. 6032, pp. 974-977, 2011.
91. H. Shen, J. C. Goodall, and J. S. Hill Gaston, "Frequency and phenotype of peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid arthritis," Arthritis and Rheumatism, Vol. 60, no. 6, pp. 1647-1656, 2009.
92. Y. Goto, C. Panea, G. Nakato et al., "Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation," Immunity, Vol. 40, no. 4, pp. 594-607, 2014.
93. T. Kuwahara, Y. Ogura, K. Oshima et al., "The lifestyle of the segmented filamentous bacterium: a non-culturable gut-associated immunostimulating microbe inferred by whole-genome sequencing," DNA Research, Vol. 18, no. 4, pp. 291-303, 2011.
94. G. S. Firestein, "Evolving concepts of rheumatoid arthritis," Nature, Vol. 423, no. 6937, pp. 356-361, 2003.
95. D. van der Woude and T. W. J. Huizinga, "Translating basic research into clinical rheumatology," Best Practice and Research: Clinical Rheumatology, Vol. 22, no. 2, pp. 299-310, 2008.
96. E. Lubberts, "Th17 cytokines and arthritis," Seminars in Immunopathology, Vol. 32, no. 1, pp. 43-53, 2010.
97. S. K. Lundy, S. Sarkar, L. A. Tesmer, and D. A. Fox, "Cells of the synovium in rheumatoid arthritis. T lymphocytes," Arthritis Research and Therapy, Vol. 9, no. 1, article 202, 2007.
98. S. L. Gafen, "The role of interleukin-17 in the pathogenesis of rheumatoid arthritis," Current Rheumatology Reports, Vol. 11, no. 5, pp. 365-370, 2009.
99. W. B. van den Berg and P. Miossec, "IL-17 as a future therapeutic target for rheumatoid arthritis," Nature Reviews Rheumatology, Vol. 5, no. 10, pp. 549-553, 2009.
100. L. Klareskog, L. Padyukov, J. Rönnelid, and L. Alfredsson, "Genes, environment and immunity in the development of rheumatoid arthritis," Current Opinion in Immunology, Vol. 18, no. 6, pp. 650-655, 2006.
101. A. K. Andersson, C. Li, and F. M. Brennan, "Recent developments in the immunobiology of rheumatoid arthritis," Arthritis Research and Therapy, Vol. 10, no. 2, article 204, 2008.
102. D. Sugiyama, K. Nishimura, K. Tamaki et al., "Impact of smoking as a risk factor for developing rheumatoid arthritis: a meta-analysis of observational studies," Annals of the Rheumatic Diseases, Vol. 69, no. 1, pp. 70-81, 2010.
103. J. U. Scher, C. Ubeda, M. Equinda et al., "Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis," Arthritis and Rheumatism, Vol. 64, no. 10, pp. 3083-3094, 2012.
104. S. G. de Aquino, S. Abdollahi-Roodsaz, M. I. Koenders et al., "Periodontal pathogens directly promote autoimmune experimental arthritis by inducing a TLR2- and IL-1-Driven Th17 Response," Journal of Immunology, Vol. 192, no. 9, pp. 4103-4111, 2014.
105. J. U. Scher and S. B. Abramson, "The microbiome and rheumatoid arthritis," Nature Reviews Rheumatology, Vol. 7, no. 10, pp. 569-578, 2011.
106. S. Abdollahi-Roodsaz, L. A. B. Joosten, M. I. Koenders et al., "Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis," The Journal of Clinical Investigation, Vol. 118, no. 1, pp. 205-216, 2008.
107. S. Abdollahi-Roodsaz, M. I. Koenders, B. Walgreen et al., "Tolllike receptor 2 controls acute immune complex-driven arthritis in mice by regulating the inhibitory Fcγ receptor IIB," Arthritis and Rheumatism, Vol. 65, no. 10, pp. 2583-2593, 2013.
108. S. Abdollahi-Roodsaz, F. A. J. van de Loo, and W. B. van den Berg, "Trapped in a vicious loop: toll-like receptors sustain the spontaneous cytokine production by rheumatoid synovium," Arthritis Research and Therapy, Vol. 13, no. 2, article 105, 2011.
109. A. Ruyssen-Witrand, A. Constantin, A. Cambon-Thomsen, and M. Thomsen, "New insights into the genetics of immune responses in rheumatoid arthritis," Tissue Antigens, Vol. 80, no. 2, pp. 105-118, 2012.
110. D. Matusevicius, P. Kivisäkk, B. He et al., "Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis," Multiple Sclerosis, Vol. 5, no. 2, pp. 101-104, 1999.
111. V. Hölttä, P. Klemetti, H. M. Salo et al., "Interleukin-17 immunity in pediatric crohn disease and ulcerative colitis," Journal of Pediatric Gastroenterology and Nutrition, Vol. 57, no. 3, pp. 287-292, 2013.
112. S. Fujino, A. Andoh, S. Bamba et al., "Increased expression of interleukin 17 in inflammatory bowel disease," Gut, Vol. 52, no. 1, pp. 65-70, 2003.
113. M. Veny, M. Esteller, E. Ricart, J. M. Pique, J. Panes, and A. Salas, "Late crohn's disease patients present an increase in peripheral Th17 cells and cytokine production compared with early patients," Alimentary Pharmacology & Therapeutics, Vol. 31, no. 5, pp. 561-572, 2010.
114. M. Merle Elloso, M. Gomez-Angelats, and A. M. Fourie, "Targeting the th17 pathway in psoriasis," Journal of Leukocyte Biology, Vol. 92, no. 6, pp. 1187-1197, 2012.
115. J. P. van Hamburg, P. S. Asmawidjaja, N. Davelaar et al., "Th17 cells, but not Th1 cells, from patients with early rheumatoid arthritis are potent inducers of matrix metalloproteinases and proinflammatory cytokines upon synovial fibroblast interaction, including autocrine interleukin-17A production," Arthritis and Rheumatism, Vol. 63, no. 1, pp. 73-83, 2011.
116. P. Miossec, T. Korn, and V. K. Kuchroo, "Interleukin-17 and type 17 helper T cells," The New England Journal of Medicine, Vol. 361, no. 9, pp. 888-898, 2009.
117. M. Samson, S. Audia, N. Janikashvili et al., "Brief report: inhibition of interleukin-6 function corrects Th17/Treg cell imbalance in patients with rheumatoid arthritis," Arthritis and Rheumatism, Vol. 64, no. 8, pp. 2499-2503, 2012.
118. W. Wang, S. Shao, Z. Jiao, M. Guo, H. Xu, and S. Wang, "The Th17/Treg imbalance and cytokine environment in peripheral blood of patients with rheumatoid arthritis," Rheumatology International, Vol. 32, no. 4, pp. 887-893, 2012.
119. A. Zanin-Zhorov, Y. Ding, S. Kumari et al., "Protein kinase C-θ mediates negative feedback on regulatory T cell function," Science, Vol. 328, no. 5976, pp. 372-376, 2010.
120. + regulatory T cells," Immunological Reviews, Vol. 212, pp. 60-73, 2006.
121. T. Korn, E. Bettelli, W. Gao et al., "IL-21 initiates an alternative pathway to induce proinflammatory T H17 cells," Nature, Vol. 448, no. 7152, pp. 484-487, 2007.
122. D. M. Roeleveld, A. E. M. van Nieuwenhuijze, W. B. van den Berg, and M. I. Koenders, "The Th17 pathway as a therapeutic target in rheumatoid arthritis and other autoimmune and inflammatory disorders," BioDrugs, Vol. 27, no. 5, pp. 439-452, 2013.
123. A. J. Macpherson and N. L. Harris, "Interactions between commensal intestinal bacteria and the immune system," Nature Reviews Immunology, Vol. 4, no. 6, pp. 478-485, 2004.
124. A. J. Macpherson, M. B. Geuking, and K. D. McCoy, "Immune responses that adapt the intestinal mucosa to commensal intestinal bacteria," Immunology, Vol. 115, no. 2, pp. 153-162, 2005.
125. S. K. Mazmanian, H. L. Cui, A. O. Tzianabos, and D. L. Kasper, "An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system," Cell, Vol. 122, no. 1, pp. 107-118, 2005.
126. I. I. Ivanov, K. Atarashi, N. Manel et al., "Induction of intestinal Th17 cells by segmented filamentous bacteria," Cell, Vol. 139, no. 3, pp. 485-498, 2009.
127. Y. K. Lee, J. S. Menezes, Y. Umesaki, and S. K. Mazmanian, "Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis," Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, supplement 1, pp. 4615-4622, 2011.
128. + T cells," inflammatory Bowel Diseases, Vol. 13, no. 10, pp. 1202-1211, 2007.
129. H. J. Wu, I. I. Ivanov, J. Darce et al., "Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells," Immunity, Vol. 32, no. 6, pp. 815-827, 2010.
130. J. L. Round and S. K. Mazmanian, "Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota," Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, no. 27, pp. 12204-12209, 2010.
131. J. Ochoa-Repáraz, D. W. Mielcarz, Y. Wang et al., "A polysaccha-ride from the human commensal Bacteroides fragilis protects against CNS demyelinating disease," Mucosal Immunology, Vol. 3, no. 5, pp. 487-495, 2010.
132. K. Atarashi, T. Tanoue, T. Shima et al., "Induction of colonic regulatory T cells by indigenous Clostridium species," Science, Vol. 331, no. 6015, pp. 337-341, 2011.
133. A. M. Morton, E. Sefik, R. Upadhyay, R. Weissleder, C. Benoist, and D. Mathis, "Endoscopic photoconversion reveals unexpectedly broad leukocyte traficking to and from the gut," Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, no. 18, pp. 6696-6701, 2014.
134. N. Cerf-Bensussan and V. Gaboriau-Routhiau, "The immune system and the gut microbiota: friends or foes?" Nature Reviews Immunology, Vol. 10, no. 10, pp. 735-744, 2010.
135. M. Stone, P. R. Fortin, C. Pacheco-Tena, and R. D. Inman, "Should tetracycline treatment be used more extensively for rheumatoid arthritis? Metaanalysis demonstrates clinical ben-efit with reduction in disease activity," Journal of Rheumatology, Vol. 30, no. 10, pp. 2112-2122, 2003.
136. P. Hannonen, T. Mottonen, M. Hakola, and M. Oka, "Sul-fasalazine in early rheumatoid arthritis: a 48-week doubleblind, prospective, placebo-controlled study," Arthritis and Rheumatism, Vol. 36, no. 11, pp. 1501-1509, 1993.
137. J. Vaahtovuo, E. Munukka, M. Korkeamäki, R. Luukkainen, and P. Toivanen, "Fecal microbiota in early rheumatoid arthritis," Journal of Rheumatology, Vol. 35, no. 8, pp. 1500-1505, 2008.
138. J. U. Scher, A. Sczesnak, R. S. Longman et al., "Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis," eLife, Vol. 2013, no. 2, Article ID e01202, 2013.
139. X. Liu, Q. Zou, B. Zeng, Y. Fang, and H. Wei, "Analysis of fecal lactobacillus community structure in patients with early rheumatoid arthritis," Current Microbiology, Vol. 67, no. 2, pp. 170-176, 2013.
140. S. Hida, N. N. Miura, Y. Adachi, and N. Ohno, "Cell wall β-glucan derived from Candida albicans acts as a trigger for autoimmune arthritis in SKG mice," Biological and Pharmaceutical Bulletin, Vol. 30, no. 8, pp. 1589-1592, 2007.
141. I. Dorozyńska, M. Majewska-Szczepanik, and K. Marcińska, "Partial depletion of natural gut flora by antibiotic aggravates collagen induced arthritis (CIA) in mice," Pharmacological Reports, Vol. 66, no. 2, pp. 250-255, 2014.
142. R. Horai, S. Saijo, H. Tanioka et al., "Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin I receptor antagonist-deficient mice," Journal of Experimental Medicine, Vol. 191, no. 2, pp. 313-320, 2000.
143. N. Sakaguchi, T. Takahashi, H. Hata et al., "Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice," Nature, Vol. 426, no. 6965, pp. 454-460, 2003.
144. A. Didierlaurent, M. Simonet, and J.-C. Sirard, "Innate and acquired plasticity of the intestinal immune system," Cellular and Molecular Life Sciences, Vol. 62, no. 12, pp. 1285-1287, 2005.
145. H. Kumar, T. Kawai, and S. Akira, "Pathogen recognition by the innate immune system," International Reviews of Immunology, Vol. 30, no. 1, pp. 16-34, 2011.
146. P. A. Hopkins and S. Sriskandan, "Mammalian toll-like receptors: to immunity and beyond," Clinical and Experimental Immunology, Vol. 140, no. 3, pp. 395-407, 2005.
147. C. Pasare and R. Medzhitov, "Toll-like receptors and acquired immunity," Seminars in Immunology, Vol. 16, no. 1, pp. 23-26, 2004.
148. A. M. Krieg, "CpG motifs in bacterial DNA and their immune effects," Annual Review of Immunology, Vol. 20, pp. 709-760, 2002.
149. F. Re and J. L. Strominger, "Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells," The Journal of Biological Chemistry, Vol. 276, no. 40, pp. 37692-37699, 2001.
150. C. Reis E Sousa, S. Hieny, T. Scharton-Kersten et al., "In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas," Journal of Experimental Medicine, Vol. 186, no. 11, pp. 1819-1829, 1997.
151. G. Trinchieri, "Interleukin-12 and the regulation of innate resistance and adaptive immunity," Nature Reviews Immunology, Vol. 3, no. 2, pp. 133-146, 2003.
152. S. Agrawal, A. Agrawal, B. Doughty et al., "Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct T responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos," The Journal of Immunology, Vol. 171, no. 10, pp. 4984-4989, 2003.
153. S. Dillon, A. Agrawal, T. Van Dyke et al., "A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells," Journal of Immunology, Vol. 172, no. 8, pp. 4733-4743, 2004.
154. V. Redecke, H. Häcker, S. K. Datta et al., "Cutting edge: activation of Toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma," Journal of Immunology, Vol. 172, no. 5, pp. 2739-2743, 2004.
155. M. G. Kattah, M. T. Wong, M. D. Yocum, and P. J. Utz, "Cytokines secreted in response to toll-like receptor ligand stimulation modulate differentiation of human Th17 cells," Arthritis and Rheumatism, Vol. 58, no. 6, pp. 1619-1629, 2008.
156. M. Veldhoen, R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger, "TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells," Immunity, Vol. 24, no. 2, pp. 179-189, 2006.
157. D. A. Piggott, S. C. Eisenbarth, L. Xu et al., "MyD88-dependent induction of allergic Th2 responses to intranasal antigen," The Journal of Clinical Investigation, Vol. 115, no. 2, pp. 459-467, 2005.
158. G. Caron, D. Duluc, I. Frémaux et al., "Direct stimulation of human T cells via TLR5 and TLR7/8: Flagellin and R-848 up-regulate proliferation and IFN-γ production by memory CD4+ T cells," Journal of Immunology, Vol. 175, no. 3, pp. 1551-1557, 2005.
159. D. Kabelitz, "Expression and function of Toll-like receptors in T lymphocytes," Current Opinion in Immunology, Vol. 19, no. 1, pp. 39-45, 2007
160. M. Komai-Koma, L. Jones, G. S. Ogg, D. Xu, and F. Y. Liew, "TLR2 is expressed activated T cells as a costimulatory receptor," Proceedings of the National Academy of Sciences of the United States of America, Vol. 101, no. 9, pp. 3029-3034, 2004.
161. + T cell survival," The Journal of Immunology, Vol. 172, no. 10, pp. 6065-6073, 2004.
162. F. Hu, Y L. Li, L. Zheng et al., "Toll-like receptors expressed by synovial fbroblasts perpetuate Th1 and th17 cell responses in rheumatoid arthritis," PLoS ONE, Vol. 9, no. 6, Article ID e100266, 2014.
163. J. H. Niess, S. Brand, X. Gu et al., "CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance," Science, Vol. 307, no. 5707, pp. 254-258, 2005.
164. C. C. Bain, C. L. Scott, H. Uronen-Hansson et al., "Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6C hi monocyte precursors," Mucosal Immunology, Vol. 6, no. 3, pp. 498-510, 2013.
165. +, antigen sampling cells migrate in lymph and serve classical dendritic cell functions," Journal of Experimental Medicine, Vol. 206, no. 13, pp. 3101-3114, 2009.
166. -dendritic cells migrate in lymph and prime effector T cells," Mucosal Immunology, Vol. 6, no. 1, pp. 104-113, 2013.
167. hi cells," Nature, Vol. 494, no. 7435, pp. 116-120, 2013.
168. A. T. Satpathy, C. G Briseno, J. S. Lee et al., "Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens," Nature Immunology, Vol. 14, no. 9, pp. 937-948, 2013.
169. + dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense," Immunity, Vol. 36, no. 2, pp. 276-287, 2012.
170. C. L. Scott, C. C. Bain, P. B. Wright et al., "CCR2CD103 intestinal dendritic cells develop from DC-committed precursors and induce interleukin-17 production by T cells," Mucosal Immunology. In press.
171. J. Farache, I. Koren, I. Milo et al., "Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation," Immunity, Vol. 38, no. 3, pp. 581-595, 2013.
172. T. Feng, Y Cong, K. Alexander, and C. O. Elson, "Regulation of Toll-like receptor 5 gene expression and function on mucosal dendritic cells," PLoS ONE, Vol. 7, no. 4, Article ID e35918, 2012.
173. + lamina propria dendritic cells in enterobacterial infection," Journal of Gastroenterology, Vol. 44, no. 8, pp. 803-811, 2009.
174. J. A. Hall, N. Bouladoux, C. M. Sun et al., "Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses," Immunity, Vol. 29, no. 4, pp. 637-649, 2008.
175. M. T. Abreu, "Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function," Nature Reviews Immunology, Vol. 10, no. 2, pp. 131-143, 2010.
176. A. Lundin, C. M. Bok, L. Aronsson et al., "Gut flora, Toll-like receptors and nuclear receptors: a tripartite communication that tunes innate immunity in large intestine," Cellular Microbiology, Vol. 10, no. 5, pp. 1093-1103, 2008.
177. h1-polarized regulatory or inflammatory type effector response in vitro," Immunobiology, Vol. 216, no. 4, pp. 518-527, 2011.
178. S. de Kivit, A. D. Kraneveld, L. M. J. Knippels, Y. van Kooyk, J. Garssen, and L. E. M. Willemsen, "Intestinal epithelium-derived galectin-9 is involved in the immunomodulating effects of nondigestible oligosaccharides," Journal of Innate Immunity, Vol. 5, no. 6, pp. 625-638, 2013.
179. X. Li, C. Wang, J. Nie, D. Lv, T. Wang, and Y. Xu, "Toll-like receptor 4 increases intestinal permeability through up-regulation of membrane PKC activity in alcoholic steatohepatitis," Alcohol, Vol. 47, no. 6, pp. 459-465, 2013.
180. E. Cario, G. Gerken, and D. K. Podolsky, "Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C," Gastroenterology, Vol. 127, no. 1, pp. 224-238, 2004.
181. A. Fasano, "Zonulin and its regulation of intestinal barrier function: The biological door to inflammation, autoimmunity, and cancer," Physiological Reviews, Vol. 91, no. 1, pp. 151-175, 2011.
182. A. Fasano, "Leaky gut and autoimmune diseases," Clinical Reviews in Allergy and Immunology, Vol. 42, no. 1, pp. 71-78, 2012.
183. J. L. Round, S. M. Lee, J. Li et al., "The toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota," Science, Vol. 332, no. 6032, pp. 974-977, 2011.
184. H. Shen, J. C. Goodall, and J. S. Hill Gaston, "Frequency and phenotype of peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid arthritis," Arthritis and Rheumatism, Vol. 60, no. 6, pp. 1647-1656, 2009.
185. Y. Goto, C. Panea, G. Nakato et al., "Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation," Immunity, Vol. 40, no. 4, pp. 594-607, 2014.
186. T. Kuwahara, Y. Ogura, K. Oshima et al., "The lifestyle of the segmented filamentous bacterium: a non-culturable gut-associated immunostimulating microbe inferred by whole-genome sequencing," DNA Research, Vol. 18, no. 4, pp. 291-303, 2011.