Immunomodulation in human and experimental arthritis: Including vitamin D, helminths and heat-shock proteins

Lupus

Volumn 23, Issue 6, 2014, Pages 577-587

  Ishikawa, Llw ^a   Shoenfeld, Y ^b   Sartori, A ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b SHEBA MEDICAL CENTER   (Israel)

Author keywords

dendritic cells; heat shock proteins; helminths; regulatory T cells; Rheumatoid arthritis; vitamin D

Indexed keywords

HEAT SHOCK PROTEIN; VITAMIN D;

ARTICLE; DENDRITIC CELL; EXPERIMENTAL ARTHRITIS; EXPERIMENTAL MODEL; HELMINTH; HUMAN; IMMUNOMODULATION; IMMUNOPATHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; ANIMAL; AUTOIMMUNITY; HOST PARASITE INTERACTION; IMMUNOLOGY; METABOLISM; PARASITOLOGY;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; AUTOIMMUNITY; DENDRITIC CELLS; HEAT-SHOCK PROTEINS; HELMINTHS; HOST-PARASITE INTERACTIONS; HUMANS; T-LYMPHOCYTES, REGULATORY; VITAMIN D;

EID: 84899556034     PISSN: 09612033     EISSN: 14770962     Source Type: Journal    
DOI: 10.1177/0961203314527369     Document Type: Article

References (123)

1. Weyand CM. Immunopathologic aspects of rheumatoid arthritis: Who is the conductor and who plays the immunologic instrument?. J Rheumatol Suppl. 2007 ; 79: 9-14
2. Klareskog L, Malmström V, Lundberg K, Padyukov L, Alfredsson L. Smoking, citrullination and genetic variability in the immunopathogenesis of rheumatoid arthritis. Semin Immunol. 2011 ; 23: 92-98
3. Imboden JB. The immunopathogenesis of rheumatoid arthritis. Annu Rev Pathol. 2009 ; 4: 417-434
4. Young A, Koduri G. Extra-articular manifestations and complications of rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2007 ; 21: 907-927
5. Van den Berg WB. Lessons from animal models of arthritis over the past decade. Arthritis Res Ther. 2009 ; 11: 250-250
6. Bolon B, Stolina M, King C, et al. Rodent preclinical models for developing novel antiarthritic molecules: Comparative biology and preferred methods for evaluating efficacy. J Biomed Biotechnol. 2011 ; 2011: 569068-569068
7. Bläss S, Engel JM, Burmester GR. The immunologic homunculus in rheumatoid arthritis. A new viewpoint of immunopathogenesis in rheumatoid arthritis and therapeutic consequences [article in German]. Z Rheumatol. 2001 ; 60: 1-16
8. Lundberg K, Nijenhuis S, Vossenaar ER, et al. Citrullinated proteins have increased immunogenicity and arthritogenicity and their presence in arthritic joints correlates with disease severity. Arthritis Res Ther. 2005 ; 7: 458-467
9. Ho PP, Lee LY, Zhao X, et al. Autoimmunity against fibrinogen mediates inflammatory arthritis in mice. J Immunol. 2010 ; 184: 379-390
10. Sokolove J, Zhao X, Chandra PE, Robinson WH. Immune complexes containing citrullinated fibrinogen costimulate macrophages via Toll-like receptor 4 and Fcγ receptor. Arthritis Rheum. 2011 ; 63: 53-62
11. Uysal H, Bockermann R, Nandakumar KS, et al. Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis. J Exp Med. 2009 ; 206: 449-462
12. Perricone C, Ceccarelli F, Valesini G. An overview on the genetic of rheumatoid arthritis: A never-ending story. Autoimmun Rev. 2011 ; 10: 599-608
13. Rieck M, Arechiga A, Onengut-Gumuscu S, Greenbaum C, Concannon P, Buckner JH. Genetic variation in PTPN22 corresponds to altered function of T and B lymphocytes. J Immunol. 2007 ; 179: 4704-4710
14. Sakaguchi N, Takahashi T, Hata H, et al. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature. 2003 ; 426: 454-460
15. Meron MK, Amital H, Shepshelovich D, et al. Infectious aspects and the etiopathogenesis of rheumatoid arthritis. Clin Rev Allergy Immunol. 2010 ; 38: 287-291
16. Balandraud N, Meynard JB, Auger I, et al. Epstein-Barr virus load in the peripheral blood of patients with rheumatoid arthritis: Accurate quantification using real-time polymerase chain reaction. Arthritis Rheum. 2003 ; 48: 1223-1228
17. Saal JG, Steidle M, Einsele H, et al. Persistence of B19 parvovirus in synovial membranes of patients with rheumatoid arthritis. Rheumatol Int. 1992 ; 12: 147-151
18. Kuwana Y, Takei M, Yajima M, et al. Epstein-Barr virus induces erosive arthritis in humanized mice. PLoS One. 2011 ; 6: e26630 - e26630
19. Cantley MD, Haynes DR, Marino V, et al. Pre-existing periodontitis exacerbates experimental arthritis in a mouse model. J Clin Periodontol. 2011 ; 38: 532-541
20. Hoovestol RA, Mikuls TR. Environmental exposures and rheumatoid arthritis risk. Curr Rheumatol Rep. 2011 ; 13: 431-439
21. Yu H, Yang YH, Rajaiah R, et al. Nicotine-induced differential modulation of autoimmune arthritis in the Lewis rat involves changes in interleukin-17 and anti-cyclic citrullinated peptide antibodies. Arthritis Rheum. 2011 ; 63: 981-991
22. van der Heijden IM, Wilbrink B, Tchetverikov I, et al. Presence of bacterial DNA and bacterial peptidoglycans in joints of patients with rheumatoid arthritis and other arthritides. Arthritis Rheum. 2000 ; 43: 593-598
23. Lee EK, Kang SM, Paik DJ, Kim JM, Youn J. Essential roles of Toll-like receptor-4 signaling in arthritis induced by type II collagen antibody and LPS. Int Immunol. 2005 ; 17: 325-333
24. Meng L, Zhu W, Jiang C, et al. Toll-like receptor 3 upregulation in macrophages participates in the initiation and maintenance of pristane-induced arthritis in rats. Arthritis Res Ther. 2010 ; 12: R103 - R103
25. Segal B, Rhodus NL, Patel K. Tumor necrosis factor (TNF) inhibitor therapy for rheumatoid arthritis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008 ; 106: 778-787
26. Notley CA, Inglis JJ, Alzabin S, McCann FE, McNamee KE, Williams RO. Blockade of tumor necrosis factor in collagen-induced arthritis reveals a novel immunoregulatory pathway for Th1 and Th17 cells. J Exp Med. 2008 ; 205: 2491-2497
27. Carvalheiro HM, da Silva JA, Souto-Carneiro MM. Potential roles for CD8(+) T cells in rheumatoid arthritis. Autoimmun Rev. 2013 ; 12: 401-409
28. Gaffen SL. The role of interleukin-17 in the pathogenesis of rheumatoid arthritis. Curr Rheumatol Rep. 2009 ; 11: 365-370
29. Lundy SK, Sarkar S, Tesmer LA, Fox DA. Cells of the synovium in rheumatoid arthritis. T lymphocytes. Arthritis Res Ther. 2007 ; 9: 202-202
30. Sato K, Suematsu A, Okamoto K, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med. 2006 ; 203: 2673-2682
31. Dong W, Zhu P. Functional niche of inflamed synovium for Th17-cell expansion and activation in rheumatoid arthritis: Implication to clinical therapeutics. Autoimmun Rev. 2012 ; 11: 844-851
32. Isomaki P, Luukkainen R, Saario R, Toivanen P, Punnonen J. Interleukin-10 functions as an antiinflammatory cytokine in rheumatoid synovium. Arthritis Rheum. 1996 ; 39: 386-395
33. Moura RA, Graca L, Fonseca JE. To B or not to B the conductor of rheumatoid arthritis orchestra. Clin Rev Allergy Immunol. 2012 ; 43: 281-291
34. Boissier MC, Assier E, Biton J, Denys A, Falgarone G, Bessis N. Regulatory T cells (Treg) in rheumatoid arthritis. Joint Bone Spine. 2009 ; 76: 10-14
35. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003 ; 4: 330-336
36. Frey O, Petrow PK, Gajda M, et al. The role of regulatory T cells in antigen-induced arthritis: Aggravation of arthritis after depletion and amelioration after transfer of CD4+CD25+ T cells. Arthritis Res Ther. 2005 ; 7: 291-301
37. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 2006 ; 441: 235-238
38. Lee YK, Mukasa R, Hatton RD, Weaver CT. Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol. 2009 ; 21: 274-280
39. Ehrenstein MR, Evans JG, Singh A, et al. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med. 2004 ; 200: 277-285
40. Hamel KM, Cao Y, Ashaye S, et al. B cell depletion enhances T regulatory cell activity essential in the suppression of arthritis. J Immunol. 2011 ; 187: 4900-4906
41. McGovern JL, Nguyen DX, Notley CA, Mauri C, Isenberg DA, Ehrenstein MR. Th17 cells are restrained by Treg cells via the inhibition of interleukin-6 in patients with rheumatoid arthritis responding to anti-tumor necrosis factor antibody therapy. Arthritis Rheum. 2012 ; 64: 3129-3138
42. Urry Z, Chambers ES, Xystrakis E, et al. The role of 1α,25- dihydroxyvitamin D3 and cytokines in the promotion of distinct Foxp3+ and IL-10+ CD4+ T cells. Eur J Immunol. 2012 ; 42: 2697-2708
43. Strauss L, Whiteside TL, Knights A, Bergmann C, Knuth A, Zippelius A. Selective survival of naturally occurring human CD4+CD25+Foxp3+ regulatory T cells cultured with rapamycin. J Immunol. 2007 ; 178: 320-329
44. Kessel A, Ammuri H, Peri R, et al. Intravenous immunoglobulin therapy affects T regulatory cells by increasing their suppressive function. J Immunol. 2007 ; 179: 5571-5575
45. Cao T, Wenzel SE, Faubion WA, Harriman G, Li L. Enhanced suppressive function of regulatory T cells from patients with immune-mediated diseases following successful ex vivo expansion. Clin Immunol. 2010 ; 136: 329-337
46. Xu W, Roos A, Daha MR, van Kooten C. Dendritic cell and macrophage subsets in the handling of dying cells. Immunobiology. 2006 ; 211: 567-575
47. Morelli AE, Larregina AT, Shufesky WJ, et al. Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: Dependence on complement receptors and effect on cytokine production. Blood. 2003 ; 101: 611-620
48. Stuart LM, Lucas M, Simpson C, Lamb J, Savill J, Lacy-Hulbert A. Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J Immunol. 2002 ; 168: 1627-1635
49. Vosters O, Nève J, de Wit D, Willems F, Goldman M, Verhasselt V. Dendritic cells exposed to nacystelyn are refractory to maturation and promote the emergence of alloreactive regulatory T cells. Transplantation. 2003 ; 75: 383-389
50. Torres-Aguilar H, Aguilar-Ruiz SR, González-Pérez G, et al. Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J Immunol. 2010 ; 184: 1765-1775
51. Zhao Y, Zhang A, Du H, Guo S, Ning B, Yang S. Tolerogenic dendritic cells and rheumatoid arthritis: Current status and perspectives. Rheumatol Int. 2012 ; 32: 837-844
52. Zanetti M, Castiglioni P, Schoenberger S, Gerloni M. The role of relB in regulating the adaptive immune response. Ann N Y Acad Sci. 2003 ; 987: 249-257
53. Zhu YB, Kang K, Zhang Y, et al. PLD1 negatively regulates dendritic branching. J Neurosci. 2012 ; 32: 7960-7969
54. Kabalak G, Dobberstein SB, Matthias T, et al. Association of immunoglobulin-like transcript 6 deficiency with Sjögren's syndrome. Arthritis Rheum. 2009 ; 60: 2923-2925
55. Criado G, Simelyte E, Inglis JJ, Essex D, Williams RO. Indoleamine 2,3 dioxygenase-mediated tryptophan catabolism regulates accumulation of Th1/Th17 cells in the joint in collagen-induced arthritis. Arthritis Rheum. 2009 ; 60: 1342-1351
56. Marin-Gallen S, Clemente-Casares X, Planas R, et al. Dendritic cells pulsed with antigen-specific apoptotic bodies prevent experimental type 1 diabetes. Clin Exp Immunol. 2010 ; 160: 207-214
57. Steinman RM, Turley S, Mellman I, Inaba K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med. 2000 ; 191: 411-416
58. Kushwah R, Wu J, Oliver JR, et al. Uptake of apoptotic DC converts immature DC into tolerogenic DC that induce differentiation of Foxp3+ Treg. Eur J Immunol. 2010 ; 40: 1022-1035
59. Humbert JM, Halary F. Viral and non-viral methods to genetically modify dendritic cells. Curr Gene Ther. 2012 ; 12: 127-136
60. Henry E, Desmet CJ, Garzé V, et al. Dendritic cells genetically engineered to express IL-10 induce long-lasting antigen-specific tolerance in experimental asthma. J Immunol. 2008 ; 181: 7230-7242
61. Li R, Zheng X, Popov I, et al. Gene silencing of IL-12 in dendritic cells inhibits autoimmune arthritis. J Transl Med. 2012 ; 10: 19-19
62. Misaki K, Morinobu A, Saegusa J, et al. Histone deacetylase inhibition alters dendritic cells to assume a tolerogenic phenotype and ameliorates arthritis in SKG mice. Arthritis Res Ther. 2011 ; 13: R77 - R77
63. Stoop JN, Harry RA, Von Delwig A, Isaacs JD, Robinson JH, Hilkens CM. Therapeutic effect of tolerogenic dendritic cells in established collagen-induced arthritis is associated with a reduction in Th17 responses. Arthritis Rheum. 2010 ; 62: 3656-3665
64. Zheng X, Suzuki M, Ichim TE, et al. Treatment of autoimmune arthritis using RNA interference-modulated dendritic cells. J Immunol. 2010 ; 184: 6457-6464
65. Ko HJ, Cho ML, Lee SY, et al. CTLA4-Ig modifies dendritic cells from mice with collagen-induced arthritis to increase the CD4+CD25+Foxp3+ regulatory T cell population. J Autoimmun. 2010 ; 34: 111-120
66. Brown AJ, Ritter CS. The vitamin D analog 1α,25-dihydroxy-2β- (3-hydroxypropyloxy) vitamin D(3) (eldecalcitol) is a potent regulator of calcium and phosphate metabolism. Calcif Tissue Int. 2011 ; 89: 372-378
67. Deluca HF, Cantorna MT. Vitamin D: Its role and uses in immunology. FASEB J. 2001 ; 15: 2579-2585
68. van Etten E, Mathieu C. Immunoregulation by 1,25-dihydroxyvitamin D3: Basic concepts. J Steroid Biochem Mol Biol. 2005 ; 97: 93-101
69. Boonstra A, Barrat FJ, Crain C, Heath VL, Savelkoul HF, O'Garra A. 1alpha,25-dihydroxyvitamin d3 has a direct effect on naive CD4(+) T cells to enhance the development of Th2 cells. J Immunol. 2001 ; 167: 4974-4980
70. Staeva-Vieira TP, Freedman LP. 1,25-dihydroxyvitamin D3 inhibits IFN-gamma and IL-4 levels during in vitro polarization of primary murine CD4+ T cells. J Immunol. 2002 ; 168: 1181-1189
71. Penna G, Amuchastegui S, Laverny G, Adorini L. Vitamin D receptor agonists in the treatment of autoimmune diseases: Selective targeting of myeloid but not plasmacytoid dendritic cells. J Bone Miner Res. 2007 ; 22: 69-73
72. Chambers ES, Hawrylowicz CM. The impact of vitamin D on regulatory T cells. Curr Allergy Asthma Rep. 2011 ; 11: 29-36
73. Souberbielle JC, Body JJ, Lappe JM, et al. Vitamin D and musculoskeletal health, cardiovascular disease, autoimmunity and cancer. Recommendations for clinical practice. Autoimmun Rev. 2010 ; 9: 709-715
74. Agmon-Levin N, Theodor E, Segal RM, Shoenfeld Y. Vitamin D in systemic and organ-specific autoimmune diseases. Clinic Rev Allerg Immunol. 2012 ; 45: 265-266
75. Petriková J, Lazúrová I, Shoenfeld Y. Polycystic ovary syndrome and autoimmunity. Eur J Intern Med. 2010 ; 21: 369-371
76. Shapira Y, Agmon-Levin N, Shoenfeld Y. Mycobacterium tuberculosis, autoimmunity, and vitamin D. Clin Rev Allerg Immunol. 2010 ; 38: 169-177
77. Orbach H, Zandman-Goddard G, Amital H, et al. Novel biomarkers in autoimmune diseases. Prolactin, ferritin, vitamin D and TPA levels in autoimmune diseases. Ann NY Acad Sci. 2007 ; 1109: 385-400
78. Shoenfeld N, Amital H, Shoenfeld Y. The effect of melanism and vitamin D synthesis on the incidence of autoimmune disease. Nature Clin Pract Rheumatol. 2009 ; 5: 99-105
79. Amital H, Szekanecz Z, Szücs G, et al. Serum concentrations of 25-OH vitamin D in patients with systemic lupus erythematosus (SLE) are inversely related to disease activity: Is it time to routinely supplement patients with SLE with vitamin D?. Ann Rheum Dis. 2010 ; 69: 1155-1157
80. Hajas A, Sandor J, Casathy L, et al. Vitamin D insufficiency in a large MCTD population. Autoimmun Rev. 2011 ; 10: 317-324
81. Cantorna MT, Hayes CE, Deluca HF. 1,25-dihydroxycholecalciferol inhibits the progression of arthritis in murine models of human arthritis. J Nutr. 1998 ; 128: 68-72
82. Gregori S, Giarratana N, Smiroldo S, Uskokovic M, Adorini L. A 1alpha,25-dihydroxyvitamin D(3) analog enhances regulatory T-cells and arrests autoimmune diabetes in NOD mice. Diabetes. 2002 ; 51: 1367-1374
83. Pedersen AE, Gad M, Walter MR, Claesson MH. Induction of regulatory dendritic cells by dexamethasone and 1alpha,25-dihydroxyvitamin D(3). Immunol Lett. 2004 ; 91: 63-69
84. Arnson Y, Amital H, Shoenfeld Y. Vitamin D and autoimmunity: New etiological and therapeutical considerations. Ann Rheum Dis. 2007 ; 66: 1137-1142
85. Oren Y, Shapira Y, Agmon-Levin N, et al. Vitamin D insufficiency in a sunny environment: A demographic and seasonal analysis. Isr Med Assoc J. 2010 ; 12: 751-756
86. Antico A, Tampoia M, Tozzoli R, Bizzaro N. Can supplementation with vitamin D reduce the risk or modify the course of autoimmune diseases? A systematic review of the literature. Autoimmun Rev. 2012 ; 12: 127-136
87. Okada H, Kuhn C, Feillet H, Bach JF. The 'hygiene hypothesis' for autoimmune and allergic diseases: An update. Clin Exp Immunol. 2010 ; 160: 1-9
88. Kivity S, Agmon-Levin N, Blank M, Shoenfeld Y. Infections and autoimmunity - friends or foes?. Trends Immunol. 2009 ; 30: 409-414
89. Rook GA. The hygiene hypothesis and the increasing prevalence of chronic inflammatory disorders. Trans R Soc Trop Med Hyg. 2007 ; 101: 1072-1074
90. Shor DB, Shoenfeld Y. Will worms cure rheumatoid arthritis?. Nature Rev Rheumatol. 2013 ; 9: 138-140
91. McInnes IB, Leung BP, Harnett M, Gracie JA, Liew FY, Harnett W. A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. J Immunol. 2003 ; 171: 2127-2133
92. Harnett MM, Kean DE, Boitelle A, et al. The phosphorycholine moiety of the filarial nematode immunomodulator ES-62 is responsible for its anti-inflammatory action in arthritis. Ann Rheum Dis. 2008 ; 67: 518-523
93. Grundtman C, Kreutmayer SB, Almanzar G, Wick MC, Wick G. Heat shock protein 60 and immune inflammatory responses in atherosclerosis. Arterioscler Thromb Vasc Biol. 2011 ; 31: 960-968
94. Jones DB, Coulson AF, Duff GW. Sequence homologies between hsp60 and autoantigens. Immunol Today. 1993 ; 14: 115-118
95. van Eden W, Wick G, Albani S, Cohen I. Stress, heat shock proteins, and autoimmunity: How immune responses to heat shock proteins are to be used for the control of chronic inflammatory diseases. Ann N Y Acad Sci. 2007 ; 1113: 217-237
96. Coelho V, Broere F, Binder RJ, Shoenfeld Y, Moudgil K. Heat-shock proteins: Inflammatory versus regulatory attributes. Cell Stress Chaperones. 2008 ; 13: 119-125
97. Sherer Y, Gerli R, Bocci EB, et al. Heat-shock protein 65 autoantibodies are differently associated with early atherosclerosis in rheumatoid arthritis and in healthy subjects. Ann N Y Acad Sci. 2007 ; 1108: 408-413
98. Coelho V, Faria AM. HSP60: Issues and insights on its therapeutic use as an immunoregulatory agent. Front Immunol. 2011 ; 2: 97-97
99. Huang MN, Yu H, Moudgil KD. The involvement of heat-shock proteins in the pathogenesis of autoimmune arthritis: A critical appraisal. Semin Arthritis Rheum. 2010 ; 40: 164-175
100. Anderton SM, van der Zee R, Prakken B, Noordzij A, van Eden W. Activation of T cells recognizing self 60-kD heat shock protein can protect against experimental arthritis. J Exp Med. 1995 ; 181: 943-952
101. Prakken BJ, Wendling U, van der Zee R, Rutten VP, Kuis W, van Eden W. Induction of IL-10 and inhibition of experimental arthritis are specific features of microbial heat shock proteins that are absent for other evolutionarily conserved immunodominant proteins. J Immunol. 2001 ; 167: 4147-4153
102. Nishikawa H, Kato T, Tawara I, et al. Definition of target antigens for naturally occurring CD4(+) CD25(+) regulatory T cells. J Exp Med. 2005 ; 201: 681-686
103. Ohue R, Hashimoto K, Nakamoto M, et al. Bacterial heat shock protein 60, GroEL, can induce the conversion of naïve T cells into a CD4 CD25(+) Foxp3-expressing phenotype. Immunol. 2001 ; 167: 4147-4153
104. Zonneveld-Huijssoon E, Roord ST, De Jager W, et al. Bystander suppression of experimental arthritis by nasal administration of a heat shock protein peptide. Ann Rheum Dis. 2011 ; 70: 2199-2206
105. Dominguez Mdel C, Lorenzo N, Barbera A, et al. An altered peptide ligand corresponding to a novel epitope from heat-shock protein 60 induces regulatory T cells and suppresses pathogenic response in an animal model of adjuvant-induced arthritis. Autoimmunity. 2011 ; 44: 471-482
106. Santos-Junior RR, Sartori A, De Franco M, et al. Immunomodulation and protection induced by DNA-hsp65 vaccination in an animal model of arthritis. Hum Gene Ther. 2005 ; 6: 1338-1345
107. Burkart V, Germaschewski L, Schloot NC, Bellmann K, Kolb H. Deficient heat shock protein 70 response to stress in leukocytes at onset of type 1 diabetes. Biochem Biophys Res Commun. 2008 ; 369: 421-425
108. Wieten L, van der Zee R, Spiering R, et al. A novel heat-shock protein coinducer boosts stress protein Hsp70 to activate T cell regulation of inflammation in autoimmune arthritis. Arthritis Rheum. 2010 ; 62: 1026-1035
109. Zanin-Zhorov A, Cahalon L, Tal G, Margalit R, Lider O, Cohen IR. Heat shock protein 60 enhances CD4+ CD25+ regulatory T cell function via innate TLR2 signaling. J Clin Invest. 2006 ; 116: 2022-2032
110. Frisenda S, Perricone C, Valesini G. Cartilage as a target of autoimmunity: A thin layer. Autoimmun Rev. 2013 ; 12: 591-598
111. Hu Y, Cheng W, Cai W, Yue Y, Li J, Zhang P. Advances in research on animal models of rheumatoid arthritis. Clin Rheumatol. 2013 ; 32: 161-165
112. Eyles JL, Hickey MJ, Norman MU, et al. A key role for G-CSF-induced neutrophil production and trafficking during inflammatory arthritis. Blood. 2008 ; 112: 5193-5201
113. Abdollahi-Roodsaz S, Joosten LA, Roelofs MF, et al. Inhibition of Toll-like receptor 4 breaks the inflammatory loop in autoimmune destructive arthritis. Arthritis Rheum. 2007 ; 56: 2957-2967
114. Kidd BA, Ho PP, Sharpe O, et al. Epitope spreading to citrullinated antigens in mouse models of autoimmune arthritis and demyelination. Arthritis Res Ther. 2008 ; 10: R119 - R119
115. Joosten LA, Abdollahi-Roodsaz S, Heuvelmans-Jacobs M, et al. T cell dependence of chronic destructive murine arthritis induced by repeated local activation of Toll-like receptor-driven pathways: Crucial role of both interleukin-1beta and interleukin-17. Arthritis Rheum. 2008 ; 58: 98-108
116. Perruche S, Saas P, Chen W. Apoptotic cell-mediated suppression of streptococcal cell wall-induced arthritis is associated with alteration of macrophage function and local regulatory T-cell increase: A potential cell-based therapy?. Arthritis Res Ther. 2009 ; 11: R104 - R104
117. Sun X, Liu YH, Lv ZY, et al. rSj16, a recombinant protein of Schistosoma japonicum-derived molecule, reduces severity of the complete Freund's adjuvant-induced adjuvant arthritis in rats' model. Parasite Immunol. 2010 ; 32: 739-748
118. Chujo S, Okamoto S, Sunahara R, et al. Cigarette smoke condensate extracts augment collagen-induced arthritis in mice. Int Immunopharmacol. 2010 ; 10: 1194-1199
119. Telekes A, Resetar A, Balint G, et al. Fermented wheat germ extract (avemar) inhibits adjuvant arthritis. Ann N Y Acad Sci. 2007 ; 1110: 348-361
120. Williams RO. Collagen-induced arthritis in mice. Methods Mol Med. 2007 ; 136: 191-199
121. Holmdahl R, Lorentzen JC, Lu S, et al. Arthritis induced in rats with nonimmunogenic adjuvants as models for rheumatoid arthritis. Immunol Rev. 2001 ; 184: 184-202
122. Lee TP, Chiang BL. Sex differences in spontaneous versus induced animal models of autoimmunity. Autoimmun Rev. 2011 ; 11: 422-429
123. Glant TT, Mikecz K. Proteoglycan aggrecan-induced arthritis: A murine autoimmune model of rheumatoid arthritis. Methods Mol Med. 2004 ; 102: 313-338