Nicotine-induced differential modulation of autoimmune arthritis in the lewis rat involves changes in interleukin-17 and anti-cyclic citrullinated peptide antibodies

Arthritis and Rheumatism

Volumn 63, Issue 4, 2011, Pages 981-991

  Yu, Hua ^a   Yang, Ying Hua ^a   Rajaiah, Rajesh ^a   Moudgil, Kamal D ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC CITRULLINATED PEPTIDE ANTIBODY; HEAT SHOCK PROTEIN 65; INTERLEUKIN 17; NICOTINE TARTRATE;

ADJUVANT ARTHRITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; CELL DIVISION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DENDRITIC CELL; DISEASE SEVERITY; IMMUNOMODULATION; LYMPH NODE CELL; LYMPHOCYTE PROLIFERATION; MALE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; RAT; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; TH1 CELL; TH17 CELL;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; ARTHRITIS, EXPERIMENTAL; AUTOIMMUNE DISEASES; BACTERIAL PROTEINS; CELL PROLIFERATION; CHAPERONIN 60; DISEASE MODELS, ANIMAL; INTERLEUKIN-17; MALE; NICOTINE; PEPTIDES, CYCLIC; RATS; RATS, INBRED LEW; SEVERITY OF ILLNESS INDEX; T-LYMPHOCYTES; TIME FACTORS;

EID: 79953675701     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.30219     Document Type: Article

References (50)

1. Lipsky PE. Rheumatoid arthritis. In: Kasper DL, Braunwald E, Fauci AS, Hauser SL, Longo DL, Jameson JL, editors. Harrison's principles of internal medicine. 16th edition. New York: McGraw- Hill; 2005. p. 1968-77.
2. Gorman CL, Cope AP. Immune-mediated pathways in chronic inflammatory arthritis. Best Pract Res Clin Rheumatol 2008;22: 221-38. (Pubitemid 351606942)
3. Hahn B. A pathophysiologic approach to the clinical management of arthritis and pain: current and future implications. J Clin Rheumatol 2004;10:S3-4. (Pubitemid 38812914)
4. Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 2010; 34:J258-65.
5. Tobon GJ, Youinou P, Saraux A. The environment, geoepidemiology, and autoimmune disease: rheumatoid arthritis. Autoimmun Rev 2010;9:A288-92.
6. Klareskog L, Stolt P, Lundberg K, Kallberg H, Bengtsson C, Grunewald J, et al. A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)- restricted immune reactions to autoantigens modified by citrullination. Arthritis Rheum 2006;54:38-46. (Pubitemid 43122184)
7. Linn-Rasker SP, van der Helm-van Mil AH, van Gaalen FA, Kloppenburg M, de Vries RR, le Cessie S, et al. Smoking is a risk factor for anti-CCP antibodies only in rheumatoid arthritis patients who carry HLA-DRB1 shared epitope alleles. Ann Rheum Dis 2006;65:366-71. (Pubitemid 43268227)
8. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000;405:458-62. (Pubitemid 30367422)
9. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, et al. Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation. Nature 2003;421:384-8. (Pubitemid 36157937)
10. Bonaz B. The cholinergic anti-inflammatory pathway and the astrointestinal tract. Gastroenterology 2007;133:1370-3. (Pubitemid 47494485)
11. Gullahorn L, Lippiello L, Karpman R. Smoking and osteoarthritis: differential effect of nicotine on human chondrocyte glycosaminoglycan and collagen synthesis. Osteoarthritis Cartilage 2005;13: 942-3. (Pubitemid 41430800)
12. Green JT, Thomas GA, Rhodes J. Nicotine: therapeutic potential for the treatment of ulcerative colitis. Expert Opin Investig Drugs 1997;6:17-22.
13. Sato KZ, Fujii T, Watanabe Y, Ando T, Kazuko F, Kawashima K. Diversity of mRNA expression for muscarinic acetylcholine receptor subtypes and neuronal nicotinic acetylcholine receptor subunits in human mononuclear leukocytes and leukemic cell lines. Neurosci Lett 1999;266:17-20. (Pubitemid 29219745)
14. Skok MV, Grailhe R, Agenes F, Changeux JP. The role of nicotinic receptors in B-lymphocyte development and activation. Life Sci 2007;80:2334-6. (Pubitemid 46818278)
15. Westman M, Engstrom M, Catrina AI, Lampa J. Cell specific synovial expression of nicotinic α7 acetylcholine receptor in rheumatoid arthritis and psoriatic arthritis. Scand J Immunol 2009;70: 136-40.
16. Aicher A, Heeschen C, Mohaupt M, Cooke JP, Zeiher AM, Dimmeler S. Nicotine strongly activates dendritic cell-mediated adaptive immunity: potential role for progression of atherosclerotic lesions. Circulation 2003;107:604-11. (Pubitemid 36176812)
17. Furie MB, Raffanello JA, Gergel EI, Lisinski TJ, Horb LD. Extracts of smokeless tobacco induce pro-inflammatory changes in cultured human vascular endothelial cells. Immunopharmacology 2000;47:13-23. (Pubitemid 30120020)
18. Totti N III, McCusker KT, Campbell EJ, Griffin GL, Senior RM. Nicotine is chemotactic for neutrophils and enhances neutrophil responsiveness to chemotactic peptides. Science 1984;223:169-71. (Pubitemid 14212062)
19. Wendell KJ, Stein SH. Regulation of cytokine production in human gingival fibroblasts following treatment with nicotine and lipopolysaccharide. J Periodontol 2001;72:1038-44. (Pubitemid 32762868)
20. Vassallo R, Kroening PR, Parambil J, Kita H. Nicotine and oxidative cigarette smoke constituents induce immune-modulatory and pro-inflammatory dendritic cell responses. Mol Immunol 2008;45:3321-9.
21. Nouri-Shirazi M, Guinet E. Evidence for the immunosuppressive role of nicotine on human dendritic cell functions. Immunology 2003;109:365-73. (Pubitemid 36783262)
22. Guinet E, Yoshida K, Nouri-Shirazi M. Nicotinic environment affects the differentiation and functional maturation of monocytes derived dendritic cells (DCs). Immunol Lett 2004;95:45-55. (Pubitemid 39119899)
23. Nouri-Shirazi M, Tinajero R, Guinet E. Nicotine alters the biological activities of developing mouse bone marrow-derived dendritic cells (DCs). Immunol Lett 2007;109:155-64. (Pubitemid 46452751)
24. Nizri E, Irony-Tur-Sinai M, Lory O, Orr-Urtreger A, Lavi E, Brenner T. Activation of the cholinergic anti-inflammatory system by nicotine attenuates neuroinflammation via suppression of Th1 and Th17 responses. J Immunol 2009;183:6681-8.
25. Geng Y, Savage SM, Johnson LJ, Seagrave J, Sopori ML. Effects of nicotine on the immune response. I. Chronic exposure to nicotine impairs antigen receptor-mediated signal transduction in lymphocytes. Toxicol Appl Pharmacol 1995;135:268-78. (Pubitemid 26031878)
26. Hamano R, Takahashi HK, Iwagaki H, Yoshino T, Nishibori M, Tanaka N. Stimulation of α7 nicotinic acetylcholine receptor inhibits CD14 and the toll-like receptor 4 expression in human monocytes. Shock 2006;26:358-64. (Pubitemid 44402020)
27. Li T, Zuo X, Zhou Y, Wang Y, Zhuang H, Zhang L, et al. The vagus nerve and nicotinic receptors involve inhibition of HMGB1 release and early pro-inflammatory cytokines function in collageninduced arthritis. J Clin Immunol 2010;30:213-20.
28. Sugano N, Shimada K, Ito K, Murai S. Nicotine inhibits the production of inflammatory mediators in U937 cells through modulation of nuclear factor-κB activation. Biochem Biophys Res Commun 1998;252:25-8. (Pubitemid 28534621)
29. Guslandi M. Long-term effects of a single course of nicotine treatment in acute ulcerative colitis: remission maintenance in a 12-month follow-up study. Int J Colorectal Dis 1999;14:261-2. (Pubitemid 30000277)
30. Lindblad SS, Mydel P, Jonsson IM, Senior RM, Tarkowski A, Bokarewa M. Smoking and nicotine exposure delay development of collagen-induced arthritis in mice. Arthritis Res Ther 2009;11: R88.
31. Van Maanen MA, Lebre MC, van der Poll T, LaRosa GJ, Elbaum D, Vervoordeldonk MJ, et al. Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum 2009;60:114-22.
32. Kim HR, Kim EY, Cerny J, Moudgil KD. Antibody responses to mycobacterial and self heat shock protein 65 in autoimmune arthritis: epitope specificity and implication in pathogenesis. J Immunol 2006;177:6634-41. (Pubitemid 44715026)
33. Tong L, Moudgil KD. Celastrus aculeatus Merr. suppresses the induction and progression of autoimmune arthritis by modulating immune response to heat-shock protein 65. Arthritis Res Ther 2007;9:R70.
34. Durai M, Kim HR, Bala KK, Moudgil KD. T cells against the pathogenic and protective epitopes of heat-shock protein 65 are crossreactive and display functional similarity: novel aspect of regulation of autoimmune arthritis. J Rheumatol 2007;34: 2134-43. (Pubitemid 350076870)
35. Kim HR, Rajaiah R, Wu QL, Satpute SR, Tan MT, Simon JE, et al. Green tea protects rats against autoimmune arthritis by modulating disease-related immune events. J Nutr 2008;138:2111-6.
36. Kroening PR, Barnes TW, Pease L, Limper A, Kita H, Vassallo R. Cigarette smoke-induced oxidative stress suppresses generation of dendritic cell IL-12 and IL-23 through ERK-dependent pathways. J Immunol 2008;181:1536-47.
37. Goldberg R, Wildbaum G, Zohar Y, Maor G, Karin N. Suppression of ongoing adjuvant-induced arthritis by neutralizing the function of the p28 subunit of IL-27. J Immunol 2004;173:1171-8. (Pubitemid 38924293)
38. Cao Y, Doodes PD, Glant TT, Finnegan A. IL-27 induces a Th1 immune response and susceptibility to experimental arthritis. J Immunol 2008;180:922-30.
39. Stumhofer JS, Laurence A, Wilson EH, Huang E, Tato CM, Johnson LM, et al. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat Immunol 2006; 7:937-45. (Pubitemid 44263907)
40. Batten M, Li J, Yi S, Kljavin NM, Danilenko DM, Lucas S, et al. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat Immunol 2006;7:929-36. (Pubitemid 44263906)
41. Cai C, La Cava A. Mimicking self-antigens with synthetic peptides in systemic autoimmune rheumatic diseases. Curr Clin Pharmacol 2009;4:142-7.
42. Uysal H, Nandakumar KS, Kessel C, Haag S, Carlsen S, Burckhardt H, et al. Antibodies to citrullinated proteins: molecular interactions and arthritogenicity. Immunol Rev 2010;233:9-33.
43. Pruijn GJ, Wiik A, van Venrooij WJ. The use of citrullinated peptides and proteins for the diagnosis of rheumatoid arthritis. Arthritis Res Ther 2010;12:203.
44. Vossenaar ER, Nijenhuis S, Helsen MM, van der Heijden A, Senshu T, van den Berg WB, et al. Citrullination of synovial proteins in murine models of rheumatoid arthritis. Arthritis Rheum 2003;48:2489-500. (Pubitemid 37129426)
45. Kuhn KA, Kulik L, Tomooka B, Braschler KL, Arend WP, Robinson WH, et al. Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J Clin Invest 2006;116:961-73.
46. Uysal H, Bockermann R, Nandakumar KS, Sehnert B, Bajtner E, Engstrom A, et al. Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis. J Exp Med 2009;206:449-62.
47. Ulmansky R, Cohen CJ, Szafer F, Moallem E, Fridlender ZG, Kashi Y, et al. Resistance to adjuvant arthritis is due to protective antibodies against heat shock protein surface epitopes and the induction of IL-10 secretion. J Immunol 2002;168:6463-9. (Pubitemid 34620071)
48. De Rosa MJ, Dionisio L, Agriello E, Bouzat C, Esandi Mdel C. Alpha 7 nicotinic acetylcholine receptor modulates lymphocyte activation. Life Sci 2009;85:444-9.
49. Kim EY, Moudgil KD. Regulation of autoimmune inflammation by pro-inflammatory cytokines. Immunol Lett 2008;120:1-5.
50. Sternberg EM. Neuroendocrine regulation of auto-immune/ inflammatory disease. J Endocrinol 2001;169:429-35. (Pubitemid 32536975)