期刊论文详细信息
Arthritis Research & Therapy
Smoking and nicotine exposure delay development of collagen-induced arthritis in mice
Maria Bokarewa ; Andrej Tarkowski ; Robert M Senior ; Ing-Marie Jonsson ; Piotr Mydel ; Sofia S Lindblad
Department of Rheumatology and Inflammation Research, University of Gothenburg, Sahlgrenska University Hospital, Guldhedsgatan 10, Göteborg, S-41346, Sweden
Department of Medicine, Division of Pulmonary and Critical Care Medicine, Washington University, 660 S. Euclid Avenue, Campus Box 8052 St. Louis, Missouri 63110, USA
Others  :  1099880
DOI  :  10.1186/ar2728
Published In 11, received in 2009-02-25, accepted in 2009-06-11
【 摘 要 】

Introduction

Recent epidemiologic studies have implicated smoking as an environmental risk factor for the development of rheumatoid arthritis (RA). The aim of the present study is the evaluation of the role of cigarette smoke (CS) in the pathogenesis of collagen-induced arthritis in mice.

Methods

DBA/1 mice exposed to CS for 16 weeks (n = 25) and mice exposed to nicotine in drinking water (n = 10) were immunized with collagen type II (CII). Severity of arthritis was evaluated clinically and morphologically and compared with control mice (n = 35). Intensity of inflammation was evaluated by serum IL-6 and TNF-α levels. Additionally, antibody response to CII (anti-CII) and citrullinated peptides (aCCP) was measured.

Results

Clinical evaluation of arthritis showed a delayed onset of arthritis in CS-exposed mice compared with non-smoking controls (P < 0.05). Histologic index and weight changes were comparable between the groups; however, smoking mice presented less weight loss during the acute phase of the disease and gained weight significantly faster in the recovery phase (P < 0.05). Similar results were obtained in the mice exposed to nicotine. Nicotine also showed a direct anti-inflammatory effect diminishing IL-6 production by stimulated splenocytes in vitro (P < 0.001). Additionally, smoking mice had lower levels of aCCP and anti-CII antibodies compared with non-smoking (P < 0.05).

Conclusions

Neither smoking nor nicotine exposure aggravates development of CII-induced arthritis in mouse model. Moreover, CS exposure was associated with a lower level of anti-CII antibodies, providing a possible explanation for a delay of arthritis onset in this group.

【 授权许可】

   
2009 Lindblad et al.; licensee BioMed Central Ltd.

【 预 览 】
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】
  • [1]Walsh NC, Gravallese EM: Bone loss in inflammatory arthritis: mechanisms and treatment strategies. Curr Opin Rheumatol 2004, 16:419-427.
  • [2]Vessey MP, Villard-Mackintosh L, Yeates D: Oral contraceptives, cigarette smoking and other factors in relation to arthritis. Contraception 1987, 35:457-464.
  • [3]Wolfe F: The effect of smoking on clinical, laboratory, and radiographic status in rheumatoid arthritis. J Rheumatol 2000, 27:630-637.
  • [4]van Gaalen FA, Linn-Rasker SP, van Venrooij WJ, de Jong BA, Breedveld FC, Verweij CL, Toes RE, Huizinga TW: Autoantibodies to cyclic citrullinated peptides predict progression to rheumatoid arthritis in patients with undifferentiated arthritis: a prospective cohort study. Arthritis Rheum 2004, 50:709-715.
  • [5]Bukhari M, Thomson W, Naseem H, Bunn D, Silman A, Symmons D, Barton A: The performance of anti-cyclic citrullinated peptide antibodies in predicting the severity of radiologic damage in inflammatory polyarthritis: results from the Norfolk Arthritis Register. Arthritis Rheum 2007, 56:2929-2935.
  • [6]Forslind K, Ahlmen M, Eberhardt K, Hafstrom I, Svensson B: Prediction of radiological outcome in early rheumatoid arthritis in clinical practice: role of antibodies to citrullinated peptides (anti-CCP). Ann Rheum Dis 2004, 63:1090-1095.
  • [7]Lundberg K, Nijenhuis S, Vossenaar ER, Palmblad K, van Venrooij WJ, Klareskog L, Zendman AJ, Harris HE: Citrullinated proteins have increased immunogenicity and arthritogenicity and their presence in arthritic joints correlates with disease severity. Arthritis Res Ther 2005, 7:R458-467. BioMed Central Full Text
  • [8]Kuhn KA, Kulik L, Tomooka B, Braschler KJ, Arend WP, Robinson WH, Holers VM: Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J Clin Invest 2006, 116:961-973.
  • [9]Valikhani M, Kavusi S, Chams-Davatchi C, Hallaji Z, Esmaili N, Ghandi N, Farahani F, Lajevardi V: Impact of smoking on pemphigus. Int J Dermatol 2008, 47:567-570.
  • [10]Manthorpe R, Benoni C, Jacobsson L, Kirtava Z, Larsson A, Liedholm R, Nyhagen C, Tabery H, Theander E: Lower frequency of focal lip sialadenitis (focus score) in smoking patients. Can tobacco diminish the salivary gland involvement as judged by histological examination and anti-SSA/Ro and anti-SSB/La antibodies in Sjogren's syndrome? Ann Rheum Dis 2000, 59:54-60.
  • [11]Wilder FV, Hall BJ, Barrett JP: Smoking and osteoarthritis: is there an association? The Clearwater Osteoarthritis Study. Osteoarthritis Cartilage 2003, 11:29-35.
  • [12]Gullahorn L, Lippiello L, Karpman R: Smoking and osteoarthritis: differential effect of nicotine on human chondrocyte glycosaminoglycan and collagen synthesis. Osteoarthritis Cartilage 2005, 13:942-943.
  • [13]Sykes AP, Brampton C, Klee S, Chander CL, Whelan C, Parsons ME: An investigation into the effect and mechanisms of action of nicotine in inflammatory bowel disease. Inflamm Res 2000, 49:311-319.
  • [14]Wang H, Liao H, Ochani M, Justiniani M, Lin X, Yang L, Al-Abed Y, Metz C, Miller EJ, Tracey KJ, Ulloa L: Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat Med 2004, 10:1216-1221.
  • [15]Saeed RW, Varma S, Peng-Nemeroff T, Sherry B, Balakhaneh D, Huston J, Tracey KJ, Al-Abed Y, Metz CN: Cholinergic stimulation blocks endothelial cell activation and leukocyte recruitment during inflammation. J Exp Med 2005, 201:1113-1123.
  • [16]Hakki A, Hallquist N, Friedman H, Pross S: Differential impact of nicotine on cellular proliferation and cytokine production by LPS-stimulated murine splenocytes. Int J Immunopharmacol 2000, 22:403-410.
  • [17]Liechti ME, Markou A: Role of the glutamatergic system in nicotine dependence: implications for the discovery and development of new pharmacological smoking cessation therapies. CNS Drugs 2008, 22:705-724.
  • [18]McNearney T, Speegle D, Lawand N, Lisse J, Westlund KN: Excitatory amino acid profiles of synovial fluid from patients with arthritis. J Rheumatol 2000, 27:739-745.
  • [19]Hinoi E, Ohashi R, Miyata S, Kato Y, Iemata M, Hojo H, Takarada T, Yoneda Y: Excitatory amino acid transporters expressed by synovial fibroblasts in rats with collagen-induced arthritis. Biochem Pharmacol 2005, 70:1744-1755.
  • [20]Adair-Kirk TL, Atkinson JJ, Griffin GL, Watson MA, Kelley DG, DeMello D, Senior RM, Betsuyaku T: Distal airways in mice exposed to cigarette smoke: Nrf2-regulated genes are increased in Clara cells. Am J Respir Cell Mol Biol 2008, 39:400-411.
  • [21]Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD: Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 1997, 277:2002-2004.
  • [22]Saetta M, Kim WD, Izquierdo JL, Ghezzo H, Cosio MG: Extent of centrilobular and panacinar emphysema in smokers' lungs: pathological and mechanical implications. Eur Respir J 1994, 7:664-671.
  • [23]Corthay A, Johansson A, Vestberg M, Holmdahl R: Collagen-induced arthritis development requires alpha beta T cells but not gamma delta T cells: studies with T cell-deficient (TCR mutant) mice. Int Immunol 1999, 11:1065-1073.
  • [24]Jonsson IM, Verdrengh M, Brisslert M, Lindblad S, Bokarewa M, Islander U, Carlsten H, Ohlsson C, Nandakumar KS, Holmdahl R, Tarkowski A: Ethanol prevents development of destructive arthritis. Proc Natl Acad Sci USA 2007, 104:258-263.
  • [25]Verdrengh M, Jonsson IM, Holmdahl R, Tarkowski A: Genistein as an anti-inflammatory agent. Inflamm Res 2003, 52:341-346.
  • [26]Klareskog L, Stolt P, Lundberg K, Kallberg H, Bengtsson C, Grunewald J, Ronnelid J, Harris HE, Ulfgren AK, Rantapaa-Dahlqvist S, Eklund A, Padyukov L, Alfredsson L: 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.
  • [27]Taneja V, Behrens M, Basal E, Sparks J, Griffiths MM, Luthra H, David CS: Delineating the role of the HLA-DR4 "shared epitope" in susceptibility versus resistance to develop arthritis. J Immunol 2008, 181:2869-2877.
  • [28]Taneja V, David CS: HLA transgenic mice as humanized mouse models of disease and immunity. J Clin Invest 1998, 101:921-926.
  • [29]Struve J: Hepatitis B virus infection among Swedish adults: aspects on seroepidemiology, transmission, and vaccine response. Scand J Infect Dis Suppl 1992, 82:1-57.
  • [30]Mili F, Flanders WD, Boring JR, Annest JL, Destefano F: The associations of race, cigarette smoking, and smoking cessation to measures of the immune system in middle-aged men. Clin Immunol Immunopathol 1991, 59:187-200.
  • [31]Sass G, Heinlein S, Agli A, Bang R, Schumann J, Tiegs G: Cytokine expression in three mouse models of experimental hepatitis. Cytokine 2002, 19:115-120.
  • [32]van Maanen MA, Lebre MC, Poll T, LaRosa GJ, Elbaum D, Vervoordeldonk MJ, Tak PP: Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum 2009, 60:114-122.
  • [33]Waldburger JM, Boyle DL, Pavlov VA, Tracey KJ, Firestein GS: Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor. Arthritis Rheum 2008, 58:3439-3449.
  • [34]Markou A: Review. Neurobiology of nicotine dependence. Philos Trans R Soc Lond B Biol Sci 2008, 363:3159-3168.
  • [35]Lawand NB, McNearney T, Westlund KN: Amino acid release into the knee joint: key role in nociception and inflammation. Pain 2000, 86:69-74.
  • [36]Harle P, Mobius D, Carr DJ, Scholmerich J, Straub RH: An opposing time-dependent immune-modulating effect of the sympathetic nervous system conferred by altering the cytokine profile in the local lymph nodes and spleen of mice with type II collagen-induced arthritis. Arthritis Rheum 2005, 52:1305-1313.
  • [37]Silman AJ, Newman J, MacGregor AJ: Cigarette smoking increases the risk of rheumatoid arthritis. Results from a nationwide study of disease-discordant twins. Arthritis Rheum 1996, 39:732-735.
  • [38]Stolt P, Bengtsson C, Nordmark B, Lindblad S, Lundberg I, Klareskog L, Alfredsson L: Quantification of the influence of cigarette smoking on rheumatoid arthritis: results from a population based case-control study, using incident cases. Ann Rheum Dis 2003, 62:835-841.
  • [39]Heliovaara M, Aho K, Aromaa A, Knekt P, Reunanen A: Smoking and risk of rheumatoid arthritis. J Rheumatol 1993, 20:1830-1835.
  文献评价指标  
  下载次数:60次 浏览次数:50次