Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Arthritis Research & Therapy
Published in: Arthritis Research & Therapy 4/2009

01-08-2009 | Review

Rheumatoid arthritis and smoking: putting the pieces together

Authors: Zsuzsanna Baka, Edit Buzás, György Nagy

Published in: Arthritis Research & Therapy | Issue 4/2009

Login to get access

Abstract

Besides atherosclerosis and lung cancer, smoking is considered to play a major role in the pathogenesis of autoimmune diseases. It has long been known that there is a connection between rheumatoid factor-positive rheumatoid arthritis and cigarette smoking. Recently, an important gene–environment interaction has been revealed; that is, carrying specific HLA-DRB1 alleles encoding the shared epitope and smoking establish a significant risk for anti-citrullinated protein antibody-positive rheumatoid arthritis. We summarize how smoking-related alteration of the cytokine balance, the increased risk of infections (the possibility of cross-reactivity) and modifications of autoantigens by citrullination may contribute to the development of rheumatoid arthritis.
Appendix
Available only for authorised users
Literature
1.
Vessey MP, Villard-Mackintosh L, Yeates D: Oral contraceptives, cigarette smoking and other factors in relation to arthritis. Contraception. 1987, 35: 457-464.CrossRefPubMed
2.
Heliovaara M, Aho K, Aromaa A, Knekt P, Reunanen A: Smoking and risk of rheumatoid arthritis. J Rheumatol. 1993, 20: 1830-1835.PubMed
3.
Symmons DP, Bankhead CR, Harrison BJ, Brennan P, Barrett EM, Scott DG, Silman AJ: Blood transfusion, smoking, and obesity as risk factors for the development of rheumatoid arthritis: results from a primary care-based incident case–control study in Norfolk, England. Arthritis Rheum. 1997, 40: 1955-1961.CrossRefPubMed
4.
Hazes JM, Dijkmans BA, Vandenbroucke JP, de Vries RR, Cats A: Lifestyle and the risk of rheumatoid arthritis: cigarette smoking and alcohol consumption. Ann Rheum Dis. 1990, 49: 980-982.PubMedCentralCrossRefPubMed
5.
Costenbader KH, Karlson EW: Cigarette smoking and autoimmune disease: what can we learn from epidemiology?. Lupus. 2006, 15: 737-745.CrossRefPubMed
6.
Green GM, Carolin D: The depressant effect of cigarette smoke on the in vitro antibacterial activity of alveolar macrophages. N Engl J Med. 1967, 276: 421-427.CrossRefPubMed
7.
Ortega E, Barriga C, Rodriguez AB: Decline in the phagocytic function of alveolar macrophages from mice exposed to cigarette smoke. Comp Immunol Microbiol Infect Dis. 1994, 17: 77-84.CrossRefPubMed
8.
King TE, Savici D, Campbell PA: Phagocytosis and killing of Listeria monocytogenes by alveolar macrophages: smokers versus nonsmokers. J Infect Dis. 1988, 158: 1309-1316.CrossRefPubMed
9.
Nguyen Van Binh P, Zhou D, Baudouin F, Martin C, Radionoff M, Dutertre H, Marchand V, Thevenin M, Warnet JM, Thien Duc H: Modulation of the primary and the secondary antibody response by tobacco smoke condensates. Biomed Pharmacother. 2004, 58: 527-530.CrossRefPubMed
10.
11.
Higashimoto Y, Shimada Y, Fukuchi Y, Ishida K, Shu C, Teramoto S, Sudo E, Matsuse T, Orimo H: Inhibition of mouse alveolar macrophage production of tumor necrosis factor alpha by acute in vivo and in vitro exposure to tobacco smoke. Respiration. 1992, 59: 77-80.CrossRefPubMed
12.
Pessina GP, Paulesu L, Corradeschi F, Luzzi E, Tanzini M, Aldinucci C, Di Stefano A, Bocci V: Chronic cigarette smoking enhances spontaneous release of tumour necrosis factor-alpha from alveolar macrophages of rats. Mediators Inflamm. 1993, 2: 423-428.PubMedCentralCrossRefPubMed
13.
Yamaguchi E, Itoh A, Furuya K, Miyamoto H, Abe S, Kawakami Y: Release of tumor necrosis factor-alpha from human alveolar macrophages is decreased in smokers. Chest. 1993, 103: 479-483.CrossRefPubMed
14.
Sauty A, Mauel J, Philippeaux MM, Leuenberger P: Cytostatic activity of alveolar macrophages from smokers and nonsmokers: role of interleukin-1 beta, interleukin-6, and tumor necrosis factor-alpha. Am J Respir Cell Mol Biol. 1994, 11: 631-637.CrossRefPubMed
15.
Singh SP, Kalra R, Puttfarcken P, Kozak A, Tesfaigzi J, Sopori ML: Acute and chronic nicotine exposures modulate the immune system through different pathways. Toxicol Appl Pharmacol. 2000, 164: 65-72.CrossRefPubMed
16.
Matsunaga K, Klein TW, Friedman H, Yamamoto Y: Involvement of nicotinic acetylcholine receptors in suppression of antimicrobial activity and cytokine responses of alveolar macrophages to Legionella pneumophila infection by nicotine. J Immunol. 2001, 167: 6518-6524.CrossRefPubMed
17.
Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, Wang H, Abumrad N, Eaton JW, Tracey KJ: Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000, 405: 458-462.CrossRefPubMed
18.
Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ: Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature. 2003, 421: 384-388.CrossRefPubMed
19.
Ouyang Y, Virasch N, Hao P, Aubrey MT, Mukerjee N, Bierer BE, Freed BM: Suppression of human IL-1β, IL-2, IFN-γ, and TNF-α production by cigarette smoke extracts. J Allergy Clin Immunol. 2000, 106: 280-287.CrossRefPubMed
20.
Choi JM, Cho YC, Cho WJ, Kim TS, Kang BY: Hydroquinone, a major component in cigarette smoke, reduces IFN-γ production in antigen-primed lymphocytes. Arch Pharm Res. 2008, 31: 337-341.CrossRefPubMed
21.
Facchinetti F, Amadei F, Geppetti P, Tarantini F, Di Serio C, Dragotto A, Gigli PM, Catinella S, Civelli M, Patacchini R: α,β-unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am J Respir Cell Mol Biol. 2007, 37: 617-623.CrossRefPubMed
22.
Nguyen C, Teo JL, Matsuda A, Eguchi M, Chi EY, Henderson WR, Kahn M: Chemogenomic identification of Ref-1/AP-1 as a therapeutic target for asthma. Proc Natl Acad Sci USA. 2003, 100: 1169-1173.PubMedCentralCrossRefPubMed
23.
Hasnis E, Bar-Shai M, Burbea Z, Reznick AZ: Cigarette smoke-induced NF-κB activation in human lymphocytes: the effect of low and high exposure to gas phase of cigarette smoke. J Physiol Pharmacol. 2007, 58 (Suppl 5): 263-274.PubMed
24.
Lannan S, Donaldson K, Brown D, MacNee W: Effects of cigarette smoke and its condensates on alveolar cell injury in vitro. Am J Physiol. 1994, 266: L92-L100.PubMed
25.
Criswell LA, Saag KG, Mikuls TR, Cerhan JR, Merlino LA, Lum RF, Pfeiffer KA, Woehl B, Seldin MF: Smoking interacts with genetic risk factors in the development of rheumatoid arthritis among older Caucasian women. Ann Rheum Dis. 2006, 65: 1163-1167.PubMedCentralCrossRefPubMed
26.
Bowes J, Barton A: Recent advances in the genetics of RA susceptibility. Rheumatology (Oxford). 2008, 47: 399-402.CrossRef
27.
Dong S, Zhang Z, Takahara H: Estrogen-enhanced peptidylarginine deiminase type IV gene (PADI4) expression in MCF-7 cells is mediated by estrogen receptor-alpha-promoted transfactors activator protein-1, nuclear factor-Y, and Sp1. Mol Endocrinol. 2007, 21: 1617-1629.CrossRefPubMed
28.
Méchin MC, Sebbag M, Arnaud J, Nachat R, Foulquier C, Adoue V, Coudane F, Duplan H, Schmitt AM, Chavanas S, Guerrin M, Serre G, Simon M: Update on peptidylarginine deiminases and deimination in skin physiology and severe human diseases. Int J Cosmet Sci. 2007, 29: 147-168.CrossRefPubMed
29.
Makrygiannakis D, Hermansson M, Ulfgren AK, Nicholas AP, Zendman AJ, Eklund A, Grunewald J, Skold CM, Klareskog L, Catrina AI: Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann Rheum Dis. 2008, 67: 1488-1492.CrossRefPubMed
30.
Baron JA, La Vecchia C, Levi F: The antiestrogenic effect of cigarette smoking in women. Am J Obstet Gynecol. 1990, 162: 502-514.CrossRefPubMed
31.
Kannel WB, D'Agostino RB, Belanger AJ: Fibrinogen, cigarette smoking, and risk of cardiovascular disease: insights from the Framingham Study. Am Heart J. 1987, 113: 1006-1010.CrossRefPubMed
32.
Masson-Bessiére C, Sebbag M, Girbal-Neuhauser E, Vincent C, Serre G: Synovial target antigens of antifilaggrin autoantibodies are deiminated forms of fibrin alpha and beta chains [abstract]. Rev Rheum. 1999, 66: 754-
33.
Nakayama-Hamada M, Suzuki A, Furukawa H, Yamada R, Yamamoto K: Citrullinated fibrinogen inhibits thrombin-catalyzed fibrin polymerization. J Biochem. 2008, 144: 393-398.CrossRefPubMed
34.
The Wellcome Trust Case Control Consortium: Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature. 2007, 447: 661-678.PubMedCentralCrossRef
35.
McInnes IB, Schett G: Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol. 2007, 7: 429-442.CrossRefPubMed
36.
Yamamoto K, Yamada R: Lessons from a genome wide association study of rheumatoid arthritis. N Engl J Med. 2007, 357: 1250-1251.CrossRefPubMed
37.
Gregersen PK: Pathways to gene identification in rheumatoid arthritis: PTPN22 and beyond. Immunol Rev. 2005, 204: 74-86.CrossRefPubMed
38.
Begovich AB, Carlton VE, Honigberg LA, Schrodi SJ, Chokkalingam AP, Alexander HC, Ardlie KG, Huang Q, Smith AM, Spoerke JM, Conn MT, Chang M, Chang SY, Saiki RK, Catanese JJ, Leong DU, Garcia VE, McAllister LB, Jeffery DA, Lee AT, Batliwalla F, Remmers E, Criswell LA, Seldin MF, Kastner DL, Amos CI, Sninsky JJ, Gregersen PK: A missense single-nucleotide polymorphism in a gene encoding a protein tyrosine phosphatase (PTPN22) is associated with rheumatoid arthritis. Am J Hum Genet. 2004, 75: 330-337.PubMedCentralCrossRefPubMed
39.
Costenbader KH, Chang SC, De Vivo I, Plenge R, Karlson EW: PTPN22, PADI-4 and CTLA-4 genetic polymorphisms and risk of rheumatoid arthritis in two longitudinal cohort studies: evidence of gene–environment interactions with heavy cigarette smoking. Arthritis Res Ther. 2008, 10: R52-PubMedCentralCrossRefPubMed
40.
Luo Y, Arita K, Bhatia M, Knuckley B, Lee YH, Stallcup MR, Sato M, Thompson PR: Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry. 2006, 45: 11727-11736.PubMedCentralCrossRefPubMed
41.
Füst G, Arason GJ, Kramer J, Szalai C, Duba J, Yang Y, Chung EK, Zhou B, Blanchong CA, Lokki ML, Bödvarsson S, Prohászka Z, Karádi I, Vatay A, Kovács M, Romics L, Thorgeirsson G, Yu CY: Genetic basis of tobacco smoking: strong association of a specific major histocompatibility complex haplotype on chromosome 6 with smoking behavior. Int Immunol. 2004, 16: 1507-1514.CrossRefPubMed
42.
Ates O, Hatemi G, Hamuryudan V, Topal-Sarikaya A: Tumor necrosis factor-alpha and interleukin-10 gene promoter polymorphisms in Turkish rheumatoid arthritis patients. Clin Rheumatol. 2008, 27: 1243-1248.CrossRefPubMed
43.
Padyukov L, Silva C, Stolt P, Alfredsson L, Klareskog L: A gene–environment interaction between smoking and shared epitope genes in HLA-DR provides a high risk of seropositive rheumatoid arthritis. Arthritis Rheum. 2004, 50: 3085-3092.CrossRefPubMed
44.
45.
Masdottir B, Jónsson T, Manfredsdottir V, Víkingsson A, Brekkan A, Valdimarsson H: Smoking, rheumatoid factor isotypes and severity of rheumatoid arthritis. Rheumatology (Oxford). 2000, 39: 1202-1205.CrossRef
46.
Uhlig T, Hagen KB, Kvien TK: Current tobacco smoking, formal education, and the risk of rheumatoid arthritis. J Rheumatol. 1999, 26: 47-54.PubMed
47.
48.
Voigt LF, Koepsell TD, Nelson JL, Dugowson CE, Daling JR: Smoking, obesity, alcohol consumption, and the risk of rheumatoid arthritis. Epidemiology. 1994, 5: 525-532.PubMed
49.
Stolt P, Bengtsson C, Nordmark B, Lindblad S, Lundberg I, Klareskog L, Alfredsson L, EIRA study group: 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.PubMedCentralCrossRefPubMed
50.
Karlson EW, Lee IM, Cook NR, Manson JE, Buring JE, Hennekens CH: A retrospective cohort study of cigarette smoking and risk of rheumatoid arthritis in female health professionals. Arthritis Rheum. 1999, 42: 910-917.CrossRefPubMed
51.
Hutchinson D, Shepstone L, Moots R, Lear JT, Lynch MP: Heavy cigarette smoking is strongly associated with rheumatoid arthritis (RA), particularly in patients without a family history of RA. Ann Rheum Dis. 2001, 60: 223-227.PubMedCentralCrossRefPubMed
52.
Criswell LA, Merlino LA, Cerhan JR, Mikuls TR, Mudano AS, Burma M, Folsom AR, Saag KG: Cigarette smoking and the risk of rheumatoid arthritis among postmenopausal women: results from the Iowa Women's Health Study. Am J Med. 2002, 112: 465-471.CrossRefPubMed
53.
Costenbader KH, Feskanich D, Mandl LA, Karlson EW: Smoking intensity, duration, and cessation, and the risk of rheumatoid arthritis in women. Am J Med. 2006, 119: e1-503.CrossRefPubMed
54.
Saag KG, Cerhan JR, Kolluri S, Ohashi K, Hunninghake GW, Schwartz DA: Cigarette smoking and rheumatoid arthritis severity. Ann Rheum Dis. 1997, 56: 463-469.PubMedCentralCrossRefPubMed
55.
Masdottir B, Jónsson T, Manfredsdottir V, Víkingsson A, Brekkan A, Valdimarsson H: Smoking, rheumatoid factor isotypes and severity of rheumatoid arthritis. Rheumatology (Oxford). 2000, 39: 1202-1205.CrossRef
56.
Nyhäll-Wåhlin BM, Jacobsson LT, Petersson IF, Turesson C, BARFOT study group: Smoking is a strong risk factor for rheumatoid nodules in early rheumatoid arthritis. Ann Rheum Dis. 2006, 65: 601-606.PubMedCentralCrossRefPubMed
57.
Struthers GR, Scott DL, Delamere JP, Sheppeard H, Kitt M: Smoking and rheumatoid vasculitis. Rheumatol Int. 1981, 1: 145-146.CrossRefPubMed
58.
Nagai S, Hoshino Y, Hayashi M, Ito I: Smoking-related interstitial lung diseases. Curr Opin Pulm Med. 2000, 6: 415-419.CrossRefPubMed
59.
Manfredsdottir VF, Vikingsdottir T, Jonsson T, Geirsson AJ, Kjartansson O, Heimisdottir M, Sigurdardottir SL, Valdimarsson H, Vikingsson A: The effects of tobacco smoking and rheumatoid factor seropositivity on disease activity and joint damage in early rheumatoid arthritis. Rheumatology (Oxford). 2006, 45: 734-740.CrossRef
60.
Papadopoulos NG, Alamanos Y, Voulgari PV, Epagelis EK, Tsifetaki N, Drosos AA: Does cigarette smoking influence disease expression, activity and severity in early rheumatoid arthritis patients?. Clin Exp Rheumatol. 2005, 23: 861-866.PubMed
61.
Finckh A, Dehler S, Costenbader KH, Gabay C, Swiss Clinical Quality Management project for RA: Cigarette smoking and radiographic progression in rheumatoid arthritis. Ann Rheum Dis. 2007, 66: 1066-1071.PubMedCentralCrossRefPubMed
62.
Westhoff G, Rau R, Zink A: Rheumatoid arthritis patients who smoke have a higher need for DMARDs and feel worse, but they do not have more joint damage than non-smokers of the same serological group. Rheumatology (Oxford). 2008, 47: 849-854.CrossRef
63.
Linn-Rasker SP, Helm-van Mil van der AH, van Gaalen FA, Kloppenburg M, de Vries RR, le Cessie S, Breedveld FC, Toes RE, Huizinga TW: 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: 366-371.PubMedCentralCrossRefPubMed
64.
Pedersen M, Jacobsen S, Klarlund M, Pedersen BV, Wiik A, Wohlfahrt J, Frisch M: Environmental risk factors differ between rheumatoid arthritis with and without auto-antibodies against cyclic citrullinated peptides. Arthritis Res Ther. 2006, 8: R133-PubMedCentralCrossRefPubMed
65.
Lee DM, Phillips R, Hagan EM, Chibnik LB, Costenbader KH, Schur PH: Quantifying Anti-CCP titer: clinical utility and association with tobacco exposure in patients with rheumatoid arthritis. Ann Rheum Dis. 2009, 68: 201-208.CrossRefPubMed
66.
Klareskog L, Stolt P, Lundberg K, Källberg H, Bengtsson C, Grunewald J, Rönnelid J, Harris HE, Ulfgren AK, Rantapää-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.CrossRefPubMed
67.
Pedersen M, Jacobsen S, Garred P, Madsen HO, Klarlund M, Svejgaard A, Pedersen BV, Wohlfahrt J, Frisch M: Strong combined gene–environment effects in anti-cyclic citrullinated peptide-positive rheumatoid arthritis: a nationwide case–control study in Denmark. Arthritis Rheum. 2007, 56: 1446-1453.CrossRefPubMed
68.
Helm-van Mil van der AH, Verpoort KN, le Cessie S, Huizinga TW, de Vries RR, Toes RE: The HLA-DRB1 shared epitope alleles differ in the interaction with smoking and predisposition to antibodies to cyclic citrullinated peptide. Arthritis Rheum. 2007, 56: 425-432.CrossRefPubMed
69.
Verpoort KN, Papendrecht-van der Voort EA, Helm-van Mil van der AH, Jol-van der Zijde CM, van Tol MJ, Drijfhout JW, Breedveld FC, de Vries RR, Huizinga TW, Toes RE: Association of smoking with the constitution of the anti-cyclic citrullinated peptide response in the absence of HLA-DRB1 shared epitope alleles. Arthritis Rheum. 2007, 56: 2913-2918.CrossRefPubMed
70.
Michou L, Teixeira VH, Pierlot C, Lasbleiz S, Bardin T, Dieudé P, Prum B, Cornélis F, Petit-Teixeira E: Associations between genetic factors, tobacco smoking and autoantibodies in familial and sporadic rheumatoid arthritis. Ann Rheum Dis. 2008, 67: 466-470.CrossRefPubMed
71.
Lee HS, Irigoyen P, Kern M, Lee A, Batliwalla F, Khalili H, Wolfe F, Lum RF, Massarotti E, Weisman M, Bombardier C, Karlson EW, Criswell LA, Vlietinck R, Gregersen PK: Interaction between smoking, the shared epitope, and anti-cyclic citrullinated peptide: a mixed picture in three large North American rheumatoid arthritis cohorts. Arthritis Rheum. 2007, 56: 1745-1753.CrossRefPubMed
72.
Mikuls TR, Hughes LB, Westfall AO, Holers VM, Parrish L, Heijde van der D, van Everdingen M, Alarcon GS, Conn DL, Jonas B, Callahan LF, Smith EA, Gilkeson G, Howard G, Moreland LW, Bridges SL: Cigarette smoking, disease severity, and autoantibody expression in African Americans with recent-onset rheumatoid arthritis. Ann Rheum Dis. 2008, 67: 1529-1534.PubMedCentralCrossRefPubMed
73.
Kallberg H, Padyukov L, Plenge RM, Ronnelid J, Gregersen PK, Helm-van Mil van der AH, Toes RE, Huizinga TW, Klareskog L, Alfredsson L, Epidemiological Investigation of Rheumatoid Arthritis Study Group: Gene–gene and gene–environment interactions involving HLA-DRB1, PTPN22, and smoking in two subsets of rheumatoid arthritis. Am J Hum Genet. 2007, 80: 867-875.PubMedCentralCrossRefPubMed
74.
Klareskog L, Rönnelid J, Lundberg K, Padyukov L, Alfredsson L: Immunity to citrullinated proteins in rheumatoid arthritis. Annu Rev Immunol. 2008, 26: 651-675.CrossRefPubMed
75.
György B, Tóth E, Tarcsa E, Falus A, Buzás EI: Citrullination: a posttranslational modification in health and disease. Int J Biochem Cell Biol. 2006, 38: 1662-1677.CrossRefPubMed
76.
Vossenaar ER, Smeets TJ, Kraan MC, Raats JM, van Venrooij WJ, Tak PP: The presence of citrullinated proteins is not specific for rheumatoid synovial tissue. Arthritis Rheum. 2004, 50: 3485-3494.CrossRefPubMed
77.
Foulquier C, Sebbag M, Clavel C, Chapuy-Regaud S, Al Badine R, Méchin MC, Vincent C, Nachat R, Yamada M, Takahara H, Simon M, Guerrin M, Serre G: Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation. Arthritis Rheum. 2007, 56: 3541-3553.CrossRefPubMed
78.
Shibata S, Tada Y, Komine M, Hattori N, Osame S, Kanda N, Watanabe S, Saeki H, Tamaki K: Anti-cyclic citrullinated peptide antibodies and IL-23p19 in psoriatic arthritis. J Dermatol Sci. 2009, 53: 34-39.CrossRefPubMed
79.
Atzeni F, Sarzi-Puttini P, Lama N, Bonacci E, Bobbio-Pallavicini F, Montecucco C, Caporali R: Anti-cyclic citrullinated peptide antibodies in primary Sjögren syndrome may be associated with non-erosive synovitis. Arthritis Res Ther. 2008, 10: R51-PubMedCentralCrossRefPubMed
80.
Moscarello MA, Mastronardi FG, Wood DD: The role of citrullinated proteins suggests a novel mechanism in the pathogenesis of multiple sclerosis. Neurochem Res. 2007, 32: 251-256.PubMedCentralCrossRefPubMed
81.
Tracey D, Klareskog L, Sasso EH, Salfeld JG, Tak PP: Tumor necrosis factor antagonist mechanisms of action: a comprehensive review. Pharmacol Ther. 2008, 117: 244-279.CrossRefPubMed
82.
Glossop JR, Dawes PT, Mattey DL: Association between cigarette smoking and release of tumour necrosis factor alpha and its soluble receptors by peripheral blood mononuclear cells in patients with rheumatoid arthritis. Rheumatology (Oxford). 2006, 45: 1223-1229.CrossRef
83.
Askling J, Baecklund E, Granath F, Geborek P, Fored M, Backlin C, Bertilsson L, Cöster L, Jacobsson L, Lindblad S, Lysholm J, Rantapää-Dahlqvist S, Saxne T, van Vollenhoven R, Klareskog L, Feltelius N: Anti-TNF therapy in RA and risk of malignant lymphomas. Relative risks and time-trends in the Swedish Biologics Register. Ann Rheum Dis. 2009, 68: 648-653.CrossRefPubMed
84.
Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V: Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006, 295: 2275-2285.CrossRefPubMed
85.
Bueno C, Criado G, McCormick JK, Madrenas J: T cell signalling induced by bacterial superantigens. Chem Immunol Allergy. 2007, 93: 161-180.CrossRefPubMed
86.
Pratesi F, Tommasi C, Anzilotti C, Chimenti D, Migliorini P: Deiminated Epstein–Barr virus nuclear antigen 1 is a target of anti-citrullinated protein antibodies in rheumatoid arthritis. Arthritis Rheum. 2006, 54: 733-741.CrossRefPubMed
87.
Toussirot E, Roudier J: Pathophysiological links between rheumatoid arthritis and the Epstein–Barr virus: an update. Joint Bone Spine. 2007, 74: 418-426.CrossRefPubMed
88.
Klareskog L, Stolt P, Lundberg K, Källberg H, Bengtsson C, Grunewald J, Rönnelid J, Harris HE, Ulfgren AK, Rantapää-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.CrossRefPubMed
89.
Laxman VK, Annaji S: Tobacco use and its effects on the periodontium and periodontal therapy. J Contemp Dent Pract. 2008, 9: 97-107.PubMed
90.
Harris ML, Darrah E, Lam GK, Bartlett SJ, Giles JT, Grant AV, Gao P, Scott WW, El-Gabalawy H, Casciola-Rosen L, Barnes KC, Bathon JM, Rosen A: Association of autoimmunity to peptidyl arginine deiminase type 4 with genotype and disease severity in rheumatoid arthritis. Arthritis Rheum. 2008, 58: 1958-1967.PubMedCentralCrossRefPubMed
91.
92.
He X, Kang AH, Stuart JM: Anti-Human type II collagen CD19+B cells are present in patients with rheumatoid arthritis and healthy individuals. J Rheumatol. 2001, 28: 2168-2175.PubMed
93.
Neeli I, Khan SN, Radic M: Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol. 2008, 180: 1895-1902.CrossRefPubMed
94.
Cutolo M, Straub RH: Stress as a risk factor in the pathogenesis of rheumatoid arthritis. Neuroimmunomodulation. 2006, 13: 277-282.CrossRefPubMed
95.
Hill JA, Southwood S, Sette A, Jevnikar AM, Bell DA, Cairns E: Cutting edge: the conversion of arginine to citrulline allows for a high-affinity peptide interaction with the rheumatoid arthritis-associated HLA-DRB1*0401 MHC class II molecule. J Immunol. 2003, 171: 538-541.CrossRefPubMed
96.
Li P, Yao H, Zhang Z, Li M, Luo Y, Thompson PR, Gilmour DS, Wang Y: Regulation of p53 target gene expression by peptidylarginine deiminase 4. Mol Cell Biol. 2008, 28: 4745-4758.PubMedCentralCrossRefPubMed
Metadata
Title
Rheumatoid arthritis and smoking: putting the pieces together
Authors
Zsuzsanna Baka
Edit Buzás
György Nagy
Publication date
01-08-2009
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 4/2009
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar2751

Other articles of this Issue 4/2009

Arthritis Research & Therapy 4/2009 Go to the issue

Research article

Methotrexate therapy associates with reduced prevalence of the metabolic syndrome in rheumatoid arthritis patients over the age of 60- more than just an anti-inflammatory effect? A cross sectional study

Research article

Reduced Fas ligand-expressing splenic CD5+B lymphocytes in severe collagen-induced arthritis

Research article

Increased production of soluble CTLA-4 in patients with spondylarthropathies correlates with disease activity

Research article

Broad-range PCR, cloning and sequencing of the full 16S rRNA gene for detection of bacterial DNA in synovial fluid samples of Tunisian patients with reactive and undifferentiated arthritis

Research article

Effect of interleukin-1β on spinal cord nociceptive transmission of normal and monoarthritic rats after disruption of glial function

Letter

How much sleep apnea is too much?
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits