Smoking, Porphyromonas gingivalis and the immune response to citrullinated autoantigens before the clinical onset of rheumatoid arthritis in a Southern European nested case-control study Clinical rheumatology and osteoporosis

BMC Musculoskeletal Disorders

Volumn 16, Issue 1, 2015, Pages

  Fisher, Benjamin A ^a   Cartwright, Alison J ^b   Quirke, Anne Marie ^b   De Pablo, Paola ^a   Romaguera, Dora ^c,d   Panico, Salvatore ^e   Mattiello, Amalia ^e   Gavrila, Diana ^f,g   Navarro, Carmen ^f,g   Sacerdote, Carlotta ^h   Vineis, Paolo ^h   Tumino, Rosario ⁱ   Lappin, David F ^j   Apazidou, Danae ^j   Culshaw, Shauna ^j   Potempa, Jan ^k,l   Michaud, Dominique S ^c,m   Riboli, Elio ^c   Venables, Patrick J ^b  

^a QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d Instituto de Salud Carlos III   (Spain)

^e UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^f DEPARTMENT OF EPIDEMIOLOGY   (Spain)

^g CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^h Human Genetics Foundation   (Italy)

ⁱ CIVILE M P AREZZO HOSPITAL   (Italy)

^j GLASGOW DENTAL HOSPITAL AND SCHOOL   (United Kingdom)

^k JAGIELLONIAN UNIVERSITY   (Poland)

^l UNIVERSITY OF LOUISVILLE   (United States)

^m BROWN UNIVERSITY   (United States)

more..

Author keywords

Anti citrullinated protein antibodies (ACPA); Citrullination; Porphyromonas gingivalis; Rheumatoid arthritis (RA); Smoking

Indexed keywords

ALPHA ENOLASE; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; FIBRINOGEN; GINGIPAIN R; VIMENTIN; ADHESIN; ARGINGIPAIN, PORPHYROMONAS GINGIVALIS; AUTOANTIGEN; CYCLIC CITRULLINATED PEPTIDE; CYCLOPEPTIDE; CYSTEINE PROTEINASE; HYDROLASE; PROTEIN-ARGININE DEIMINASE;

ADULT; ANTIBODY DETECTION; ANTIGEN DETECTION; ARTICLE; CASE CONTROL STUDY; COHORT ANALYSIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME SPECIFICITY; FEMALE; HUMAN; IMMUNE RESPONSE; IMMUNOREACTIVITY; MAJOR CLINICAL STUDY; MALE; MULTICENTER STUDY; ONTOGENY; POLYMERASE CHAIN REACTION; POPULATION RESEARCH; PORPHYROMONAS GINGIVALIS; PROSPECTIVE STUDY; QUESTIONNAIRE; RANDOMIZED CONTROLLED TRIAL; RHEUMATOID ARTHRITIS; SEX DIFFERENCE; SMOKING; SOUTHERN EUROPEAN; VALIDATION PROCESS; ADVERSE EFFECTS; ARTHRITIS, RHEUMATOID; CLINICAL TRIAL; COMPLICATION; ENZYMOLOGY; EUROPE; IMMUNOLOGY; MICROBIOLOGY; MIDDLE AGED; PERIODONTITIS;

ADHESINS, BACTERIAL; ADULT; ARTHRITIS, RHEUMATOID; AUTOANTIGENS; CASE-CONTROL STUDIES; CYSTEINE ENDOPEPTIDASES; EUROPE; FEMALE; HUMANS; HYDROLASES; MALE; MIDDLE AGED; PEPTIDES, CYCLIC; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PROSPECTIVE STUDIES; SMOKING;

EID: 84946232867     PISSN: None     EISSN: 14712474     Source Type: Journal    
DOI: 10.1186/s12891-015-0792-y     Document Type: Article

References (52)

1. Gerlag DM, Raza K, van Baarsen LG, Brouwer E, Buckley CD, Burmester GR, et al. EULAR recommendations for terminology and research in individuals at risk of rheumatoid arthritis: report from the Study Group for Risk Factors for Rheumatoid Arthritis. Ann Rheum Dis. 2012;71(5):638-41.
2. van der Woude D, Rantapaa-Dahlqvist S, Ioan-Facsinay A, Onnekink C, Schwarte CM, Verpoort KN, et al. Epitope spreading of the anti-citrullinated protein antibody response occurs before disease onset and is associated with the disease course of early arthritis. Ann Rheum Dis. 2010;69(8):1554-61.
3. van de Stadt LA, de Koning MH, van de Stadt RJ, Wolbink G, Dijkmans BA, Hamann D, et al. Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis. Arthritis Rheum. 2011;63(11):3226-33.
4. Sokolove J, Bromberg R, Deane KD, Lahey LJ, Derber LA, Chandra PE, et al. Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS One. 2012;7(5):e35296.
5. Brink M, Hansson M, Mathsson L, Jakobsson PJ, Holmdahl R, Hallmans G, et al. Multiplex analyses of antibodies against citrullinated peptides in individuals prior to development of rheumatoid arthritis. Arthritis Rheum. 2013;65(4):899-910.
6. de Pablo P, Chapple IL, Buckley CD, Dietrich T. Periodontitis in systemic rheumatic diseases. Nat Rev Rheumatol. 2009;5(4):218-24.
7. Demoruelle MK, Deane KD, Holers VM. When and where does inflammation begin in rheumatoid arthritis? Curr Opin Rheumatol. 2014;26(1):64-71.
8. Kinloch AJ, Alzabin S, Brintnell W, Wilson E, Barra L, Wegner N, et al. Immunization with Porphyromonas gingivalis enolase induces autoimmunity to mammalian alpha-enolase and arthritis in DR4-IE-transgenic mice. Arthritis Rheum. 2011;63(12):3818-23.
9. Lundberg K, Kinloch A, Fisher BA, Wegner N, Wait R, Charles P, et al. Antibodies to citrullinated alpha-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum. 2008;58(10):3009-19.
10. Quirke AM, Lugli EB, Wegner N, Hamilton BC, Charles P, Chowdhury M, et al. Heightened immune response to autocitrullinated Porphyromonas gingivalis peptidylarginine deiminase: a potential mechanism for breaching immunologic tolerance in rheumatoid arthritis. Ann Rheum Dis. 2014;73(1):263-9.
11. Wegner N, Wait R, Sroka A, Eick S, Nguyen KA, Lundberg K, et al. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and alpha-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum. 2010;62(9):2662-72.
12. de Pablo P, Dietrich T, Chapple IL, Milward M, Chowdhury M, Charles PJ, et al. The autoantibody repertoire in periodontitis: a role in the induction of autoimmunity to citrullinated proteins in rheumatoid arthritis? Ann Rheum Dis. 2014;73(3):580-6.
13. Montgomery AB, Kopec J, Shrestha L, Thezenas ML, Burgess-Brown NA, Fischer R et al. Crystal structure of Porphyromonas gingivalis peptidylarginine deiminase: implications for autoimmunity in rheumatoid arthritis. Ann Rheum Dis 2015, doi: 10.1136/annrheumdis-2015-207656.
14. Konig MF, Paracha AS, Moni M, Bingham CO, III, Andrade F. Defining the role of Porphyromonas gingivalis peptidylarginine deiminase (PPAD) in rheumatoid arthritis through the study of PPAD biology. Ann Rheum Dis. 2015;74(11):2054-61.
15. 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(1):38-46.
16. Lee HS, Irigoyen P, Kern M, Lee A, Batliwalla F, Khalili H, et al. 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(6):1745-53.
17. van der Helm-van Mil 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(2):425-32.
18. Kokkonen H, Brink M, Hansson M, Lassen E, Mathsson-Alm L, Holmdahl R, et al. Associations of antibodies against citrullinated peptides with human leukocyte antigen-shared epitope and smoking prior to the development of rheumatoid arthritis. Arthritis Res Ther. 2015;17:125. doi: 10.1186/s13075-015-0638-x. 125-0638.
19. Zee KY. Smoking and periodontal disease. Aust Dent J. 2009;54 Suppl 1:S44-50. doi: 10.1111/j.1834-7819.2009.01142.x.:S44-S50.
20. Tomar SL, Asma S. Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol. 2000;71(5):743-51.
21. Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5(6B):1113-24.
22. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988;31(3):315-24.
23. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham III CO, et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Ann Rheum Dis. 2010;69(9):1580-8.
24. Verpoort KN, Cheung K, Ioan-Facsinay A, van der Helm-van Mil AH, de Vries-Bouwstra JK, Allaart CF, et al. Fine specificity of the anti-citrullinated protein antibody response is influenced by the shared epitope alleles. Arthritis Rheum. 2007;56(12):3949-52.
25. Lappin DF, Apatzidou D, Quirke AM, Oliver-Bell J, Butcher JP, Kinane DF, et al. Influence of periodontal disease, Porphyromonas gingivalis and cigarette smoking on systemic anti-citrullinated peptide antibody titres. J Clin Periodontol. 2013;40(10):907-15.
26. Apatzidou DA, Riggio MP, Kinane DF. Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J Clin Periodontol. 2005;32(9):973-83.
27. Hensvold AH, Magnusson PK, Joshua V, Hansson M, Israelsson L, Ferreira R, et al. Environmental and genetic factors in the development of anticitrullinated protein antibodies (ACPAs) and ACPA-positive rheumatoid arthritis: an epidemiological investigation in twins. Ann Rheum Dis. 2015;74(2):375-80.
28. Arlestig L, Mullazehi M, Kokkonen H, Rocklov J, Ronnelid J, Dahlqvist SR. Antibodies against cyclic citrullinated peptides of IgG, IgA and IgM isotype and rheumatoid factor of IgM and IgA isotype are increased in unaffected members of multicase rheumatoid arthritis families from northern Sweden. Ann Rheum Dis. 2012;71(6):825-9.
29. Hitchon CA, Chandad F, Ferucci ED, Willemze A, Ioan-Facsinay A, van der Woude D, et al. Antibodies to porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol. 2010;37(6):1105-12.
30. Kolfenbach JR, Deane KD, Derber LA, O'Donnell C, Weisman MH, Buckner JH, et al. A prospective approach to investigating the natural history of preclinical rheumatoid arthritis (RA) using first-degree relatives of probands with RA. Arthritis Rheum. 2009;61(12):1735-42.
31. Barra L, Scinocca M, Saunders S, Bhayana R, Rohekar S, Racape M, et al. Anti-citrullinated protein antibodies in unaffected first-degree relatives of rheumatoid arthritis patients. Arthritis Rheum. 2013;65(6):1439-47.
32. Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun. 2010;34(3):J258-65.
33. 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(10):6681-8.
34. 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(2):187-200.
35. 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. 1-57.
36. Carrillo T, de Rodriguez CF, Cuevas M, Diaz F, Cabrera P. Effect of cigarette smoking on the humoral immune response in pigeon fanciers. Allergy. 1991;46(4):241-4.
37. Roseman C, Truedsson L, Kapetanovic MC. The effect of smoking and alcohol consumption on markers of systemic inflammation, immunoglobulin levels and immune response following pneumococcal vaccination in patients with arthritis. Arthritis Res Ther. 2012;14(4):R170.
38. 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(1):114-22.
39. 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(3):R88.
40. Mahdi H, Fisher BA, Kallberg H, Plant D, Malmstrom V, Ronnelid J, et al. Specific interaction between genotype, smoking and autoimmunity to citrullinated alpha-enolase in the etiology of rheumatoid arthritis. Nat Genet. 2009;41(12):1319-24.
41. Lundberg K, Bengtsson C, Kharlamova N, Reed E, Jiang X, Kallberg H, et al. Genetic and environmental determinants for disease risk in subsets of rheumatoid arthritis defined by the anticitrullinated protein/peptide antibody fine specificity profile. Ann Rheum Dis. 2013;72(5):652-8.
42. Fisher BA, Bang SY, Chowdhury M, Lee HS, Kim JH, Charles P, et al. Smoking, the HLA-DRB1 shared epitope and ACPA fine-specificity in Koreans with rheumatoid arthritis: evidence for more than one pathogenic pathway linking smoking to disease. Ann Rheum Dis. 2014;73(4):741-7.
43. Mikuls TR, Thiele GM, Deane KD, Payne JB, O'Dell JR, Yu F, et al. Porphyromonas gingivalis and disease-related autoantibodies in individuals at increased risk of rheumatoid arthritis. Arthritis Rheum. 2012;64(11):3522-30.
44. Mikuls TR, Payne JB, Reinhardt RA, Thiele GM, Maziarz E, Cannella AC, et al. Antibody responses to Porphyromonas gingivalis (P. gingivalis) in subjects with rheumatoid arthritis and periodontitis. Int Immunopharmacol. 2009;9(1):38-42.
45. de Smit M, van de Stadt LA, Janssen KM, Doornbos-van der Meer B, Vissink A, van Winkelhoff AJ, et al. Antibodies against Porphyromonas gingivalis in seropositive arthralgia patients do not predict development of rheumatoid arthritis. Ann Rheum Dis. 2014;73(6):1277-9
46. Mikuls TR, Payne JB, Yu F, Thiele GM, Reynolds RJ, Cannon GW et al. Periodontitis and Porphyromonas gingivalis in Patients with Rheumatoid Arthritis. Arthritis Rheum. 2014;66(5)1090-100
47. Scher JU, Ubeda C, Equinda M, Khanin R, Buischi Y, Viale A, et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum. 2012;64(10):3083-94.
48. Ferucci ED, Darrah E, Smolik I, Choromanski TL, Robinson DB, Newkirk MM, et al. Prevalence of anti-peptidylarginine deiminase type 4 antibodies in rheumatoid arthritis and unaffected first-degree relatives in indigenous North American Populations. J Rheumatol. 2013;40(9):1523-8.
49. Kolfenbach JR, Deane KD, Derber LA, O'Donnell CI, Gilliland WR, Edison JD, et al. Autoimmunity to peptidyl arginine deiminase type 4 precedes clinical onset of rheumatoid arthritis. Arthritis Rheum. 2010;62(9):2633-9.
50. Harris ML, Darrah E, Lam GK, Bartlett SJ, Giles JT, Grant AV, et al. Association of autoimmunity to peptidyl arginine deiminase type 4 with genotype and disease severity in rheumatoid arthritis. Arthritis Rheum. 2008;58(7):1958-67.
51. Chan KW, Felson DT, Yood RA, Walker AM. The lag time between onset of symptoms and diagnosis of rheumatoid arthritis. Arthritis Rheum. 1994;37(6):814-20.
52. Majka DS, Deane KD, Parrish LA, Lazar AA, Baron AE, Walker CW, et al. Duration of preclinical rheumatoid arthritis-related autoantibody positivity increases in subjects with older age at time of disease diagnosis. Ann Rheum Dis. 2008;67(6):801-7.