Anti-citrullinated peptide autoantibodies, human leukocyte antigen shared epitope and risk of future rheumatoid arthritis: A nested case-control study

Arthritis Research and Therapy

Volumn 15, Issue 5, 2013, Pages

  Arkema, Elizabeth V ^a,b   Goldstein, Barbara L ^a   Robinson, William ^c   Sokolove, Jeremy ^c   Wagner, Catriona A ^c   Malspeis, Susan ^a   Rosner, Bernard ^b   Grodstein, Francine ^b,d   Karlson, Elizabeth W ^a   Costenbader, Karen H ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC CITRULLINATED PEPTIDE ANTIBODY; EPITOPE; HUMAN LEUKOCYTE ANTIGEN SHARED EPITOPE; LEUKOCYTE ANTIGEN; UNCLASSIFIED DRUG; AUTOANTIBODY; CYCLIC CITRULLINATED PEPTIDE; CYCLOPEPTIDE; HLA ANTIGEN;

ADULT; ARTICLE; CONTROLLED STUDY; FEMALE; HLA SYSTEM; HUMAN; MAJOR CLINICAL STUDY; MEDICAL RECORD; MENOPAUSE; POSTMENOPAUSE; RHEUMATOID ARTHRITIS; RISK FACTOR; ALLELE; BLOOD; CASE CONTROL STUDY; GENETICS; IMMUNOLOGY; MIDDLE AGED; RISK; STATISTICAL MODEL; TIME;

ADULT; ALLELES; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; CASE-CONTROL STUDIES; EPITOPES; FEMALE; HLA ANTIGENS; HUMANS; LOGISTIC MODELS; MIDDLE AGED; ODDS RATIO; PEPTIDES, CYCLIC; RISK FACTORS; TIME FACTORS;

EID: 84886014796     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4342     Document Type: Article

References (36)

1. Whiting PF, Smidt N, Sterne JA, Harbord R, Burton A, Burke M, Beynon R, Ben-Shlomo Y, Axford J, Dieppe P. Systematic review: accuracy of anti-citrullinated peptide antibodies for diagnosing rheumatoid arthritis. Ann Intern Med 2010, 152:456-464. W155-166, 10.7326/0003-4819-152-7-201004060-00010, 20368651.
2. Montes A, Perez-Pampin E, Calaza M, Gomez-Reino JJ, Gonzalez A. Association of anti-citrullinated vimentin and anti-citrullinated α-enolase antibodies with subsets of rheumatoid arthritis. Arthritis Rheum 2012, 64:3102-3110. 10.1002/art.34569, 22674012.
3. Lundberg K, Bengtsson C, Kharlamova N, Reed E, Jiang X, Kallberg H, Pollak-Dorocic I, Israelsson L, Kessel C, Padyukov L, Holmdahl R, Alfredsson L, Klareskog L. 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, 72:652-658. 10.1136/annrheumdis-2012-201484, 22661643.
4. Snir O, Widhe M, von Spee C, Lindberg J, Padyukov L, Lundberg K, Engstrom A, Venables PJ, Lundeberg J, Holmdahl R, Klareskog L, Malmström V. Multiple antibody reactivities to citrullinated antigens in sera from patients with rheumatoid arthritis: association with HLA-DRB1 alleles. Ann Rheum Dis 2009, 68:736-743. 10.1136/ard.2008.091355, 18635594.
5. van de Stadt LA, de Koning MH, van de Stadt RJ, Wolbink G, Dijkmans BA, Hamann D, van Schaardenburg D. Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis. Arthritis Rheum 2011, 63:3226-3233. 10.1002/art.30537, 21792832.
6. Sokolove J, Bromberg R, Deane KD, Lahey LJ, Derber LA, Chandra PE, Edison JD, Gilliland WR, Tibshirani RJ, Norris JM, Holers VM, Robinson WH. Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS One 2012, 7:e35296. 10.1371/journal.pone.0035296, 3360701, 22662108.
7. Aggarwal R, Liao K, Nair R, Ringold S, Costenbader KH. Anti-citrullinated peptide antibody assays and their role in the diagnosis of rheumatoid arthritis. Arthritis Rheum 2009, 61:1472-1483. 10.1002/art.24827, 2859449, 19877103.
8. van de Stadt LA, van der Horst AR, de Koning MH, Bos WH, Wolbink GJ, van de Stadt RJ, Pruijn GJ, Dijkmans BA, van Schaardenburg D, Hamann D. The extent of the anti-citrullinated protein antibody repertoire is associated with arthritis development in patients with seropositive arthralgia. Ann Rheum Dis 2011, 70:128-133. 10.1136/ard.2010.132662, 21062853.
9. van der Woude D, Rantapää-Dahlqvist S, Ioan-Facsinay A, Onnekink C, Schwarte CM, Verpoort KN, Drijfhout JW, Huizinga TW, Toes RE, Pruijn GJ. 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, 69:1554-1561. 10.1136/ard.2009.124537, 20448290.
10. Brink M, Hansson M, Mathsson L, Jakobsson PJ, Holmdahl R, Hallmans G, Stenlund H, Rönnelid J, Klareskog L, Rantapää-Dahlqvist S. Multiplex analyses of antibodies against citrullinated peptides in individuals prior to development of rheumatoid arthritis. Arthritis Rheum 2013, 65:899-910. 10.1002/art.37835, 23310951.
11. Fernando MM, Stevens CR, Walsh EC, De Jager PL, Goyette P, Plenge RM, Vyse TJ, Rioux JD. Defining the role of the MHC in autoimmunity: a review and pooled analysis. PLoS Genet 2008, 4:e1000024. 10.1371/journal.pgen.1000024, 2291482, 18437207.
12. Jawaheer D, Li W, Graham RR, Chen W, Damle A, Xiao X, Monteiro J, Khalili H, Lee A, Lundsten R, Begovich A, Bugawan T, Erlich H, Elder JT, Criswell LA, Seldin MF, Amos CI, Behrens TW, Gregersen PK. Dissecting the genetic complexity of the association between human leukocyte antigens and rheumatoid arthritis. Am J Hum Genet 2002, 71:585-594. 10.1086/342407, 449696, 12181776.
13. Gregersen PK, Silver J, Winchester RJ. The shared epitope hypothesis: an approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum 1987, 30:1205-1213. 10.1002/art.1780301102, 2446635.
14. Mahdi H, Fisher BA, Kallberg H, Plant D, Malmstrom V, Ronnelid J, Charles P, Ding B, Alfredsson L, Padyukov L, Symmons DP, Venables PJ, Klareskog L, Lundberg K. Specific interaction between genotype, smoking and autoimmunity to citrullinated α-enolase in the etiology of rheumatoid arthritis. Nat Genet 2009, 41:1319-1324. 10.1038/ng.480, 19898480.
15. Berglin E, Padyukov L, Sundin U, Hallmans G, Stenlund H, van Venrooij WJ, Klareskog L, Dahlqvist SR. A combination of autoantibodies to cyclic citrullinated peptide (CCP) and HLA-DRB1 locus antigens is strongly associated with future onset of rheumatoid arthritis. Arthritis Res Ther 2004, 6:R303-R308. 10.1186/ar1187, 464874, 15225365.
16. Balsa A, Cabezón A, Orozco G, Cobo T, Miranda-Carus E, López-Nevot MA, Vicario JL, Martín-Mola E, Martín J, Pascual-Salcedo D. Influence of HLA DRB1 alleles in the susceptibility of rheumatoid arthritis and the regulation of antibodies against citrullinated proteins and rheumatoid factor. Arthritis Res Ther 2010, 12:R62. 10.1186/ar2975, 2888213, 20370905.
17. Karlson EW, Chibnik LB, Cui J, Plenge RM, Glass RJ, Maher NE, Parker A, Roubenoff R, Izmailova E, Coblyn JS, Weinblatt ME, Shadick NA. Associations between human leukocyte antigen, PTPN22, CTLA4 genotypes and rheumatoid arthritis phenotypes of autoantibody status, age at diagnosis and erosions in a large cohort study. Ann Rheum Dis 2008, 67:358-363. 2945890, 17666451.
18. Verpoort KN, Cheung K, Ioan-Facsinay A, van der Helm-van Mil AH, de Vries-Bouwstra JK, Allaart CF, Drijfhout JW, de Vries RR, Breedveld FC, Huizinga TW, Pruijn GJ, Toes RE. Fine specificity of the anti-citrullinated protein antibody response is influenced by the shared epitope alleles. Arthritis Rheum 2007, 56:3949-3952. 10.1002/art.23127, 18050209.
19. 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. 10.1002/art.22703, 17530703.
20. 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, 56:425-432. 10.1002/art.22373, 17265477.
21. 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. 10.1002/art.21575, 16385494.
22. Karlson EW, Mandl LA, Hankinson SE, Grodstein F. Do breast-feeding and other reproductive factors influence future risk of rheumatoid arthritis? Results from the Nurses' Health Study. Arthritis Rheum 2004, 50:3458-3467. 10.1002/art.20621, 15529351.
23. Karlson EW, Chibnik LB, Tworoger SS, Lee IM, Buring JE, Shadick NA, Manson JE, Costenbader KH. Biomarkers of inflammation and development of rheumatoid arthritis in women from two prospective cohort studies. Arthritis Rheum 2009, 60:641-652. 10.1002/art.24350, 2715148, 19248103.
24. Karlson EW, Sanchez-Guerrero J, Wright EA, Lew RA, Daltroy LH, Katz JN, Liang MH. A connective tissue disease screening questionnaire for population studies. Ann Epidemiol 1995, 5:297-302. 10.1016/1047-2797(94)00096-C, 8520712.
25. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, Medsger TA, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder GG. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988, 31:315-324. 10.1002/art.1780310302, 3358796.
26. Monach PA, Hueber W, Kessler B, Tomooka BH, BenBarak M, Simmons BP, Wright J, Thornhill TS, Monestier M, Ploegh H, Robinson WH, Mathis D, Benoist C. A broad screen for targets of immune complexes decorating arthritic joints highlights deposition of nucleosomes in rheumatoid arthritis. Proc Natl Acad Sci USA 2009, 106:15867-15872. 10.1073/pnas.0908032106, 2747210, 19720992.
27. 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, 119:503. e1-503.e9.
28. 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. 10.1186/ar2022, 1779386, 16872514.
29. Källberg H, Ding B, Padyukov L, Bengtsson C, Rönnelid J, Klareskog L, Alfredsson L. EIRA Study Group: Smoking is a major preventable risk factor for rheumatoid arthritis: estimations of risks after various exposures to cigarette smoke. Ann Rheum Dis 2011, 70:508-511. 10.1136/ard.2009.120899, 3033966, 21149499, EIRA Study Group: .
30. Källberg H, Jacobsen S, Bengtsson C, Pedersen M, Padyukov L, Garred P, Frisch M, Karlson EW, Klareskog L, Alfredsson L. Alcohol consumption is associated with decreased risk of rheumatoid arthritis: results from two Scandinavian case-control studies. Ann Rheum Dis 2009, 68:222-227. 10.1136/ard.2007.086314, 2937278, 18535114.
31. Wesley A, Bengtsson C, Elkan AC, Klareskog L, Alfredsson L, Wedrén S. Epidemiological Investigation of Rheumatoid Arthritis Study Group Association between body mass index and anti-citrullinated protein antibody-positive and anti-citrullinated protein antibody-negative rheumatoid arthritis: results from a population-based case-control study. Arthritis Care Res (Hoboken) 2013, 65:107-112. 10.1002/acr.21749, 22674870, Epidemiological Investigation of Rheumatoid Arthritis Study Group.
32. Hosmer DW, Lemeshow S. Confidence interval estimation of interaction. Epidemiology 1992, 3:452-456. 10.1097/00001648-199209000-00012, 1391139.
33. van der Helm-van Mil AH, Verpoort KN, Breedveld FC, Huizinga TW, Toes RE, de Vries RR. The HLA-DRB1 shared epitope alleles are primarily a risk factor for anti-cyclic citrullinated peptide antibodies and are not an independent risk factor for development of rheumatoid arthritis. Arthritis Rheum 2006, 54:1117-1121. 10.1002/art.21739, 16572446.
34. 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.
35. Wegner N, Lundberg K, Kinloch A, Fisher B, Malmström V, Feldmann M, Venables PJ. Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Immunol Rev 2010, 233:34-54. 10.1111/j.0105-2896.2009.00850.x, 20192991.
36. van der Woude D, Alemayehu WG, Verduijn W, de Vries RR, Houwing-Duistermaat JJ, Huizinga TW, Toes RE. Gene-environment interaction influences the reactivity of autoantibodies to citrullinated antigens in rheumatoid arthritis. Nat Genet 2010, 42:814-816. 10.1038/ng1010-814, 20877316.