The case for measuring antibodies to specific citrullinated antigens

References

• Schellekens GA, de Jong BA, van den Hoogen FH, van de Putte LB, van Venrooij WJ. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J. Clin. Invest. 101(1), 273–281 (1998).
   PubMed Web of Science ®Google Scholar
• Vincent C, Simon M, Sebbag M et al. Immunoblotting detection of autoantibodies to human epidermis filaggrin: a new diagnostic test for rheumatoid arthritis. J. Rheumatol. 25(5), 838–846 (1998).
   PubMedGoogle Scholar
• Lundberg K, Kinloch A, Fisher BA et al. Antibodies to citrullinated alpha-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum. 58(10), 3009–3019 (2008).
   PubMedGoogle Scholar
• van Beers JJ, Schwarte CM, Stammen-Vogelzangs J, Oosterink E, Božič B, Pruijn GJ. The rheumatoid arthritis synovial fluid citrullinome reveals novel citrullinated epitopes in apolipoprotein E, myeloid nuclear differentiation antigen, and β-actin. Arthritis Rheum. 65(1), 69–80 (2013).
   PubMed Web of Science ®Google Scholar
• Trouw LA, Mahler M. Closing the serological gap: promising novel biomarkers for the early diagnosis of rheumatoid arthritis. Autoimmun. Rev. 12(2), 318–322 (2012).
   PubMed Web of Science ®Google Scholar
• Wegner N, Lundberg K, Kinloch A et al. Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Immunol. Rev. 233(1), 34–54 (2010).
   PubMed Web of Science ®Google Scholar
• Sebbag M, Moinard N, Auger I et al. Epitopes of human fibrin recognized by the rheumatoid arthritis-specific autoantibodies to citrullinated proteins. Eur. J. Immunol. 36(8), 2250–2263 (2006).
   PubMedGoogle Scholar
• Trier NH, Leth ML, Hansen PR, Houen G. Cross-reactivity of a human IgG1 anticitrullinated fibrinogen monoclonal antibody to a citrullinated profilaggrin peptide. Protein Sci. 21(12), 1929–1941 (2012).
   PubMedGoogle Scholar
• Amara K, Steen J, Murray F et al. Monoclonal IgG antibodies generated from joint-derived B cells of RA patients have a strong bias toward citrullinated autoantigen recognition. J. Exp. Med. 210(3), 445–455 (2013).
   PubMed Web of Science ®Google Scholar
• van de Stadt LA, van Schouwenburg PA, Bryde S et al. Monoclonal anti-citrullinated protein antibodies selected on citrullinated fibrinogen have distinct targets with different cross-reactivity patterns. Rheumatology (Oxford), 52(4), 631–635 (2012).
   PubMedGoogle Scholar
• Snir O, Widhe M, von Spee C et al. Multiple antibody reactivities to citrullinated antigens in sera from patients with rheumatoid arthritis: association with HLA-DRB1 alleles. Ann. Rheum. Dis. 68(5), 736–743 (2009).
   PubMedGoogle Scholar
• Goules JD, Goules AV, Tzioufas AG. Fine specificity of anti-citrullinated peptide antibodies discloses a heterogeneous antibody population in rheumatoid arthritis. Clin. Exp. Immunol. 174(1), 10–17 (2013).
   PubMedGoogle Scholar
• Ioan-Facsinay A, el-Bannoudi H, Scherer HU et al. Anti-cyclic citrullinated peptide antibodies are a collection of anti-citrullinated protein antibodies and contain overlapping and non-overlapping reactivities. Ann. Rheum. Dis. 70(1), 188–193 (2011).
   PubMed Web of Science ®Google Scholar
• Suwannalai P, Scherer HU, van der Woude D et al. Anti-citrullinated protein antibodies have a low avidity compared with antibodies against recall antigens. Ann. Rheum. Dis. 70(2), 373–379 (2011).
   PubMedGoogle Scholar
• Shi J, Willemze A, Janssen GM et al. Recognition of citrullinated and carbamylated proteins by human antibodies: specificity, cross-reactivity and the ‘AMC-Senshu’ method. Ann. Rheum. Dis. 72(1), 148–150 (2013).
   PubMedGoogle Scholar
• van de Stadt LA, Witte BI, Bos WH, van Schaardenburg D. A prediction rule for the development of arthritis in seropositive arthralgia patients. Ann. Rheum. Dis. doi”>10.1136/annrheumdis-2012-202127 (2012) ( Epub ahead of print).
   Google Scholar
• van der Woude D, Rantapää-Dahlqvist S, Ioan-Facsinay A 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. 69(8), 1554–1561 (2010).
   PubMed Web of Science ®Google Scholar
• van de Stadt LA, de Koning MH, van de Stadt RJ et al. Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis. Arthritis Rheum. 63(11), 3226–3233 (2011).
   PubMedGoogle Scholar
• Sokolove J, Bromberg R, Deane KD et al. Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS ONE 7(5), e35296 (2012).
   PubMed Web of Science ®Google Scholar
• Barra L, Scinocca M, Saunders S et al. Anti-citrullinated protein antibodies (ACPA) in unaffected first degree relatives of rheumatoid arthritis patients. Arthritis Rheum. 65(6), 1439–1447 (2013).
   PubMedGoogle Scholar
• Nicaise Roland P, Grootenboer Mignot S, Bruns A et al. Antibodies to mutated citrullinated vimentin for diagnosing rheumatoid arthritis in anti-CCP-negative patients and for monitoring infliximab therapy. Arthritis Res. Ther. 10(6), R142 (2008).
   PubMedGoogle Scholar
• Bartoloni E, Alunno A, Bistoni O et al. Diagnostic value of anti-mutated citrullinated vimentin in comparison to anti-cyclic citrullinated peptide and anti-viral citrullinated peptide 2 antibodies in rheumatoid arthritis: an Italian multicentric study and review of the literature. Autoimmun. Rev. 11(11), 815–820 (2012).
   PubMedGoogle Scholar
• Nicaise-Roland P, Nogueira L, Demattei C et al. Autoantibodies to citrullinated fibrinogen compared with anti-MCV and anti-CCP2 antibodies in diagnosing rheumatoid arthritis at an early stage: data from the French ESPOIR cohort. Ann. Rheum. Dis. 72(3), 357–362 (2013).
   PubMedGoogle Scholar
• Pratt AG, Charles PJ, Chowdhury M, Wilson G, Venables PJ, Isaacs JD. Serotyping for an extended anti-citrullinated peptide autoantibody panel does not add value to CCP2 testing for diagnosing RA in an early undifferentiated arthritis cohort. Ann. Rheum. Dis. 70(11), 2056–2058 (2011).
   PubMedGoogle Scholar
• Lundberg K, Bengtsson C, Kharlamova N 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. 72(5), 652–8 (2012).
   PubMedGoogle Scholar
• Willemze A, Böhringer S, Knevel R et al. The ACPA recognition profile and subgrouping of ACPA-positive RA patients. Ann. Rheum. Dis. 71(2), 268–274 (2012).
   PubMedGoogle Scholar
• Fisher BA, Plant D, Brode M et al. Antibodies to citrullinated alpha-enolase peptide 1 and clinical and radiological outcomes in rheumatoid arthritis. Ann. Rheum. Dis. 70(6), 1095–1098 (2011).
   PubMed Web of Science ®Google Scholar
• van Oosterhout M, Bajema I, Levarht EW, Toes RE, Huizinga TW, van Laar JM. Differences in synovial tissue infiltrates between anti-cyclic citrullinated peptide-positive rheumatoid arthritis and anti-cyclic citrullinated peptide-negative rheumatoid arthritis. Arthritis Rheum. 58(1), 53–60 (2008).
   PubMedGoogle Scholar
• van der Woude D, Syversen SW, van der Voort EI et al. The ACPA isotype profile reflects long-term radiographic progression in rheumatoid arthritis. Ann. Rheum. Dis. 69(6), 1110–1116 (2010).
   PubMed Web of Science ®Google Scholar
• Aubart F, Crestani B, Nicaise-Roland P et al. High levels of anti-cyclic citrullinated peptide autoantibodies are associated with co-occurrence of pulmonary diseases with rheumatoid arthritis. J. Rheumatol. 38(6), 979–982 (2011).
   PubMed Web of Science ®Google Scholar
• Giles JT, Danoff SK, Sokolove J et al. Association of fine specificity and repertoire expansion of anticitrullinated peptide antibodies with rheumatoid arthritis associated interstitial lung disease. Ann. Rheum. Dis. doi:10.1136/annrheumdis-2012-203160 (2013) ( Epub ahead of print).
   Google Scholar
• Harlow L, Rosas IO, Gochuico BR et al. Identification of citrullinated hsp90 isoforms as novel autoantigens in rheumatoid arthritis-associated interstitial lung disease. Arthritis Rheum. 65(4), 869–879 (2013).
   PubMedGoogle Scholar
• De Rycke L, Baeten D, Kruithof E, Van den Bosch F, Veys EM, De Keyser F. The effect of TNFalpha blockade on the antinuclear antibody profile in patients with chronic arthritis: biological and clinical implications. Lupus 14(12), 931–937 (2005).
   PubMedGoogle Scholar
• Caramaschi P, Biasi D, Tonolli E et al. Antibodies against cyclic citrullinated peptides in patients affected by rheumatoid arthritis before and after infliximab treatment. Rheumatol. Int. 26(1), 58–62 (2005).
   PubMedGoogle Scholar
• van Dongen H, van Aken J, Lard LR et al. Efficacy of methotrexate treatment in patients with probable rheumatoid arthritis: a double-blind, randomized, placebo-controlled trial. Arthritis Rheum. 56(5), 1424–1432 (2007).
   PubMed Web of Science ®Google Scholar
• Fisher BA, Plant D, Lundberg K et al. Heterogeneity of anticitrullinated peptide antibodies and response to anti-tumor necrosis factor agents in rheumatoid arthritis. J. Rheumatol. 39(5), 929–932 (2012).
   PubMed Web of Science ®Google Scholar
• van Aken J, Heimans L, Gillet-van Dongen H et al. Five-year outcomes of probable rheumatoid arthritis treated with methotrexate or placebo during the first year (the PROMPT study). Ann. Rheum. Dis. doi:10.1136/annrheumdis-2012-202967 (2013) ( Epub ahead of print).
   Google Scholar
• Visser K, Verpoort KN, van Dongen H et al. Pretreatment serum levels of anti-cyclic citrullinated peptide antibodies are associated with the response to methotrexate in recent-onset arthritis. Ann Rheum. Dis. 67(8), 1194–1195 (2008).
   PubMedGoogle Scholar
• Verpoort KN, Jol-van der Zijde CM, Papendrecht-van der Voort EA et al. Isotype distribution of anti-cyclic citrullinated peptide antibodies in undifferentiated arthritis and rheumatoid arthritis reflects an ongoing immune response. Arthritis Rheum. 54(12), 3799–3808 (2006).
   PubMedGoogle Scholar
• Chibnik LB, Mandl LA, Costenbader KH, Schur PH, Karlson EW. Comparison of threshold cutpoints and continuous measures of anti-cyclic citrullinated peptide antibodies in predicting future rheumatoid arthritis. J. Rheumatol. 36(4), 706–711 (2009).
   PubMed Web of Science ®Google Scholar
• Brink M, Hansson M, Mathsson L et al. Multiplex analyses of antibodies against citrullinated peptides in individuals prior to development of rheumatoid arthritis. Arthritis Rheum. 65(4), 899–910 (2013).
   PubMedGoogle Scholar
• Suwannalai P, van de Stadt LA, Radner H et al. Avidity maturation of anti-citrullinated protein antibodies in rheumatoid arthritis. Arthritis Rheum. 64(5), 1323–1328 (2012).
   PubMedGoogle Scholar
• Zhao X, Okeke NL, Sharpe O et al. Circulating immune complexes contain citrullinated fibrinogen in rheumatoid arthritis. Arthritis Res. Ther. 10(4), R94 (2008).
   PubMed Web of Science ®Google Scholar
• Sokolove J, Zhao X, Chandra PE, Robinson WH. Immune complexes containing citrullinated fibrinogen costimulate macrophages via Toll-like receptor 4 and Fcgamma receptor. Arthritis Rheum. 63(1), 53–62 (2011).
   PubMedGoogle Scholar
• Laurent L, Clavel C, Lemaire O et al. Fcγ receptor profile of monocytes and macrophages from rheumatoid arthritis patients and their response to immune complexes formed with autoantibodies to citrullinated proteins. Ann. Rheum. Dis. 70(6), 1052–1059 (2011).
   PubMed Web of Science ®Google Scholar
• Scherer HU, van der Woude D, Ioan-Facsinay A et al. Glycan profiling of anti-citrullinated protein antibodies isolated from human serum and synovial fluid. Arthritis Rheum. 62(6), 1620–1629 (2010).
   PubMed Web of Science ®Google Scholar
• Trouw LA, Haisma EM, Levarht EW et al. Anti-cyclic citrullinated peptide antibodies from rheumatoid arthritis patients activate complement via both the classical and alternative pathways. Arthritis Rheum. 60(7), 1923–1931 (2009).
   PubMed Web of Science ®Google Scholar
• Harre U, Georgess D, Bang H et al. Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J. Clin. Invest. 122(5), 1791–1802 (2012).
   PubMed Web of Science ®Google Scholar
• Lu MC, Lai NS, Yu HC, Huang HB, Hsieh SC, Yu CL. Anti-citrullinated protein antibodies bind surface-expressed citrullinated Grp78 on monocyte/macrophages and stimulate tumor necrosis factor alpha production. Arthritis Rheum. 62(5), 1213–1223 (2010).
   PubMed Web of Science ®Google Scholar
• Klareskog L, Malmström V, Lundberg K, Padyukov L, Alfredsson L. Smoking, citrullination and genetic variability in the immunopathogenesis of rheumatoid arthritis. Semin. Immunol. 23(2), 92–98 (2011).
   PubMedGoogle Scholar
• Makrygiannakis D, Hermansson M, Ulfgren AK et al. Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann. Rheum. Dis. 67(10), 1488–1492 (2008).
   PubMed Web of Science ®Google Scholar
• Mercado FB, Marshall RI, Bartold PM. Inter-relationships between rheumatoid arthritis and periodontal disease. A review. J. Clin. Periodontol. 30(9), 761–772 (2003).
   PubMedGoogle Scholar
• Scher JU, Ubeda C, Equinda M et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum. 64(10), 3083–3094 (2012).
   PubMed Web of Science ®Google Scholar
• Lappin DF, Apatzidou D, Quirke AM et al. Influence of periodontal disease, Porphyromonas gingivalis and cigarette smoking on systemic anti-citrullinated peptide antibody titres. J. Clin. Periodontol. 40(10), 907–915 (2013).
   PubMed Web of Science ®Google Scholar
• Svärd A., Kastbom A, Sommarin Y, Skogh T. Salivary IgA antibodies to cyclic citrullinated peptides (CCP) in rheumatoid arthritis. Immunobiology 218(2), 232–237 (2013).
   PubMedGoogle Scholar
• Wegner N, Wait R, Sroka A et al. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum. 62(9), 2662–2672 (2010).
   PubMed Web of Science ®Google Scholar
• Quirke AM, Lugli EB, Wegner N et al. Heightened immune response to autocitrullinated Porphyromonas gingivalis peptidylarginine deiminase: a potential mechanism for breaching immunologic tolerance in rheumatoid arthritis. Ann. Rheum. Dis. (2013) ( Epub ahead of print).
   Google Scholar
• de Pablo P, Dietrich T, Chapple IL et al. The autoantibody repertoire in periodontitis: a role in the induction of autoimmunity to citrullinated proteins in rheumatoid arthritis? Ann. Rheum. Dis. (2013).
   Google Scholar
• Kinloch AJ, Alzabin S, Brintnell W et al. Immunization with Porphyromonas gingivalis enolase induces autoimmunity to mammalian α-enolase and arthritis in DR4-IE-transgenic mice. Arthritis Rheum. 63(12), 3818–3823 (2011).
   PubMed Web of Science ®Google Scholar
• Hill JA, Bell DA, Brintnell W et al. Arthritis induced by posttranslationally modified (citrullinated) fibrinogen in DR4-IE transgenic mice. J. Exp. Med. 205(4), 967–979 (2008).
   PubMed Web of Science ®Google Scholar
• Bell DA, Hill JA, Cairns E. An intriguing relationship between the immune response to citrullinated vimentin and the HLA shared epitope: comment on the article by Verpoort et al. Arthritis Rheum. 58(10), 3277, author reply 3277–3278 (2008).
   PubMedGoogle Scholar
• Perricone C, Ceccarelli F, Valesini G. An overview on the genetic of rheumatoid arthritis: a never-ending story. Autoimmun. Rev. 10(10), 599–608 (2011).
   PubMed Web of Science ®Google Scholar
• 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. 171(2), 538–541 (2003).
   PubMed Web of Science ®Google Scholar
• Menard L, Saadoun D, Isnardi I et al. The PTPN22 allele encoding an R620W variant interferes with the removal of developing autoreactive B cells in humans. J. Clin. Invest. 121(9), 3635–3644 (2011).
   PubMed Web of Science ®Google Scholar
• Verpoort KN, Cheung K, Ioan-Facsinay A et al. Fine specificity of the anti-citrullinated protein antibody response is influenced by the shared epitope alleles. Arthritis Rheum. 56(12), 3949–3952 (2007).
   PubMedGoogle Scholar
• Fisher BA, Bang SY, Chowdhury M 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. (2013) ( Epub ahead of print).
   Google Scholar
• 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. 64(10), 3102–3110 (2012).
   PubMedGoogle Scholar
• Hansson M, Mathsson L, Schlederer T et al. Validation of a multiplex chip-based assay for the detection of autoantibodies against citrullinated peptides. Arthritis Res. Ther. 14(5), R201 (2012).
   PubMedGoogle Scholar
• Snir O, Widhe M, Hermansson M et al. Antibodies to several citrullinated antigens are enriched in the joints of rheumatoid arthritis patients. Arthritis Rheum. 62(1), 44–52 (2010).
   PubMedGoogle Scholar
• Schulte S, Unger C, Mo JA et al. Arthritis-related B cell epitopes in collagen II are conformation-dependent and sterically privileged in accessible sites of cartilage collagen fibrils. J. Biol. Chem. 273(3), 1551–1561 (1998).
   PubMedGoogle Scholar