Autoantibodies from Single Circulating Plasmablasts React with Citrullinated Antigens and Porphyromonas gingivalis in Rheumatoid Arthritis

Arthritis and Rheumatology

Volumn 68, Issue 3, 2016, Pages 614-626

  Li, Song ^a,b   Yu, Yangsheng ^b   Yue, Yinshi ^b   Liao, Hongyan ^b   Xie, Wanqin ^b   Thai, Jessica ^b   Mikuls, Ted R ^b   Thiele, Geoffrey M ^b   Duryee, Michael J ^b   Sayles, Harlan ^b   Payne, Jeffrey B ^b   Klassen, Lynell W ^b   O'Dell, James R ^b   Zhang, Zhixin ^b,c   Su, Kaihong ^b,d  

^a SHANDONG UNIVERSITY   (China)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c SICHUAN UNIVERSITY   (China)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI CITRULLINATED PROTEIN ANTIBODY; ANTIGEN; AUTOANTIBODY; CITRULLINATED ANTIGEN; ENOLASE; OUTER MEMBRANE ANTIGEN; OUTER MEMBRANE PROTEIN; RECOMBINANT ANTIBODY; UNCLASSIFIED DRUG; CYCLIC CITRULLINATED PEPTIDE; CYCLOPEPTIDE; IMMUNOGLOBULIN;

ANTIBODY PRODUCTION; ANTIGEN ANTIBODY REACTION; ANTIGEN RECOGNITION; ARTICLE; CLINICAL ARTICLE; CLONING; CONTROLLED STUDY; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOBLOTTING; MASS SPECTROMETRY; NONHUMAN; PLASMABLAST; POLYMERASE CHAIN REACTION; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; PLASMA CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOBLOTTING; IMMUNOGLOBULINS; MASS SPECTROMETRY; PEPTIDES, CYCLIC; PLASMA CELLS; PORPHYROMONAS GINGIVALIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84963831507     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39455     Document Type: Article

References (46)

1. McInnes IB, Schett G., The pathogenesis of rheumatoid arthritis. N Engl J Med 2011; 365: 2205-19.
2. Firestein GS., Evolving concepts of rheumatoid arthritis. Nature 2003; 423: 356-61.
3. Van Venrooij WJ, van Beers JJ, Pruijn GJ., Anti-CCP antibodies: the past, the present and the future. Nat Rev Rheumatol 2011; 7: 391-8.
4. Van Venrooij WJ, Pruijn GJ., How citrullination invaded rheumatoid arthritis research. Arthritis Res Ther 2014; 16: 103.
5. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO III, et al., 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 2010; 62: 2569-81.
6. Masson-Bessiere C, Sebbag M, Girbal-Neuhauser E, Nogueira L, Vincent C, Senshu T, et al., The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the α- and β-chains of fibrin. J Immunol 2001; 166: 4177-84.
7. Vossenaar ER, Despres N, Lapointe E, van der Heijden A, Lora M, Senshu T, et al., Rheumatoid arthritis specific anti-Sa antibodies target citrullinated vimentin. Arthritis Res Ther 2004; 6: R142-50.
8. Kinloch A, Tatzer V, Wait R, Peston D, Lundberg K, Donatien P, et al., Identification of citrullinated α-enolase as a candidate autoantigen in rheumatoid arthritis. Arthritis Res Ther 2005; 7: R1421-9.
9. Kastbom A, Strandberg G, Lindroos A, Skogh T., Anti-CCP antibody test predicts the disease course during 3 years in early rheumatoid arthritis (the Swedish TIRA project). Ann Rheum Dis 2004; 63: 1085-9.
10. Ronnelid J, Wick MC, Lampa J, Lindblad S, Nordmark B, Klareskog L, et al., Longitudinal analysis of citrullinated protein/peptide antibodies (anti-CP) during 5 year follow up in early rheumatoid arthritis: anti-CP status predicts worse disease activity and greater radiological progression. Ann Rheum Dis 2005; 64: 1744-9.
11. Kroot EJ, de Jong BA, van Leeuwen MA, Swinkels H, van den Hoogen FH, van 't Hof M, et al., The prognostic value of anti-cyclic citrullinated peptide antibody in patients with recent-onset rheumatoid arthritis. Arthritis Rheum 2000; 43: 1831-5.
12. Vencovsky J, Machacek S, Sedova L, Kafkova J, Gatterova J, Pesakova V, et al., Autoantibodies can be prognostic markers of an erosive disease in early rheumatoid arthritis. Ann Rheum Dis 2003; 62: 427-30.
13. Kuhn KA, Kulik L, Tomooka B, Braschler KJ, Arend WP, Robinson WH, et al., Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J Clin Invest 2006; 116: 961-73.
14. Lundberg K, Nijenhuis S, Vossenaar ER, Palmblad K, van Venrooij WJ, Klareskog L, et al., Citrullinated proteins have increased immunogenicity and arthritogenicity and their presence in arthritic joints correlates with disease severity. Arthritis Res Ther 2005; 7: R458-67.
15. Thiele GM, Duryee MJ, Dusad A, Hunter CD, Lacy JP, Anderson DR, et al., Citrullinated mouse collagen administered to DBA/1J mice in the absence of adjuvant initiates arthritis. Int Immunopharmacol 2012; 13: 424-31.
16. Trouw LA, Haisma EM, Levarht EW, van der Woude D, Ioan-Facsinay A, Daha MR, et al., Anti-cyclic citrullinated peptide antibodies from rheumatoid arthritis patients activate complement via both the classical and alternative pathways. Arthritis Rheum 2009; 60: 1923-31.
17. Clavel C, Nogueira L, Laurent L, Iobagiu C, Vincent C, Sebbag M, et al., Induction of macrophage secretion of tumor necrosis factor α through Fcγ receptor IIa engagement by rheumatoid arthritis-specific autoantibodies to citrullinated proteins complexed with fibrinogen. Arthritis Rheum 2008; 58: 678-88.
18. Sokolove J, Zhao X, Chandra PE, Robinson WH., Immune complexes containing citrullinated fibrinogen costimulate macrophages via Toll-like receptor 4 and Fcγ receptor. Arthritis Rheum 2011; 63: 53-62.
19. Samuels J, Ng YS, Coupillaud C, Paget D, Meffre E., Impaired early B cell tolerance in patients with rheumatoid arthritis. J Exp Med 2005; 201: 1659-67.
20. Amara K, Steen J, Murray F, Morbach H, Fernandez-Rodriguez BM, Joshua V, 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 2013; 210: 445-55.
21. Oracki SA, Walker JA, Hibbs ML, Corcoran LM, Tarlinton DM., Plasma cell development and survival. Immunol Rev 2010; 237: 140-59.
22. Bellatin MF, Han M, Fallena M, Fan L, Xia D, Olsen N, et al., Production of autoantibodies against citrullinated antigens/peptides by human B cells. J Immunol 2012; 188: 3542-50.
23. Kerkman PF, Rombouts Y, van der Voort EI, Trouw LA, Huizinga TW, Toes RE, et al., Circulating plasmablasts/plasmacells as a source of anticitrullinated protein antibodies in patients with rheumatoid arthritis. Ann Rheum Dis 2013; 72: 1259-63.
24. Tan YC, Kongpachith S, Blum LK, Ju CH, Lahey LJ, Lu DR, et al., Barcode-enabled sequencing of plasmablast antibody repertoires in rheumatoid arthritis. Arthritis Rheumatol 2014; 66: 2706-15.
25. Kaur S, White S, Bartold PM., Periodontal disease and rheumatoid arthritis: a systematic review. J Dent Res 2013; 92: 399-408.
26. Bartold PM, Marino V, Cantley M, Haynes DR., Effect of Porphyromonas gingivalis-induced inflammation on the development of rheumatoid arthritis. J Clin Periodontol 2010; 37: 405-11.
27. Wegner N, Wait R, Sroka A, Eick S, Nguyen KA, Lundberg K, et al., Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 2010; 62: 2662-72.
28. 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: 315-24.
29. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC., Predominant autoantibody production by early human B cell precursors. Science 2003; 301: 1374-7.
30. Giudicelli V, Brochet X, Lefranc MP., IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb Protoc 2011; 2011: 695-715.
31. Mikuls TR, Payne JB, Yu F, Thiele GM, Reynolds RJ, Cannon GW, et al., Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol 2014; 66: 1090-100.
32. Friguet B, Chaffotte AF, Djavadi-Ohaniance L, Goldberg ME., Measurements of the true affinity constant in solution of antigen-antibody complexes by enzyme-linked immunosorbent assay. J Immunol Methods 1985; 77: 305-19.
33. 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: 3522-30.
34. Owczarczyk K, Lal P, Abbas AR, Wolslegel K, Holweg CT, Dummer W, et al., A plasmablast biomarker for nonresponse to antibody therapy to CD20 in rheumatoid arthritis. Sci Transl Med 2011; 3: 101ra92.
35. Vital EM, Dass S, Rawstron AC, Buch MH, Goeb V, Henshaw K, et al., Management of nonresponse to rituximab in rheumatoid arthritis: predictors and outcome of re-treatment. Arthritis Rheum 2010; 62: 1273-9.
36. Shlomchik MJ, Marshak-Rothstein A, Wolfowicz CB, Rothstein TL, Weigert MG., The role of clonal selection and somatic mutation in autoimmunity. Nature 1987; 328: 805-11.
37. Li S, Yu Y, Yue Y, Zhang J, Su K., Microbial infection and rheumatoid arthritis. J Clin Cell Immunol 2013; 4: 174.
38. Yoshimura F, Murakami Y, Nishikawa K, Hasegawa Y, Kawaminami S., Surface components of Porphyromonas gingivalis. J Periodontal Res 2009; 44: 1-12.
39. Lundberg K, Kinloch A, Fisher BA, Wegner N, Wait R, Charles P, et al., Antibodies to citrullinated α-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum 2008; 58: 3009-19.
40. Snir O, Widhe M, Hermansson M, von Spee C, Lindberg J, Hensen S, et al., Antibodies to several citrullinated antigens are enriched in the joints of rheumatoid arthritis patients. Arthritis Rheum 2010; 62: 44-52.
41. Wegner N, Lundberg K, Kinloch A, Fisher B, Malmstrom V, Feldmann M, et al., Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Immunol Rev 2010; 233: 34-54.
42. Ioan-Facsinay A, el-Bannoudi H, Scherer HU, van der Woude D, Menard HA, Lora M, 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 2011; 70: 188-93.
43. Van de Stadt LA, van Schouwenburg PA, Bryde S, Kruithof S, van Schaardenburg D, Hamann D, et al., Monoclonal anti-citrullinated protein antibodies selected on citrullinated fibrinogen have distinct targets with different cross-reactivity patterns. Rheumatology (Oxford) 2013; 52: 631-5.
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: 38-42.
45. 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: 263-9.
46. Totaro M, Cattani P, Ria F, Tolusso B, Gremese E, Fedele A, et al., Porphyromonas gingivalis and the pathogenesis of rheumatoid arthritis: analysis of various compartments including the synovial tissue. Arthritis Res Ther 2013; 15: R66.