Type II collagen antibody response is enriched in the synovial fluid of rheumatoid joints and directed to the same major epitopes as in collagen induced arthritis in primates and mice

Arthritis Research and Therapy

Volumn 16, Issue 4, 2014, Pages

  Lindh, Ingrid ^a   Snir, Omri ^b,d   Lönnblom, Erik ^a   Uysal, Hüseyin ^a,e   Andersson, Ida ^a   Nandakumar, Kutty S ^a   Vierboom, Michel ^c   't Hart, Bert ^c   Malmström, Vivianne ^b   Holmdahl, Rikard ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

^e ÇANAKKALE ONSEKIZ MART UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CITRULLINE PROTEIN ANTIBODY; COLLAGEN ANTIBODY; COLLAGEN TYPE 2; COLLAGEN TYPE 2 ANTIBODY; EPITOPE; HLA DRB1 ANTIGEN; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; AUTOANTIBODY; AUTOANTIGEN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY LIBRARY; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN BINDING; ARTHRITIS; ARTICLE; CALLITHRIX; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE COURSE; EPITOPE MAPPING; FEMALE; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; MALE; MOUSE; NONHUMAN; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; RHESUS MONKEY; RHEUMATOID ARTHRITIS; SYNOVIAL FLUID; SYNOVIAL FLUID LEVEL; ANIMAL; ANTIBODY PRODUCTION; BAGG ALBINO MOUSE; EXPERIMENTAL ARTHRITIS; IMMUNOLOGY; MIDDLE AGED; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIBODY FORMATION; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; AUTOANTIGENS; CALLITHRIX; COLLAGEN TYPE II; EPITOPES, B-LYMPHOCYTE; FEMALE; HUMANS; MACACA MULATTA; MALE; MICE; MICE, INBRED BALB C; MIDDLE AGED; SYNOVIAL FLUID; YOUNG ADULT;

EID: 84903808546     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4605     Document Type: Article

References (30)

1. Brink M, Hansson M, Mathsson L, Jakobsson P-J, Holmdahl R, Hallmans G, Stenlund H, Rönnelid J, Klareskog L, Dahlqvist SR. 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.
2. Holmdahl R, Malmström V, Vuorio E. Autoimmune recognition of cartilage collagens. Ann Med 1993, 25:251-264. 10.3109/07853899309147871, 8333924.
3. Cook AD, Rowley MJ, Mackay IR, Gough A, Emery P. Antibodies to type II collagen in early rheumatoid arthritis. Correlation with disease progression. Arthritis Rheum 1996, 39:1720-1727. 10.1002/art.1780391015, 8843863.
4. Mullazehi M, Wick MC, Klareskog L, van Vollenhoven R, Rönnelid J. Anti-type II collagen antibodies are associated with early radiographic destruction in rheumatoid arthritis. Arthritis Res Ther 2012, 14:R100. 10.1186/ar3825, 3446477, 22548748.
5. Holmdahl R, Rubin K, Klareskog L, Larsson E, Wigzell H. Characterization of the antibody response in mice with type II collagen-induced arthritis, using monoclonal anti-type II collagen antibodies. Arthritis Rheum 1986, 29:400-410. 10.1002/art.1780290314, 2421741.
6. Dobritzsch D, Lindh I, Uysal H, Nandakumar KS, Burkhardt H, Schneider G, Holmdahl R. Crystal structure of an arthritogenic anticollagen immune complex. Arthritis Rheum 2011, 63:3740-3748. 10.1002/art.30611, 22127694.
7. Raposo B, Dobritzsch D, Ge C, Ekman D, Xu B, Lindh I, Förster M, Uysal H, Nandakumar KS, Schneider G, Holmdahl R. Epitope-specific antibody response is controlled by immunoglobulin V(H) polymorphisms. J Exp Med 2014, 211:405-411. 10.1084/jem.20130968, 24534192.
8. Nandakumar KS, Bajtner E, Hill L, Böhm B, Rowley MJ, Burkhardt H, Holmdahl R. Arthritogenic antibodies specific for a major type II collagen triple-helical epitope bind and destabilize cartilage independent of inflammation. Arthritis Rheum 2008, 58:184-196. 10.1002/art.23049, 18163493.
9. Holmdahl R, Mo JA, Jonsson R, Karlstrom K, Scheynius A. Multiple epitopes on cartilage type II collagen are accessible for antibody binding in vivo. Autoimmunity 1991, 10:27-34. 10.3109/08916939108997144, 1720677.
10. Rowley MJ, Nandakumar KS, Holmdahl R. The role of collagen antibodies in mediating arthritis. Mod Rheumatol 2008, 18:429-441. 10.3109/s10165-008-0080-x, 18521704.
11. Snir O, Widhe M, Hermansson M, Spee Von C, Lindberg J, Hensen S, Lundberg K, Engström A, Venables PJW, Toes REM, Holmdahl R, Klareskog L, Malmström V. Antibodies to several citrullinated antigens are enriched in the joints of rheumatoid arthritis patients. Arthritis Rheum 2010, 62:44-52. 10.1002/art.25036, 20039432.
12. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988, 31:315-324. 10.1002/art.1780310302, 3358796.
13. Vierboom MPM, Breedveld E, Kondova I, 't Hart T. Collagen-induced arthritis in common marmosets: a new nonhuman primate model for chronic arthritis. Arthritis Res Ther 2010, 12:R200. 10.1186/ar3172, 2991037, 20977720.
14. Miller EJ, Rhodes RK. Preparation and characterization of the different types of collagen. Meth Enzymol 1982, 82:33-64.
15. Smith BD, Martin GR, Miller EJ, Dorfman A, Swarm R. Nature of the collagen synthesized by a transplanted chondrosarcoma. Arch Biochem Biophys 1975, 166:181-186. 10.1016/0003-9861(75)90378-1, 1122133.
16. Fields GB. Synthesis and biological applications of collagen-model triple-helical peptides. Org Biomol Chem 2010, 8:1237-1258. 10.1039/b920670a, 3951274, 20204190.
17. Frank S, Kammerer RA, Mechling D, Schulthess T, Landwehr R, Bann J, Guo Y, Lustig A, Bächinger HP, Engel J. Stabilization of short collagen-like triple helices by protein engineering. J Mol Biol 2001, 308:1081-1089. 10.1006/jmbi.2001.4644, 11352592.
18. Stetefeld J, Frank S, Jenny M, Schulthess T, Kammerer RA, Boudko S, Landwehr R, Okuyama K, Engel J. Collagen stabilization at atomic level: crystal structure of designed (GlyProPro)10foldon. Structure 2003, 11:339-346. 10.1016/S0969-2126(03)00025-X, 12623021.
19. Mo JA, Holmdahl R. The B cell response to autologous type II collagen: biased V gene repertoire with V gene sharing and epitope shift. J Immunol 1996, 157:2440-2448.
20. Wernhoff P, Unger C, Bajtner E, Burkhardt H, Holmdahl R. Identification of conformation-dependent epitopes and V gene selection in the B cell response to type II collagen in the DA rat. Int Immunol 2001, 13:909-919. 10.1093/intimm/13.7.909, 11431421.
21. Nandakumar KS, Lindqvist A-KB, Holmdahl R. A dominant suppressive MHC class II haplotype interacting with autosomal genes controls autoantibody production and chronicity of arthritis. Ann Rheum Dis 2011, 70:1664-1670. 10.1136/ard.2011.151738, 21613311.
22. Yoo TJ, Kim SY, Stuart JM, Floyd RA, Olson GA, Cremer MA, Kang AH. Induction of arthritis in monkeys by immunization with type II collagen. J Exp Med 1988, 168:777-782. 10.1084/jem.168.2.777, 2189004, 3411292.
23. Grab B, Miles AJ, Furcht LT, Fields GB. Promotion of fibroblast adhesion by triple-helical peptide models of type I collagen-derived sequences. J Biol Chem 1996, 271:12234-12240. 10.1074/jbc.271.21.12234, 8647820.
24. Mo JA, Scheynius A, Nilsson S, Holmdahl R. Germline-encoded IgG antibodies bind mouse cartilage in vivo: epitope- and idiotype-specific binding and inhibition. Scand J Immunol 1994, 39:122-130. 10.1111/j.1365-3083.1994.tb03350.x, 7507597.
25. Cao D, Khmaladze I, Jia H, Bajtner E, Nandakumar KS, Blom T, Mo JA, Holmdahl R. Pathogenic autoreactive B cells are not negatively selected toward matrix protein collagen II. J Immunol 2011, 187:4451-4458. 10.4049/jimmunol.1101378, 21940677.
26. Burkhardt H, Hüffmeier U, Spriewald B, Böhm B, Rau R, Kallert S, Engström A, Holmdahl R, Reis A. Association between protein tyrosine phosphatase 22 variant R620W in conjunction with the HLA-DRB1 shared epitope and humoral autoimmunity to an immunodominant epitope of cartilage-specific type II collagen in early rheumatoid arthritis. Arthritis Rheum 2006, 54:82-89. 10.1002/art.21498, 16385499.
27. Cook AD, Stockman A, Brand CA, Tait BD, Mackay IR, Muirden KD, Bernard CC, Rowley MJ. Antibodies to type II collagen and HLA disease susceptibility markers in rheumatoid arthritis. Arthritis Rheum 1999, 42:2569-2576. 10.1002/1529-0131(199912)42:12<2569::AID-ANR9>3.0.CO;2-3, 10616002.
28. Förster M, Raposo B, Ekman D, Klaczkowska D, Popovic M, Nandakumar KS, Lindvall T, Hultqvist M, Teneva I, Johannesson M, Ahlqvist E, Holmdahl R. Genetic control of antibody production during collagen-induced arthritis development in heterogeneous stock mice. Arthritis Rheum 2012, 64:3594-3603. 10.1002/art.34658, 22886420.
29. Uysal H, Bockermann R, Nandakumar KS, Sehnert B, Bajtner E, Engström A, Serre G, Burkhardt H, Thunnissen MMGM, Holmdahl R. Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis. J Exp Med 2009, 206:449-462. 10.1084/jem.20081862, 2646582, 19204106.
30. Haag S, Schneider N, Mason DE, Tuncel J, Andersson IE, Peters EC, Burkhardt H, Holmdahl R. Mass spectrometric analysis of citrullinated type II collagen reveals new citrulline-specific autoantibodies, which bind to human arthritic cartilage. Arthritis Rheumatol 2014, 66:1440-1449. 10.1002/art.38383, 24470447.