Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis

Journal of Experimental Medicine

Volumn 206, Issue 2, 2009, Pages 449-462

  Uysal, Hüseyin ^a,c   Bockermann, Robert ^b   Nandakumar, Kutty S ^b,c   Sehnert, Bettina ^d   Bajtner, Estelle ^b   Engström, Åke ^e   Serre, Guy ^f   Burkhardt, Harald ^g   Thunnissen, Marjolein M G M ^a   Holmdahl, Rikard ^b,c  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e UPPSALA UNIVERSITY   (Sweden)

^f Institut Federatif de Biologie   (France)

^g GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CITRULLINE; COLLAGEN TYPE 2; EPITOPE; IMMUNOGLOBULIN F(AB) FRAGMENT; MONOCLONAL ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ANTIBODY STRUCTURE; ARTHRITIS; ARTICLE; AUTOIMMUNITY; CARTILAGE; CONFORMATION; CONTROLLED STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PRIORITY JOURNAL; SYNOVIAL FLUID; SYNOVIUM; ANIMAL; CHEMICAL STRUCTURE; COMPARATIVE STUDY; DNA SEQUENCE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; IMMUNOPRECIPITATION; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ARTHRITIS, EXPERIMENTAL; AUTOIMMUNITY; BASE SEQUENCE; CITRULLINE; COLLAGEN TYPE II; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOGLOBULIN FAB FRAGMENTS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SEQUENCE ANALYSIS, DNA; SYNOVIAL FLUID;

EID: 63049101247     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20081862     Document Type: Article

References (60)

1. Aho, K., T. Palosuo, V. Raunio, P. Puska, A. Aromaa, and J.T. Salonen. 1985. When does rheumatoid disease start? Arthritis Rheum. 28:485-489.
2. Schellekens, G.A., B.A. de Jong, F.H. van den Hoogen, L.B. van de Putte, and W.J. van Venrooij. 1998. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J. Clin. Invest. 101:273-281.
3. Girbal-Neuhauser, E., J.J. Durieux, M. Arnaud, P. Dalbon, M. Sebbag, G. Vincent, M. Simon, T. Senshu, C. Masson-Bessiére, C. J olivet- Reynaud, et al. 1999. The epitopes targeted by the rheumatoid arthritis- associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (pro)filaggrin by deimination of arginine residues. J. Immunol. 162:585-594.
4. Vossenaar, E.R., A.J. Zendman, W.J. van Venrooij, and G.J. Pruijn. 2003. PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays. 25:1106-1118.
5. Vossenaar, E.R., S. Nijenhuis, M.M. Helsen, A. van der Heijden, T. Senshu, W.B. van den Berg, W.J. van Venrooij, and L.A. Joosten. 2003. Citrullination of synovial proteins in murine models of rheumatoid arthritis. Arthritis Rheum. 48:2489-2500.
6. Chang, X., R. Yamada, A. Suzuki, Y. Kochi, T. Sawada, and K. Yamamoto. 2005. Citrullination of fibronectin in rheumatoid arthritis synovial tissue. Rheumatology (Oxford). 44:1374-1382.
7. Vossenaar, E.R., T.R. Radstake, A. van der Heijden, M.A. van Mansum, C. Dieteren, D.J. de Rooij, P. Barrera, A.J. Zendman, and W.J. van Venrooij. 2004. Expression and activity of citrullinating pep- tidylarginine deiminase enzymes in monocytes and macrophages. Ann. Rheum. Dis. 63:373-381.
8. Baeten, D., I. Peene, A. Union, L. Meheus, M. Sebbag, G. Serre, E.M. Veys, and F. De Keyser. 2001. Specific presence of intracellular citrullinated proteins in rheumatoid arthritis synovium: relevance to antifilag- grin autoantibodies. Arthritis Rheum. 44:2255-2262.
9. Foulquier, C., M. Sebbag, C. Clavel, S. Chapuy-Regaud, R. Al Badine, M.C. Mechin, C. Vincent, R. Nachat, M. Yamada, H. Takahara, et al. 2007. Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation. Arthritis Rheum. 56:3541-3553.
10. Schwab, B.L., D. Guerini, C. Didszun, D. Bano, E. Ferrando-May, E. Fava, J. Tam, D. Xu, S. Xanthoudakis, D.W. Nicholson, et al. 2002. Cleavage of plasma membrane calcium pumps by caspases: a link between apoptosis and necrosis. Cell Death Differ. 9:818-831.
11. Masson-Bessiere, C., M. Sebbag, J.J. Durieux, L. Nogueira, C. Vincent, E. Girbal-Neuhauser, R. Durroux, A. Cantagrel, and G. Serre. 2000. In the rheumatoid pannus, anti-filaggrin autoantibodies are produced by local plasma cells and constitute a higher proportion of IgG than in synovial fluid and serum. Clin. Exp. Immunol. 119:544-552.
12. Caspi, D., M. Anouk, I. Golan, D. Paran, I. Kaufman, I. Wigler, D. Levartovsky, I. Litinsky, and O. Elkayam. 2006. Synovial fluid levels of anti-cyclic citrullinated peptide antibodies and IgA rheumatoid factor in rheumatoid arthritis, psoriatic arthritis, and osteoarthritis. Arthritis Rheum. 55:53-56.
13. Rantapää-Dahlqvist, S., B.A. de Jong, E. Berglin, G. Hallmans, G. Wadell, H. Stenlund, U. Sundin, and W.J. van Venrooij. 2003. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum. 48:2741-2749.
14. Reparon-Schuijt, C.C., W.J. van Esch, C. van Kooten, G.A. Schellekens, B.A. de Jong, W.J. van Venrooij, F.C. Breedveld, and C.L. Verweij. 2001. Secretion of anti-citrulline-containing peptide antibody by B lymphocytes in rheumatoid arthritis. Arthritis Rheum. 44:41-47.
15. Masson-Bessiere, C., M. Sebbag, E. Girbal-Neuhauser, L. Nogueira, C. Vincent, T. Senshu, and G. Serre. 2001. The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alpha- and beta-chains of fibrin. J. Immunol. 166:4177-4184.
16. Hill, J.A., D.A. Bell, W. Brintnell, D. Yue, B. Wehrli, A.M. Jevnikar, D.M. Lee, W. Hueber, W.H. Robinson, and E. Cairns. 2008. Arthritis induced by posttranslationally modified (citrullinated) fibrinogen in DR4-IE transgenic mice. J. Exp. Med. 205:967-979.
17. Chapuy-Regaud, S., M. Sebbag, D. Baeten, C. Clavel, C. Foulquier, F. De Keyser, and G. Serre. 2005. Fibrin deimination in synovial tissue is not specific for rheumatoid arthritis but commonly occurs during synovitides. J. Immunol. 174:5057-5064.
18. Hill, J.A., S. Southwood, A. Sette, A.M. Jevnikar, D.A. Bell, and E. Cairns. 2003. 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. 171:538-541.
19. Molberg, O., S.N. McAdam, R. Korner, H. Quarsten, C. Kristiansen, L. Madsen, L. Fugger, H. Scott, O. Noren, P. Roepstorff, et al. 1998. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat. Med. 4:713-717.
20. Backlund, J., S. Carlsen, T. Hoger, B. Holm, L. Fugger, J. Kihlberg, H. Burkhardt, and R. Holmdahl. 2002. Predominant selection of T cells specific for glycosylated collagen type II peptide (263-270) in humanized transgenic mice and in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA. 99:9960-9965.
21. Brunsberg, U., K. Gustafsson, L. Jansson, E. Michaelsson, L. Ahrlund- Richter, S. Pettersson, R. Mattsson, and R. Holmdahl. 1994. Expression of a transgenic class II Ab gene confers susceptibility to collagen-induced arthritis. Eur. J. Immunol. 24:1698-1702.
22. Michaëlsson, E., M. Andersson, A. Engstrom, and R. Holmdahl. 1992. Identification of an immunodominant type-II collagen peptide recognized by T cells in H-2q mice: self tolerance at the level of determinant selection. Eur. J. Immunol. 22:1819-1825.
23. Burkhardt, H., T. Koller, A. Engström, K.S. Nandakumar, J. Turnay, H.G. Kraetsch, J.R. Kalden, and R. Holmdahl. 2002. Epitope-specific recognition of type II collagen by rheumatoid arthritis antibodies is shared with recognition by antibodies that are arthritogenic in collagen- induced arthritis in the mouse. Arthritis Rheum. 46:2339-2348.
24. Schulte, S., C. Unger, J.A. Mo, O. Wendler, E. Bauer, S. Frischholz, K. von der Mark, J.R. Kalden, R. Holmdahl, and H. Burkhardt. 1998. Arthritis-related B cell epitopes in collagen II are conformation-dependent and sterically privileged in accessible sites of cartilage collagen fibrils. J. Biol. Chem. 273:1551-1561.
25. Burkhardt, H., B. Sehnert, R. Bockermann, A. Engstrom, J.R. Kalden, and R. Holmdahl. 2005. Humoral immune response to citrullinated collagen type II determinants in early rheumatoid arthritis. Eur. J. Immunol. 35:1643-1652.
26. Stanfield, R.L., A. Zemla, I.A. Wilson, and B. Rupp. 2006. Antibody elbow angles are influenced by their light chain class. J. Mol. Biol. 357:1566-1574.
27. Krissinel, E., and K. Henrick. 2005. Detection of protein assemblies in crystals. In Computational Life Sciences. First International Symposium, CompLife 2005, Konstanz, Germany, September 25-27, 2005, Proceedings. M.R. Berthold, R. Glen, K. Diederichs, O. Kohlbacher, and I. Fischer, editors. Springer, Berlin/Heidelberg, Germany. 163-174.
28. Hoffmann, M.H., J. Tuncel, K. Skriner, M. Tohidast- Akrad, B. Turk, S. Pinol- Roma, G. Serre, G. Schett, J.S. Smolen, R. Holmdahl, and G. Steiner. 2007. The rheumatoid arthritis-associated autoantigen hnRNP- A2 (RA33) is a major stimulator of autoimmunity in rats with pristane- induced arthritis. J. Immunol. 179:7568-7576.
29. Kuhn, K.A., L. Kulik, B. Tomooka, K.J. Braschler, W.P. Arend, W.H. Robinson, and V.M. Holers. 2006. Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J. Clin. Invest. 116:961-973.
30. Kanazawa, S., S. Ota, C. Sekine, T. Tada, T. Otsuka, T. Okamoto, G. S0nderstrup, and B.M. Peterlin. 2006. Aberrant MHC class II expression in mouse joints leads to arthritis with extraarticular manifestations similar to rheumatoid arthritis. Proc. Natl. Acad. Sci. USA. 103:14465-14470.
31. Kidd, B.A., P.P. Ho, O. Sharpe, X. Zhao, B.H. Tomooka, J.L. Kanter, L. Steinman, and W.H. Robinson. 2008. Epitope spreading to citrulli- nated antigens in mouse models of autoimmune arthritis and demyelin- ation. Arthritis Res. Ther. 10:R119.
32. Dyson, H.J., and P.E. Wright. 1995. Antigenic peptides. FASEB J. 9:37-42.
33. Nair, D.T., K. Singh, Z. Siddiqui, B.P. Nayak, K.V. Rao, and D.M. Salunke. 2002. Epitope recognition by diverse antibodies suggests conformational convergence in an antibody response. J. Immunol. 168:2371-2382.
34. Tarcsa, E., L.N. Marekov, G. Mei, G. Melino, S.C. Lee, and P.M. Steinert. 1996. Protein unfolding by peptidylarginine deiminase. Substrate specificity and structural relationships of the natural substrates trichohya- lin and filaggrin. J. Biol. Chem. 271:30709-30716.
35. Bella, J., M. Eaton, B. Brodsky, and H.M. Berman. 1994. Crystal and molecular structure of a collagen-like peptide at 1.9 A resolution. Science. 266:75-81.
36. Emsley, J., C.G. Knight, R.W. Farndale, M.J. Barnes, and R.C. Liddington. 2000. Structural basis of collagen recognition by integrin alpha2beta1. Cell. 101:47-56.
37. Emsley, J., C.G. Knight, R.W. Farndale, and M.J. Barnes. 2004. Structure of the integrin alpha2beta1-binding collagen peptide. J. Mol. Biol. 335:1019-1028.
38. Stetefeld, J., S. Frank, M. J enny, T. Schulthess, R.A. Kammerer, S. Boudko, R. Landwehr, K. Okuyama, and J. Engel. 2003. Collagen stabilization at atomic level: crystal structure of designed (GlyProPro)10foldon. Structure. 11:339-346.
39. Zong, Y., Y. Xu, X. Liang, D.R. Keene, A. Hook, S. Gurusiddappa, M. Hook, and S.V. Narayana. 2005. A 'Collagen Hug' model for Staphylococcus aureus CNA binding to collagen. EMBO J. 24:4224-4236.
40. Vossenaar, E.R., T.J. Smeets, M.C. Kraan, J.M. Raats, W.J. van Venrooij, and P.P. Tak. 2004. The presence of citrullinated proteins is not specific for rheumatoid synovial tissue. Arthritis Rheum. 50:3485-3494.
41. Rosloniec, E.F., D.D. Brand, L.K. Myers, K.B. Whittington, M. Gumanovskaya, D.M. Zaller, A. Woods, D.M. Altmann, J.M. Stuart, and A.H. Kang. 1997. An HLA-DR1 transgene confers susceptibility to collagen-induced arthritis elicited with human type II collagen. J. Exp. Med. 185:1113-1122.
42. Andersson, E.C., B.E. Hansen, H. Jacobsen, L.S. Madsen, C.B. Andersen, J. Engberg, J.B. Rothbard, G.S. McDevitt, V. Malmstrom, R. Holmdahl, et al. 1998. Definition of MHC and T cell receptor contacts in the HLA- DR4 restricted immunodominant epitope in type II collagen and characterization of collagen-induced arthritis in HLA-DR4 and human CD4 transgenic mice. Proc. Natl. Acad. Sci. USA. 95:7574-7579.
43. von Delwig, A., D.M. Altmann, J.D. Isaacs, C.V. Harding, R. Holmdahl, N. McKie, and J.H. Robinson. 2006. The impact of glycosylation on HLA-DR1-restricted T cell recognition of type II collagen in a mouse model. Arthritis Rheum. 54:482-491.
44. van der Helm-van Mil, A.H., K.N. Verpoort, S. le Cessie, T.W. Huizinga, R.R. de Vries, and R.E. Toes. 2006. The HLA-DRB1 shared epitope alleles are primarily a risk factor for anti-cyclic citrul- linated peptide antibodies and are not an independent risk factor for development of rheumatoid arthritis. Arthritis Rheum. 54:1117-1121.
45. Auger, I., M. Sebbag, C. Vincent, N. Balandraud, S. Guis, L. Nogueira, B. Svensson, A. Cantagrel, G. Serre, and J. Roudier. 2005. Influence of HLA-DR genes on the production of rheumatoid arthritis-specific autoantibodies to citrullinated fibrinogen. Arthritis Rheum. 52:3424-3432.
46. Grab, B., A.J. Miles, L.T. Furcht, and G.B. Fields. 1996. Promotion of fibroblast adhesion by triple-helical peptide models of type I collagen- derived sequences. J. Biol. Chem. 271:12234-12240.
47. Schellekens, G.A., H. Visser, B.A. de Jong, F.H. van den Hoogen, J.M. Hazes, F.C. Breedveld, and W.J. van Venrooij. 2000. The diagnostic properties of rheumatoid arthritis antibodies recognizing a cyclic citrul- linated peptide. Arthritis Rheum. 43:155-163.
48. Vander Cruyssen, B., T. Cantaert, L. Nogueira, C. Clavel, L. De Rycke, A. Dendoven, M. Sebag, D. Deforce, C. Vincent, D. Elewaut, et al. 2006. Diagnostic value of anti-human citrullinated fibrinogen ELISA and comparison with four other anti - citrullinated protein assays. Arthritis Res. Ther. 8:R122.
49. Nandakumar, K.S., B. Johansson, L. Bjorck, and R. Holmdahl. 2007. Blocking of experimental arthritis by cleavage of IgG antibodies in vivo. Arthritis Rheum. 56:3253-3260.
50. Giudicelli, V., D. Chaume, and M.P. Lefranc. 2004. IMGT/V- QUEST, an integrated software program for immunoglobulin and T cell receptor V-J and V-D-J rearrangement analysis. Nucleic Acids Res. 32:W435-W440.
51. Yousfi Monod, M., V. Giudicelli, D. Chaume, and M.P. Lefranc. 2004. IMGT/JunctionAnalysis: the first tool for the analysis of the immuno- globulin and T cell receptor complex V-J and V-D-J JUNCTIONs. Bioinformatics. 20:i379-i385.
52. Lefranc, M.P., V. Giudicelli, C. Ginestoux, N. Bosc, G. Folch, D. Guiraudou, J. Jabado-Michaloud, S. Magris, D. Scaviner, V. Thouvenin, et al. 2004. IMGT-ONTOLOGY for immunogenetics and immuno- informatics. In Silico Biol. 4:17-29.
53. Kabsch, W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Cryst. 26:795-800.
54. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
55. Read, R.J. 2001. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 57:1373-1382.
56. Uysal, H., B. Sehnert, K.S. Nandakumar, U. Boiers, H. Burkhardt, R. Holmdahl, and M.M.G.M. Thunnissen. 2008. The crystal structure of the pathogenic collagen type II specific mouse monoclonal antibody CIIC1 Fab: structure to function analysis. Mol. Immunol. 45:2196-2204.
57. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
58. Murshudov, G.N., A.A. Vagin, and E.J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
59. Winn, M.D., M.N. Isupov, and G.N. Murshudov. 2001. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57:122-133.
60. DeLano, W.L. 2002. Unraveling hot spots in binding interfaces: progress and challenges. Curr. Opin. Struct. Biol. 12:14-20.