Type II collagen-specific antibodies induce cartilage damage in mice independent of inflammation

Arthritis and Rheumatism

Volumn 65, Issue 3, 2013, Pages 650-659

  Croxford, Allyson M ^a   Whittingham, Senga ^a   McNaughton, Donald ^a   Nandakumar, Kutty Selva ^b   Holmdahl, Rikard ^b   Rowley, Merrill J ^a  

^a MONASH UNIVERSITY   (Australia)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; COLLAGEN; COLLAGEN TYPE 2; COMPLEMENT COMPONENT C5; LIPOPOLYSACCHARIDE; MONOCLONAL ANTIBODY; PROTEOGLYCAN; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL HYPERPLASIA; CELL SURFACE; COLLAGEN ANTIBODY INDUCED ARTHRITIS; CONTROLLED STUDY; DISEASE MODEL; HISTOPATHOLOGY; IMMUNE RESPONSE; INFLAMMATION; INFRARED SPECTROSCOPY; INTERPHALANGEAL JOINT; MICROSCOPY; MORPHOMETRICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; RHEUMATOID ARTHRITIS; SYNCHROTRON;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; CARTILAGE, ARTICULAR; CHONDROCYTES; COLLAGEN TYPE II; DISEASE MODELS, ANIMAL; EPITOPES; HUMANS; HYBRIDOMAS; MICE; MICE, CONGENIC; MICE, KNOCKOUT; PROTEOGLYCANS; SPECIES SPECIFICITY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84874425084     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.37805     Document Type: Article

References (51)

1. Holmdahl R, Andersson M, Goldschmidt TJ, Gustafsson K, Jansson L, Mo JA,. Type II collagen autoimmunity in animals and provocations leading to arthritis. Immunol Rev 1990; 118: 193-232.
2. 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: 400-10.
3. Schulte S, Unger C, Mo JA, Wendler O, Bauer E, Frischholz S, 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 1998; 273: 1551-61.
4. Terato K, Hasty KA, Reife RA, Cremer MA, Kang AH, Stuart JM,. Induction of arthritis with monoclonal antibodies to collagen. J Immunol 1992; 148: 2103-8.
5. Nandakumar KS, Svensson L, Holmdahl R,. Collagen type II-specific monoclonal antibody-induced arthritis in mice: description of the disease and the influence of age, sex, and genes. Am J Pathol 2003; 163: 1827-37.
6. Nandakumar KS, Holmdahl R,. Antibody-induced arthritis: disease mechanisms and genes involved at the effector phase of arthritis. Arthritis Res Ther 2006; 8: 223.
7. Wipke BT, Wang Z, Nagengast W, Reichert DE, Allen PM,. Staging the initiation of autoantibody-induced arthritis: a critical role for immune complexes. J Immunol 2004; 172: 7694-702.
8. Crombie DE, Turer M, Zuasti BB, Wood B, McNaughton D, Nandakumar KS, et al. Destructive effects of murine arthritogenic antibodies to type II collagen on cartilage explants in vitro. Arthritis Res Ther 2005; 7: R927-37.
9. Croxford AM, Crombie D, McNaughton D, Holmdahl R, Nandakumar KS, Rowley MJ,. Specific antibody protection of the extracellular cartilage matrix against collagen antibody-induced damage. Arthritis Rheum 2010; 62: 3374-84.
10. Amirahmadi SF, Pho MH, Gray RE, Crombie DE, Whittingham SF, Zuasti BB, et al. An arthritogenic monoclonal antibody to type II collagen, CII-C1, impairs cartilage formation by cultured chondrocytes. Immunol Cell Biol 2004; 82: 427-34.
11. Amirahmadi SF, Whittingham S, Crombie DE, Nandakumar KS, Holmdahl R, Mackay IR, et al. Arthritogenic anti-type II collagen antibodies are pathogenic for cartilage-derived chondrocytes independent of inflammatory cells. Arthritis Rheum 2005; 52: 1897-906.
12. 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: 2440-8.
13. Bajtner E, Nandakumar KS, Engstrom A, Holmdahl R,. Chronic development of collagen-induced arthritis is associated with arthritogenic antibodies against specific epitopes on type II collagen. Arthritis Res Ther 2005; 7: R1148-57.
14. Dobritzsch D, Lindh I, Uysal H, Nandakumar KS, Burkhardt H, Schneider G, et al. Crystal structure of an arthritogenic anticollagen immune complex. Arthritis Rheum 2011; 63: 3740-8.
15. Nandakumar KS, Holmdahl R,. Efficient promotion of collagen antibody induced arthritis (CAIA) using four monoclonal antibodies specific for the major epitopes recognized in both collagen induced arthritis and rheumatoid arthritis. J Immunol Methods 2005; 304: 126-36.
16. Johansson AC, Sundler M, Kjellen P, Johannesson M, Cook A, Lindqvist AK, et al. Genetic control of collagen-induced arthritis in a cross with NOD and C57BL/10 mice is dependent on gene regions encoding complement factor 5 and FcγRIIb and is not associated with loci controlling diabetes. Eur J Immunol 2001; 31: 1847-56.
17. Kiraly K, Lapvetelainen T, Arokoski J, Torronen K, Modis L, Kiviranta I, et al. Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry. Histochem J 1996; 28: 577-90.
18. Mankin HJ, Dorfman H, Lippiello L, Zarins A,. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 1971; 53: 523-37.
19. Van der Sluijs JA, Geesink RG, van der Linden AJ, Bulstra SK, Kuyer R, Drukker J,. The reliability of the Mankin score for osteoarthritis. J Orthop Res 1992; 10: 58-61.
20. Croxford AM, Nandakumar KS, Holmdahl R, Tobin MJ, McNaughton D, Rowley MJ,. Chemical changes demonstrated in cartilage by synchrotron infrared microspectroscopy in an antibody- induced murine model of rheumatoid arthritis. J Biomed Opt 2011; 16: 066004.
21. Lasch P, Haensch W, Naumann D, Diem M,. Imaging of colorectal adenocarcinoma using FT-IR microspectroscopy and cluster analysis. Biochim Biophys Acta 2004; 1688: 176-86.
22. Wood BR, Tait B, McNaughton D,. Fourier transform infrared spectroscopy as a method for monitoring the molecular dynamics of lymphocyte activation. Appl Spectrosc 2000; 54: 353-9.
23. Petibois C, Gouspillou G, Wehbe K, Delage JP, Deleris G,. Analysis of type I and IV collagens by FT-IR spectroscopy and imaging for a molecular investigation of skeletal muscle connective tissue. Anal Bioanal Chem 2006; 386: 1961-6.
24. Oakes BW, Handley CJ, Lisner F, Lowther DA,. An ultrastructural and biochemical study of high density primary cultures of embryonic chick chondrocytes. J Embryol Exp Morphol 1977; 38: 239-63.
25. Urban JP, Hall AC, Gehl KA,. Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes. J. Cell Physiol 1993; 154: 262-70.
26. Nandakumar KS, Bajtner E, Hill L, Bohm B, Rowley MJ, Burkhardt H, et al. Arthritogenic antibodies specific for a major type II collagen triple-helical epitope bind and destabilize cartilage independent of inflammation. Arthritis Rheum 2008; 58: 184-96.
27. Jonsson R, Karlsson AL, Holmdahl R,. Demonstration of immunoreactive sites on cartilage after in vivo administration of biotinylated anti-type II collagen antibodies. J Histochem Cytochem 1989; 37: 265-8.
28. 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.
29. Lin PM, Chen CT, Torzilli PA,. Increased stromelysin-1 (MMP-3), proteoglycan degradation (3B3- and 7D4) and collagen damage in cyclically load-injured articular cartilage. Osteoarthritis Cartilage 2004; 12: 485-96.
30. Fosang AJ, Stanton H, Little CB, Atley LM,. Neoepitopes as biomarkers of cartilage catabolism. Inflamm Res 2003; 52: 277-82.
31. Aigner T, Kim HA,. Apoptosis and cellular viability: issues in osteoarthritic cartilage degeneration [review]. Arthritis Rheum 2002; 46: 1986-96.
32. Sandell LJ, Aigner T,. Articular cartilage and changes in arthritis: cell biology of osteoarthritis. Arthritis Res 2001; 3: 107-13.
33. Yang C, Li SW, Helminen HJ, Khillan JS, Bao Y, Prockop DJ,. Apoptosis of chondrocytes in transgenic mice lacking collagen II. Exp Cell Res 1997; 235: 370-3.
34. Muir H,. The chondrocyte, architect of cartilage: biomechanics, structure, function and molecular biology of cartilage matrix macromolecules. Bioessays 1995; 17: 1039-48.
35. Carlsen S, Nandakumar KS, Holmdahl R,. Type IX collagen deficiency enhances the binding of cartilage-specific antibodies and arthritis severity. Arthritis Res Ther 2006; 8: R102.
36. Rowley MJ, Nandakumar KS, Holmdahl R,. The role of collagen antibodies in mediating arthritis [review]. Mod Rheumatol 2008; 18: 429-41.
37. Uysal H, Bockermann R, Nandakumar KS, Sehnert B, Bajtner E, Engstrom A, et al. Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis. J Exp Med 2009; 206: 449-62.
38. Klareskog L, Johnell O, Hulth A, Holmdahl R, Rubin K,. Reactivity of monoclonal anti-type II collagen antibodies with cartilage and synovial tissue in rheumatoid arthritis and osteoarthritis. Arthritis Rheum 1986; 29: 730-8.
39. Kopp S, Mejersjo C, Clemensson E,. Induction of osteoarthrosis in the guinea pig knee by papain. Oral Surg Oral Med Oral Pathol 1983; 55: 259-66.
40. Murat N, Karadam B, Ozkal S, Karatosun V, Gidener S,. Quantification of papain-induced rat osteoarthritis in relation to time with the Mankin score. Acta Orthop Traumatol Turc 2007; 41: 233-7. In Turkish.
41. Van der Kraan PM, Vitters EL, van de Putte LB, van den Berg WB,. Development of osteoarthritic lesions in mice by "metabolic" and "mechanical" alterations in the knee joints. Am J Pathol 1989; 135: 1001-14.
42. Cook AD, Rowley MJ, Stockman A, Muirden KD, Mackay IR,. Specificity of antibodies to type II collagen in early rheumatoid arthritis. J Rheumatol 1994; 21: 1186-9.
43. Ronnelid J, Lysholm J, Engstrom-Laurent A, Klareskog L, Heyman B,. Local anti-type II collagen antibody production in rheumatoid arthritis synovial fluid: evidence for an HLA-DR4- restricted IgG response. Arthritis Rheum 1994; 37: 1023-9.
44. Jasin HE,. Autoantibody specificities of immune complexes sequestered in articular cartilage of patients with rheumatoid arthritis and osteoarthritis. Arthritis Rheum 1985; 28: 241-8.
45. Pereira RS, Black CM, Duance VC, Jones VE, Jacoby RK, Welsh KI,. Disappearing collagen antibodies in early rheumatoid arthritis: correlation with disease progression. Lancet 1985; 2: 501-2.
46. Fujii K, Tsuji M, Kitamura A, Murato K,. The diagnostic significance of anti-type II collagen antibodies assay in rheumatoid arthritis. Int Orthop 1992; 16: 272-6.
47. 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: 1720-7.
48. Cook AD, Gray R, Ramshaw J, Mackay IR, Rowley MJ,. Antibodies against the CB10 fragment of type II collagen in rheumatoid arthritis. Arthritis Res Ther 2004; 6: R477-83.
49. Burkhardt H, Koller T, Engstrom A, Nandakumar KS, Turnay J, Kraetsch HG, et al. 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 2002; 46: 2339-48.
50. Mewar D, Wilson AG,. Autoantibodies in rheumatoid arthritis: a review. Biomed Pharmacother 2006; 60: 648-55.
51. 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.