Collagen induced arthritis as an experimental model for rheumatoid arthritis. Immunogenetics, pathogenesis and autoimmunity

APMIS

Volumn 97, Issue 7, 1989, Pages 575-584

  Holmdahl, R ^a   Andersson, M E ^a   Goldschmidt, T J ^a   Jansson, L ^a   Karlsson, M ^a   Malmstrom, V ^a   Mo, J ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; COLLAGEN TYPE 2; GAMMA INTERFERON; RHEUMATOID FACTOR;

ANIMAL MODEL; ARTHRITIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS;

EID: 0024338671     PISSN: 09034641     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1699-0463.1989.tb00446.x     Document Type: Review

References (82)

1. Banerjee, S., Haqqi, T. M., Luthra, H. S., Stuart, J. M. & David, C. S.: Possible role of Vβ T cell receptor genes in susceptibility to collagen‐induced arthritis in mice. J. Exp. Med. 167: 832–839, 1988.
2. Boissier, M. C., Carlioz, A. & Fournier, C.: Experimental autoimmune arthritis in mice. II. Early events in the elicitation of the autoimmune phenomenon induced by homologous type II collagen. Clin. Immunol. Immunopathol. 48: 225–237, 1988.
3. Buchan, G., Barrett, K., Fujita, T., Taniguchi, T., Maini, R. & Feldmann, M.: Detections of activated T cell products in the rheumatoid joint using cDNA probes to interleukin‐2 (IL‐2), IL‐2 receptor and IFN‐gamma. Clin. exp. Immunol. 71: 295–301, 1988.
4. Burmester, G. R., Jahn, B., Gramatzki, M., Zacher, J. & Kalden, J. R.: Activated T cells in vitro and in vivo: Divergence in expression of Tac and Ia antigens in the nonblastoid small T cells of inflammation and normal T cells activated in vitro. J. Immunol. 133: 1230–1234, 1984.
5. Butler, L., Simmons, B., Zimmerman, J., DeRiso, P. & Phadke, K.: Characteristics of cellular immune response to collagen type I or collagen type II. Cell. Immunol. 100: 314–330, 1986.
6. Carlson, R. P., Balzek, E. M., Datko, L. J. & Lewis, A. J.: Humoral and cellular immunological responses in collagen‐induced arthritis in rats: their correlation with severity of arthritis. J. Immunopharmacol. 6: 379–388, 1984.
7. Carson, D. A., Chen, P. P., Fox, R. I., Kipps, T. J., Jirik, F., Goldfien, R. D., Silverman, G., Radoux, V. & Fong, S.: Rheumatoid factor and immune networks. Ann. Rev. Immunol. 5: 109–126, 1987.
8. Caulfield, J. P., Hein, A., Dynesius‐Trentham, R. & Trentham, D. E.: Morphologic demonstration of two stages in the development of type II collagen‐induced arthritis. Lab. Invest. 46: 321–343, 1982.
9. Chang, Y.‐H., Pearson, C. M. & Abe, C.: Adjuvant polyarthritis. IV. Induction by a synthetic adjuvant: Immunologic, histopathologic, and other studies. Arthritis Rheum. 23: 62–71, 1980.
10. Claque, R. B. & Moore, L. J.: IgG and IgM antibody to native type II collagen in rheumatoid arthritis serum and synovial fluid. Evidence for the presence of collagen‐anticollagen immune complexes in synovial fluid. Arthritis Rheum. 27: 1370–1377, 1984.
11. Courtenay, J. S., Dallman, M. J., Dayan, A. D., Martin, A. & Mosedal, B.: Immunization against heterologous type II collagen induces arthritis in mice. Nature 283: 666–667, 1980.
12. Currey, H. L. F. & Ziff, M.: Suppression of adjuvant disease in the rat by heterologous antilymphocyte globulin. J. Exp. Med. 127: 185–195, 1968.
13. Dalldorf, F. G., Cromartie, W. J., Anderle, S. K., Clark, R. L. & Schwab, J. H.: The relation of experimental arthritis to the distribution of streptococcal cell wall fragments. Am. J. Pathol. 100: 383–402, 1980.
14. Farmer, L. M., Watt, G., Glatt, M., Blaettler, A., Loutis, N. & Feige, U.: Delayed type hypersensitivity (DTH) to type II collagen (CII) in DBA‐1 mice. Clin. Exp. Immunol. 65: 329–335, 1986.
15. Fujita, M., Mishima, M., Iwabuchi, K., Katsume, C., Gotohda, T., Ogasawara, K., Mizuno, Y., Good, R. A. & Onoe, K.: A study on type II collagen‐induced arthritis in allogeneic bone marrow chimaeras. Immunology 66: 422–427, 1989.
16. Glant, T. T., Mikecz, K., Arzoumanian, A. & Poole, A. R.: Proteoglycan‐induced arthritis in Balb/c mice. Arthritis Rheum. 30: 201–212, 1987.
17. Hang, L., Therofilopoulos, A. N. & Dixon, F. J.: A spntaneous rheumatoid arthritis‐like disease in MRL/1 mice. J. Exp. Med. 155: 1690–1701, 1982.
18. Haqqi, T. M., Banerjee, S., Jones, W. L., Anderson, G., Behlke, M. A., Loh, D. Y., Luthra, H. S. & David, C. S.: Identification of T‐cell receptor Vβ deletion mutant mouse strain AU/ssJ (H‐2q) which is resistant to collagen‐induced arthritis. Immunogenetics 29: 180–185, 1989.
19. Hayakawa, K., Hardy, R. R., Parks, D. R. & Herzenberg, L. A.: The Ly‐1 B cell subpopulation in normal, immunodefective and autoimmune mice. J. Exp. Med. 157: 202–218, 1983.
20. Heinz, H. P., Rubin, K., Loos, M. & Laurell, A. B.: Common epitopes in Clq and collagen type II. In press. Mol. Immunol. 1988.
21. Helfgott, S. M., Dynesius‐Trentham, R. E., Brahn, E. & Trentham, D. E.: An arthritogenic lymphokine in the rat. J. Exp. Med. 162: 1531–1445, 1985.
22. Holmdahl, R., Andersson, M., Enander, I., Goldschmidt, T., Jansson, L., Larsson, P., Nordlin, C. & Klareskog, L.: Nature of the type II collagen autoimmunity in mice. Int. Rev. Immunol. 4: 49–64, 1988a.
23. Holmdahl, R., Andersson, M. & Tarkowski, A.: Origin of the autoreactive anti‐type II collagen response. I: Frequency of specific and multispecific B cells in primed murine lymph nodes. Immunology 61: 369–374, 1987a.
24. Holmdahl, R., Bailey, C., Enander, I., Mayer, R., Klareskog, L., Moran, T. & Bona, C.: Origin of the autoreactive anti type II collagen response. I. Specificities, isotypes and usage of V gene families of anti type II collagen autoantibodies. J. Immunol. 142: 1881–1886, 1989.
25. Holmdahl, R. & Jansson, L.: Estrogen induced supression of collagen arthritis. III. Adult thymectomy does not affect the course of arthritis or the estrogen mediated suppression of T cell immunity. Brain Behav. Immun. 2: 123–132, 1988.
26. Holmdahl, R., Jansson, L. & Andersson, M.: Female sex hormones suppress development of collagen‐induced arthritis in mice. Arthritis Rheum. 29: 1501–1509, 1986a.
27. Holmdahl, R., Jansson, L., Andersson, M. & Larsson, E.: Immunogenetics of type II collagen autoimmunity and susceptibility to collagen arthritis. Immunology 65: 305–310, 1988b.
28. Holmdahl, R., Jansson, L., Gullberg, D., Rubin, K., Forsberg, P. O. & Klareskog, L.: Incidence of arthritis and autoreactivity of anti‐collagen antibodies after immunization of DBA/1 mice with heterologous and autologous collagen II. Clin. exp. Immunol. 62: 639–646, 1985a.
29. Holmdahl, R., Jansson, L., Larsson, E., Rubin, K. & Klareskog, L.: Homologous type II collagen induces chronic and progressive arthritis in mice. Arthritis Rheum. 29: 106–113, 1986b.
30. Holmdahl, R., Jonsson, R., Larsson, P. & Klareskog, L.: Early appearence of activated CD4 positive T lymphocytes and Ia‐expressing cells in joints of DBA/1 mice immunized with type II collagen. Lab. Invest. 58: 53–60, 1988c.
31. Holmdahl, R., Klareskog, L., Andersson, M. & Hansen, C.: High antibody response to autologous type II collagen is restricted to H‐2q. Immunogenetics 24: 84–89, 1986c.
32. Holmdahl, R., Klareskog, L., Rubin, K., Björk, J., Smedegard, G., Jonsson, R. & Andersson, M.: Role of T lymphocytes in murine collagen induced arthritis. Agents actions 19: 1–11, 1986d.
33. Holmdahl, R., Klareskog, L., Rubin, K., Larsson, E. & Wigzell, H.: T lymphotyes in collagen II‐induced arthritis in mice. Characterization of arthritogenic collagen II‐specific T cell lines and clones. Scand. J. Immunol. 22: 295–306, 1985b.
34. Holmdahl, R., Nordling, C., Rubin, K., Tarkowski, A. & Klareskog, L.: Generation of monoclonal rheumatoid factors after immunization with collagen II ‐ anti collagen II immune complexes. Scand. J. Immunol. 24: 197–203, 1986c.
35. Holmdahl, R., Rubin, K., Klareskog, L., Dencker, L., Gustafsson, G. & Larsson, E.: Appearence of different lymphoid cells in synovial tissue and in peripheral blood during the course of collagen II‐induced arthritis in rats. Scand. J. Immunol. 21: 197–204, 1985c.
36. 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. 29: 400–410, 1986f.
37. Holmdahl, R., Tarkowski, A., Nordling, C., Rubin, K. & Klareskog, L.: Connection between autoimmunity to cartilage type II collagen and rheumatoid factor production. Monographs in Allergy 22: 71–80, 1987b.
38. Holoshitz, J., Mattitau, A. & Cohen, I. R.: Arthritis induced in rats by cloned T lymphocytes responsive to Mycobacteria but not to collagen type II. J. Clin. Invest. 73: 211–215, 1984.
39. Holoshitz, J., Naparstek, Y., Ben‐Nun, A. & Cohen, I. R.: Lines of T lymphocytes induce or vaccinate against autoimmune arthritis. Science 219: 57–59, 1983.
40. Janossy, G., Panai, G., Duke, O., Bofill, M., Poulter, L. W. & Goldstein, G.: Rheumatoid arthritis: a disease of T lymphocyte/macrophage immunoregulation. Lancet ii: 839–843, 1981.
41. Jasin, H. E.: Autoantibody specificties of immune complexes sequestered in articular cartilage of patients with rheumatoid arthritis and osteoarthritis. Arthritis Rheum. 28: 241–248, 1985.
42. Jonsson, R., Karlsson, A. L. & Holmdahl, R.: Demonstration of immune‐reactive sites on cartilage after in vivo administration of biotinylated anti‐type II collagen antibodies. J. Histochem. Cytochem. 37: 265–268, 1989.
43. Kakimoto, K., Katsuki, M., Hirofuji, T., Iwata, H. & Koga, T.: Isolation of T cell line capable of protecting mice against collagen‐induced arthritis. J. Immunol. 140: 78–83, 1988.
44. Kerwar, S. S., Englert, M. E., McReynolds, R. A., Landes, M. J., Lloyd, J. M., Oronsky, A. L. & Wilson, F. J.: Type II collagen‐induced arthritis. Studies with purified anticollagen immunoglobin. Arthritis Rheum. 26: 1120–1131, 1983.
45. Klareskog, L., Forsum, U., Scheynius, A., Kabelitz, D. & Wigzell, H.: Evidence in support of a self‐perpetuating HLA‐DR dependent delayed‐type hypersensitivity reaction in rheumatoid arthritis. Proc. Natl. Acad. Sci. (USA). 79: 3632–3636, 1982.
46. Kohasi, O., Aihara, K., Ozawa, A., Kotani, S. & Azuma, I.: New model of a synthetic adjuvant, N‐acetylmuramyl‐L‐alanyl‐D‐isoglutamine‐induced arthritis. Lab. Invest. 47: 27–36, 1982.
47. Larsson, P., Holmdahl, R., Dencker, L. & Klareskog, L.: In vivo treatment with W3/13 (anti‐pan T) but not with OX8 (anti‐suppressor/cytotoxic T) monoclonal antibodies impedes the development of adjuvant arthritis in rats. Immunology 56: 383–391, 1985.
48. Larsson, P., Kleinau, S., Holmdahl, R. & Klareskog, L.: Autologous collagen‐II induced arthritis in rats. Demonstration of clinically distinct forms of arthritis in two strains of rats. Arthritis Rheum. In press 1989.
49. Londei, M., Savill, C. M., Verhoef, A., Brennan, F., Leech, Z. A., Duance, V., Maini, R. N. & Feldmann, M.: Persistence of collagen type II‐specific T‐cell clones in the synovial membrane of a patient with rheumatoid arthritis. Proc. Natl. Acad. Sci. (USA). 86: 636–640, 1989.
50. Lotz, M. & Vaughan, J. H.: Rheumatoid Arthritis, Little, Brown and Company, Boston Toronto. ii: 1365–1416, 1988.
51. Mauritz, N. J., Holmdahl, R., Johnsson, R., Van Der Meide, P., Schynius, A. & Klareskog, L.: Treatment with interferon gamma triggers onset of collagen arthritis in mice. Arthritis Rheum. 31: 1297–1304, 1988.
52. Mikecz, K., Glant, T. T. & Poole, A. R.: Immunity to cartilage proteoglycans in Balb/c mice with progressive polyarthritis and ankylosing spondylitis induced by injection of human cartilage proteoglycan. Arthritis Rheum. 30: 306–318, 1987.
53. Nagao, S. & Tanaka, A.: Muramyl dipeptide‐induced adjuvant arthritis. Infection & Immunity. 28: 624–626, 1980.
54. Nepom, G. T., Byers, P., Seyfried, C., Healey, L. A., Wilske, K. R., Stage, D. & Nepom, B. S.: HLA genes associated with rheumatoid arthritis. Identification of susceptibility alleles using specific oligonucleotide probes. Arthritis Rheum. 32: 15–21, 1989.
55. Palacios‐Boix, A. A., Estrada‐G, I., Colston, M. J. & Panayi, G. S.: HLA‐DR4 restricted lymphocyte proliferation to a mycobacterium tuberculosis extract in rheumatoid arthritis and healthy subjects. J. Immunol. 140: 1844–1850, 1988.
56. Pearson, C. M.: Development of arthritis, periarthritis and periostitis in rats given adjuvants. Proc. Soc. Exp. Biol. Med. 91: 95, 1956.
57. Pearson, C. M. & Wood, F. D.: Passive transfer of adjuvant arthritis by lymph node or spleen cells. J. Exp. Med 120: 547–573, 1964.
58. Peck, A. B., Darby, BN. & Wakeland, E. K.: Variant Class II molecules from H‐2 haplotypes in wild mouse populations: Functional characteristics of closely related class II gene products, J. Immunol. 131: 2432–2439, 1983.
59. Ranges, G. E., Srfram, S. & Cooper, S. M.: Prevention of type II collagen‐induced arthritis by in vivo treatment with anti‐L3T4. J. Exp. Med. 162: 1105–1110, 1985.
60. Samuelson, C. O., Griffiths, M. M., Mathews, J. L., Clegg, D. O. & Ward, J. R.: Susceptibility and resistance to 6‐sulfanilamidoindazole‐induced arthritis among inbred strains of rats. Arthritis Rheum. 27: 689–693, 1984.
61. Scher, M. G., Beller, D. I. & Unanue, E. R.: Demonstration of a soluble mediator that induces exudates rich in Ia‐positive macrophages. J. Exp. Med. 152: 1684–1698, 1980.
62. Stuart, J. M., Cremer, M. A., Kang, A. H. & Townes, A. S.: Collagen induced arthritis. Evaluation of early immunological events. Arthritis Rheum. 22: 1344–1351, 1979.
63. Stuart, J. M., Cremer, M. A., Townes, A. S. & Kang, A. H.: Type II collagen‐induced arthritis in rats. Passive transfer with serum and evidence that IgG anti‐collagen antibodies can cause arthritis. J. Exp. Med. 155: 1–16, 1982.
64. Stuart, J. M. & Dixon, F. J.: Serum transfer of collagen induced arthritis in mice. J. Exp. Med. 158: 378–392, 1983.
65. Stuart, J. M., Townes, A. S. & Kang, A. H.: Nature and specificity of the immune response to collagen in type II collagen induced arthritis in mice. J. Clin. Invest. 69: 673–683, 1982.
66. Tacchini‐Cottier, F. M. & Jones, P. P.: Defective E‐beta expression in three mouse H‐2 haplotypes results from aberrant RNA splicing. J. Immunol. 141: 3647–3653, 1988.
67. Tarkowski, A., Jonsson, R., Holmdahl, R. & Klareskog, L.: Immunohistochemical characterization of synovial cells in arthritic MRL‐lpr/lpr mice. Arthritis Rheum. 30: 75–82, 1987.
68. Taurog, J. D., Sandberg, G. P. & Mahowald, M. L.: The cellular basis of adjuvant arthritis. I. Enhancement of cellmediated passive transfer by concanavalin A and by immunosuppressive pretreatment of the recipient. Cell. Immunol. 75: 271–282, 1983.
69. Theofilopoulos, A. N. & Dixon, F. J.: Murine models of systemic lupus erythematosus. Adv. Immunol. 37: 269–390, 1985.
70. Trentham, D. E.: Collagen arthritis as a relevant model for rheumatoid arthritis. Evidence pro and con. Arthritis Rheum. 25: 911–916, 1982.
71. Trentham, D. E., Dynesius, R. A., Rocklin, R. E. & David, J. R.: Cellular sensitivity to collagen in rheumatoid arthritis. New. Engl. J. Med. 299: 327–332, 1978a.
72. Trentham, D. E., Townes, A. S. & Kang, A. H.: Autoimmunity to type II collagen: an experimental model of arthritis. J. Exp. Med. 146: 857–868, 1977.
73. Trentham, D. E., Townes, A. S., Kang, A. H. & David, J. R.: Humoral and cellular sensitivity to collagen in type II collagen induced arthritis in rats. J. Clin. Invest. 61: 89–96, 1978b.
74. Vandenbroucke, J. P., Valkenburg, H. A., Boersma, J. W., Cats, A., Festen, J. J. M., Huber‐Bruning, O. & Rasker, J. J.: Oral contraceptives and rheumatoid arthritis: further evidence for a preventive effect. Lancet ii: 839–842, 1962.
75. Van der Zee, R., Van Eden, W., Meloen, R. H., Noordzij, A. & VanEmbden, J. D. A.: Efficient mapping and characterization of a T cell epitope by the simultaneous synthesis of multiple peptides. Eur. J. Immunol. 19: 43–47, 1989.
76. Watson, W. C. & Townes, A. S.: Genetic susceptibility to murine collagen II autoimmune arthritis. Proposed relationship to the IgG2 autoantibody subclass response, complement C5, major histocompatibility complex (MHC) and non‐MHC loci. J. Exp. Med. 162: 1878–1891, 1985.
77. Weston, K. M., Ju, S.‐T., Lu, C. Y. & Sy, M.‐S.: Autoreactive T cells in MRL/Mp‐lpr/lpr mice. Characterization of the lymphokines produced and analysis of antigen presenting cells required. J. Immunol. 141: 1941–1948, 1988.
78. Winchester, R. J.: The major histocompatibility complex. Philadelphia: WB Saunders Company. In press 1988.
79. Wooley, P. H., Luthra, H. S., Lafuse, W. P., Huse, A., Stuart, J. M. & David, C. S.: Type II collagen induced arthritis in mice. IV. Variations in immunogenetic regulation provide evidence for multiple arthritogenic epitopes on the collagen molecule. J. Immunol. 135: 2443–2451, 1985.
80. Wooley, P. H., Luthra, H. S., Stuart, J. M. & David, C. S.: Type II collagen induced arthritis in mice. I. Major histocompatibility complex (I‐region) linkage and antibody correlates. J. Exp. Med. 154: 688–700, 1981.
81. Yoo, T. J., Kim, S. Y., Stuart, J. M., Floyd, R. A., Olson, G. A., Cremer, M. A. & Kang, A. H.: Induction of arthritis in monkeys by immunization with type II collagen. J. Exp. Med. 168: 777–782, 1988.
82. Zvaifler, N. J.: The immunopathology of joint inflammation in rheumatoid arthritis. Adv. Immunol. 16: 265–336, 1973.