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Rat models of arthritis: Similarities, differences, advantages, and disadvantages in the identification of novel therapeutics

  • Lisa R. Schopf
  • Karen Anderson
  • Bruce D. Jaffee
Part of the Progress in Inflammation Research book series (PIR)

Keywords

Adjuvant Arthritis Dark Agouti Human Rheumatoid Arthritis Streptococcal Cell Wall Minodronic Acid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Carlson RP, Jacobson PB (1999) Comparison of adjuvant and streptococcal cell wall-induced arthritis. In: DW Morgan, LA Marshall (eds): In vivo Models of Inflammation. Birkhäuser Verlag, Basel/Boston/Berlin, 1–50Google Scholar
  2. 2.
    Bendele A (2001) Animal models of rheumatoid arthritis. J Musculoskelet Neuronal Interact 1(4): 377–385PubMedGoogle Scholar
  3. 3.
    Kannan K, Ortmann RA, Kimpel D (2005) Animal models of rheumatoid arthritis and their relevance to human disease. Pathophysiology 12(3): 167–181PubMedCrossRefGoogle Scholar
  4. 4.
    Weichman B (1989) Rat Adjuvant Arthritis: A Model of Chronic Inflammtion. In: JY Chang, AJ Lewis (eds): Pharmacological Methods in the Control of Inflammation. Alan R. Liss, New York, 363–380Google Scholar
  5. 5.
    Philippe L, Gegout-Pottie P, Guingamp C, Bordji K, Terlain B, Netter P, Gillet P (1997) Relations between functional, inflammatory, and degenerative parameters during adjuvant arthritis in rats. Am J Physiol 273(4 Pt 2): R1550–1556PubMedGoogle Scholar
  6. 6.
    Van Eden W, Waksman BH (2003) Immune regulation in adjuvant-induced arthritis: possible implications for innovative therapeutic strategies in arthritis. Arthritis Rheum 48(7): 1788–1796PubMedCrossRefGoogle Scholar
  7. 7.
    Trentham DE, Townes AS, Kang AH (1977) Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med 146(3): 857–868PubMedCrossRefGoogle Scholar
  8. 8.
    Trentham DE, Dynesius-Trentham RA (1989) Type II ccollagen-induced arthritis in the rat. In: JY Chang, AJ Lewis (eds): Pharmacological Methods in the Control of Inflammation. Alan R. Liss, New York, 395–413Google Scholar
  9. 9.
    Schimmer RC, Schrier DJ, Flory CM, Laemont KD, Tung D, Metz AL, Friedl HP, Conroy MC, Warren JS, Beck B et al (1998) Streptococcal cell wall-induced arthritis: requirements for IL-4, IL-10, IFN-gamma, and monocyte chemoattractant protein-1. J Immunol 160(3): 1466–1471PubMedGoogle Scholar
  10. 10.
    Schwab JH, Anderle SK, Brown RR, Dalldorf FG, Thompson RC (1991) Pro-and anti-inflammatory roles of interleukin-1 in recurrence of bacterial cell wall-induced arthritis in rats. Infect Immun 59(12): 4436–4442PubMedGoogle Scholar
  11. 11.
    Stoerk H (1954) Chronic polyarthritis in rats injected with spleen in adjuvants. Am J Pathol 30: 616–621Google Scholar
  12. 12.
    Pearson CM (1956) Development of arthritis, periarthritis and periostitis in rats given adjuvants. Proc Soc Exp Biol Med 91(1): 95–101PubMedGoogle Scholar
  13. 13.
    Jaffee BD, Kerr JS, Jones EA, Giannaras JV, McGowan M, Ackerman NR (1989) The effect of immunomodulating drugs on adjuvant-induced arthritis in Lewis rats. Agents Actions 27(3–4): 344–346PubMedCrossRefGoogle Scholar
  14. 14.
    Rovensky J, Svik K, Stancikova M, Istok R (2003) Effect of immunostimulatory ribomunyl on the preventive treatment of rat adjuvant arthritis with cyclosporine and methotrexate. J Rheumatol 30(9): 2027–2032PubMedGoogle Scholar
  15. 15.
    Rovensky J, Svik K, Matha V, Istok R, Kamarad V, Ebringer L, Ferencik M, Stancikova M (2005) Combination treatment of rat adjuvant-induced arthritis with methotrexate, probiotic bacteria Enterococcus faecium, and selenium. Ann NY Acad Sci 1051: 570–581PubMedCrossRefGoogle Scholar
  16. 16.
    Silva MA, Ishii-Iwamoto EL, Bracht A, Caparroz-Assef SM, Kimura E, Cuman RK, Bersani-Amado CA (2005) Efficiency of combined methotrexate/chloroquine therapy in adjuvant-induced arthritis. Fundam Clin Pharmacol 19(4): 479–489PubMedCrossRefGoogle Scholar
  17. 17.
    Noguchi M, Kimoto A, Kobayashi S, Yoshino T, Miyata K, Sasamata M (2005) Effect of celecoxib, a cyclooxygenase-2 inhibitor, on the pathophysiology of adjuvant arthritis in rat. Eur J Pharmacol 513(3): 229–235PubMedCrossRefGoogle Scholar
  18. 18.
    Bendele A, McAbee T, Sennello G, Frazier J, Chlipala E, McCabe D (1999) Efficacy of sustained blood levels of interleukin-1 receptor antagonist in animal models of arthritis: comparison of efficacy in animal models with human clinical data. Arthritis Rheum 42(3): 498–506PubMedCrossRefGoogle Scholar
  19. 19.
    Bendele AM, Chlipala ES, Scherrer J, Frazier J, Sennello G, Rich WJ, Edwards CK, 3rd (2000) Combination benefit of treatment with the cytokine inhibitors interleukin-1 receptor antagonist and PEGylated soluble tumor necrosis factor receptor type I in animal models of rheumatoid arthritis. Arthritis Rheum 43(12): 2648–2659PubMedCrossRefGoogle Scholar
  20. 20.
    Miwatashi S, Arikawa Y, Kotani E, Miyamoto M, Naruo K, Kimura H, Tanaka T, Asahi S, Ohkawa S (2005) Novel inhibitor of p38 MAP kinase as an anti-TNF-alpha drug: discovery of N-{4-[2-ethyl-4-(3-methylphenyl)-1,3-thiazol-5-yl]-2-pyridyl}benzamide (TAK-715) as a potent and orally active anti-rheumatoid arthritis agent. J Med Chem 48(19): 5966–5979PubMedCrossRefGoogle Scholar
  21. 21.
    Cole P, Rabassed, X (2004) The soluble tumor necrosis factor receptor etanercept: a new strategy for the treatment of autoimmune rheumatic disease. Drugs Today (Barc) 40(4): 281–324CrossRefGoogle Scholar
  22. 22.
    Kamada H, Goto M, Matsuura S, Takaoka Y, Nagai H (1997) Immunopharmacological studies on collagen-induced arthritis in dark Agouti (DA) rats. Jpn J Pharmacol 74(4): 313–322PubMedGoogle Scholar
  23. 23.
    Smith RJ, Sly LM (1996) Type II collagen-induced arthritis in the diabetic-resistant biobreeding rat: inflammatory and histopathological features of joint pathology and effects of antiinflammatory and antirheumatic drugs on this chronic arthritic process. J Pharmacol Exp Ther 277(3): 1801–1813PubMedGoogle Scholar
  24. 24.
    Cuzzocrea S, Mazzon E, di Paola R, Genovese T, Muia C, Caputi AP, Salvemini D (2005) Synergistic interaction between methotrexate and a superoxide dismutase mimetic: pharmacologic and potential clinical significance. Arthritis Rheum 52(12): 3755–3760PubMedCrossRefGoogle Scholar
  25. 25.
    Brahn E, Peacock DJ, Banquerigo ML (1991) Suppression of collagen-induced arthritis by combination cyclosporin A and methotrexate therapy. Arthritis Rheum 34(10): 1282–1288PubMedGoogle Scholar
  26. 26.
    Lange F, Bajtner E, Rintisch C, Nandakumar KS, Sack U, Holmdahl R (2005) Methotrexate ameliorates T cell dependent autoimmune arthritis and encephalomyelitis but not antibody induced or fibroblast induced arthritis. Ann Rheum Dis 64(4): 599–605PubMedCrossRefGoogle Scholar
  27. 27.
    Nishikawa M, Myoui A, Tomita T, Takahi K, Nampei A, Yoshikawa H (2003) Prevention of the onset and progression of collagen-induced arthritis in rats by the potent p38 mitogen-activated protein kinase inhibitor FR167653. Arthritis Rheum 48(9): 2670–2681PubMedCrossRefGoogle Scholar
  28. 28.
    Esser RE, Anderle SK, Chetty C, Stimpson SA, Cromartie WJ, Schwab JH (1986) Comparison of inflammatory reactions induced by intraarticular injection of bacterial cell wall polymers. Am J Pathol 122(2): 323–334PubMedGoogle Scholar
  29. 29.
    Esser RE, Stimpson SA, Cromartie WJ, Schwab JH (1985) Reactivation of streptococcal cell wall-induced arthritis by homologous and heterologous cell wall polymers. Arthritis Rheum 28(12): 1402–1411PubMedGoogle Scholar
  30. 30.
    Rioja I, Bush KA, Buckton JB, Dickson MC, Life, PF (2004) Joint cytokine quantification in two rodent arthritis models: kinetics of expression, correlation of mRNA and protein levels and response to prednisolone treatment. Clin Exp Immunol 137(1): 65–73PubMedCrossRefGoogle Scholar
  31. 31.
    Stimpson SA, Schwab, JH (1989) Chronic remittent erosive arthritis induced by bacterial peptidoglycan-polysaccharide structures. In: JY Chang, AJ Lewis (eds): Pharmacological Methods in the Control of Inflammation. Alan R. Liss, New York, 381–394Google Scholar
  32. 32.
    Voll RE, Kalden JR (2005) Do we need new treatment that goes beyond tumor necrosis factor blockers for rheumatoid arthritis? Ann NY Acad Sci 1051: 799–810PubMedCrossRefGoogle Scholar
  33. 33.
    Smolen JS, Steiner G (2003) Therapeutic strategies for rheumatoid arthritis. Nat Rev Drug Discov 2(6): 473–488PubMedCrossRefGoogle Scholar
  34. 34.
    O’Dell JR (2004) Therapeutic strategies for rheumatoid arthritis. N Engl J Med 350(25): 2591–2602PubMedCrossRefGoogle Scholar
  35. 35.
    Olsen NJ, Stein CM (2004) New drugs for rheumatoid arthritis. N Engl J Med 350(21): 2167–2179PubMedCrossRefGoogle Scholar
  36. 36.
    Lee DM, Weinblatt ME (2001) Rheumatoid arthritis. Lancet 358(9285): 903–911PubMedCrossRefGoogle Scholar
  37. 37.
    Inoue K, Fujisawa H, Motonaga A, Inoue Y, Kyoi T, Ueda F, Kimura K (1994) Anti-inflammatory effects of etodolac: comparison with other non-steroidal anti-inflammatory drugs. Biol Pharm Bull 17(12): 1577–1583PubMedGoogle Scholar
  38. 38.
    Bartlett RR, Schleyerbach R (1985) Immunopharmacological profile of a novel isoxazol derivative, HWA 486, with potential antirheumatic activity — I. Disease modifying action on adjuvant arthritis of the rat. Int J Immunopharmacol 7(1): 7–18PubMedCrossRefGoogle Scholar
  39. 39.
    Sakuma S, Nishigaki F, Magari K, Ogawa T, Miyata S, Ohkubo Y, Goto T (2001) FK506 is superior to methotrexate in therapeutic effects on advanced stage of rat adjuvant-induced arthritis. Inflamm Res 50(10): 509–514PubMedCrossRefGoogle Scholar
  40. 40.
    Bendele A, McComb J, Gould T, McAbee T, Sennello G, Chlipala E, Guy M (1999) Animal models of arthritis: relevance to human disease. Toxicol Pathol 27(1): 134–142PubMedGoogle Scholar
  41. 41.
    Segawa Y, Tsuzuike N, Itokazu Y, Omata T, Inoue N, Aota S, Okazaki Y, Nakamura T (1999) Age-depending effects of methotrexate treatment on systemic bone turnover in experimental adjuvant arthritis. Arzneimittelforschung 49(1): 38–43PubMedGoogle Scholar
  42. 42.
    Komoriya K, Nagata I, Kunisawa K, Takeshita T, Naruchi T (1987) Anti-arthritic and immunoregulatory effects of TI-31 on collagen-induced arthritis. Jpn J Pharmacol 45(3): 389–396PubMedGoogle Scholar
  43. 43.
    Kaibara N, Hotokebuchi T, Takagishi K, Katsuki I (1983) Paradoxical effects of cyclosporin A on collagen arthritis in rats. J Exp Med 158(6): 2007–2015PubMedCrossRefGoogle Scholar
  44. 44.
    Kliwinski C, Kukral D, Postelnek J, Krishnan B, Killar L, Lewin A, Nadler S, Townsend R (2005) Prophylactic administration of abatacept prevents disease and bone destruction in a rat model of collagen-induced arthritis. J Autoimmun 25(3): 165–171PubMedCrossRefGoogle Scholar
  45. 45.
    Kremer JM, Cannon GW (2004) Benefit/risk of leflunomide in rheumatoid arthritis. Clin Exp Rheumatol 22(5 Suppl 35): S95–100Google Scholar
  46. 46.
    Ofosu-Appiah WA, Morgan K, Holt PJ (1984) Native type II collagen-induced arthritis in the rat. Studies of the humoral response to collagen at the cellular level. J Rheumatol 11(4): 432–437PubMedGoogle Scholar
  47. 47.
    Bendele AM, McComb J, Gould T, Frazier J, Chlipala E, Seely J, Kieft G, Edwards CK, 3rd (1999) Effects of PEGylated soluble tumor necrosis factor receptor type I (PEG sTNF-RI) alone and in combination with methotrexate in adjuvant arthritic rats. Clin Exp Rheumatol 17(5): 553–560PubMedGoogle Scholar
  48. 48.
    Jones RS, Ward JR (1963) Studies on adjuvant-induced polyarthritis in rats. II. Histogenesis of joint and visceral lesions. Arthritis Rheum 6: 23–35Google Scholar
  49. 49.
    Schett G, Middleton S, Bolon B, Stolina M, Brown H, Zhu L, Pretorius J, Zack DJ, Kostenuik P, Feige U (2005) Additive bone-protective effects of anabolic treatment when used in conjunction with RANKL and tumor necrosis factor inhibition in two rat arthritis models. Arthritis Rheum 52(5): 1604–1611PubMedCrossRefGoogle Scholar
  50. 50.
    Kohashi O, Kuwata J, Umehara K, Uemura F, Takahashi T, Ozawa A (1979) Susceptibility to adjuvant-induced arthritis among germfree, specific-pathogen-free, and conventional rats. Infect Immun 26(3): 791–794PubMedGoogle Scholar
  51. 51.
    van den Broek MF, van Bruggen MC, Koopman JP, Hazenberg MP, van den Berg WB (1992) Gut flora induces and maintains resistance against streptococcal cell wallinduced arthritis in F344 rats. Clin Exp Immunol 88(2): 313–317PubMedCrossRefGoogle Scholar
  52. 52.
    Fathalla B, Hamada K, Vannier E, Smith D, Edwards C, 3rd, and Roubenoff R (2004) Effects of aging and cytokine blockade on inflammatory cachexia. Clin Exp Rheumatol 22(1): 85–90PubMedGoogle Scholar
  53. 53.
    Sternberg EM, Hill JM, Chrousos GP, Kamilaris T, Listwak SJ, Gold PW, Wilder RL (1989) Inflammatory mediator-induced hypothalamic-pituitary-adrenal axis activation is defective in streptococcal cell wall arthritis-susceptible Lewis rats. Proc Natl Acad Sci USA 86(7): 2374–2378PubMedCrossRefGoogle Scholar
  54. 54.
    Waksman BH, Pearson CM, Sharp JT (1960) Studies of arthritis and other lesions induced in rats by injection of mycobacterial adjuvant. II. Evidence that the disease is a disseminated immunologic response to exogenous antigen. J Immunol 85: 403–417PubMedGoogle Scholar
  55. 55.
    Waksman BH (2002) Immune regulation in adjuvant disease and other arthritis models: relevance to pathogenesis of chronic arthritis. Scand J Immunol 56(1): 12–34PubMedCrossRefGoogle Scholar
  56. 56.
    Whitehouse DJ, Whitehouse MW, Pearson CM (1969) Passive transfer of adjuvantinduced arthritis and allergic encephalomyelitis in rats using thoracic duct lymphocytes. Nature 224(226): 1322PubMedCrossRefGoogle Scholar
  57. 57.
    Allen JB, Malone DG, Wahl SM, Calandra GB, Wilder RL (1985) Role of the thymus in streptococcal cell wall-induced arthritis and hepatic granuloma formation. Comparative studies of pathology and cell wall distribution in athymic and euthymic rats. J Clin Invest 76(3): 1042–1056PubMedCrossRefGoogle Scholar
  58. 58.
    Ridge SC, Zabriske JB, Oronsky AL, Kerwar SS (1985) Streptococcal cell wall arthritis: studies with nude (athymic) inbred Lewis rats. Cell Immunol 96(1): 231–234PubMedCrossRefGoogle Scholar
  59. 59.
    Santos LL, Morand EF, Hutchinson P, Boyce NW, Holdsworth SR (1997) Anti-neutrophil monoclonal antibody therapy inhibits the development of adjuvant arthritis. Clin Exp Immunol 107(2): 248–253PubMedCrossRefGoogle Scholar
  60. 60.
    Brahn E, Trentham DE (1984) Effect of antithymocyte serum on collagen arthritis in rats: evidence that T cells are involved in its pathogenesis. Cell Immunol 86(2): 421–428PubMedCrossRefGoogle Scholar
  61. 61.
    DeJoy SQ, Ferguson KM, Sapp TM, Zabriskie JB, Oronsky AL, Kerwar SS (1989) Streptococcal cell wall arthritis. Passive transfer of disease with a T cell line and crossreactivity of streptococcal cell wall antigens with Mycobacterium tuberculosis. J Exp Med 170(2): 369–382PubMedCrossRefGoogle Scholar
  62. 62.
    Firestein GS (2005) Immunologic mechanisms in the pathogenesis of rheumatoid arthritis. J Clin Rheumatol 11(3 Suppl): S39–44PubMedCrossRefGoogle Scholar
  63. 63.
    Firestein GS, Zvaifler NJ (1990) How important are T cells in chronic rheumatoid synovitis? Arthritis Rheum 33(6): 768–773PubMedGoogle Scholar
  64. 64.
    Kremer JM, Dougados M, Emery P, Durez P, Sibilia J, Shergy W, Steinfeld S, Tindall E, Becker JC, Li T et al (2005) Treatment of rheumatoid arthritis with the selective costimulation modulator abatacept: twelve-month results of a phase iib, double-blind, randomized, placebo-controlled trial. Arthritis Rheum 52(8): 2263–2271PubMedCrossRefGoogle Scholar
  65. 65.
    van Eden W, Thole JE, van der Zee R, Noordzij A, van Embden JD, Hensen EJ, Cohen IR (1988) Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature 331(6152): 171–173PubMedCrossRefGoogle Scholar
  66. 66.
    Prakken BJ, Roord S, Ronaghy A, Wauben M, Albani S, van Eden W (2003) Heat shock protein 60 and adjuvant arthritis: a model for T cell regulation in human arthritis. Springer Semin Immunopathol 25(1): 47–63PubMedCrossRefGoogle Scholar
  67. 67.
    van Eden W, Holoshitz J, Nevo Z, Frenkel A, Klajman A, Cohen IR (1985) Arthritis induced by a T-lymphocyte clone that responds to Mycobacterium tuberculosis and to cartilage proteoglycans. Proc Natl Acad Sci USA 82(15): 5117–5120PubMedCrossRefGoogle Scholar
  68. 68.
    Billingham ME, Carney S, Butler R, Colston MJ (1990) A mycobacterial 65-kD heat shock protein induces antigen-specific suppression of adjuvant arthritis, but is not itself arthritogenic. J Exp Med 171(1): 339–344PubMedCrossRefGoogle Scholar
  69. 69.
    Prakken BJ, Roord S, van Kooten PJ, Wagenaar JP, van Eden W, Albani S, Wauben MH (2002) Inhibition of adjuvant-induced arthritis by interleukin-10-driven regulatory cells induced via nasal administration of a peptide analog of an arthritis-related heat-shock protein 60 T cell epitope. Arthritis Rheum 46(7): 1937–1946PubMedCrossRefGoogle Scholar
  70. 70.
    van den Broek MF (1989) Streptococcal cell wall-induced polyarthritis in the rat. Mechanisms for chronicity and regulation of susceptibility. APMIS 97(10): 861–878PubMedCrossRefGoogle Scholar
  71. 71.
    Beech JT, Siew LK, Ghoraishian M, Stasiuk LM, Elson CJ, Thompson SJ (1997) CD4+ Th2 cells specific for mycobacterial 65-kilodalton heat shock protein protect against pristane-induced arthritis. J Immunol 159(8): 3692–3697PubMedGoogle Scholar
  72. 72.
    Paul AG, van Kooten PJ, van Eden W, van der Zee R (2000) Highly autoproliferative T cells specific for 60-kDa heat shock protein produce IL-4/IL-10 and IFN-gamma and are protective in adjuvant arthritis. J Immunol 165(12): 7270–7277PubMedGoogle Scholar
  73. 73.
    Wilder RL, Allen JB, Hansen C (1987) Thymus-dependent and-independent regulation of Ia antigen expression in situ by cells in the synovium of rats with streptococcal cell wall-induced arthritis. Differences in site and intensity of expression in euthymic, athymic, and cyclosporin A-treated LEW and F344 rats. J Clin Invest 79(4): 1160–1171PubMedGoogle Scholar
  74. 74.
    Stimpson SA, Esser RE, Carter PB, Sartor RB, Cromartie WJ, Schwab JH (1987) Lipopolysaccharide induces recurrence of arthritis in rat joints previously injured by peptidoglycan-polysaccharide. J Exp Med 165(6): 1688–1702PubMedCrossRefGoogle Scholar
  75. 75.
    Lichtman SN, Wang J, Sartor RB, Zhang C, Bender D, Dalldorf FG, Schwab JH (1995) Reactivation of arthritis induced by small bowel bacterial overgrowth in rats: role of cytokines, bacteria, and bacterial polymers. Infect Immun 63(6): 2295–2301PubMedGoogle Scholar
  76. 76.
    Stuart JM, Townes AS, Kang AH (1982) The role of collagen autoimmunity in animal models and human diseases. J Invest Dermatol 79Suppl 1: 121s–127sPubMedCrossRefGoogle Scholar
  77. 77.
    Stuart JM, Tomoda K, Yoo TJ, Townes AS, Kang AH (1983) Serum transfer of collageninduced arthritis. II. Identification and localization of autoantibody to type II collagen in donor and recipient rats. Arthritis Rheum 26(10): 1237–1244PubMedGoogle Scholar
  78. 78.
    Cremer MA, Rosloniec EF, Kang AH (1998) The cartilage collagens: a review of their structure, organization, and role in the pathogenesis of experimental arthritis in animals and in human rheumatic disease. J Mol Med 76(3–4): 275–288PubMedCrossRefGoogle Scholar
  79. 79.
    Chaiamnuay S, Bridges SL Jr (2005) The role of B cells and autoantibodies in rheumatoid arthritis. Pathophysiology 12(3): 203–216PubMedCrossRefGoogle Scholar
  80. 80.
    Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, Stevens RM, Shaw T (2004) Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 350(25): 2572–2581PubMedCrossRefGoogle Scholar
  81. 81.
    Cohen SB (2005) B-cell depletion for rheumatic diseases: where are we? MedGenMed 7(2): 72PubMedGoogle Scholar
  82. 82.
    Vossenaar ER, van Boekel MA, van Venrooij WJ, Lopez-Hoyoz M, Merino J, Merino R, Joosten LA (2004) Absence of citrulline-specific autoantibodies in animal models of autoimmunity. Arthritis Rheum 50(7): 2370–2372PubMedCrossRefGoogle Scholar
  83. 83.
    Caulfield JP, Hein A, Dynesius-Trentham R, Trentham DE (1982) Morphologic demonstration of two stages in the development of type II collagen-induced arthritis. Lab Invest 46(3): 321–343PubMedGoogle Scholar
  84. 84.
    Harris HE, Liljestrom M, Lindroos E, Kleinau S (1997) Characterization of adhesion molecule expression in the pathogenesis of homologous collagen-induced arthritis in the DA rat. Clin Immunol Immunopathol 85(1): 40–46PubMedCrossRefGoogle Scholar
  85. 85.
    Pearson CM, Wood FD (1963) Studies of arthritis and other lesions induced in rats by the injection of mycobacterial adjuvant. VII. Pathologic details of the arthritis and spondylitis. Am J Pathol 42: 73–95PubMedGoogle Scholar
  86. 86.
    Issekutz AC, Issekutz TB (1991) Quantitation and kinetics of polymorphonuclear leukocyte and lymphocyte accumulation in joints during adjuvant arthritis in the rat. Lab Invest 64(5): 656–663PubMedGoogle Scholar
  87. 87.
    Ward PA (1997) Neutrophils and adjuvant arthritis. Clin Exp Immunol 107(2): 225–226PubMedCrossRefGoogle Scholar
  88. 88.
    Bush KA, Walker JS, Lee CS, Kirkham BW (2001) Cytokine expression and synovial pathology in the initiation and spontaneous resolution phases of adjuvant arthritis: interleukin-17 expression is upregulated in early disease. Clin Exp Immunol 123(3): 487–495PubMedCrossRefGoogle Scholar
  89. 89.
    Szekanecz Z, Halloran MM, Volin MV, Woods JM, Strieter RM, Kenneth Haines G 3rd, Kunkel SL, Burdick MD, Koch AE (2000) Temporal expression of inflammatory cytokines and chemokines in rat adjuvant-induced arthritis. Arthritis Rheum 43(6): 1266–1277PubMedCrossRefGoogle Scholar
  90. 90.
    Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ (1999) Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20(3): 345–357PubMedCrossRefGoogle Scholar
  91. 91.
    Teitelbaum SL (2000) Bone resorption by osteoclasts. Science 289(5484): 1504–1508PubMedCrossRefGoogle Scholar
  92. 92.
    Tyler JA, Benton HP (1988) Synthesis of type II collagen is decreased in cartilage cultured with interleukin 1 while the rate of intracellular degradation remains unchanged. Coll Relat Res 8(5): 393–405PubMedGoogle Scholar
  93. 93.
    Reginato AM, Sanz-Rodriguez C, Diaz A, Dharmavaram RM, Jimenez SA (1993) Transcriptional modulation of cartilage-specific collagen gene expression by interferon gamma and tumour necrosis factor alpha in cultured human chondrocytes. Biochem J 294(Pt 3): 761–769PubMedGoogle Scholar
  94. 94.
    Saklatvala J (1986) Tumour necrosis factor alpha stimulates resorption and inhibits synthesis of proteoglycan in cartilage. Nature 322(6079): 547–549PubMedCrossRefGoogle Scholar
  95. 95.
    Goldring SR (2003) Inflammatory mediators as essential elements in bone remodeling. Calcif Tissue Int 73(2): 97–100PubMedCrossRefGoogle Scholar
  96. 96.
    Goldring SR (2003) Pathogenesis of bone and cartilage destruction in rheumatoid arthritis. Rheumatology (Oxford) 42(Suppl 2): ii11–16PubMedGoogle Scholar
  97. 97.
    Kirwan JR (2001) Links between radiological change, disability, and pathology in rheumatoid arthritis. J Rheumatol 28(4): 881–886PubMedGoogle Scholar
  98. 98.
    Kirwan J, Byron M, Watt I (2001) The relationship between soft tissue swelling, joint space narrowing and erosive damage in hand X-rays of patients with rheumatoid arthritis. Rheumatology (Oxford) 40(3): 297–301PubMedCrossRefGoogle Scholar
  99. 99.
    Molenaar ET, Voskuyl AE, Dinant HJ, Bezemer PD, Boers M, Dijkmans BA (2004) Progression of radiologic damage in patients with rheumatoid arthritis in clinical remission. Arthritis Rheum 50(1): 36–42PubMedCrossRefGoogle Scholar
  100. 100.
    Lipsky PE, van der Heijde DM, St Clair EW, Furst DE, Breedveld FC, Kalden JR, Smolen JS, Weisman M, Emery P, Feldmann M et al (2000) Infliximab and methotrexate in the treatment of rheumatoid arthritis. Anti-Tumor Necrosis Factor Trial in Rheumatoid Arthritis with Concomitant Therapy Study Group. N Engl J Med 343(22): 1594–1602PubMedCrossRefGoogle Scholar
  101. 101.
    Smolen JS, Han C, Bala M, Maini RN, Kalden JR, van der Heijde D, Breedveld FC, Furst DE, Lipsky PE (2005) Evidence of radiographic benefit of treatment with infliximab plus methotrexate in rheumatoid arthritis patients who had no clinical improvement: a detailed subanalysis of data from the anti-tumor necrosis factor trial in rheumatoid arthritis with concomitant therapy study. Arthritis Rheum 52(4): 1020–1030PubMedCrossRefGoogle Scholar
  102. 102.
    Bresnihan B, Alvaro-Gracia JM, Cobby M, Doherty M, Domljan Z, Emery P, Nuki G, Pavelka K, Rau R, Rozman B et al (1998) Treatment of rheumatoid arthritis with recombinant human interleukin-1 receptor antagonist. Arthritis Rheum 41(12): 2196–2204PubMedCrossRefGoogle Scholar
  103. 103.
    Fujikawa Y, Quinn JM, Sabokbar A, McGee JO, Athanasou NA (1996) The human osteoclast precursor circulates in the monocyte fraction. Endocrinology 137(9): 4058–4060PubMedCrossRefGoogle Scholar
  104. 104.
    Takayanagi H, Iizuka H, Juji T, Nakagawa T, Yamamoto A, Miyazaki T, Koshihara Y, Oda H, Nakamura K, Tanaka S (2000) Involvement of receptor activator of nuclear factor kappaB ligand/osteoclast differentiation factor in osteoclastogenesis from synoviocytes in rheumatoid arthritis. Arthritis Rheum 43(2): 259–269PubMedCrossRefGoogle Scholar
  105. 105.
    Billingham ME (1983) Models of arthritis and the search for anti-arthritic drugs. Pharmacol Ther 21(3): 389–428PubMedCrossRefGoogle Scholar
  106. 106.
    Schmidt-Weber CB, Pohlers D, Siegling A, Schadlich H, Buchner E, Volk HD, Palombo-Kinne E, Emmrich F, Kinne RW (1999) Cytokine gene activation in synovial membrane, regional lymph nodes, and spleen during the course of rat adjuvant arthritis. Cell Immunol 195(1): 53–65PubMedCrossRefGoogle Scholar
  107. 107.
    Smith-Oliver T, Noel LS, Stimpson SS, Yarnall DP, Connolly KM (1993) Elevated levels of TNF in the joints of adjuvant arthritic rats. Cytokine 5(4): 298–304PubMedCrossRefGoogle Scholar
  108. 108.
    Magari K, Miyata S, Ohkubo Y, Mutoh S (2004) Inflammatory cytokine levels in paw tissues during development of rat collagen-induced arthritis: effect of FK506, an inhibitor of T cell activation. Inflamm Res 53(9): 469–474PubMedCrossRefGoogle Scholar
  109. 109.
    Seed MP, Gardner CR (2005) The modulation of intra-articular inflammation, cartilage matrix and bone loss in mono-articular arthritis induced by heat-killed Myobacterium tuberculosis. Inflammopharmacology 12(5): 551–567PubMedCrossRefGoogle Scholar
  110. 110.
    Larsson E, Erlandsson Harris H, Larsson A, Mansson B, Saxne T, Klareskog L (2004) Corticosteroid treatment of experimental arthritis retards cartilage destruction as determined by histology and serum COMP. Rheumatology (Oxford) 43(4): 428–434PubMedCrossRefGoogle Scholar
  111. 111.
    Larsson E, Mussener A, Heinegard D, Klareskog L, Saxne T (1997) Increased serum levels of cartilage oligomeric matrix protein and bone sialoprotein in rats with collagen arthritis. Br J Rheumatol 36(12): 1258–1261PubMedCrossRefGoogle Scholar
  112. 112.
    Sims NA, Green JR, Glatt M, Schlict S, Martin TJ, Gillespie MT, Romas E (2004) Targeting osteoclasts with zoledronic acid prevents bone destruction in collagen-induced arthritis. Arthritis Rheum 50(7): 2338–2346PubMedCrossRefGoogle Scholar
  113. 113.
    Badger AM, Griswold DE, Kapadia R, Blake S, Swift BA, Hoffman SJ, Stroup GB, Webb E, Rieman DJ, Gowen M et al (2000) Disease-modifying activity of SB 242235, a selective inhibitor of p38 mitogen-activated protein kinase, in rat adjuvant-induced arthritis. Arthritis Rheum 43(1): 175–183PubMedCrossRefGoogle Scholar
  114. 114.
    Silva MD, Savinainen A, Kapadia R, Ruan J, Siebert E, Avitahl N, Mosher R, Anderson K, Jaffee B, Schopf L et al (2004) Quantitative analysis of micro-CT imaging and histopathological signatures of experimental arthritis in rats. Mol Imaging 3(4): 312–318PubMedCrossRefGoogle Scholar
  115. 115.
    Jacobson PB, Morgan SJ, Wilcox DM, Nguyen P, Ratajczak CA, Carlson RP, Harris RR, Nuss M (1999) A new spin on an old model: in vivo evaluation of disease progression by magnetic resonance imaging with respect to standard inflammatory parameters and histopathology in the adjuvant arthritic rat. Arthritis Rheum 42(10): 2060–2073PubMedCrossRefGoogle Scholar
  116. 116.
    Yamane I, Hagino H, Okano T, Enokida M, Yamasaki D, Teshima R (2003) Effect of minodronic acid (ONO-5920) on bone mineral density and arthritis in adult rats with collagen-induced arthritis. Arthritis Rheum 48(6): 1732–1741PubMedCrossRefGoogle Scholar
  117. 117.
    Okazaki Y, Tsurukami H, Nishida S, Okimoto N, Aota S, Takeda S, Nakamura T (1998) Prednisolone prevents decreases in trabecular bone mass and strength by reducing bone resorption and bone formation defect in adjuvant-induced arthritic rats. Bone 23(4): 353–360PubMedCrossRefGoogle Scholar
  118. 118.
    Okamoto A, Yamamura M, Iwahashi M, Aita T, Ueno A, Kawashima M, Yamana J, Kagawa H, Makino H (2003) Pathophysiological functions of CD30+ CD4+ T cells in rheumatoid arthritis. Acta Med Okayama 57(6): 267–277PubMedGoogle Scholar
  119. 119.
    Osterman T, Virtamo T, Lauren L, Kippo K, Pasanen I, Hannuniemi R, Vaananen K, Sellman R (1997) Slow-release clodronate in prevention of inflammation and bone loss associated with adjuvant arthritis. J Pharmacol Exp Ther 280(2): 1001–1007PubMedGoogle Scholar
  120. 120.
    Osterman T, Kippo K, Lauren L, Hannuniemi R, Sellman R (1995) Effect of clodronate on established collagen-induced arthritis in rats. Inflamm Res 44(6): 258–263PubMedCrossRefGoogle Scholar
  121. 121.
    Harkness JE, Ridgway MD (1980) Chromodacryorrhea in laboratory rats (Rattus norvegicus): etiologic considerations. Lab Anim Sci 30(5): 841–844PubMedGoogle Scholar
  122. 122.
    Wilder RL (1988) Streptococcal cell-wall-induced arthritis in rats: an overview. Int J Tissue React 10(1): 1–5PubMedGoogle Scholar
  123. 123.
    Neuman RG, Wilson BD, Barkley M, Kimball ES, Weichman BM, Wood DD (1987) Inhibition of prostaglandin biosynthesis by etodolac. I. Selective activities in arthritis. Agents Actions 21(1–2): 160–166PubMedCrossRefGoogle Scholar
  124. 124.
    Tanaka K, Shimotori T, Makino S, Aikawa Y, Inaba T, Yoshida C, Takano S (1992) Pharmacological studies of the new antiinflammatory agent 3-formylamino-7-methylsulfonylamino-6-phenoxy-4H-1-benzopyran-4-o ne. 1st communication: antiinflammatory, analgesic and other related properties. Arzneimittelforschung 42(7): 935–944PubMedGoogle Scholar
  125. 125.
    Calhoun W, Gilman SC, Datko LJ, Copenhaver TW, Carlson RP (1992) Interaction studies of tilomisole, aspirin, and naproxen in acute and chronic inflammation with assessment of gastrointestinal irritancy in the rat. Agents Actions 36(1–2): 99–106PubMedCrossRefGoogle Scholar
  126. 126.
    Ackerman NR, Rooks WH, 2nd, Shott L, Genant H, Maloney P, West E (1979) Effects of naproxen on connective tissue changes in the adjuvant arthritic rat. Arthritis Rheum 22(12): 1365–1374PubMedGoogle Scholar
  127. 127.
    Carlson RP, Hartman DA, Tomchek LA, Walter TL, Lugay JR, Calhoun W, Sehgal SN, Chang JY (1993) Rapamycin, a potential disease-modifying antiarthritic drug. J Pharmacol Exp Ther 266(2): 1125–1138PubMedGoogle Scholar
  128. 128.
    Magari K, Miyata S, Nishigaki F, Ohkubo Y, Mutoh S (2004) Comparison of antiarthritic properties of leflunomide with methotrexate and FK506: effect on T cell activation-induced inflammatory cytokine production in vitro and rat adjuvant-induced arthritis. Inflamm Res 53(10): 544–550PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag Basel/Switzerland 2006

Authors and Affiliations

  • Lisa R. Schopf
    • 1
  • Karen Anderson
    • 1
  • Bruce D. Jaffee
    • 1
  1. 1.Millennium PharmaceuticalsCambridgeUSA

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