Best Practice & Research Clinical Rheumatology
Volume 22, Issue 2 , Pages 253-267 , April 2008

Animal models for arthritis

  • Robert Dinser (Doctor)

      Affiliations

    • Corresponding Author InformationTel.: +49 (0) 6032 9960; Fax: +49 (0) 6032 996 2809.

References 

  1. Williams RO, Feldmann M, Maini RN. Anti-tumor necrosis factor ameliorates joint disease in murine collagen-induced arthritis. Proceedings of the National Academy of Sciences of the United States of America. 1992;89:9784–9788
  2. Elliott MJ, Maini RN, Feldmann M, et al. Treatment of rheumatoid arthritis with chimeric monoclonal antibodies to tumor necrosis factor alpha. Arthritis & Rheumatism. 1993;36:1681–1690
  3. Joosten LA, Helsen MM, Saxne T, et al. Il-1ab blockade prevents cartilage and bone destruction in murine type II collagen-induced arthritis, whereas TNF-α blockade only ameliorates joint inflammation. Journal of Immunology. 1999;163:5049–5055
  4. Bresnihan B, Alvaro-Gracia JM, Cobby M, et al. Treatment of rheumatoid arthritis with recombinant human interleukin-1 receptor antagonist. Arthritis & Rheumatism. 1998;41:2196–2204
  5. Bathon JM, Martin RW, Fleischmann RM, et al. A comparison of etanercept and methotrexate in patients with early rheumatoid arthritis. The New England Journal of Medicine. 2000;343:1586–1593
  6. Smolen JS, Aletaha D, Koeller M, et al. New therapies for treatment of rheumatoid arthritis. Lancet. 2007;370:1861–1874
  7. Koenders MI, Lubberts E, Oppers-Walgreen B, et al. Blocking of interleukin-17 during reactivation of experimental arthritis prevents joint inflammation and bone erosion by decreasing RANKL and interleukin-1. American Journal of Pathology. 2005;167:141–149
  8. Maini RN, Taylor PC, Szechinski J, et al. Double-blind randomized controlled clinical trial of the interleukin-6 receptor antagonist, tocilizumab, in European patients with rheumatoid arthritis who had an incomplete response to methotrexate. Arthritis & Rheumatism. 2006;54:2817–2829
  9. Ruth JH, Haas CS, Park CC, et al. CXCL16-mediated cell recruitment to rheumatoid arthritis synovial tissue and murine lymph nodes is dependent upon the MAPK pathway. Arthritis & Rheumatism. 2006;54:765–778
  10. Brand DD, Kang AH, Rosloniec EF. Immunopathogenesis of collagen arthritis. Springer Seminars in Immunopathology. 2003;25:3–18
  11. Kannan K, Ortmann RA, Kimpel D. Animal models of rheumatoid and their relevance to human disease. Pathophysiology. 2005;12:167–181
  12. Sakaguchi S, Sakaguchi N. Animal models of arthritis caused by systemic alteration of the immune system. Current Opinion In Immunology. 2005;17:589–594
  13. Vierboom MPM, Jonker M, Bontrop RE, t'Hart B. Modeling human arthritic diseases in non-human primates. Arthritis Research & Therapy. 2005;7:145–154
  14. Müller-Ladner U, Kriegsmann J, Franklin BN, et al. Synovial fibroblasts of patients with rheumatoid arthritis attach to and invade normal human cartilage when engrafted into SCID mice. American Journal of Pathology. 1996;149:1607–1615
  15. Tolbboom TC, van der Helm-van Mil AH, Nelissen RG, et al. Invasiveness of fibroblast-like synoviocytes is an individual patient characteristic associated with the rate of joint destruction in patients with rheumatoid arthritis. Arthritis & Rheumatism. 2005;52:1999–2002
  16. Fiehn C, Neumann E, Wunder A, et al. Methotrexate and albumin coupled with MTX supress synovial fibroblast invasion and cartilage degradation in vivo. Annals of the Rheumatic Diseases. 2004;63:884–886
  17. Neumann E, Judex M, Kullmann F, et al. Inhibition of cartilage destruction by double gene transfer of IL-1Ra and IL-10 involves the activin pathway. Gene Therapy. 2002;9:1508–1519
  18. Schett G, Stolina M, Bolon B, et al. Analysis of the kinetics of osteoclastogenesis in arthritic rats. Arthritis & Rheumatism. 2005;52:3192–3201
  19. Hayer S, Redlich K, Korb A, et al. Tenosynovitis and osteoclast formation as the initial preclinical changes in a murine model of inflammatory arthritis. Arthritis & Rheumatism. 2007;56:79–88
  20. Wei S, Kitaura H, Zhou P, et al. IL-1 mediates TNF-induced osteoclastogenesis. The Journal of Clinical Investigation. 2005;115:282–290
  21. Stolina M, Adamu S, Ominsky M, et al. RANKL is a marker and mediator of local and systemic bone loss in two rat models of inflammatory arthritis. Journal of Bone and Mineral Research. 2005;20:1757–1765
  22. Kitaura H, Zhou P, Kim HJ, et al. M-CSF mediated TNF-induced inflammatory osteolysis. The Journal of Clinical Investigation. 2005;115:3418–3427
  23. Kamijo S, Nakajima A, Ikeda K, et al. Amelioration of bone loss in collagen-induced arthritis by neutralizing anti-RANKL monoclonal antibody. Biochemical and Biophysical Research. 2006;347:124–132
  24. Schett G, Middleton S, Bolon B, et al. Additive bone protective effects of anabolic treatment when used in conjunction with RANKL and tumor necrosis factor inhibition in two rat arthritis models. Arthritis & Rheumatism. 2005;52:1604–1611
  25. Miyachi K, Ihara A, Hankins RW, et al. Efficacy of imatinib mesylate (ST1571) treatment for a patient with rheumatoid arthritis developing chronic myelogenous leukema. Clinical Rheumatology. 2003;22:329–332
  26. Dewar AL, Cambareri AC, Zannettino AC, et al. Macrophage colony stimulating factor receptor, c-fms, is a novel target of imatinib. Blood. 2005;105:3127–3132
  27. Ando W, Hashimoto J, Nampei A, et al. Imatinib mesylate inhibits osteoclastogenesis and joint destruction in rats with collagen-induced arthritis. Journal of Bone and Mineral Research. 2006;24:274–282
  28. Paniagua RT, Sharpe O, Ho PP, et al. Selective tyrosine kinase inhibition by imatinib mesylate for the treatment of autoimmune arthritis. The Journal of Clinical Investigation. 2006;116:2633–2644
  29. Jarrett SJ, Conaghan PG, Sloan VS, et al. Preliminary evidence for a structural benefit of the new bisphosphonate zoledronic acid in early rheumatoid arthritis. Arthritis & Rheumatism. 2006;54:1410–1414
  30. Lu J, Kasama T, Kobayashi K, et al. Vascular endothelial growth factor expression and regulation of murine collagen-induced arthritis. Journal of Immunology. 2000;164:5922–5927
  31. Mould AW, Tonks ID, Cahill MM, et al. Vegfb gene knock-out mice display reduced pathology and synovial angiogenesis in both antigen-induced and collagen-induced models of arthritis. Arthritis & Rheumatism. 2003;48:2660–2669
  32. Clavel G, Valvason C, Yamaoka K, et al. Relationship between angiogenesis and inflammation in experimental arthritis. European Cytokine Network. 2006;17:202–210
  33. Park YW, Kang YM, Butterfield J, et al. Thrombospondin 2 functions as an endogenous regulator of angiogenesis and inflammation in rheumatoid arthritis. American Journal of Pathology. 2004;165:2087–2098
  34. Hashimoto A, Tarner IH, Bohle RM, et al. Analysis of vascular gene expression in arthritic synovium by laser-mediated microdissection. Arthritis & Rheumatism. 2007;56:1094–1105
  35. Afuwape AO, Felödmann M, Paleolog EM. Adenoviral delivery of soluble VEGF receptor 1 abrogates disease activity in murine collagen-induced arthritis. Gene Therapy. 2003;10:1950–1960
  36. Yoo SA, Bae DG, Ryoo JW, et al. Arginine-rich anti-vascular endothelial growth factor (anti-VEGF) hexapeptide inhibits collagen-induced arthritis and VEGF-stimulated productions of TNF-alpha and IL-6 by human monocytes. Journal of Immunology. 2005;174:5846–5855
  37. Sone H, Kawakami Y, Sakauchi M, et al. Neutralisation of vascular endothelial growth factor prevents collagen-induced arthritis and ameliorates established disease in mice. Biochemical and Biophysical Research. 2001;281:562–568
  38. Tsai CY, Shiau AL, Chen SY, et al. Amelioration of collagen-induced arthritis in rats by nanogold. Arthritis & Rheumatism. 2007;56:544–554
  39. Yin G, Liu W, An P, et al. Endostatin gene transfer inhibits joint angiogenesis and pannus formation in inflammatory arthritis. Molecular Therapy. 2002;5:547–554
  40. Kim JM, Ho SH, Park EJ, et al. Angiostatin gene transfer as an effective treatment strategy in murine collagen-induced arthritis. Arthritis & Rheumatism. 2002;46:793–801
  41. Jou IM, Shiau AL, Chen SY, et al. Thrombospondin 1 as an effective gene therapeutic strategy in collagen-induced arthritis. Arthritis & Rheumatism. 2005;52:339–344
  42. Davidson BEN, Vitters EL, van der Kraan PM, van den Berg WB. Expression of transforming growth factor-beta (TGFbeta) and the TGFbeta signalling molecule SMAD-2P in spontaneous and instability induced osteoarthritis: role in cartilage degradation, chondrogenesis and osteophyte formation. Annals of the Rheumatic Diseases. 2006;65:1414–1421
  43. Ameye L, Young MF. Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy and corneal diseases. Glycobiology. 2002;12:107–116
  44. Ameye L, Aria D, Jepsen K, et al. Abnormal collagen fibrils in tendons of biglycan/fibromodulin-deficient mice lead to gait impairment, ectopic ossification, and osteoarthritis. FASEB Journal. 2002;16:673–680
  45. Zemmyo M, Meharra EJ, Kuhn K, et al. Accelerated, aging-dependent development of osteoarthritis in alpha1 integrin-deficient mice. Arthritis & Rheumatism. 2003;48:2873–2880
  46. Hagg R, Hedbom E, Mollers U, et al. Absence of the alpha1(IX) chain leads to a functional knock-out of the entire collagen IX protein in mice. The Journal of Biological Chemistry. 1997;272:20650–20654
  47. Hu K, Xu L, Cao L, et al. Pathogenesis of osteoarthritis-like changes in the joints of mice deficient in type IX collagen. Arthritis & Rheumatism. 2006;54:2891–2900
  48. De Hooge AS, van de Lo FA, Bennink MB, et al. Male IL-6 gene knock out mice developed more advanced osteoarthritis upon aging. Osteoarthritis and Cartilage. 2005;13:66–73
  49. Zhang YW, Su Y, Lanning N, et al. Targeted disruption of Mig-6 in the mouse genome leads to early onset degenerative joint disease. Proceedings of the National Academy of Sciences of the United States of America. 2005;102:11740–11745
  50. Rountree RB, Schor M, Chen H, et al. BMP receptor signalling is required for postnatal maintenance of articular cartilage. PLoS Biology. 2004;2:e355
  51. Kamekura S, Hoshi K, Shimoaka T, et al. Osteoarthritis development in novel experimental mouse models induced by knee joint instability. Osteoarthritis and Cartilage. 2005;13:632–641
  52. Bolbos R, Benoit-Cattin H, Langlois JB, et al. Knee cartilage thickness measurements using MRI: a 4 1/2 month longitudinal study in the meniscectomized guinea pig model of OA. Osteoarthritis and Cartilage. 2007;15:656–665
  53. Miot-Noirault E, Vidal A, Pastoureau P, et al. Early detection and monitoring of cartilage alteration in the experimental meniscectomised guinea pig model of osteoarthritis by 99mTc-NTP 15-5 scintigraphy. European Journal of Nuclear Medicine and Molecular Imaging. 2007;34:1280–1290
  54. Kamekura S, Kawasaki Y, Hoshi H, et al. Contribution of runt-related transcription factor 2 to the pathogenesis of osteoarthritis in mice after induction of knee joint instability. Arthritis & Rheumatism. 2006;54:2462–2470
  55. Robertson CM, Pennock AT, Harwood FL, et al. Characterizsation of pro-apoptotic and matrix-degenerative gene expression following induction of osteoarthritis in mature and aged rabbits. Osteoarthritis and Cartilage. 2006;14:471–476
  56. Appleton CTG, McErlain DD, Pitelka V, et al. Forced mobilization accelerates pathogenesis: characterization of a preclinical surgical model of osteoarthritis. Arthritis Research & Therapy. 2007;9:R13
  57. Bove SE, Laemont KD, Brooker RM, et al. Surgically induced osteoarthritis in the rat results in the development of both osteoarthritis-like pain and secondary hyperalgesia. Osteoarthritis and Cartilage. 2006;14:1041–1048
  58. Reginster JY, Deroisy R, Rovati LC, et al. Long-term effects of glucosamine sulphate on osteoarthritis progression: a randomised-controlled clinical trial. Lancet. 2001;357:251–256
  59. Tiraloche G, Girard C, Chouinard L, et al. Effect of oral glucosamine on cartilage degradation in a rabbit model of osteoarthritis. Arthritis & Rheumatism. 2005;52:1118–1128
  60. Goldberg VM, Buckwalter JA. Hyaluronans in the treatment of osteoarthritis of the knee: evidence for a disease-modifying activity. Osteoarthritis and Cartilage. 2005;13:216–224
  61. Clemmons DR, Busby WH, Garmong A, et al. Inhibition of insulin-like growth factor binding protein 5 proteolysis in articular cartilage and joint fluid results in enhanced concentrations of insulin-like growth factor 1 and is associated with improved osteoarthritis. Arthritis & Rheumatism. 2002;46:694–703
  62. Inoue A, Takahashi KA, Arai Y, et al. The therapeutic effects of basic fibroblast growth factor contained in gelatine hydrogel microspheres on experimental osteoarthritis in the rabbit knee. Arthritis & Rheumatism. 2006;54:264–270
  63. Van der Kraan PM, Vitters EL, van de Putte LBA, van den Berg WB. Development of osteoarthritic lesions in mice by metabolic and mechanical alterations in knee joints. American Journal of Pathology. 1989;135:1001–1014
  64. Guingamp C, Gegout-Pottie P, Philippe L, et al. Monoiodoacetate induced experimental osteoarthritis. Arthritis & Rheumatism. 1997;40:1670–1679
  65. Cledes G, Felizardo R, Foucart JM, Cerpentier P. Validation of a chemical osteoarthritis model in rabbit temporomandibular joint: a compliment to biomechanical models. International Journal of Oral and Maxillofacial Surgery. 2006;35:1026–1033
  66. Pomonis JD, Boulet JM, Gottshall SL, et al. Development and pharmacological characterization of a rat model of osteoarthritis pain. Pain. 2005;114:339–346
  67. Beyreuther B, Callizot N, Stöhr T. Antinociceptive efficacy of lacosamide in the monosidum iodoacetate rat model for osteoarthritis pain. Arthritis Research & Therapy. 2007;9:R14
  68. Scharstuhl A, Vitters EL, van der Kraan PM, van den Berg WB. Reduction of osteophyte formation and synovial thickening by adenoviral overexpression of transforming growth factor ß/bone morphogenetic protein inhibitors during experimental osteoarthritis. Arthritis & Rheumatism. 2003;48:3442–3451
  69. Barve RA, Minnerly JC, Weiss DJ, et al. Transcriptional profiling and pathway analysis of monosodium iodoacetate-induced experimental osteoarthritis in rats: relevance to human disease. Osteoarthritis and Cartilage. 2007;15:1190–1198
  70. Nishida T, Kubota S, Kojima S, et al. Regeneration of defects in articular cartilage in rat knee joints by CCN 2. Journal of Bone and Mineral Research. 2004;19:1308–1319
  71. Grossin L, Cournil-Henrionnet C, Pinzano A, et al. Gene transfer with HSP70 in rat chondrocytes confers cytoprotection in vitro and during experimental osteoarthritis. FASEB Journal. 2006;20:65–75
  72. Gay S, Jones RE, Huang GQ, Gay RE. Immunohistologic demonstration of platelet-derived growth factor and sis-conogene expression in scleroderma. The Journal of Investigation Dermatology. 1989;92:201–203
  73. Yamakage A, Kikuchi K, Smith EA, et al. Selective upregulation of platelet-derived growth factor alpha receptors by transforming growth factor beta in scleroderma fibroblasts. The Journal of Experimental Medicine. 1992;175:1227–1234
  74. Distler JHW, Jüngel A, Huber LC, et al. Imatinib mesylate reduces production of extracellular matrix and prevents development of experimental dermal fibrosis. Arthritis & Rheumatism. 2007;56:311–322
  75. Ghofrani HA, Seeger W, Grimminger F. Imatinib for the treatment of pulmonary arterial hypertension. The New England Journal of Medicine. 2005;353:1412–1413
  76. Hoi AY, Hickey MJ, Hall P, et al. Macrophage migration inhibitory factor deficiency attenuates macrophage recruitment, glomerulonephritis, and lethality in MRL/lpr mice. Journal of Immunology. 2006;177:5687–5696
  77. Marquina R, Diez MA, Lopez-Hoyos M, et al. Inhibition of B-cell death causes the development of an IgA nephropathy in (New Zealand White×C57BL/6)F1-bcl-2 transgenic mice. Journal of Immunology. 2004;172:7177–7185
  78. Gonzalez J, Tamayo E, Santiuste I, et al. CD4+CD25+T cell-dependent inhibition of autoimmunity in transgenic mice overexpressing human Bcl-2 in T-lymphocytes. Journal of Immunology. 2007;178:2778–2786
  79. Bachmann MP, Bartsch H, Gross JK, et al. Autoimmunity as a result of escape from RNA surveillance. Journal of Immunology. 2006;177:1698–1707
  80. Scofield RH, Asfa S, Obeso D, et al. Immunization with short peptides from the 60-kDa Ro antigen recapitulates the serological and pathological findings as well as the salivary gland dysfunction of Sjögren's syndrome. Journal of Immunology. 2005;175:8409–8414
  81. Hacquard-Bouder C, Ittah M, Breban M. Animal models of HLA-B27 associated diseases: new outcomes. Joint Bone Spine. 2006;73:132–138
  82. Hacquard-Bouder C, Falgarone G, Bosquet A, et al. Defective costimulatory function is a striking feature of antigen-presenting cells in an HLA-B27-transgenic rat model of spondyloarthropathy. Arthritis & Rheumatism. 2004;50:1624–1635
  83. Turner MJ, Sowders DP, Delay ML, et al. HLA-B27 misfolding in transgenic rats is associated with the activation of the unfolded protein response. Journal of Immunology. 2005;175:2438–2448
  84. Taurog JD, Maika SD, Satumtira N, et al. Inflammatory disease in HLA-B27 transgenic rats. Immunological Reviews. 1999;169:209–223
  85. Tran TM, Dorris ML, Satumtira N, et al. Additional human ß2-microglobulin curbs HLA-B27 misfolding and promotes arthritis and spondylitis without colitis in male HLA-B27-transgenic rats. Arthritis & Rheumatism. 2006;54:1317–1327
  86. Bardos T, Zhang J, Mikecz K, et al. Mice lacking endogenous major histocompatibility complex class II develop arthritis resembling psoriatic arthritis at an advanced age. Arthritis & Rheumatism. 2002;46:2465–2475
  87. Cook PW, Brown JR, Cornell KA, Pittelkow MR. Suprabasal expression of human amphiregulin in the epidermis of transgenic mice induces a severe, early-onset, psoriasis-like skin pathology: expression of amphiregulin in the basal epidermis is also associated with synovitis. Experimental Dermatology. 2004;13:347–356
  88. Zenz R, Eferl R, Kenner L, et al. Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature. 2005;437:369–375
  89. Pendleton A, Johnson MD, Hughes A, et al. Mutations in ANKH cause chondrocalcinosis. American Journal of Human Genetics. 2002;71:933–940
  90. Gurley KA, Reimer RJ, Kingsley DM. Biochemical and genetic analysis of ANK in arthritis and bone disease. American Journal of Human Genetics. 2006;79:1017–1029
  91. Getting SJ, Lam CW, Chen AS, et al. Melanocortin 3 receptors control crystal-induced inflammation. FASEB Journal. 2006;20:2234–2241
  92. Getting SJ, Christian HC, Flower RJ, Perretti M. Activation of melanocortin type 3 receptor as a molecular mechanism for adrenocorticotropic hormone efficacy in gouty arthritis. Arthritis & Rheumatism. 2002;46:2765–2775
  93. Steere AC, Glickstein L. Elucidation of Lyme arthritis. Nature Reviews. Immunology. 2004;4:143–152
  94. Ma Y, Seiler KP, Eichwald EJ, et al. Distinct characteristics of resistance to Borrelia burgdorferi-induced arthritis in C57BL/6N mice. Infection and Immunity. 1998;66:161–168
  95. Steere AC, Angelis SM. Therapy for Lyme arthritis: strategies for the treatment of antibiotic-refractory arthritis. Arthritis & Rheumatism. 2006;54:3079–3086

PII: S1521-6942(08)00007-7

doi: 10.1016/j.berh.2008.01.007

Best Practice & Research Clinical Rheumatology
Volume 22, Issue 2 , Pages 253-267 , April 2008