Lessons for joint destruction from animal models

Current Opinion in Rheumatology

Volumn 9, Issue 3, 1997, Pages 221-228

  Van Den Berg, Wim B ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6; NEUTRALIZING ANTIBODY; RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; CARTILAGE DEGENERATION; FIBROBLAST; GENE TRANSFER; JOINT DESTRUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ARTHRITIS; AUTOIMMUNITY; CARTILAGE, ARTICULAR; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYMES; INTERLEUKINS; JOINTS;

EID: 0030927006     PISSN: 10408711     EISSN: None     Source Type: Journal    
DOI: 10.1097/00002281-199705000-00008     Document Type: Review

References (71)

1. Van de Loo AAJ, Joosten LAB, van Lent PLEM, Arntz OJ, van den Berg WB: Role of interleukin-1, tumor necrosis factor α and interleukin-6 in cartilage proteoglycan metabolism and destruction: effect of in situ cytokine blocking in murine antigen- and zymosan-induced arthritis. Arthritis Rheum 1995, 38:164-172.
2. Joosten LAB, Helsen MMA, van den Berg WB: Effect of IL-10 on murine SCW arthritis: role of TNF and IL-1 in joint inflammation and cartilage destruction. Arthritis Rheum 1995, 38(suppl 9):S401.
3. Joosten LAB, Helsen MMA, van de Loo FAJ, van den Berg WB: Anticytokine treatment of established type II collagen-induced arthritis in DBA/1 mice. Arthritis Rheum 1996, 39:797-809. This paper reports that TNF is only involved in onset of arthritis, whereas interleukin-1 is a dominant cytokine in both early and late stages. Interleukin-1 is then generated independently of TNF. Interleukin-1β is the pivotal isotype in this model.
4. Probert L, Plows D, Kontogeorgos G, Kollias G: The type I interleukin receptor acts in series with TNF to induce arthritis in TNF-transgenic mice. Eur J Immunol 1995, 25:1794-1798. Provides definite proof that TNF alone is neither arthritogenic nor destructive.
5. Mori L, Iselin S, Delibero G, Lesslauer W: Attenuation of collagen induced arthritis in 55 kDa TNF receptor type 1(TNFR1) IgG1 treated and TNFR1 deficient mice. J Immunol 1996, 157:3178-3182. This study hows that arthritis can occur in the absence of TNF receptor activation and that the destructive stage of established collagen arthritis is independent of TNF.
6. Campion GV, Lebsack ME, Lookabaugh J, Gordon G, Catalano M, Borenstein D, Caldwell J, Cohen SA, Cohen SB, Fleischmann R, et al.: Dose-range and dose-frequency study of recombinant human IL-1ra in patients with rheumatoid arthritis. Arthritis Rheum 1996, 39:1092-1101.
7. Breshnihan B, on behalf of the collaborating investigators, J Lookabaugh K, Witt P, Musikic P: Treatment with recombinant human IL-1ra in rheumatoid arthritis: results of a randomized double-blind, placebo-controlled multicenter trial. Arthritis Rheum 1996, 39(suppl 9):S73.
8. Jouvenne P, Fossiez F, Garonne P, Djossou O, Banchereau J, Miossec P: Increased incidence of neutralizing autoantibodies against IL-1α in nondestructive chronic polyarthritis. J Clin Immunol 1996, 16:283-290.
9. Zheng H, Fletcher D, Kozak W, Jiang M, Hofmann KJ, Conn CA, Soszynski D, Grabiec C, Kostura MJ, Stevens K, et al.: Resistance to fever induction and impaired acute-phase response in IL-1β-deficient mice. Immunity 1995, 3:9-19. The generated IL-1β-deficient mice show normal immune responses, and proof is provided that they can be used as an excellent tool to analyze IL-1β-dependent processes.
10. Fantuzzi G, Hui Z, Faggioni R, Benigni F, Ghezzi P, Sipe JD, Shaw AR, Dinarello CA: Effect of endotoxin in IL-1β deficient mice. J Immunol 1996, 157:291-296.
11. Fantuzzi G, Dinarello CA: The inflammatory response in IL-1β-deficient mice: comparison with other cytokine-related kock-out mice. J Leukocyte Biol 1996, 59:489-493.
12. Ku G, Faust T, Lauffer LL, Livingston DJ, Harding MW: IL-1β converting enzyme inhibition blocks progression of type II collagen-induced arthritis in mice. Cytokine 1996, 8:377-386. Using specific ICE inhibitors, it is shown that interleukin-1β is a dominant cytokine in collagen arthritis, further indicating that ICE is a relevant target in arthritis.
13. Pasparakis M, Alexopoulou L, Episkopou V, Kollias G: Immune and inflammatory responses in TNFα deficient mice: a critical requirement for TNFα in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune responses. J Exp Med 1996, 184:1397-1411.
14. Georgopoulos S, Plows D, Kollias G: Transmembrane TNF is sufficient to induce localized tissue toxity and chronic inflammatory arthritis in transgenic mice. J Inflamm 1996, 46:86-97. Convincing demonstration that membrane-associated TNF is sufficient in the induction of an arthritic process.
15. Douni E, Akassoglou K, Alexopoulou L, Georgopoulos S, Haralambous S, Hill S, Kassiotis G, Kontoyannis D, Pasparakis M, Plows D, Probert L, Kollias G: Transgenic and knockout analyses of the role of TNF in immune regulation and disease pathogenesis. J Inflamm 1996, 47:27-38.
16. Makarov SS, Olsen JC, Johnston WN, Anderle SK, Brown RR, Baldwin AS Jr, Haskill KS, Schwab JH: Suppression of experimental arthritis by gene transfer of IL-1ra cDNA. Proc Natl Acad Sci U S A 1996, 93:402-406. Evidence supporting the applicability of local gene transfer in arthritis and underlining involvement of local interleukin-1 in bacterial arthritis.
17. Bakker AC, Joosten LAB, Arntz OJ, Helsen MMA, Bendele A, van de Loo FAJ, van den Berg WB: Gene therapy of murine collagen-induced arthritis: Local expression of the human IL-1ra protein prevents onset. Arthritis Rheum 1997, in press. Provides proof of local involvement of interleukin-1 in onset of collagen arthritis and shows a concomitant protective effect of local gene therapy on nearby joints.
18. Otani K, Nita I, Macaulay W, Georgescu HI, Robbins PD, Evans CH: Suppression of antigen-induced arthritis in rabbits by ex vivo gene therapy. J Immunol 1996, 156:3558-3562. This convincing study shows excellent gene expression in an inflamed joint and confirms involvement of interleukin-1 in inflammation and cartilage breakdown in this model, as well as its pivotal role in chondrocyte proteoglycan synthesis inhibition.
19. Van Lent PLEM, van de Loo FAJ, Holthuysen AEM, van den Bersselaar LAM, Vermeer H, van den Berg WB: Major role for IL-1 but not for TNF in early cartilage damage in immune complex arthritis in mice. J Rheumatol 1995, 22:2250-2258.
20. Fukumoto T, Matsukawa A, Ohkawara S, Takagi K, Yoshinaga M: Administration of neutralizing antibody against rabbit IL-1ra exacerbates lipopolysaccharide-induced arthritis in rabbits. Inflamm Res 1996, 45:479-485.
21. Caron JP, Fernandes JC, Martel-Pelletier J, Tardif G, Mineau F, Geng C, Pelletier JP: Chondroprotective effect of intraarticular injections of IL-1ra in experimental osteoarthritis. Arthritis Rheum 1996, 39:1535-1544.
22. Van de Loo FAJ, Kuiper S, van Enckevort FHJ, Arntz OJ, van den Berg WB: IL-6 ameliorates cartilage destruction during experimental arthritis: a study in IL-6 deficient mice. Am J Pathol 1997, in press. This paper provides cogent evidence that interleukin-6 enhances inflammation, yet is a protective mediator with respect to cartilage destruction and underlines the potential uncoupling of arthritis and cartilage destruction.
23. Walmsley M, Katsikis PD, Abney E, Parry S, Williams RO, Maini RN, Feldmann M: IL-10 inhibition of the progression of established collagen-induced arthritis. Arthritis Rheum 1996, 39:495-503. First demonstration that interleukin-10 treatment suppresses murine arthritis.
24. Kasama T, Strieter RM, Lukacs NW, Lincoln PM, Burdick MD: IL-10 expression and chemokine regulation during the evolution of murine type II collagen-induced arthritis. J Clin Invest 1995, 95:2868-2876.
25. Joosten LAB, Lubberts E, Durez P, Helsen MMA, Jacobs MJM, Goldman M, van den Berg WB: Role of IL-4 and IL-10 in murine collagen-induced arthritis. Arthritis Rheum 1997, 40:00-00. These authors provide proof that interleukin-10 is a major endogenous inhibitor of arthritis expression and shows that therapeutic effects of interleukin-10 on cartilage damage are markedly enhanced by combination with interleukin-4. Such treatment suppresses TNF and interleukin-1 production and improves the balance between IL-1ra and interleukin-1 in cartilage.
26. Mauri C, Williams RO, Walmsley M, Feldmann M: Relationship between Th/Th2 cytokine patterns and the arthritogenic response in collagen-induced arthritis. Eur J Immunol 1996, 26:1511-1518.
27. Williams RO, Whyte A: Anti-CD4 monoclonal antibodies suppress murine collagen-induced arthritis only at the time of primary immunisation. Cell Immunol 1996, 170:291-295.
28. 2 cytokines provides a mechanistic basis for the efficacy of this type of CD4 therapy.
29. Tanaka Y, Otsuka T, Hotokebuchi T, Miyahara H, Nakashima H, Kuga S, Nemoto Y, Niiro H, Niho Y: Effect of IL-10 on collagen-induced arthritis in mice. Inflamm Res 1996, 45:283-288.
30. Yoshino S: Downregulation of silicone-induced chronic arthritis by gastric administration of type II collagen. Immunopharmacology 1995, 31:103-108.
31. Yoshino S: Oral administration of type II collagen suppresses non-specifically induced chronic arthritis in rats. Biomed Pharmacother 1996, 50:24-28.
32. Segal BM, Shevach EM: IL-12 unmasks latent autoimmune disease in resistant mice. J Exp Med 1996, 164:771-775.
33. Germann T, Szeliga J, Hess H, Störkel S, Podlaski F, Gately M, Schmitt E, Rüde E: Administration of IL-12 in combination with type II collagen induces severe arthritis in DBA/1 mice. Proc Natl Acad Sci U S A 1995, 92:4823. First demonstration of a pronounced stimulatory effect of interleukin-12 on expression of collagen arthritis, linked to skewing of anticollagen type II autoimmunity.
34. Szeliga J, Hess H, Rüde E, Schmitt E, Germann T: IL-12 promotes cellular but not humoral type II collagen-specific Th1-type responses in C57BI/6 and B10.Q mice and fails to induce arthritis. Int Immunol 1996, 8:1221-1227.
35. Terato K, Harper DS, Griffiths MM, Hasty DL, Ye XJ, Cremer MA, Seyer JM: Collagen-induced arthritis in mice: synergistic effect of E. coli lipopolysaccharide bypasses epitope specificity in the induction of arthritis with monoclonal antibodies to type II collagen. Autoimmunity 1995, 22:137-147.
36. Hess H, Gately MK, Rude E, Schmitt E, Szeliga J, Germann T: High doses of IL-12 inhibit the development of Joint disease in DBA/1 mice immunized with type II collagen in complete Freund's adjuvant. Eur J Immunol 1996, 26:187-191.
37. Van den Berg WB, Joosten LAB, Lubberts E, Helsen MMA: Dual role of IL-12 in early and late stages of murine collagen arthritis. Arthritis Rheum 1996, 39(suppl 9):S78.
38. Edwards CK, Zhou T, Zhang J, Baker TJ, Long RE, Borcherding DR, Bowlin TL, Bluethmann H, Mountz JD: Inhibition of superantigen-induced proinflammatory cytokine production and inflammatory arthritis in MRL-lpr/lpr mice by a transcriptional inhibitor of TNFα. J Immunol 1996, 157:1758-1772. Convincing demonstration that bacterial superantigens can provoke exacerbation of nonrelated arthritis, through TNF generation, and proof of efficacy of a novel transcriptional TNF inhibitor in this arthritis.
39. Fujisawa K, Asahara H, Okamoto K, Aono H, Hasunuma T, Kobata T, Iwakra Y, Yonehara S, Sumida T, Nishioka K: Therapeutic effect of the anti-Fas antibody on arthritis in HTLV-I fax transgenic mice. J Clin Invest 1996, 98:271-278.
40. Kunkel SL, Lukacs N, Kasama T, Strieter RM: The role of chemokines in inflammatory joint disease. J Leukoc Biol 1996, 59:6-12. Excellent review of the role of chemokines in arthritis and application of antichemokine antibodies.
41. Issekutz AC, Ayer L, Miyasaka M, Issekutz TB: Treatment of established adjuvant arthritis in rats with monoclonal antibody to CD18 and very late activation antigen-4 integrins suppresses neutrophil and T-lymphocyte migration to the Joints and improves clinical disease. Immunol 1996, 88:596-576.
42. Kinne RW, Schmidtweber CB, Hoppe R, Buchner E, Palombokinne E, Nurnberg E, Emmrich F: Long-term amelioration of rat adjuvant arthritis following systemic elimination of macrophages by clodronate-containing liposomes. Arthritis Rheum 1995, 38:1777-1790.
43. Van Lent PLEM, Holthuysen AEM, van den Bersselaar L, van Rooijen N, van de Putte LBA, van den Berg WB: Role of macrophage-like synovial lining cells in localization and expression of experimental arthritis. Scand J Rheumatol 1995, 24(suppl 101):83-89.
44. Osterman T, Kippo K, Lauren L, Hannuniemi R, Sellman R: Effect of clodronate on established collagen induced arthritis in rats. Inflamm Res 1995, 44:258-263.
45. Van Lent PLEM, Holthuysen AEM, van den Bersselaar LAM, van Rooijen N, Joosten LAB, van de Loo FAJ, van de Putte LBA, van den Berg WB: Phagocytic lining cells determine local expression of inflammation in type II collagen-induced arthritis. Arthritis Rheum 1996, 39:1545-1555. This paper provides compelling evidence that activation of synovial lining macrophages is a decisive step in the expression of cartilage-directed autoimmune arthritis.
46. Van Lent PLEM, Blom A, Holthuysen AEM, Jacobs CWM, van den Berg WB: Monocytes/macrophages rather than PMN are involved in early cartilage degradation in cationic immune complex arthritis in mice. J Leukoc Biol 1997, 61:61.
47. Van den Berg WB, van Lent PLEM: Role of macrophages in chronic arthritis. Immunobiology 1996, 195:614-623.
48. Sack U, Kuhn H, Kampfer I, Genest M, Arnold S, Pfeiffer G, Emmrich F: Orthotopic implantation of inflamed synovial tissue from RA patients induces a characteristic arthritis in immunodeficient mice. J Autoimmun 1996, 51:58. This article elegantly demonstrates that the arthritogenic properties of RA synovial tissue can be studied by orthotopic engraftment in SCID mice.
49. Müller-Ladner U, Kriegsmann J, Franklin BN, Matsumoto S, Geiler T, Gay RE, Gay S: Synovial fibroblasts of patients with rheumatoid arthritis attach to and invade normal human cartilage when engrafted into SCID mice. Am J Pathol 1996, 149:1607-1615. This paper provides convincing evidence that cartilage destruction can occur by RA synovial fibroblasts, in the absence of T cells and further underlines the aggressive behavior of RA synovial fibroblasts as compared with cells from patients with OA and normal control patients.
50. Mima T, Saeki Y, Ohshima S, Nishimoto N, Matsushita M, Shimizu M, Kobayshi Y, Nomura T, Kishimoto T: Transfer of rheumatoid arthritis into severe combined immunodeficent mice: the pathogenic implications of T cell populations oligoclonally expanding in the rheumatoid joints. J Clin Invest 1995, 96:1746-1758.
51. Sakata A, Sakata K, Ping H, Ohmura T, Tsukano M, Kakimoto K: Successful induction of severe destructive arthritis by the transfer of in vitro-activated synovial fluid T cells from patients with rheumatoid arthritis in severe combined immunodeficient mice. Clin Exp Immunol 1996, 104:247-254. T cells from patients with RA display arthritogenic and destructive potential and are enriched in the synovial fluid of affected joints.
52. Peacock DJ, Banquerigo ML, Brahn E: A novel angiogenesis inhibitor suppresses rat adjuvant arthritis. Cell Immunol 1995, 160:178-184.
53. Oliver SJ, Cheng TP, Banquerigo ML, Brahn E: Suppression of collagen-induced arthritis by an angiogenesis inhibitor, AGM-1470, in combination with cyclosporin: reduction of vascular endothelial growth factor (VEGF). Cell Immunol 1995, 166:196-206.
54. Sugiura N, Iwasaki S, Aoki S, Hori Y, Sakurai K, Suzuki S, Kimata K: Suppression of pannus-like extension of synovial cells by lipid-derivatized chondroitin sulphate: in vitro and in vivo studies using Escherichia coli-induced arthritic rabbits. Int J Exp Pathol 1995, 76:369-379.
55. Kim HK, Kerr RG, Cruz TF, Salter RB: Effects of continous passive motion and immobilization on synovitis and cartilage degradation in antigen induced arthritis. J Rheumatol 1995, 22:1714-1721.
56. Bogoch ER, Moran E, Crowe S, Fornasier V: Arthritis not immobilization causes bone loss in the carrageenan injection model of inflammatory arthritis. J Orthop Res 1995, 13:777-782.
57. Singer II, Kawka DW, Bayne EK, Donatelli SA, Weidner JR, Williams HR, Ayala JM, Mumford RA, Lark MW, Glant TT, Nabozny GH, David CS: VDIPEN, a metalloproteinase-generated neoepitope, is induced and immunolocalized in articular cartilage during inflammatory arthritis. J Clin Invest 1995, 95:2178-2186.
58. Olzewski JM, Moore VL, McDonnell J, Williams H, Saphos CA, Green BG, Knight WB, Chapman KT, Hagmann WK, Dorn CP, Hale JJ, Mumford RA: Proteoglycan-degrading activity of human stromelysin-1 and leukocyte elastase in rabbit joints: quantitation of proteoglycan and a stromelysin-induced HABR fragment of aggrecan in synovial fluid and cartilage. Connect Tissue Res 1996, 33:291-299.
59. Olzewski J, McDonnell J, Stevens K, Visco O, Moore V: A matrix metalloproteinase-generated aggrecan neoepitope as a marker of skeletal maturation and aging in cartilage. Arthritis Rheum 1996, 39:1234-1237.
60. Fosang AJ, Last K, Maciewicz RA: Aggrecan is degraded by matrix metalloproteinases in human arthritis: evidence that matrix metalloproteinase and aggrecanase activities can be independent. J Clin Invest 1996, 98:2292-2299. This elegant demonstration of metalloproteinase involvement in aggrecan breakdown in human arthritis and support for separate metalloproteinase and aggrecanase attack on particular aggrecan molecules in articular cartilage underlines the finding that there is more than just aggrecanase.
61. Van Meurs JBJ, van Lent PLEM, Singer II, Bayne EK, van de Loo FAJ, van den Berg WB: IL-1 receptor antagonist prevents expression of the metalloproteinase-generated neoepitope VDIPEN during antigen induced arthritis. Arthritis Rheum 1996, 39(suppl 9):S79.
62. 2 is involved in interleukin-1-mediated stromelysin expression and cartilage damage.
63. Flory CM, Pavco PA, Jarvis TC, Lesch ME, Wincott FE, Beigelman L, Hunt SW, Schrier DJ: Nuclease-resistant ribozymes decrease stromelysin mRNA levels in rabbit synovium following exogenous delivery to the knee joint. Proc Nat Acad Sci U S A 1996, 93:754-758. A neat demonstration that ribozymes can be applied to joint tissue and show stable and specific activity at this site.
64. Kakimoto K, Matsukawa A, Yoshinaga M, Nakamura H: Suppressive effect of a neutrophil elastase inhibitor on the development of collagen-induced arthritis. Cell Immunol 1995, 165:26-32.
65. Prigent D, Trancart MM, Seed MP, Willoughby DA: Proteoglycan degrading activity in granulomatous inflammation: comparison between the C57BI/6 and C57bg/bg mouse. Inflamm Res 1996, 45:494-498.
66. Maksymowych WP, Nation N, Nash P, Macen J, Lucas A, McFadden G, Russell AS: Amelioration of antigen induced arthritis in rabbits treated with a secreted viral serine proteinase inhibitor. J Rheumatol 1996, 23:878-882.
67. Malmström V, Michaëlsson E, Burkhardt H, Mattsson R, Vuorio E, Holmdahl R: Systemic versus cartilage-specific expression of a type II collagen-specific T-cell epitope determines the level of tolerance and susceptibility to arthritis. Proc Natl Acad Sci U S A 1996, 93:4480-4485. Elegant use of collagen type II targeted transgenic mice to gain further insight in the regulation of cartilage-specific autoimmunity, which may direct future regulation of tolerance.
68. Leroux JY, Guerassimov A, Cartman A, Delaunay N, Webber C, Rosenberg LC, Banerjee S, Poole AR: Immunity to the G1 globular domain of the cartilage proteoglycan aggrecan can induce inflammatory erosive polyarthritis and spondylitis in BALB/c mice but immunity to G1 is inhibited by covalently bound keratan sulfate in vitro and in vivo. J Clin Invest 1996, 97:621-632.
69. Buzas EI, Brennan FR, Mikecz K, Garzo M, Negroiu G, Hollo K, Cs-Szabo G, Pintye E, Glant TT: A proteoglycan(aggrecan)-specific T cell hybridoma induces arthritis in BALB/c mice. J Immunol 1995, 155:2679-2687.
70. Vingsbo C, Sahlstrand P, Brun JG, Jonsson R, Saxne T, Holmdahl R: Pristane-induced arthritis in rats: a new model for RA with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. Am J Pathol 1996, 149:1675-1683.
71. Remmers EF, Longman RE, Du Y, Ohare A, Cannon GW, Griffiths MM, Wilder RL: A genome scan localizes five non MHC loci controlling collagen-induced arthritis in rats. Nat Genet 1996, 14:82-85.