Interleukin-18 promotes joint inflammation and induces interleukin-1-driven cartilage destruction

American Journal of Pathology

Volumn 165, Issue 3, 2004, Pages 959-967

  Joosten, Leo A B ^a   Smeets, Ruben L ^a   Koenders, Marije I ^a   Van Den Bersselaar, Liduine A M ^a   Helsen, Monique M A ^a   Oppers Walgreen, Birgitte ^a   Lubberts, Erik ^a   Iwakura, Yoichiro ^b   Van De Loo, Fons A J ^a   Van Den Berg, Wim B ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; INTERLEUKIN 1; INTERLEUKIN 18; INTERLEUKIN 1BETA; PROTEOGLYCAN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; CARTILAGE DEGENERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE TRANSFER; HISTOPATHOLOGY; INFLAMMATORY CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; WILD TYPE;

EID: 4344717421     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63357-3     Document Type: Article

References (57)

1. Nakamura K, Okamura H, Wada M, Nagata K, Tamura T: Endotoxin-induced serum factor that stimulates gamma interferon production. Infect Immun 1989, 57:590-595
2. Ushio S, Namba M, Okura T, Hattori K, Nukada Y, Akita K, Tanabe F, Konishi K, Micallef M, Fujii M, Torigoe K, Tanimoto T, Fukuda S, Ikeda M, Okamura H, Kurimoto M: Cloning of the cDNA for human IFN-gamma-inducing factor, expression in Escherichia coli, and studies on the biologic activities of the protein. J Immunol 1996, 156:4274-4279
3. Kohno K, Kataoka J, Ohtsuki T, Suemoto Y, Okamoto I, Usui M, Ikeda M, Kurimoto M: IFN-gamma-inducing factor (IGIF) is a costimulatory factor on the activation of Th1 but not Th2 cells and exerts its effect independently of IL-12. J Immunol 1997, 158:1541-1550
4. Gu Y, Kuida K, Tsutsui H, Ku G, Hsiao K, Fleming MA, Hayashi N, Higashino K, Okamura H, Nakanishi K, Kurimoto M, Tanimoto T, Flavell RA, Sato V, Harding MW, Livingston DJ, Su MS: Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science 1997, 275:206-209
5. Dinarello CA: Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann NY Acad Sci 1993, 856:1-11
6. Dinarello CA: Interleukin-18, a proinflammatory cytokine. Eur Cytokine Netw 2000, 11:483-486
7. Schonbeck U, Mach F, Libby P: Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol 1998, 161:3340-3346
8. Coeshott C, Ohnemus C, Pilyavskaya A, Ross S, Wieczorek M, Kroona H, Leimer AH, Cheronis J: Converting enzyme-independent release of tumor necrosis factor alpha and IL-1 beta from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3. Proc Natl Acad Sci USA 1999, 96:6261-6266
9. Sugawara S, Uehara A, Nochi T, Yamaguchi T, Ueda H, Sugiyama A, Hanzawa K, Kumagai K, Okamura H, Takada H: Neutrophil proteinase 3-mediated induction of bioactive IL-18 secretion by human oral epithelial cells. J Immunol 2001, 167:6568-6575
10. Tsutsui H, Kayagaki N, Kuida K, Nakano H, Hayashi N, Takeda K, Matsui K, Kashiwamura S, Hada T, Akira S, Yagita H, Okamura H, Nakanishi K: Caspase-1-independent, Fas/Fas ligand-mediated IL-18 secretion from macrophages causes acute liver injury in mice. Immunity 1999, 11:359-367
11. Okamura H, Tsutsui H, Kashiwamura S, Yoshimoto T, Nakanishi K: Interleukin-18: a novel cytokine that augments both innate and acquired immunity. Adv Immunol 1998, 70:281-312
12. Stoll S, Jonuleit H, Schmitt E, Muller G, Yamauchi H, Kurimoto M, Knop J, Enk AH: Production of functional IL-18 by different subtypes of murine and human dendritic cells (DC): DC-derived IL-18 enhances IL-12-dependent Th1 development. Eur J Immunol 1998, 28:3231-3239
13. Brossart P, Grunebach F, Stuhler G, Reichardt VL, Mohle R, Kanz L, Brugger W: Generation of functional human dendritic cells from adherent peripheral blood monocytes by CD40 ligation in the absence of granulocyte-macrophage colony-stimulating factor. Blood 1998, 92:4238-4247
14. Udagawa N, Horwood NJ, Elliott J, Mackay A, Owens J, Okamura H, Kurimoto M, Chambers TJ, Martin TJ, Gillespie MT: Interleukin-18 (interferon-gamma- inducing factor) is produced by osteoblasts and acts via granulocyte/macrophage colony-stimulating factor and not via interferon-gamma to inhibit osteoclast formation. J Exp Med 1997, 185:1005-1012
15. Olee T, Hashimoto S, Quach J, Lotz M: IL-18 is produced by articular chondrocytes and induces proinflammatory and catabolic responses. J Immunol 1999, 162:1096-1100
16. Akira S: The role of IL-18 in innate immunity. Curr Opin Immunol 2000, 12:59-63
17. Suzuki N, Chen NJ, Millar DG, Suzuki S, Horacek T, Hara H, Bouchard D, Nakanishi K, Penninger JM, Ohashi PS, Yeh WC: IL-1 receptor-associated kinase 4 is essential for IL-18-mediated NK and Th1 cell responses. J Immunol 2003, 170:4031-405
18. Kalina U, Kauschat D, Koyama N, Nuernberger H, Ballas K, Koschmieder S, Bug G, Hofmann WK, Hoelzer D, Ottmann OG: IL-18 activates STAT3 in the natural killer cell line 92, augments cytotoxic activity, and mediates IFN-gamma production by the stress kinase p38 and by the extracellular regulated kinases p44erk-1 and p42erk-21. J Immunol 2000, 165:1307-1313
19. Morel JC, Park CC, Kumar P, Koch AE: Interleukin-18 induces rheumatoid arthritis synovial fibroblast CXC chenokine production through NFkappaB activation. Lab Invest 2001, 81:1371-1383
20. Morel JC, Park CC, Zhu K, Kumar P, Ruth JH, Koch AE: Signal transduction pathways involved in rheumatoid arthritis synovial fibroblast interleukin-18-induced vascular cell adhesion molecule-1 expression. J Biol Chem 2002, 277:34679-34691
21. Novick D, Kim SH, Fantuzzi G, Reznikov LL, Dinarello CA, Rubinstein M: Interleukin-18 binding protein: a novel modulator of the Th1 cytokine response. Immunity 1999, 10:127-136
22. Kim SH, Eisenstein M, Reznikov L, Fantuzzi G, Novick D, Rubinstein M, Dinarello CA: Structural requirements of six naturally occurring isoforms of the IL-18 binding protein to inhibit IL-18. Proc Natl Acad Sci USA 2000, 97:1190-1195
23. Gracie JA, Forsey RJ, Chan WL, Gilmour A, Leung BP, Greer MR, Kennedy K, Carter R, Wei XQ, Xu D, Field M, Foulis A, Liew FY, McInnes IB: A proinflammatory role for IL-18 in rheumatoid arthritis. J Clin Invest 1999, 104:1393-1401
24. Pizarro TT, Michie MH, Bentz M, Woraratanadharm J, Smith Jr MF, Foley E, Moskaluk CA, Bickston SJ, Cominelli F: IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn's disease: expression and localization in intestinal mucosal cells. J Immunol 1999, 162:6829-6835
25. Joosten LA, Radstake TR, Lubberts E, van den Bersselaar LA, van Riel PL, vanLent PL, Barrera P, van den Berg WB: Association of interleukin-18 expression with enhanced levels of both interleukin-1beta and tumor necrosis factor alpha in knee synovial tissue of patients with rheumatoid arthritis. Arthritis Rheum 2003, 48:339-347
26. Leung BP, Culshaw S, Gracie JA, Hunter D, Canetti CA, Campbell C, Cunha F, Liew FY, McInnes IB: A role for IL-18 in neutrophil activation. J Immunol 2001, 167:2879-2886
27. Park CC, Morel JC, Amin MA, Connors MA, Harlow LA, Koch AE: Evidence of IL-18 as a novel angiogenic mediator. J Immunol 2001, 167:1644-1653
28. Komai-Koma M, Gracie JA, Wei XQ, Xu D, Thomson N, McInnes IB, Liew FY: Chemoattraction of human T cells by IL-18. J Immunol 2003, 170:1084-1090
29. Joosten LA, van De Loo FA, Lubberts E, Helsen MM, Netea MG, van Der Meer JW, Dinarello CA, van Den Berg WB: An IFN-gamma-independent proinflammatory role of IL-18 in murine streptococcal cell wall arthritis. J Immunol 2000, 165:6553-6558
30. Takeda K, Tsutsui H, Yoshimoto T, Adachi O, Yoshida N, Kishimoto T, Okamura H, Nakanishi K, Akira S: Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 1998, 8:383-390
31. Wei XQ, Leung BP, Arthur HM, McInnes IB, Liew FY: Reduced incidence and severity of collagen-induced arthritis in mice lacking IL-18. J Immunol 2001, 166:517-521
32. Plater-Zyberk C, Joosten LA, Helsen MM, Sattonnet-Roche P, Siegfried C, Alouani S, van De Loo FA, Graber P, Aloni S, Cirillo R, Lubberts E, Dinarello CA, van Den Berg WB, Chvatchko Y: Therapeutic effect of neutralizing endogenous IL-18 activity in the collagen-induced model of arthritis. J Clin Invest 2001, 108:1825-1832
33. Smeets RL, van de Loo FA, Arntz OJ, Bennink MB, Joosten LA, van den Berg WB: Adenoviral delivery of IL-18 binding protein C ameliorates collagen-induced arthritis in mice. Gene Ther 2003, 10:1004-1011
34. Reznikov LL, Kim SH, Westcott JY, Frishman J, Fantuzzi G, Novick D, Rubinstein M, Dinarello CA: IL-18 binding protein increases spontaneous and IL-1-induced prostaglandin production via inhibition of IFN-gamma. Proc Natl Acad Sci USA 2000, 97:2174-2179
35. Pasparakis M, Alexopoulou L, Episkopou V, Kollias G: Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J Exp Med 1996, 184:1397-1411
36. Zheng H, Fletcher D, Kozak W, Jiang M, Hofmann KJ, Conn CA, Soszynski D, Grabiec C, Trumbauer ME, Shaw A: Resistance to fever induction and impaired acute-phase response in interleukin-1 beta-deficient mice. Immunity 1995, 3:9-19
37. Horai R, Asano M, Sudo K, Kanuka H, Suzuki M, Nishihara M, Takahashi M, Iwakura Y: Production of mice deficient in genes for interleukin (IL)-talpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1 beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J Exp Med 1998, 187:1463-1475
38. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B: A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 1998, 95:2509-2514
39. Lens JW, van den Berg WB, van de Putte LB: Quantitation of arthritis by 99mTc-uptake measurements in the mouse knee-joint: correlation with histological joint inflammation scores. Agents Actions 1984, 14:723-728
40. Joosten LA, Koenders MI, Smeets RL, Heuvelmans-Jacobs M, Helsen MM, Takeda K, Akira S, Lubberts E, van de Loo FA, van den Berg WB: Toll-like receptor 2 pathway drives streptococcal cell wall-induced joint inflammation: critical role of myeloid differentiation factor 88. J Immunol 2003, 171:6145-6153
41. De Jager W, Te Velthuis H, Prakken BJ, Kuls W, Rijkers GT: Simultaneous detection of 15 human cytokines in a single sample of stimulated peripheral blood mononuclear cells. Clin Diagn Lab Immunol 2003, 10:133-139
42. Joosten LA, Heuvelmans-Jacobs M, Lubberts E, van de Loo FA, Bakker AC, Helsen MM, Richards CD, van den Berg WB: Local interleukin-12 gene transfer promotes conversion of an acute arthritis to a chronic destructive arthritis. Arthritis Rheum 2002, 46:1379-1389
43. Joosten LA, Helsen MM, Saxne T, van De Loo FA, Heinegard D, van Den Berg WB: IL-1 alpha beta blockade prevents cartilage and bone destruction in murine type II collagen-induced arthritis, whereas TNF-alpha blockade only ameliorates joint inflammation. J Immunol 1999, 163:5049-5055
44. De Vries BJ, van den Berg WB, van de Putte LB: Salicylate-induced depletion of endogenous inorganic sulfate. Potential role in the suppression of sulfated glycosaminoglycan synthesis in murine articular cartilage. Arthritis Rheum 1985, 8:922-929
45. McInnes IB, Gracie JA, Leung BP, Wei XQ, Liew FY: Interleukin 18: a pleiotropic participant in chronic inflammation, Immunol Today 2000, 21:312-315
46. Canetti CA, Leung BP, Culshaw S, McInnes IB, Cunha FQ, Liew FY: IL-18 enhances collagen-induced arthritis by recruiting neutrophils via TNF-alpha and leukotriene B4. J Immunol 2003, 171:1009-1015
47. Kuiper S, Joosten LA, Bendele AM, Edwards III CK, Arntz OJ, Helsen MM, Van de Loo FA, Van den Berg WB: Different roles of tumour necrosis factor alpha and interleukin 1 in murine streptococcal cell wall arthritis. Cytokine 1998, 10:690-702
48. Netea MG, Vonk AG, van den Hoven M, Verschueren I, Joosten LA, van Krieken JH, van den Berg WB, Van der Meer JW, Kuliberg BJ: Differential role of IL-18 and IL-12 in the host defense against disseminated Candida albicans infection. Eur J Immunol 2003, 33:3409-3417
49. Saklatvala J, Pilsworth LM, Sarsfield SJ, Gavrilovic J, Heath JK: Pig catabolin is a form of interleukin 1. Cartilage and bone resorb, fibroblasts make prostaglandin and collagenase, and thymocyte proliferation is augmented in response to one protein. Biochem J 1984, 224:461-466
50. Arend WP, Dayer JM: Inhibition of the production and effects of interleukin-1 and tumor necrosis factor alpha in rheumatoid arthritis. Arthritis Rheum 1995, 38:151-160
51. Van de Loo FA, Arntz OJ, van Enckevort FH, van Lent PL, van den Berg WB: Reduced cartilage proteoglycan loss during zymosan-induced gonarthritis in NOS2-deficient mice and in anti-interleukin-1-treated wild-type mice with unabated joint inflammation. Arthritis Rheum 1998, 41:634-646
52. Goupille P, Giraubeau B, Conrozier T, Marliere J, Kiefer P, Chevalier X: Safety and efficacy of intra-articular injection of IL-1Ra (IL-1 receptor antagonist) in patients with painful osteoarthritis of the knee: a multicenter, double blind study. Arthritis Rheum 2003, 48:3696
53. Fernandez P, Guillen MI, Gomar F, Alcaraz MJ: Expression of heme oxygenase-1 and regulation by cytokines in human osteoarthritic chondrocytes. Biochem Pharmacol 2003, 66:2049-2052
54. Gong P, Cederbaum Al, Nieto N: Increased expression of cytochrome P450 2E1 induces heme oxygenase-1 through ERK MAPK pathway. J Biol Chem 2003, 278:29693-29700
55. Martin D, Rojo AI, Salinas M, Diaz R, Gallardo G, Alam J, Ruiz De Galarreta CM, Cuadrado A: Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3 kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical, carnosol. J Biol Chem 2004, 279:8919-8929
56. Puren AJ, Fantuzzi G, Gu Y, Su MS, Dinarello CA: Interleukin-18 (IFNgamma-inducing factor) induces IL-8 and IL-1beta via TNFalpha production from non-GDI4+ human blood mononuclear cells. J Clin Invest 1998, 101:711-721
57. Dai SM, Matsuno H, Nakamura H, Nishioka K, Yudoh K: Interleukin-18 enhances monocyte tumor necrosis factor alpha and interleukin-1beta production induced by direct contact with T lymphocytes: implications in rheumatoid arthritis. Arthritis Rheum 2004, 50:432-443