The role of IL-17 and family members in the pathogenesis of arthritis

Current Opinion in Investigational Drugs

Volumn 4, Issue 5, 2003, Pages 572-577

  Lubberts, Erik ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Autoimmune disease; Cartilage; Cytokine; IL 17; IL 17 family members; IL 17F; IL 23; Osteoclasts; RANKL

Indexed keywords

ANTIRHEUMATIC AGENT; CHEMOKINE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1 ANTIBODY; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; OSTEOCLAST DIFFERENTIATION FACTOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; ARTHRITIS; AUTOIMMUNE DISEASE; CARTILAGE; HUMAN; JOINT DESTRUCTION; MEMORY CELL; OSTEOCLAST; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ARTHRITIS, RHEUMATOID; HUMANS; INTERLEUKIN-17;

EID: 0038518197     PISSN: 14724472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (71)

1. Arend WP, Dayer J-M: Inhibition of the production and effects of interleukin-1 and tumor necrosis factor α in rheumatoid arthritis. Arthritis Rheum (1995) 38(2):151-160.
2. Thorbecke GJ, Shah R, Leu CH, Kuruvilla AP, Hardison AM, Palladino MA: Involvement of endogenous tumor necrosis factor α and transforming growth factor β during induction of collagen type II arthritis in mice. Proc Natl Acad Sci USA (1992) 89(16):7375-7379.
3. Van Den Berg WB, Joosten LAB, Helsen MMA, Van De Loo AJJ: Amelioration of established murine collagen-induced arthritis with anti-IL-1 treatment. Clin Exp Immunol (1994) 95(2):237-243.
4. Chabaud M, Durand JM, Buchs N, Fossiez F, Page G, Frappart L, Miossec P: Human interleukin-17: A T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthritis Rheum (1999) 42(5):963-970. First demonstration of IL-17 expression in the synovium of RA patients.
5. Yao Z, Painter SL, Fanslow WC, Ulrich D, Macduff BM, Spriggs MK, Armitage RJ: Human IL-17: A novel cytokine derived from T cells. J Immunol (1995) 155(12):5483-5486.
6. Yao Z, Fanslow WC, Seldin MF, Rousseau A-M, Painter SL, Comeau MR, Cohen JI, Spriggs MK: Herpes virus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity (1995) 3(6):811-821. First description of the IL-17 receptor as a new member of the cytokine family.
7. Fossiez F, Djossou O, Chomarat P, Flores-Romo L, Ait-Yahia S, Maat C, Pin J-J, Garrone P, Garcia E, Saeland S, Blanchard D et al: T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med (1996) 183(6):2593-2603. First study that demonstrated the cytokine-inducing capacity of IL-17 in different cell types.
8. Jovanovic DV, Di Battista JA, Martel-Pelletier J, Jolicoeur FC, He Y, Zhang M, Mineau F, Pelletier J-P: IL-17 stimulates the production and expression of proinflammatory cytokines, IL-1β and TNF-α, by human macrophages. J Immunol (1998) 160(7):3513-3521.
9. Lubberts E, Joosten LAB, Oppers B, Van Den Bersselaar L, Coenen-De Roo CJ, Kolls JK, Schwarzenberger P, Van De Loo FA, Van Den Berg WB: IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis. J Immunol (2001) 167(2):1004-1013. First demonstration that neutralization of endogenous IL-17 in vivo during early onset of collagen arthritis suppresses joint pathology. Furthermore, an IL-1-independent role of IL-17 in joint inflammation and destruction was described.
10. Lubberts E, Joosten LAB, Van De Loo FA, Schwarzenberger P, Kolls J, Van Den Berg WB: Overexpression of IL-17 in the knee joint of collagen type II immunized mice promotes collagen arthritis and aggravates joint destruction. Inflamm Res (2002) 51(2):102-104.
11. Chabaud M, Miossec P: The combination of tumor necrosis factor α blockade with interleukin-1 and interleukin-17 blockade is more effective for controlling synovial inflammation and bone resorption in an ex vivo model. Arthritis Rheum (2001) 44(6):1293-1303. This study reported that blockade of TNF in combination with IL-1 and IL-17 increased the inhibition of IL-16 and collagen degradation in vitro.
12. Aggarwal S, Gurney AL: IL-17: Prototype member of an emerging cytokine family. J Leukocyte Biol (2002) 71(1):1-8. Excellent review describing different subfamily members of the IL-17 family with focus on IL-17E and IL-17F.
13. Li H, Chen J, Huang A, Stinson J, Heldens S, Foster J, Dowd P, Gurney AL, Wood WI: Cloning and characterization of IL-17B and IL-17C, two new members of the IL-17 cytokine family. Proc Natl Acad Sci USA (2000) 97(2):773-778.
14. Shi Y, Ullrich SJ, Zhang J, Connolly K, Grzegorzewski KJ, Barber MC, Wang W, Wathen K, Hodge V, Fisher CL, Olsen H et al: A novel cytokine receptor-ligand pair. Identification, molecular characterization, and in vivo immunomodulatory activity. J Biol Chem (2000) 275(25):19167-19176.
15. Lee J, Ho WH, Maruoka M, Corpuz RT, Baldwin DT, Foster JS, Goddard AD, Yansura DG, Vandlen RL, Wood WI, Gurney AL: IL-17E, a novel proinflammatory ligand for the IL-17 receptor homolog IL-17Rh1. J Biol Chem (2001) 276(2):1660-1664.
16. Starnes T, Robertson MJ, Sledge G, Kelich S, Nakshatri H, Broxmeyer HE, Hromas R: Cutting edge: IL-17F, a novel cytokine selectively expressed in activated T cells and monocytes, regulates angiogenesis and endothelial cell cytokine production. J Immunol (2001) 167(8):4137-4140.
17. Hymowitz SG, Filvaroff EH, Yin JP, Lee J, Cai L, Risser P, Maruoka M, Mao W, Foster J, Kelley RF, Pan G et al: IL-17s adopt a cystine knot fold: Structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO J (2001) 20(19):5332-5341.
18. Rouvier E, Luciani M-F, Mattei M-G, Denizot F, Golstein P: CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene. J Immunol (1993) 150(12):5445-5456.
19. Schwandner R, Yamaguchi K, Cao Z: Requirement of tumor necrosis factor receptor-associated factor (TRAF)6 in interleukin-17 signal transduction. J Exp Med (2000) 191(7):1233-1240.
20. Awane M, Andres PG, Li DJ, Reinecker HC: NF-κ-B-inducing kinase is a common mediator of IL-17-, TNF-α, and IL-1 β-induced chemokine promoter activation in intestinal epithelial cells. J Immunol (1999) 162(9):5337-5344.
21. Shalom-Barak T, Quach J, Lotz M: Interleukin-17-induced gene expression in articular chondrocytes is associated with activation of mitogen-activated protein kinases and NF-κB. J Biol Chem (1998) 273(42):27467-27473.
22. Laan M, Lotvall J, Chung KF, Linden A: IL-17-induced cytokine release in human bronchial epithelial cells in vitro: Role of mitogen-activated protein (MAP) kinases. Br J Pharmacol (2001) 133(1):200-206.
23. Kehlen A, Thiele K, Riemann D, Langner J: Expression, modulation and signaling of IL-17 receptor in fibroblast-like synoviocytes of patients with rheumatoid arthritis. Clin Exp Immunol (2002) 127(3):539-546.
24. Subramaniam SV, Cooper RS, Adunyah SE: Evidence for the involvement of JAK/STAT pathway in the signaling mechanism of interleukin-17. Biochem Biophys Res Commun (1999) 262(1):14-19.
25. Haudenschild D, Moseley T, Rose L, Reddi AH: Soluble and transmembrane isoforms of novel interleukin-17 receptor-like protein by RNA splicing and expression in prostate cancer. J Biol Chem (2002) 277(6):4309-4316.
26. Moseley TA, Haudenschild DR, Rose L, Reddi AH: Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev (2003) 14(2):155-174. Excellent review describing the biological actions of IL-17 signaling in different tissues.
27. Katz Y, Nadiv O, Rapoport MJ, Loos M: IL-17 regulates gene expression and protein synthesis of the complement system, C3 and factor B, in skin fibroblasts. Clin Exp Immunol (2000) 120(1):22-29.
28. Schwarzenberger P, La Russa V, Miller A, Ye P, Huang W, Zieske A, Nelson S, Bagby GJ, Stoltz D, Mynatt RL, Spriggs M et al: IL-17 stimulates granulopoiesis in mice: Use of an alternate, novel gene therapy-derived method for in vivo evaluation of cytokines. J Immunol (1998) 161(11):6383-6389.
29. Laan M, Cui ZH, Hoshino H, Lotvall J, Sjostrand M, Gruenert DC, Skoogh BE, Linden A: Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol (1999) 162(4):2347-2352.
30. Numasaki M, Fukushi J, Ono M, Narula SK, Zavodny PJ, Kudo T, Robbins PD, Tahara H, Lotze MT: Interleukin-17 promotes angiogenesis and tumor growth. Blood (2003) 101(7):2620-2627.
31. Antonysamy MA, Fanslow WC, Fu F, Li W, Qian S, Troutt AB, Thomson AW: Evidence for a role of IL-17 in organ allograft rejection: IL-17 promotes the functional differentiation of dendritic cell progenitors. J Immunol (1999) 162(1):577-584.
32. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, Homma I, Sekikawa K, Asano M, Iwakura Y: Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity (2002) 17(3):375-387. This study used IL-17-deficient mice to demonstrate that IL-17 plays a role in various disease models.
33. Infante-Duarte C, Horton HF, Byrne MC, Kamradt T: Microbial lipopeptides induce the production of IL-17 in Th cells. J Immunol (2000) 165(11):6107-6115.
34. Ziolkowska M, Koc A, Luszczykiewicz G, Ksiezopolska-Pietrzak K, Klimczak E, Chwalinska-Sadowska H, Maslinski W: High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism. J Immunol (2000) 164(5):2832-2838.
35. Ferretti S, Bonneau O, Dubois GR, Jones CE, Trifilieff A: IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J Immunol (2003) 170(4):2106-2112.
36. Aggarwal S, Gilardi N, Xie MH, De Sauvage FJ, Gurney AL: Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem (2003) 278(3):1910-1914. This study reported the role of IL-23 in the induction of IL-17A and IL-17F in vitro.
37. Happel KI, Zheng M, Young E, Quinton LJ, Lockhart E, Ramsay AJ, Shellito JE, Schurr JR, Bagby GJ, Nelson S, Kolls JK: Cutting edge: Roles of toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J Immunol (2003) 170(9):4432-4436.
38. Thiele K, Riemann D, Navarrete Santos A, Langner J, Kehlen A: Cell-cell contact of human T cells with fibroblasts changes lymphocytic mRNA expression: Increased mRNA expression of interleukin-17 and interleukin-17 receptor. Eur Cytokine Netw (2000) 11(1):53-58.
39. Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, Menon S, Seymour B, Jackson C, Kung TT, Brieland JK et al: New IL-17 family members promote Th1 or Th2 responses in the lung: In vivo function of the novel cytokine IL-25. J Immunol (2002) 169(1):443-453.
40. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, Bamba T, Fujiyama Y: Increased expression of interleukin 17 in inflammatory bowel disease. Gut (2003) 52(1):65-70.
41. Katz Y, Nadiv O, Beer Y: Interleukin-17 enhances tumor necrosis factor α-induced synthesis of interleukin 1, 6, and 8 in skin and synovial fibroblasts: A possible role as a "fine-tuning cytokine" in inflammation processes. Arthritis Rheum (2001) 44(9):2176-2184.
42. Toda M, Leung DY, Molet S, Boguniewicz M, Taha R, Christodoulopoulos P, Fukuda T, Elias JA, Hamid QA: Polarized in vivo expression of IL-11 and IL-17 between acute and chronic skin lesions. J Allergy Clin Immunol (2003) 111(4):75-81.
43. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, Shellito JE et al: Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defence. J Exp Med (2001) 194(4):519-527.
44. Pan G, French D, Mao W, Maruoka M, Risser P, Lee J, Foster J, Aggarwal S, Nicholes K, Guillet S, Schow P et al: Forced expression of murine IL-17E induces growth retardation, jaundice, a Th2-biased response, and multiorgan inflammation in mice. J Immunol (2001) 167(11):6559-6567.
45. Kato T, Furumoto H, Ogura T, Onishi Y, Irahara M, Yamano S, Kamada M, Aono T: Expression of IL-17 mRNA in ovarian cancer. Biochem Biophys Res Commun (2001) 282(3):735-738.
46. Tartour E, Fossiez F, Joyeux L, Galinha A, Gey A, Claret E, Sastre-Garau X, Couturier J, Mosseri V, Vives V, Banchereau J et al: Interleukin-17, a T-cell-derived cytokine, promotes tumorigenicity of human cervical tumors in nude mice. Cancer Res (1999) 59(15):3698-3704.
47. Lock C, Hermans G, Pedotti R, Brendolan A, Schadt E, Garren H, Langer-Gould A, Strober S, Cannella B, Allard J, Klonowski P et al: Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med (2002) 8(5):500-508.
48. Kurasawa K, Hirose K, Sano H, Endo H, Shinkai H, Nawata Y, Takabayashi K, Iwamoto I: Increased interleukin-17 production in patients with systemic sclerosis. Arthritis Rheum (2000) 43(11):2455-2463.
49. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ et al: IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest (1999) 103(9):1345-1352. First demonstration in vitro that IL-17 may play a role in osteoclastogenesis in RA via RANKL induction in osteoblasts.
50. Aarvak T, Chabaud M, Miossec P, Natvig JB: IL-17 is produced by some proinflammatory Th1/Th0 cells but not by Th2 cells. J Immunol (1999) 162(3):1246-1251.
51. Chabaud M, Fossiez F, Taupin JL, Miossec P: Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines. J Immunol (1998) 161(1):409-414.
52. 1 Fc fusion protein. Arthritis Rheum (2002) 46(3):802-805.
53. Chabaud M, Lubberts E, Joosten L, Van Den Berg W, Miossec P: IL-17 derived from juxta-articular bone and synovium contributes to joint degradation in rheumatoid arthritis. Arthritis Res (2001) 3(3):168-177.
54. Lubberts E, Joosten LAB, Van De Loo FAJ, Van Den Gersselaar LA, Van Den Berg WB: Reduction of interleukin-17-induced inhibition of chondrocyte proteoglycan synthesis in intact murine articular cartilage by interleukin-4. Arthritis Rheum (2000) 43(6):1300-1306.
55. Dudler J, Renggli-Zulliger N, Busso N, Lotz M, So A: Effect of interleukin-17 on proteoglycan degradation in murine knee joints. Ann Rheum Dis (2000) 59(7):529-532.
56. Cai L, Yin JP, Starovasnik MA, Hogue DA, Hillan KJ, Mort JS, Filvaroff EH: Pathways by which interleukin 17 induces articular cartilage breakdown in vitro and in vivo. Cytokine (2001) 16(1):10-21.
57. Chabaud M, Garnero P, Dayer JM, Guerne PA, Fossiez F, Miossec P: Contribution of interleukin 17 to synovium matrix destruction in rheumatoid arthritis. Cytokine (2000) 12(7):1092-1099.
58. Benderdour M, Tardif G, Pelletier JP, Di Battista JA, Reboul P, Ranger P, Martel-Pelletier J: Interleukin 17 (IL-17) induces collagenase-3 production in human osteoarthritic chondrocytes via AP-1 dependent activation: Differential activation of AP-1 members by IL-17 and IL-1β. J Rheumatol (2002) 29(6):1262-1272.
59. Koshy PJ, Henderson N, Logan C, Life PF, Cawston TE, Rowan AD: Interleukin 17 induces cartilage collagen breakdown: Novel synergistic effects in combination with proinflammatory cytokines. Ann Rheum Dis (2002) 61(8):704-713.
60. Van Den Berg WB: Anti-cytokine therapy in chronic destructive arthritis. Arthritis Res (2001) 3(1):18-26.
61. Attur MG, Patel RN, Abramson SB, Amin AR: Interleukin-17 up-regulation of nitric oxide production in human osteoarthritis cartilage. Arthritis Rheum (1997) 40(6):1050-1053.
62. Martel-Pelletier J, Mineau F, Jovanovic D, Di Battista JA, Pelletier JP: Mitogen-activated protein kinase and nuclear factor κB together regulate interleukin-17-induced nitric oxide production in human osteoarthritic chondrocytes: Possible role of transactivating factor mitogen-activated protein kinase-activated protein kinase (MAPKAPK). Arthritis Rheum (1999) 42(11):2399-2409.
63. LeGrand A, Fermor B, Fink C, Pisetsky DS, Weinberg JB, Vail TP, Guilak F: Interleukin-1, tumor necrosis factor α, and interleukin-17 synergistically up-regulate nitric oxide and prostaglandin E2 production in explants of human osteoarthritic knee menisci. Arthritis Rheum (2001) 44(9):2078-2083.
64. Van Bezooijen RL, Van Der Wee-Pals L, Papaoulos SE, Lowik CW: Interleukin 17 synergises with tumour necrosis factor α to induce cartilage destruction in vitro. Ann Rheum Dis (2002) 61(10):870-876.
65. Van Bezooijen RL, Farih-Sips HC, Papapoulos SE, Lowik CW: Interleukin-17: A new bone acting cytokine in vitro. J Bone Miner Res (1999) 14(9):1513-1521.
66. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, Morony S, Oliveira-Dos-Santos AJ, Van G, Itie A, Khoo W et al: OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature (1999) 397(6717):315-323.
67. Dougall WC, Glaccum M, Charrier K, Rohrbach K, Brasel K, De Smedt T, Daro E, Smith J, Tometsko ME, Maliszewski CR, Armstrong A et al: RANK is essential for osteoclast and lymph node development. Genes Dev (1999) 13(18):2412-2424.
68. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G et al: Osteoprotegerin: A novel secreted protein involved in the regulation of bone density. Cell (1997) 89(2):309-319.
69. Lubberts E, Joosten LAB, Chabaud M, Van Den Bersselaar L, Oppers B, Coenen-De Roo CJJ, Richards CD, Miossec P, Van Den Berg WB: IL-4 gene therapy for collagen arthritis suppresses synovial IL-17 and osteoprotegerin ligand and prevents bone erosion. J Clin Invest (2000) 105(12):1697-1710. First demonstration that overexpression of the regulatory Th2 cytokine IL-4 prevents cartilage and bone erosion without influencing joint inflammation via downregulation of IL-17 and RANKL.
70. Lubberts E, Van Den Bersselaar L, Oppers-Walgreen B, Schwarzenberger P, Coenen-De Roo CJJ, Kolls JK, Joosten LAB, Van Den Berg WB: IL-17 promotes bone erosion in murine collagen-induced arthritis through loss of the receptor activator of NF-κB ligand/osteoprotegerin balance. J Immunol (2003) 170(5):2655-2662. First demonstration of the mechanism of IL-17 in bone erosion in vivo.
71. Miossec P: Interleukin-17 in rheumatoid arthritis: If T cells were to contribute to inflammation and destruction through synergy. Arthritis Rheum (2003) 48(3):594-601.