IL-17/Th17 targeting: On the road to prevent chronic destructive arthritis?

Cytokine

Volumn 41, Issue 2, 2008, Pages 84-91

  Lubberts, Erik ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Autoimmunity; Cytokine; Inflammation; Interleukin 17; Th17 cell

Indexed keywords

CYTOKINE RECEPTOR ANTAGONIST; INTERLEUKIN 17;

ANTIGEN EXPRESSION; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CARTILAGE DEGENERATION; CELL LINEAGE; CHRONIC DISEASE; HUMAN; IMMUNOPATHOGENESIS; IMMUNOREGULATION; JOINT DESTRUCTION; LYMPHOCYTE SUBPOPULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL;

ANIMALS; ARTHRITIS, RHEUMATOID; HUMANS; INTERLEUKIN-17; RECEPTORS, INTERLEUKIN-17; T-LYMPHOCYTES, HELPER-INDUCER;

MURINAE; MUS;

EID: 38949197817     PISSN: 10434666     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cyto.2007.09.014     Document Type: Review

References (80)

1. Arend W.P., and Dayer J.-M. Inhibition of the production and effects of interleukin-1 and tumor necrosis factor alpha in rheumatoid arthritis. Arthritis Rheum 38 (1995) 151-160
2. Chabaud M., Durand J.M., Buchs N., Fossiez F., Page G., Frappart L., and Miossec P. Human interleukin-17: a T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthritis Rheum 42 (1999) 963-970
3. Raza K., Scheel-Toellner D., Lee C.Y., Pilling D., Curnow S.J., Falciani F., Trevino V., Kumar K., Assi L.K., Lord J.M., Gordon C., Buckley C.D., and Salmon M. Synovial fluid leukocyte apoptosis is inhibited in patients with very early rheumatoid arthritis. Arthritis Res Ther 8 (2006) R120
4. Yao Z., Painter S.L., Fanslow W.C., Ulrich D., Macduff B.M., Spriggs M.K., and Armitage R.J. Human IL-17: a novel cytokine derived from T cells. J Immunol 155 (1995) 5483-5486
5. Yao Z., Fanslow W.C., Seldin M.F., Rousseau A.-M., Painter S.L., Comeau M.R., Cohen J.I., and Spriggs M.K. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3 (1995) 811-821
6. 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., Gaillard C., Mahapatra B.D., Rouvier E., Golstein P., Banchereau J., and Lebecque S. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 183 (1996) 2593-2603
7. Jovanovic D.V., DiBattista J.A., Martel-Pelletier J., Jolicoeur F.C., He Y., Zhang M., Mineau F., and Pelletier J.-P. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-1beta and TNFalpha, by human macrophages. J Immunol 160 (1998) 3513-3521
8. Lubberts E., Joosten L.A.B., Oppers B., Van den Bersselaar L., Coenen-de Roo C.J., Kolls J.K., Schwarzenberger P., Van de Loo F.A., and Van den Berg W.B. IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis. J Immunol 167 (2001) 1004-1013
9. Lubberts E., Joosten L.A.B., Van de Loo F.A., Schwarzenberger P., Kolls J.K., and Van den Berg W.B. Overexpression of IL-17 in the knee joint of collagen type II immunized mice promotes collagen arthritis and aggravates joint destruction. Inflam Res 51 (2002) 102-104
10. Chabaud M., and Miossec P. The combination of tumor necrosis factor alpha 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 44 (2001) 1293-1303
11. Lubberts E., Schwarzenberger P., Huang W., Schurr J.R., Peschon J.J., van den Berg W.B., and Kolls J.K. Requirement of IL-17 receptor signaling in radiation-resistant cells in the joint for full progression of destructive synovitis. J Immunol 175 (2005) 3360-3368
12. Ziolkowska M., Koc A., Luszczykiewics G., Ksiezopolska-Pietrzak K., Klimczak E., Chwalinska-Sadowska H., and 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 164 (2000) 2832-2838
13. Kotake S., Udagawa N., Takahashi N., Matsuzaki K., Itoh K., Ishiyama S., Saito S., Inoue K., Kamatani N., Gillespie M.T., Martin T.J., and Suda T. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103 (1999) 1345-1352
14. Aarvak T., Chabaud M., Miossec P., and Natvig J.B. IL-17 is produced by some proinflammatory Th1/Th0 cells but not by Th2 cells. J Immunol 162 (1999) 1246-1251
15. Katz Y., Nadiv O., and Beer Y. Interleukin-17 enhances tumor necrosis factor alpha-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 44 (2001) 2176-2184
16. Chabaud M., Fossiez F., Taupin J.L., and 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 161 (1998) 409-414
17. Chabaud M., Garnero P., Dayer J.M., Guerne P.A., Fossiez F., and Miossec P. Contribution of interleukin 17 to synovium matrix destruction in rheumatoid arthritis. Cytokine 12 (2000) 1092-1099
18. Benderdour M., Tardif G., Pelletier J.P., Di Battista J.A., Reboul P., Ranger P., and Martel-Pelletier J. Interleukin 17 (IL-17) induces collagenase-3 production in human osteoclastic chondrocytes via AP-1 dependent activation: differential activation of AP-1 members by IL-17 and IL-1beta. J Rheum 29 (2002) 1262-1272
19. Koshy P.J., Henderson N., Logan C., Life P.F., Cawston T.E., and Rowan A.D. Interleukin 17 induces cartilage collagen breakdown: novel synergistic effects in combination with proinflammatory cytokines. Ann Rheum Dis 61 (2002) 704-713
20. Kirkham B.W., Lassere M.N., Edmonds J.P., Juhasz K.M., Bird P.A., Lee C.S., Shnier R., and Portek I.J. Synovial membrane cytokine expression is predictive of joint damage progression in rheumatoid arthritis: a two-year prospective study (the DAMAGE study cohort). Arthritis Rheum 54 (2006) 1122-1131
21. Nakae S., Saijo S., Horai R., Sudo K., Mori S., and Iwakura Y. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci USA 100 (2003) 5986-5990
22. Nakae S., Nambu A., Sudo K., and Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol 171 (2003) 6173-6177
23. Bush K.A., Farmer K.M., Walker J.S., and Kirkham B.W. Reduction of joint inflammation and bone erosion in rat adjuvant arthritis by treatment with interleukin-17 receptor IgG1 Fc fusion protein. Arthritis Rheum 46 (2002) 802-805
24. Lubberts E., Koenders M.I., Oppers-Walgreen B., Van den Bersselaar L., Coenen-de Roo C.J.J., Joosten L.A.B., and Van den Berg W.B. Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum 50 (2004) 650-659
25. Chabaud M., Lubberts E., Joosten L., Van den Berg W., and Miossec P. IL-17 derived from juxta-articular bone and synovium contributes to joint degradation in rheumatoid arthritis. Arthritis Res 3 (2001) 168-177
26. Lubberts E., Joosten L.A.B., Van de Loo F.A.J., Van den Bersselaar L., and Van den Berg W.B. Reduction of interleukin-17-induced inhibition of chondrocyte proteoglycan synthesis in intact murine articular cartilage by interleukin-4. Arthritis Rheum 43 (2000) 1300-1306
27. Dudler J., Renggli-Zulliger N., Busso N., Lotz M., and So A. Effect of interleukin-17 on proteoglycan degradation in murine knee joints. Ann Rheum Dis 59 (2000) 529-532
28. Cai L., Yin J.P., Starovasnik M.A., Hogue D.A., Hillan K.J., Mort J.S., and Filvaroff E.H. Pathways by which interleukin 17 induces articular cartilage breakdown in vitro and in vivo. Cytokine 16 (2001) 10-21
29. Van Bezooijen R.L., Van der Wee-Pals L., Papapoulos S.E., and Lowik C.W. Interleukin 17 synergises with tumour necrosis factor alpha to induce cartilage destruction in vitro. Ann Rheum Dis 61 (2002) 870-876
30. Bezooijen R., Farih-Sips H.C., Papapoulos S.E., and Lowik C.W. Interleukin-17: a new bone acting cytokine in vitro. J Bone Min Res 14 (1999) 1513-1521
31. Koenders M.I., Kolls J.K., Oppers-Walgreen B., van den Bersselaar L., Joosten L.A., Schurr J.R., Schwarzenberger P., van den Berg W.B., and Lubberts E. Interleukin-17 receptor deficiency results in impaired synovial expression of interleukin-1 and matrix metalloproteinases 3, 9, and 13 and prevents cartilage destruction during chronic reactivated streptococcal cell wall-induced arthritis. Arthritis Rheum 52 (2005) 3239-3247
32. Miossec P. Interleukin-17 in rheumatoid arthritis. If T cells were to contribute to inflammation and destruction through synergy. Arthritis Rheum 48 (2003) 594-601
33. Lubberts E., Koenders M.I., and van den Berg W.B. The role of T-cell interleukin-17 in conducting destructive arthritis: lessons from animal models. Arthritis Res Ther 7 (2005) 29-37
34. Attur M.G., Patel R.N., Abramson S.B., and Amin A.R. Interleukin-17 up-regulation of nitric oxide production in human osteoarthritis cartilage. Arthritis Rheum 40 (1997) 1050-1053
35. Martel-Pelletier J., Mineau F., Jovanovic D., Di Battista J.A., and Pelletier J.P. 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 42 (1999) 2399-2409
36. LeGrand A., Fermor B., Fink C., Pisetsky D.S., Weinberg J.B., Vail T.P., and Guilak F. Interleukin-1, tumor necrosis factor alpha, and interleukin-17 synergistically up-regulate nitric oxide and prostaglandin E2 production in explants of human osteoarthritic knee menisci. Arthritis Rheum 44 (2001) 2078-2083
37. Koenders M.I., Lubberts E., Oppers-Walgreen B., van den Bersselaar L., Helsen M.M., Kolls J.K., Joosten L.A., and van den Berg W.B. Induction of cartilage damage by overexpression of T cell interleukin-17A in experimental arthritis in mice deficient in interleukin-1. Arthritis Rheum 52 (2005) 975-983
38. Koenders M.I., Lubberts E., van de Loo F.A., Oppers-Walgreen B., van den Bersselaar L., Helsen M.M., Kolls J.K., Di Padova F.E., Joosten L.A., and van den Berg W.B. Interleukin-17 acts independently of TNF-alpha under arthritic conditions. J Immunol 176 (2006) 6262-6269
39. Benderdour M., Tardif G., Pelletier J.P., Di Battista J.A., Reboul P., Ranger P., and Martel-Pelletier J. Interleukin 17 (IL-17) induces collagenase-3 production in human osteoclastic chondrocytes via AP-1 dependent activation: differential activation of AP-1 members by IL-17 and IL-1beta. J Rheum 29 (2002) 1262-1272
40. Hymowitz S.G., Filvaroff E.H., Yin J.P., Lee J., Cai L., Risser P., Maruoka M., Mao W., Foster J., Kelley R.F., Pan G., Gurney A.L., de Vos A.M., and Starovasnik M.A. IL-17s adopt a cystine knot fold: structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO J 20 (2001) 5332-5341
41. Moseley T.A., Haudenschild D.R., Rose L., and Reddi A.H. Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev 14 (2003) 155-174
42. Lubberts E., Joosten L.A.B., Chabaud M., Van den Bersselaar L., Oppers B., Coenen-de Roo C.J.J., Richards C.D., Miossec P., and Van den Berg W.B. IL-4 gene therapy for collagen arthritis suppresses synovial IL-17 and osteoprotegerin ligand and prevents bone erosion. J Clin Invest 105 (2000) 1697-1710
43. Lubberts E., Joosten L.A., van Den Bersselaar L., Helsen M.M., Bakker A.C., van Meurs J.B., Graham F.L., Richards C.D., and van Den Berg W.B. Adenoviral vector-mediated overexpression of IL-4 in the knee joint of mice with collagen-induced arthritis prevents cartilage destruction. J Immunol 163 (1999) 4546-4556
44. Lubberts E., Van den Bersselaar L., Oppers-Walgreen B., Schwarzenberger P., Coenen-de Roo C.J.J., Kolls J.K., Joosten L.A.B., and Van den Berg W.B. IL-17 promotes bone erosion in murine collagen-induced arthritis through loss of the RANKL/OPG balance. J Immunol 170 (2003) 2655-2662
45. Toy D., Kugler D., Wolfson M., Vanden Bos T., Gurgel J., Derry J., Tocker J., and Peschon J. Cutting edge: interleukin 17 signals through a heteromeric receptor complex. J Immunol 177 (2006) 36-39
46. Rong Z., Cheng L., Ren Y., Li Z., Li Y., Li X., Li H., Fu X.Y., and Chang Z. Interleukin-17F signaling requires ubiquitination of interleukin-17 receptor via TRAF6. Cell Signal 19 (2007) 1514-1520
47. Honorati M.C., Meliconi R., Pulsatelli L., Cane S., Frizziero L., and Facchini A. High in vivo expression of interleukin-17 receptor in synovial endothelial cells and chondrocytes from arthritis patients. Rheumatology (Oxford) 40 (2001) 522-527
48. Kehlen A., Thiele K., Riemann D., and Langner J. Expression, modulation and signalling of IL-17 receptor in fibroblast-like synoviocytes of patients with rheumatoid arthritis. Clin Exp Immunol 127 (2002) 539-546
49. Honorati M.C., Bovara M., Cattini L., Piacentini A., and Facchini A. Contribution of interleukin 17 to human cartilage degradation and synovial inflammation in osteoarthritis. Osteoarthritis Cartilage 10 (2002) 799-807
50. Hwang S.Y., and Kim H.Y. Expression of IL-17 homologs and their receptors in the synovial cells of rheumatoid arthritis patients. Mol Cells 19 (2005) 180-184
51. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedwick J.D., McClanahan T., Kastelein R.A., and Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201 (2005) 233-240
52. Harrington L.E., et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6 (2005) 1123-1132
53. Park H., et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing IL-17. Nat Immunol 6 (2005) 1133-1141
54. Cua D.J., et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421 (2003) 744-748
55. Murphy C.A., et al. Divergent pro- and anti-inflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198 (2003) 1951-1957
56. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., and Stockinger B. TGF-β in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 (2006) 179-189
57. Bettelli E., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006) 235-238
58. Mangan P.R., et al. Transforming growth factor-β induces development of TH17 lineage. Nature 441 (2006) 231-234
59. Liang S.C., Tan X.-Y., Luxenberg D.P., Karim R., Dunussi-Joannopoulos K., Collins M., and Fouser L.A. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 203 (2006) 2271-2279
60. Mus A.M.C., Ferry Cornelissen F., Asmawidjaja P., Hendriks R., and Lubberts E. IL-23 induces Th17 polarization in splenic T cells from type II collagen-immunized DBA-1 mice and is critical for Th17 specific IL-22 expression. Ann Rheum Dis (2007) OP0086
61. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., Oukka M., and Kuchroo V.K. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448 (2007) 484-487
62. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., Levy D.E., Leonard W.J., and Littman D.R. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 8 (2007) 967-974
63. Infante-Duarte C., Horton H.F., Byrne M.C., and Kamradt T. Microbial lipopeptides induce the production of IL-17 in Th cells. J Immunol 165 (2000) 6107-6115
64. Aggarwal S., Ghilardi N., Xie M.H., de Sauvage F.J., and Guerne A.L. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 278 (2003) 1910-1914
65. Zheng Y., Danilenko D.M., Valdez P., Kasman I., Eastham-Anderson J., Wu J., and Ouyang W. Interleukin-22, a TH17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445 (2007) 648-651
66. Wilson N.J., Boniface K., Chan J.R., McKenzie B.S., Blumenschein W.M., Mattson J.D., Basham B., Smith K., Chen T., Morel F., Lecron J.C., Kastelein R.A., Cua D.J., McClanahan T.K., Bowman E.P., and de Waal Malefyt R. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 8 (2007) 950-957
67. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., and Littman D.R. The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17+ T helper cells. Science 126 (2006) 1121-1133
68. Owyang A.M., et al. Interleukin-25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J Exp Med 203 (2006) 843-849
69. Batten M., Li J., Yi S., Kljavin N.M., Danilenko D.M., Lucas S., Lee J., de Sauvage F.J., and Ghilardi N. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat Immunol 7 (2006) 929-936
70. Van Hamburg J.P., Mus A.M.C., De Bruyn M., Asmawidjaja P., De Vogel L., Hendriks R., and Lubberts E. T cell specific overexpression of GATA-3 prevents Th17 polarization and protects against severe joint inflammation during experimental arthritis. Ann Rheum Dis (2007) OP0075
71. Sato W., Aranami T., and Yamamura T. Cutting edge: Human Th17 cells are identified as bearing CCR2+CCR5- phenotype. J Immunol 178 (2007) 7525-7529
72. Acosta-Rodriguez E.V., Napolitani G., Lanzavecchia A., and Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 8 (2007) 942-949
73. Annunziato F., Cosmi L., Santarlasci V., Maggi L., Liotta F., Mazzinghi B., Parente E., Fili L., Ferri S., Frosali F., Giudici F., Romagnani P., Parronchi P., Tonelli F., Maggi E., and Romagnani S. Phenotypic and functional features of human Th17 cells. J Exp Med 204 (2007) 1849-1861
74. Aarvak T., Chabaud M., Kallberg E., Miossec P., and Natvig J.B. Change in the Th1/Th2 phenotype of memory T-cell clones from rheumatoid arthritis synovium. Scand J Immunol 50 (1999) 1-9
75. Hirota K., Hashimoto M., Yoshitomi H., Tanaka S., Nomura T., Yamaguchi T., Iwakura Y., Sakaguchi N., and Sakaguchi S. T cell self-reactivity forms a cytokine milieu for spontaneous development of IL-17+ Th cells that cause autoimmune arthritis. J Exp Med 204 (2007) 41-47
76. Sato K., Suematsu A., Okamoto K., Yamaguchi A., Morishita Y., Kadono Y., Tanaka S., Kodama T., Akira S., Iwakura Y., Cua D.J., and Takayanagi H. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 203 (2006) 2673-2682
77. Langrish C.L., McKenzie B.S., Wilson N.J., de Waal Malefyt R., Kastelein R.A., and Cua D.J. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev 202 (2004) 96-105
78. Kolls J.K., and Linden A. Interleukin-17 family members and inflammation. Immunity 21 (2004) 467-476
79. Lubberts E. The role of IL-17 and family members in the pathogenesis of arthritis. Curr Opin Investig Drugs 4 (2003) 572-577
80. Lard L.R., Visser H., Speyer I., vander Horst-Bruinsma I.E., Zwinderman A.H., Breedveld F.C., and Hazes J.M. Early versus delayed treatment in patients with recent-onset rheumatoid arthritis: comparison of two cohorts who received different treatment strategies. Am J Med 111 (2001) 446-451