Selective tyrosine kinase inhibition by imatinib mesylate for the treatment of autoimmune arthritis

Journal of Clinical Investigation

Volumn 116, Issue 10, 2006, Pages 2633-2642

  Paniagua, Ricardo T ^a,b   Sharpe, Orr ^a,b   Ho, Peggy P ^a   Chan, Steven M ^a   Chang, Anna ^a,b   Higgins, John P ^a   Tomooka, Beren H ^a,b   Thomas, Fiona M ^a,b   Song, Jason J ^a,b   Goodman, Stuart B ^a   Lee, David M ^c   Genovese, Mark C ^a   Utz, Paul J ^a   Steinman, Lawrence ^a   Robinson, William H ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; IMATINIB; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG INHIBITION; IMMUNOGLOBULIN PRODUCTION; IN VITRO STUDY; MACROPHAGE; MALE; MAST CELL; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNOVIAL FLUID; SYNOVIOCYTE; T LYMPHOCYTE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; AUTOANTIGENS; B-LYMPHOCYTES; CELL PROLIFERATION; COLLAGEN TYPE II; HUMANS; MACROPHAGES, PERITONEAL; MALE; MAST CELLS; MICE; MICE, INBRED DBA; MICE, TRANSGENIC; PHOSPHORYLATION; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-KIT; PYRIMIDINES; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; STEM CELL FACTOR; SYNOVIAL FLUID; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33749446861     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI28546     Document Type: Article

References (65)

1. Firestein, G.S. 2003. Evolving concepts of rheumatoid arthritis. Nature. 423:356-361.
2. Druker, B.J., et al. 2001. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 344:1031-1037.
3. Demetri, G.D., et al. 2002. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N. Engl. J. Med. 347:472-480.
4. Buchdunger, E., Matter, A., and Druker, B.J. 2001. Bcr-Abl inhibition as a modality of CML therapeutics. Biochim. Biophys. Acta. 1551:M11-M18.
5. Dewar, A.L., et al. 2005. Macrophage colony-stimulating factor receptor c-fms is a novel target of imatinib. Blood. 105:3127-3132.
6. Fabian, M.A., et al. 2005. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 23:329-336.
7. Burmester, G.R., Stuhlmuller, B., Keyszer, G., and Kinne, R.W. 1997. Mononuclear phagocytes and rheumatoid synovitis. Mastermind or workhorse in arthritis? Arthritis Rheum. 40:5-18.
8. Kinne, R.W., Brauer, R., Stuhlmuller, B., Palombo-Kinne, E., and Burmester, G.R. 2000. Macrophages in rheumatoid arthritis. Arthritis Res. 2:189-202.
9. Kontoyiannis, D., Pasparakis, M., Pizarro, T.T., Cominelli, F., and Kollias, G. 1999. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity. 10:387-398.
10. Weinblatt, M.E., et al. 1999. A trial of etanercept, a recombinant tumor necrosis factor receptor:Fc fusion protein, in patients with rheumatoid arthritis receiving methotrexate. N. Engl. J. Med. 340:253-259.
11. Pixley, F.J., and Stanley, E.R. 2004. CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol. 14:628-638.
12. Wolf, A.M., et al. 2005. The kinase inhibitor imatinib mesylate inhibits TNF-alpha production in vitro and prevents TNF-dependent acute hepatic inflammation. Proc. Natl. Acad. Sci. U. S. A. 102:13622-13627.
13. Woolley, D.E. 2003. The mast cell in inflammatory arthritis. N. Engl. J. Med. 348:1709-1711.
14. Woolley, D.E., and Tetlow, L.C. 2000. Mast cell activation and its relation to proinflammatory cytokine production in the rheumatoid lesion. Arthritis Res. 2:65-74.
15. Benoist, C., and Mathis, D. 2002. Mast cells in autoimmune disease. Nature. 420:875-878.
16. Gordon, J.R., and Galli, S.J. 1990. Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature. 346:274-276.
17. Nigrovic, P.A., and Lee, D.M. 2005. Mast cells in inflammatory arthritis. Arthritis Res. Ther. 7:1-11.
18. Bromley, M., Fisher, W.D., and Woolley, D.E. 1984. Mast cells at sites of cartilage erosion in the rheumatoid joint. Ann. Rheum. Dis. 43:76-79.
19. Juurikivi, A., et al. 2005. Inhibition of c-kit tyrosine kinase by imatinib mesylate induces apoptosis in mast cells in rheumatoid synovia: a potential approach to the treatment of arthritis. Ann. Rheum. Dis. 64:1126-1131.
20. Lee, D.M., et al. 2002. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science. 297:1689-1692.
21. Van den Broek, M.F., van den Berg, W.B., and van de Putte, L.B. 1988. The role of mast cells in antigen induced arthritis in mice. J. Rheumatol. 15:544-551.
22. Cheon, H., et al. 2004. Platelet-derived growth factor-AA increases IL-1beta and IL-8 expression and activates NF-kappaB in rheumatoid fibroblast-like synoviocytes. Scand. J. Immunol. 60:455-462.
23. Watanabe, N., et al. 2002. Gene expression profile analysis of rheumatoid synovial fibroblast cultures revealing the overexpression of genes responsible for tumor-like growth of rheumatoid synovium. Biochem. Biophys. Res. Commun. 294:1121-1129.
24. Remmers, E.F., et al. 1991. Production of platelet derived growth factor B chain (PDGF-B/c-sis) mRNA and immunoreactive PDGF B-like polypeptide by rheumatoid synovium: coexpression with heparin binding acidic fibroblast growth factor-1. J. Rheumatol. 18:7-13.
25. Edwards, J.C., et al. 2004. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350:2572-2581.
26. Nielen, M.M., et al. 2004. Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum. 50:380-386.
27. Kuhn, K.A., et al. 2006. Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J. Clin. Invest. 116:961-973. doi:10.1172/JCI25422.
28. Miyachi, K., et al. 2003. Efficacy of imatinib mesylate (STI571) treatment for a patient with rheumatoid arthritis developing chronic myelogenous leukemia. Clin. Rheumatol. 22:329-332.
29. Eklund, K.K., and Joensuu, H. 2003. Treatment of rheumatoid arthritis with imatinib mesylate: clinical improvement in three refractory cases. Ann. Med. 35:362-367.
30. Wolff, N.C., Randle, D.E., Egorin, M.J., Minna, J.D., and Ilaria, R.L., Jr. 2004. Imatinib mesylate efficiently achieves therapeutic intratumor concentrations in vivo but has limited activity in a xenograft model of small cell lung cancer. Clin. Cancer Res. 10:3528-3534.
31. Young, J.D., Liu, C.C., Butler, G., Cohn, Z.A., and Galli, S.J. 1987. Identification, purification, and characterization of a mast cell-associated cytolytic factor related to tumor necrosis factor. Proc. Natl. Acad. Sci. U. S. A. 84:9175-9179.
32. Furuta, G.T., Ackerman, S.J., Lu, L., Williams, R.E., and Wershil, B.K. 1998. Stem cell factor influences mast cell mediator release in response to eosinophil-derived granule major basic protein. Blood. 92:1055-1061.
33. Tsai, M., et al. 1996. The C1.MC/C57.1 (C57) mouse mast cell line is of BALB/c origin and is tumorigenic in BALB/c mice [abstract]. FASEB J. 10:A1253.
34. Chan, S.M., Ermann, J., Su, L., Fathman, C.G., and Utz, P.J. 2004. Protein microarrays for multiplex analysis of signal transduction pathways. Nat. Med. 10:1390-1396.
35. Kakizoe, E., et al. 1999. Increases in mast cells and chymase in fibroproliferative paws of collagen-induced arthritic mice. Inflamm. Res. 48:318-324.
36. Campbell, I.K., Rich, M.J., Bischof, R.J., and Hamilton, J.A. 2000. The colony-stimulating factors and collagen-induced arthritis: exacerbation of disease by M-CSF and G-CSF and requirement for endogenous M-CSF. J. Leukoc. Biol. 68:144-150.
37. Robinson, W.H., et al. 2002. Autoantigen microarrays for multiplex characterization of autoantibody responses. Nat. Med. 8:295-301.
38. Hueber, W., et al. 2005. Antigen microarray profiling of autoantibodies in rheumatoid arthritis. Arthritis Rheum. 52:2645-2655.
39. Tusher, V.G., Tibshirani, R., and Chu, G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98:5116-5121.
40. Osman, G.E., et al. 1998. Expression of a type II collagen-specific TCR transgene accelerates the onset of arthritis in mice. Int. Immunol. 10:1613-1622.
41. Galli, S.J., Nakae, S., and Tsai, M. 2005. Mast cells in the development of adaptive immune responses. Nat. Immunol. 6:135-142.
42. Abdollahi, A., et al. 2005. Inhibition of platelet-derived growth factor signaling attenuates pulmonary fibrosis. J. Exp. Med. 201:925-935.
43. Robinson, W.H., et al. 2003. Protein microarrays guide tolerizing DNA vaccine treatment of autoimmune encephalomyelitis. Nat. Biotechnol. 21:1033-1039.
44. Ho, P.P., et al. 2005. A suppressive oligodeoxynucleotide enhances the efficacy of myelin cocktail/IL-4-tolerizing DNA vaccination and treats autoimmune disease. J. Immunol. 175:6226-6234.
45. Zipfel, P.A., et al. 2000. The c-Abl tyrosine kinase is regulated downstream of the B cell antigen receptor and interacts with CD19. J. Immunol. 165:6872-6879.
46. Genovese, M.C., et al. 2005. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N. Engl. J. Med. 353:1114-1123.
47. Dietz, A.B., et al. 2004. Imatinib mesylate inhibits T-cell proliferation in vitro and delayed-type hypersensitivity in vivo. Blood. 104:1094-1099.
48. Akiyama, T., et al. 1987. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 262:5592-5595.
49. Akiyama, T., and Ogawara, H. 1991. Use and specificity of genistein as inhibitor of protein-tyrosine kinases. Methods Enzymol. 201:362-370.
50. Satoh, K., et al. 2001. Involvement of ErbB-2 in rheumatoid synovial cell growth. Arthritis Rheum. 44:260-265.
51. Kehlen, A., Thiele, K., Riemann, D., and Langner, J. 2002. Expression, modulation and signalling of IL-17 receptor in fibroblast-like synoviocytes of patients with rheumatoid arthritis. Clin. Exp. Immunol. 127:539-546.
52. Verdrengh, M., Jonsson, I.M., Holmdahl, R., and Tarkowski, A. 2003. Genistein as an anti-inflammatory agent. Inflamm. Res. 52:341-346.
53. Druker, B.J. 2002. Inhibition of the Bcr-Abl tyrosine kinase as a therapeutic strategy for CML. Oncogene. 21:8541-8546.
54. Ando, W., et al. 2006. Imatinib mesylate inhibits osteoclastogenesis and joint destruction in rats with collagen-induced arthritis (CIA). J. Bone Miner. Metab. 24:274-282.
55. Miyagawa, S., Fujimoto, H., Ko, S., Hirota, S., and Kitamura, Y. 2002. Improvement of psoriasis during imatinib therapy in a patient with a metastatic gastrointestinal stromal tumour. Br. J. Dermatol. 147:406-407.
56. Sadanaga, A., et al. 2005. Amelioration of autoimmune nephritis by imatinib in MRL/lpr mice. Arthritis Rheum. 52:3987-3996.
57. Davidson, A., and Diamond, B. 2001. Autoimmune diseases. N. Engl. J. Med. 345:340-350.
58. Camps, M., et al. 2005. Blockade of PI3Kgamma suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat. Med. 11:936-943.
59. Nagar, B., et al. 2002. Crystal structures of the kinase domain of c-Abl in complex with the small molecule inhibitors PD173955 and imatinib (STI-571). Cancer Res. 62:4236-4243.
60. Arnett, F.C., et al. 1988. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 31:315-324.
61. Coligan, J.E., Kruisbeek, A.M., Margulies, D.H., Shevach, E.M., and Strober, W. 1994. Collageninduced arthritis. In Current protocols in immunology [book on CD-ROM]. John Wiley and Sons Inc. Hoboken, New Jersey, USA. 15.15.11-15.15.24.
62. Deng, G.M., Zheng, L., Chan, F.K., and Lenardo, M. 2005. Amelioration of inflammatory arthritis by targeting the pre-ligand assembly domain of tumor necrosis factor receptors. Nat. Med. 11:1066-1072.
63. Valencia, X., et al. 2004. Cadherin-11 provides specific cellular adhesion between fibroblast-like synoviocytes. J. Exp. Med. 200:1673-1679.
64. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868.
65. Storey, J.D. 2002. A direct approach to false discovery rates. J. R. Stat. Soc. 64:479-498.