Tyrosine kinase inhibitors ameliorate autoimmune encephalomyelitis in a mouse model of multiple sclerosis

Journal of Clinical Immunology

Volumn 31, Issue 6, 2011, Pages 1010-1020

  Crespo, Oliver ^a,b   Kang, Stacey C ^a   Daneman, Richard ^a   Lindstrom, Tamsin M ^a,b   Ho, Peggy P ^c   Sobel, Raymond A ^a   Steinman, Lawrence ^c   Robinson, William H ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c STANFORD UNIVERSITY   (United States)

Author keywords

Astrocyte proliferation; Experimental autoimmune encephalomyelitis; Imatinib; Macrophages; Sorafenib; TNF; Tyrosine kinase inhibitors

Indexed keywords

COLONY STIMULATING FACTOR 1; GW 2580; IMATINIB; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE INHIBITOR; SORAFENIB; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL INFILTRATION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE ACTIVATION; MOUSE; MULTIPLE SCLEROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TREATMENT DURATION;

ANIMALS; ANISOLES; ASTROCYTES; BENZENESULFONATES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DISEASE PROGRESSION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PYRIDINES; PYRIMIDINES; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84857048686     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-011-9579-6     Document Type: Article

References (66)

1. Steinman L. Multiple sclerosis: a two-stage disease. Nat Immunol. 2001;2:762-4.
2. Hedegaard CJ, Krakauer M, Bendtzen K, Lund H, Sellebjerg F, Nielsen CH. Thelper cell type 1 (Th1), Th2 and Th17 responses to myelin basic protein and disease activity in multiple sclerosis. Immunology. 2008;125:161-9.
3. Oh S, Cudrici C, Ito T, Rus H. B-cells and humoral immunity in multiple sclerosis. Implications for therapy. Immunol Res. 2007;40(3):224-34.
4. Storch MK, Piddlesden S, Haltia M, Iivanainen M, Morgan P, Lassmann H. Multiple sclerosis: in situ evidence for antibody-and complement-mediated demyelination. Ann Neurol. 1998;43:465-71. (Pubitemid 28231721)
5. Benveniste E. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J Mol Med. 1997;75 (3):165-73. (Pubitemid 27132679)
6. Huitinga I, Ruuls SR, Jung S, Van Rooijen N, Hartung HP, Dijkstra CD. Macrophages in T cell line-mediated, demyelinating, and chronic relapsing experimental autoimmune encephalomyeli-tis in Lewis rats. Clin Exp Immunol. 1995;100:344-51.
7. Sayed BA, Christy AL, Walker ME, Brown MA. Meningeal mast cells affect early T cell central nervous system infiltration and blood-brain barrier integrity through TNF: a role for neutrophil recruitment? J Immunol. 2010;184(12):6891-900.
8. Vercellino M, Merola A, Piacentino C, Votta B, Capello E, Mancardi GL, et al. Altered glutamate reuptake in relapsing-remitting and secondary progressive multiple sclerosis cortex: correlation with microglia infiltration, demyelination, and neuronal and synaptic damage. J Neuropathol Exp Neurol. 2007;66:732-9. (Pubitemid 47344252)
9. Werner P, Pitt D, Raine CS. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann Neurol. 2001;50:169-80. (Pubitemid 32738141)
10. Steinman L, Zamvil SS. Virtues and pitfalls of EAE for the development of therapies for multiple sclerosis. Trends Immunol. 2005;26:565-71. (Pubitemid 41726443)
11. Healy BC, Engler D, Gholipour T, Weiner H, Bakshi R, Chitnis T. Accounting for disease modifying therapy in models of clinical progression in multiple sclerosis. J Neurol Sci. 2011;303(1-2):109-13.
12. Liblau R. Glatiramer acetate for the treatment of multiple sclerosis: evidence for a dual anti-inflammatory and neuro-protective role. J Neurol Sci. 2009;287:S17-23.
13. Vos CM, van Haastert ES, de Groot CJ, van der Valk P, de Vries HE. Matrix metalloproteinase-12 is expressed in phagocytotic macrophages in active multiple sclerosis lesions. J Neuroimmu-nol. 2003;138:106-14. (Pubitemid 36566424)
14. Bruck W, Friede RL. L-fucosidase treatment blocks myelin phagocytosis by macrophages in vitro. J Neuroimmunol. 1990;27:217-27. (Pubitemid 20146291)
15. Zhang X, Haaf M, Todorich B, Grosstephan E, Schieremberg H, Surguladze N, et al. Cytokine toxicity to oligodendrocyte precursors is mediated by iron. Glia. 2005;52:199-208. (Pubitemid 43078509)
16. Kassiotis G, Kollias G. TNF and receptors in organ-specific autoimmune disease: multi-layered functioning mirrored in animal models. J Clin Invest. 2001;107:1507-8. (Pubitemid 32574636)
17. Kollias G, Douni E, Kassiotis G, Kontoyiannis D. On the role of tumor necrosis factor and receptors in models of multiorgan failure, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease. Immunol Rev. 1999;169:175-94. (Pubitemid 29338732)
18. Bhasin M, Wu M, Tsirka SE. Modulation of microglial/macro-phage activation by macrophage inhibitory factor (TKP) or tuftsin (TKPR) attenuates the disease course of experimental autoimmune encephalomyelitis. BMC Immunol. 2007;8:10.
19. Martiney JA, Rajan AJ, Charles PC, Cerami A, Ulrich PC, Macphail S, et al. Prevention and treatment of experimental autoimmune encephalomyelitis by CNI-1493, a macrophage-deactivating agent. J Immunol. 1998;160:5588-95. (Pubitemid 28267853)
20. Brosnan CF, Bornstein MB, Bloom BR. The effects of macro-phage depletion on the clinical and pathologic expression of experimental allergic encephalomyelitis. J Immunol. 1981;126:614-20. (Pubitemid 11136722)
21. Huitinga I, van Rooijen N, de Groot CJ, Uitdehaag BM, Dijkstra CD. Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J Exp Med. 1990;172:1025-33. (Pubitemid 20343201)
22. Tran EH, Hoekstra K, van Rooijen N, Dijkstra CD, Owens T. Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice. J Immunol. 1998;161:3767-75.
23. Cecchini MG, Dominguez MG, Mocci S, Wetterwald A, Felix R, Fleisch H, et al. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development. 1994;120 (6):1357-72. (Pubitemid 24175881)
24. MacDonald KP, Palmer JS, Cronau S, Seppanen E, Olver S, Raffelt NC, et al. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue-and tumor-associated macrophages but does not inhibit inflammation. Blood. 2010;116:3955-63.
25. Sasaki A, Yokoo H, Naito M, Kaizu C, Shultz LD, Nakazato Y. Effects of macrophage-colony-stimulating factor deficiency on the maturation of microglia and brain macrophages and on their expression of scavenger receptor. Neuropathology. 2000;20:134-42. (Pubitemid 30326181)
26. Wiktor-Jedrzejczak WW, Ahmed A, Szczylik C, Skelly RR. Hematological characterization of congenital osteopetrosis in op/op mouse. Possible mechanism for abnormal macrophage differentiation. J Exp Med. 1982;156:1516-27. (Pubitemid 13232211)
27. Pradervand S, Maurya M, Subramaniam S. Identification of signaling components required for the prediction of cytokine release in RAW 264.7 macrophages. Genome Biol. 2006;7(2): R11.
28. Campbell IK, Rich MJ, Bischof RJ, Hamilton JA. 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. 2000;68:144-50.
29. Gallo P, Pagni S, Giometto B, Piccinno MG, Bozza F, Argentiero V, et al. Macrophage-colony stimulating factor (M-CSF) in the cerebrospinal fluid. J Neuroimmunol. 1990;29:105-12. (Pubitemid 20283787)
30. D'Alfonso S, Nistico L, Zavattari P, Marrosu MG, Murru R, Lai M, et al. Linkage analysis of multiple sclerosis with candidate region markers in Sardinian and Continental Italian families. Eur J Hum Genet. 1999;7:377-85. (Pubitemid 29213745)
31. Campbell IL, Eddleston M, Kemper P, Oldstone MB, Hobbs MV. Activation of cerebral cytokine gene expression and its correlation with onset of reactive astrocyte and acute-phase response gene expression in scrapie. J Virol. 1994;68:2383-7. (Pubitemid 24091917)
32. Ransom B, Behar T, Nedergaard M. New roles for astrocytes (stars at last). Trends Neurosci. 2003;26:520-2. (Pubitemid 37176905)
33. Williams A, Piaton G, Lubetzki C. Astrocytes-friends or foes in multiple sclerosis? Glia. 2007;55:1300-12.
34. Bannerman P, Hahn A, Soulika A, Gallo V, Pleasure D. Astrogliosis in EAE spinal cord: derivation from radial glia, and relationships to oligodendroglia. Glia. 2006;55(1):57-64.
35. Luo J, Miller MW. Platelet-derived growth factor-mediated signal transduction underlying astrocyte proliferation: site of ethanol action. J Neurosci. 1999;19:10014-25. (Pubitemid 30226673)
36. Koehler NK, Roebbert M, Dehghani K, Ballmaier M, Claus P, von Hoersten S, et al. Up-regulation of platelet-derived growth factor by peripheral-blood leukocytes during experimental allergic encephalomyelitis. J Neurosci Res. 2008;86:392-402. (Pubitemid 351196744)
37. Paniagua RT. Selective tyrosine kinase inhibition by imatinib mesylate for the treatment of autoimmune arthritis. J Clin Invest. 2006;116(10):2633-42. (Pubitemid 44511627)
38. Louvet C, Szot G, Lang J, Lee M, Martinier N, Bollag G, et al. Tyrosine kinase inhibitors reverse type 1 diabetes in nonobese diabetic mice. Proc Natl Acad Sci USA. 2008;105(48):18895-900.
39. Stromnes IM, Goverman JM. Active induction of experimental allergic encephalomyelitis. Nat Protoc. 2006;1:1810-9. (Pubitemid 46773300)
40. Paniagua RT, Chang A, Mariano MM, Stein EA, Wang Q, Lindstrom TM, et al. c-Fms-mediated differentiation and priming of monocyte lineage cells play a central role in autoimmune arthritis. Arthritis Res Ther. 2010;12(1):R32.
41. Druker B, Talpaz M, Resta D, Peng B, Buchdunger E, Ford J, et al. Sawyers C (2001) Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001;344:1031-7. (Pubitemid 32267972)
42. Wolff NC, Randle DE, Egorin MJ, Minna JD, Ilaria Jr RL. 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. 2004;10:3528-34. (Pubitemid 38685463)
43. Huynh H, Lee JW, Chow PK, Ngo VC, Lew GB, Lam IW, et al. Sorafenib induces growth suppression in mouse models of gastrointestinal stromal tumor. Mol Cancer Ther. 2009;8:152-9.
44. Chung EJ, Yoo S, Lim HJ, Byeon SH, Lee JH, Koh HJ. Inhibition of choroidal neovascularisation in mice by systemic administration of the multikinase inhibitor, sorafenib. Br J Ophthalmol. 2009;93:958-63.
45. Strumberg D, Voliotis D, Moeller JG, Hilger RA, Richly H, Kredtke S, et al. Results of phase I pharmacokinetic and pharmacodynamic studies of the Raf kinase inhibitor BAY 43-9006 in patients with solid tumors. Int J Clin Pharmacol Ther. 2002;40:580-1.
46. Conway JG, McDonald B, Parham J, Keith B, Rusnak DW, Shaw E, et al. Inhibition of colony-stimulating-factor-1 signaling in vivo with the orally bioavailable cfms kinase inhibitor gw2580. Proc Natl Acad Sci USA. 2005;102(44):16078-83. (Pubitemid 41552870)
47. Katz-Levy Y, Neville KL, Girvin AM, Vanderlugt CL, Pope JG, Tan LJ, et al. Endogenous presentation of self myelin epitopes by CNS-resident APCs in Theiler's virus-infected mice. J Clin Invest. 1999;104:599-610.
48. Awada A, Hendlisz A, Gil T, Bartholomeus S, Mano M, De Valeriola D, et al. Phase I safety and pharmacokinetics of BAY 43-9006 administered for 21 days on/7 days off in patients with advanced, refractory solid tumours. Br J Cancer. 2005;92 (10):1855-61. (Pubitemid 40826133)
49. Wilhelm S, Chien DS. BAY 43-9006: preclinical data. Curr Pharm Des. 2002;8:2255-7. (Pubitemid 35189898)
50. Wilhelm SM, Adnane L, Newell P, Villanueva A, Llovet JM, Lynch M. Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Mol Cancer Ther. 2008;7(10):3129-40.
51. Tong FK, Chow S, HD. Pharmacodynamic monitoring of BAY 43-9006 (Sorafenib) in phase I clinical trials involving solid tumor and AML/MDS patients, using flow cytometry to monitor activation of the ERK pathway in peripheral blood cells. Cytometry B Clin Cytom. 2006;70(3):107-14.
52. Conway JG, McDonald B, Parham J, Keith B, Rusnak DW, Shaw E, et al. Inhibition of colony-stimulating-factor-1 signaling in vivo with the orally bioavailable cFMS kinase inhibitor GW2580. Proc Natl Acad Sci USA. 2005;102:16078-83. (Pubitemid 41552870)
53. Valcamonico F, Ferrari V, Amoroso V, Rangoni G, Simoncini E, Marpicati P, et al. Long-lasting successful cerebral response with sorafenib in advanced renal cell carcinoma. J Neurooncol. 2009;9 (1):47-50.
54. Czyzewski K, Styczynski J. Imatinib is a substrate for various multidrug resistance proteins. Neoplasma. 2009;56:202-7.
55. Tonra JR, Reiseter BS, Kolbeck R, Nagashima K, Robertson R, Keyt B, et al. Comparison of the timing of acute blood-brain barrier breakdown to rabbit immunoglobulin G in the cerebellum and spinal cord of mice with experimental autoimmune enceph-alomyelitis. J Comp Neurol. 2001;430:131-44.
56. Uemura Y, Ohno H, Ohzeki Y, Takanashi H, Murooka H, Kubo K, et al. The selective M-CSF receptor tyrosine kinase inhibitor Ki20227 suppresses experimental autoimmune encephalomyelitis. J Neuroimmunol. 2008;195:73-80.
57. Lock C, Oksenberg J, Steinman L. The role of TNFalpha and lymphotoxin in demyelinating disease. Ann Rheum Dis. 1999;58 Suppl 1:I121-8.
58. Sharief MK, Hentges R. Association between tumor necrosis factor-alpha and disease progression in patients with multiple sclerosis. N Engl J Med. 1991;325:467-72.
59. Sicotte NL, Voshkul RR. Onset of multiple sclerosis associated with anti-TNF therapy. Neurology. 2001;57(10):1885-8. (Pubitemid 33096700)
60. Robinson WH, Genovese MC, Moreland LW. Demyelinating and neurologic events reported in association with tumor necrosis factor alpha antagonism: by what mechanisms could tumor necrosis factor alpha antagonists improve rheumatoid arthritis but exacerbate multiple sclerosis? Arthritis Rheum. 2001;44:1977-83. (Pubitemid 33644038)
61. El Chartouni C, Benner C, Eigner M, Lichtinger M, Rehli M. Transcriptional effects of colony-stimulating factor-1 in mouse macrophages. Immunobiology. 2010;215(6):466-74.
62. Dalton D, Wittmer S. Nitric-oxide-dependent and independent mechanisms of protection from CNS inflammation during Th1-mediated autoimmunity: evidence from EAE in iNOS KO mice. J Neuroimmunol. 2005;160(1-2):110-21. (Pubitemid 40248600)
63. Rovida E, Baccarini M, Olivotto M, Dello Sbarba P. Opposite effects of different doses of MCSF on ERK phosphorylation and cell proliferation in macrophages. Oncogene. 2002;21:3670-6. (Pubitemid 34620530)
64. Karpiak VC, Bridges RJ, Eyer CL. Organotins disrupt components of glutamate homeostasis in rat astrocyte cultures. J Toxicol Environ Health A. 2001;63:273-87. (Pubitemid 32553736)
65. Conway J, Pink H, Bergquist M, Han B, Depee S, Tadepalli S, et al. Effects of the cFMS kinase inhibitor 5-(3-methoxy-4-((4-methoxybenzyl)oxy) benzyl)pyrimidine-2,4-diamine (GW2580) in normal and arthritic rats. J Pharmacol Exp Ther. 2008;326(1):41-50. (Pubitemid 351872132)
66. Valdo P, Stegagno C, Mazzucco S, Zuliani E, Zanusso G, Moretto G, et al. Enhanced expression of NGF receptors in multiple sclerosis lesions. J Neuropathol Exp Neurol. 2002;61:91-8. (Pubitemid 34027724)