The effects of dasatinib on IgE receptor dependent activation and histamine release in human basophils

Blood

Volumn 111, Issue 6, 2008, Pages 3097-3107

  Kneidinger, Michael ^a   Schmidt, Uwe ^b   Rix, Uwe ^c   Gleixner, Karoline V ^a   Vales, Anja ^a   Baumgartner, Christian ^a   Lupinek, Christian ^a   Weghofer, Margit ^a   Bennett, Keiryn L ^c   Herrmann, Harald ^a   Schebesta, Alexandra ^b   Thomas, Wayne R ^d   Vrtata, Susanne ^a   Valenta, Rudolf ^a   Lee, Francis Y ^e   Ellmeier, Wilfried ^b   Superti Furga, Giulio ^c   Valent, Peter ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; ANTILEUKEMIC AGENT; BRUTON TYROSINE KINASE; CALCIUM IONOPHORE; CD164 ANTIGEN; CD203C ANTIGEN; CD63 ANTIGEN; COMPLEMENT COMPONENT C5A; CYTOKINE; DASATINIB; HISTAMINE; IMMUNOGLOBULIN E RECEPTOR; INTERLEUKIN 3; INTERLEUKIN 4; MEMBRANE ANTIGEN; MICROSOMAL AMINOPEPTIDASE; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; AGAMMAGLOBULINAEMIA TYROSINE KINASE; PYRIMIDINE DERIVATIVE; THIAZOLE DERIVATIVE;

ADOLESCENT; ADULT; ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BASOPHIL; CELL CULTURE; CLINICAL ARTICLE; DOSE RESPONSE; EFFECTOR CELL; FEMALE; HISTAMINE RELEASE; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; MALE; MOUSE; MYELOID LEUKEMIA; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; DRUG EFFECT; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PROTEIN BINDING; SECRETION;

ADOLESCENT; ADULT; ALLERGENS; ANIMALS; BASOPHILS; CELLS, CULTURED; FEMALE; HISTAMINE RELEASE; HUMANS; INTERLEUKIN-4; MALE; MICE; MIDDLE AGED; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; PYRIMIDINES; RECEPTORS, IGE; THIAZOLES; UP-REGULATION;

EID: 42449139172     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-08-104372     Document Type: Article

References (60)

1. IshizakaT, De Bernardo R. Tomioka H, Lichtenstein LM, Ishizaka K. Identification of basophil granulocytes as a site of allergic histamine release. J Immunol. 1972;108:1000-1008.
2. Valent P, Bettelheim P. The human basophil. Grit Rev Oncol Hematol. 1990;10:327-352.
3. Falcone FH, Haas H, Gibbs BF. The human basophil: a new appreciation of its role in immune responses. Blood. 2000:96:4028-4038.
4. Schroeder JT, MacGlashan DW Jr, Lichtenstein LM. Human basophils: mediator release and cytokine production. Adv Immunol. 2001;77:93-122.
5. Schroeder JT, MacGlashan DW Jr, Kagey-Sobotka A, White JM, Lichtenstein LM. Cytokine generation by human basophils. J Allergy Clin Immunol. 1994;94:1189-1195.
6. MacGlashan DW. Signal transduction and cytokine production by human basophils. Chem Immunol. 1995;61:88-113.
7. Turner H, Kinet JP. Signaling through the highaffinity IgE receptor Fc-epsilon Rl. Nature. 1999; 402:24-30.
8. Oliver JM, Kepley CL, Ortega E, Wilson BS. Immunologically mediated signaling in basophils and mast cells: finding therapeutic targets for allergic diseases in the human Fc-epsilon Rl signaling pathway. Immunopharmacology. 2000:48: 269-281.
9. Nadler MJ, Matthews SA, Turner H, Kinet JP. Signal transduction by the high-affinity immunoglobulin E receptor Fc-epsilon Rl: coupling form to function. Adv Immunol. 2000;76:325-355.
10. Benhamou M, Feuillard J, Lortholary O, et al. Protein tyrosine kinases in activation signal of human basophils through the immunoglobulin E receptor type I. J Leukoc Biol. 1996;59:461-470.
11. Eiseman E. Bolen JB. Engagement of the highaffinity IgE receptor activates src protein-related tyrosine kinases. Nature. 1992;355:78-80.
12. Nishizumi H, Yamamoto T. Impaired tyrosine phosphorylation and Ca2+ mobilization, but not degranulation, in lyn-deficient bone marrow-derived mast cells. J Immunol. 1997;158:2350-2355.
13. Jouvin MH, Adamczewski M, Numerof R, Letourneur O, Valle A, Kinet J P. Differential control of the tyrosine kinases Lyn and Syk by the two signaling chains of the high affinity immunoglobulin E receptor. J Biol Chem. 1994;269:5918-5925.
14. Zhang J, Berenstein EH, Evans RL, Siraganian RP. Transfection of Syk protein tyrosine kinase reconstitutes high affinity IgE receptor-mediated degranulation in a Syk-negative variant of rat basophilic leukemia RBL-2H3 cells. J Exp Med. 1996;184:71-79.
15. Costello PS, Turner M, Walters AE, et al. Critical role for the tyrosine kinase Syk in signalling through the high affinity IgE receptor of mast cells. Oncogene. 1996;13:2595-2605.
16. Kawakami Y, Yao L, MiuraT, Tsukada S, Witte ON, Kawakami T Tyrosine phosphorylation and activation of Bruton tyrosine kinase upon Fc epsilon Rl cross-linking. Mol Cell Biol. 1994:14:5108-5113.
17. Hata D, Kawakami Y, Inagaki N, et al. Involvement of Bruton's tyrosine kinase in FcepsilonRI-dependent mast cell degranulation and cytokine production. J Exp Med. 1998;187:1235-1247.
18. Kepley CL, Wilson BS, Oliver JM. Identification of the Fc epsilonRI-activated tyrosine kinases Lyn, Syk, and Zap-70 in human basophils. J Allergy Clin Immunol. 1998;102:304-315.
19. Miura K, MacGlashan DW. Phosphatidylinositol-3 kinase regulates p21 ras activation during IgE-mediated stimulation of human basophils. Blood. 2000:96:2199-2205.
20. Gibbs BF, Plath KE. Wolff HH. Grabbe J. Regulation of mediator secretion in human basophils by p38 mitogen-activated protein kinase: phosphorylation is sensitive to the effects of phosphatidylinositol 3-kinase inhibitors and calcium mobilization. J Leukoc Biol. 2002;72:391-400.
21. Kepley CL, Youssef L, Andrews RP, Wilson BS, Oliver JM. Syk deficiency in nonreleaser basophils. J Allergy Clin Immunol. 1999;104:279-284.
22. Kepley CL, Youssef L, Andrews RP, Wilson BS, Oliver JM. Multiple defects in Fc epsilon Rl signaling in Syk-deficient nonreleaser basophils and IL-3-induced recovery of Syk expression and secretion. J Immunol. 2000;165:5913-5920.
23. Lavens-Phillips SE, MacGlashan DW Jr. The tyrosine kinases p53/561yn and p72syk are differentially expressed at the protein level but not at the messenger RNA level in nonreleasing human basophils. Am J Respir Cell Mol Biol. 2000;23: 566-571.
24. Hernandez-Hansen V, Smith AJ, Surviladze Z, et al. Dysregulated FcepsilonRI signaling and altered Fyn and SHIP activities in Lyn-deficient mast cells. J Immunol. 2004;173:100-112.
25. Gomez G, Gonzalez-Espinosa C. Odom S, et al. Impaired FcepsilonRI-dependent gene expression and defective eicosanoid and cytokine production as a consequence of Fyn deficiency in mast cells. J Immunol. 2005;175:7602-7610.
26. MacGlashan D Jr, Miura K, Lavens-Phillips S. Pharmacology of IgE-mediated desensitization of human basophils: effects of protein kinase C and src-family kinase inhibitors. Biochem Pharmacol. 2000;60:1717-1727.
27. Oliver JM, Kepley CL, Ortega E, Wilson BS. Immunologically mediated signaling in basophils and mast cells: finding therapeutic targets for allergic diseases in the human Fc-epsilonR1 signaling pathway. Immunopharmacology. 2000;48: 269-281.
28. Luskova P, Draber P. Modulation of the Fcepsilon receptor I signaling by tyrosine kinase inhibitors: search for therapeutic targets of inflammatory and allergy diseases. Curr Pharm Des. 2004;10: 1727-1737.
29. Shah NP, Tran C, Lee FY, Chen P, Norris D, Sawyers CL. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science. 2004;305: 399-401.
30. Lombardo LJ, Lee FY, Chen P, et al. Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxyethyl)-piperazin-1-yl)-2-methylpyrimidin-4-ylamino) thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem. 2004;47:6658-6661.
31. Doggrell SA. BMS-354825: a novel drug with potential for the treatment of imatinib-resistant chronic myeloid leukaemia. Expert Opin Investig Drugs. 2005;14:89-91.
32. Gambacorti-Passerini C. Gasser M, Ahmed S, Assouline S, Scapozza L. Abl inhibitor BMS-354825 binding mode in Abelson kinase revealed by molecular docking studies. Leukemia. 2005;19:1267-1269.
33. Talpaz M, Shah NP, Kantarjian H, et al. Dasatinib in imatinib-resistant Philadelphia chromosomepositive leukemias. N Engl J Med. 2006;354: 2531-2541.
34. Schittenhelm MM, Shiraga S, Schroeder A, et al. Dasatinib (BMS-354825), a dual SRC/ABL kinase inhibitor, inhibits the kinase activity of wild-type, juxtamembrane, and activation loop mutant KIT isoforms associated with human malignancies. Cancer Res. 2006;66:473-481.
35. Shah NP, Lee FY, Luo R, Jiang Y, Donker M, Akin C. Dasatinib (BMS-354825) inhibits KITD816V, an imatinib-resistant activating mutation that triggers neoplastic growth in most patients with systemic mastocytosis. Blood. 2006;108:286-291.
36. Gleixner KV, Mayerhofer M, Sonneck K, et al. Synergistic growth-inhibitory effects of two tyrosine kinase inhibitors, dasatinib and PKC412, on neoplastic mast cells expressing the D816V-mutated oncogenic variant of KIT. Hematologica. 2007;92:1451-1459.
37. Hales BJ, Shen HD, Thomas WR. Cytokine responses to Der p 1 and Der p 7: house dust mite allergens with different IgE-binding activities. Clin Exp Allergy. 2000;30:934-943.
38. Valent P, Besemer J, Muhm M, Majdic O, Lechner K, Bettelheim P. Interleukin 3 activates human blood basophils via high-affinity binding sites. Proc Natl Acad Sci U S A. 1989;86:5542-5546.
39. Rottem M, Goff JP, Albert JP, Metcalfe DD. The effects of stem cell factor on the ultrastructure of Fc epsilon RI+ cells developing in IL-3-dependent murine bone marrow-derived cell cultures. J Immunol. 1993;151:4950-4963.
40. Yoshimoto T, Tsutsui H, Tominaga K, et al. IL-18, although antiallergic when administered with IL-12, stimulates IL-4 and histamine release by basophils. Proc Natl Acad Sci U S A. 1999;96: 13962-13966.
41. Khan WN, Alt FW, Gerstein RM, et al. Defective B cell development and function in Btk-deficient mice. Immunity. 1995;3:283-299.
42. Gleixner KV, Mayerhofer M, Aichberger KJ, et al. PKC412 inhibits in vitro growth of neoplastic human mast cells expressing the D816V-mutated variant of KIT: comparison with AMN107, imatinib, and cladribine (2CdA) and evaluation of cooperative drug effects. Blood. 2006;107:752-759.
43. Kishi K. A new leukemia cell line with Philadelphia chromosome characterized as basophil precursors. Leuk Res. 1985;9:381-390.
44. Rix U, Hantschel O, Dürnberger G, et al. Chemical proteomic profiling of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal different interaction networks and novel kinase and nonkinase targets. Blood. 2007;110:4055-4063.
45. Hauswirth AW, Natter S, Ghannadan M, et al. Recombinant allergens promote expression of CD203c on basophils in sensitized individuals. J Allergy Clin Immunol. 2002;110:102-109.
46. Hennersdorf F, Florian S, Jakob A, et al. Identification of CD13, CD107a, and CD164 as novel basophil-activation markers and dissection of two response patterns in time kinetics of IgE-dependent upregulation. Cell Res. 2005;15: 325-335.
47. Buhring HJ, Streble A, Valent P. The basophilspecific ectoenzyme E-NPP3 (CD203c) as a marker for cell activation and allergy diagnosis. Int Arch Allergy Immunol. 2004;133:317-329.
48. Guilhot F, Apperley J, Kim DW, et al. Dasatinib induces significant hematologic and cytogenetic responses in patients with imatinib-resistant or-intolerant chronic myeloid leukemia in accelerated phase. Blood. 2007;109:4143-4150.
49. Quintas-Cardama A, Kantarjian H, Jones D, et al. Dasatinib (BMS-354825) is active in Philadelphia chromosome-positive chronic myelogenous leukemia after imatinib and nilotinib (AMN107) therapy failure. Blood. 2007:109:497-499.
50. Cortes J, Rousselot P, Kim DW, et al. Dasatinib induces complete hematologic and cytogenetic responses in patients with imatinib-resistant or-intolerant chronic myeloid leukemia in blast crisis. Blood. 2007;109:3207-3213.
51. SchadeAE, Schieven GL, Townsend R, et al. Dasatinib, a small molecule protein tyrosine kinase inhibitor, inhibits T cell activation and proliferation. Blood. 2008;111:1366-1377.
52. Schittenhelm MM. Shiraga S, Schroeder A, et al. Dasatinib (BMS-354825), a dual SRC/ABL kinase inhibitor, inhibits the kinase activity of wild-type, juxtamembrane, and activation loop mutant KIT isoforms associated with human malignancies. Cancer Res. 2006;66:473-481.
53. Fureder W, Agis H, Willheim M, et al. Differential expression of complement receptors on human basophils and mast cells: evidence for mast cell heterogeneity and CD88/C5aR expression on skin mast cells. J Immunol. 1995;155:3152-3160.
54. Arock M, Merle-Beral H, Dugas B, et al. IL-4 release by human leukemic and activated normal basophils. J Immunol. 1993;151:1441-1447.
55. Brunner T, Heusser CH, Dahinden CA. Human peripheral blood basophils primed by interleukin 3 (IL-3) produce IL-4 in response to immunoglobulin E receptor stimulation. J Exp Med. 1993;177: 605-611.
56. Hantschel O, Rix U, Schmidt U, et al. The Btk tyrosine kinase is a major target of the Bcr-Abl inhibitor dasatinib. Proc Natl Acad Sci U S A. 2007; 104:13283-13288.
57. Luo FR, Yang Z, Camuso A, et al. Dasatinib (BMS-354825) pharmacokinetics and pharmacodynamic biomarkers in animal models predict optimal clinical exposure. Clin Cancer Res. 2006; 12:7180-7186.
58. Atallah E, Kantarjian H, Cortes J. Emerging safety issues with imatinib and other Abl tyrosine kinase inhibitors. Glin Lymphoma Myeloma. 2007;3:S105-S112.
59. Odom S, Gomez G, Kovarova M, et al. Negative regulation of immunoglobulin E-dependent allergic responses by Lyn kinase. J Exp Med. 2004; 199:1491-1502.
60. Xiao W, Nishimoto H, Hong H, et al. Positive and negative regulation of mast cell activation by Lyn via the Fcepsilon RI. J Immunol. 2005; 175:6885-6892.