The kinase inhibitor dasatinib induces apoptosis in chronic lymphocytic leukemia cells in vitro with preference for a subgroup of patients with unmutated IgVH genes

Blood

Volumn 112, Issue 4, 2008, Pages 1443-1452

  Veldurthy, Aditya ^a   Patz, Michaela ^a   Hagist, Susanne ^a   Pallasch, Christian P ^a   Wendtner, Clemens Martin ^a   Hallek, Michael ^a   Krause, Günter ^a  

^a UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DASATINIB; FLUDARABINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL XL; PROTEIN KINASE B; PROTEIN MCL 1; PROTEIN P53; PROTEIN TYROSINE KINASE; CASPASE; DRUG DERIVATIVE; IMMUNOGLOBULIN HEAVY CHAIN; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; PYRIMIDINE DERIVATIVE; THIAZOLE DERIVATIVE; VIDARABINE;

ADULT; AGED; APOPTOSIS; ARTICLE; CELL ISOLATION; CELL PROLIFERATION; CELL SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG SENSITIVITY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOGLOBULIN HEAVY CHAIN GENE; IMMUNOGLOBULIN VARIABLE REGION; LEUKEMIA CELL; MALE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; B CELL LEUKEMIA; CELL CULTURE; DOSE RESPONSE; DRUG EFFECT; DRUG POTENTIATION; GENETICS; KINETICS; METABOLISM; PATHOLOGY;

BCL-X PROTEIN; CASPASES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; KINETICS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIMIDINES; THIAZOLES; TUMOR CELLS, CULTURED; VIDARABINE;

EID: 51649130092     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-11-123984     Document Type: Article

References (50)

1. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005;352:804- 815.
2. HamblinTJ, Davis Z, Gardiner A. Oscier DG, Stevenson FK. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood. 1999;94:1848- 1854.
3. Wiestner A, Rosenwald A. Barry TS. et al. ZAP-70 expression identifies a chronic lymphocytic leukemia subtype with unmutated immunoglobulin genes, interior clinical outcome, and distinct gene expression profile. Blood. 2003:101: 4944-4951.
4. Crespo M, Bosch F Villamor N, et al. ZAP-70 expression as a surrogate for immunoglobulin-variable-region mutations in chronic lymphocytic leukemia. N Engl J Med. 2003;348:1764-1775.
5. Orchard JA, Ibbotson RE. Davis Z. et al. ZAP-70 expression and prognosis in chronic lymphocytic leukaemia. Lancet. 2004:363:105-111.
6. Deglesne PA. Chevallier N. Letestu R. et al. Survival response to B-cell receptor ligation is restricted to progressive chronic lymphocytic leukemia cells irrespective of Zap70 expression. Cancer Res. 2006;66:7158-7166.
7. Contri A, Brunati AM, Trentin L, et al. Chronic lymphocytic leukemia B cells contain anomalous Lyn tyrosine kinase, a putative contribution to detective apoptosis. J Clin Invest. 2005;115:369-378.
8. Hu Y, Liu Y, Pelletier S, et al. Requirement of Src kinases Lyn. Hck and Fgr for BCR-ABL1-induced B-lymphoblastic leukemia but not chronic myeloid leukemia. Nat Genet. 2004;36:453-461.
9. Druker BJ. Circumventing resistance to kinase- inhibitor therapy. N Engl J Med. 2006;354:2594- 2596.
10. Weisberg E, Manley PW, Cowan-Jacob SW, Hochhaus A. Griffin JD. Second generation inhibitors of BCR-ABL for the treatment of imatinib-resistant chronic myeloid leukaemia. Nat Rev Cancer. 2007;7:345-356.
11. Kantarjian H, Giles F, Wunderle L, et al. Nilotinib in imatinib-resistant CML and Philadelphia chromosome-positive ALL. N Engl J Med. 2006; 354:2542-2551.
12. Lombardo LJ, Lee FY, Chen P, et al. Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxy- ethyl)- 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.
13. Das J. Chen P. Norris D, et al. 2-aminothiazole as a novel kinase inhibitor template. Structure- activity relationship studies toward the discovery of N-(2-chloro-6-methylphenyl)-2-[[6-[4-(2-hy- droxyethyl)-1 -piperazinyl)]-2-methyl-4-pyrimidi- nyl]amino)]-1, 3-thiazole-5-carboxamide (dasat- inib. BMS-354825) as a potent pan-Src kinase inhibitor. J Med Chem. 49:6819-6832, 2006.
14. Burgess MR, Skaggs BJ, Shah NR Lee FY, Sawyers CL. Comparative analysis of two clinically active BCR-ABL kinase inhibitors reveals the role of conformation-specific binding in resistance. Proc Natl Acad Sci USA. 2005;102:3395- 3400.
15. Tokarski JS, Newitt JA, Chang CY et al. The structure of dasatinib (BMS-354825) bound to activated ABL kinase domain elucidates its inhibitory activity against imatinib-resistant ABL mutants. Cancer Res. 2006;66:5790-5797.
16. Talpaz M, Shah NP, Kantarjian H. et al. Dasatinib in imatinib-resistant Philadelphia chromosome- positive leukemias. N Engl J Med. 2006;354: 2531-2541.
17. SchindlerT, Bornmann W, Pellicena P, Miller WT, Clarkson B, Kuriyan J. Structural mechanism tor STI-571 inhibition of abelson tyrosine kinase. Science. 2000;289:1938-1942.
18. Carter TA, Wodicka LM, Shah NP, et al. Inhibition of drug-resistant mutants of ABL, KIT, and EGF receptor kinases. Proc Natl Acad Sci USA. 2005;102:11011-11016.
19. 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.
20. BoggonTJ, Eck MJ. Structure and regulation of Src family kinases. Oncogene. 2004;23:7918-7927.
21. Cheson BD, Bennett JM, Grever M, et al. National Gancer Institute-sponsored Working Group guidelines for chronic lymphocytic leukemia: revised guidelines for diagnosis and treatment. Blood. 1996:87:4990-4997.
22. Rassenti LZ, Huynh L, Toy TL, et al. ZAP-70 compared with immunoglobulin heavy-chain gene mutation status as a predictor of disease progression in chronic lymphocytic leukemia. N Engl J Med. 2004;351:893-901.
23. Durig J, Naschar M, Schmucker U, et al. CD38 expression is an important prognostic marker in chronic lymphocytic leukaemia. Leukemia. 2002; 16:30-35.
24. Matthews C, Catherwood M, Morris TC, Alexander HD. Routine analysis of lgVH mutational status in CLL patients using BIOMED-2 standardized primers and protocols. Leuk Lymphoma. 2004;45:1899-1904.
25. Niiro H, Clark EA. Regulation of B-cell fate by antigen-receptor signals. Nat Rev Immunol. 2002;2:945-956.
26. Kawauchi K, OgasawaraT, Yasuyama M. Activation of extracellular signal-regulated kinase through B-cell antigen receptor in B-cell chronic lymphocytic leukemia. Int J Hematol. 2002;75: 508-513.
27. Barragan M. Bellosillo B. Campas C. Colomer D, Pons G, Gil J. Involvement of protein kinase C and phosphatidylinositol 3-kinase pathways in the survival of B-cell chronic lymphocytic leukemia cells. Blood. 2002;99:2969-2976.
28. Longo PG, Laurenti L, Gobessi S, et al. The Akt signaling pathway determines the different proliferative capacity of chronic lymphocytic leukemia B-cells from patients with progressive and stable disease. Leukemia. 2007;21:110-120.
29. Melo JV. Foroni L, Brito-Babapulle V, Luzzatto L, Catovsky D. The establishment of cell lines from chronic B cell leukaemias: evidence of leukaemic origin by karyotypic abnormalities and Ig gene rearrangement. Clin Exp Immunol. 1988;73:23- 28.
30. Stacchini A, Aragno M, Vallario A. et al. MEC1 and MEC2: two new cell lines derived from B-chronic lymphocytic leukaemia in prolymphocy- toid transformation. Leuk Res. 1999;23:127-136.
31. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. 2004;116:205-219.
32. Pettitt AR, Sherrington PD, Stewart G, Cawley JC, Taylor AM, Stankovic T. p53 dysfunction in B-cell chronic lymphocytic leukemia: inactivation of ATM as an alternative to TP53 mutation. Blood. 2001;98:814-822.
33. Lin K, Sherrington PD, Dennis M, Matrai Z, Cawley JC, Pettitt AR. Relationship between p53 dysfunction, GD38 expression, and IgV(H) mutation in chronic lymphocytic leukemia. Blood. 2002;100:1404-1409.
34. Panasci L, Paiement JP, Christodoulopoulos G, Belenkov A, Malapetsa A, Aloyz R. Chlorambucil drug resistance in chronic lymphocytic leukemia: the emerging role of DNA repair. Clin Cancer Res. 2001;7:454-461.
35. Aloyz R, Grzywacz K, Xu ZY Loignon M, Alaoui- Jamali MA, Panasci L. Imatinib sensitizes CLL lymphocytes to chlorambucil. Leukemia. 2004;18: 409-414.
36. Nam S, Williams A, Vultur A, et al. Dasatinib (BMS-354825) inhibits Stat5 signaling associated with apoptosis in chronic myelogenous leukemia cells. Mol Cancer Ther. 2007;6:1400-1405.
37. rd, Treiber DK, et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat Biotechnol. 2005;23:329- 336.
38. Yu C, Rahmani M, Almenara J, Sausville EA, Dent P, Grant S. Induction of apoptosis in human leukemia cells by the tyrosine kinase inhibitor adaphostin proceeds through a RAF-1 /M EK/ ERK- and AKT-dependent process. Oncogene. 2004;23:1364-1376.
39. Vega Ml, Huerta-Yepaz S, Garban H, Jazirehi A, Emmanouilides C, Bonavida B. Rituximab inhibits p38 MAPK activity in 2F7 B NHL and decreases IL-10 transcription: pivotal role of p38 MAPK in drug resistance. Oncogene. 2004;23:3530-3540.
40. Henrich S, Christopherson Rl. Multiple forms of nuclear p53 formed in human Raji and MEC1 cells treated with fludarabine. Leukemia. 2008; 22:657-660.
41. Hu Y, Swerdlow S, Duffy TM, Weinmann R, Lee FY Li S. Targeting multiple kinase pathways in leukemic progenitors and stem cells is essential for improved treatment of Ph+ leukemia in mice. Proc Natl Acad Sci USA. 2006;103:16870- 16875.
42. ShanafeltTD. Lee YK. Bone ND, et al. Adaphostin-induced apoptosis in CLL B cells is associated with induction of oxidative stress and exhibits synergy with fludarabine. Blood. 2005; 105:2099-2106.
43. Luo FR, Yang Z, Camuso A, et al. Dasatinib (BMS-354825) pharmacokinetics and pharmacodynamic biomarkers in animal models predict optimal clinical exposure. Clin Gancer Res. 2006; 12:7180-7186.
44. Serrels A, Macpherson IR. Evans TR. et al. Identification of potential biomarkers for measuring inhibition of Src kinase activity in colon cancer cells following treatment with dasatinib. Mol Cancer Ther. 2006;5:3014-3022.
45. Amrein L, Loignon M, Goulet AC, et al. Chlorambucil cytotoxicity in malignant B lymphocytes is synergistically increased by 2-(morpholin-4-yl)- benzo[h]chomen-4-one (NU7026)-mediated inhibition of DNA double-strand break repair via inhibition of DNA-dependent protein kinase. J Pharmacol Exp Ther. 2007;321:848-855.
46. Mansour A, Ghang VT Srinivas S, Harrison J, Raveche E. Correlation of ZAP-70 expression in B cell leukemias to the ex vivo response to a combination of fludarabine/genistein. Cancer Immunol Immunother. 2007;56:501-514.
47. Warmuth M, Simon N, Mitina O, et al. Dualspecific Src and Abl kinase inhibitors, PP1 and CGP76030, inhibit growth and survival of cells expressing imatinib mesylate-resistant Bcr-Abl kinases. Blood. 2003;101:664-672.
48. Neumann C, Zehentmaier G, Danhauser-Riedl S, Emmerich B. Hallek M. lnterleukin-6 induces tyrosine phosphorylation of the Ras activating protein Shc, and its complex formation with Grb2 in the human multiple myeloma cell line LP-1. Eur J Immunol. 1996;26:379-384.
49. Schaeffer M, Schneiderbauer M, Weidler S, et al. Signaling through a novel domain of gp130 mediates cell proliferation and activation of Hck and Erk kinases. Mol Cell Biol. 2001 ;21:8068-8081.
50. Hausherr A, Tavares R, Schaffer M, et al. Inhibition of IL-6-dependent growth of myeloma cells by an acidic peptide repressing the gp130- mediated activation of Src family kinases. Oncogene. 2007;26:4987-4998.