Imatinib mesylate (STI571) abrogates the resistance to doxorubicin in human K562 chronic myeloid leukemia cells by inhibition of BCR/ABL kinase-mediated DNA repair

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 603, Issue 1, 2006, Pages 74-82

  Majsterek, Ireneusz ^a   Sliwinski, Tomasz ^a   Poplawski, Tomasz ^a   Pytel, Dariusz ^a   Kowalski, Michal ^b   Slupianek, Artur ^c   Skorski, Tomasz ^c   Blasiak, Janusz ^a  

^a UNIVERSITY OF LODZ   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

^c Temple University   (United States)

Author keywords

BCR ABL; DNA repair; Drug resistance; Leukemia; STI571

Indexed keywords

ANTILEUKEMIC AGENT; BCR ABL PROTEIN; CRK LIKE PROTEIN; DOXORUBICIN; IMATINIB; PROTEIN TYROSINE KINASE INHIBITOR;

ANIMAL CELL; ARTICLE; CHRONIC MYELOID LEUKEMIA; COMET ASSAY; CONTROLLED STUDY; DNA REPAIR; DRUG MECHANISM; DRUG SPECIFICITY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LYMPHATIC LEUKEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING;

ANTIBIOTICS, ANTINEOPLASTIC; BLOTTING, WESTERN; DNA DAMAGE; DNA REPAIR; DOXORUBICIN; DRUG INTERACTIONS; DRUG RESISTANCE, NEOPLASM; HUMANS; KINETICS; LEUKEMIA, MYELOID, CHRONIC; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PYRIMIDINES; TUMOR CELLS, CULTURED;

MURINAE;

EID: 33644835864     PISSN: 13835718     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2005.10.010     Document Type: Article

References (52)

1. G.Q. Daley, R.A. Van Etten, and D. Baltimore Transformation of an interleukin 3-dependent hematopoietic cell line by the chronic myelogenous leukemia-specific P210bcr/abl protein Science 247 1990 824 830
2. T.G. Lugo, A.M. Pendergast, A.J. Muller, and O.N. Witte Tyrosine kinase activity and transformation potency of BCR/ABL oncogene products Science 247 1990 1079 1082
3. M. Sattler, and R. Salgia Activation of hematopoietic growth factor signal transduction pathways by the human oncogene BCR/ABL Leukemia 12 1998 637 644
4. B.J. Druker, S. Tamura, E. Buchdunger, S. Ohno, G.M. Segal, S. Fanning, J. Zimmermann, and N.B. Lydon Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of BCR/ABL positive cells Nat. Med. 2 1996 561 566
5. B. Nagar, W.G. Bornmann, P. Pellicena, T. Schindler, D.R. Veach, W.T. Miller, B. Clarkson, and J. Kuriyan Crystal structures of the kinase domain of c-Abl in complex with the small molecule inhibitors PD173955 and imatinib (STI-571) Cancer Res. 62 2002 4236 4243
6. B. Nagar, O. Hantschel, M.A. Young, K. Scheffzek, D. Veach, W. Bornmann, B. Clarkson, G. Superti-Furga, and J. Kuriyan Structural basis for the autoinhibition of c-Abl tyrosine kinase Cell 112 2003 859 871
7. I.M. Grumbach, I.A. Mayer, S. Uddin, F. Lekmine, B. Majchrzak, H. Yamauchi, S. Fujita, B. Druker, E.N. Fish, and L.C. Platanias Engagement of the CrkL adaptor in interferon alpha signalling in BCR/ABL-expressing cells Br. J. Haematol. 112 2001 327 336
8. A. Slupianek, C. Schmutte, G. Tombline, M. Nieborowska-Skorska, G. Hoser, M.O. Nowicki, A.J. Pierce, R. Fishel, and T. Skorski BCR/ABL regulates mammalian RecA homologs resulting in drug resistance Mol. Cell 8 2001 795 806
9. A. Slupianek, G. Hoser, I. Majsterek, A. Bronisz, M. Malecki, J. Blasiak, R. Fishel, and T. Skorski Fusion tyrosine kinases induce therapeutic drug resistance by stimulation of homology-dependent recombination repair, prolongation of G2/M phase and protection from apoptosis Mol. Cell. Biol. 22 2002 4189 4201
10. I. Majsterek, J. Blasiak, W. Mlynarski, G. Hoser, and T. Skorski Does the bcr/abl-mediated increase in the efficacy of DNA repair play a role in the drug resistance of cancer cells? Cell Biol. Int. 26 2002 363 370
11. G. Hoser, I. Majsterek, D.L. Romana, A. Slupianek, J. Blasiak, and T. Skorski Fusion oncogenic tyrosine kinases alter DNA damage and repair after genotoxic treatment: role in drug resistance? Leuk. Res. 27 2003 267 273
12. I. Majsterek, A. Slupianek, G. Hoser, T. Skorski, and J. Blasiak ABL-fusion oncoproteins activate multi-pathway of DNA repair: role in drug resistance? Biochimie 86 2004 53 65
13. I. Majsterek, A. Slupianek, and J. Blasiak TEL-fusion oncogenic tyrosine kinases determine leukemic cells response to idarubicin Anticancer Drugs 14 2003 625 631
14. E. Buchdunger, J. Zimmermann, H. Mett, T. Meyer, M. Muller, B.J. Druker, and N.B. Lydon Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative Cancer Res. 56 1996 100 104
15. B.J. Druker, M. Talpaz, and D.J. Resta Efficacy and safety of a specific inhibitor of the BCR/ABL tyrosine kinase in chronic myeloid leukemia N. Engl. J. Med. 344 2001 1031 1037
16. B.J. Druker, C.L. Sawyers, H. Kantarjian, D.J. Resta, S.F. Reese, J.M. Ford, R. Capdeville, and M. Talpaz Activity of a specific inhibitor of the BCR/ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome N. Engl. J. Med. 344 2001 1038 1042
17. S.G. O'Brien, F. Guilhot, R.A. Larson, I. Gathmann, M. Baccarani, F. Cervantes, J.J. Cornelissen, T. Fischer, A. Hochhaus, T. Hughes, K. Lechner, J.L. Nielsen, P. Rousselot, J. Reiffers, G. Saglio, J. Shepherd, B. Simonsson, A. Gratwohl, J.M. Goldman, H. Kantarjian, K. Taylor, G. Verhoef, A.E. Bolton, R. Capdeville, and B.J. Druker Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia N. Engl. J. Med. 348 2003 994 1004
18. M.J. Mauro, M. O'Dwyer, M.C. Heinrich, and B.J. Druker STI571: a paradigm of new agents for cancer therapeutics Clin. Oncol. 20 2002 325 334
19. R. Kurzrock, H.M. Kantarjian, B.J. Druker, and M. Talpaz Philadelphia chromosome-positive leukemias: from basic mechanisms to molecular therapeutics Ann. Int. Med. 138 2003 819 830
20. B.J. Druker Chronic myeloid leukemia in the imatinib era Semin. Hematol. 40 2003 50 58
21. M.W. Deininger, and B.J. Druker Specific targeted therapy of chronic myelogenous leukemia with imatinib Pharmacol. Rev. 55 2003 401 423
22. A.J. Tipping, and J.V. Melo Imatinib mesylate in combination with other chemotherapeutic drugs: in vitro studies Semin. Hematol. 40 2, Suppl. 2 2003 83 91
23. P. Zhang, W.Y. Gao, S. Turner, and B.S. Ducatman Gleevec (STI-571) inhibits lung cancer cell growth (A549) and potentiates the cisplatin effect in vitro Mol. Cancer 2 2003 1
24. T. Yin, Y.L. Wu, H.P. Sun, G.L. Sun, Y.Z. Du, K.K. Wang, J. Zhang, G.Q. Chen, S.J. Chen, and Z. Chen Combined effects of As4S4 and imatinib on chronic myeloid leukemia cells and BCR-ABL oncoprotein Blood 104 2004 4219 4225
25. P. Borchmann, K. Hubel, R. Schnell, and A. Engert Idarubicin: a brief overview on pharmacology and clinical use Int. J. Clin. Pharmacol. 35 1997 80 83
26. J. Blasiak, E. Gloc, K. Woźniak, W. Mlynarski, M. Stolarska, T. Skorski, and I. Majsterek Genotoxicity of idarubicin and its modulation by vitamins C and E and amifostine Chem. Biol. Interact. 140 2002 1 18
27. W.Y. Siu, T. Arooz, and R.Y.C. Poon Differential responses of proliferating versus quiescent cells to adriamycin Exp. Cell Res. 250 1999 131 141
28. F. Grandjean, L. Bremaud, M. Verdier, J. Robert, and M.H. Ratinaud Sequential gene expression of P-glycoprotein (P-gp), multidrug resistance-associated protein (MRP) and lung resistance protein: functional activity of P-gp and MRP present in the doxorubicin-resistant human K562 cell lines Anticancer Drugs 12 2001 247 258
29. A. Laroche-Clary, A. Larrue, and J. Robert Down-regulation of BCR/ABL and bcl-xl expression in a leukemia cell line and its doxorubicine-resistant variant by topoisomerase II inhibitors Biochem. Pharmacol. 60 2000 1828 1832
30. W.Y. Siu, T. Arooz, and R.Y.C. Poon Differential responses of proliferating versus quiescent cells to adriamycin Exp. Cell Res. 250 1999 131 141
31. N.P. Singh, T. McCoy, R.R. Tice, and E.L. Schneider A simple technique for quantitation of low levels of DNA damage in individual cells Exp. Cell Res. 175 1988 184 192
32. M. Klaude, S. Eriksson, J. Nygren, and G. Ahnstrom The comet assay: mechanisms and technical considerations Mutat. Res. 12 1996 89 96
33. J.A. Ashby, H. Tinwell, P.A. Lefevre, and M.A. Browne The single cell gel electrophoresis assay for induced DNA damage (comet assay): measurement of tail length and moment Mutagenesis 10 1995 85 90
34. K. Senechal, C. Heaney, B. Druker, and C.L. Sawyers Structural requirements for function of the Crkl adapter protein in fibroblasts and hematopoietic cells Mol. Cell. Biol. 18 1998 5082 5090
35. A. Hochhaus, S. Kreil, A.S. Corbin, P. La Rosee, M.C. Muller, T. Lahaye, B. Hanfstein, C. Schoch, N.C. Cross, U. Berger, H. Gschaidmeier, B.J. Druker, and R. Hehlmann Molecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy Leukemia 16 2002 2190 2196
36. T. Skorski Oncogenic tyrosine kinases and the DNA-damage response Nat. Rev. Cancer 2 2002 351 360
37. T. Skorski BCR/ABL regulates response to DNA damage: the role in resistance to genotoxic treatment and in genomic instability Oncogene 21 2002 8591 8604
38. A. Bedi, J.P. Barber, and G.C. Bedi BCR/ABL-mediated inhibition of apoptosis with delay of G2/M transition after DNA damage: a mechanism of resistance to multiple anticancer agents Blood 86 1995 1148 1158
39. G.P. Amarante-Mendes, A.J. McGahon, W.K. Nishioka, D.E. Afar, O.N. Witte, and D.R. Green Bcl-2 independent BCR/ABL-mediated resistance to apoptosis: protection is correlated with up regulation of Bcl-xL Oncogene 16 1998 1383 1390
40. K. Nishii, J.H. Kabarowski, D.L. Gibbons, S.D. Griffiths, I. Titley, L.M. Wiedemann, and M.F. Greaves ts BCR/ABL kinase activation confers increased resistance to genotoxic damage via cell cycle block Oncogene 13 1996 2225 2234
41. G.P. Amarante-Mendes, C. Naekyung Kim, L. Liu, Y. Huang, C.L. Perkins, D.R. Green, and K. Bhalla BCR/ABL exerts its antiapoptotic effect against diverse apoptotic stimuli through blockage of mitochondrial release of cytochrome C and activation of caspase-3 Blood 91 1998 1700 1705
42. A. Shinohara, and T. Ogawa Homologous recombination and the roles of double-strand breaks Trends Biochem. Sci. 20 1995 387 391
43. Y. Canitrot, R. Falinski, T. Louat, G. Laurent, C. Cazaux, J.S. Hoffmann, D. Lautier, and T. Skorski p210 BCR/ABL kinase regulates nucleotide excision repair (NER) and resistance to UV radiation Blood 102 2003 2632 2637
44. D.A. Thomas, S. Faderl, J. Cortes, S. O'Brien, F.J. Giles, S.M. Kornblau, G. Garcia-Manero, M.J. Keating, M. Andreeff, S. Jeha, M. Beran, S. Verstovsek, S. Pierce, L. Letvak, A. Salvado, R. Champlin, M. Talpaz, and H. Kantarjian Treatment of Philadelphia chromosome-positive acute lymphocytic leukemia with hyper-CVAD and imatinib mesylate Blood 103 2004 4396 4407
45. S. Dan, M. Naito, and T. Tsuruo Selective induction of apoptosis in Philadelphia chromosome-positive chronic myelogenous leukemia cells by an inhibitor of BCR-ABL tyrosine kinase, CGP 57148 Cell Death Differ. 5 1998 710 715
46. N.C. Wolff, and R.L. Ilaria Jr. Establishment of a murine model for therapy-treated chronic myelogenous leukemia using the tyrosine kinase inhibitor STI571 Blood 98 2001 2808 2816
47. T. Nishihara, Y. Miura, Y. Tohyama, C. Mizutani, T. Hishita, S. Ichiyama, T. Uchiyama, and K. Tohyama Effects of the tyrosine kinase inhibitor imatinib mesylate on a BCR/ABL-positive cell line: suppression of autonomous cell growth but no effect on decreased adhesive property and morphological changes Int. J. Hematol. 78 2003 233 240
48. F. Traina, J.B. Carvalheira, M.J. Saad, F.F. Costa, and S.T. Saad BCR/ABL binds to IRS-1 and IRS-1 phosphorylation is inhibited by imatinib in K562 cells FEBS Lett. 535 2003 17 22
49. K. Kawauchi, T. Ogasawara, M. Yasuyama, and S. Ohkawa Involvement of Akt kinase in the action of STI571 on chronic myelogenous leukemia cells Blood Cells Mol. Dis. 31 2003 11 17
50. N. Komatsu, T. Watanabe, M. Uchida, M. Mori, K. Kirito, S. Kikuchi, Q. Liu, T. Tauchi, K. Miyazawa, H. Endo, T. Nagai, and K. Ozawa A member of Forkhead transcription factor FKHRL1 is a downstream effector of STI571-induced cell cycle arrest in BCR/ABL-expressing cells J. Biol. Chem. 278 2003 6411 6419
51. R.W. Sobol, M. Kartalou, K.H. Almeida, D.F. Joyce, B.P. Engelward, J.K. Horton, R. Prasad, L.D. Samson, and S.H. Wilson Base excision repair intermediates induce p53-independent cytotoxic andgenotoxic responses J. Biol. Chem. 278 2003 39951 39959
52. J.S. Russel, K. Brady, M.A. Cerra, K.A. Oswald, K. Camphausen, and P.J. Tofilon Gleevec-mediated inhibition of Rad 51 expression and enhancement of tumor cell radiosensitivity Cancer Res. 63 2003 7377 7383