A novel mechanism for imatinib mesylate-induced cell death of BCR-ABL-positive human leukemic cells: Caspase-independent, necrosis-like programmed cell death mediated by serine protease activity

Blood

Volumn 103, Issue 6, 2004, Pages 2299-2307

  Okada, Masayuki ^b   Adachi, Souichi ^a   Imai, Tsuyoshi ^b   Watanabe, Ken Ichiro ^b   Toyokuni, Shin Ya ^b   Ueno, Masaki ^b   Zervos, Artonis S ^b   Kroemer, Guido ^b   Nakahata, Tatsutoshi ^b  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; CASPASE INHIBITOR; ENDONUCLEASE; ENDONUCLEASE G; IMATINIB; PROTEIN TYROSINE KINASE INHIBITOR; REACTIVE OXYGEN METABOLITE; SERINE PROTEINASE; SERINE PROTEINASE OMI; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CELL VACUOLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME RELEASE; HUMAN; HUMAN CELL; LEUKEMIA CELL; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL;

EID: 1542283719     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2003-05-1605     Document Type: Article

References (66)

1. Druker BJ. Inhibition of the Bcr-Abl tyrosine kinase as a therapeutic strategy for CML. Oncogene. 2002;21:8541-8546.
2. Salesse S, Verfaillie CM. BCR/ABL: from molecular mechanisms of leukemia induction to treatment of chronic myelogenous leukemia. Oncogene. 2002;21:8547-8559.
3. Yu C, Krystal G, Varticovksi L, et al. Pharmacologic mitogen-activated protein/extracellular signal-regulated kinase kinase/mitogen-activated protein kinase inhibitors interact synergistically with STI571 to induce apoptosis in Bcr/Abl-expressing human leukemia cells. Cancer Res. 2002;62:188-199.
4. Sonoyama J, Matsumura I, Ezoe S, et al. Functional cooperation among Ras, STAT5, and phosphatidylinositol 3-kinase is required for full oncogenic activities of BCR/ABL in K562 cells. J Biol Chem. 2002;277:8076-8082.
5. Nimmanapalli R, Bhalla K. Novel targeted therapies for Bcr-Abl positive acute leukemias: beyond STI571. Oncogene. 2002;21:8584-8590.
6. Amarante-Mendes GP, McGahon AJ, Nishioka WK, Afar DE, Witte ON, Green DR. Bcl-2-independent Bcr-Abl-mediated resistance to apoptosis: protection is correlated with up regulation of Bcl-xL. Oncogene. 1998;16:1383-1390.
7. Amarante-Mendes GP, Naekyung Kim C, Liu L, et al. Bcr-Abl exerts its antiapoptotic effect against diverse apoptotic stimuli through blockage of mitochondrial release of cytochrome C and activation of caspase-3. Blood. 1998;91:1700-1705.
8. Deininger MW, Goldman JM, Lydon N, Melo JV. The tyrosine kinase inhibitor CGP57148B selectively inhibits the growth of BCR-ABL-positive cells. Blood. 1997;90:3691-3698.
9. Beran M, Cao X, Estrov Z, et al. Selective inhibition of cell proliferation and BCR-ABL phosphorylation in acute lymphoblastic leukemia cells expressing Mr 190,000 BCR-ABL protein by a tyrosine kinase inhibitor (CGP-57148). Clin Cancer Res. 1998;4:1661-1672.
10. Gambacorti-Passerini C, le Coutre P, Mologni L, et al. Inhibition of the ABL kinase activity blocks the proliferation of BCR/ABL+ leukemic cells and induces apoptosis. Blood Cells Mol Dis. 1997;23:380-394.
11. Dan S, Naito M, Tsuruo T. 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. 1998;5:710-715.
12. Mow BM, Chandra J, Svingen PA, et al. Effects of the Bcr/abl kinase inhibitors STI571 and adaphostin (NSC 680410) on chronic myelogenous leukemia cells in vitro. Blood. 2002;99:664-671.
13. Druker BJ, Talpaz M, Resta DJ, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001;344:1031-1037.
14. Druker BJ, Sawyers CL, Kantarjian H, et al. 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. 2001;344:1038-1042.
15. Kantarjian H, Sawyers C, Hochhaus A, et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med. 2002;346:645-652.
16. Talpaz M, Silver RT, Druker BJ, et al. Imatinib induces durable hematologic and cytogenetic responses in patients with accelerated phase chronic myeloid leukemia: results of a phase 2 study. Blood. 2002;99:1928-1937.
17. Sawyers CL, Hochhaus A, Feldman E, et al. Imatinib induces hematologic and cytogenetic responses in patients with chronic myelogenous leukemia in myeloid blast crisis: results of a phase 11 study. Blood. 2002;99:3530-3539.
18. Kantarjian HM, Cortes J, O'Brien S, et al. Imatinib mesylate (STI571) therapy for Philadelphia chromosome-positive chronic myelogenous leukemia in blast phase. Blood. 2002;99:3547-3553.
19. Braziel RM, Launder TM, Druker BJ, et al. Hematopathologic and cytogenetic findings in imatinib mesylate-treated chronic myelogenous leukemia patients: 14 months' experience. Blood. 2002;100:435-441.
20. Kantarjian HM, O'Brien S, Cortes JE, et al. Imatinib mesylate therapy for relapse after allogeneic stem cell transplantation for chronic myelogenous leukemia. Blood. 2002;100:1590-1595.
21. O'Dwyer ME, Mauro MJ, Kurilik G, et al. The impact of clonal evolution on response to imatinib mesylate (STI571) in accelerated phase CML. Blood. 2002;100:1628-1633.
22. Ottmann OG, Druker BJ, Sawyers CL, et al. A phase 2 study of imatinib in patients with relapsed or refractory Philadelphia chromosome-positive acute lymphoid leukemias. Blood. 2002;100:1965-1971.
23. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239-257.
24. Wyllie AH, Morris RG, Smith AL, Dunlop D. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol. 1984;142:67-77.
25. Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407:770-776.
26. Kitanaka C, Kuchino Y. Caspase-independent programmed cell death with necrotic morphology. Cell Death Differ. 1999;6:508-515.
27. Bursch W. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 2001;8:569-581.
28. Proskuryakov SY, Konoplyannikov AG, Gabai VL. Necrosis: a specific form of programmed cell death? Exp Cell Res. 2003;283:1-16.
29. Mathiasen IS, Jaattela M. Triggering caspase-independent cell death to combat cancer. Trends Mol Med. 2002;8:212-220.
30. Vercammen D, Beyaert R, Denecker G, et al. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med. 1998;187:1477-1485.
31. Kawahara A, Ohsawa Y, Matsumura H, Uchiyama Y, Nagata S. Caspase-independent cell killing by Fas-associated protein with death domain. J Cell Biol. 1998;143:1353-1360.
32. van Loo G, Saelens X, van Gurp M, MacFarlane M, Martin SJ, Vandenabeele P. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 2002;9:1031-1042.
33. Leist M, Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol. 2001;2:589-598.
34. Fleury C, Mignotte B, Vayssiere JL. Mitochondrial reactive oxygen species in cell death signaling. Biochimie. 2002;84:131-141.
35. Rose AL, Smith BE, Maloney DG. Glucocorticoids and rituximab in vitro: synergistic direct antiproliferative and apoptotic effects. Blood. 2002;100:1765-1773.
36. Gottlieb RA, Adachi S. Nitrogen cavitation for cell disruption to obtain mitochondria from cultured cells. Methods Enzymol. 2000;322:213-221.
37. Zamzami N, Marchetti P, Castedo M, et al. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J Exp Med. 1995;181:1661-1672.
38. Kroemer G, Petit P, Zamzami N, Vayssiere JL, Mignotte B. The biochemistry of programmed cell death. Faseb J. 1995;9:1277-1287.
39. Susin SA, Zamzami N, Kroemer G. Mitochondria as regulators of apoptosis: doubt no more. Biochim Biophys Acta. 1998;1366:151-165.
40. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med. 2000;6:513-519.
41. Martinou JC, Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol. 2001;2:63-67.
42. Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature. 2001;412:95-99.
43. Sattler M, Verma S, Shrikhande G, et al. The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J Biol Chem. 2000;275:24273-24278.
44. Dumont C, Durrbach A, Bidere N, et al. Caspase-independent commitment phase to apoptosis in activated blood T lymphocytes: reversibility at low apoptotic insult. Blood. 2000;96:1030-1038.
45. Susin SA, Lorenzo HK, Zamzami N, et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 1999;397:441-446.
46. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell. 2001;8:613-621.
47. Narvaez CJ, Welsh J. Role of mitochondria and caspases in vitamin D-mediated apoptosis of MCF-7 breast cancer cells. J Biol Chem. 2001;276:9101-9107.
48. Hirsch T, Marchetti P, Susin SA, et al. The apoptosis-necrosis paradox: apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene. 1997;15:1573-1581.
49. Xiang J, Chao DT, Korsmeyer SJ. BAX-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc Natl Acad Sci U S A. 1996;93:14559-14563.
50. Liu CY, Takemasa A, Liles WC, et al. Broad-spectrum caspase inhibition paradoxically augments cell death in TNF-alpha-stimulated neutrophils. Blood. 2003;101:295-304.
51. Maianski NA, Roos D, Kuijpers TW. Tumor necrosis factor alpha induces a caspase-independent death pathway in human neutrophils. Blood. 2003;101:1987-1995.
52. van Loo G, van Gurp M, Depuydt B, et al. The serine protease Omi/HtrA2 is released from mitochondria during apoptosis: Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ. 2002;9:20-26.
53. Hegde R, Srinivasula SM, Zhang Z, et al. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J Biol Chem. 2002;277:432-438.
54. Martins LM, Iaccarino I, Tenev T, et al. The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J Biol Chem. 2002;277:439-444.
55. Verhagen AM, Silke J, Ekert PG, et al. HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J Biol Chem. 2002;277:445-454.
56. Huang Y, Sheikh MS, Fornace AJ Jr, Holbrook NJ. Serine protease inhibitor TPCK prevents Taxol-induced cell death and blocks c-Raf-1 and Bcl-2 phosphorylation in human breast carcinoma cells. Oncogene. 1999;18:3431-3439.
57. Mitsui C, Sakai K, Ninomiya T, Koike T. Involvement of TLCK-sensitive serine protease in colchicine-induced cell death of sympathetic neurons in culture. J Neurosci Res. 2001;66:601-611.
58. Cromlish JA, Roeder RG. Human transcription factor IIIC (TFIIIC): purification, polypeptide structure, and the involvement of thiol groups in specific DNA binding. J Biol Chem. 1989;264:18100-18109.
59. Cilenti L, Lee Y, Hess S, et al. Characterization of a novel and specific inhibitor for the pro-apoptotic protease Omi/HtrA2. J Biol Chem. 2003;278:11489-11494.
60. Jin S, Kalkum M, Overholtzer M, Stoffel A, Chait BT, Levine AJ. CIAP1 and the serine protease HTRA2 are involved in a novel p53-dependent apoptosis pathway in mammals. Genes Dev. 2003;17:359-367.
61. Hirt UA, Gantner F, Leist M. Phagocytosis of non-apoptotic cells dying by caspase-independent mechanisms. J Immunol. 2000;164:6520-6529.
62. Reiter I, Krammer B, Schwamberger G. Cutting edge: differential effect of apoptotic versus necrotic tumor cells on macrophage antitumor activities. J Immunol. 1999;163:1730-1732.
63. Chen Y, Douglass T, Jeffes EW, et al. Living T9 glioma cells expressing membrane macrophage colony-stimulating factor produce immediate tumor destruction by polymorphonuclear leukocytes and macrophages via a "paraptosis"-induced pathway that promotes systemic immunity against intracranial T9 gliomas. Blood. 2002;100:1373-1380.
64. Gough MJ, Melcher AA, Ahmed A, et al. Macrophages orchestrate the immune response to tumor cell death. Cancer Res. 2001;61:7240-7247.
65. Steinman RM, Turley S, Mellman I, Inaba K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med. 2000;191:411-416.
66. Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med. 2000;191:423-434.