The novel pyrrolo-1,5-benzoxazepine, PBOX-21, potentiates the apoptotic efficacy of STI571 (imatinib mesylate) in human chronic myeloid leukaemia cells

Biochemical Pharmacology

Volumn 77, Issue 3, 2009, Pages 310-321

  Bright, Sandra A ^a   Greene, Lisa M ^a   Greene, Tom F ^a   Campiani, Giuseppe ^b   Butini, Stefania ^b   Brindisi, Margherita ^b   Lawler, Mark ^c   Meegan, Mary J ^a   Williams, D Clive ^a   Zisterer, Daniela M ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF SIENA   (Italy)

^c ST JAMES S HOSPITAL   (Ireland)

Author keywords

Apoptosis; CML; PBOX; Serine proteases; STI571

Indexed keywords

BCR ABL PROTEIN; BENZODIAZEPINE DERIVATIVE; BIM PROTEIN; CASPASE 8; CASPASE 9; CHYMOTRYPSIN; CYTOCHROME C; IMATINIB; KETONE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PBOX 21; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; PROTEINASE; TOSYLPHENYLALANYL CHLOROMETHYL KETONE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL STRAIN HL 60; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN SECRETION; UPREGULATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CARBAMATES; CELL LINE, TUMOR; DOWN-REGULATION; DRUG SYNERGISM; FLOW CYTOMETRY; FUSION PROTEINS, BCR-ABL; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MEMBRANE POTENTIALS; OXAZEPINES; PIPERAZINES; PYRIMIDINES; UP-REGULATION;

EID: 58649117744     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.10.008     Document Type: Article

References (44)

1. Deininger M., Goldman J., and Melo J. The molecular biology of chronic myeloid leukaemia. Blood 96 (2000) 3343-3356
2. Druker B., Sawyers C., Capdeville R., Ford J., Baccarani M., and Goldman J. Chronic myelogenous leukemia. Hematol Am Soc Hematol Educ Program 1 (2001) 87-112
3. Faderl S., Talpaz M., Estrov Z., and Kantarjian H. Chronic myelogenous leukemia: biology and therapy. Ann Intern Med 131 (1999) 207-219
4. Deininger M., Buchdunger E., and Druker B. The development of imatinib as a therapeutic agent for chronic myeloid leukaemia. Blood 105 (2005) 2640-2653
5. Talpaz M., Silver R., Druker B., Goldman J., Gambacorti-Passerini C., Guilhot F., et al. Imatinib induces durable hematologic and cytogenetic responses in patients with accelerated phase chronic myeloid leukemia: results of a phase 2 study. Blood 99 (2002) 1928-1937
6. Gorre M., Mohammed M., Ellwood K., Hsu N., Paquette R., Nagesh Rao P., et al. Clinical resistance to STI571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293 (2001) 876-880
7. Roche-Lestienne C., Soenen-Cornu V., Grardel-Duflos N., Lai J., Philippe N., Facon T., et al. Several types of mutations of the Abl gene can be found in chronic myeloid leukemia patients resistant to STI571 and they can pre-exist to the onset of treatment. Blood 100 (2002) 1014-1018
8. Kano Y., Akutsu M., Tsunoda S., Mano H., Sato Y., Honma Y., et al. In vitro cytotoxic effects of a tyrosine kinase inhibitor STI571 in combination with commonly used antileukemic agents. Blood 97 (2001) 1999-2007
9. Borthakur G., Kantarjian H., Daley G., Talpaz M., O'Brien S., Garcia-Manero G., et al. Pilot study of lonafarnib, a farnesyl transferase inhibitor, in patients with chronic myeloid leukemia in the chronic or accelerated phase that is resistant or refractory to imatinib therapy. Cancer 106 (2006) 346-352
10. Yu C., Krystal G., Dent P., and Grant S. Flavopiridol potentiates STI571-induced mitochondrial damage and apoptosis in BCR-ABL-positive human leukemia cells. Clin Cancer Res 8 (2002) 2976-2984
11. Nimmanapalli R., Fuino L., Stobaugh C., Richon V., and Bhalla K. Cotreatment with the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) enhances imatinib-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Blood 101 (2003) 3236-3239
12. Yu C., Rahmani M., Almenara J., Subler M., Krystal G., Conrad D., et al. Histone deacetylase inhibitors promote STI571-mediated apoptosis in STI571-sensitive and -resistant Bcr/Abl+ human myeloid leukemia cells. Cancer Res 63 (2003) 2118-2126
13. Yu C., Krystal G., Varticovksi L., McKinstry R., Rahmani M., Dent P., 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 62 (2002) 188-199
14. Nguyen T., Rahmani M., Gao N., Kramer L., Corbin A., Druker B., et al. Synergistic interactions between DMAG and mitogen-activated protein kinase kinase 1/2 inhibitors in Bcr/abl+ leukemia cells sensitive and resistant to imatinib mesylate. Clin Cancer Res 12 (2006) 2239-2247
15. Wyllie A., Kerr J., and Currie A. Cell death: the significance of apoptosis. Int Rev Cytol 68 (1980) 251-306
16. Ellis H., and Horvitz H. Genetic control of programmed cell death in the nematode C. elegans. Cell 44 (1986) 817-829
17. Chang H., and Yang X. Proteases for cell suicide: functions and regulation of caspases. Microbiol Mol Biol Rev 64 (2000) 821-846
18. O'Connell A., Holohan C., Torriglia A., Lee B., and Stenson-Cox C. Characterization of a serine protease-mediated cell death program activated in human leukemia cells. Exp Cell Res 312 (2006) 27-39
19. Mulligan J.M., Campiani G., Ramunno A., Nacci V., and Zisterer D.M. Inhibition of G1 cyclin-dependent kinase activity during growth arrest of human astrocytoma cells by the pyrrolo-1,5-benzoxazepine, PBOX-21. Biochim Biophys Acta 1639 (2003) 43-52
20. Greene L.M., Fleeton M., Mulligan J., Gowda C., Sheahan B.J., Atkins G.J., et al. The pyrrolo-1,5-benzoxazepine, PBOX-6, inhibits the growth of breast cancer cells in vitro independent of estrogen receptor status and inhibits breast tumour growth in vivo. Oncol Rep 14 (2005) 1357-1363
21. Greene L.M., Kelly L., Onnis V., Campiani G., Lawler M., Williams D.C., et al. STI-571 enhances the apoptotic efficacy of PBOX-6, a novel microtubule targeting agent, in both STI-571-sensitive and -resistant Bcr-Abl-positive human chronic myeloid leukemia cells. J Pharmacol Exp Ther 321 (2007) 288-297
22. Zisterer D.M., Campiani G., Nacci V., and Williams D.C. Pyrrolo-1,5-benzoxazepines induce apoptosis in HL-60, Jurkat, and Hut-78 cells: a new class of apoptotic agents. J Pharmacol Exp Ther 293 (2000) 48-59
23. Mc Gee M.M., Campiani G., Ramunno A., Fattorusso C., Nacci V., Lawler M., et al. Pyrrolo-1,5-benzoxazepines induce apoptosis in chronic myelogenous leukemia (CML) cells by bypassing the apoptotic suppressor bcr-abl. J Pharmacol Exp Ther 296 (2001) 31-40
24. Campiani G., Nacci V., Fiorini I., De Filippis M., Garofalo A., Ciani S., et al. Synthesis, biological activity, and SARs of pyrrolobenzoxazepine derivatives, a new class of specific "peripheral-type" benzodiazepine receptor ligands. J Med Chem 39 (1996) 3435-3450
25. Kaufmann S., Desnoyers S., Ottaviano Y., Davidson N., and Poirier G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res 53 (1993) 3976-3985
26. Brown T.L., Patil S., Basnett R.K., and Howe P.H. Caspase inhibitor BD-fmk distinguishes transforming growth factor beta-induced apoptosis from growth inhibition. Cell Growth Differ 9 (1998)
27. Drakos E., Rassidakis G.Z., Lai R., Herling M., O'Connor S.L., Schmitt-Graeff A., et al. Caspase-3 activation in systemic anaplastic large-cell lymphoma. Mod Pathol 17 January (1) (2004) 109-116
28. Stenson-Cox C., FitzGerald U., and Samali A. In the cut and thrust of apoptosis, serine proteases come of age. Biochem Pharmacol 66 (2003) 1469-1474
29. Wolf B., and Green D. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 274 (1999) 20049-20052
30. Kelly W., Richon V., O'Connor O., Curley T., MacGregor-Curtelli B., Tong W., et al. Phase I clinical trial of histone deacetylase inhibitor: suberoylanilide hydroxamic acid administered intravenously. Clin Cancer Res 10 (2003) 3578-3588
31. Fiskus W., Pranpat M., Balasis M., Bali P., Estrella V., Kumaraswamy S., et al. Cotreatment with vorinostat (suberoylanilide hydroxamic acid) enhances activity of dasatinib (BMS-354825) against imatinib mesylate-sensitive or imatinib mesylate-resistant chronic myelogenous leukemia cells. Clin Cancer Res 12 (2006) 5869-5878
32. Yanovich S., Hall R., and Gewirtz D. Characterization of a K562 multidrug-resistant cell line. Cancer Res 49 (1989) 4499-4503
33. Horita M., Andreu E., Benito A., Arbona C., Sanz C., Benet I., et al. Blockade of the Bcr-Abl kinase activity induces apoptosis of chronic myelogenous leukemia cells by suppressing signal transducer and activator of transcription 5-dependent expression of Bcl-XL. J Exp Med 191 (2000) 977-984
34. Donato N., Wu J., Zhang L., Kantarjian H., and Talpaz M. Down-regulation of interleukin-3/granulocyte-macrophage colony-stimulating factor receptor beta-chain in Bcr-Abl (+) human leukemic cells: association with loss of cytokine-mediated Stat-5 activation and protection from apoptosis after Bcr-Abl inhibition. Blood 97 (2001) 2846-2853
35. Zhu J., Xiong L., Yu B., and Wu J. Apoptosis induced by a new member of saponin family is mediated through caspase-8-dependent cleavage of Bcl-2. Mol Pharmacol 68 (2005) 1831-1838
36. Kamei T., Inui M., Nakamura S., Okumura K., Goto A., Tagawa T., et al. Anti-Fas antibody-induced apoptosis in human melanoma cell lines and its relationship to bcl-2 cleavage and bak expression. Melanoma Res 13 (2003) 153-159
37. Lin H., Zhang X., Chen C., and Chen B. Apoptosis of Mo7e leukemia cells is associated with the cleavage of Bcl-2 into a shortened fragment that is not functional for heterodimerization with Bcl-2 and Bax. Exp Cell Res 261 (2000) 180-186
38. Kuroda J., Puthalakath H., Cragg M., Kelly P., Bouillet P., Huang D., et al. Bim and Bad mediate imatinib-induced killing of Bcr/Abl+ leukemic cells, and resistance due to their loss is overcome by a BH3 mimetic. Proc Natl Acad Sci USA 103 (2006) 14907-14912
39. Essafi A., Fernandez de Mattos S., Hassen Y., Soeiro I., Mufti G., Thomas N., et al. Direct transcriptional regulation of Bim by FoxO3a mediates STI571-induced apoptosis in Bcr-Abl-expressing cells. Oncogene 24 (2005) 2317-2329
40. Maquarre E., Artus C., Gadhoum Z., Jasmin C., Smadja-Joffe F., and Robert-Lezenes J. CD44 ligation induces apoptosis via caspase- and serine protease-dependent pathways in acute promyelocytic leukemia cells. Leukemia 19 (2005) 2296-2303
41. Rotolo J., Zhang J., Donepudi M., Lee H., Fuks Z., and Kolesnick R. Caspase-dependent and -independent activation of acid sphingomyelinase signaling. J Biol Chem 280 (2005) 26425-26434
42. Okada M., Adachi S., Imai T., Watanabe K., Toyokuni S.Y., Ueno M., et al. 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 103 (2004) 2299-2307
43. Radujkovic A., Topaly J., Fruehauf S., and Zeller W.J. Combination treatment of imatinib-sensitive and -resistant BCR-ABL-positive CML cells with imatinib and farnesyltransferase inhibitors. Anticancer Res 26 (2006) 2169-2177
44. Miyoshi T., Nagai T., Ohmine K., Nakamura M., Kano Y., Muroi K., et al. Relative importance of apoptosis and cell cycle blockage in the synergistic effect of combined R115777 and imatinib treatment in BCR/ABL-positive cell lines. Biochem Pharmacol 69 (2005) 1585-1594