The novel tubulin-targeting agent pyrrolo-1,5-benzoxazepine-15 induces apoptosis in poor prognostic subgroups of chronic lymphocytic leukemia

Cancer Research

Volumn 69, Issue 21, 2009, Pages 8366-8375

  McElligott, Anthony M ^a   Maginn, Elaina N ^a   Greene, Lisa M ^a   McGuckin, Siobhan ^b   Hayat, Amjad ^a,e   Browne, Paul V ^b   Butini, Stefania ^c   Campiani, Giuseppe ^c   Catherwood, Mark A ^d   Vandenberghe, Elisabeth ^b   Williams, D Clive ^a   Zisterer, Daniela M ^a   Lawler, Mark ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ST JAMES S HOSPITAL   (Ireland)

^c UNIVERSITY OF SIENA   (Italy)

^d BELFAST CITY HOSPITAL   (United Kingdom)

^e UNIVERSITY HOSPITAL GALWAY   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 8; FLUDARABINE; PROTEIN KINASE ZAP 70; PYRROLOBENZOXAZEPINE 4 ACETOXY 5 (1 NAPHTHYL)NAPHTHA PYRROL[1,4]OXAZEPINE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ADULT; AGED; APOPTOSIS; ARTICLE; CHROMOSOME 17P; CHROMOSOME DELETION; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IC 50; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 8; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNOBLOTTING; IMMUNOGLOBULIN HEAVY CHAINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MICROTUBULES; MIDDLE AGED; OXAZEPINES; PROGNOSIS; PYRROLES; TUBULIN; VIDARABINE; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 70350528658     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-0131     Document Type: Article

References (47)

1. Caligaris-Cappio F, Hamblin TJ. B-cell chronic lymphocytic leukemia: a bird of a different feather. J Clin Oncol 1999;17:399-408. (Pubitemid 29022419)
2. Chiorazzi N. Cell proliferation and death: forgotten features of chronic lymphocytic leukemia B cells. Best Pract Res Clin Haematol 2007;20:399-413. (Pubitemid 47250501)
3. Tam CS, Keating MJ. Chemoimmunotherapy of chronic lymphocytic leukemia. Best Pract Res Clin Haematol 2007;20:479-498
4. Zisterer DM, Campiani G, Nacci V, Williams DC. Pyrrolo-1,5-benzoxazepines induce apoptosis in HL-60, Jurkat, and Hut-78 cells: a new class of apoptotic agents. J Pharmacol Exp Ther 2000;293:48-59. (Pubitemid 30180922)
5. Mulligan JM, Campiani G, Ramunno A, Nacci V, Zisterer DM. 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 2003;1639:43-52. (Pubitemid 37020953)
6. Greene LM, Fleeton M, Mulligan 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 2005;14:1357-1363
7. Mulligan JM, Greene LM, Cloonan S, et al. Identification of tubulin as the molecular target of proapoptotic pyrrolo-1,5-benzoxazepines. Mol Pharmacol 2006;70: 60-70. (Pubitemid 43920796)
8. Kavallaris M, Verrills NM, Hill BT. Anticancer therapy with novel tubulin-interacting drugs. Drug Resist Updat 2001;4:392-401. (Pubitemid 34746873)
9. Thomson AER, Robinson MA. Cytocidal action of colchicine in vitro on lymphocytes in chronic lymphocytic leukaemia. Lancet 1967;2:868-870
10. Wetherley-Mein G, Thomson AE, O'Connor TW, Peel WE, Singh AK. Colchicine ultrasensitivity of lymphocytes in chronic lymphocytic leukaemia. Br J Haematol 1983;54:111-120
11. Vilpo JA, Koski T, Vilpo LM. Selective toxicity of vincristine against chronic lymphocytic leukemia cells in vitro. Eur J Hematol 2000;65:370-378
12. Beswick RW, Ambrose HE, Wagner SD. Nocodazole, a microtubule depolymerising agent, induces apoptosis of chronic lymphocytic leukaemia cells associated with changes in Bcl-2 phosphorylation and expression. Leuk Res 2006;30:427-436
13. 2-M arrest in a chronic lymphocytic leukemia (CLL) cell line and apoptosis in primary CLL cells. Cancer Res 2002;62:5711-5719
14. Zhou Y, Hileman EO, Plunkett W, Keating MJ, Huang P. Free radical stress in chronic lymphocytic leukemia cells and its role in cellular sensitivity to ROS-generating anticancer agents. Blood 2003;101: 4098-4104 (Pubitemid 36857891)
15. Fernandez JA, Keshvara LM, Peters JD, et al. Phosphorylation- and activation-independent association of the tyrosine kinase Syk and the tyrosine kinase substrates Cbl and Vav with tubulin in B-cells. J Biol Chem 1999;274:1401-1406 (Pubitemid 129507727)
16. Lanham S, Hamblin T, Oscier D, et al. Differential signaling via surface IgM is associated with V-H gene mutational status and CD38 expression in chronic lymphocytic leukemia. Blood 2003;101:1087-1093 (Pubitemid 36139383)
17. Elder ME, Lin D, Clever J, et al. Human severe combined immunodeficiency due to a defect in ZAP-70, a T-cell tyrosine kinase. Science 1994;264:1596-1599 (Pubitemid 24227716)
18. Chen LG, Apgar J, Huynh L, et al. ZAP-70 directly enhances IgM signaling in chronic lymphocytic leukemia. Blood 2005;105:2036-2041 (Pubitemid 40731789)
19. Campiani G, Nacci V, Fiorini I, et al. Synthesis, biological activity, and SARs of pyrrolobenzoxazepine derivatives, a new class of specific "peripheral-type" benzodiazepine receptor ligands. J Med Chem 1996;39: 3435-3450
20. McGee MM, Gemma S, Butini S, et al. Pyrrolo[1,5] benzoxa(thia)zepines as a new class of potent apoptotic agents. Biological studies and identification of an intracellular location of their drug target. J Med Chem 2005; 48:4367-4377
21. Hayat A, O'Brien D, O'Rourke P, et al. CD38 expression level and pattern of expression remains a reliable and robust marker of progressive disease in chronic lymphocytic leukemia. Leuk Lymphoma 2006;47: 2371-2379 (Pubitemid 44768432)
22. 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 (Pubitemid 36514707)
23. Myhrinder AL, Hellqvist E, Sidorova E, et al. A new perspective: molecular motifs on oxidized LDL, apoptotic cells, and bacteria are targets for chronic lymphocytic leukemia antibodies. Blood 2008;111:3838-3848
24. Vermes I , Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995;184:39-51.
25. McGee MM, Campiani G, Ramunno A, et al. Pyrrolo-1, 5-benzoxazepines induce apoptosis in chronicmyelogenous leukemia (CML) cells by bypassing the apoptotic suppressor bcr-abl. J Pharmacol Exp Ther 2001;296:31-40. (Pubitemid 32015057)
26. Greene LM, Campiani G, Lawler M, Williams DC, Zisterer DM. BubR1 is required for a sustained mitotic spindle checkpoint arrest in human cancer cells treated with tubulin-targeting pyrrolo-1,5-benzoxazepines. Mol Pharmacol 2008;73:419-430 (Pubitemid 351159212)
27. Verma NK, Dempsey E, Conroy J, et al. A new microtubule-targeting compound PBOX-15 inhibits T-cell migration via post-translational modifications of tubulin. J Mol Med 2008;86:457-469
28. Pessina A, Malerba F, Gribaldo L. Hematotoxicity testing by cell clonogenic assay in drug development and preclinical trials. Curr Pharm Des 2005;11: 1055-1065 (Pubitemid 40331306)
29. Gandhi V, Kemena A, Keating MJ, Plunkett W. Cellular pharmacology of fludarabine triphosphate in chronic lymphocytic-leukemia cells during fludarabine therapy. Leuk Lymphoma 1993;10:49-56. (Pubitemid 23239858)
30. Dohner H, Fischer K, Bentz M, et al. P53 gene deletion predicts for poor survival and nonresponse to therapy with purine analogs in chronic B-cell leukemias. Blood 1995;85:1580-1589
31. Turgut B, Vural O, Pala FS, et al. 17p deletion is associated with resistance of B-cell chronic lymphocytic leukemia cells to in vitro fludarabine-induced apoptosis. Leuk Lymphoma 2007;48:311-320 (Pubitemid 46994881)
32. McGee MM, Greene LM, Ledwidge S, et al. Selective induction of apoptosis by the pyrrolo-1,5-benzoxazepine 7-[dimethylcarbamoyl]oxy]-6-(2-naphthyl) pyrrolo-[2,1-d] (1,5)-benzoxazepine (PBOX-6) in leukemia cells occurs via the c-Jun NH2-terminal kinase-dependent phosphorylation and inactivation of Bcl-2 and Bcl-XL. J Pharmacol Exp Ther 2004;310:1084-1095
33. Ruvolo PP, Deng X, May WS. Phosphorylation of Bcl2 and regulation of apoptosis. Leukemia 2001;15: 515-522
34. Thomas A, Pepper C, Hoy T, Bentley P. Bryostatin induces protein kinase Cmod ulation, Mcl-1 upregulation and phosphorylation of Bcl-2 resulting in cellular differentiation and resistance to drug-induced apoptosis in B-cell chronic lymphocytic leukemia cells. Leuk Lymphoma 2004;45:997-1008.
35. Poggi A, Catellani S, Bruzzone A, et al. Lack of the leukocyte-associated Ig-like receptor-1 expression in high-risk chronic lymphocytic leukaemia results in the absence of a negative signal regulating kinase activation and cell division. Leukemia 2008;22:980-988 (Pubitemid 351689880)
36. McGee MM, Campiani G, Ramunno A, et al. Activation of the c-Jun N-terminal kinase (JNK) signaling pathway is essential during PBOX-6-induced apoptosis in chronic myelogenous leukemia (CML) cells. J Biol Chem 2002;277:18383-18389 (Pubitemid 34952383)
37. Mirzapoiazova T, Kolosova IA, Moreno L, et al. Suppression of endotoxin-induced inflammation by Taxol. Eur Respir J 2007;30:429-435
38. Du LH, Lyle CS, Chambers TC. Characterization of vinblastine-induced Bcl-xL and Bcl-2 phosphorylation: evidence for a novel protein kinase and a coordinated phosphorylation/dephosphorylation cycle associated with apoptosis induction. Oncogene 2005;24:107-117
39. Romano C, De Fanis U, Sellitto A, et al. Induction of CD95 upregulation does not render chronic lymphocytic leukemia B-cells susceptible to CD95-mediated apoptosis. Immunol Lett 2005;97:131-139 (Pubitemid 40038864)
40. Secchiero P, Tiribelli M, Barbarotto E, et al. Aberrant expression of TRAIL in B chronic lymphocytic leukemia (B-CLL) cells. J Cell Physiol 2005;205:246-252 (Pubitemid 41428907)
41. Kang J, Kisenge RR, Toyoda H, et al. Chemical sensitization and regulation of TRAIL-induced apoptosis in a panel of B-lymphocytic leukaemia cell lines. Br J Hematol 2003;123:921-932 (Pubitemid 37533305)
42. Lagneaux L, Gillet N, Stamatopoulos B, et al. Valproic acid induces apoptosis in chronic lymphocytic leukemia cells through activation of the death receptor pathway and potentiates TRAIL response. Exp Hematol 2007;35: 1527-1537 (Pubitemid 47419135)
43. Genini D, Adachi S, Chao Q, et al. Deoxyadenosine analogs induce programmed cell death in chronic lymphocytic leukemia cells by damaging the DNA and by directly affecting the mitochondria. Blood 2000;96: 3537-3543 (Pubitemid 30836336)
44. Byrd JC, Kitada S, Flinn IW, et al. The mechanism of tumor cell clearance by rituximab in vivo in patients with B-cell chronic lymphocytic leukemia: evidence of caspase activation and apoptosis induction. Blood 2002;99:1038-1043 (Pubitemid 34525569)
45. Kipps TJ. The B-cell receptor and ZAP-70 in chronic lymphocytic leukemia. Best Pract Res Clin Hematol 2007;20:415-424 (Pubitemid 47263408)
46. Petlickovski A, Laurenti L, Li XP, et al. Sustained signaling through the B-cell receptor induces Mcl-1 and promotes survival of chronic lymphocytic leukemia B cells. Blood 2005;105:4820-4827 (Pubitemid 40807309)
47. Niiro H, Clark EA. Regulation of B-cell fate by antigen-receptor signals. Nat Rev Immunol 2002;2: 945-956 (Pubitemid 37323215)