Inhibition of late-stage autophagy synergistically enhances pyrrolo-1,5-benzoxazepine-6-induced apoptotic cell death in human colon cancer cells

International Journal of Oncology

Volumn 43, Issue 3, 2013, Pages 927-935

  Greene, Lisa M ^a   Nolan, Derek P ^a   Regan Komito, Daniel ^a   Campiani, Giuseppe ^b   Williams, D Clive ^a   Zisterer, Daniela M ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b European Research Centre for Drug Discovery and Development   (Italy)

Author keywords

Pyrrolo 1,5 benzoxazepines autophagy apoptosis

Indexed keywords

BAFILOMYCIN A1; DIBENZOXAZEPINE DERIVATIVE; PROTEIN MCL 1; PYRROLO 1,5 BENZOXAZEPINE 6; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER CHEMOTHERAPY; CELL PROTECTION; CELL SURVIVAL; COLON CANCER; CONTROLLED STUDY; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT RESPONSE;

ADENOCARCINOMA; ANIMALS; APOPTOSIS; AUTOPHAGY; CASPASES; CELL LINE, TUMOR; CELL SURVIVAL; COLONIC NEOPLASMS; DRUG SYNERGISM; HUMANS; LYSOSOMES; MACROLIDES; MICE; MICROTUBULE-ASSOCIATED PROTEINS; OXAZEPINES; PYRROLES;

EID: 84880602546     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.1989     Document Type: Article

References (52)

1. Campiani G, Nacci V, Fiorini I, De Filippis MP, Garofalo A, Ciani SM, Greco G, Novellino E, Williams DC, Zisterer DM, et al: Synthesis, biological activity, and SARs of pyrrolobenzoxazepine derivatives, a new class of specific 'peripheral-type' benzodiazepine receptor ligands. J Med Chem 39: 3435-3450, 1996.
2. Zisterer DM, McGee MM, Campiani G, Ramunno A, Fattorusso C, Nacci V, Lawler M and Williams DC: Pyrrolo-1,5-benzoxazepines: a new class of apoptotic agents. Biochem Soc Trans 29: 704-706, 2001.
3. Mulligan JM, Greene LM, Cloonan S, McGee MM, Onnis V, Campiani G, Fattorusso C, Lawler M, Williams DC and Zisterer DM: Identification of tubulin as the molecular target of proapoptotic pyrrolo-1,5-benzoxazepines. Mol Pharmacol 70: 60-70, 2006.
4. McGee MM, Greene LM, Ledwidge S, Campiani G, Nacci V, Lawler M, Williams DC and Zisterer DM: 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 310: 1084-1095, 2004.
5. Greene LM, Fleeton M, Mulligan J, Gowda C, Sheahan BJ, Atkins GJ, Campiani G, Nacci V, Lawler M, Williams DC, 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: 1357-1363, 2005.
6. Greene LM, Campiani G, Lawler M, Williams DC and 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 73: 419-430, 2008.
7. Nathwani SM, Butler S, Fayne D, McGovern NN, Sarkadi B, Meegan MJ, Lloyd DG, Campiani G, Lawler M, Williams DC, et al: Novel microtubule-targeting agents, pyrrolo-1,5-benzoxazepines, induce apoptosis in multi-drug-resistant cancer cells. Cancer Chemother Pharmacol 66: 585-596, 2010.
8. McElligott AM, Maginn EN, Greene LM, McGuckin S, Hayat A, Browne PV, Butini S, Campiani G, Catherwood MA, Vandenberghe E, et al: The novel tubulin-targeting agent pyrrolo-1,5-benzoxazepine-15 induces apoptosis in poor prognostic subgroups of chronic lymphocytic leukemia. Cancer Res 69: 8366-8375, 2009.
9. Bright SA, McElligott AM, O'Connell JW, O'Connor L, Carroll P, Campiani G, Deininger MW, Conneally E, Lawler M, Williams DC, et al: Novel pyrrolo-1,5-benzoxazepine compounds display significant activity against resistant chronic myeloid leukaemia cells in vitro, in ex vivo patient samples and in vivo. Br J Cancer 102: 1474-1482, 2010.
10. Nathwani SM, Butler S, Meegan MJ, Campiani G, Lawler M, Williams DC and Zisterer DM: Dual targeting of tumour cells and host endothelial cells by novel microtubule-targeting agents, pyrrolo-1,5-benzoxazepines. Cancer Chemother Pharmacol 65: 289-300, 2010.
11. Sato K, Tsuchihara K, Fujii S, Sugiyama M, Goya T, Atomi Y, Ueno T, Ochiai A and Esumi H: Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res 67: 9677-9684, 2007.
12. Wu YC, Wang XJ, Yu L, Chan FK, Cheng AS, Yu J, Sung JJ, Wu WK and Cho CH: Hydrogen sulfide lowers proliferation and induces protective autophagy in colon epithelial cells. PLoS One 7: e37572, 2012.
13. Li J, Hou N, Faried A, Tsutsumi S and Kuwano H: Inhibition of autophagy augments 5-fluorouracil chemotherapy in human colon cancer in vitro and in vivo model. Eur J Cancer 46: 1900-1909, 2010.
14. Li DD, Sun T, Wu XQ, Chen SP, Deng R, Jiang S, Feng GK, Pan JX, Zhang XS, Zeng YX, et al: The inhibition of autophagy sensitises colon cancer cells with wild-type p53 but not mutant p53 to topotecan treatment. PLoS One 7: e45058, 2012.
15. Paillas S, Causse A, Marzi L, de Medina P, Poirot M, Denis V, Vezzio-Vie N, Espert L, Arzouk H, Coquelle A, et al: MAPK14/p38alpha confers irinotecan resistance to TP53-defective cells by inducing survival autophagy. Autophagy 8: 1098-1112, 2012.
16. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, et al: Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 90: 1383-1435, 2010.
17. Han W, Sun J, Feng L, Wang K, Li D, Pan Q, Chen Y, Jin W, Wang X, Pan H, et al: Autophagy inhibition enhances daunorubicin-induced apoptosis in K562 cells. PLoS One 6: e28491, 2011.
18. Shen S, Kepp O and Kroemer G: The end of autophagic cell death? Autophagy 8: 1-3, 2012.
19. Greene LM, O'Boyle NM, Nolan DP, Meegan MJ and Zisterer DM: The vascular targeting agent Combretastatin-A4 directly induces autophagy in adenocarcinoma-derived colon cancer cells. Biochem Pharmacol 84: 612-624, 2012.
20. Cook KL, Shajahan AN and Clarke R: Autophagy and endocrine resistance in breast cancer. Expert Rev Anticancer Ther 11: 1283-1294, 2011.
21. Zois CE and Koukourakis MI: Radiation-induced autophagy in normal and cancer cells: towards novel cytoprotection and radio-sensitization policies? Autophagy 5: 442-450, 2009.
22. Clarke PG and Puyal J: Autophagic cell death exists. Autophagy 8: 867-869, 2012.
23. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, et al: Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25: 1025-1040, 2005.
24. Wu YC, Wu WK, Li Y, Yu L, Li ZJ, Wong CC, Li HT, Sung JJ and Cho CH: Inhibition of macroautophagy by bafilomycin A1 lowers proliferation and induces apoptosis in colon cancer cells. Biochem Biophys Res Commun 382: 451-456, 2009.
25. Bing L, Dejuan K, Yang L, Nan L, Mengzi H, Shumei M and Xiaodong L: Autophagy inhibition plays the synergetic killing roles with radiation in the multi-drug resistant SKVCR ovarian cancer cells. Radiat Oncol 7: 213, 2012.
26. Zhu S, Cao L, Yu Y, Yang L, Yang M, Liu K, Huang J, Kang R, Livesey KM and Tang D: Inhibiting autophagy potentiates the anticancer activity of IFNα in chronic myeloid leukemia cells. Autophagy 9: 317-327, 2012.
27. Swampillai AL, Salomoni P and Short SC: The role of autophagy in clinical practice. Clin Oncol (R Coll Radiol) 24: 387-395, 2012.
28. Garcia-Echeverria C and Sellers WR: Drug discovery approaches targeting the PI3K/Akt pathway in cancer. Oncogene 27: 5511-5526, 2008.
29. Cerniglia GJ, Karar J, Tyagi S, Christofidou-Solomidou M, Rengan R, Koumenis C and Maity A: Inhibition of autophagy as a strategy to augment radiosensitization by the dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor NVP-BEZ235. Mol Pharmacol 82: 1230-1240, 2012.
30. Yang ZJ, Chee CE, Huang S and Sinicrope FA: The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther 10: 1533-1541, 2011.
31. Maycotte P and Thorburn A: Autophagy and cancer therapy. Cancer Biol Ther 11: 127-137, 2011.
32. Nakatogawa H, Suzuki K, Kamada Y and Ohsumi Y: Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10: 458-467, 2009.
33. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R and Tashiro Y: Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23: 33-42, 1998.
34. Jahreiss L, Menzies FM and Rubinsztein DC: The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9: 574-587, 2008.
35. Klionsky DJ, Elazar Z, Seglen PO and Rubinsztein DC: Does bafilomycin A1 block the fusion of autophagosomes with lysosomes? Autophagy 4: 849-950, 2008.
36. Maginn EN, Browne PV, Hayden P, Vandenberghe E, MacDonagh B, Evans P, Goodyer M, Tewari P, Campiani G, Butini S, et al: PBOX-15, a novel microtubule targeting agent, induces apoptosis, upregulates death receptors, and potentiates TRAIL-mediated apoptosis in multiple myeloma cells. Br J Cancer 104: 281-289, 2011.
37. Greene LM, Kelly L, Onnis V, Campiani G, Lawler M, Williams DC and Zisterer DM: STI-571 (imatinib mesylate) enhances the apoptotic efficacy of pyrrolo-1,5-benzoxazepine-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: 288-297, 2007.
38. Bright SA, Greene LM, Greene TF, Campiani G, Butini S, Brindisi M, Lawler M, Meegan MJ, Williams DC and Zisterer DM: The novel pyrrolo-1, 5-benzoxazepine, PBOX-21, potentiates the apoptotic efficacy of STI571 (imatinib mesylate) in human chronic myeloid leukaemia cells. Biochem Pharmacol 77: 310-321, 2009.
39. Bright SA, Campiani G, Deininger MW, Lawler M, Williams DC and Zisterer DM: Sequential treatment with flavopiridol synergistically enhances pyrrolo-1,5-benzoxazepine-induced apoptosis in human chronic myeloid leukaemia cells including those resistant to imatinib treatment. Biochem Pharmacol 80: 31-38, 2010.
40. Nathwani SM, Cloonan SM, Stronach M, Campiani G, Lawler M, Williams DC and Zisterer DM: Novel microtubule-targeting agents, pyrrolo-1,5-benzoxazepines, induce cell cycle arrest and apoptosis in prostate cancer cells. Oncol Rep 24: 1499-1507, 2010.
41. Forde JC, Maginn EN, McNamara G, Martin LM, Campiani G, Williams DC, Zisterer D, McElligott AM, Lawler M, Lynch TH, et al: Microtubule-targeting- compound PBOX-15 radiosensitizes cancer cells in vitro. Cancer Biol Ther 11: 421-428, 2011.
42. Kimura T, Takabatake Y, Takahashi A and Isaka Y: Chloroquine in cancer therapy: a double-edged sword of autophagy. Cancer Res 73: 3-7, 2013.
43. Trmcic MV, Matovic RV, Tovilovic GI, Ristic BZ, Trajkovic VS, Ferjancic ZB and Saicic RN: A novel C,D-spirolactone analogue of paclitaxel: autophagy instead of apoptosis as a previously unknown mechanism of cytotoxic action for taxoids. Org Biomol Chem 25: 4933-4942, 2012.
44. Kanematsu S, Uehara N, Miki H, Yoshizawa K, Kawanaka A, Yuri T and Tsubura A: Autophagy inhibition enhances sulforaphane-induced apoptosis in human breast cancer cells. Anticancer Res 30: 3381-3390, 2010.
45. Sasazawa Y, Futamura Y, Tashiro E and Imoto M: Vacuolar H+-ATPase inhibitors overcome Bcl-xL-mediated chemoresistance through restoration of a caspase-independent apoptotic pathway. Cancer Sci 100: 1460-1467, 2009.
46. Hettiarachchi KD, Zimmet PZ and Myers MA: The plecomacrolide vacuolar-ATPase inhibitor bafilomycin, alters insulin signaling in MIN6 beta-cells. Cell Biol Toxicol 22: 169-181, 2006.
47. Pliyev BK and Menshikov M: Differential effects of the autophagy inhibitors 3-methyladenine and chloroquine on spontaneous and TNF-alpha-induced neutrophil apoptosis. Apoptosis 17: 1050-1065, 2012.
48. Rubinstein AD, Eisenstein M, Ber Y, Bialik S and Kimchi A: The autophagy protein Atg12 associates with antiapoptotic Bcl-2 family members to promote mitochondrial apoptosis. Mol Cell 44: 698-709, 2011.
49. Luo S and Rubinsztein DC: BCL2L11/BIM: A novel molecular link between autophagy and apoptosis. Autophagy 9: 104-105, 2013.
50. Huynh KK, Eskelinen EL, Scott CC, Malevanets A, Saftig P and Grinstein S: LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J 26: 313-324, 2007.
51. Kundra R and Kornfeld S: Asparagine-linked oligosaccharides protect Lamp-1 and Lamp-2 from intracellular proteolysis. J Biol Chem 274: 31039-31046, 1999.
52. Yogalingam G and Pendergast AM: Abl kinases regulate autophagy by promoting the trafficking and function of lysosomal components. J Biol Chem 283: 35941-35953, 2008.