PBOX-15 induces apoptosis and improves the efficacy of oxaliplatin in human colorectal cancer cell lines

European Journal of Pharmacology

Volumn 714, Issue 1-3, 2013, Pages 379-387

  Gangemi, Giuseppina ^a   Gazzerro, Patrizia ^a   Fiore, Donatella ^a   Proto, Maria Chiara ^a   Butini, Stefania ^b   Gemma, Sandra ^b   Casagni, Alice ^b   Laezza, Chiara ^c   Vitale, Mario ^e   Ligresti, Alessia ^c   Di Marzo, Vincenzo ^c   Zisterer, Daniela M ^d   Nathwani, Seema ^d   Williams, D Clive ^d   Campiani, Giuseppe ^b   Bifulco, Maurizio ^e  

^a UNIVERSITY OF SALERNO   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

^c CNR   (Italy)

^d TRINITY COLLEGE DUBLIN   (Ireland)

^e UNIVERSITY OF SALERNO   (Italy)

Author keywords

Colorectal cancer; Combinatorial effect; FAAH inhibitor; Pyrrolo 1,5 benzoxazepine

Indexed keywords

EID: 84885480286     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.07.011     Document Type: Article

References (34)

1. Alberts, S.R., Horvath, W.L, Sternfeld, W.C, Goldberg, R.M., Mahoney, M.R., Dakhil, S.R., Levitt, R., Rowland, K., Nair, S., Sargent, D.J., Donohue, J.H., 2005. Oxaliplatin, fluorouracil, and leucovorin for patients with unresectable liver-only metastases from colorectal cancer: a North Central Cancer Treatment Group Phase II Study. J Clin Oncol. 23, 9243-9249.
2. André, T., Boni, C, Mounedji-Boudiaf, L., Navarro, M., Tabernero, J., Hickish, T., Topham, C, Zaninelli, M., Clingan, P., Bridgewater, J., Tabah-Fisch, I., de Gramont, A., 2004. Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N. Engl. J. Med. 350, 2343-2351. (Pubitemid 38702845)
3. Bifulco, M., Di Marzo, V., 2002. Targeting the endocannabinoid system in cancer therapy: a call for further research. Nat. Med. 8, 547-550. (Pubitemid 34633419)
4. Bifulco, M., Laezza, C, Valenti, M., Ligresti, A., Portella, G., DI Marzo, V., 2004. A new strategy to block tumor growth by inhibiting endocannabinoid inactivation. FASEB J. 18, 1606-1608. (Pubitemid 39561648)
5. Bisogno, T., De Petrocellis, L., Di Marzo, V., 2002. Fatty acid amide hydrolase, an enzyme with many bioactive substrates. Possible therapeutic implications. Curr. Pharm. Des. 8, 533-547. (Pubitemid 34449864)
6. Bright, S.A., McElligott, A.M., O'Connell, J.W., O'Connor, L, Carroll, P., Campiani, G., Deininger, M.W, Conneally, E., Lawler, M., Williams, D.C, Zisterer, D.M., 2010. 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.
7. Campiani, G., Nacci, V., Fiorini, I., De Filippis, M.P., Garofalo, A., Ciani, S.M., Greco, G., Novellino, E., Williams, D.C, Zisterer, D.M., Woods, M.J., Mihai, C, Manzoni, C, Mennini, T, 1996. Synthesis, biological activity, and SARs of pyrrolobenzox-azepine derivatives, a new class of specific "peripheral-type," benzodiazepine receptor ligands. J. Med. Chem. 39, 3435-3450. (Pubitemid 26307848)
8. Cassidy, J., Tabernero, J., Twelves, C, Brunet, R., Butts, C, Conroy, T., Debraud, F., Figer, A., Grossmann, J., Sawada, N., Schöffski, P., Sobrero, A., Van Cutsem, E., Díaz-Rubio, E., 2004. XELOX (capecitabine plus oxaliplatin): active first-line therapy for patients with metastatic colorectal cancer. J. Clin. Oncol. 22, 2084-2091. (Pubitemid 41095141)
9. Chou, T.C., Talalay, P., 1984. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 22, 27-55.
10. Cravatt, B.F., Demarest, K., Patricelli, M.P., Bracey, M.H., Giang, D.K., Martin, B.R., Lichtman, A.H., 2001. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. USA. 98, 9371-9376. (Pubitemid 32743923)
11. Elowe, S., Hümmer, S., Uldschmid, A., Li, X., Nigg, E.A., 2007. Tensionsensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev. 21, 2205-2219. (Pubitemid 47360842)
12. Goldberg, R.M., Sargent, D.J., Morton, R.F., Fuchs, CS., Ramanathan, R.K., Williamson, S.K., Findlay, B.P., Pitot, H.C, Alberts, S.R., 2004. A randomized controlled trial of fluorouracil plus leucovorin, irinotecan, and oxaliplatin combinations in patients with previously untreated metastatic colorectal cancer. J. Clin. Oncol. 22, 23-30. (Pubitemid 41095110)
13. Greene, L.M., Campiani, G., Lawler, M., Williams, D.C., Zisterer, D.M., 2008. 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. (Pubitemid 351159212)
14. Ho, W.-S.V., Hillard, C.J., 2005. Cannabinoids. In: Pertwee (Ed.), Handbook of Experimental Pharmacology. Springer-Verlag, Heidelberg, Germany, p. 187.
15. Izzo, A.A., Aviello, G., Petrosino, S., Orlando, P., Marsicano, G., Lutz, B., Borrelli, F., Capasso, R., Nigam, S., Capasso, F., Di Marzo, V., 2008. Endocannabinoid Research Group, 2008. Increased endocannabinoid levels reduce the development of precancerous lesions in the mouse colon. J. Mol. Med. (Berl) 86, 89-98.
16. Jänicke, R.U., Sprengart, M.L., Wati, M.R., Porter, A.G., 1998. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273, 9357-9360. (Pubitemid 28183012)
17. Ligresti, A., Bisogno, T., Matias, I., De Petrocellis, L., Cascio, M.G., Cosenza, V., D'argenio, G., Scaglione, G., Bifulco, M., Sorrentini, I., Di Marzo, V., 2003. Possible endocannabinoid control of colorectal cancer growth. Gastroenterology 125, 677-687. (Pubitemid 37070686)
18. Lysaght, J., Verma, N.K., Maginn, E.N., Ryan, J.M., Campiani, G., Zisterer, D.M., Williams, D.C., Browne, P.V., Lawler, M.P., McElligott, A.M., 2013. The micro-tubule targeting agent PBOX-15 inhibits integrin-mediated cell adhesion and induces apoptosis in acute lymphoblastic leukaemia cells. Int. J. Oncol. 42, 239-246.
19. Maginn, E.N., Browne, P.V., Hayden, P., Vandenberghe, E., MacDonagh, B., Evans, P., Goodyer, M., Tewari, P, Campiani, G., Butini, S., Williams, D.C., Zisterer, D.M., Lawler, M.P., McElligott, A.M., 2011. 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.
20. Malfitano, A.M., Ciaglia, E., Gangemi, G., Gazzerro, P., Laezza, C., Bifulco, M., 2011. Update on the endocannabinoid system as an anticancer target. Expert Opinion Ther. Targets 15 (3), 297-308.
21. McElligott, A.M., Maginn, E.N., Greene, L.M., McGuckin, S., Hayat, A., Browne, P.V., Butini, S., Campiani, G., Catherwood, M.A., Vandenberghe, E., Williams, D.C., Zisterer, D.M., Lawler, M., 2009. 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.
22. Meyerhardt, J.A., Mayer, R.J., 2005. Systemic therapy for colorectal cancer. N. Engl. J. Med. 352, 476-487.
23. Mulligan, J.M., Greene, L.M., Cloonan, S., McGee, M.M., Onnis, V., Campiani, G., Fattorusso, C., Lawler, M., Williams, D.C., Zisterer, D.M., 2006. Identification of tubulin as the molecular target of proapoptotic pyrrolo-1,5-benzoxazepines. Mol. Pharmacol. 70, 60-70.
24. Nathwani, S.M., Butler, S., Fayne, D., McGovern, N.N., Sarkadi, B., Meegan, M.J., Lloyd, D.G., Campiani, G., Lawler, M., Williams, D.C., Zisterer, D.M., 2009. Novel microtubule-targeting agents, pyrrolo-1,5-benzoxazepines, induce apoptosis in multi-drug-resistant cancer cells. Cancer Chemother. Pharmacol. 66, 585-596.
25. 1 receptor in human colon cancer cell lines. Scand. J. Gastroenterol. 43, 66-72.
26. Parsels, L.A., Qian, Y., Tanska, D.M., Gross, M., Zhao, L., Hassan, M.C., Arumugarajah, S., Parsels, J.D., Hylander-Gans, L., Simeone, D.M., Morosini, D., Brown, J.L., Zabludoff, S.D., Maybaum, J., Lawrence, T.S., Morgan, M.A., 2011. Assessment of Chk1 phosphorylation as a pharmacodynamic biomarker of Chk1 inhibition. Clin. Cancer Res. 17, 3706-3715.
27. Proto, M.C., Gazzerro, P., Di Croce, L., Santoro, A., Malfitano, A.M., Pisanti, S., Laezza, C., Bifulco, M., 2012. Interaction of endocannabinoid system and steroid hormones in the control of colon cancer cell growth. J. Cell Physiol. 227, 250-258.
28. Slattery, M.L., Anderson, K., Curtin, K., Ma, K., Schaffer, D., Edwards, S., Samowitz, W., 2001. Lifestyle factors and Ki-ras mutations in colon cancer tumors. Mutat. Res. 483, 73-81. (Pubitemid 33000068)
29. Takahashi, N., Li, W., Banerjee, D., Guan, Y., Wada-Takahashi, Y., Brennan, M.F., Chou, T.C., Scotto, K.W., Bertino, J.R., 2002. Sequence dependent synergistic cytotoxicity of ecteinascidin-743 and paclitaxel in human breast cancer cell lines in vitro and in vivo. Cancer Res. 62, 6909-6915. (Pubitemid 35424080)
30. Talos, F., Moll, U.M., 2010. Role of the p53 family in stabilizing the genome and preventing polyploidization. Adv. Exp. Med. Biol. 676, 73-91.
31. Verma, N.K., Dempsey, E., Conroy, J., Olwell, P., Mcelligott, A.M., Davies, A.M., Kelleher, D., Butini, S., Campiani, G., Williams, D.C., Zisterer, D.M., Lawler, M., Volkov, Y., 2008. A new microtubule-targeting compound PBOX-15 inhibits T-cell migration via post-translational modifications of tubulin. J. Mol. Med. (Berl) 86, 457-469.
32. Wada-Hiraike, O., Warner, M., Gustafsson, J.A., 2006. New developments in oestrogen signalling in colonic epithelium. Biochem. Soc. Trans. 34, 1114-1116. (Pubitemid 46772912)
33. Zachos, G., Black, E.J., Walker, M., Scott, M.T., Vagnarelli, P., Earnshaw, W.C., Gillespie, D.A., 2007. Chk1 is required for spindle checkpoint function. Dev. Cell 12, 247-260. (Pubitemid 46193970)
34. Zhang, N., Yin, Y., Xu, S.J., Chen, W.S., 2008. 5-Fluorouracil: mechanisms of resistance and reversal strategies. Molecules 13, 1551-1569.