Cannabinoid-associated cell death mechanisms in tumor models (review)

International Journal of Oncology

Volumn 41, Issue 2, 2012, Pages 407-413

  Calvaruso, Giuseppe ^a   Pellerito, Ornella ^a   Notaro, Antonietta ^a   Giuliano, Michela ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

Apoptosis; Autophagy; Cannabinoids; Synergistic effects

Indexed keywords

2 ARACHYDONOYL GLYCEROL; 2 METHYL 3 (1 NAPHTHOYL) 1 PROPYLINDOLE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ANANDAMIDE; CANNABIDIOL; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; CERAMIDE; DEXANABINOL; DRONABINOL; FLUOROURACIL; GEMCITABINE; GPR 55; HU 331; METHANANDAMIDE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; TEMOZOLOMIDE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AUTOPHAGY; CANCER CELL; CANCER INHIBITION; CANCER THERAPY; CELL CYCLE ARREST; CELL DEATH; CELL SURVIVAL; COLORECTAL CARCINOMA; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG MECHANISM; DRUG POTENTIATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GLIOBLASTOMA; GLIOMA; LIPID RAFT; LIVER CELL CARCINOMA; LUNG ADENOCARCINOMA; OSTEOSARCOMA; OXIDATIVE STRESS; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; CANNABINOIDS; DRUG SYNERGISM; HUMANS; NEOPLASMS;

EID: 84863576915     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2012.1476     Document Type: Review

References (60)

1. Weinberg RA: The molecular basis of oncogenes and tumor suppressor genes. Ann NY Acad Sci 758: 331-338, 1995.
2. Yuspa SH, Długosz AA, Cheng CK, Denning MF, Tennenbaum T, Glick AB and Weinberg WC: Role of oncogenes and tumor suppressor genes in multistage carcinogenesis. J Invest Dermatol 103: S90-S95, 1994.
3. Lowe SW and Lin AW: Apoptosis in cancer. Carcinogenesis 21: 485-495, 2000. (Pubitemid 30137934)
4. Brown JM and Attardi LD: The role of apoptosis in cancer development and treatment response. Nat Rev Cancer 5: 231-237, 2005. (Pubitemid 40314954)
5. Brown JM and Wilson G: Apoptosis genes and resistance to cancer therapy: what does the experimental and clinical data tell us? Cancer Biol Ther 2: 477-490, 2003.
6. Tsatsanis C and Spandidos DA: Oncogenic kinases signaling in human neoplasms. Ann NY Acad Sci 1028: 168-175, 2004. (Pubitemid 40361821)
7. Degterev A, Boyce M and Yuan J: A decade of caspases. Oncogene 22: 8543-8567, 2003. (Pubitemid 38028527)
8. Peter ME and Krammer PH: The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 10: 26-35, 2003. (Pubitemid 36511830)
9. Green DR and Kroemer G: The pathophysiology of mitochondrial cell death. Science 305: 626-629, 2004. (Pubitemid 39006738)
10. Fassetta M, D'Alessandro L, Coltella N, Di Renzo MF and Rasola A: Hepatocyte growth factor installs a survival platform for colorectal cancer cell invasive growth and overcomes p38 MAPK-mediated apoptosis. Cell Signal 18: 1967-1976, 2006. (Pubitemid 44485988)
11. Altieri DC: Survivin and IAP proteins in cell-death mechanisms. Biochem J 430: 199-205, 2010.
12. Tokunaga E, Oki E, Egashira A, Sadanaga N, Morita M, Kakeji Y and Maehara Y: Deregulation of the AKT pathway in human cancer. Curr Cancer Drug Targets 8: 27-36, 2008. (Pubitemid 351237907)
13. Mathew R: Role of autophagy in cancer. Nat Rev Cancer 7: 961-967, 2007.
14. Kimmelman AC: The dynamic nature of autophagy in cancer. Genes Dev 25: 1999-2010, 2011.
15. Krick R, Muehe Y, Prick T, Bremer S, Schlotterhose P, Eskelinen EL, Millen J, Goldfarb DS and Thumm M: Microautophagy of the nucleus requires the core macroautophagy genes. Mol Biol Cell 19: 4492-4505, 2008.
16. Farré JC and Subramani S: Peroxisome turnover by micropexophagy: an autophagy-related process Cell Biol 14: 515-523, 2004.
17. Periyasamy-Thandavan S, Jiang M, Schoenlein P and Dong Z: Autophagy: molecular machinery, regulation, and implications for renal pathophysiology. Am J Physiol Renal Physiol 297: F244-F256, 2009.
18. Mizushima N: The role of the Atg1/ULK1 complex in autophagy regulation. Curr Op Cell Biol 22: 132-139, 2010.
19. Sarbassov DD, Guertin DA, Ali SM and Sabatini DM: Phosphorylation and regulation of AKT/PKB by the rictor-mTOR complex. Science 307: 1098-1101, 2005. (Pubitemid 40262113)
20. Hardie D: AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8: 774-781, 2007.
21. Eisenberg-Lerner A and Kimchi A: The paradox of autophagy and its implication in cancer etiology and therapy. Apoptosis 14: 376-391, 2009.
22. Djavaheri-Mergny M, Maiuri MC and Kroemer G: Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin 1. Oncogene 29: 1717-1719, 2010.
23. Wong CH, Iskandar KB, Yadav SK Hirpara JL, Loh T and Pervaiz S: Simultaneous induction of non-canonical autophagy and apoptosis in cancer cells by ROS-dependent ERK and JNK activation. PLoS One 5: e9996, 2010.
24. Pertwee RG: Cannabinoid receptor ligands: clinical and neuropharmacological considerations, relevant to future drug discovery and development. Expt Op Invest Drugs 9: 1553-1571, 2000.
25. Guzmàn M: Cannabinoids: potential anticancer agents. Nat Rev Cancer 3: 745-755, 2003.
26. Freimuth N, Ramer R and Hinz B: Antitumorigenic effects of cannabinoids beyond apoptosis. J Pharmacol Exp Therapeutics 332: 336-344, 2010.
27. Munson AE, Harris LS, Friedman MA, Dewey WL and Carchman RA: Antineoplastic activity of cannabinoids. J Natl Cancer Inst 55: 597-602, 1975.
28. Demuth DG and Molleman A: Cannabinoid signalling. Life Sci 78: 549-563, 2006. (Pubitemid 41785760)
29. Herrera B, Carracedo A, Diez-Zaera M, Gómez del Pulgar T, Guzmán M and Velasco G: The CB2 cannabinoid receptor signals apoptosis via ceramide-dependent activation of the mitochondrial intrinsic pathway. Exp Cell Res 312: 2121-2131, 2006. (Pubitemid 43850936)
30. Bifulco M, Malfitano AM, Pisanti S and Laezza C: Endocannabinoids in endocrine and related tumours. Endocr Relat Cancer 15: 391-408, 2008. (Pubitemid 351880830)
31. Maccarrone M, Lorenzon T, Bari M, Melino G and Finazzi-Agro A: Anandamide induces apoptosis in human cells via vanilloid receptors. Evidence for a protective role of cannabinoid receptors. J Biol Chem 275: 31938-31945, 2000.
32. Yang Q, Liu HY, Zhang YW, Wu WJ and Tang WX: Anandamide induces cell death through lipid rafts in hepatic stellate cells. J Gastroenterol Hepatol 25: 991-1001, 2010.
33. Giuliano M, Pellerito O, Portanova P, Calvaruso G, Santulli A, De Blasio A, Vento R and Tesoriere G: Apoptosis induced in HepG2 cells by the synthetic cannabinoid WIN: involvement of the transcription factor PPARgamma. Biochimie 91: 457-465, 2009.
34. Scuderi MR, Cantarella G, Scollo M, Lempereur L, Palumbo M, Saccani-Jotti G and Bernardini R: The antimitogenic effect of the cannabinoid receptor agonist WIN55212-2 on human melanoma cells is mediated by the membrane lipid raft. Cancer Lett 310: 240-249, 2011.
35. Oddi S, Dainese E, Sandiford S, Fezza F, Lanuti M, Chiurchiù V, Totaro A, Catanzaro G, Barcaroli D, De Laurenzi V, et al: Palmitoylation of cysteine 415 of helix 8: effect on membrane localisation and signalling of the CB(1) cannabinoid receptor. Br J Pharmacol 165: 2635-2651, 2011.
36. Hu G, Ren G and Shi Y: The putative cannabinoid receptor GPR55 promotes cancer cell proliferation. Oncogene 30: 139-141, 2011.
37. Gustafsson K, Christensson B, Sander B and Flygare J: Cannabinoid receptor-mediated apoptosis induced by R(+)- methanandamide and Win55,212-2 is associated with ceramide accumulation and p38 activation in mantle cell lymphoma. Mol Pharmacol 70: 1612-1620, 2006.
38. Blazquez C, Carracedo A, Salazar M, Lorente M, Egia A, Gonzalez-Feria L, Haro A, Velasco G and Guzman M: Down-regulation of tissue inhibitor of metalloproteinases-1 in gliomas: a new marker of cannabinoid antitumoral activity? Neuropharmacology 54: 235-243, 2008. (Pubitemid 350299404)
39. Cianchi F, Papucci L, Schiavone N, Lulli M, Magnelli L, Vinci MC, Messerini L, Manera C, Ronconi E, Romagnani P, et al: Cannabinoid receptor activation induces apoptosis through tumor necrosis factor alpha-mediated ceramide de novo synthesis in colon cancer cells. Clin Cancer Res 14: 7691-7700, 2008.
40. Carracedo A, Gironella M, Lorente M, Garcia S, Guzman M, Velasco G and Iovanna JL: Cannabinoids induce apoptosis of pancreatic tumor cells via endoplasmic reticulum stress-related genes. Cancer Res 66: 6748-6755, 2006. (Pubitemid 44085633)
41. Olea-Herrero N, Vara D, Malagarie-Cazenave S and Díaz-Laviada I: The cannabinoid R+ methanandamide induces IL-6 secretion by prostate cancer PC3 cells. J Immunotoxicol 6: 249-256, 2009.
42. Giuliano M, Calvaruso G, Pellerito O, Portanova P, Carlisi D, Vento R and Tesoriere G: Anandamide-induced apoptosis in Chang liver cells involves ceramide and JNK/AP-1 pathway. Int J Mol Med 17: 811-819, 2006.
43. Massi P, Vaccani A, Bianchessi S, Costa B, Macchi P and Parolaro D: The non-psychoactive cannabidiol triggers caspase activation and oxidative stress in human glioma cells. Cell Mol Life Sci 63: 2057-2066, 2006. (Pubitemid 44359745)
44. McKallip RJ, Jia W, Schlomer J, Warren JW, Nagarkatti PS and Nagarkatti M: Cannabidiol-induced apoptosis in human leukemia cells: a novel role of cannabidiol in the regulation of p22phox and Nox4 expression. Mol Pharmacol 70: 897-908, 2006. (Pubitemid 44268447)
45. Malhotra JD and Kaufman RJ: Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9: 2277-2293, 2007. (Pubitemid 350059010)
46. Salazar M, Carracedo A, Salanueva IJ, Hernández-Tiedra S, Egia A, Lorente M, Vázquez P, Torres S, Iovanna JL, Guzmán M, et al: TRB3 links ER stress to autophagy in cannabinoid antitumoral action. Autophagy 5: 1048-1049, 2009.
47. Pellerito O, Calvaruso G, Portanova P, De Blasio A, Santulli A, Vento R, Tesoriere G and Giuliano M: The synthetic cannabinoid WIN 55,212-2 sensitizes hepatocellular carcinoma cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)- induced apoptosis by activating p8/CCAAT/enhancer binding protein homologous protein (CHOP)/death receptor 5 (DR5) axis. Mol Pharmacol 77: 854-863, 2010.
48. Galve-Roperh I, Sanchez C, Cortes ML, del Pulgar TG, Izquierdo M and Guzman M: Anti-tumoral action of cannabinoids: involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat Med 6: 313-319, 2000. (Pubitemid 30148624)
49. Luca T, Di Benedetto G, Scuderi MR, Palumbo M, Clementi S, Bernardini R and Cantarella G: The CB1/CB2 receptor agonist WIN-55,212-2 reduces viability of human Kaposi's sarcoma cells in vitro. Eur J Pharmacol 616: 16-21, 2009.
50. Park JM, Xian XS, Choi MG, Park H, Cho YK, Lee IS, Kim SW and Chung IS: Antiproliferative mechanism of a cannabinoid agonist by cell cycle arrest in human gastric cancer cells. J Cell Biochem 112: 1192-1205, 2011.
51. Piñeiro R, Maffucci T and Falasca M: The putative cannabinoid receptor GPR55 defines a novel autocrine loop in cancer cell proliferation. Oncogene 30: 142-152, 2011.
52. Hers I, Vincent EE and Tavaré JM: Akt signalling in health and disease. Cell Signal 23: 1515-1527, 2011.
53. Cudaback E, Marrs W, Moeller T and Stella N: The expression level of CB1 and CB2 receptors determines their efficacy at inducing apoptosis in astrocytomas. PLoS One 5: e8702, 2010.
54. Salazar M, Carracedo A, Salanueva IJ, Hernández-Tiedra S, Lorente M, Egia A, Vázquez P, Blázquez C, Torres S, García S, et al: Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Invest 119: 1359-1372, 2009.
55. Torres S, Lorente M, Rodríguez-Fornés F, Hernández-Tiedra S, Salazar M, García-Taboada E, Barcia J, Guzmán M and Velasco G: A combined preclinical therapy of cannabinoids and temozolomide against glioma. Mol Cancer Ther 10: 90-103, 2011.
56. Vara D, Salazar M, Olea-Herrero N, Guzmán M, Velasco G and Díaz-Laviada I: Anti-tumoral action of cannabinoids on hepatocellular carcinoma: role of AMPK-dependent activation of autophagy. Cell Death Differ 18: 1099-1111, 2011.
57. Shrivastava A, Kuzontkoski PM, Groopman JE and Prasad A: Cannabidiol induces programmed cell death in breast cancer cells by coordinating the cross-talk between apoptosis and autophagy. Mol Cancer Ther 10: 1161-1172, 2011.
58. Wasik AM, Almestrand S, Wang X, Hultenby K, Dackland ÅL, Andersson P, Kimby E, Christensson B and Sander B: WIN55,212-2 induces cytoplasmic vacuolation in apoptosis-resistant MCL cells. Cell Death Dis 2: e225, 2011.
59. Donadelli M, Dando I, Zaniboni T, Costanzo C, Dalla Pozza E, Scupoli MT, Scarpa A, Zappavigna S, Marra M, Abbruzzese A, et al: Gemcitabine/cannabinoid combination triggers autophagy in pancreatic cancer cells through a ROS-mediated mechanism. Cell Death Dis 2: e152, 2011.
60. Gustafsson SB, Lindgren T, Jonsson M and Jacobsson SO: Cannabinoid receptor-independent cytotoxic effects of cannabinoids in human colorectal carcinoma cells: synergism with 5-fluorouracil. Cancer Chemother Pharmacol 63: 691-701, 2009.