The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells

Cancer Cell

Volumn 9, Issue 4, 2006, Pages 301-312

  Carracedo, Arkaitz ^a   Lorente, Mar ^a   Egia, Ainara ^a   Blázquez, Cristina ^a   García, Stephane ^b   Giroux, Valentin ^b   Malicet, Cedric ^b   Villuendas, Raquel ^c   Gironella, Meritxell ^b   González Feria, Luis ^d   Piris, Miguel Ángel ^c   Iovanna, Juan L ^b   Guzmán, Manuel ^a   Velasco, Guillermo ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b INSERM   (France)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d Canary University Hospital Consortium   (Spain)

Author keywords

CELLCYCLE; DNA

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CANNABINOID; CERAMIDE; DRONABINOL; PROTEIN DERIVATIVE; STRESS REGULATED PROTEIN P8; TEMOZOLOMIDE; TRANSCRIPTION FACTOR; TRIBBLES HOMOLOG 3 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DRUG EFFECT; EMBRYO; ENDOPLASMIC RETICULUM; GENE ACTIVATION; GLIOBLASTOMA; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPOGENESIS; MEDIATOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR GROWTH; TUMOR RECURRENCE; TUMOR RESISTANCE; UPREGULATION;

ANIMALIA;

EID: 33645763253     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2006.03.005     Document Type: Article

References (47)

1. Benali-Furet N.L., Chami M., Houel L., De Giorgi F., Vernejoul F., Lagorce D., Buscail L., Bartenschlager R., Ichas F., Rizzuto R., et al. Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion. Oncogene 24 (2005) 4921-4933
2. Blazquez C., Casanova M.L., Planas A., Gómez del Pulgar T., Villanueva C., Fernandez-Acenero M.J., Aragones J., Huffman J.W., Jorcano J.L., and Guzman M. Inhibition of tumor angiogenesis by cannabinoids. FASEB J. 17 (2003) 529-531
3. Blazquez C., Gonzalez-Feria L., Alvarez L., Haro A., Casanova M.L., and Guzman M. Cannabinoids inhibit the vascular endothelial growth factor pathway in gliomas. Cancer Res. 64 (2004) 5617-5623
4. Casanova M.L., Blazquez C., Martinez-Palacio J., Villanueva C., Fernandez-Acenero M.J., Huffman J.W., Jorcano J.L., and Guzman M. Inhibition of skin tumor growth and angiogenesis in vivo by activation of cannabinoid receptors. J. Clin. Invest. 111 (2003) 43-50
5. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., and Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258 (1992) 1946-1949
6. Di Marzo V., Bifulco M., and De Petrocellis L. The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 3 (2004) 771-784
7. Emberley E.D., Niu Y., Curtis L., Troup S., Mandal S.K., Myers J.N., Gibson S.B., Murphy L.C., and Watson P.H. The S100A7-c-Jun activation domain binding protein 1 pathway enhances prosurvival pathways in breast cancer. Cancer Res. 65 (2005) 5696-5702
8. Galve-Roperh I., Sanchez C., Cortes M.L., Gómez del Pulgar T., Izquierdo M., and Guzman M. Anti-tumoral action of cannabinoids: involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat. Med. 6 (2000) 313-319
9. Gaoni Y., and Mechoulam R. Isolation, structure and partial synthesis of an active constituent of hashish. J. Am. Chem. Soc. 86 (1964) 1646-1647
10. Garcia-Montero A.C., Vasseur S., Giono L.E., Canepa E., Moreno S., Dagorn J.C., and Iovanna J.L. Transforming growth factor β-1 enhances Smad transcriptional activity through activation of p8 gene expression. Biochem. J. 357 (2001) 249-253
11. Gomez del Pulgar T., Velasco G., Sanchez C., Haro A., and Guzman M. De novo-synthesized ceramide is involved in cannabinoid-induced apoptosis. Biochem. J. 363 (2002) 183-188
12. Gomez del Pulgar T., De Ceballos M.L., Guzman M., and Velasco G. Cannabinoids protect astrocytes from ceramide-induced apoptosis through the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 277 (2002) 36527-36533
13. Gouaze V., Liu Y.Y., Prickett C.S., Yu J.Y., Giuliano A.E., and Cabot M.C. Glucosylceramide synthase blockade down-regulates P-glycoprotein and resensitizes multidrug-resistant breast cancer cells to anticancer drugs. Cancer Res. 65 (2005) 3861-3867
14. Guzman M. Cannabinoids: potential anticancer agents. Nat. Rev. Cancer 3 (2003) 745-755
15. Hoffmeister A., Ropolo A., Vasseur S., Mallo G.V., Bodeker H., Ritz-Laser B., Dressler G.R., Vaccaro M.I., Dagorn J.C., Moreno S., et al. The HMG-I/Y-related protein p8 binds to p300 and Pax2 trans-activation domain-interacting protein to regulate the trans-activation activity of the Pax2A and Pax2B transcription factors on the glucagon gene promoter. J. Biol. Chem. 277 (2002) 22314-22319
16. Howlett A.C., Barth F., Bonner T.I., Cabral G., Casellas P., Devane W.A., Felder C.C., Herkenham M., Mackie K., Martin B.R., et al. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol. Rev. 54 (2002) 161-202
17. Ito Y., Yoshida H., Motoo Y., Iovanna J.L., Nakamura Y., Kakudo K., Uruno T., Takamura Y., Miya A., Noguchi S., et al. Expression of p8 protein in breast carcinoma; an inverse relationship with apoptosis. Anticancer Res. 25 (2005) 833-837
18. Iynedjian P.B. Lack of evidence for a role of TRB3/NIPK as an inhibitor of PKB-mediated insulin signalling in primary hepatocytes. Biochem. J. 386 (2005) 113-118
19. Jiang X., Kim H.E., Shu H., Zhao Y., Zhang H., Kofron J., Donnelly J., Burns D., Ng S.C., Rosenberg S., et al. Distinctive roles of PHAP proteins and prothymosin-α in a death regulatory pathway. Science 299 (2003) 223-226
20. Jiang W.G., Davies G., and Fodstad O. Com-1/P8 in oestrogen regulated growth of breast cancer cells, the ER-β connection. Biochem. Biophys. Res. Commun. 330 (2005) 253-262
21. Jiang W.G., Watkins G., Douglas-Jones A., Mokbel K., Mansel R.E., and Fodstad O. Expression of Com-1/P8 in human breast cancer and its relevance to clinical outcome and ER status. Int. J. Cancer 117 (2005) 30-37
22. Li X.D., Lankinen H., Putkuri N., Vapalahti O., and Vaheri A. Tula hantavirus triggers pro-apoptotic signals of ER stress in Vero E6 cells. Virology 333 (2005) 180-189
23. Ma Y., and Hendershot L.M. The role of the unfolded protein response in tumour development: friend or foe?. Nat. Rev. Cancer 4 (2004) 966-977
24. Ma Y., Brewer J.W., Diehl J.A., and Hendershot L.M. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318 (2002) 1351-1365
25. Malicet C., Lesavre N., Vasseur S., and Iovanna J.L. p8 inhibits the growth of human pancreatic cancer cells and its expression is induced through pathways involved in growth inhibition and repressed by factors promoting cell growth. Mol. Cancer 2 (2003) 37
26. Mallo G.V., Fiedler F., Calvo E.L., Ortiz E.M., Vasseur S., Keim V., Morisset J., and Iovanna J.L. Cloning and expression of the rat p8 cDNA, a new gene activated in pancreas during the acute phase of pancreatitis, pancreatic development, and regeneration, and which promotes cellular growth. J. Biol. Chem. 272 (1997) 32360-32369
27. Mandic A., Hansson J., Linder S., and Shoshan M.C. Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J. Biol. Chem. 278 (2003) 9100-9106
28. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., and Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346 (1990) 561-564
29. McKallip R.J., Lombard C., Fisher M., Martin B.R., Ryu S., Grant S., Nagarkatti P.S., and Nagarkatti M. Targeting CB2 cannabinoid receptors as a novel therapy to treat malignant lymphoblastic disease. Blood 100 (2002) 627-634
30. Mechoulam R., Ben-Shabat S., Hanus L., Ligumsky M., Kaminski N.E., Schatz A.R., Gopher A., Almog S., Martin B.R., Compton D.R., et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 50 (1995) 83-90
31. Mimeault M., Pommery N., Wattez N., Bailly C., and Henichart J.P. Anti-proliferative and apoptotic effects of anandamide in human prostatic cancer cell lines: implication of epidermal growth factor receptor down-regulation and ceramide production. Prostate 56 (2003) 1-12
32. Munro S., Thomas K.L., and Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 365 (1993) 61-65
33. Ogretmen B., and Hannun Y.A. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat. Rev. Cancer 4 (2004) 604-616
34. Ohoka N., Yoshii S., Hattori T., Onozaki K., and Hayashi H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 24 (2005) 1243-1255
35. Piomelli D. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4 (2003) 873-884
36. Portella G., Laezza C., Laccetti P., De Petrocellis L., Di Marzo V., and Bifulco M. Inhibitory effects of cannabinoid CB1 receptor stimulation on tumor growth and metastatic spreading: actions on signals involved in angiogenesis and metastasis. FASEB J. 17 (2003) 1771-1773
37. Riboni L., Campanella R., Bassi R., Villani R., Gaini S.M., Martinelli-Boneschi F., Viani P., and Tettamanti G. Ceramide levels are inversely associated with malignant progression of human glial tumors. Glia 39 (2002) 105-113
38. 9-tetrahydrocannabinol induces apoptosis in human prostate PC-3 cells via a receptor-independent mechanism. FEBS Lett. 458 (1999) 400-404
39. 9-tetrahydrocannabinol induces apoptosis in C6 glioma cells. FEBS Lett. 436 (1998) 6-10
40. Sarfaraz S., Afaq F., Adhami V.M., and Mukhtar H. Cannabinoid receptor as a novel target for the treatment of prostate cancer. Cancer Res. 65 (2005) 1635-1641
41. Schroder M., and Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 74 (2005) 739-789
42. Su S.B., Motoo Y., Iovanna J.L., Berthezene P., Xie M.J., Mouri H., Ohtsubo K., Matsubara F., and Sawabu N. Overexpression of p8 is inversely correlated with apoptosis in pancreatic cancer. Clin. Cancer Res. 7 (2001) 1320-1324
43. Tajiri S., Oyadomari S., Yano S., Morioka M., Gotoh T., Hamada J.I., Ushio Y., and Mori M. Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ. 11 (2004) 403-415
44. Tessitore A., del P Martin M., Sano R., Ma Y., Mann L., Ingrassia A., Laywell E.D., Steindler D.A., Hendershot L.M., and d' Azzo A. GM1-ganglioside-mediated activation of the unfolded protein response causes neuronal death in a neurodegenerative gangliosidosis. Mol. Cell 15 (2004) 753-766
45. Vasseur S., Vidal Mallo G., Fiedler F., Bodeker H., Canepa E., Moreno S., and Iovanna J.L. Cloning and expression of the human p8, a nuclear protein with mitogenic activity. Eur. J. Biochem. 259 (1999) 670-675
46. Vasseur S., Hoffmeister A., Garcia S., Bagnis C., Dagorn J.C., and Iovanna J.L. p8 is critical for tumour development induced by rasV12 mutated protein and E1A oncogene. EMBO Rep. 3 (2002) 165-170
47. Vasseur S., Hoffmeister A., Garcia-Montero A., Mallo G.V., Feil R., Kuhbandner S., Dagorn J.C., and Iovanna J.L. p8-deficient fibroblasts grow more rapidly and are more resistant to adriamycin-induced apoptosis. Oncogene 21 (2002) 1685-1694