Antitumor Effects of Cannabidiol, a Nonpsychoactive Cannabinoid, on Human Glioma Cell Lines

Journal of Pharmacology and Experimental Therapeutics

Volumn 308, Issue 3, 2004, Pages 838-845

  Massi, Paola ^a   Vaccani, Angelo ^b   Ceruti, Stefania ^a   Colombo, Arianna ^a   Abbracchio, Maria P ^a   Parolaro, Daniela ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; ALPHA TOCOPHEROL; CANNABIDIOL; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CAPSAZEPINE; CERAMIDE; RECEPTOR BLOCKING AGENT; RIMONABANT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR; VANILLOID RECEPTOR ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER GRAFT; CANCER INHIBITION; DRUG ANTAGONISM; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IC 50; MITOCHONDRIAL RESPIRATION; MOUSE; NITROBLUE TETRAZOLIUM TEST; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CANNABIDIOL; CANNABINOIDS; CELL DIVISION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; GLIOMA; HUMANS; MICE; NEOPLASM TRANSPLANTATION; NEOPLASMS, EXPERIMENTAL; PERTUSSIS TOXIN; RECEPTORS, DRUG; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 1342280974     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: 10.1124/jpet.103.061002     Document Type: Article

References (37)

1. Bifulco M and Di Marzo V (2002) Targeting the endocannabinoid system in cancer therapy: a call for further research. Nat Med 8:547-550.
2. Bisogno T, Hanus L, De Petrocellis L, Tchilibon S, Ponde DE, Brandi I, Moriello AS, Davis JB, Mechoulam R, and Di Marzo V (2001) Molecular targets for cannabidiol and its synthetic analogues: effect on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br J Pharmacol 134:845-852.
3. Braida D, Pegorini S, Arcidiacono MV, Consalez GG, Croci L, and Sala M (2003) Post-ischemic treatment with cannabidiol prevents electroencephalographic flattening, hyperlocomotion and neuronal injury in gerbils. Neurosci Lett 346:61-64.
4. Campbell VA (2001) Tetrahydrocannabinol-induced apoptosis of cultured cortical neurones is associated with cytochrome c release and caspase-3 activation. Neuropharmacology 40:702-709.
5. Carchman RA, Harris LS, and Munson AE (1976) The inhibition of DNA synthesis by cannabinoids. Cancer Res 36:95-100.
6. Ceruti S, Franceschi C, Barbieri D, Malorni W, Camurri A, Giammarioli AM, Ambrosini A, Racagni G, Cattabeni F, and Abbracchio MP (2000) Apoptosis induced by 2-chloro-adenosine and 2-chloro-2′-deoxy-adenosine in a human astrocytoma cell line: differential mechanisms and possible clinical relevance. J Neurosci Res 60:388-400.
7. Chan GC, Hinds TR, Impey S, and Storm DR (1998) Hippocampal neurotoxicity of Delta9-tetrahydrocannabinol. J Neurosci 18:5322-5332.
8. Faubert Kaplan BL, Rockwell CE, and Kaminski NE (2003) Evidence for cannabinoid receptor-dependent and -independent mechanism of action in leukocytes. J Pharmacol Exp Ther 306:1077-1085.
9. Frankfurt SO and Krishan A (2001) Enzyme-linked immunosorbent assay (ELISA) for the specific detection of apoptotic cells and its application to rapid drug screening. J Immunol Methods 253:133-144.
10. Galve-Roperh I, Sanchez C, Cortes ML, Gomez del Pulgar T, Izquierdo M, and Guzman M (2000) Anti-tumoral action of cannabinoids: involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat Med 6:313-319.
11. Gomez del Pulgar T, Velasco G, Sanchez C, Haro A, and Guzman M (2002) De novo-synthesized ceramide is involved in cannabinoid-induced apoptosis. Biochem J 363:183-188.
12. Goutopoulos A and Makriyannis A (2002) From cannabis to cannabinergics: new therapeutic opportunities. Pharmacol Ther 95:103-117.
13. Guzman M, Sanchez C, and Galve Roperh I (2002) Cannabinoids and cell fate. Pharmacol Ther 95:175-184.
14. Hampson AJ, Grimaldi M, Lolic M, Wink D, Rosenthal R, and Axelrod J (2000) Neuroprotective antioxidants from marijuana. Ann N Y Acad Sci 899:274-282.
15. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, et al. (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161-2002.
16. Jacobsson SO, Rongard E, Stridh M, Tiger G, and Fowler CJ (2000) Serum-dependent effects of tamoxifen and cannabinoids upon C6 glioma cell viability. Biochem Pharmacol 60:1807-1813.
17. Jacobsson SO, Wallin T, and Fowler CJ (2001) Inhibition of rat C6 glioma cell proliferation by endogenous and synthetic cannabinoids. Relative involvement of cannabinoid and vanilloid receptors. J Pharmacol Exp Ther 299:951-959.
18. Jarai Z, Wagner JA, Varga K, Lake KD, Compton DR, Martin BR, Zimmer AM, Bonner TI, Buckley NE, Mezey E, et al. (1999) Cannabinoid-induced mesenteric vasodilation through an endothelial site distinct from CB1 or CB2 receptors. Proc Natl Acad Sci USA 96:14136-14141.
19. Killestein J, Hoogervorst ELJ, Reif M, Blauw B, Smits M, Uitdehaag BMJ, Nagelkerken L, and Polman CH (2003) Immunomodulatory effects of orally administered cannabinoids in multiple sclerosis. J Neuroimmunol 137:140-143.
20. Maccarrone M, Lorenzon T, Bari M, Melino G, and Finazzi-Agro A (2000) Anandamide induces apoptosis in human cells via vanilloid receptors. Evidence for a protective role of cannabinoid receptors. J Biol Chem 275:31938-31945.
21. Malfait AM, Gallily R, Sumariwalla PF, Malik AS, Andreakos E, Mechoulam R, and Feldmann M (2000) The nonpsychoactive cannabis constituent cannabidiol is an oral anti-arthritic therapeutic in murine collagen-induced arthritis. Proc Natl Acad Sci USA 97:9561-9566.
22. Munson AE, Harris LS, Friedman MA, Dewey WL, and Carchman RA (1975) Anti-neoplastic activity of cannabinoids. J Natl Cancer Inst 55:597-602.
23. Pertwee RG and Ross RA (2002) Cannabinoid receptors and their ligands. Prostaglandins Leukot Essent Fatty Acids 66:101-121.
24. Recht LD, Salmonsen R, Rosetti R, Jang T, Pipia G, Kubiatowski T, Karim P, Ross AH, Zurier R, Litofsky NS, and Burstein S (2001) Antitumor effects of ajulemic acid (CT3), a synthetic non-psychoactive cannabinoid. Biochem Pharmacol 62:755-763.
25. Ruiz L, Miguel A, and Diaz-Laviada I (1999) Delta9-tetrahydrocannabinol induces apoptosis in human prostate PC-3 cells via a receptor-independent mechanism. FEBS Lett 458:400-404.
26. Sanchez C, de Ceballos ML, Gomez del Pulgar T, Rueda D, Corbacho C, Velasco G, Galve-Roperh I, Huffman JW, Ramon y Cajal S, and Guzman M (2001) Inhibition of glioma growth in vivo by selective activation of the CB(2) cannabinoid receptor. Cancer Res 61:5784-5789.
27. Sanchez C, Galve-Roperh I, Canova C, Brachet P, and Guzman M (1998) Delta9-tetrahydrocannabinol induces apoptosis in C6 glioma cells. FEBS Lett 436:6-10.
28. Sancho R, Calzado MA, Di Marzo V, Appendino G, and Munoz E (2003) Anandamide inhibits nuclear factor-kB activation through a cannabinoid receptor-independent pathway. Mol Pharmacol 63:429-438.
29. Sarafian TA, Kouyoumjian S, Khoshaghideh F, Tashkin DP, and Roth MD (2003) Delta 9-tetrahydrocannabinol disrupts mitochondrial function and cell energetics. Am J Physiol 284:L298-L306.
30. Sarker KP and Maruyama I (2003) Anadamide induces cell death independently of cannabinoid receptors or vanilloid receptor 1: possible involvement of lipid raas rafts. Cell Mol Life Sci 60:1200-1208.
31. Sarker KP, Obara S, Nakata M, Kitajima I, and Maruyama I (2000) Anandamide induces apoptosis of PC-12 cells: involvement of superoxide and caspase-3. FEBS Lett 472:39-44.
32. Showalter VM, Compton DR, Martin BR, and Abood ME (1996) Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): identification of cannabinoid receptor subtype selective ligands. J Pharmacol Exp Ther 278:989-999.
33. Smith MS, Yamamoto Y, Newton C, Friedman H, and Klein T (1997) Psychoactive cannabinoids increase mortality and acute phase cytokine responses in mice sublethally infected with Legionella pneumophila. Proc Soc Exp Biol Med 214:69-75.
34. 9Tetrahydrocannabinol and cannabidiol alter cytokine production by human immune cells. Immunopharmacology 40:179-185.
35. Watanabe K, Kayano Y, Matsunaga T, Yamamoto I, and Yoshimura H (1996) Inhibition of anandamide amidase activity in mouse brain microsomes by cannabinoids. Biol Pharm Bull 19:1109-1111.
36. Zheng ZM, Specter S, and Friedman H (1993) Serum proteins affect the inhibition by delta-tetrahydrocannabinol of tumor necrosis factor alpha production by mouse macrophages. Adv Zhu Exp Med Biol 335:89-93.
37. Zhu LX, Sharma S, Stolina M, Gardner B, Roth MD, Tashkin DP, and Dubinett SM (2000) Delta-9-tetrahydrocannabinol inhibits antitumor immunity by a CB2 receptor-mediated, cytokine-dependent pathway. J Immunol 165:373-380.