Inhibition of colon carcinogenesis by a standardized Cannabis sativa extract with high content of cannabidiol

Phytomedicine

Volumn 21, Issue 5, 2014, Pages 631-639

  Romano, Barbara ^a,b,c   Borrelli, Francesca ^a,b   Pagano, Ester ^a,b   Cascio, Maria Grazia ^c   Pertwee, Roger G ^c   Izzo, Angelo A ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b Endocannabinoid Research Group   (Italy)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Cancer cell growth; Cannabidiol; Cannabinoid receptors; Chemoprevention; Colorectal cancer

Indexed keywords

4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; ANTINEOPLASTIC AGENT; AZOXYMETHANE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABIS DERIVATIVE; CBD BDS; UNCLASSIFIED DRUG; CANNABIDIOL; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CANNABIS; PLANT EXTRACT;

ABERRANT CRYPT FOCUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CELL PROLIFERATION; CELL STRAIN HCT116; CELL VIABILITY; COLON CARCINOGENESIS; COLORECTAL CARCINOMA; COLORECTAL POLYP; COLORECTAL TUMOR; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG RECEPTOR BINDING; FEMALE; HUMAN; HUMAN CELL; IC 50; IN VIVO STUDY; MALE; MOUSE; MTT ASSAY; MURINE MODEL; NONHUMAN; PRECANCER; PRIORITY JOURNAL; TUMOR XENOGRAFT; ANIMAL; CARCINOGENESIS; CARCINOMA; CELL SURVIVAL; CHO CELL LINE; COLONIC NEOPLASMS; CRICETULUS; DRUG EFFECTS; DRUG SCREENING; EPITHELIUM CELL; HAMSTER; HCT116 CELL LINE; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PHYTOTHERAPY; RANDOMIZATION;

CANNABIS; CANNABIS SATIVA; MUS;

ANIMALS; AZOXYMETHANE; CANNABIDIOL; CANNABINOID RECEPTOR ANTAGONISTS; CANNABIS; CARCINOGENESIS; CARCINOMA; CELL PROLIFERATION; CELL SURVIVAL; CHO CELLS; COLONIC NEOPLASMS; CRICETINAE; CRICETULUS; EPITHELIAL CELLS; HCT116 CELLS; HUMANS; MALE; MICE, INBRED ICR; PHYTOTHERAPY; PLANT EXTRACTS; RANDOM ALLOCATION; RECEPTORS, CANNABINOID; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84898058079     PISSN: 09447113     EISSN: 1618095X     Source Type: Journal    
DOI: 10.1016/j.phymed.2013.11.006     Document Type: Article

References (49)

1. G. Aviello, J.M. Canadanovic-Brunet, N. Milic, R. Capasso, E. Fattorusso, and O. Taglialatela-Scafati et al. Potent antioxidant and genoprotective effects of boeravinone G, a rotenoid isolated from Boerhaavia diffusa PLoS ONE 6 2011 e19628
2. G. Aviello, B. Romano, F. Borrelli, R. Capasso, L. Gallo, and F. Piscitelli et al. Chemopreventive effect of the non-psychotropic phytocannabinoid cannabidiol on experimental colon cancer J. Mol. Med. (Berl.) 90 2012 925 934
3. G.P. Boivin, K. Washington, K. Yang, J.M. Ward, T.P. Pretlow, and R. Russell et al. Pathology of mouse models of intestinal cancer: consensus report and recommendations Gastroenterology 124 2013 762 777
4. F. Borrelli, A.A. Izzo, G. Di Carlo, P. Maffia, A. Russo, and F.M. Maiello et al. Effect of a propolis extract and caffeic acid phenethyl ester on formation of aberrant crypt foci and tumors in the rat colon Fitoterapia 73 2002 S38 S43
5. R. Capasso, G. Aviello, F. Borrelli, B. Romano, M. Ferro, and L. Castaldo et al. Inhibitory effect of standardized cannabis sativa extract and its ingredient cannabidiol on rat and human bladder contractility Urology 77 2011 1006.e9 1006.e15
6. G.T. Carter, A.M. Flanagan, M. Earleywine, D.I. Abrams, S.K. Aggarwal, and L. Grinspoon Cannabis in palliative medicine: improving care and reducing opioid-related morbidity Am. J. Hosp. Palliat. Care 28 2011 297 303
7. M.G. Cascio, L.A. Gauson, L.A. Stevenson, R.A. Ross, and R.G. Pertwee Evidence that the plant cannabinoid cannabigerol is a highly potent alpha2-adrenoceptor agonist and moderately potent 5HT1A receptor antagonist Br. J. Pharmacol. 159 2010 129 141
8. 50) of an enzymatic reaction Biochem. Pharmacol. 22 1973 3099 3108
9. F. Cianchi, L. Papucci, N. Schiavone, M. Lulli, L. Magnelli, and M.C. Vinci 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 2008 7691 7700
10. F. Comelli, G. Giagnoni, I. Bettoni, M. Colleoni, and B. Costa Antihyperalgesic effect of a Cannabis sativa extract in a rat model of neuropathic pain: mechanisms involved Phytother. Res. 22 2008 1017 1024
11. E.P. de Meijer, M. Bagatta, A. Carboni, P. Crucitti, V.M. Moliterni, P. Ranalli, and G. Mandolino The inheritance of chemical phenotype in Cannabis sativa L. Genetics 163 2003 335 346
12. L. De Petrocellis, A. Ligresti, A. Schiano Moriello, M. Iappelli, R. Verde, and C.G. Stott et al. Non-THC cannabinoids inhibit prostate carcinoma growth in vitro and in vivo: pro-apoptotic effects and underlying mechanisms Br. J. Pharmacol. 168 2013 79 102
13. M.M. Derry, K. Raina, C. Agarwal, and R. Agarwal Identifying molecular targets of lifestyle modifications in colon cancer prevention Front. Oncol. 14 2013 119
14. M. Duran, E. Pérez, S. Abanades, X. Vidal, C. Saura, and M. Majem et al. Preliminary efficacy and safety of an oromucosal standardized cannabis extract in chemotherapy-induced nausea and vomiting Br. J. Clin. Pharmacol. 70 2010 656 663
15. J.M. Ebos, and R.S. Kerbel Antiangiogenic therapy: impact on invasion, disease progression, and metastasis Nat. Rev. Clin. Oncol. 8 2011 316
16. C.J. Fowler, S.B. Gustafsson, S.C. Chung, E. Persson, S.O. Jacobsson, and A. Bergh Targeting the endocannabinoid system for the treatment of cancer - a practical view Curr. Top. Med. Chem. 10 2010 814 827
17. S. Franceschi, and C.P. Wild Meeting the global demands of epidemiologic transition - the indispensable role of cancer prevention Mol. Oncol. 7 2013 1 13
18. D. Hernán Pérez de la Ossa, M. Lorente, M.E. Gil-Alegre, S. Torres, E. García-Taboada, and R. Aberturas Mdel et al. Local delivery of cannabinoid-loaded microparticles inhibits tumor growth in a murine xenograft model of glioblastoma multiforme PLoS ONE 8 2013 e54795
19. A.A. Izzo, G. Aviello, S. Petrosino, P. Orlando, G. Marsicano, and B. Lutz et al. Increased endocannabinoid levels reduce the development of precancerous lesions in the mouse colon J. Mol. Med. (Berl.) 86 2008 89 98
20. A.A. Izzo, and A.A. Coutts Cannabinoids and the digestive tract Handb. Exp. Pharmacol. 168 2005 573 598
21. A.A. Izzo, and M. Camilleri Cannabinoids in intestinal inflammation and cancer Pharmacol. Res. 60 2009 117 125
22. J.R. Johnson, M. Burnell-Nugent, D. Lossignol, E.D. Ganae-Motan, R. Potts, and M.T. Fallon Multicenter, double-blind, randomized, placebo-controlled, parallel-group study of the efficacy, safety, and tolerability of THC:CBD extract and THC extract in patients with intractable cancer-related pain J. Pain Symptom Manage. 39 2010 167 179
23. J.R. Johnson, D. Lossignol, M. Burnell-Nugent, and M.T. Fallon An open-label extension study to investigate the long-term safety and tolerability of THC/CBD oromucosal spray and oromucosal THC spray in patients with terminal cancer-related pain refractory to strong opioid analgesics J. Pain Symptom Manage. 2012 pii:S0885-3924(12)00439-3
24. J. Kargl, J. Haybaeck, A. Stancic, L. Andersen, G. Marsche, A. Heinemann, and R. Schicho O-1602, an atypical cannabinoid, inhibits tumor growth in colitis-associated colon cancer through multiple mechanisms J. Mol. Med. (Berl.) 91 2013 449 458
25. N.M. Kogan, M. Schlesinger, M. Peters, G. Marincheva, R. Beeri, and R. Mechoulam A cannabinoid anticancer quinone, HU-331, is more potent and less cardiotoxic than doxorubicin: a comparative in vivo study J. Pharmacol. Exp. Ther. 322 2007 646 653
26. C. Kriza, M. Emmert, P. Wahlster, C. Niederländer, and P. Kolominsky-Rabas Cost of illness in colorectal cancer: an international review Pharmacoeconomics 31 2013 577 588
27. A. Ligresti, T. Bisogno, I. Matias, L. De Petrocellis, M.G. Cascio, and V. Cosenza et al. Possible endocannabinoid control of colorectal cancer growth Gastroenterology 125 2003 677 687
28. A. Ligresti, A.S. Moriello, K. Starowicz, I. Matias, S. Pisanti, and L. De Petrocellis et al. Antitumor activity of plant cannabinoids with emphasis on the effect of cannabidiol on human breast carcinoma J. Pharmacol. Exp. Ther. 318 2006 1375 1387
29. Y. Maor, J. Yu, P.M. Kuzontkoski, B.J. Dezube, X. Zhang, and J.E. Groopman Cannabidiol inhibits growth and induces programmed cell death in kaposi sarcoma-associated herpesvirus-infected endothelium Genes Cancer 3 2012 512 520
30. P. Massi, M. Solinas, V. Cinquina, and D. Parolaro Cannabidiol as potential anticancer drug Br. J. Clin. Pharmacol. 75 2013 303 312
31. S.D. McAllister, R. Murase, R.T. Christian, D. Lau, A.J. Zielinski, and J. Allison et al. Pathways mediating the effects of cannabidiol on the reduction of breast cancer cell proliferation, invasion, and metastasis Breast Cancer Res. Treat. 129 2011 37 47
32. R.G. Pertwee Pharmacological actions of cannabinoids Handb. Exp. Pharmacol. 168 2005 1 51
33. R.G. Pertwee The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol, cannabidiol and delta9- tetrahydrocannabivarin Br. J. Pharmacol. 153 2008 199 215
34. R.G. Pertwee Targeting the endocannabinoid system with cannabinoid receptor agonists: pharmacological strategies and therapeutic possibilities Philos. Trans. R. Soc. Lond. B: Biol. Sci. 367 2012 3353 3363
35. F. Pollastro, O. Taglialatela-Scafati, M. Allarà, E. Muñoz, V. Di Marzo, L. De Petrocellis, and G. Appendino Bioactive prenylogous cannabinoid from fiber hemp (Cannabis sativa) J. Nat. Prod. 74 2011 2019 2022
36. R.K. Portenoy, E.D. Ganae-Motan, S. Allende, R. Yanagihara, L. Shaiova, and S. Weinstein et al. Nabiximols for opioid-treated cancer patients with poorly controlled chronic pain: a randomized, placebo-controlled, graded-dose trial J. Pain 13 2012 438 449
37. R. Ramer, K. Bublitz, N. Freimuth, J. Merkord, H. Rohde, and M. Haustein et al. Cannabidiol inhibits lung cancer cell invasion and metastasis via intercellular adhesion molecule-1 FASEB J. 26 2012 1535 1548
38. R. Ramer, J. Merkord, H. Rohde, and B. Hinz Cannabidiol inhibits cancer cell invasion via upregulation of tissue inhibitor of matrix metalloproteinases-1 Biochem. Pharmacol. 79 2010 955 966
39. R.A. Ross, H.C. Brockie, L.A. Stevenson, V.L. Murphy, F. Templeton, and A. Makriyannis et al. Agonist-inverse agonist characterization at CB1 and CB2 cannabinoid receptors of L759633, L759656 and AM630 Br. J. Pharmacol. 126 1999 665 672
40. R.A. Ross, T.M. Gibson, L.A. Stevenson, B. Saha, P. Crocker, and R.K. Razdan et al. Structural determinants of the partial agonist-inverse agonist properties of 6'-azidohex-2'-yne-D8-tetrahydrocannabinol at cannabinoid receptors Br. J. Pharmacol. 128 1999 735 743
41. E.B. Russo Taming THC: potential cannabis synergy and phytocannabinoid-terpenoid entourage effects Br. J. Pharmacol. 163 2011 1344 1364
42. A. Shrivastava, P.M. Kuzontkoski, J.E. Groopman, and A. Prasad Cannabidiol induces programmed cell death in breast cancer cells by coordinating the cross-talk between apoptosis and autophagy Mol. Cancer Ther. 10 2011 1161 1172
43. R. Siegel, D. Naishadham, and A. Jemal Cancer statistics, 2013 Cancer J. Clin. 63 2013 11 30
44. M. Solinas, P. Massi, A.R. Cantelmo, M.G. Cattaneo, R. Cammarota, and D. Bartolini et al. Cannabidiol inhibits angiogenesis by multiple mechanisms Br. J. Pharmacol. 167 2012 1218 1231
45. S. Sreevalsan, S. Joseph, I. Jutooru, G. Chadalapaka, and S.H. Safe Induction of apoptosis by cannabinoids in prostate and colon cancer cells is phosphatase dependent Anticancer Res. 31 2011 3799 3807
46. D. Thapa, Y. Kang, P.H. Park, S.K. Noh, Y.R. Lee, and S.S. Han et al. Anti-tumor activity of the novel hexahydrocannabinol analog LYR-8 in Human colorectal tumor xenograft is mediated through the inhibition of Akt and hypoxia-inducible factor-1a activation Biol. Pharm. Bull. 35 2012 924 932
47. G. Velasco, C. Sánchez, and M. Guzmán Towards the use of cannabinoids as antitumour agents Nat. Rev. Cancer 12 2012 436 444
48. M.K. Washington, A.E. Powell, R. Sullivan, J.P. Sundberg, N. Wright, R.J. Coffey, and W.F. Dove Pathology of rodent models of intestinal cancer: progress report and recommendations Gastroenterology 144 2013 705 717
49. J.D. Wilkinson, and E.M. Williamson Cannabinoids inhibit human keratinocyte proliferation through a non-CB1/CB2 mechanism and have a potential therapeutic value in the treatment of psoriasis J. Dermatol. Sci. 45 2007 87 92