Cannabis-derived substances in cancer therapy - an emerging anti- inflammatory role for the cannabinoids

Current Clinical Pharmacology

Volumn 5, Issue 4, 2010, Pages 281-287

  Liu, Wai M ^a   Fowler, Daniel W ^a   Dalgleish, Angus G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cannabinoids; Cannabis plant; Immune modulation; Inflammation

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTINEOPLASTIC AGENT; CANNABINOID;

DRUG EFFECT; HUMAN; INFLAMMATION; NEOPLASM; REVIEW; SIGNAL TRANSDUCTION;

ANTI-INFLAMMATORY AGENTS; ANTINEOPLASTIC AGENTS; CANNABINOIDS; HUMANS; INFLAMMATION; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 79952279722     PISSN: 15748847     EISSN: None     Source Type: Journal    
DOI: 10.2174/157488410793352049     Document Type: Article

References (102)

1. Iversen LL. Pharmacology. Medical uses of marijuana? Nature 1993 365: 12-3.
2. Grotenhermen F. Pharmacokinetics and pharmacodynamics of cannabinoids. Clin Pharmacokinet 2003;42: 327-60.
3. Liu WM and Powles TB. Cannabinoids: Do they have a role in cancer therapy? Lett Drug Des Discov 2006; 3: 76-82.
4. Kreitzer FR, Stella N. The therapeutic potential of novel cannabinoid receptors. Pharmacol Ther 2009; 122: 83-96.
5. Herkenham M, Lynn AB, Little MD, et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci 1990; 87: 1932-6.
6. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993; 365: 61-5.
7. Anand U, Otto WR, Sanchez-Herrera D, et al. Cannabinoid receptor CB2 localisation and agonist-mediated inhibition of capsaicin responses in human sensory neurons. Pain 2008; 138: 667-80.
8. Mukhopadhyay S, Shim JY, Assi AA, Norford D, Howlett AC. CB(1) cannabinoid receptor-G protein association: a possible mechanism for differential signaling. Chem Phys Lipids 2002; 121: 91-109.
9. Ma'ayan A, Jenkins SL, Barash A, Iyengar R. Neuro2A differentiation by Galphai/o pathway. Sci Signal 2009; 2: cm1-cm7.
10. Vannacci A, Giannini L, Masini E, Mannaioni PF. Cannabinoidinduced activation of ERK and AKT in mast cells may be mediated by intracellular NO production. J Immunol 2003; 171: 2767.
11. Galve-Roperh I, Rueda D, Gómez del Pulgar T, Velasco G, Guzmán M. Mechanism of extracellular signal-regulated kinase activation by the CB(1) cannabinoid receptor. Mol Pharmacol 2002; 62: 1385-92.
12. Davis MI, Ronesi J, Lovinger DM. A predominant role for inhibition of the adenylate cyclase/protein kinase A pathway in ERK activation by cannabinoid receptor 1 in N1E-115 neuroblastoma cells. J Biol Chem 2003; 278: 48973-80.
13. Faubert Kaplan BL, Kaminski NE. Cannabinoids inhibit the activation of ERK MAPK in PMA/Io-stimulated mouse splenocytes. Int Immunopharmacol 2003; 3: 1503-10.
14. Powles T, te Poele R, Shamash J, et al. Cannabis-induced cytotoxicity in leukemic cell lines: the role of the cannabinoid receptors and the MAPK pathway. Blood 2005; 105: 1214-21.
15. Greenhough A, Patsos HA, Williams AC, Paraskeva C. The cannabinoid delta(9)-tetrahydrocannabinol inhibits RAS-MAPK and PI3K-AKT survival signalling and induces BAD-mediated apoptosis in colorectal cancer cells. Int J Cancer 2007; 121: 2172-80.
16. Ellert-Miklaszewska A, Kaminska B, Konarska L. Cannabinoids down-regulate PI3K/Akt and Erk signalling pathways and activate proapoptotic function of Bad protein. Cell Signal 2005; 17: 25-37.
17. Jia W, Hegde VL, Singh NP, et al. Delta9-tetrahydrocannabinolinduced apoptosis in Jurkat leukemia T cells is regulated by translocation of Bad to mitochondria. Mol Cancer Res 2006; 4: 549-62.
18. Yuan TL, Cantley LC. PI3K pathway alterations in cancer: variations on a theme. Oncogene 2008; 27: 5497-510.
19. Engelman JA. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 2009; 9: 550-62.
20. Luo J, Manning BD, Cantley LC. Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell 2003; 4: 257-62.
21. Ozaita A, Puighermanal E, Maldonado R. Regulation of PI3K/Akt/GSK-3 pathway by cannabinoids in the brain. J Neurochem 2007; 102: 1105-14.
22. Athanasiou A, Clarke AB, Turner AE, et al. Cannabinoid receptor agonists are mitochondrial inhibitors: a unified hypothesis of how cannabinoids modulate mitochondrial function and induce cell death. Biochem Biophys Res Commun 2007; 364: 131-7.
23. Schug ZT, Gottlieb E. Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis. Biochim Biophys Acta 2009; 1788: 2022-31
24. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000; 103: 239-52.
25. Kanda H, Miura M. Regulatory roles of JNK in programmed cell death. J Biochem 2004; 136: 1-6.
26. Downer EJ, Fogarty MP, Campbell VA. Tetrahydrocannabinolinduced neurotoxicity depends on CB1 receptor-mediated c-Jun Nterminal kinase activation in cultured cortical neurons. Br J Pharmacol 2003; 140: 547-57.
27. Bosier B, Lambert DM, Hermans E. Reciprocal influences of CB1 cannabinoid receptor agonists on ERK and JNK signalling in N1E- 115 cells. FEBS Lett 2008; 582: 3861-7.
28. Lee YM, Uhm KO, Lee ES, Kwon J, Park SH, Kim HS. AM251 suppresses the viability of HepG2 cells through the AMPK (AMPactivated protein kinase)-JNK (c-Jun N-terminal kinase)-ATF3 (ac tivating transcription factor 3) pathway. Biochem Biophys Res Commun 2008; 370: 641-5.
29. Luca T, Di Benedetto G, Scuderi MR, et al. The CB1/CB2 receptor agonist WIN-55,212-2 reduces viability of human Kaposi's sarcoma cells in vitro. Eur J Pharmacol 2009; 616: 16-21.
30. Olea-Herrero N, Vara D, Malagarie-Cazenave S, Díaz-Laviada I. Inhibition of human tumour prostate PC-3 cell growth by cannabinoids R(+)-Methanandamide and JWH-015: involvement of CB2. Br J Cancer 2009; 101: 940-50.
31. Rueda D, Galve-Roperh I, Haro A, Guzmán M. The CB(1) cannabinoid receptor is coupled to the activation of c-Jun N-terminal kinase. Mol Pharmacol 2000; 58: 814-20.
32. Blazquez C, Galve-Roperh I, Guzmán M. De novo-synthesized ceramide signals apoptosis in astrocytes via extracellular signalregulated kinase. FASEB J 2000; 14: 2315-22.
33. Guzman M, Galve-Roperh I, Sánchez C. Ceramide: a new second messenger of cannabinoid action. Trends Pharmacol Sci 2001; 22: 19-22.
34. Taha TA, Mullen TD, Obeid LM. A house divided: ceramide, sphingosine, and sphingosine-1-phosphate in programmed cell death. Biochim Biophys Acta 2006; 1758: 2027-36.
35. Sawada M, Nakashima S, Banno Y, et al. Ordering of ceramide formation, caspase activation, and Bax/Bcl-2 expression during etoposide-induced apoptosis in C6 glioma cells. Cell Death Differ 2000; 7: 761-72.
36. Chalfant CE, Rathman K, Pinkerman RL, et al. De novo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells. Dependence on protein phosphatase-1. J Biol Chem 2002; 277: 12587-95.
37. Ganesan V, Perera MN, Colombini D, Datskovskiy D, Chadha K, Colombini M. Ceramide and activated Bax act synergistically to permeabilize the mitochondrial outer membrane. Apoptosis 2010; 15(5): 553-62.
38. Cuvillier O, Rosenthal DS, Smulson ME, Spiegel S. Sphingosine 1- phosphate inhibits activation of caspases that cleave poly(ADPribose) polymerase and lamins during Fas- and ceramide-mediated apoptosis in Jurkat T lymphocytes. J Biol Chem 1998; 273: 2910-6.
39. Liu WM. Enhancing the cytotoxic activity of novel targeted therapies-- is there a role for a combinatorial approach? Curr Clin Pharmacol 2008; 3: 108-17.
40. Liu WM, Scott KA, Shamash J, Joel S, Powles TB. Enhancing the in vitro cytotoxic activity of Delta9-tetrahydrocannabinol in leukemic cells through a combinatorial approach. Leuk Lymphoma 2008; 49: 1800-9.
41. Gazzerro P, Malfitano AM, Proto MC, et al. Synergistic inhibition of human colon cancer cell growth by the cannabinoid CB1 receptor antagonist rimonabant and oxaliplatin. Oncol Rep 2010; 23: 171-5.
42. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000; 407: 249-57.
43. Freimuth N, Ramer R, Hinz B. Antitumorigenic effects of cannabinoids beyond apoptosis. J Pharmacol Exp Ther 2010; 332: 336-44.
44. Portella G, Laezza C, Laccetti P, De Petrocellis L, Di Marzo V, 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 2003; 17: 1771-3.
45. Preet A, Ganju RK, Groopman JE. Delta9-Tetrahydrocannabinol inhibits epithelial growth factor-induced lung cancer cell migration in vitro as well as its growth and metastasis in vivo. Oncogene 2008; 27: 339-46.
46. Ramer R, Merkord J, Rohde H, Hinz B. Cannabidiol inhibits cancer cell invasion via upregulation of tissue inhibitor of matrix metalloproteinases- 1. Biochem Pharmacol 2010; 79: 955-66.
47. Mechoulam R, Parker LA, Gallily R. Cannabidiol: an overview of some pharmacological aspects. J Clin Pharmacol 2002; 42: 11S-19S.
48. Mechoulam R, Peters M, Murillo-Rodriguez E, Hanus LO. Cannabidiol-- recent advances. Chem Biodivers 2007; 4: 1678-92.
49. Thomas A, Baillie GL, Phillips AM, Razdan RK, Ross RA, Pertwee RG. Cannabidiol displays unexpectedly high potency as an antagonist of CB1 and CB2 receptor agonists in vitro. Br J Pharmacol 2007; 150: 613-23.
50. Izzo AA, Camilleri M. Cannabinoids in intestinal inflammation and cancer. Pharmacol Res 2009; 60: 117-25.
51. Gallily R, Even-Chena T, Katzavian G, Lehmann D, Dagan A, Mechoulam R. Gamma-irradiation enhances apoptosis induced by cannabidiol, a non-psychotropic cannabinoid, in cultured HL-60 myeloblastic leukemia cells. Leuk Lymphoma 2003; 44: 1767-73.
52. Massi P, Vaccani A, Ceruti S, Colombo A, Abbracchio MP, Parolaro D. Antitumor effects of cannabidiol, a nonpsychoactive cannabinoid, on human glioma cell lines. J Pharmacol Exp Ther 2004; 308: 838-45.
53. Zoratti C, Kipmen-Korgun D, Osibow K, Malli R, Graier WF. Anandamide initiates Ca(2+) signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells. Br J Pharmacol 2003; 140: 1351-62.
54. Ligresti A, Moriello AS, Starowicz K, et al. Antitumor activity of plant cannabinoids with emphasis on the effect of cannabidiol on human breast carcinoma. J Pharmacol Exp Ther 2006; 318: 1375-87.
55. McKallip RJ, Jia W, Schlomer J, Warren JW, Nagarkatti PS, Nagarkatti M. Cannabidiol-induced apoptosis in human leukemia cells: A novel role of cannabidiol in the regulation of p22phox and Nox4 expression. Mol Pharmacol 2006; 70: 897-908.
56. Marcu JP, Christian RT, Lau D, et al. Cannabidiol enhances the inhibitory effects of Delta9-tetrahydrocannabinol on human glioblastoma cell proliferation and survival. Mol Cancer Ther 2010; 9: 180-9.
57. Khatami M. Inflammation, aging, and cancer: tumoricidal versus tumorigenesis of immunity: a common denominator mapping chronic diseases. Cell Biochem Biophys 2009; 55: 55-79
58. Hussain SP, Harris CC. Inflammation and cancer: an ancient link with novel potentials. Int J Cancer 2007; 121: 2373-80.
59. Vasto S, Carruba G, Candore G, Italiano E, Di Bona D, Caruso C. Inflammation and prostate cancer. Future Oncol 2008; 4: 637-45.
60. Abdel-Latif MM, Duggan S, Reynolds JV, Kelleher D. Inflammation and esophageal carcinogenesis. Curr Opin Pharmacol 2009; 9: 396-404.
61. Kraus S, Arber N. Inflammation and colorectal cancer. Curr Opin Pharmacol 2009; 9: 405-10.
62. Wang D, Dubois RN, Richmond A. The role of chemokines in intestinal inflammation and cancer. Curr Opin Pharmacol 2009; 9: 688-96.
63. Yao H, Rahman I. Current concepts on the role of inflammation in COPD and lung cancer. Curr Opin Pharmacol 2009; 9: 375-83.
64. Gonda TA, Tu S, Wang TC. Chronic inflammation, the tumor microenvironment and carcinogenesis. Cell Cycle 2009; 8: 2005-13.
65. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001; 357: 539-45
66. Forman D, Newell DG, Fullerton F, et al. Association between infection with Helicobacter pylori and risk of gastric cancer: evidence from a prospective investigation. BMJ 1991; 302: 1302-5.
67. zur Hausen H. Papillomaviruses in the causation of human cancers - a brief historical account. Virology 2009; 384: 260-5
68. Cuzick J, Otto F, Baron JA, et al. Aspirin and non-steroidal antiinflammatory drugs for cancer prevention: an international consensus statement. Lancet Oncol 2009; 10: 501-7.
69. Visconti R, Grieco D. New insights on oxidative stress in cancer. Curr Opin Drug Discov Devel 2009; 12: 240-5.
70. Zhang X, Mosser DM. Macrophage activation by endogenous danger signals. J Pathol 2008; 214: 161-78.
71. Bogdan C, Röllinghoff M, Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 2000; 12: 64-76.
72. Ma N, Kawanishi M, Hiraku Y, et al. Reactive nitrogen speciesdependent DNA damage in EBV-associated nasopharyngeal carcinoma: the relation to STAT3 activation and EGFR expression. Int J Cancer 2008; 122: 2517-25.
73. Meira LB, Bugni JM, Green SL, et al. DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice. J Clin Invest 2008; 118: 2516-25.
74. Katsurahara M, Kobayashi Y, Iwasa M, et al. Reactive nitrogen species mediate DNA damage in Helicobacter pylori-infected gastric mucosa. Helicobacter 2009; 14: 552-8.
75. Germano G, Allavena P, Mantovani A. Cytokines as a key component of cancer-related inflammation. Cytokine 2008; 43: 374-9.
76. Paulnock DM, Coller SP. Analysis of macrophage activation in African trypanosomiasis. J Leukoc Biol 2001; 69: 685-90.
77. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002; 196: 254-65.
78. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006; 441: 431-6.
79. Yan B, Wang H, Rabbani ZN, et al. Tumor necrosis factor-alpha is a potent endogenous mutagen that promotes cellular transformation. Cancer Res 2006; 66: 11565-70.
80. Kimsey TF, Campbell AS, Albo D, Wilson M, Wang TN. Colocalization of macrophage inflammatory protein-3alpha (Mip- 3alpha) and its receptor, CCR6, promotes pancreatic cancer cell invasion. Cancer J 2004; 10: 374-80.
81. Chen JJ, Lin YC, Yao PL, et al. Tumor-associated macrophages: the double-edged sword in cancer progression. J Clin Oncol 2005; 23: 953-64.
82. Harris RE. Cyclooxygenase-2 (cox-2) blockade in the chemoprevention of cancers of the colon, breast, prostate, and lung. Inflammopharmacology 2009; 17: 55-67
83. Galiegue S, Mary S, Marchand J, et al. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 1995; 232: 54-61.
84. Tanasescu R, Constantinescu CS. Cannabinoids and the immune system: An overview. Immunobiology 2010; 215(8): 588-97.
85. Klein TW, Newton CA, Nakachi N, Friedman H. Delta-9- tetrahydrocannabinol treatment suppresses immunity and early IFN-gamma, IL-12, and IL-12 receptor beta 2 responses to Legionella pneumophila infection. J Immunol 2000; 164: 6461-6.
86. Massi P, Fuzio D, Viganò D, Sacerdote P, Parolaro D. Relative involvement of cannabinoid CB(1) and CB(2) receptors in the Delta(9)-tetrahydrocannabinol-induced inhibition of natural killer activity. Eur J Pharmacol 2000; 387: 343-7.
87. Zhu LX, Sharma S, Stolina M, et al. Delta-9-tetrahydrocannabinol inhibits antitumor immunity by a CB2 receptor mediated, cytokinedependent pathway. J Immunol 2000; 165: 373-80.
88. Facci L, Dal Toso R, Romanello S, Buriani A, Skaper SD, Leon A. Mast cells express a peripheral cannabinoid receptor with differential sensitivity to anandamide and palmitoylethanolamide. Proc Natl Acad Sci USA 1995; 92: 3376-80.
89. Smith SR, Terminelli C, Denhardt G. Effects of cannabinoid receptor agonist and antagonist ligands on production of inflammatory cytokines and anti-inflammatory interleukin-10 in endotoxemic mice. J Pharmacol Exp Ther 2000; 293: 136-50.
90. Klein TW. Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat Rev Immunol 2005; 5: 400-11.
91. Correa F, Hernangómez M, Mestre L, et al. Anandamide enhances IL-10 production in activated microglia by targeting CB(2) receptors: roles of ERK1/2, JNK, and NF-kappaB. Glia 2010; 58: 135-47.
92. Izzo AA, Camilleri M. Emerging role of cannabinoids in gastrointestinal and liver diseases: basic and clinical aspects. Gut 2008; 57: 1140-55.
93. Wright KL, Duncan M, Sharkey KA. Cannabinoid CB2 receptors in the gastrointestinal tract: a regulatory system in states of inflammation. Br J Pharmacol 2008; 153: 263-70.
94. Massa F, Storr M, Lutz B. The endocannabinoid system in the physiology and pathophysiology of the gastrointestinal tract. J Mol Med 2005; 83: 944-54.
95. Machado Rocha FC, Stéfano SC, De Cássia haiek r, Rosa Oliveira LM, Da Silveira DX. Therapeutic use of Cannabis sativa on chemotherapy- induced nausea and vomiting among cancer patients: systematic review and meta-analysis. Eur J Cancer Care (Engl) 2008; 17: 431-43.
96. Kirkham TC. Cannabinoids and appetite: food craving and food pleasure. Int Rev Psychiatry 2009; 21: 163-71.
97. Izzo AA, Borrelli F, Capasso R, Di Marzo V, Mechoulam R. Nonpsychotropic plant cannabinoids: new therapeutic opportunities from an ancient herb. Trends Pharmacol Sci 2009; 30: 515-27.
98. Di Marzo V, Izzo AA. Endocannabinoid overactivity and intestinal inflammation. Gut 2006; 55: 1373-6.
99. Ihenetu K, Molleman A, Parsons ME, Whelan CJ. Inhibition of interleukin-8 release in the human colonic epithelial cell line HT- 29 by cannabinoids. Eur J Pharmacol 2003; 458: 207-15.
100. Schuerer-Maly CC, Eckmann L, Kagnoff MF, Falco MT, Maly FE. Colonic epithelial cell lines as a source of interleukin-8: stimulation by inflammatory cytokines and bacterial lipopolysaccharide. Immunology 1994; 81: 85-91.
101. Burstein SH, Zurier RB. Cannabinoids, endocannabinoids, and related analogs in inflammation. AAPS J 2009; 11: 109-19.
102. Liu WM, Meyer B, Dalgleish AG. How immunotherapy can enhance the response to other modalities and improve outcome and quality of life. J BUON 2009; 14: S103-9.