Cannabidiol inhibits cancer cell invasion via upregulation of tissue inhibitor of matrix metalloproteinases-1

Biochemical Pharmacology

Volumn 79, Issue 7, 2010, Pages 955-966

  Ramer, Robert ^a   Merkord, Jutta ^a   Rohde, Helga ^a   Hinz, Burkhard ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Cannabidiol; Experimental lung metastasis; Human cancer cells; Matrigel cell invasion; Metalloproteinases 1; Tissue inhibitor of matrix

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; CANNABIDIOL; CANNABINOID 1 RECEPTOR ANTAGONIST; CANNABINOID 2 RECEPTOR ANTAGONIST; CANNABINOID RECEPTOR ANTAGONIST; CAPSAZEPINE; MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; SMALL INTERFERING RNA; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; ANTINEOPLASTIC AGENT; CANNABINOID RECEPTOR; GELATINASE A; GELATINASE B; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL ASSAY; CELL INVASION; CELL VIABILITY; CONTROLLED STUDY; DRUG INHIBITION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG CANCER; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; THYMUS; TUMOR CELL; TUMOR XENOGRAFT; UTERINE CERVIX CANCER; ANIMAL; CANCER INVASION; DOSE RESPONSE; GENETICS; LUNG TUMOR; METASTASIS; PHYSIOLOGY; TUMOR CELL LINE; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CANNABIDIOL; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; NEOPLASM INVASIVENESS; RECEPTORS, CANNABINOID; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TRPV CATION CHANNELS; UP-REGULATION;

EID: 77449127143     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.11.007     Document Type: Article

References (41)

1. Jacobsson SO,Wallin T, Fowler CJ. Inhibition of rat C6 gliomacell proliferation by endogenous and synthetic cannabinoids. Relative involvement of cannabinoid and vanilloid receptors. J Pharmacol Exp Ther 2001;299:951-9. (Pubitemid 33104965)
2. Blázquez C, Carracedo A, Barrado L, Real PJ, Fernández-Luna JL, Velasco G, et al. Cannabinoid receptors as novel targets for the treatment of melanoma. FASEB J 2006;20:2633-5.
3. Galve-Roperh I, Sánchez C, Cortés ML, del Pulgar TG, Izquierdo M, Guzmán M. Antitumoral action of cannabinoids: Involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat Med 2000;6:313-9. (Pubitemid 30148624)
4. Hinz B, Ramer R, Eichele K, Weinzierl U, Brune K. Up-regulation of cyclooxygenase- 2 expression is involved in R(+)-methanandamide-induced apoptotic death of human neuroglioma cells. Mol Pharmacol 2004;66:1643-51. (Pubitemid 39564792)
5. 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.
6. Blázquez C, Casanova ML, Planas A, Gómez Del Pulgar T, Villanueva C, Fernández-Aceñero MJ, et al. Inhibition of tumor angiogenesis by cannabinoids. FASEB J 2003;17:529-31.
7. Blázquez C, Gonzá lez-Feria L, Alvarez L, Haro A, Casanova ML, Guzmán M. Cannabinoids inhibit the vascular endothelial growth factor pathway in gliomas. Cancer Res 2004;64:5617-23. (Pubitemid 39095557)
8. Pisanti S, Borselli C, Oliviero O, Laezza C, Gazzerro P, Bifulco M. Antiangiogenic activity of the endocannabinoid anandamide: Correlation to its tumor-suppressor efficacy. J Cell Physiol 2007;211:495-503. (Pubitemid 46580103)
9. Wade DT, Makela P, Robson P, House H, Bateman C. Do cannabis-based medicinal extracts have general or specific effects on symptoms in multiple sclerosis? A double-blind, randomized, placebo-controlled study on 160 patients. Mult Scler 2004;10:434-41. (Pubitemid 39117341)
10. Thomas BF, Gilliam AF, Burch DF, Roche MJ, Seltzman HH. Comparative receptor binding analyses of cannabinoid agonists and antagonists. J Pharmacol Exp Ther 1998;285:285-92. (Pubitemid 28207598)
11. Sacerdote P, Martucci C, Vaccani A, Bariselli F, Panerai AE, Colombo A, et al. The nonpsychoactive component of marijuana cannabidiol modulates chemotaxis and IL-10 and IL-12 production of murine macrophages both in vivo and in vitro. J Neuroimmunol 2005;159:97-105. (Pubitemid 40126181)
12. 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. (Pubitemid 38263956)
13. 2 cannabinoid receptors as a novel therapy to treat malignant lymphoblastic disease. Blood 2002;100:627-34. (Pubitemid 34761128)
14. 2 receptor agonists in vitro. Br J Pharmacol 2007;150:613-23. (Pubitemid 46355558)
15. Hayakawa K,Mishima K, HazekawaM, Sano K, Irie K, Orito K, et al. Cannabidiol potentiates pharmacological effects of Delta(9)-tetrahydrocannabinol via CB1 receptor-dependent mechanism. Brain Res 2008;1188:157-64. (Pubitemid 350296050)
16. Watanabe K, Kayano Y, Matsunaga T, Yamamoto I, Yoshimura H. Inhibition of anandamide amidase activity in mouse brain microsomes by cannabinoids. Biol Pharm Bull 1996;19:1109-11. (Pubitemid 26303382)
17. Ligresti A, Moriello AS, Starowicz K, Matias I, Pisanti S, De Petrocellis L, 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. (Pubitemid 44268348)
18. de Filippis D, Iuvone T, d'Amico A, Esposito G, Steardo L, Herman AG, et al. Effect of cannabidiol on sepsis-induced motility disturbances in mice: Involvement of CB receptors and fatty acid amide hydrolase. Neurogastroenterol Motil 2008;20:919-27. (Pubitemid 352019711)
19. Costa B, Giagnoni G, Franke C, Trovato AE, Colleoni M. Vanilloid TRPV1 receptor mediates the antihyperalgesic effect of the nonpsychoactive cannabinoid, cannabidiol, in a rat model of acute inflammation. Br J Pharmacol 2004;143:247-50. (Pubitemid 39315144)
20. Ryberg E, Larsson N, Sjögren S, Hjorth S, Hermansson NO, Leonova J, et al. The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 2007;152:1092-101. (Pubitemid 350166046)
21. McAllister SD, Christian RT, Horowitz MP, Garcia A, Desprez PY. Cannabidiol as a novel inhibitor of Id-1 gene expression in aggressive breast cancer cells. Mol Cancer Ther 2007;6:2921-7. (Pubitemid 350206770)
22. Blázquez C, Salazar M, Carracedo A, Lorente M, Egia A, Gonzá lez-Feria L, et al. Cannabinoids inhibit glioma cell invasion by down-regulating matrix metalloproteinase- 2 expression. Cancer Res 2008;68:1945-52. (Pubitemid 351416581)
23. Ramer R, Hinz B. Inhibition of cancer cell invasion by cannabinoids via increased expression of tissue inhibitor of matrix metalloproteinases-1. J Natl Cancer Inst 2008;100:59-69. (Pubitemid 351767340)
24. Curran S, Murray GI. Matrix metalloproteinases: Molecular aspects of their roles in tumour invasion and metastasis. Eur J Cancer 2000;36:1621-30. (Pubitemid 30616366)
25. Khokha R, Zimmer MJ, Graham CH, Lala PK, Waterhouse P. Suppression of invasion by inducible expression of tissue inhibitor of metalloproteinase-1 (TIMP-1) in B16-F10 melanoma cells. J Natl Cancer Inst 1992;84:1017-22.
26. Cattaneo M, Fontanella E, Canton C, Delia D, Biunno I. SEL1L affects human pancreatic cancer cell cycle and invasiveness throughmodulation of PTEN and genes related to cell-matrix interactions. Neoplasia 2005;7:1030-8.
27. 3) inhibits invasion of HT1080 human fibrosarcoma cells: Role of nuclear factor-kappaB and reactive oxygen species. J Cell Biochem 2005;95:955-69. (Pubitemid 41420143)
28. Park HJ, Lee HJ, Min HY, Chung HJ, Suh ME, Park-Choo HY, et al. Inhibitory effects of a benz(f)indole-4,9-dione analog on cancer cell metastasis mediated by the down-regulation of matrix metalloproteinase expression in human HT1080 fibrosarcoma cells. Eur J Pharmacol 2005;527:31-6. (Pubitemid 41745148)
29. Ramer R, Eichele K, Hinz B. Upregulation of tissue inhibitor of matrix metalloproteinases- 1 confers the anti-invasive action of cisplatin on human cancer cells. Oncogene 2007;26:5822-7. (Pubitemid 47312810)
30. Khokha R, Waterhouse P, Yagel S, Lala PK, Overall CM, Norton G, et al. Antisense RNA-induced reduction in murine TIMP levels confers oncogenicity on Swiss 3T3 cells. Science 1989;24:3947-50.
31. Chan VY, Chan MW, Leung WK, Leung PS, Sung JJ, Chan FK. Intestinal trefoil factor promotes invasion in non-tumorigenic Rat-2 fibroblast cell. Regul Pept 2005;127:87-94. (Pubitemid 40179246)
32. Tong L, Smyth D, Kerr C, Catterall J, Richards CD. Mitogen-activated protein kinases Erk1/2 and p38 are required for maximal regulation of TIMP-1 by oncostatin M in murine fibroblasts. Cell Signal 2004;16:1123-32. (Pubitemid 38900515)
33. Han R, Smith TJ. Induction by IL-1 beta of tissue inhibitor of metalloproteinase- 1 in human orbital fibroblasts: Modulation of gene promoter activity by IL-4 and IFN-gamma. J Immunol 2005;174:3072-9. (Pubitemid 40279729)
34. 2 cannabinoid receptors expressed in prostate PC-3 cells. Involvement in Raf-1 stimulation and NGF induction. Cell Signal 2003;15:851-9. (Pubitemid 36776659)
35. 2 receptor-induced apoptosis of human leukaemia cells. FEBS Lett 2005;579:5084-8. (Pubitemid 41242857)
36. Hinz B, Rosch S, Ramer R, Tamm ER, Brune K. Latanoprost induces matrix metalloproteinase-1 expression in human nonpigmented ciliary epithelial cells through a cyclooxygenase-2-dependentmechanism. FASEB J 2005;19:1929-31. (Pubitemid 41598798)
37. 2 cannabinoid receptors. Eur J Pharmacol 2004;05:1-9. (Pubitemid 39535670)
38. Sativex Product Monograph. Salisbury, Wiltshire U.K.: GW Pharma Ltd.; SP4 0JQ Submission Control No: 091289; April 2005.
39. Consroe P, Kennedy K, Schram K. Assay of plasma cannabidiol by capillary gas chromatography/iontrapmass spectroscopyfollowinghigh-dose repeateddaily oral administration in humans. Pharmacol Biochem Behav 1991;40:517-22.
40. Brandt S, Heller H, Schuster KD, Grote J. Tamoxifen induces suppression of cell viability and apoptosis in the human hepatoblastoma cell line HepG2 via down-regulation of telomerase activity. Liver Int 2004;24:46-54. (Pubitemid 38351213)
41. Kobayashi H, Takemura Y, Ohnuma T. Relationship between tumor cell density and drug concentration and the cytotoxic effects of doxorubicin or vincristine: Mechanism of inoculum effects. Cancer Chemother Pharmacol 1992;31:6-10.