Cannabidiol inhibits lung cancer cell invasion and metastasis via intercellular adhesion molecule-1

FASEB Journal

Volumn 26, Issue 4, 2012, Pages 1535-1548

  Ramer, Robert ^a   Bublitz, Katharina ^a   Freimuth, Nadine ^a   Merkord, Jutta ^a   Rohde, Helga ^a   Haustein, Maria ^a   Borchert, Philipp ^a   Schmuhl, Ellen ^a   Linnebacher, Michael ^a   Hinz, Burkhard ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Cannabinoids; Experimental metastasis; ICAM 1; Tissue inhibitor of metalloproteinases 1

Indexed keywords

BETA ACTIN; CANNABIDIOL; CANNABINOID RECEPTOR; DRONABINOL; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; METHANANDAMIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUTRALIZING ANTIBODY; TISSUE INHIBITOR OF METALLOPROTEINASE 1; VANILLOID RECEPTOR 1;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CANCER PATIENT; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; LUNG CANCER; LUNG NODULE; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN INDUCTION; TUMOR XENOGRAFT; UPREGULATION;

AGED; ANIMALS; CANNABIDIOL; FEMALE; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; LUNG NEOPLASMS; MALE; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; RANDOM ALLOCATION; RNA, SMALL INTERFERING; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TRPV CATION CHANNELS; TUMOR CELLS, CULTURED; UP-REGULATION;

ANIMALIA; MUS MUSCULUS;

EID: 84860895849     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-198184     Document Type: Article

References (60)

1. Jacobsson, S. O., Wallin, T., and Fowler, C. J. (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 (Pubitemid 33104965)
2. Blázquez, C., Carracedo, A., Barrado, L., Real, P. J., Fernández-Luna, J. L., Velasco, G., Malumbres, M., and Guzmán, M. (2006) Cannabinoid receptors as novel targets for the treatment of melanoma. FASEB J. 20, 2633-2635
3. Blázquez, C., Casanova, M. L., Planas, A., Gómez Del Pulgar, T., Villanueva, C., Fernández-Aceñero, M. J., Aragonés, J., Huffman, J. W., Jorcano, J. L., and Guzmán, M. (2003) Inhibition of tumor angiogenesis by cannabinoids. FASEB J. 17, 529-531
4. Blázquez, C., González-Feria, L., Alvarez, L., Haro, A., Casanova, M. L., and Guzmán, M. (2004) Cannabinoids inhibit the vascular endothelial growth factor pathway in gliomas. Cancer Res. 64, 5617-5623
5. Pisanti, S., Borselli, C., Oliviero, O., Laezza, C., Gazzerro, P., and Bifulco, M. (2007) Antiangiogenic activity of the endocannabinoid anandamide: correlation to its tumor-suppressor efficacy. J. Cell. Physiol. 211, 495-503 (Pubitemid 46580103)
6. Galve-Roperh, I., Sánchez, C., Cortés, M. L., del Pulgar, T. G., Izquierdo, M., and Guzmán, M. (2000) Antitumoral action of cannabinoids: involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat. Med. 6, 313-319 (Pubitemid 30148624)
7. Hinz, B., Ramer, R., Eichele, K., Weinzierl, U., and Brune, K. (2004) Up-regulation of cyclooxygenase-2 expression is involved in R(+)-methanandamide- induced apoptotic death of human neuroglioma cells. Mol. Pharmacol. 66, 1643-1651 (Pubitemid 39564792)
8. Salazar, M., Carracedo, A., Salanueva, I. J., Hernández-Tiedra, S., Lorente, M., Egia, A., Vázquez, P., Blázquez, C., Torres, S., García, S., Nowak, J., Fimia, G. M., Piacentini, M., Cecconi, F., Pandolfi, P. P., González-Feria, L., Iovanna, J. L., Guzmán, M., Boya, P., and Velasco, G. (2009) Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J. Clin. Invest. 119, 1359-1372
9. Blázquez, C., Salazar, M., Carracedo, A., Lorente, M., Egia, A., González-Feria, L., Haro, A., Velasco, G., and Guzmán, M. (2008) Cannabinoids inhibit glioma cell invasion by downregulating matrix metalloproteinase-2 expression. Cancer Res. 68, 1945-1952
10. 9- Tetrahydrocannabinol inhibits epithelial growth factor-induced lung cancer cell migration in vitro as well as its growth and metastasis in vivo. Oncogene 27, 339-346
11. Ramer, R., and Hinz, B. (2008) Inhibition of cancer cell invasion by cannabinoids via increased expression of tissue inhibitor of matrix metalloproteinases-1. J. Natl. Cancer Inst. 100, 59-69 (Pubitemid 351767340)
12. McAllister, S. D., Christian, R. T., Horowitz, M. P., Garcia, A., and Desprez, P. Y. (2007) Cannabidiol as a novel inhibitor of Id-1 gene expression in aggressive breast cancer cells. Mol. Cancer Ther. 6, 2921-2927 (Pubitemid 350206770)
13. Ramer, R., Merkord, J., Rohde, H., and Hinz, B. (2010) Cannabidiol inhibits cancer cell invasion via upregulation of tissue inhibitor of matrix metalloproteinases-1. Biochem. Pharmacol. 79, 955-966
14. Ramer, R., Rohde, A., Merkord, J., Rohde, H., and Hinz, B. (2010) Decrease of plasminogen activator inhibitor-1 may contribute to the anti-invasive action of cannabidiol on human lung cancer cells. Pharm. Res. 27, 2162-2174
15. Nithipatikom, K., Endsley, M. P., Isbell, M. A., Falck, J. R., Iwamoto, Y., Hillard, C. J., and Campbell, W. P. (2004) 2-Arachidonoylglycerol: a novel inhibitor of androgen-independent prostate cancer cell invasion. Cancer Res. 64, 8826-8830 (Pubitemid 39665485)
16. Xian, X. S., Park, H., Cho, Y. K., Lee, I. S., Kim, S. W., Choi, M. G., Chung, I. S., Han, K. H., and Park, J. M. (2010) Effect of a synthetic cannabinoid agonist on the proliferation and invasion of gastric cancer cells. J. Cell. Biochem. 110, 321-332
17. 9-tetrahydrocannabinol/cannabidiol for neuropathic pain associated with multiple sclerosis: an uncontrolled, open-label, 2-year extension trial. Clin. Ther. 29, 2068-2079
18. Kogan, N. M., Blázquez, C., Alvarez, L., Gallily, R., Schlesinger, M., Guzmán, M., and Mechoulam, R. (2006) Cannabinoid quinone inhibits angiogenesis by targeting vascular endothelial cells. Mol. Pharmacol. 70, 51-59
19. Ligresti, A., Moriello, A. S., Starowicz, K., Matias, I., Pisanti, S., De Petrocellis, L., Laezza, C., Portella, G., Bifulco, M., and Di Marzo, V. (2006) Antitumor activity of plant cannabinoids with emphasis on the effect of cannabidiol on human breast carcinoma. J. Pharmacol. Exp. Ther. 318, 1375-1387 (Pubitemid 44268348)
20. McKallip, R. J., Jia, W., Schlomer, J., Warren, J. W., Nagarkatti, P. S., and Nagarkatti, M. (2006) Cannabidiol-induced apoptosis in human leukaemia cells: a novel role of cannabidiol in the regulation of p22phox and Nox4 expression. Mol. Pharmacol. 70, 897-908 (Pubitemid 44268447)
21. Massi, P., Vaccani, A., Ceruti, S., Colombo, A., Abbracchio, M. P., and Parolaro, D. (2004) Antitumor effects of cannabidiol, a nonpsychoactive cannabinoid, on human glioma cell lines. J. Pharmacol. Exp. Ther. 308, 838-845 (Pubitemid 38263956)
22. Hubbard, A. K., and Rothlein, R. (2000) Intercellular adhesion molecule-1 (ICAM-1) expression and cell signaling cascades. Free Radic. Biol. Med. 28, 1379-1386 (Pubitemid 30623498)
23. Melis, M., Spatafora, M., Melodia, A., Pace, E., Gjomarkaj, M., Merendino, A. M., and Bonsignore, G. (1996) ICAM-1 expression by lung cancer cell lines: effects of upregulation by cytokines on the interaction with LAK cells. Eur. Respir. J. 9, 1831-1838 (Pubitemid 26294752)
24. Sunami, T., Yashiro, M., and Chung, K. H. (2000) ICAM-1 (intercellular adhesion molecule-1) gene transfection inhibits lymph node metastasis by human gastric cancer cells. Jpn. J. Cancer Res. 91, 925-933
25. Kelly C. P., O'Keane J. C., Orellana J., Schroy P. C. 3rd, Yang S., LaMont, J. T., and Brady, H. R. (1992) Human colon cancer cells express ICAM-1 in vivo and support LFA-1-dependent lymphocyte adhesion in vitro. Am. J. Physiol. 263, G864-G870 (Pubitemid 23033273)
26. Vanky, F., Wang, P., Patarroyo, M., and Klein, E. (1990) Expression of the adhesion molecule ICAM-1 and major histocompatibility complex class I antigens on human tumor cells is required for their interaction with autologous lymphocytes in vitro. Cancer Immunol. Immunother. 31, 19-27 (Pubitemid 20045584)
27. Altomonte, M., Gloghini, A., Bertola, G., Gasparollo, A., Carbone, A., Ferrone, S., and Maio, M. (1993) Differential expression of cell adhesion molecules CD54/CD11a and CD58/CD2 by human melanoma cells and functional role in their interaction with cytotoxic cells. Cancer Res. 53, 3343-3348 (Pubitemid 23223307)
28. Sawada, T., Kimura, K., Nishihara, T., Onoda, N., Teraoka, H., Yamashita, Y., Yamada, N., Yashiro, M., Ohira, M., and Hirakawa, K. (2006) TGF-beta1 down-regulates ICAM-1 expression and enhances liver metastasis of pancreatic cancer. Adv. Med. Sci. 51, 60-65
29. Ogawa, Y., Hirakawa, K., Nakata, B., Fujihara, T., Sawada, T., Kato, Y., Yoshikawa, K., and Sowa, M. (1998) Expression of intercellular adhesion molecule-1 in invasive breast cancer reflects low growth potential, negative lymph node involvement, and good prognosis. Clin. Cancer Res. 4, 31-36 (Pubitemid 28062874)
30. Fujihara, T., Yashiro, M., Inoue, T., Sawada, T., Kato, Y., Ohira, M., Nishiguchi, Y., Ishikawa, T., Sowa, M., and Chung, K. H. (1999) Decrease in ICAM-1 expression on gastric cancer cells is correlated with lymph node metastasis. Gastric Cancer 2, 221-225
31. Maeda, K., Kang, S. M., Sawada, T., Nishiguchi, Y., Yashiro, M., Ogawa, Y., Ohira, M., Ishikawa, T., and Hirakawa-YS Chung, K. (2002) Expression of intercellular adhesion molecule-1 and prognosis in colorectal cancer. Oncol. Rep. 9, 511-514
32. Huang, W. C., Chan, S. T., Yang, T. L., Tzeng, C. C., and Chen, C. C. (2004) Inhibition of ICAM- 1 gene expression, monocyte adhesion and cancer cell invasion by targeting IKK complex: Molecular and functional study of novel alpha-methylene-gamma- butyrolactone derivatives. Carcinogenesis 25, 1925-1934
33. Rosette, C., Roth, R. B., Oeth, P., Braun, A., Kammerer, S., Ekblom, J., and Denissenko, M. F. (2005) Role of ICAM1 in invasion of human breast cancer cells. Carcinogenesis 26, 943-950 (Pubitemid 41214323)
34. Lin, Y. C., Shun, C. T., Wu, M. S., and Chen, C. C. (2006) A novel anticancer effect of thalidomide: inhibition of intercellular adhesion molecule-1-mediated cell invasion and metastasis through suppression of nuclear factor-κB. Clin. Cancer Res. 12, 7165-7173
35. Miele, M. E., Bennett, C. F., Miller, B. E., and Welch, D. R. (1994) Enhanced metastatic ability of TNF-α-treated malignant melanoma cells is reduced by intercellular adhesion molecule-1 (ICAM-1, CD54) antisense oligonucleotides. Exp. Cell Res. 214, 231-241 (Pubitemid 24302397)
36. Koyama, Y., Tanaka, Y., Saito, K., Abe, M., Nakatsuka, K., Morimoto, I., Auron, P. E., and Eto, S. (1996) Cross-linking of intercellular adhesion molecule 1 (CD54) induces AP-1 activation and IL-1β transcription. J. Immunol. 157, 5097-5103 (Pubitemid 126449591)
37. Sano, H., Nakagawa, N., Chiba, R., Kurasawa, K., Saito, Y., and Iwamoto, I. (1998) Cross-linking of intercellular adhesion molecule- 1 induces interleukin-8 and RANTES production through the activation of MAP kinases in human vascular endothelial cells. Biochem. Biophys. Res. Commun. 250, 694-698 (Pubitemid 28484790)
38. Lawson, C., Ainsworth, M., Yacoub, M., and Rose, M. (1999) Ligation of ICAM-1 on endothelial cells leads to expression of VCAM-1 via a nuclear factor-κB-independent mechanism. J. Immunol. 162, 2990-2996 (Pubitemid 29309328)
39. Blaber, R., Stylianou, E., Clayton, A., and Steadman, R. (2003) Selective regulation of ICAM-1 and RANTES gene expression after ICAM-1 ligation on human renal fibroblasts. J. Am. Soc. Nephrol. 14, 116-127 (Pubitemid 36026303)
40. Edwards, D. R., Rocheleau, H., Sharma, R. R., Wills, A. J., Cowie, A., Hassell, J. A., and Heath, J. K. (1992) Involvement of AP1 and PEA3 binding sites in the regulation of murine tissue inhibitor of metalloproteinases-1 (TIMP-1) transcription. Biochim. Biophys. Acta 1171, 41-55
41. Bugno, M., Graeve, L., Gatsios, P., Koj, A., Heinrich, P. C., Travis, J., and Kordula, T. (1995) Identification of the interleukin-6/oncostatin M response element in the rat tissue inhibitor of metalloproteinases-1 (TIMP-1) promoter. Nucleic Acids Res. 23, 5041-5047 (Pubitemid 26012487)
42. Ramer, R., Eichele, K., and Hinz, B. (2007) Upregulation of tissue inhibitor of matrix metalloproteinases-1 confers the anti-invasive action of cisplatin on human cancer cells. Oncogene 26, 5822-5827 (Pubitemid 47312810)
43. Hinz, B., Rösch, S., Ramer, R., Tamm, E. R., and Brune, K. (2005) Latanoprost induces matrix metalloproteinase-1 expression in human nonpigmented ciliary epithelial cells through a cyclooxygenase-2-dependent mechanism. FASEB J. 19, 1929-1931 (Pubitemid 41598798)
44. Mukherjee, S., Adams, M., Whiteaker, K., Daza, A., Kage, K., Cassar, S., Meyer, M., and Yao, B. B. (2004) Species comparison and pharmacological characterization of rat and human CB2cannabinoid receptors. Eur. J. Pharmacol. 505, 1-9 (Pubitemid 39535670)
45. Izzo, A. A., Borrelli, F., Capasso, R., Di Marzo, V., and Mechoulam, R. (2009) Non-psychotropic plant cannabinoids: new therapeutic opportunities from an ancient herb. Trends Pharmacol. Sci. 30, 515-527
46. Consroe, P., Kennedy, K., and Schram, K. (1991) Assay of plasma cannabidiol by capillary gas chromatography/ion trap mass spectroscopy following high-dose repeated daily oral administration in humans. Pharmacol. Biochem. Behav. 40, 517-522
47. Scaldaferri, F., Sans, M., Vetrano, S., Correale, C., Arena, V., Pagano, N., Rando, G., Romeo, F., Potenza, A. E., Repici, A., Malesci, A., and Danese, S. (2009) The role of MAPK in governing lymphocyte adhesion to and migration across the microvasculature in inflammatory bowel disease. Eur. J. Immunol. 39, 290-300
48. Sapna, S., and Shivakumar, K. (2007) Hypoxia and antioxidants enhance soluble ICAM-1 release from cardiac fibroblasts. Mol. Cell. Biochem. 303, 259-262 (Pubitemid 47261325)
49. Lee, H. M., Kim, H. J., Won, K. J., Choi, W. S., Lee, K. Y., Bae, Y. M., Park, P. J., Park, T. K., Lee, Y. L., Lee, C. K., and Kim, B. (2008) Contribution of soluble intercellular adhesion molecule- 1 to the migration of vascular smooth muscle cells. Eur. J. Pharmacol. 579, 260-268
50. Chen, C., Chou, C., Sun, Y., and Huang, W. (2001) Tumor necrosis factor alpha-induced activation of downstream NF-κB site of the promoter mediates epithelial ICAM-1 expression and monocyte adhesion. Involvement of PKCα, tyrosine kinase, and IKK2, but not MAPKs, pathway. Cell. Signal. 13, 543-553 (Pubitemid 32722113)
51. Radisavljevic, Z., Avraham, H., and Avraham, S. (2000) Vascular endothelial growth factor up-regulates ICAM-1 expression via the phosphatidylinositol 3 OH-kinase/AKT/Nitric oxide pathway and modulates migration of brain microvascular endothelial cells. J. Biol. Chem. 275, 20770-20774 (Pubitemid 30457667)
52. Natali, P., Nicotra, M. R., Cavaliere, R., Bigotti, A., Romano, G., Temponi, M., and Ferrone, S. (1990) Differential expression of intercellular adhesion molecule 1 in primary and metastatic melanoma lesions. Cancer Res. 50, 1271-1278 (Pubitemid 20084022)
53. Hosch, S. B., Meyer, A. J., Schneider, C., Stoecklein, N., Prenzel, K. L., Pantel, K., Broelsch, C. E., and Izbicki, J. R. (1997) Expression and prognostic significance of HLA class I, ICAM-1, and tumor-infiltrating lymphocytes in esophageal cancer. J. Gastrointest. Surg. 1, 316-323 (Pubitemid 127432776)
54. Shin, H. S., Jung, C. H., Park, H. D., and Lee, S. S. (2004) The relationship between the serum intercellular adhesion molecule-1 level and the prognosis of the disease in lung cancer. Korean J. Intern. Med. 19, 48-52 (Pubitemid 41237489)
55. Yu, M., Han, J., Cui, P., Dai, M., Li, H., Zhang, J., and Xiu, R. (2008) Cisplatin up-regulates ICAM-1 expression in endothelial cell via a NF-κB dependent pathway. Cancer Sci. 99, 391-397 (Pubitemid 351228497)
56. Mukhopadhyay, P., Rajesh, M., Pan, H., Patel, V., Mukhopadhyay, B., Bátkai, S., Gao, B., Haskó G, and Pacher, P. (2010) Cannabinoid-2 receptor limits inflammation, oxidative/nitrosative stress, and cell death in nephropathy. Free Radic. Biol. Med. 48, 457-467
57. Rajesh, M., Mukhopadhyay, P., Bátkai, S., Haskó G, Liaudet, L., Drel, V. R., Obrosova, I. G., and Pacher, P. (2007) Cannabidiol attenuates high glucose-induced endothelial cell inflammatory response and barrier disruption. Am. J. Physiol. Heart Circ. Physiol. 293, H610-H619 (Pubitemid 47105122)
58. Shepherd, F. A., Giaccone, G., Seymour, L., Debruyne, C., Bezjak, A., Hirsh, V., Smylie, M., Rubin, S., Martins, H., Lamont, A., Krzakowski, M., Sadura, A., and Zee, B. (2002) Prospective, randomized, double-blind, placebo-controlled trial of marimastat after response to first-line chemotherapy in patients with small-cell lung cancer: a trial of the National Cancer Institute of Canada-Clinical Trials Group and the European Organization for Research and Treatment of Cancer. J. Clin. Oncol. 20, 4434-4439 (Pubitemid 35334754)
59. Bramhall, S. R., Schulz, J., Nemunaitis, J., Brown, P. D., Baillet, M., and Buckels, J. A. (2002) A double-blind placebo-controlled, randomised study comparing gemcitabine and marimastat with gemcitabine and placebo as first line therapy in patients with advanced pancreatic cancer. Br. J. Cancer 87, 161-167
60. Bissett, D., O'Byrne, K. J., von Pawel, J., Gatzemeier, U., Price, A., Nicolson, M., Mercier, R., Mazabel, E., Penning, C., Zhang, M. H., Collier, M. A., and Shepherd, F. A. (2005) Phase III study of matrix metalloproteinase inhibitor prinomastat in non-small-cell lung cancer. J. Clin. Oncol. 23, 842-849 (Pubitemid 46224184)