Inhibition of skin tumor growth and angiogenesis in vivo by activation of cannabinoid receptors

Journal of Clinical Investigation

Volumn 111, Issue 1, 2003, Pages 43-50

  Llanos Casanova, M ^a   Blázquez, Cristina ^b   Martínez Palacio, Jesús ^a   Villanueva, Concepción ^c   Fernández Aceñero, M Jesús ^c   Huffman, John W ^d   Jorcano, José L ^a   Guzmán, Manuel ^b  

^a CIEMAT   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c HOSPITAL DE MÓSTOLES   (Spain)

^d CLEMSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ANGIOPOIETIN 2; ANTINEOPLASTIC AGENT; CANNABINOID RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CULTURE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; EPIDERMIS CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SKIN TUMOR;

ANGIOGENESIS INDUCING AGENTS; ANGIOPOIETIN-2; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; BROMODEOXYURIDINE; CANNABINOIDS; CELL LINE, TRANSFORMED; ENDOTHELIAL GROWTH FACTORS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOKINES; MICE; MORPHOLINES; NAPHTHALENES; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, CANNABINOID; RECEPTORS, DRUG; SKIN NEOPLASMS; TIME FACTORS; TISSUE DISTRIBUTION; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0037253496     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200316116     Document Type: Article

References (42)

1. Fuchs, E. 1990. Epidermal differentiation: the bare essential. J. Cell Biol. 11:2807-2814.
2. Limmer, B.L. 2001. Nonmelanoma skin cancer: today's epidemic. Tex. Med. 97:56-58.
3. Morris, R.J., Tryson, K.A., and Wu, K.Q. 2000. Evidence that the epidermal targets of carcinogen action are found in the interfollicular epidermis of infundibulum as well as in the hair follicles. Cancer Res. 60:226-229.
4. Bolontrade, M.F., et al. 1998. Angiogenesis is an early event in the development of chemically induced skin tumors. Carcinogenesis. 19:2107-2113.
5. Zhang, H.T., et al. 1995. Enhancement of tumor growth and vascular density by transfection of vascular endothelial cell growth factor into MCF-7 human breast carcinoma cells. J. Natl. Cancer Inst. 87:213-219.
6. Larcher, F., et al. 1996. Up-regulation of vascular endothelial growth factor/vascular permeability factor in mouse skin carcinogenesis correlates with malignant progression state and activated H-ras expression levels. Cancer Res. 56:5391-5396.
7. Larcher, F., Murillas, R., Bolontrade, M., Conti, C.J., and Jorcano, J.L. 1998. VEGF/VPF overexpression in skin of transgenic mice induces angiogenesis, vascular hyperpermeability and accelerated tumor development. Oncogene. 17:303-311.
8. Sibilia, M., et al. 2000. The EGF receptor provides an essential survival signal for SOS-dependent skin tumor development. Cell. 102:211-220.
9. Casanova, M.L., et al. 2002. A critical role for ras-mediated, EGFR-dependent angiogenesis in mouse skin carcinogenesis. Cancer Res. 62:3402-3407.
10. Skidmore, R.A., and Flowers, F.P. 1998. Nonmelanoma skin cancer. Med. Clin. North Am. 82:1309-1323.
11. Leber, K., Perron, V.D., and Sinni-McKeehen, B. 1999. Common skin cancers in the United States: a practical guide for diagnosis and treatment. Nurse Pract. Forum. 10:106-112.
12. De Rosa, F.S., and Bentley, M.V. 2000. Photodynamic therapy of skin cancers: sensitizers, clinical studies and future directives. Pharm. Res. 17:1447-1455.
13. Pertwee, R.G. 2000. Cannabinoid receptor ligands: clinical and neuropharmacological considerations, relevant to future drug discovery and development. Exp. Opin. Investig. Drugs. 9:1-19.
14. Piomelli, D., Giuffrida, A., Calignano, A., and Rodríguez de Fonseca, F. 2000. The endocannabinoid system as a target for therapeutic drugs. Trends Pharmacol. Sci. 21:218-224.
15. Porter, A.C., and Felder, C.C. 2001. The endocannabinoid nervous system: unique opportunities for therapeutic intervention. Pharmacol. Ther. 90:45-60.
16. Devane, W.A., et al. 1992. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science. 258:1946-1949.
17. Mechoulam, R., et al. 1995. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 50:83-90.
18. Matsuda, L.A., Lolait, S.J., Brownstein, M., Young, A., and Bonner, T.I. 1990. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature. 346:561-564.
19. Munro, S., Thomas, K.L., and Abu-Shaar, M. 1993. Molecular characterization of a peripheral receptor for cannabinoids. Nature. 365:61-65.
20. Munson, A.E., Harris, L.S., Friedman, M.A., Dewey, W.L., and Carchman, R.A. 1975. Antineoplastic activity of cannabinoids. J. Natl. Cancer Inst. 55:597-602.
21. Galve-Roperh, I., et al. 2000. Anti-tumoral action of cannabinoids: Involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat. Med. 6:313-319.
22. 2 cannabinoid receptor. Cancer Res. 61:5784-5789.
23. Bifulco, M., et al. 2001. Control by the endogenous cannabinoid system of ras oncogene-dependent tumor growth. FASEB J. 15:2745-2747.
24. Guzmán, M., Sánchez, C., and Galve-Roperh, I. 2001. Control of the cell survival/death decision by cannabinoids. J. Mol. Med. 78:613-625.
25. 2 receptor. Bioorg. Med. Chem. Lett. 7:2905-2914.
26. Blázquez, C., Galve-Roperh, I., and Guzmán, M. 2000. De novo-synthesized ceramide signals apoptosis in astrocytes via extracellular signal-regulated kinase. FASEB J. 14:2315-2322.
27. Chomczynski, P., and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 162:156-159.
28. Carmeliet, P., and Jain, R.K. 2000. Angiogenesis in cancer and other diseases. Nature. 407:249-257.
29. Yancopoulos, G.D., et al. 2000. Vascular-specific growth factors and blood vessel formation. Nature. 407:242-248.
30. Hunts, J, et al. 1985. Hyperproduction and gene amplifications of the EGFR in squamous cell carcinomas. Jpn. J. Cancer Res. 76:633-666.
31. Rho, O., Beltran, L.M., Conti-Giménez, I.B., and DiGiovanni, J. 1994. Altered expression of the epidermal growth factor receptor and transforming growth factor-alpha during multistage skin carcinogenesis in SENCAR mice. Mol. Carcinog. 11:19-28.
32. Hawighorst, T., et al. 2001. Thrombospondin-2 plays a protective role in multistep carcinogenesis: a novel host anti-tumor defense mechanism. EMBO J. 20:2631-2640.
33. Grugel, S., Finkenzeller, G., Weindel, K., Barleon, B., and Marme, D. 1995. Both v-Ha-Ras and v-Raf stimulate expression of the vascular endothelial growth factor in NIH 3T3 cells. J. Biol. Chem. 270:25915-25919.
34. Rak, J., et al. 1995. Mutant ras oncogenes upregulate VEGF/VPF expression: implications for induction and inhibition of tumor angiogenesis. Cancer Res. 55:4575-4580.
35. Luetteke, N.C., et al. 1993. TGF alpha deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell. 73:263-278.
36. Luetteke, N.C., et al. 1994. The mouse waved-2 phenotype results from a point mutation in the EGF receptor tyrosine kinase. Genes Dev. 8:399-413.
37. Murillas, R., Larcher, F., Conti, C.J., Santos, M., and Jorcano, J.L. 1995. Expression of a dominant negative mutant of epidermal growth factor receptor in the epidermis of transgenic mice elicits striking alterations in hair follicle development and skin structure. EMBO J. 14:5216-5223.
38. Jost, M., Kari, C., and Rodeck, U. 2000. The EGF receptor - An essential regulator of multiple epidermal functions. Eur. J. Dermatol. 10:505-510.
39. Izumi, Y., Xu, L., Di Tomaso, E., Fukumura, D., and Jain, R.K. 2002. Herceptin acts as an anti-angiogenic cocktail. Nature. 416:279-280.
40. Calignano, A., La Rana, G., Giuffrida, A., and Piomelli, D. 1998. Control of pain initiation by endogenous cannabinoids. Nature. 394:277-281.
41. 2, a peripheral cannabinoid receptor. Proc. Natl. Acad. Sci. USA. 96:14228-14233.
42. 2 cannabinoid receptor-mediated peripheral antinociception. Pain. 93:239-245.