Novel Hedgehog pathway targets against basal cell carcinoma

Toxicology and Applied Pharmacology

Volumn 224, Issue 3, 2007, Pages 257-264

  Tang, Jean Y ^a   So, Po Lin ^a   Epstein Jr , Ervin H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Basal cell carcinoma; Chemoprevention; Hedgehog signaling; Ptch; Skin cancer; Statins; UV light; Vitamin D

Indexed keywords

20 HYDROXYCHOLESTEROL; 25 HYDROXYCHOLESTEROL; 7 DEHYDROCHOLESTEROL; ANTINEOPLASTIC AGENT; CHOLESTEROL DERIVATIVE; CYCLODEXTRIN; CYCLOPAMINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; ISOTRETINOIN; N (3 METHOXYBENZYL) 3,3 DIMETHYL N [1 (3,4 METHYLENEDIOXYBENZYL) 2 (1 PIPERAZINYLCARBONYL) 4 PYRROLIDINYL]BUTYRAMIDE; PROTEIN PATCHED 1; RETINOID; SIMVASTATIN; SONIC HEDGEHOG PROTEIN; STEROL; TAZAROTENE; UNCLASSIFIED DRUG; VITAMIN D;

BASAL CELL CARCINOMA; BASAL CELL NEVUS SYNDROME; CANCER INCIDENCE; CARCINOGENESIS; CHEMOPROPHYLAXIS; DIET THERAPY; HETEROZYGOSITY; HUMAN; LOW FAT DIET; NONHUMAN; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SUNLIGHT; VITAMIN SUPPLEMENTATION;

ANIMALS; CARCINOMA, BASAL CELL; HEDGEHOG PROTEINS; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; STEROLS; VITAMIN D; VITAMINS;

ERINACEIDAE; VERTEBRATA;

EID: 35348872467     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2006.12.011     Document Type: Review

References (60)

1. Armstrong B.K., and Kricker A. The epidemiology of UV induced skin cancer. J. Photochem. Photobiol., B 63 (2001) 8-18
2. Aszterbaum M., Rothman A., Johnson R.L., Fisher M., Xie J., Bonifas J.M., Zhang X., Scott M.P., and Epstein Jr. E.H. Identification of mutations in the human PATCHED gene in sporadic basal cell carcinomas and in patients with the basal cell nevus syndrome. J. Invest. Dermatol. 110 (1998) 885-888
3. Aszterbaum M., Epstein J., Oro A., Douglas V., LeBoit P.E., Scott M.P., and Epstein Jr. E.H. Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice. Nat. Med. 5 (1999) 1285-1291
4. Athar M., Li C., Tang X., Chi S., Zhang X., Kim A.L., Tyring S.K., Kopelovich L., Hebert J., Epstein Jr. E.H., et al. Inhibition of Smoothened signaling prevents ultraviolet B-induced basal cell carcinomas through regulation of Fas expression and apoptosis. Cancer Res. 64 (2004) 7545-7552
5. Athar M., Tang X., Lee J.L., Kopelovich L., and Kim A.L. Hedgehog signalling in skin development and cancer. Exp. Dermatol. 15 (2006) 667-677
6. Bianchi L., Orlandi A., Campione E., Angeloni C., Costanzo A., Spagnoli L.G., and Chimenti S. Topical treatment of basal cell carcinoma with tazarotene: a clinicopathological study on a large series of cases. Br. J. Dermatol. 151 (2004) 148
7. 3 secretion. PLoS Biol. 4 8 (2006) 1397-1410
8. Black H.S., Herd J.A., Goldberg L.H., Wolf Jr. J.E., Thornby J.I., Rosen T., Bruce S., Tschen J.A., Foreyt J.P., Scott L.W., et al. Effect of a low-fat diet on the incidence of actinic keratosis. N. Engl. J. Med. 330 (1994) 1272-1275
9. Black H.S., Thornby J.I., Wolf Jr. J.E., Goldberg L.H., Herd J.A., Rosen T., Bruce S., Tschen J.A., Scott L.W., Jaax S., et al. Evidence that a low-fat diet reduces the occurrence of non-melanoma skin cancer. Int. J. Cancer 62 (1995) 165-169
10. Chen Y., Gallaher N., Goodman R.H., and Smolik S.M. Protein kinase A directly regulates the activity and proteolysis of cubitus interruptus. Proc. Natl. Acad. Sci. 95 (1998) 2349-2354
11. Chen J.K., Taipale J., Cooper M.K., and Beachy P.A. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16 (2002) 2743-2748
12. Chen J.K., Taipale J., Young K.E., Maiti T., and Beachy P.A. Small molecule modulation of Smoothened activity. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 14071
13. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., and Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383 (1996) 407-413
14. Christenson L.J., Borrowman T.A., Vachon C.M., Tollefson M.M., Otley C.C., Weaver A.L., and Roenigk R.K. Incidence of basal cell and squamous cell carcinomas in a population younger than 40 years. JAMA 294 (2005) 681-690
15. Chuang P.-T., and McMahon A.P. Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature 397 (1999) 617
16. Cooper M.K., Porter J.A., Young K.E., and Beachy P.A. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 280 (1998) 1603
17. Cooper M.K., Wassif C.A., Krakowiak P.A., Taipale J., Gong R., Kelley R.I., Porter F.D., and Beachy P.A. A defective response to Hedgehog signaling in disorders of cholesterol biosynthesis. Nat. Genet. 33 (2003) 508-513
18. Corbit K.C., Aanstad P., Singla V., Norman A.R., Stainier D.Y.R., and Reiter J.F. Vertebrate Smoothened functions at the primary cilium. Nature 437 (2005) 1018
19. Corcoran R.B., and Scott M.P. Oxysterols stimulate Sonic hedgehog signal transduction and proliferation of medulloblastoma cells. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 8408-8413
20. Corona R., Dogliotti E., D'Errico M., Sera F., Iavarone I., Baliva G., Chinni L.M., Gobello T., Mazzanti C., Puddu P., and Pasquini P. Risk factors for basal cell carcinoma in a Mediterranean population: role of recreational sun exposure early in life. Arch. Dermatol. 137 (2001) 1162-1168
21. Dahmane N., Lee J., Robins P., Heller P., and Ruiz i Altaba A. Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature 389 (1997) 876-881
22. Dellavalle R., Drake A., Graber M., Heilig L., Hester E., Johnson K., McNealy K., Schilling L., and Dellavalle R. Statins and fibrates for preventing melanoma. Cochrane Database Syst. Rev. (2005) CD003697
23. Demierre M.F., Higgins P.D., Gruber S.B., Hawk E., and Lippman S.M. Statins and cancer prevention. Nat. Rev., Cancer 5 (2005) 930-942
24. Edison R.J., and Muenke M. Central nervous system and limb anomalies in case reports of first-trimester statin exposure. N. Engl. J. Med. 350 (2004) 1579-1582
25. Eichberger T., Regl G., Ikram M.S., Neill G.W., Philpott M.P., Aberger F., and Frischauf A.M. FOXE1, a new transcriptional target of GLI2 is expressed in human epidermis and basal cell carcinoma. J. Invest. Dermatol. 122 (2004) 1180-1187
26. Fan H., Oro A.E., Scott M.P., and Khavari P.A. Induction of basal cell carcinoma features in transgenic human skin expressing Sonic Hedgehog. Nat. Med. 3 (1997) 788-792
27. Frieling U.M., Schaumberg D.A., Kupper T.S., Muntwyler J., and Hennekens C.H. A randomized, 12-year primary-prevention trial of beta carotene supplementation for nonmelanoma skin cancer in the physicians' health study. Arch. Dermatol. 136 (2000) 179-184
28. Garland C., Barrett-Connor E., Rossof A., Shekelle R., Criqui M., and Paul O. Dietary vitamin D and calcium and risk of colorectal cancer: a 19-year prospective study in men. Lancet 325 (1985) 307
29. Garland C.F., Garland F.C., Gorham E.D., Lipkin M., Newmark H., Mohr S.B., and Holick M.F. The role of vitamin D in cancer prevention. Am. J. Public Health 96 (2006) 252-261
30. Goodrich L.V., Milenkovic L., Higgins K.M., and Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277 (1997) 1109
31. Grachtchouk M., Mo R., Yu S., Zhang X., Sasaki H., Hui C.C., and Dlugosz A.A. Basal cell carcinomas in mice overexpressing Gli2 in skin. Nat. Genet. 24 (2000) 216-217
32. Grachtchouk V., Grachtchouk M., Lowe L., Johnson T., Wei L., Wang A., de Sauvage F., and Dlugosz A.A. The magnitude of hedgehog signaling activity defines skin tumor phenotype. EMBO J. 22 (2003) 2741-2751
33. Grau M.V., Baron J.A., Langholz B., Karagas M., Greenberg E.R., Stukel T.A., and Mandel J.S. Effect of NSAIDs on the recurrence of nonmelanoma skin cancer. Int. J. Cancer 119 (2006) 682-686
34. Green A., Williams G., Nale R., Hart V., Leslie D., Parsons P., Marks G.C., Gaffney P., Battistutta D., and Frost C. Daily sunscreen application and betacarotene supplementation in prevention of basal-cell and squamous-cell carcinomas of the skin: a randomised controlled trial. Lancet 354 (1999) 723
35. Hahn H., Wicking C., Zaphiropoulous P.G., Gailani M.R., Shanley S., Chidambaram A., Vorechovsky I., Holmberg E., Unden A.B., Gillies S., et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 85 (1996) 841
36. Hooper J.E., and Scott M.P. Communicating with Hedgehogs. Nat. Rev., Mol. Cell Biol. 6 (2005) 306-317
37. Hutchin M.E., Kariapper M.S., Grachtchouk M., Wang A., Wei L., Cummings D., Liu J., Michael L.E., Glick A., and Dlugosz A.A. Sustained Hedgehog signaling is required for basal cell carcinoma proliferation and survival: conditional skin tumorigenesis recapitulates the hair growth cycle. Genes Dev. 19 (2005) 214-223
38. Incardona J.P., and Roelink H. The role of cholesterol in Shh signaling and teratogen-induced holoprosencephaly. Cell. Mol. Life Sci. 57 (2000) 1709-1719
39. Ingham P.W., and McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15 (2001) 3059-3087
40. Johnson R.L., Rothman A.L., Xie J., Goodrich L.V., Bare J.W., Bonifas J.M., Quinn A.G., Myers R.M., Cox D.R., Epstein Jr. E.H., and Scott M.P. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 272 (1996) 1668-1671
41. Kogerman P., Grimm T., Kogerman L., Krause D., Unden A.B., Sandstedt B., Toftgard R., and Zaphiropoulos P.G. Mammalian Suppressor-of-Fused modulates nuclear-cytoplasmic shuttling of GLI-1. Nat. Cell Biol. 1 (1999) 312
42. Ling G., Ahmadian A., Persson A., Unden A.B., Afink G., Williams C., Uhlen M., Toftgard R., Lundeberg J., and Ponten F. PATCHED and p53 gene alterations in sporadic and hereditary basal cell cancer. Oncogene 20 (2001) 7770-7778
43. Mancuso M., Pazzaglia S., Tanori M., Hahn H., Merola P., Rebessi S., Atkinson M.J., Di Majo V., Covelli V., and Saran A. Basal cell carcinoma and its development: insights from radiation-induced tumors in Ptch1-deficient mice. Cancer Res. 64 (2004) 934-941
44. Martinez M.E., Giovannucci E.L., Colditz G.A., Stampfer M.J., Hunter D.J., Speizer F.E., Wing A., and Willett W.C. Calcium, vitamin D, and the occurrence of colorectal cancer among women. J. Natl. Cancer Inst. 88 (1996) 1375
45. McNaughton S.A., Marks G.C., and Green A.C. Role of dietary factors in the development of basal cell cancer and squamous cell cancer of the skin. Cancer Epidemiol., Biomarkers Prev. 14 (2005) 1596-1607
46. Miller D.L., and Weinstock M.A. Nonmelanoma skin cancer in the United States: incidence. J. Am. Acad. Dermatol. 30 (1994) 774-778
47. 3 in rat colon carcinogenesis. Nutr. Cancer 38 (2000) 65-73
48. Nilsson M., Unden A.B., Krause D., Malmqwist U., Raza K., Zaphiropoulos P.G., and Toftgard R. Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc. Natl. Acad. Sci. 97 (2000) 3438-3443
49. Quinn A.G., and Epstein Jr. E. Patched, hedgehog, and skin cancer. Methods Mol. Biol. 222 (2003) 85-95
50. Regl G., Kasper M., Schnidar H., Eichberger T., Neill G.W., Philpott M.P., Esterbauer H., Hauser-Kronberger C., Frischauf A.M., and Aberger F. Activation of the BCL2 promoter in response to Hedgehog/GLI signal transduction is predominantly mediated by GLI2. Cancer Res. 64 (2004) 7724-7731
51. Rubin L.L., and de Sauvage F.J. Targeting the Hedgehog pathway in cancer. Nat. Rev., Drug Discov. 5 (2006) 1026
52. Rubin A.I., Chen E.H., and Ratner D. Basal-cell carcinoma. N. Engl. J. Med. 353 (2005) 2262-2269
53. So P.L., Langston A.W., Daniallinia N., Hebert J.L., Fujimoto M.A., Khaimskiy Y., Aszterbaum M., and Epstein Jr. E.H. Long-term establishment, characterization and manipulation of cell lines from mouse basal cell carcinoma tumors. Exp. Dermatol. 15 (2006) 742-750
54. Svard J., Henricson K.H., Persson-Lek M., Rozell B., Lauth M., Bergstrom A., Ericson J., Toftgard R., and Teglund S. Genetic elimination of suppressor of fused reveals an essential repressor function in the mammalian hedgehog signaling pathway. Dev. Cell 10 (2006) 187
55. Taipale J., Cooper M.K., Maiti T., and Beachy P.A. Patched acts catalytically to suppress the activity of Smoothened. Nature 418 (2002) 892-897
56. Teh M.T., Wong S.T., Neill G.W., Ghali L.R., Philpott M.P., and Quinn A.G. FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res. 62 (2002) 4773-4780
57. Williams J.A., Guicherit O.M., Zaharian B.I., Xu Y., Chai L., Wichterle H., Kon C., Gatchalian C., Porter J.A., Rubin L.L., and Wang F.Y. Identification of a small molecule inhibitor of the hedgehog signaling pathway: effects on basal cell carcinoma-like lesions. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 4616-4621
58. Wright T.I., Spencer J.M., and Flowers F.P. Chemoprevention of nonmelanoma skin cancer. J. Am. Acad. Dermatol. 54 (2006) 933
59. Xie J., Murone M., Luoh S.M., Ryan A., Gu Q., Zhang C., Bonifas J.M., Lam C.W., Hynes M., Goddard A., et al. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 391 (1998) 90-92
60. Zinser G.M., Sundberg J.P., and Welsh J. Vitamin D(3) receptor ablation sensitizes skin to chemically induced tumorigenesis. Carcinogenesis 23 (2002) 2103-2109