Sonic hedgehog signaling in basal cell carcinomas

Cancer Letters

Volumn 225, Issue 2, 2005, Pages 181-192

  Daya Grosjean, Leela ^a   Couvé Privat, Sophie ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

Basal cell carcinoma; Mutation; Patched; Smoothened; Sonic hedgehog; Ultraviolet

Indexed keywords

ALKALOID; CYCLOPAMINE; HEDGEHOG INTERACTING PROTEIN; IMMUNOSUPPRESSIVE AGENT; MEMBRANE PROTEIN; N (3 METHOXYBENZYL) 3,3 DIMETHYL N [1 (3,4 METHYLENEDIOXYBENZYL) 2 (1 PIPERAZINYLCARBONYL) 4 PYRROLIDINYL]BUTYRAMIDE; PLANT EXTRACT; PROTEIN; PROTEIN INHIBITOR; PROTEIN PATCHED; PROTEIN PATCHED 2; PROTEIN SMOOTHENED; PROTEIN WINGED; PSORALEN; RECOMBINANT PROTEIN; SIGNAL PEPTIDE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR GLI3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BASAL CELL CARCINOMA; BASAL CELL NEVUS SYNDROME; CANCER RISK; CAUCASIAN; CODON; ENVIRONMENTAL EXPOSURE; EXPERIMENTAL MODEL; FRAMESHIFT MUTATION; GENE INACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ENGINEERING; GEOGRAPHIC DISTRIBUTION; GERM LINE; HUMAN; IMMUNE DEFICIENCY; IONIZING RADIATION; MELANOMA; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; NONSENSE MUTATION; PRIORITY JOURNAL; PROTO ONCOGENE; RADIATION CARCINOGENESIS; RADIATION EXPOSURE; REGULATORY MECHANISM; SHORT SURVEY; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; TUMOR SUPPRESSOR GENE; ULTRAVIOLET RADIATION; XERODERMA PIGMENTOSUM;

ERINACEIDAE;

EID: 20644431776     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2004.10.003     Document Type: Review

References (96)

1. A.P. McMahon, P.W. Ingham, and C.J. Tabin Developmental roles and clinical significance of hedgehog signaling Curr. Top. Dev. Biol. 53 2003 1 114
2. Y. Echelard, D.J. Epstein, B. St-Jacques, L. Shen, J. Mohler, J.A. McMahon, and A.P. McMahon Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity Cell 75 1993 1417 1430
3. S. Pathi, S. Pagan-Westphal, D.P. Baker, E.A. Garber, P. Rayhorn, and D. Bumcrot Comparative biological responses to human Sonic, Indian, and Desert hedgehog Mech. Dev. 106 2001 107 117
4. A. Ruiz i Altaba, P. Sanchez, and N. Dahmane Gli and hedgehog in cancer: tumours, embryos and stem cells Nat. Rev. Cancer 2 2002 361 372
5. I.A.A. Ruiz, V. Palma, and N. Dahmane Hedgehog-Gli signalling and the growth of the brain Nat. Rev. Neurosci. 3 2002 24 33
6. E. Belloni, M. Muenke, E. Roessler, G. Traverso, J. Siegel-Bartelt, and A. Frumkin Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly Nat. Genet. 14 1996 353 356
7. E. Roessler, E. Belloni, K. Gaudenz, P. Jay, P. Berta, and S.W. Scherer Mutations in the human Sonic Hedgehog gene cause holoprosencephaly Nat. Genet. 14 1996 357 360
8. R.J. Gorlin Nevoid basal cell carcinoma syndrome Dermatol. Clin. 13 1995 113 125
9. J.L. Mullor, P. Sanchez, and A.R. Altaba Pathways and consequences: hedgehog signaling in human disease Trends Cell. Biol. 12 2002 562 569
10. C. Wetmore Sonic hedgehog in normal and neoplastic proliferation: insight gained from human tumors and animal models Curr. Opin. Genet. Dev. 13 2003 34 42
11. D.M. Berman, S.S. Karhadkar, A. Maitra, R. Montes De Oca, M.R. Gerstenblith, and K. Briggs Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours Nature 425 2003 846 851
12. S.P. Thayer, M.P. di Magliano, P.W. Heiser, C.M. Nielsen, D.J. Roberts, and G.Y. Lauwers Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis Nature 425 2003 851 856
13. D.N. Watkins, D.M. Berman, S.G. Burkholder, B. Wang, P.A. Beachy, and S.B. Baylin Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer Nature 422 2003 313 317
14. C.S. Wong, R.C. Strange, and J.T. Lear Basal cell carcinoma Br Med J 327 2003 794 798
15. E.C. Friedberg How nucleotide excision repair protects against cancer Nat. Rev. Cancer 1 2001 22 33
16. A. Stary, and A. Sarasin The genetics of the hereditary xeroderma pigmentosum syndrome Biochimie 84 2002 49 60
17. A.R. Lehmann DNA repair-diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy Biochimie 85 2003 1101 1111
18. L. Daya-Grosjean, C. Robert, C. Drougard, H. Suarez, and A. Sarasin High mutation frequency in ras genes of skin tumors isolated from DNA repair deficient xeroderma pigmentosum patients Cancer Res. 53 1993 1625 1629
19. S. Couve-Privat, B. Bouadjar, M.F. Avril, A. Sarasin, and L. Daya-Grosjean Significantly high levels of ultraviolet-specific mutations in the smoothened gene in basal cell carcinomas from DNA repair-deficient xeroderma pigmentosum patients Cancer Res. 62 2002 7186 7189
20. S. Couve-Privat, M. Le Bret, E. Traiffort, S. Queille, J. Coulombe, and B. Bouadjar Functional analysis of novel sonic hedgehog gene mutations identified in basal cell carcinomas from xeroderma pigmentosum patients Cancer Res. 64 2004 3559 3565
21. N. Dumaz, C. Drougard, A. Sarasin, and L. Daya-Grosjean Specific UV-induced mutation spectrum in the p53 gene of skin tumors from DNA-repair-deficient xeroderma pigmentosum patients Proc. Natl Acad. Sci. USA 90 1993 10529 10533
22. N. Bodak, S. Queille, M.F. Avril, B. Bouadjar, C. Drougard, and A. Sarasin High levels of patched gene mutations in basal-cell carcinomas from patients with xeroderma pigmentosum Proc. Natl Acad. Sci. USA 96 1999 5117 5122
23. N. Soufir, L. Daya-Grosjean, P. de la Salmoniere, J.P. Moles, L. Dubertret, and A. Sarasin Association between INK4a-ARF and p53 mutations in skin carcinomas of xeroderma pigmentosum patients J. Natl Cancer Inst. 92 2000 1841 1847
24. M. Manfredi, P. Vescovi, M. Bonanini, and S. Porter Nevoid basal cell carcinoma syndrome: a review of the literature Int. J. Oral Maxillofac. Surg. 33 2004 117 124
25. P.A. Farndon, R.G. Del Mastro, D.G. Evans, and M.W. Kilpatrick Location of gene for Gorlin syndrome Lancet 339 1992 581 582
26. M.R. Gailani, S.J. Bale, D.J. Leffell, J.J. DiGiovanna, G.L. Peck, and S. Poliak Developmental defects in Gorlin syndrome related to a putative tumor suppressor gene on chromosome 9 Cell 69 1992 111 117
27. H. Hahn, C. Wicking, P.G. Zaphiropoulous, M.R. Gailani, S. Shanley, and A. Chidambaram Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome Cell 85 1996 841 851
28. R.L. Johnson, A.L. Rothman, J. Xie, L.V. Goodrich, J.W. Bare, and J.M. Bonifas Human homolog of patched, a candidate gene for the basal cell nevus syndrome Science 272 1996 1668 1671
29. I. Vorechovsky, A.B. Unden, B. Sandstedt, R. Toftgard, and M. Stahle-Backdahl Trichoepitheliomas contain somatic mutations in the overexpressed PTCH gene: support for a gatekeeper mechanism in skin tumorigenesis Cancer Res. 57 1997 4677 4681
30. I. Vorechovsky, O. Tingby, M. Hartman, B. Stromberg, M. Nister, and V.P. Collins Somatic mutations in the human homologue of Drosophila patched in primitive neuroectodermal tumours Oncogene 15 1997 361 366
31. I. Vorechovsky, K.P. Benediktsson, and R. Toftgard The patched/hedgehog/smoothened signalling pathway in human breast cancer: no evidence for H133Y SHH, PTCH and SMO mutations Eur. J. Cancer 35 1999 711 713
32. M.R. Gailani, M. Stahle-Backdahl, D.J. Leffell, M. Glynn, P.G. Zaphiropoulos, and C. Pressman The role of the human homologue of Drosophila patched in sporadic basal cell carcinomas Nat. Genet. 14 1996 78 81
33. J.A. Porter, D.P. von Kessler, S.C. Ekker, K.E. Young, J.J. Lee, and K. Moses The product of hedgehog autoproteolytic cleavage active in local and long-range signalling Nature 374 1995 363 366
34. J.A. Porter, K.E. Young, and P.A. Beachy Cholesterol modification of hedgehog signaling proteins in animal development Science 274 1996 255 259
35. R.K. Mann, and P.A. Beachy Novel lipid modifications of secreted protein signals Annu. Rev. Biochem. 73 2004 891 923
36. X. Zeng, J.A. Goetz, L.M. Suber, W.J. Scott Jr., C.M. Schreiner, and D.J. Robbins A freely diffusible form of Sonic hedgehog mediates long-range signalling Nature 411 2001 716 720
37. R. Burke, D. Nellen, M. Bellotto, E. Hafen, K.A. Senti, and B.J. Dickson Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells Cell 99 1999 803 815
38. J.B. Rubin, Y. Choi, and R.A. Segal Cerebellar proteoglycans regulate sonic hedgehog responses during development Development 129 2002 2223 2232
39. P.T. Chuang, and A.P. McMahon Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein Nature 397 1999 617 621
40. D. Carpenter, D.M. Stone, J. Brush, A. Ryan, M. Armanini, and G. Frantz Characterization of two patched receptors for the vertebrate hedgehog protein family Proc. Natl Acad. Sci. USA 95 1998 13630 13634
41. I. Smyth, M.A. Narang, T. Evans, C. Heimann, Y. Nakamura, and G. Chenevix-Trench Isolation and characterization of human patched 2 (PTCH2), a putative tumour suppressor gene inbasal cell carcinoma and medulloblastoma on chromosome 1p32 Hum. Mol. Genet. 8 1999 291 297
42. J. Taipale, M.K. Cooper, T. Maiti, and P.A. Beachy Patched acts catalytically to suppress the activity of Smoothened Nature 418 2002 892 897
43. I.A.A. Ruiz The works of GLI and the power of hedgehog Nat. Cell Biol. 1 1999 E147 E148
44. P.W. Ingham, and A.P. McMahon Hedgehog signaling in animal development: paradigms and principles Genes Dev. 15 2001 3059 3087
45. M. Murone, S.M. Luoh, D. Stone, W. Li, A. Gurney, and M. Armanini Gli regulation by the opposing activities of fused and suppressor of fused Nat. Cell Biol. 2 2000 310 312
46. M. Merchant, F.F. Vajdos, M. Ultsch, H.R. Maun, U. Wendt, and J. Cannon Suppressor of fused regulates Gli activity through a dual binding mechanism Mol. Cell Biol. 24 2004 8627 8641
47. M.T. Teh, S.T. Wong, G.W. Neill, L.R. Ghali, M.P. Philpott, and A.G. Quinn FOXM1 is a downstream target of Gli1 in basal cell carcinomas Cancer Res. 62 2002 4773 4780
48. J. Xie, M. Aszterbaum, X. Zhang, J.M. Bonifas, C. Zachary, and E. Epstein A role of PDGFRalpha in basal cell carcinoma proliferation Proc. Natl Acad. Sci. USA 98 2001 9255 9259
49. T. Eichberger, G. Regl, M.S. Ikram, G.W. Neill, M.P. Philpott, and F. Aberger FOXE1, a new transcriptional target of GLI2 is expressed in human epidermis and basal cell carcinoma J. Invest. Dermatol. 122 2004 1180 1187
50. H. Fan, and P.A. Khavari Sonic hedgehog opposes epithelial cell cycle arrest J. Cell Biol. 147 1999 71 76
51. E.A. Barnes, M. Kong, V. Ollendorff, and D.J. Donoghue Patched1 interacts with cyclin B1 to regulate cell cycle progression Eur. Mol. Biol. Org. J. 20 2001 2214 2223
52. J.M. Bonifas, S. Pennypacker, P.T. Chuang, A.P. McMahon, and M. Williams Activation of expression of hedgehog target genes in basal cell carcinomas J. Invest. Dermatol. 116 2001 739 742
53. M. Kallassy, R. Toftgard, M. Ueda, K. Nakazawa, I. Vorechovsky, and H. Yamasaki Patched (ptch)-associated preferential expression of smoothened (smoh) in human basal cell carcinoma of the skin Cancer Res. 57 1997 4731 4735
54. G. Regl, G.W. Neill, T. Eichberger, M. Kasper, M.S. Ikram, and J. Koller Human GLI2 and GLI1 are part of a positive feedback mechanism in Basal Cell Carcinoma Oncogene 21 2002 5529 5539
55. J. Reifenberger, M. Wolter, R.G. Weber, M. Megahed, T. Ruzicka, and P. Lichter Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system Cancer Res. 58 1998 1798 1803
56. M. Tojo, T. Mori, H. Kiyosawa, Y. Honma, Y. Tanno, and K.Y. Kanazawa Expression of sonic hedgehog signal transducers, patched and smoothened, in human basal cell carcinoma Pathol. Int. 49 1999 687 694
57. A.B. Unden, P.G. Zaphiropoulos, K. Bruce, R. Toftgard, and M. Stahle-Backdahl Human patched (PTCH) mRNA is overexpressed consistently in tumor cells of both familial and sporadic basal cell carcinoma Cancer Res. 57 1997 2336 2340
58. P. Kogerman, D. Krause, F. Rahnama, L. Kogerman, A.B. Unden, and P.G. Zaphiropoulos Alternative first exons of PTCH1 are differentially regulated in vivo and may confer different functions to the PTCH1 protein Oncogene 21 2002 6007 6016
59. F. Rahnama, R. Toftgard, and P.G. Zaphiropoulos Distinct roles of PTCH2 splice variants in Hedgehog signalling Biochem. J. 378 2004 325 334
60. K.W. Kinzler, S.H. Bigner, D.D. Bigner, J.M. Trent, M.L. Law, and S.J. O'Brien Identification of an amplified, highly expressed gene in a human glioma Science 236 1987 70 73
61. J.M. Ruppert, B. Vogelstein, and K.W. Kinzler The zinc finger protein GLI transforms primary cells in cooperation with adenovirus E1A Mol. Cell Biol. 11 1991 1724 1728
62. M. Tojo, H. Kiyosawa, K. Iwatsuki, K. Nakamura, and F. Kaneko Expression of the GLI2 oncogene and its isoforms in human basal cell carcinoma Br. J. Dermatol. 148 2003 892 897
63. G. Regl, M. Kasper, H. Schnidar, T. Eichberger, G.W. Neill, and M.S. Ikram The zinc-finger transcription factor GLI2 antagonizes contact inhibition and differentiation of human epidermal cells Oncogene 23 2004 1263 1274
64. M.S. Ikram, G.W. Neill, G. Regl, T. Eichberger, A.M. Frischauf, and F. Aberger GLI2 is expressed in normal human epidermis and BCC and induces GLI1 expression by binding to its promoter J. Invest. Dermatol. 122 2004 1503 1509
65. A.E. Oro, and K. Higgins Hair cycle regulation of Hedgehog signal reception Dev. Biol. 255 2003 238 248
66. J. Green, I.M. Leigh, R. Poulsom, and A.G. Quinn Basal cell carcinoma development is associated with induction of the expression of the transcription factor Gli-1 Br. J. Dermatol. 139 1998 911 915
67. C. Cui, T. Elsam, Q. Tian, J.T. Seykora, M. Grachtchouk, and A. Dlugosz Gli proteins up-regulate the expression of basonuclin in Basal cell carcinoma Cancer Res. 64 2004 5651 5658
68. M. Tojo, H. Kiyosawa, K. Iwatsuki, and F. Kaneko Expression of a sonic hedgehog signal transducer, hedgehog-interacting protein, by human basal cell carcinoma Br. J. Dermatol. 146 2002 69 73
69. A.E. Oro, K.M. Higgins, Z. Hu, J.M. Bonifas, E.H. Epstein Jr., and M.P. Scott Basal cell carcinomas in mice overexpressing sonic hedgehog Science 276 1997 817 821
70. C. Wicking, T. Evans, B. Henk, N. Hayward, L.A. Simms, and G. Chenevix-Trench No evidence for the H133Y mutation in SONIC HEDGEHOG in a collection of common tumour types Oncogene 16 1998 1091 1093
71. E. Roessler, E. Belloni, K. Gaudenz, F. Vargas, S.W. Scherer, and L.C. Tsui Mutations in the C-terminal domain of Sonic Hedgehog cause holoprosencephaly Hum. Mol. Genet. 6 1997 1847 1853
72. L. Nanni, J.E. Ming, M. Bocian, K. Steinhaus, D.W. Bianchi, and C. Die-Smulders The mutational spectrum of the sonic hedgehog gene in holoprosencephaly: SHH mutations cause a significant proportion of autosomal dominant holoprosencephaly Hum. Mol. Genet. 8 1999 2479 2488
73. A.E. Bale, and K.P. Yu The hedgehog pathway and basal cell carcinomas Hum. Mol. Genet. 10 2001 757 762
74. M.R. Gailani, D.J. Leffell, A. Ziegler, E.G. Gross, D.E. Brash, and A.E. Bale Relationship between sunlight exposure and a key genetic alteration in basal cell carcinoma J. Natl Cancer Inst. 88 1996 349 354
75. A.B. Unden, E. Holmberg, B. Lundh-Rozell, M. Stahle-Backdahl, P.G. Zaphiropoulos, and R. Toftgard Mutations in the human homologue of Drosophila patched (PTCH) in basal cell carcinomas and the Gorlin syndrome: different in vivo mechanisms of PTCH inactivation Cancer Res. 56 1996 4562 4565
76. M. Wolter, J. Reifenberger, C. Sommer, T. Ruzicka, and G. Reifenberger Mutations in the human homologue of the Drosophila segment polarity gene patched (PTCH) in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system Cancer Res. 57 1997 2581 2585
77. M. Aszterbaum, A. Rothman, R.L. Johnson, M. Fisher, J. Xie, and J.M. Bonifas 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
78. M. D'Errico, A. Calcagnile, F. Canzona, B. Didona, P. Posteraro, and R. Cavalieri UV mutation signature in tumor suppressor genes involved in skin carcinogenesis in xeroderma pigmentosum patients Oncogene 19 2000 463 467
79. L. Daya-Grosjean, and A. Sarasin UV-specific mutations of the human patched gene in basal cell carcinomas from normal individuals and xeroderma pigmentosum patients Mutat. Res. 450 2000 193 199
80. D. Matt, H. Xin, A.O. Vortmeyer, Z. Zhuang, G. Burg, and R. Boni Sporadic trichoepithelioma demonstrates deletions at 9q22.3 Arch. Dermatol. 136 2000 657 660
81. J. Xie, M. Murone, S.M. Luoh, A. Ryan, Q. Gu, and C. Zhang Activating smoothened mutations in sporadic basal-cell carcinoma Nature 391 1998 90 92
82. C.W. Lam, J. Xie, K.F. To, H.K. Ng, K.C. Lee, and N.W. Yuen A frequent activated smoothened mutation in sporadic basal cell carcinomas Oncogene 18 1999 833 836
83. H. Fan, A.E. Oro, M.P. Scott, and P.A. Khavari Induction of basal cell carcinoma features in transgenic human skin expressing Sonic Hedgehog Nat. Med. 3 1997 788 792
84. M. Nilsson, A.B. Unden, D. Krause, U. Malmqwist, K. Raza, and P.G. Zaphiropoulos Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1 Proc. Natl Acad. Sci. USA 97 2000 3438 3443
85. M. Grachtchouk, R. Mo, S. Yu, X. Zhang, H. Sasaki, and C.C. Hui Basal cell carcinomas in mice overexpressing Gli2 in skin Nat. Genet. 24 2000 216 217
86. H. Sheng, S. Goich, A. Wang, M. Grachtchouk, L. Lowe, and R. Mo Dissecting the oncogenic potential of Gli2: deletion of an NH(2)-terminal fragment alters skin tumor phenotype Cancer Res. 62 2002 5308 5316
87. L.V. Goodrich, L. Milenkovic, K.M. Higgins, and M.P. Scott Altered neural cell fates and medulloblastoma in mouse patched mutants Science 277 1997 1109 1113
88. H. Hahn, L. Wojnowski, A.M. Zimmer, J. Hall, G. Miller, and A. Zimmer Rhabdomyosarcomas and radiation hypersensitivity in a mouse model of Gorlin syndrome Nat. Med. 4 1998 619 622
89. M. Aszterbaum, J. Epstein, A. Oro, V. Douglas, P.E. LeBoit, and M.P. Scott Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice Nat. Med. 5 1999 1285 1291
90. J. Taipale, J.K. Chen, M.K. Cooper, B. Wang, R.K. Mann, and L. Milenkovic Effects of oncogenic mutations in smoothened and patched can be reversed by cyclopamine Nature 406 2000 1005 1009
91. J.K. Chen, J. Taipale, K.E. Young, T. Maiti, and P.A. Beachy Small molecule modulation of smoothened activity Proc. Natl Acad. Sci. USA 99 2002 14071 14076
92. J.A. Williams, O.M. Guicherit, B.I. Zaharian, Y. Xu, L. Chai, and H. Wichterle Identification of a small molecule inhibitor of the hedgehog signaling pathway: effects on basal cell carcinoma-like lesions Proc. Natl Acad. Sci. USA 4 2003 4616 4621
93. M. Frank-Kamenetsky, X.M. Zhang, S. Bottega, O. Guicherit, H. Wichterle, and H. Dudek Small-molecule modulators of Hedgehog signaling: identification and characterization of Smoothened agonists and antagonists J. Biol. 1 2002 10.1 10.19
94. M.K. Cooper, J.A. Porter, K.E. Young, and P.A. Beachy Teratogen-mediated inhibition of target tissue response to Shh signaling Science 280 1998 1603 1607
95. J.P. Incardona, W. Gaffield, R.P. Kapur, and H. Roelink The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction Development 125 1998 3553 3562
96. A. Vogt, P.T. Chuang, J. Hebert, J. Hwang, Y. Lu, and L. Kopelovich Immunoprevention of basal cell carcinomas with recombinant hedgehog-interacting protein J. Exp. Med. 199 2004 753 761