Evasion of p53 and G 2 /M checkpoints are characteristic of Hh-driven basal cell carcinoma

Oncogene

Volumn 33, Issue 20, 2014, Pages 2674-2680

  Li, Z J ^a,b   Mack, S C ^a,b   Mak, T H ^a   Angers, S ^b,c   Taylor, M D ^a,b   Hui, C C ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

basal cell carcinoma; cell cycle; Hedgehog; p53; Ptc1; Sufu

Indexed keywords

CYCLIN B1; CYCLIN D1; PROTEIN P53; PROTEIN PATCHED 1; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR GLI3; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEIN; SONIC HEDGEHOG PROTEIN; TP53 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BASAL CELL CARCINOMA; CELL ACTIVATION; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELLULAR DISTRIBUTION; COLLAGEN METABOLISM; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE EXPRESSION PROFILING; GENOMIC INSTABILITY; HAIR FOLLICLE; HEDGEHOG; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; M PHASE CELL CYCLE CHECKPOINT; MOUSE; NONHUMAN; OVERLAPPING GENE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN STABILITY; SKIN DEFECT; SUFU GENE; TUMOR ESCAPE; TUMOR GROWTH; UPREGULATION; WESTERN BLOTTING; CELL CYCLE G2 PHASE; CELL DIVISION; METABOLISM; PATHOLOGY; PHYSIOLOGY; SKIN TUMOR;

ERINACEIDAE;

CARCINOMA, BASAL CELL; CELL DIVISION; G2 PHASE; HEDGEHOG PROTEINS; HUMANS; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84901239611     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.212     Document Type: Article

References (41)

1. Ribeiro GR, Francisco G, Teixeira LV, Romao-Correia RF, Sanches Jr. JA, Neto CF et al. Repetitive DNA alterations in human skin cancers. J Dermatol Sci 2004; 36: 79-86. (Pubitemid 39424130
2. Sardi I, Piazzini M, Palleschi G, Pinzi C, Taddei I, Arrigucci S et al. Molecular detection of microsatellite instability in basal cell carcinoma. Oncol Rep 2000; 7: 1119-1122
3. Reifenberger J, Wolter M, Knobbe CB, Kohler B, Schonicke A, Scharwachter C et al. Somatic mutations in the PTCH, SMOH, SUFUH and TP53 genes in sporadic basal cell carcinomas. Br J Dermatol 2005; 152: 43-51
4. Hutchin ME, Kariapper MS, Grachtchouk M, Wang A, Wei L, Cummings D et al. Sustained Hedgehog signaling is required for basal cell carcinoma proliferation and survival: Conditional skin tumorigenesis recapitulates the hair growth cycle. Genes Dev 2005; 19: 214-223. (Pubitemid 40111117
5. Epstein EH. Basal cell carcinomas: Attack of the hedgehog. Nat Rev Cancer 2008; 8: 743-754
6. Adolphe C, Hetherington R, Ellis T, Wainwright B. Patched1 functions as a gatekeeper by promoting cell cycle progression. Cancer Res 2006; 66: 2081-2088
7. Kasper M, Jaks V, Are A, Bergstrom A, Schwager A, Barker N et al. Wounding enhances epidermal tumorigenesis by recruiting hair follicle keratinocytes. Proc Natl Acad Sci USA 2011; 108: 4099-4104
8. Villani RM, Adolphe C, Palmer J, Waters MJ, Wainwright BJ. Patched1 inhibits epidermal progenitor cell expansion and basal cell carcinoma formation by limiting Igfbp2 activity. Cancer Prev Res (Phila) 2010; 3: 1222-1234
9. Humke EW, Dorn KV, Milenkovic L, Scott MP, Rohatgi R. The output of Hedgehog signaling is controlled by the dynamic association between suppressor of Fused and the Gli proteins. Genes Dev 2010; 24: 670-682
10. Tukachinsky H, Lopez LV, Salic A. A mechanism for vertebrate Hedgehog signaling: Recruitment to cilia and dissociation of SuFu-Gli protein complexes. J Cell Biol 2010; 191: 415-428
11. Li ZJ, Nieuwenhuis E, Nien W, Zhang X, Zhang J, Puviindran V et al. Kif7 regulates Gli2 through Sufu-dependent and -independent functions during skin Development and tumorigenesis. Development 2012; 139: 4152-4161
12. Mill P, Mo R, Fu H, Grachtchouk M, Kim PC, Dlugosz AA et al. Sonic hedgehogdependent activation of Gli2 is essential for embryonic hair follicle development. Genes Dev 2003; 17: 282-294. (Pubitemid 36105899
13. Nilsson M, Unden AB, Krause D, Malmqwist U, Raza K, Zaphiropoulos PG et al. Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc Natl Acad Sci USA 2000; 97: 3438-3443. (Pubitemid 30183321
14. Grachtchouk M, Mo R, Yu S, Zhang X, Sasaki H, Hui CC et al. Basal cell carcinomas in mice overexpressing Gli2 in skin. Nat Genet 2000; 24: 216-217. (Pubitemid 30132187
15. Mill P, Mo R, Hu MC, Dagnino L, Rosenblum ND, Hui CC. Shh controls epithelial proliferation via independent pathways that converge on N-Myc. Dev Cell 2005; 9: 293-303. (Pubitemid 41051747
16. Kenney AM, Rowitch DH. Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 2000; 20: 9055-9067
17. Kenney AM, Cole MD, Rowitch DH. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in Developing cerebellar granule neuron precursors. Development 2003; 130: 15-28. (Pubitemid 36113940
18. Abe Y, Oda-Sato E, Tobiume K, Kawauchi K, Taya Y, Okamoto K et al. Hedgehog signaling overrides p53-mediated tumor suppression by activating Mdm2. Proc Natl Acad Sci USA 2008; 105: 4838-4843. (Pubitemid 351753833
19. Fan H, Khavari PA. Sonic hedgehog opposes epithelial cell cycle arrest. J Cell Biol 1999; 147: 71-76. (Pubitemid 30211797
20. Cooper AF, Yu KP, Brueckner M, Brailey LL, Johnson L, McGrath JM et al. Cardiac and CNS defects in a mouse with targeted disruption of suppressor of fused. Development 2005; 132: 4407-4417. (Pubitemid 41576701
21. Goodrich LV, Johnson RL, Milenkovic L, McMahon JA, Scott MP. Conservation of the hedgehog/patched signaling pathway from flies to mice: Induction of a mouse patched gene by Hedgehog. Genes Dev 1996; 10: 301-312. (Pubitemid 26058963
22. Svard J, Heby-Henricson K, Persson-Lek M, Rozell B, Lauth M, Bergstrom A et al. Genetic elimination of suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. Dev Cell 2006; 10: 187-197. (Pubitemid 43174952
23. Ng D, Stavrou T, Liu L, Taylor MD, Gold B, Dean M et al. Retrospective family study of childhood medulloblastoma. Am J Med Genet A 2005; 134: 399-403. (Pubitemid 40604066
24. Aszterbaum M, Epstein J, Oro A, Douglas V, LeBoit PE, Scott MP et al. Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice. Nat Med 1999; 5: 1285-1291. (Pubitemid 29535606
25. Mancuso M, Pazzaglia S, Tanori M, Hahn H, Merola P, Rebessi S et al. Basal cell carcinoma and its development: Insights from radiation-induced tumors in Ptch1-deficient mice. Cancer Res 2004; 64: 934-941. (Pubitemid 38176895
26. Nieuwenhuis E, Motoyama J, Barnfield PC, Yoshikawa Y, Zhang X, Mo R et al. Mice with a targeted mutation of patched2 are viable but develop alopecia and epidermal hyperplasia. Mol Cell Biol 2006; 26: 6609-6622. (Pubitemid 44277898
27. Oro AE, Higgins K. Hair cycle regulation of Hedgehog signal reception. Dev Biol 2003; 255: 238-248. (Pubitemid 36331946
28. Grachtchouk V, Grachtchouk M, Lowe L, Johnson T, Wei L, Wang A et al. The magnitude of hedgehog signaling activity defines skin tumor phenotype. EMBO J 2003; 22: 2741-2751. (Pubitemid 36712370
29. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-15550. (Pubitemid 41528093
30. Merico D, Isserlin R, Stueker O, Emili A, Bader GD. Enrichment map: A networkbased method for gene-set enrichment visualization and interpretation. PLoS ONE 2010; 5: E13984
31. Howell BG, Solish N, Lu C, Watanabe H, Mamelak AJ, Freed I et al. Microarray profiles of human basal cell carcinoma: Insights into tumor growth and behavior. J Dermatol Sci 2005; 39: 39-51. (Pubitemid 40835832
32. O'Driscoll L, McMorrow J, Doolan P, McKiernan E, Mehta JP, Ryan E et al. Investigation of the molecular profile of basal cell carcinoma using whole genome microarrays. Mol Cancer 2006; 5: 74
33. Welss T, Papoutsaki M, Michel G, Reifenberger J, Chimenti S, Ruzicka T et al. Molecular basis of basal cell carcinoma: Analysis of differential gene expression by differential display PCR and expression array. Int J Cancer 2003; 104: 66-72. (Pubitemid 36184148
34. Gambichler T, Skrygan M, Kaczmarczyk JM, Hyun J, Tomi NS, Sommer A et al. Increased expression of TGF-beta/Smad proteins in basal cell carcinoma. Eur J Med Res 2007; 12: 509-514. (Pubitemid 350110853
35. Lange D, Persson U, Wollina U, ten Dijke P, Castelli E, Heldin CH et al. Expression of TGF-beta related Smad proteins in human epithelial skin tumors. Int J Oncol 1999; 14: 1049-1056
36. Van Haren R, Feldman D, Sinha AA. Systematic comparison of nonmelanoma skin cancer microarray datasets reveals lack of consensus genes. Br J Dermatol 2009; 161: 1278-1287
37. Barnes EA, Kong M, Ollendorff V, Donoghue DJ. Patched1 interacts with cyclin B1 to regulate cell cycle progression. EMBO J 2001; 20: 2214-2223. (Pubitemid 32410591
38. Takizawa CG, Morgan DO. Control of mitosis by changes in the subcellular location of cyclin-B1-Cdk1 and Cdc25C. Curr Opin Cell Biol 2000; 12: 658-665
39. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434: 907-913. (Pubitemid 40559004
40. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434: 864-870. (Pubitemid 40558993
41. Cwinn MA, Mazerolle C, McNeill B, Ringuette R, Thurig S, Hui CC et al. Suppressor of fused is required to maintain the multipotency of neural progenitor cells in the retina. J Neurosci 2011; 31: 5169-5180