Hedgehog signaling drives cellular survival in human colon carcinoma cells

Cancer Research

Volumn 71, Issue 3, 2011, Pages 1092-1102

  Mazumdar, Tapati ^a   DeVecchio, Jennifer ^a   Shi, Ting ^a   Jones, Janay ^a   Agyeman, Akwasi ^a   Houghton, Janet A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLOPAMINE; DEATH RECEPTOR 5; FAS ANTIGEN; GANT 61; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN BCL 2; SHORT HAIRPIN RNA; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; UNCLASSIFIED DRUG;

ARTICLE; CARCINOMA CELL; CELL SURVIVAL; CLONOGENESIS; COLON CARCINOMA; CYTOTOXICITY; DOWN REGULATION; DRUG MECHANISM; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

CELL LINE, TUMOR; CELL SURVIVAL; COLONIC NEOPLASMS; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; HCT116 CELLS; HEDGEHOG PROTEINS; HT29 CELLS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIDINES; PYRIMIDINES; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VERATRUM ALKALOIDS;

EID: 79551540949     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-2315     Document Type: Article

References (50)

1. Lum L, Beachy PA. The Hedgehog response network: sensors, switches, and routers. Science 2004;304:1755-9.
2. Ruiz i Altaba A. Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 1999;126:3205-16.
3. Ruiz i Altaba A, Mas C, Stecca B. The Gli code: an information nexus regulating cell fate, stemness and cancer. Trends Cell Biol 2007;17:438-47.
4. Kasper M, Schnidar H, Neill GW, Hanneder M, Klingler S, Blaas L, et al. Selective modulation of Hedgehog/GLI target gene expression by epidermal growth factor signaling in human keratinocytes. Mol Cell Biol 2006;26:6283-98.
5. Kinzler KW, Bigner SH, Bigner DD, Trent JM, Law ML, O'Brien SJ, et al. Identification of an amplified, highly expressed gene in a human glioma. Science 1987;236:70-3.
6. Khatib ZA, Matsushime H, Valentine M, Shapiro DN, Sherr CJ, Look AT. Coamplification of the CDK4 gene with MDM2 and GLI in human sarcomas. Cancer Res 1993;53:5535-41. (Pubitemid 23342180)
7. Snijders AM, Schmidt BL, Fridlyand J, Dekker N, Pinkel D, Jordan RC, et al. Rare amplicons implicate frequent deregulation of cell fate specification pathways in oral squamous cell carcinoma. Oncogene 2005;24:4232-42.
8. Katoh Y, Katoh M. Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr Mol Med 2009;9:873-86.
9. Zurawel RH, Allen C, Wechsler-Reya R, Scott MP, Raffel C. Evidence that haploinsufficiency of Ptch leads to medulloblastoma in mice. Genes Chromosomes Cancer 2000;28:77-81.
10. Stecca B, Mas C, Clement V, Zbinden M, Correa R, Piguet V, et al. Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc Natl Acad Sci USA 2007;104:5895-900.
11. Sanchez P, Hernandez AM, Stecca B, Kahler AJ, DeGueme AM, Barrett A, et al. Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc Natl Acad Sci USA 2004;101:12561-6. (Pubitemid 39122063)
12. Yoshikawa K, Shimada M, Miyamoto H, Higashijima J, Miyatani T, Nishioka M, et al. Sonic hedgehog relates to colorectal carcinogenesis. J Gastroenterol 2009;44:1113-7.
13. Varnat F, Duquet A, Malerba M, Zbinden M, Mas C, Gervaz P, et al. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med 2009;1:338-51.
14. Varnat F, Zacchetti G, Ruiz i Altaba A. Hedgehog pathway activity is required for the lethality and intestinal phenotypes of mice with hyperactive Wnt signaling. Mech Dev;127:73-81.
15. van den Brink GR, Bleuming SA, Hardwick JC, Schepman BL, Offerhaus GJ, Keller JJ, et al. Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat Genet 2004;36:277-82.
16. Kasper M, Regl G, Frischauf AM, Aberger F. GLI transcription factors: mediators of oncogenic Hedgehog signalling. Eur J Cancer 2006;42:437-45.
17. Eichberger T, Sander V, Schnidar H, Regl G, Kasper M, Schmid C, et al. Overlapping and distinct transcriptional regulator properties of the GLI1 and GLI2 oncogenes. Genomics 2006;87:616-32.
18. Thiyagarajan S, Bhatia N, Reagan-Shaw S, Cozma D, Thomas-Tikhonenko A, Ahmad N, et al. Role of GLI2 transcription factor in growth and tumorigenicity of prostate cells. Cancer Res 2007;67:10642-6.
19. Ikram MS, Neill GW, Regl G, Eichberger T, Frischauf AM, Aberger F, et al. GLI2 is expressed in normal human epidermis and BCC and induces GLI1 expression by binding to its promoter. J Invest Dermatol 2004;122:1503-9.
20. Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 2002;129:4753-61. (Pubitemid 35277202)
21. Yoon JW, Kita Y, Frank DJ, Majewski RR, Konicek BA, Nobrega MA, et al. Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J Biol Chem 2002;277:5548-55.
22. Teh MT, Wong ST, Neill GW, Ghali LR, Philpott MP, Quinn AG. FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res 2002;62:4773-80.
23. Shi T, Mazumdar T, Devecchio J, Duan ZH, Agyeman A, Aziz M, et al. cDNA microarray gene expression profiling of hedgehog signaling pathway inhibition in human colon cancer cells. PLoS One 2010;5. pii: e13054.
24. Li C, Chi S, He N, Zhang X, Guicherit O, Wagner R, et al. IFNalpha induces Fas expression and apoptosis in hedgehog pathway activated BCC cells through inhibiting Ras-Erk signaling. Oncogene 2004;23:1608-17.
25. Xie J, Aszterbaum M, Zhang X, Bonifas JM, Zachary C, Epstein E, et al. A role of PDGFRalpha in basal cell carcinoma proliferation. Proc Natl Acad Sci USA 2001;98:9255-9. (Pubitemid 32743903)
26. Regl G, Kasper M, Schnidar H, Eichberger T, Neill GW, Philpott MP, et al. Activation of the BCL2 promoter in response to Hedgehog/GLI signal transduction is predominantly mediated by GLI2. Cancer Res 2004;64:7724-31.
27. Athar M, Li C, Tang X, Chi S, Zhang X, Kim AL, et al. Inhibition of smoothened signaling prevents ultraviolet B-induced basal cell carcinomas through regulation of Fas expression and apoptosis. Cancer Res 2004;64:7545-52.
28. Houghton JA, Harwood FG, Tillman DM. Thymineless death in colon carcinoma cells is mediated via fas signaling. Proc Natl Acad Sci USA 1997;94:8144-9.
29. Tillman DM, Petak I, Houghton JA. A Fas-dependent component in 5-fluorouracil/leucovorin-induced cytotoxicity in colon carcinoma cells. Clin Cancer Res 1999;5:425-30.
30. Izeradjene K, Douglas L, Tillman DM, Delaney AB, Houghton JA. Reactive oxygen species regulate caspase activation in tumor necrosis factor-related apoptosis-inducing ligand-resistant human colon carcinoma cell lines. Cancer Res 2005;65:7436-45.
31. Lauth M, Bergstrom A, Shimokawa T, Toftgard R. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc Natl Acad Sci USA 2007;104:8455-60. (Pubitemid 47175509)
32. Nawrocki ST, Carew JS, Douglas L, Cleveland JL, Humphreys R, Houghton JA. Histone deacetylase inhibitors enhance lexatumumab-induced apoptosis via a p21Cip1-dependent decrease in survivin levels. Cancer Res 2007;67:6987-94.
33. Izeradjene K, Douglas L, Delaney AB, Houghton JA. Casein kinase I attenuates tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by regulating the recruitment of fas-associated death domain and procaspase-8 to the death-inducing signaling complex. Cancer Res 2004;64:8036-44.
34. Tillman DM, Izeradjene K, Szucs KS, Douglas L, Houghton JA. Rottlerin sensitizes colon carcinoma cells to tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis via uncoupling of the mitochondria independent of protein kinase C. Cancer Res 2003;63:5118-25.
35. Jani TS, DeVecchio J, Mazumdar T, Agyeman A, Houghton JA. Inhibition of NF-kappaB signaling by quinacrine is cytotoxic to human colon carcinoma cell lines and is synergistic in combination with tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) or oxaliplatin. J Biol Chem;285:19162-72.
36. Kogerman P, Grimm T, Kogerman L, Krause D, Undén AB, Sandstedt B, et al. Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling of Gli-1. Nat Cell Biol 1999;1:312-9.
37. Qualtrough D, Buda A, Gaffield W, Williams AC, Paraskeva C. Hedgehog signalling in colorectal tumour cells: induction of apoptosis with cyclopamine treatment. Int J Cancer 2004;110:831-7.
38. Ward RJ, Lee L, Graham K, Satkunendran T, Yoshikawa K, Ling E, et al. Multipotent CD15+ cancer stem cells in patched-1-deficient mouse medulloblastoma. Cancer Res 2009;69:4682-90.
39. Bailey JM, Mohr AM, Hollingsworth MA. Sonic hedgehog paracrine signaling regulates metastasis and lymphangiogenesis in pancreatic cancer. Oncogene 2009;28:3513-25.
40. Ecke I, Rosenberger A, Obenauer S, Dullin C, Aberger F, Kimmina S, et al. Cyclopamine treatment of full-blown Hh/Ptch-associated RMS partially inhibits Hh/Ptch signaling, but not tumor growth. Mol Carcinog 2008;47:361-72.
41. Vorechovsky I, Benediktsson KP, Toftgard R. The patched/hedgehog/ smoothened signalling pathway in human breast cancer: no evidence for H133Y SHH, PTCH and SMO mutations. Eur J Cancer 1999;35:711-3.
42. Lee J, Platt KA, Censullo P, Ruiz i Altaba A. Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 1997;124:2537-52.
43. Feldmann G, Habbe N, Dhara S, Bisht S, Alvarez H, Fendrich V, et al. Hedgehog inhibition prolongs survival in a genetically engineered mouse model of pancreatic cancer. Gut 2008;57:1420-30.
44. Rudin CM, Hann CL, Laterra J, Yauch RL, Callahan CA, Fu L, et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N Engl J Med 2009;361:1173-8.
45. Von Hoff DD, LoRusso PM, Rudin CM, Reddy JC, Yauch RL, Tibes R, et al. Inhibition of the hedgehog pathway in advanced basal-cell carcinoma. N Engl J Med 2009;361:1164-72.
46. Nolan-Stevaux O, Lau J, Truitt ML, Chu GC, Hebrok M, Fernández- Zapico ME, et al. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Genes Dev 2009;23:24-36.
47. Lauth M, Toftgard R. Non-canonical activation of GLI transcription factors: implications for targeted anti-cancer therapy. Cell Cycle 2007;6:2458-63.
48. Mazumder S, Plesca D, Almasan A. Caspase-3 activation is a critical determinant of genotoxic stress-induced apoptosis. Methods Mol Biol 2008;414:13-21.
49. Bhardwaj A, Aggarwal BB. Receptor-mediated choreography of life and death. J Clin Immunol 2003;23:317-32.
50. Herbeuval JP, Lambert C, Sabido O, Cottier M, Fournel P, Dy M, et al. Macrophages from cancer patients: analysis of TRAIL, TRAIL receptors, and colon tumor cell apoptosis. J Natl Cancer Inst 2003;95:611-21.