Hedgehog signaling pathway is inactive in colorectal cancer cell lines

International Journal of Cancer

Volumn 121, Issue 12, 2007, Pages 2622-2627

  Chatel, Guillaume ^a   Ganeff, Corine ^a   Boussif, Naima ^a   Delacroix, Laurence ^a   Briquet, Alexandra ^a   Nolens, Gregory ^a   Winkler, Rosita ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Colon cancer; Cyclopamine; Hedgehog

Indexed keywords

CYCLOPAMINE; SONIC HEDGEHOG PROTEIN;

ARTICLE; CANCER CELL; COLORECTAL CANCER; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEDGEHOG PROTEINS; HUMANS; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOMATINE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VERATRUM ALKALOIDS;

EID: 36248953744     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22998     Document Type: Article

References (43)

1. Ingham PW, McMahon AP. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 2001;15:3059-87.
2. Pan Y, Bai CB, Joyner AL, Wang B. Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol Cell Biol 2006;26:3365-77.
3. Osterlund T, Kogerman P. Hedgehog signalling: how to get from Smo to Ci and Gli. Trends Cell Biol 2006;16:176-80.
4. Park HL, Bai C, Platt KA, Mause MP, Beeghly A, Hui CC, Nakashima M, Joyner AL. Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 2000;127:1593-605.
5. 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.
6. Roessler E, Du YZ, Mullor JL, Casas E, Allen WP, Gillessen-Kaesbach G, Roeder ER, Ming JE, Altaba A, Muenke M. Loss-of-function mutations in the human GLI2 gene are associated with pituitary anomalies and holoprosencephaly-like features. Proc Natl Acad Sci USA 2003;100:13424-9.
7. Ikram MS. Neill GW, Regl G, Eichberger T, Frischauf AM, Aberger F, Quinn A, Philpott M. 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.
8. Sasaki H, Hui C, Nakafuku M, Kondoh H. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 1997;124:1313-22.
9. Hynes M, Stone DM, Dowd M, Pitts-Meek S, Goddard A, Gurney A, Rosenthal A. Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron 1997;19:15-26.
10. Altaba A. Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 1999;126:3205-16.
11. Chuang PT, McMahon AP. Vertebrate Hedgehog signaling modulated by induction of a Hedgehog-binding protein. Nature 1999;397:617-21.
12. Olsen CL, Hsu PP, Glienke J, Rubanyi GM, Brooks AR. Hedgehog-interacting protein is highly expressed in endothelial cells but down-regulated during angiogenesis and in several human tumors. BMC Cancer 2004;4:43.
13. Svard J, Heby-Henricson K, Persson-Lek M, Rozell B, Lauth M, Bergstrom A, Ericson J, Toftgard R, Teglund S. Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. Dev Cell 2006;10:187-97.
14. Varjosalo M, Taipale J. Hedgehog signaling. J Cell Sci 2007;120:3-6.
15. Lee J, Platt KA, Censullo P, Altaba A. Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 1997;124:2537-52.
16. Marigo V, Tabin CJ. Regulation of patched by sonic hedgehog in the developing neural tube. Proc Natl Acad Sci USA 1996;93:9346-51.
17. Lees C, Howie S, Sartor RB, Satsangi J. The hedgehog signalling pathway in the gastrointestinal tract: implications for development, homeostasis, and disease. Gastroenterology 2005;129:1696-710.
18. Ramalho-Santos M, Melton DA, McMahon AP. Hedgehog signals regulate multiple aspects of gastrointestinal development. Development 2000;127:2763-72.
19. van den Brink GR, Bleuming SA. Hardwick JC, Schepman BL, Offerhaus GJ, Keller JJ, Nielsen C, Gaffield W, van Deventer SJ, Roberts DJ, Peppelenbosch MP. Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat Genet 2004;36:277-82.
20. Pasca di MM, Hebrok M. Hedgehog signalling in cancer formation and maintenance. Nat Rev Cancer 2003;3:903-11.
21. Evangelista M, Tian H, de Sauvage FJ. The hedgehog signaling pathway in cancer. Clin Cancer Res 2006;12:5924-8.
22. Hu Z, Bonifas JM, Aragon G, Kopelovich L, Liang Y, Ohta S, Israel MA, Bickers DR, Aszterbaum M, Epstein EH, Jr. Evidence for lack of enhanced hedgehog target gene expression in common extracutaneous tumors. Cancer Res 2003;63:923-8.
23. Zhu Y, James RM, Peter A, Lomas C, Cheung F, Harrison DJ, Bader SA. Functional Smoothened is required for expression of GLI3 in colorectal carcinoma cells. Cancer Lett 2004;207:205-14.
24. Wang WS, Chen PM, Su Y. Colorectal carcinoma: from tumorigenesis to treatment. Cell Mol Life Sci 2006;63:663-71.
25. Bhardwaj G, Murdoch B, Wu D, Baker DP, Williams KP, Chadwick K, Ling LE, Karanu FN, Bhatia M. Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat Immunol 2001;2:172-80.
26. Stone DM, Murone M, Luoh S, Ye W, Armanini MP, Gurney A, Phillips H, Brush J, Goddard A, de Sauvage FJ, Rosenthal A. Characterization of the human suppressor of fused, a negative regulator of the zinc-finger transcription factor Gli J Cell Sci 1999;112:4437-48.
27. Taylor MD, Liu L, Raffel C, Hui CC, Mainprize TG, Zhang X, Agatep R, Chiappa S, Gao L, Lowrance A, Hao A, Goldstein AM, et al. Mutations in SUFU predispose to medulloblastoma. Nat Genet 2002;31:306-10.
28. Sheng T, Li C, Zhang X, Chi S, He N, Chen K, McCormick F, Gatalica Z, Xie J. Activation of the hedgehog pathway in advanced prostate cancer. Mol Cancer 2004;3:29.
29. Taipale J, Chen JK, Cooper MK, Wang B, Mann RK, Milenkovic L, Scott MP, Beachy PA. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 2000;406:1005-9.
30. Berman DM, Karhadkar SS, Maitra A, Montes De OR, Gerstenblith MR, Briggs K, Parker AR, Shimada Y, Eshleman JR, Watkins DN, Beachy PA. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 2003;425:846-51.
31. 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.
32. Kogerman P, Krause D, Rahnama F, Kogerman L, Unden AB, Zaphiropoulos PG, Toftgard R. Alternative first exons of PTCH1 are differentially regulated in vivo and may confer different functions to the PTCHl protein. Oncogene 2002;21:6007-16.
33. Agren M, Kogerman P, Kleman MI, Wessling M, Toftgard R. Expression of the PTCH1 tumor suppressor gene is regulated by alternative promoters and a single functional Gli-binding site. Gene 2004;330:101-14.
34. Madison BB, Braunstein K, Kuison E, Portman K, Qiao XT, Gumucio DL. Epithelial hedgehog signals pattern the intestinal crypt-villus axis. Development 2005;132:279-89.
35. Martin ST, Sato N, Dhara S, Chang R, Hustinx SR, Abe T, Maitra A, Goggins M. Aberrant methylation of the Human Hedgehog interacting protein (HHIP) gene in pancreatic neoplasms. Cancer Biol Ther 2005;4:728-33.
36. Bose J, Grotewold L, Ruther U. Pallister-Hall syndrome phenotype in mice mutant for Gli3. Hum Mol Genet 2002;11:1129-35.
37. Taylor MD, Zhang X, Liu L, Hui CC, Mainprize TG, Scherer SW, Wainwright B, Hogg D, Rutka JT. Failure of a medulloblastoma-derived mutant of SUFU to suppress WNT signaling. Oncogene 2004;23:4577-83.
38. Dwyer JR, Sever N, Carlson M, Nelson SF, Beachy PA, Parhami F. Oxysterols are novel activators of the hedgehog signaling pathway in pluripotent mesenchymal cells. J Biol Chem 2007;282:8959-68.
39. Oniscu A, James RM, Morris RG, Bader S, Malcomson RD, Harrison DJ. Expression of Sonic hedgehog pathway genes is altered in colonic neoplasia. J Pathol 2004;203:909-17.
40. Douard R, Moutereau S, Pernet P, Chimingqi M, Allory Y, Manivet P, Conti M, Vaubourdolle M, Cugnenc PH, Loric S. Sonic Hedgehog-dependent proliferation in a series of patients with colorectal cancer. Surgery 2006;139:665-70.
41. Akiyoshi T, Nakamura M, Koga K, Nakashima H, Yao T, Tsuneyoshi M, Tanaka M, Katano M. Gli1, downregulated in colorectal cancers, inhibits proliferation of colon cancer cells involving Wnt signalling activation. Gut 2006;55:991-9.
42. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007;445:106-10.
43. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De MR. Identification and expansion of human colon-cancer-initiating cells. Nature 2007;445:111-5.