Hedgehog signaling and the Gli code in stem cells, cancer, and metastases

Science Signaling

Volumn 4, Issue 200, 2011, Pages

  Ruiz I Altaba, Ariel ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; PROTEIN KINASE B; RAS PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR NANOG; GLI1 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MYC PROTEIN, HUMAN; NANOG PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P21; PROTEIN P53; PTEN PROTEIN, HUMAN; TP53 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

CANCER INVASION; CANCER RECURRENCE; CELL SURVIVAL; CONFERENCE PAPER; HUMAN; METASTASIS; NEOPLASM; PRIORITY JOURNAL; STEM CELL; TUMOR CELL; TUMOR GROWTH; ANIMAL; ARTICLE; CANCER STEM CELL; COLON TUMOR; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; WNT SIGNALING PATHWAY;

ERINACEIDAE;

ANIMALS; COLONIC NEOPLASMS; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; ONCOGENE PROTEIN P21(RAS); PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MYC; PTEN PHOSPHOHYDROLASE; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; WNT SIGNALING PATHWAY;

EID: 81855173503     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002540     Document Type: Conference Paper

References (55)

1. N. Dahmane, A. Ruiz i Altaba, Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126, 3089-3100 (1999).
2. V. A. Wallace, Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9, 445-448 (1999).
3. R. J. Wechsler-Reya, M. P. Scott, Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114 (1999).
4. N. Dahmane, P. Sánchez, Y. Gitton, V. Palma, T. Sun, M. Beyna, H. Weiner, A. Ruiz i Altaba, The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. Development 128, 5201-5212 (2001).
5. V. Clement, P. Sanchez, N. de Tribolet, I. Radovanovic, A. Ruiz i Altaba, HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr. Biol. 17, 165-172 (2007).
6. A. Ruiz i Altaba, Catching a Gli-mpse of Hedgehog. Cell 90, 193-196 (1997).
7. A. Ruiz i Altaba, P. Sánchez, N. Dahmane, Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat. Rev. Cancer 2, 361-372 (2002).
8. A. Ruiz i Altaba, C. Mas, B. Stecca, The Gli code: an information nexus regulating cell fate, stemness and cancer. Trends Cell Biol. 17, 438-447 (2007).
9. I. Ben-Porath, M. W. Thomson, V. J. Carey, R. Ge, G. W. Bell, A. Regev, R. A. Weinberg, An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet. 40, 499-507 (2008).
10. N. Dahmane, J. Lee, P. Robins, P. Heller, A. Ruiz i Altaba, Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature 389, 876-881 (1997).
11. B. Stecca, C. Mas, V. Clement, M. Zbinden, R. Correa, V. Piguet, F. Beermann, A. Ruiz I Altaba, Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc. Natl. Acad. Sci. U.S.A. 104, 5895-5900 (2007).
12. R. L. Yauch, S. E. Gould, S. J. Scales, T. Tang, H. Tian, C. P. Ahn, D. Marshall, L. Fu, T. Januario, D. Kallop, M. Nannini-Pepe, K. Kotkow, J. C. Marsters, L. L. Rubin, F. J. de Sauvage, A paracrine requirement for hedgehog signalling in cancer. Nature 455, 406-410 (2008).
13. A. Ruiz i Altaba, Therapeutic inhibition of Hedgehog-GLI signaling in cancer: epithelial, stromal, or stem cell targets? Cancer Cell 14, 281-283 (2008).
14. A. Ruiz i Altaba, F. Varnat, On hedgehogs and human cancer. EMBO Mol. Med. 2, 386-387 (2010).
15. J. Lee, K. A. Platt, P. Censullo, A. Ruiz i Altaba, Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 124, 2537-2552 (1997).
16. P. Sánchez, A. M. Hernández, B. Stecca, A. J. Kahler, A. M. DeGueme, A. Barrett, M. Beyna, M. W. Datta, S. Datta, A. Ruiz i Altaba, Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc. Natl. Acad. Sci. U.S.A. 101, 12561-12566 (2004).
17. F. Varnat, A. Duquet, M. Malerba, M. Zbinden, C. Mas, P. Gervaz, A. Ruiz i Altaba, 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. 1, 338-351 (2009).
18. A. Ruiz i Altaba, Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development 125, 2203-2212 (1998).
19. L. V. Goodrich, L. Milenkovic, K. M. Higgins, M. P. Scott, Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113 (1997).
20. A. E. Oro, K. M. Higgins, Z. Hu, J. M. Bonifas, E. H. Epstein, Jr, M. P. Scott, Basal cell carcinomas in mice overexpressing sonic hedgehog. Science 276, 817-821 (1997).
21. M. Nilsson, A. B. Undèn, D. Krause, U. Malmqwist, K. Raza, P. G. Zaphiropoulos, R. Toftgård, Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc. Natl. Acad. Sci. U.S.A. 97, 3438-3443 (2000).
22. M. K. Cooper, J. A. Porter, K. E. Young, P. A. Beachy, Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 280, 1603-1607 (1998).
23. T. Sheng, C. Li, X. Zhang, S. Chi, N. He, K. Chen, F. McCormick, Z. Gatalica, J. Xie, Activation of the hedgehog pathway in advanced prostate cancer. Mol. Cancer 3, 29 (2004).
24. S. S. Karhadkar, G. S. Bova, N. Abdallah, S. Dhara, D. Gardner, A. Maitra, J. T. Isaacs, D. M. Berman, P. A. Beachy, Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 431, 707-712 (2004).
25. D. M. Berman, S. S. Karhadkar, A. R. Hallahan, J. I. Pritchard, C. G. Eberhart, D. N. Watkins, J. K. Chen, M. K. Cooper, J. Taipale, J. M. Olson, P. A. Beachy, Medulloblastoma growth inhibition by hedgehog pathway blockade. Science 297, 1559-1561 (2002).
26. E. E. Bar, A. Chaudhry, A. Lin, X. Fan, K. Schreck, W. Matsui, S. Piccirillo, A. L. Vescovi, F. DiMeco, A. Olivi, C. G. Eberhart, Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 25, 2524-2533 (2007).
27. C. D. Peacock, Q. Wang, G. S. Gesell, I. M. Corcoran-Schwartz, E. Jones, J. Kim, W. L. Devereux, J. T. Rhodes, C. A. Huff, P. A. Beachy, D. N. Watkins, W. Matsui, Hedgehog signaling maintains a tumor stem cell compartment in multiple myeloma. Proc. Natl. Acad. Sci. U.S.A. 104, 4048-4053 (2007).
28. P. Sanchez, A. Ruiz i Altaba, In vivo inhibition of endogenous brain tumors through systemic interference of Hedgehog signaling in mice. Mech. Dev. 122, 223-230 (2005).
29. J. T. Romer, H. Kimura, S. Magdaleno, K. Sasai, C. Fuller, H. Baines, M. Connelly, C. F. Stewart, S. Gould, L. L. Rubin, T. Curran, Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1(+/-)p53(-/-) mice. Cancer Cell 6, 229-240 (2004).
30. D. Qualtrough, A. Buda, W. Gaffield, A. C. Williams, C. Paraskeva, Hedgehog signalling in colorectal tumour cells: induction of apoptosis with cyclopamine treatment. Int. J. Cancer 110, 831-837 (2004).
31. G. Chatel, C. Ganeff, N. Boussif, L. Delacroix, A. Briquet, G. Nolens, R. Winkler, Hedgehog signaling pathway is inactive in colorectal cancer cell lines. Int. J. Cancer 121, 2622-2627 (2007).
32. R. Brewster, J. L. Mullor, A. Ruiz i Altaba, Gli2 functions in FGF signaling during antero-posterior patterning. Development 127, 4395-4405 (2000).
33. V. Palma, A. Ruiz i Altaba, Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 131, 337-345 (2004).
34. V. Palma, D. A. Lim, N. Dahmane, P. Sánchez, T. C. Brionne, C. D. Herzberg, Y. Gitton, A. Carleton, A. Alvarez-Buylla, A. Ruiz i Altaba, Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 132, 335-344 (2005).
35. M. Kasper, H. Schnidar, G. W. Neill, M. Hanneder, S. Klingler, L. Blaas, C. Schmid, C. Hauser-Kronberger, G. Regl, M. P. Philpott, F. Aberger, Selective modulation of Hedgehog/GLI target gene expression by epidermal growth factor signaling in human keratinocytes. Mol. Cell. Biol. 26, 6283-6298 (2006).
36. B. Stecca, A. Ruiz I Altaba, Context-dependent regulation of the GLI code in cancer by HEDGEHOG and non-HEDGEHOG signals. J. Mol. Cell Biol. 2, 84-95 (2010).
37. N. A. Riobó, K. Lu, X. Ai, G. M. Haines, C. P. Emerson, Jr., Phosphoinositide 3-kinase and Akt are essential for Sonic Hedgehog signaling. Proc. Natl. Acad. Sci. U.S.A. 103, 4505-4510 (2006).
38. B. Stecca, A. Ruiz i Altaba, A GLI1-p53 inhibitory loop controls neural stem cell and tumour cell numbers. EMBO J. 28, 663-676 (2009).
39. Y. Abe, E. Oda-Sato, K. Tobiume, K. Kawauchi, Y. Taya, K. Okamoto, M. Oren, N. Tanaka, Hedgehog signaling overrides p53-mediated tumor suppression by activating Mdm2. Proc. Natl. Acad. Sci. U.S.A. 105, 4838-4843 (2008).
40. A. Ruiz i Altaba, Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 126, 3205-3216 (1999).
41. V. Nguyen, A. L. Chokas, B. Stecca, A. Ruiz i Altaba, Cooperative requirement of the Gli proteins in neurogenesis. Development 132, 3267-3279 (2005).
42. A. Ruiz i Altaba, B. Stecca, P. Sánchez, Hedgehog-Gli signaling in brain tumors: stem cells and paradevelopmental programs in cancer. Cancer Lett. 204, 145-157 (2004).
43. K. Lai, B. K. Kaspar, F. H. Gage, D. V. Schaffer, Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat. Neurosci. 6, 21-27 (2003).
44. M. Zbinden, A. Duquet, A. Lorente-Trigos, S. N. Ngwabyt, I. Borges, A. Ruiz i Altaba, NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J. 29, 2659-2674 (2010).
45. J. L. Mullor, N. Dahmane, T. Sun, A. Ruiz i Altaba, Wnt signals are targets and mediators of Gli function. Curr. Biol. 11, 769-773 (2001).
46. K. W. Kinzler, B. Vogelstein, Lessons from hereditary colorectal cancer. Cell 87, 159-170 (1996).
47. H. Shibata, K. Toyama, H. Shioya, M. Ito, M. Hirota, S. Hasegawa, H. Matsumoto, H. Takano, T. Akiyama, K. Toyoshima, R. Kanamaru, Y. Kanegae, I. Saito, Y. Nakamura, K. Shiba, T. Noda, Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 278, 120-123 (1997).
48. F. Varnat, G. Zacchetti, A. Ruiz i Altaba, Hedgehog pathway activity is required for the lethality and intestinal phenotypes of mice with hyperactive Wnt signaling. Mech. Dev. 127, 73-81 (2010b).
49. S. Arimura, A. Matsunaga, T. Kitamura, K. Aoki, M. Aoki, M. M. Taketo, Reduced level of smoothened suppresses intestinal tumorigenesis by down-regulation of Wnt signaling. Gastroenterology 137, 629-638 (2009).
50. M. van de Wetering, E. Sancho, C. Verweij, W. de Lau, I. Oving, A. Hurlstone, K. van der Horn, E. Batlle, D. Coudreuse, A. P. Haramis, M. Tjon-Pon-Fong, P. Moerer, M. van den Born, G. Soete, S. Pals, M. Eilers, R. Medema, H. Clevers, The betacatenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241-250 (2002).
51. F. Varnat, I. Siegl-Cachedenier, M. Malerba, P. Gervaz, A. Ruiz i Altaba, Loss of WNT-TCF addiction and enhancement of HH-GLI1 signalling define the metastatic transition of human colon carcinomas. EMBO Mol. Med. 2, 440-457 (2010).
52. A. Po, E. Ferretti, E. Miele, E. De Smaele, A. Paganelli, G. Canettieri, S. Coni, L. Di Marcotullio, M. Biffoni, L. Massimi, C. Di Rocco, I. Screpanti, A. Gulino, Hedgehog controls neural stem cells through p53-independent regulation of Nanog. EMBO J. 29, 2646-2658 (2010).
53. A. Ruiz i Altaba, D. A. Melton, Interaction between peptide growth factors and homoeobox genes in the establishment of antero-posterior polarity in frog embryos. Nature 341, 33-38 (1989).
54. F. Nothias, G. Fishell, A. Ruiz i Altaba, Cooperation of intrinsic and extrinsic signals in the elaboration of regional identity in the posterior cerebral cortex. Curr. Biol. 8, 459-462 (1998).
55. C. Mas, A. Ruiz i Altaba, Small molecule modulation of HH-GLI signaling: current leads, trials and tribulations. Biochem. Pharmacol. 80, 712-723 (2010).