Loss of the tumor suppressor Snf5 leads to aberrant activation of the Hedgehog-Gli pathway

Nature Medicine

Volumn 16, Issue 12, 2010, Pages 1429-1434

  Jagani, Zainab ^a   Mora Blanco, E Lorena ^b   Sansam, Courtney G ^b   McKenna, Elizabeth S ^b   Wilson, Boris ^b   Chen, Dongshu ^a   Klekota, Justin ^a   Tamayo, Pablo ^c   Nguyen, Phuong T L ^b   Tolstorukov, Michael ^d   Park, Peter J ^d   Cho, Yoon Jae ^b,c   Hsiao, Kathy ^a   Buonamici, Silvia ^a   Pomeroy, Scott L ^b   Mesirov, Jill P ^c   Ruffner, Heinz ^e   Bouwmeester, Tewis ^e   Luchansky, Sarah J ^a   Murtie, Joshua ^a   Kelleher, Joseph F ^a   Warmuth, Markus ^a   Sellers, William R ^a   Roberts, Charles W M ^b   Dorsch, Marion ^a,f   more..

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d Harvard Medical School Center for Biomedical Informatics   (United States)

^e NOVARTIS PHARMA AG   (Switzerland)

^f Sanofi Aventis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR SNF; TRANSCRIPTION FACTOR SNF5; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; GENE EXPRESSION PROFILING; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RHABDOID TUMOR;

ANIMALS; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA PRIMERS; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; MASS SPECTROMETRY; MICE; MICROARRAY ANALYSIS; RHABDOID TUMOR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ERINACEIDAE;

EID: 78649999605     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2251     Document Type: Article

References (39)

1. Jiang, J. & Hui, C.C. Hedgehog signaling in development and cancer. Dev. Cell 15, 801-812 (2008).
2. Ruiz i Altaba, A., Mas, C. & Stecca, B. The Gli code: an information nexus regulating cell fate, stemness and cancer. Trends Cell Biol. 17, 438-447 (2007).
3. Gailani, M.R. et al. The role of the human homologue of Drosophila patched in sporadic basal cell carcinomas. Nat. Genet. 14, 78-81 (1996).
4. Raffel, C. et al. Sporadic medulloblastomas contain PTCH mutations. Cancer Res. 57, 842-845 (1997).
5. Kinzler, K.W. et al. Identifcation of an amplifed, highly expressed gene in a human glioma. Science 236, 70-73 (1987).
6. Northcott, P.A. et al. Multiple recurrent genetic events converge on control of histone lysine methylation in medulloblastoma. Nat. Genet. 41, 465-472 (2009).
7. Kogerman, P. et al. Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling of Gli-1. Nat. Cell Biol. 1, 312-319 (1999).
8. Roberts, C.W. & Orkin, S.H. The SWI/SNF complex-chromatin and cancer. Nat. Rev. Cancer 4, 133-142 (2004).
9. Weissman, B. & Knudsen, K.E. Hijacking the chromatin remodeling machinery: impact of SWI/SNF perturbations in cancer. Cancer Res. 69, 8223-8230 (2009).
10. Wu, J.I., Lessard, J. & Crabtree, G.R. Understanding the words of chromatin regulation. Cell 136, 200-206 (2009).
11. Goodrich, L.V., Johnson, R.L., Milenkovic, L., McMahon, J.A. & Scott, M.P. Conservation of the hedgehog/patched signaling pathway from fies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev. 10, 301-312 (1996).
12. Lee, J., Platt, K.A., Censullo, P. & Ruiz i Altaba, A. Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 124, 2537-2552 (1997).
13. Isakoff, M.S. et al. Inactivation of the Snf5 tumor suppressor stimulates cell cycle progression and cooperates with p53 loss in oncogenic transformation. Proc. Natl. Acad. Sci. USA 102, 17745-17750 (2005).
14. Logan, M. et al. Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80 (2002).
15. Martin, J.F. & Olson, E.N. Identifcation of a prx1 limb enhancer. Genesis 26, 225-229 (2000).
16. Theil, T., Kaesler, S., Grotewold, L., Bose, J. & Ruther, U. Gli genes and limb development. Cell Tissue Res. 296, 75-83 (1999).
17. Wang, X. et al. Oncogenesis caused by loss of the SNF5 tumor suppressor is dependent on activity of BRG1, the ATPase of the SWI/SNF chromatin remodeling complex. Cancer Res. 69, 8094-8101 (2009).
18. Biegel, J.A. et al. Germ-line and acquired mutations of INI1 in atypical teratoid and rhabdoid tumors. Cancer Res. 59, 74-79 (1999).
19. Sévenet, N. et al. Constitutional mutations of the hSNF5/INI1 gene predispose to a variety of cancers. Am. J. Hum. Genet. 65, 1342-1348 (1999).
20. Versteege, I. et al. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394, 203-206 (1998).
21. McKenna, E.S. et al. Loss of the epigenetic tumor suppressor SNF5 leads to cancer without genomic instability. Mol. Cell. Biol. 28, 6223-6233 (2008).
22. McKenna, E.S. & Roberts, C.W. Epigenetics and cancer without genomic instability. Cell Cycle 8, 23-26 (2009).
23. Pomeroy, S.L. et al. Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 415, 436-442 (2002).
24. Wisniewski, D. et al. Characterization of potent inhibitors of the Bcr-Abl and the c-kit receptor tyrosine kinases. Cancer Res. 62, 4244-4255 (2002).
25. Hyman, J.M. et al. Small-molecule inhibitors reveal multiple strategies for Hedgehog pathway blockade. Proc. Natl. Acad. Sci. USA 106, 14132-14137 (2009).
26. Pan, S. et al. Discovery of NVP-LDE225, a potent and selective smoothened antagonist. ACS Med. Chem. Lett. 1, 130-134 (2010).
27. Chai, J., Charboneau, A.L., Betz, B.L. & Weissman, B.E. Loss of the hSNF5 gene concomitantly inactivates p21CIP/WAF1 and p16INK4a activity associated with replicative senescence in A204 rhabdoid tumor cells. Cancer Res. 65, 10192-10198 (2005).
28. Lee, D. et al. SWI/SNF complex interacts with tumor suppressor p53 and is necessary for the activation of p53-mediated transcription. J. Biol. Chem. 277, 22330-22337 (2002).
29. Nagl, N.G. Jr., Zweitzig, D.R., Thimmapaya, B., Beck, G.R. Jr. & Moran, E. The c-myc gene is a direct target of mammalian SWI/SNF-related complexes during differentiation-associated cell cycle arrest. Cancer Res. 66, 1289-1293 (2006).
30. Tsikitis, M., Zhang, Z., Edelman, W., Zagzag, D. & Kalpana, G.V. Genetic ablation of cyclin D1 abrogates genesis of rhabdoid tumors resulting from Ini1 loss. Proc. Natl. Acad. Sci. USA 102, 12129-12134 (2005).
31. Rudin, C.M. et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N. Engl. J. Med. 361, 1173-1178 (2009).
32. Bouwmeester, T. et al. A physical and functional map of the human TNF-α/NF-κB signal transduction pathway. Nat. Cell Biol. 6, 97-105 (2004).
33. Frank-Kamenetsky, M. et al. Small-molecule modulators of Hedgehog signaling: identifcation and characterization of Smoothened agonists and antagonists. J. Biol. 1, 10 (2002).
34. Turner, F.B., Cheung, W.L. & Cheung, P. Chromatin immunoprecipitation assay for mammalian tissues. Methods Mol. Biol. 325, 261-272 (2006).
35. Roberts, C.W., Leroux, M.M., Fleming, M.D. & Orkin, S.H. Highly penetrant, rapid tumorigenesis through conditional inversion of the tumor suppressor gene Snf5. Cancer Cell 2, 415-425 (2002).
36. Riddle, R.D., Johnson, R.L., Laufer, E. & Tabin, C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416 (1993).
37. Irizarry, R.A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264 (2003).
38. Barbie, D.A. et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462, 108-112 (2009).
39. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profles. Proc. Natl. Acad. Sci. USA 102, 15545-15550 (2005).