Histone deacetylase and Cullin3-REN KCTD11 ubiquitin ligase interplay regulates Hedgehog signalling through Gli acetylation

Nature Cell Biology

Volumn 12, Issue 2, 2010, Pages 132-142

  Canettieri, Gianluca ^a   Di Marcotullio, Lucia ^a   Greco, Azzura ^a   Coni, Sonia ^a   Antonucci, Laura ^a   Infante, Paola ^a   Pietrosanti, Laura ^a   De Smaele, Enrico ^a   Ferretti, Elisabetta ^a   Miele, Evelina ^a   Pelloni, Marianna ^a   De Simone, Giuseppina ^d   Pedone, Emilia Maria ^d   Gallinari, Paola ^b   Giorgi, Alessandra ^a   Steinkühler, Christian ^b   Vitagliano, Luigi ^d   Pedone, Carlo ^d   Schinin, M Eugeni ^a   Screpanti, Isabella ^a   Gulino, Alberto ^a,c   more..

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRBM   (Italy)

^c IRCCS NEUROMED   (Italy)

^d CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CULLIN; CULLIN 3; HISTONE DEACETYLASE; PROTEIN REN KCTD11; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ARTICLE; CELL GROWTH; CELL STRAIN 3T3; CELL STRAIN HEK293; CELL TRANSFORMATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; MEDULLOBLASTOMA; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ACETYLATION; ANIMALS; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CULLIN PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HEDGEHOG PROTEINS; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASES; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MEDULLOBLASTOMA; MICE; NERVE TISSUE PROTEINS; NIH 3T3 CELLS; ONCOGENE PROTEINS; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRANS-ACTIVATORS;

ERINACEIDAE;

EID: 75949106376     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb2013     Document Type: Article

References (42)

1. Ruiz i Altaba, A. Hedgehog-Gli Signaling in Human Diseases (Plenum 2006).
2. Jiang, J. & Hui, C. C. Hedgehog signaling in development and cancer. Dev. Cell 15, 801-812 (2008).
3. Ruppert, J. M., Vogelstein, B. & Kinzler, K. W. The zinc finger protein GLI transforms primary cells in cooperation with adenovirus E1A. Mol. Cell Biol. 11, 1724-1728 (1991).
4. Kimura, H., Stephen, D., Joyner, A. & Curran, T. Gli1 is important for medulloblastoma formation in Ptc1+/-mice. Oncogene 24, 4026-4036 (2005).
5. Ferretti, E. et al. Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 27, 2616-2627 (2008).
6. Huntzicker, E. G. et al. Dual degradation signals control Gli protein stability and tumor formation. Genes Dev. 20, 276-281 (2006).
7. Di Marcotullio, L. et al. Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination. Nature Cell Biol. 8, 1415-1423 (2006).
8. Minucci, S. & Pelicci, P. G. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nature Rev. Cancer 6, 38-51 (2006).
9. Glozak, M. A., Sengupta, N., Zhang, X. & Seto, E. Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23 (2005).
10. Zupkovitz, G. et al. Negative and positive regulation of gene expression by mouse histone deacetylase 1. Mol. Cell Biol. 26, 7913-7928 (2006).
11. Yang, X. J. & Seto, E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nature Rev. Mol. Cell Biol. 9, 206-218 (2008).
12. Dai, P. et al. Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274, 8143-8152 (1999).
13. Dai, P. et al. Ski is involved in transcriptional regulation by the repressor and full-length forms of Gli3. Genes Dev. 16, 2843-2848 (2002).
14. Yoon, J. W. et al. GLI activates transcription through a herpes simplex viral protein 16-like activation domain. J. Biol. Chem. 273, 3496-3501 (1998).
15. Di Marcotullio, L. et al. REN(KCTD11) is a suppressor of Hedgehog signaling and is deleted in human medulloblastoma. Proc. Natl Acad. Sci. USA 101, 10833-10838 (2004).
16. Taipale, J. et al. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406, 1005-1009 (2000).
17. Chen, J. K., Taipale, J., Young, K. E., Maiti, T. & Beachy, P. A. Small molecule modulation of Smoothened activity. Proc. Natl Acad. Sci. USA 99, 14071-14076 (2002).
18. Canettieri, G. et al. The coactivator CRTC1 promotes cell proliferation and transformation via AP-1. Proc. Natl Acad. Sci. USA 106, 1445-1450 (2009).
19. Cheng, S. Y. & Bishop, J. M. Suppressor of Fused represses Gli-mediated transcription by recruiting the SAP18-mSin3 corepressor complex. Proc. Natl Acad. Sci. USA 99, 5442-5447 (2002).
20. Argenti, B. et al. Hedgehog antagonist REN(KCTD11) regulates proliferation and apoptosis of developing granule cell progenitors. J. Neurosci. 25, 8338-8346 (2005).
21. Goodrich, L. V., MilenkoviC, L., Higgins, K. M. & Scott, M. P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113 (1997).
22. Pintard, L., Willems, A. & Peter, M. Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J. 23, 1681-1687 (2004).
23. Bar, E. E., Chaudhry, A., Farah, M. H. & Eberhart, C. G. Hedgehog signaling promotes medulloblastoma survival via Bc/II. Am. J. Pathol. 170, 347-355 (2007).
24. Montgomery, R. L., Hsieh, J., Barbosa, A. C., Richardson, J. A. & Olson, E. N. Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc. Natl Acad. Sci. USA 106, 7876-7881 (2009).
25. Shakéd, M. et al. Histone deacetylases control neurogenesis in embryonic brain by inhibition of BMP2/4 signaling. PLoS One 3, e2668 (2008).
26. Zhao, H., Ayrault, O., Zindy, F., Kim, J. H. & Roussel, M. F. Post-transcriptional down-regulation of Atoh1/Math1 by bone morphogenic proteins suppresses medulloblastoma development. Genes Dev. 22, 722-727 (2008).
27. Rios, I., Alvarez-Rodriguez, R., Martí, E. & Pons, S. Bmp2 antagonizes sonic hedgehog-mediated proliferation of cerebellar granule neurones through Smad5 signalling. Development 131, 3159-3168 (2004).
28. Cunliffe, V. T. Histone deacetylase 1 is required to repress Notch target gene expression during zebrafish neurogenesis and to maintain the production of motoneurones in response to hedgehog signalling. Development 131, 2983-2995 (2004).
29. Kim, J. E., Chen, J. & Lou, Z. DBC1 is a negative regulator of SIRT1. Nature 451, 583-586 (2008).
30. Zhao, W. et al. Negative regulation of the deacetylase SIRT1 by DBC1. Nature 451, 587-590 (2008).
31. Spiller, S. E., Ravanpay, A. C., Hahn, A. W. & Olson, J. M. Suberoylanilide hydroxamic acid is effective in preclinical studies of medulloblastoma. J. Neurooncol. 79, 259-270 (2006).
32. Ecke, I. et al. Antitumor effects of a combined 5-aza-2'deoxycytidine and valproic acid treatment on rhabdomyosarcoma and medulloblastoma in Ptch mutant mice. Cancer Res. 69, 887-895 (2009).
33. Scales, S. J. & de Sauvage, F. J. Mechanisms of Hedgehog pathway activation in cancer and implications for therapy. Trends Pharmacol. Sci. 30, 303-312 (2009).
34. Chun, S. G., Zhou, W. & Yee, N. S. Combined targeting of histone deacetylases and hedgehog signaling enhances cytoxicity in pancreatic cancer. Cancer Biol. Ther. 8, 1328-1339 (2009).
35. Canettieri, G. et al. Attenuation of a phosphorylation-dependent activator by an HDAC-PP1 complex. Nature Struct. Biol. 10, 175-181 (2003).
36. Zhang, Q. et al. A hedgehog-induced BTB protein modulates hedgehog signaling by degrading Ci/Gli transcription factor. Dev. Cell 10, 719-729 (2006).
37. Peschiaroli, A. et al. SCFβTrCP-mediated degradation of Claspin regulates recovery from the DNA replication checkpoint response. Mol. Cell 23, 319-329 (2006).
38. Gu, W. & Roeder, R. G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90, 595-606 (1997).
39. Zhao, X. et al. The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nature Cell Biol. 10, 643-653 (2008).
40. Lahm, A. et al. Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc. Natl Acad. Sci. USA 104, 17335-17340 (2007).
41. Pappin, D. J. Peptide mass fingerprinting using MALDI-TOF mass spectrometry. Methods Mol. Biol. 211, 211-219 (2003).
42. Skp2 SCF ubiquitin ligase complex. Nature 416, 703-709 (2002).