An Acetylation/Deacetylation-SUMOylation Switch through a Phylogenetically Conserved ψKXEP Motif in the Tumor Suppressor HIC1 Regulates Transcriptional Repression Activity

REFERENCES

• Bereshchenko, O. R., W. Gu, and R. Dalla-Favera. 2002. Acetylation inactivates the transcriptional repressor BCL6. Nat. Genet. 32:606–613.
   PubMed Web of Science ®Google Scholar
• Bertrand, S., S. Pinte, N. Stankovic-Valentin, S. Deltour-Balerdi, C. Guerardel, A. Begue, V. Laudet, and D. Leprince. 2004. Identification and developmental expression of the zebrafish orthologue of the tumor suppressor gene HIC1. Biochim. Biophys. Acta 1678:57–66.
   PubMedGoogle Scholar
• Blander, G., J. Olejnik, E. Krzymanska-Olejnik, T. McDonagh, M. Haigis, M. B. Yaffe, and L. Guarente. 2005. SIRT1 shows no substrate specificity in vitro. J. Biol. Chem. 280:9780–9785.
   PubMedGoogle Scholar
• Bossis, G., and F. Melchior. 2006. Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol. Cell 21:349–357.
   PubMed Web of Science ®Google Scholar
• Bourachot, B., M. Yaniv, and C. Muchardt. 2003. Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation. EMBO J. 22:6505–6515.
   PubMed Web of Science ®Google Scholar
• Braun, H., R. Koop, A. Ertmer, S. Nacht, and G. Suske. 2001. Transcription factor Sp3 is regulated by acetylation. Nucleic Acids Res. 29:4994–5000.
   PubMed Web of Science ®Google Scholar
• Britschgi, C., M. Rizzi, T. J. Grob, M. P. Tschan, B. Hugli, V. A. Reddy, A. C. Andres, B. E. Torbett, A. Tobler, and M. F. Fey. 2006. Identification of the p53 family-responsive element in the promoter region of the tumor suppressor gene hypermethylated in cancer 1. Oncogene 25:2030–2039.
   PubMedGoogle Scholar
• Capelson, M., and V. G. Corces. 2006. SUMO conjugation attenuates the activity of the gypsy chromatin insulator. EMBO J. 25:1906–1914.
   PubMedGoogle Scholar
• Carter, M. G., M. A. Johns, X. Zeng, L. Zhou, M. C. Zink, J. L. Mankowski, D. M. Donovan, and S. B. Baylin. 2000. Mice deficient in the candidate tumor suppressor gene Hic1 exhibit developmental defects of structures affected in the Miller-Dieker syndrome. Hum. Mol. Genet. 9:413–419.
   PubMedGoogle Scholar
• Chakrabarti, S. R., R. Sood, S. Nandi, and G. Nucifora. 2000. Posttranslational modification of TEL and TEL/AML1 by SUMO-1 and cell-cycle-dependent assembly into nuclear bodies. Proc. Natl. Acad. Sci. USA 97:13281–13285.
   PubMed Web of Science ®Google Scholar
• Chen, W., T. K. Cooper, C. A. Zahnow, M. Overholtzer, Z. Zhao, M. Ladanyi, J. E. Karp, N. Gokgoz, J. S. Wunder, I. L. Andrulis, A. J. Levine, J. L. Mankowski, and S. B. Baylin. 2004. Epigenetic and genetic loss of Hic1 function accentuates the role of p53 in tumorigenesis. Cancer Cells 6:387–398.
   PubMed Web of Science ®Google Scholar
• Chen, W. Y., D. H. Wang, R. C. Yen, J. Luo, W. Gu, and S. B. Baylin. 2005. Tumor suppressor HIC1 directly regulates SIRT1 to modulate p53-dependent DNA-damage responses. Cell 123:437–448.
   PubMed Web of Science ®Google Scholar
• Chen, W. Y., X. Zeng, M. G. Carter, C. N. Morrell, R. W. Chiu-Yen, M. Esteller, D. N. Watkins, J. G. Herman, J. L. Mankowski, and S. B. Baylin. 2003. Heterozygous disruption of Hic1 predisposes mice to a gender-dependent spectrum of malignant tumors. Nat. Genet. 33:197–202.
   PubMed Web of Science ®Google Scholar
• Deltour, S., C. Guerardel, and D. Leprince. 1999. Recruitment of SMRT/N-CoR-mSin3A-HDAC-repressing complexes is not a general mechanism for BTB/POZ transcriptional repressors: the case of HIC-1 and γFBP-B. Proc. Natl. Acad. Sci. USA 96:14831–14836.
   PubMedGoogle Scholar
• Deltour, S., S. Pinte, C. Guerardel, and D. Leprince. 2001. Characterization of HRG22, a human homologue of the putative tumor suppressor gene HIC1. Biochem. Biophys. Res. Commun. 287:427–434.
   PubMedGoogle Scholar
• Deltour, S., S. Pinte, C. Guerardel, B. Wasylyk, and D. Leprince. 2002. The human candidate tumor suppressor gene HIC1 recruits CtBP through a degenerate GLDLSKK motif. Mol. Cell. Biol. 22:4890–4901.
   PubMedGoogle Scholar
• Desterro, J. M., M. S. Rodriguez, and R. T. Hay. 1998. SUMO-1 modification of IκBα inhibits NF-κB activation. Mol. Cell 2:233–239.
   PubMed Web of Science ®Google Scholar
• Dhordain, P., O. Albagli, S. Ansieau, M. H. Koken, C. Deweindt, S. Quief, D. Lantoine, A. Leutz, J. P. Kerckaert, and D. Leprince. 1995. The BTB/POZ domain targets the LAZ3/BCL6 oncoprotein to nuclear dots and mediates homomerisation in vivo. Oncogene 11:2689–2697.
   PubMed Web of Science ®Google Scholar
• Dhordain, P., O. Albagli, R. J. Lin, S. Ansieau, S. Quief, A. Leutz, J. P. Kerckaert, R. M. Evans, and D. Leprince. 1997. Corepressor SMRT binds the BTB/POZ repressing domain of the LAZ3/BCL6 oncoprotein. Proc. Natl. Acad. Sci. USA 94:10762–10767.
   PubMed Web of Science ®Google Scholar
• Fu, M., M. Liu, A. A. Sauve, X. Jiao, X. Zhang, X. Wu, M. J. Powell, T. Yang, W. Gu, M. L. Avantaggiati, N. Pattabiraman, T. G. Pestell, F. Wang, A. A. Quong, C. Wang, and R. G. Pestell. 2006. Hormonal control of androgen receptor function through SIRT1. Mol. Cell. Biol. 26:8122–8135.
   PubMed Web of Science ®Google Scholar
• Fujita, N., D. L. Jaye, C. Geigerman, A. Akyildiz, M. R. Mooney, J. M. Boss, and P. A. Wade. 2004. MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119:75–86.
   PubMedGoogle Scholar
• Gill, G. 2005. Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 15:536–541.
   PubMed Web of Science ®Google Scholar
• Gill, G. 2004. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18:2046–2059.
   PubMed Web of Science ®Google Scholar
• Girdwood, D., D. Bumpass, O. A. Vaughan, A. Thain, L. A. Anderson, A. W. Snowden, E. Garcia-Wilson, N. D. Perkins, and R. T. Hay. 2003. P300 transcriptional repression is mediated by SUMO modification. Mol. Cell 11:1043–1054.
   PubMedGoogle Scholar
• Gong, Z., M. Brackertz, and R. Renkawitz. 2006. SUMO modification enhances p66-mediated transcriptional repression of the Mi-2/NuRD complex. Mol. Cell. Biol. 26:4519–4528.
   PubMedGoogle Scholar
• Grégoire, S., A. M. Tremblay, L. Xiao, Q. Yang, K. Ma, J. Nie, Z. Mao, Z. Wu, V. Giguere, and X. J. Yang. 2006. Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation. J. Biol. Chem. 281:4423–4433.
   PubMed Web of Science ®Google Scholar
• Grégoire, S., and X. J. Yang. 2005. Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol. Cell. Biol. 25:2273–2287.
   PubMed Web of Science ®Google Scholar
• Hay, R. T. 2005. SUMO: a history of modification. Mol. Cell 18:1–12.
   PubMed Web of Science ®Google Scholar
• Hietakangas, V., J. Anckar, H. A. Blomster, M. Fujimoto, J. J. Palvimo, A. Nakai, and L. Sistonen. 2006. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc. Natl. Acad. Sci. USA 103:45–50.
   PubMed Web of Science ®Google Scholar
• Jones, G., P. Willett, R. C. Glen, A. R. Leach, and R. Taylor. 1997. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267:727–748.
   PubMed Web of Science ®Google Scholar
• Kagey, M. H., T. A. Melhuish, S. E. Powers, and D. Wotton. 2005. Multiple activities contribute to Pc2 E3 function. EMBO J. 24:108–119.
   PubMedGoogle Scholar
• Kagey, M. H., T. A. Melhuish, and D. Wotton. 2003. The polycomb protein Pc2 is a SUMO E3. Cell 113:127–137.
   PubMed Web of Science ®Google Scholar
• Kirsh, O., J. S. Seeler, A. Pichler, A. Gast, S. Muller, E. Miska, M. Mathieu, A. Harel-Bellan, T. Kouzarides, F. Melchior, and A. Dejean. 2002. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21:2682–2691.
   PubMed Web of Science ®Google Scholar
• Langley, E., M. Pearson, M. Faretta, U. M. Bauer, R. A. Frye, S. Minucci, P. G. Pelicci, and T. Kouzarides. 2002. Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO J. 21:2383–2396.
   PubMed Web of Science ®Google Scholar
• Lefebvre, T., S. Pinte, C. Guerardel, S. Deltour, N. Martin-Soudant, M. C. Slomianny, J. C. Michalski, and D. Leprince. 2004. The tumor suppressor HIC1 (hypermethylated in cancer 1) is O-GlcNAc glycosylated. Eur. J. Biochem. 271:3843–3854.
   PubMedGoogle Scholar
• Lehembre, F., P. Badenhorst, S. Muller, A. Travers, F. Schweisguth, and A. Dejean. 2000. Covalent modification of the transcriptional repressor Tramtrack by the ubiquitin-related protein Smt3 in Drosophila flies. Mol. Cell. Biol. 20:1072–1082.
   PubMedGoogle Scholar
• Luo, J., A. Y. Nikolaev, S. Imai, D. Chen, F. Su, A. Shiloh, L. Guarente, and W. Gu. 2001. Negative control of p53 by Sir2α promotes cell survival under stress. Cell 107:137–148.
   PubMed Web of Science ®Google Scholar
• Melnick, A., G. Carlile, K. F. Ahmad, C. L. Kiang, C. Corcoran, V. Bardwell, G. G. Prive, and J. D. Licht. 2002. Critical residues within the BTB domain of PLZF and Bcl-6 modulate interaction with corepressors. Mol. Cell. Biol. 22:1804–1818.
   PubMed Web of Science ®Google Scholar
• Meziane-Tani, M., P. Lagant, A. Semmoud, and G. Vergoten. 2006. The SPASIBA force field for chondroitin sulfate: vibrational analysis of d-glucuronic and N-acetyl-d-galactosamine 4-sulfate sodium salts. J. Phys. Chem. A. 110:11359–11370.
   PubMed Web of Science ®Google Scholar
• Perdomo, J., A. Verger, J. Turner, and M. Crossley. 2005. Role for SUMO modification in facilitating transcriptional repression by BKLF. Mol. Cell. Biol. 25:1549–1559.
   PubMedGoogle Scholar
• Pichler, A., A. Gast, J. S. Seeler, A. Dejean, and F. Melchior. 2002. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108:109–120.
   PubMed Web of Science ®Google Scholar
• Pinte, S., N. Stankovic-Valentin, S. Deltour, B. R. Rood, C. Guerardel, and D. Leprince. 2004. The tumor suppressor gene HIC1 (hypermethylated in cancer 1) is a sequence-specific transcriptional repressor: definition of its consensus binding sequence and analysis of its DNA binding and repressive properties. J. Biol. Chem. 279:38313–38324.
   PubMedGoogle Scholar
• Ross, S., J. L. Best, L. I. Zon, and G. Gill. 2002. SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol. Cell 10:831–842.
   PubMed Web of Science ®Google Scholar
• Roth, S. Y., J. M. Denu, and C. D. Allis. 2001. Histone acetyltransferases. Annu. Rev. Biochem. 70:81–120.
   PubMed Web of Science ®Google Scholar
• Rui, H. L., E. Fan, H. M. Zhou, Z. Xu, Y. Zhang, and S. C. Lin. 2002. SUMO-1 modification of the C-terminal KVEKVD of Axin is required for JNK activation but has no effect on Wnt signaling. J. Biol. Chem. 277:42981–42986.
   PubMedGoogle Scholar
• Sapetschnig, A., G. Rischitor, H. Braun, A. Doll, M. Schergaut, F. Melchior, and G. Suske. 2002. Transcription factor Sp3 is silenced through SUMO modification by PIAS1. EMBO J. 21:5206–5215.
   PubMedGoogle Scholar
• Sato, Y., K. Miyake, H. Kaneoka, and S. Iijima. 2006. Sumoylation of CCAAT/enhancer-binding protein alpha and its functional roles in hepatocyte differentiation. J. Biol. Chem. 281:21629–21639.
   PubMedGoogle Scholar
• Schmidt, D., and S. Muller. 2003. PIAS/SUMO: new partners in transcriptional regulation. Cell. Mol. Life Sci. 60:2561–2574.
   PubMed Web of Science ®Google Scholar
• Seeler, J. S., and A. Dejean. 2003. Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell Biol. 4:690–699.
   PubMed Web of Science ®Google Scholar
• Seeler, J. S., A. Marchio, R. Losson, J. M. Desterro, R. T. Hay, P. Chambon, and A. Dejean. 2001. Common properties of nuclear body protein SP100 and TIF1α chromatin factor: role of SUMO modification. Mol. Cell. Biol. 21:3314–3324.
   PubMedGoogle Scholar
• Shalizi, A., B. Gaudilliere, Z. Yuan, J. Stegmuller, T. Shirogane, Q. Ge, Y. Tan, B. Schulman, J. W. Harper, and A. Bonni. 2006. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311:1012–1017.
   PubMed Web of Science ®Google Scholar
• Song, J., Z. Zhang, W. Hu, and Y. Chen. 2005. Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J. Biol. Chem. 280:40122–40129.
   PubMed Web of Science ®Google Scholar
• Stankovic-Valentin, N., A. Verger, S. Deltour-Balerdi, K. G. Quinlan, M. Crossley, and D. Leprince. 2006. A L225A substitution in the human tumour suppressor HIC1 abolishes its interaction with the corepressor CtBP. FEBS J. 273:2879–2890.
   PubMedGoogle Scholar
• Stogios, P. J., G. S. Downs, J. J. Jauhal, S. K. Nandra, and G. G. Prive. 2005. Sequence and structural analysis of BTB domain proteins. Genome Biol. 6:R82.
   PubMed Web of Science ®Google Scholar
• Valenta, T., J. Lukas, L. Doubravska, B. Fafilek, and V. Korinek. 2006. HIC1 attenuates Wnt signaling by recruitment of TCF-4 and β-catenin to the nuclear bodies. EMBO J. 25:2326–2337.
   PubMedGoogle Scholar
• Vaziri, H., S. K. Dessain, E. Ng Eaton, S. I. Imai, R. A. Frye, T. K. Pandita, L. Guarente, and R. A. Weinberg. 2001. hSIR2SIRT1 functions as an NAD-dependent p53 deacetylase. Cell 107:149–159.
   PubMed Web of Science ®Google Scholar
• Verger, A., J. Perdomo, and M. Crossley. 2003. Modification with SUMO. A role in transcriptional regulation. EMBO Rep. 4:137–142.
   PubMed Web of Science ®Google Scholar
• Vo, N., C. Fjeld, and R. H. Goodman. 2001. Acetylation of nuclear hormone receptor-interacting protein RIP140 regulates binding of the transcriptional corepressor CtBP. Mol. Cell. Biol. 21:6181–6188.
   PubMedGoogle Scholar
• Wales, M. M., M. A. Biel, W. El Deiry, B. D. Nelkin, J. P. Issa, W. K. Cavenee, S. J. Kuerbitz, and S. B. Baylin. 1995. p53 activates expression of HIC-1, a new candidate tumour suppressor gene on 17p13.3. Nat Med. 1:570–577.
   PubMed Web of Science ®Google Scholar
• Wang, J. M., C. Y. Ko, L. C. Chen, W. L. Wang, and W. C. Chang. 2006. Functional role of NF-IL6β and its sumoylation and acetylation modifications in promoter activation of cyclooxygenase 2 gene. Nucleic Acids Res. 34:217–231.
   PubMedGoogle Scholar
• Wynshaw-Boris, A., and M. J. Gambello. 2001. LIS1 and dynein motor function in neuronal migration and development. Genes Dev. 15:639–651.
   PubMed Web of Science ®Google Scholar
• Yang, S. H., and A. D. Sharrocks. 2004. SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell 13:611–617.
   PubMed Web of Science ®Google Scholar
• Yang, X. J., and S. Gregoire. 2006. A recurrent phospho-sumoyl switch in transcriptional repression and beyond. Mol. Cell 23:779–786.
   PubMedGoogle Scholar
• Zhao, X., T. Sternsdorf, T. A. Bolger, R. M. Evans, and T. P. Yao. 2005. Regulation of MEF2 by histone deacetylase 4- and SIRT1 deacetylase-mediated lysine modifications. Mol. Cell. Biol. 25:8456–8464.
   PubMed Web of Science ®Google Scholar