Role of SUMO-Interacting Motif in Daxx SUMO Modification, Subnuclear Localization, and Repression of Sumoylated Transcription Factors

Molecular Cell

Volumn 24, Issue 3, 2006, Pages 341-354

  Lin, Ding Yen ^a,b   Huang, Yen Sung ^a,c   Jeng, Jen Chong ^a,c   Kuo, Hong Yi ^a,c   Chang, Che Chang ^a   Chao, Ting Ting ^a,c   Ho, Chun Chen ^a   Chen, Yun Ching ^a   Lin, Tong Ping ^a   Fang, Hsin I ^a   Hung, Chih Chang ^c   Suen, Ching Shu ^a   Hwang, Ming Jing ^a   Chang, Kun Sang ^d   Maul, Gerd G ^e   Shih, Hsiu Ming ^a,c  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^c Graduate Institute of Life Sciences at TKU   (Taiwan)

^d Laboratory Medicine   (United States)

^e WISTAR INSTITUTE   (United States)

Author keywords

CELLBIO; PROTEINS

Indexed keywords

ARSENIC TRIOXIDE; DAXX PROTEIN; GLUCOCORTICOID RECEPTOR; SUMO PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELLULAR DISTRIBUTION; EMBRYO; FEMALE; GENE REPRESSION; HUMAN; HUMAN CELL; INTRANUCLEAR SPACE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; ONCOGENE; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ARSENICALS; CARRIER PROTEINS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; DEXAMETHASONE; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; NUCLEAR PROTEINS; OXIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, GLUCOCORTICOID; REPRESSOR PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 33750491062     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.10.019     Document Type: Article

References (44)

1. Ahn J.H., Xu Y., Jang W.J., Matunis M.J., and Hayward G.S. Evaluation of interactions of human cytomegalovirus immediate-early IE2 regulatory protein with small ubiquitin-like modifiers and their conjugation enzyme Ubc9. J. Virol. 75 (2001) 3859-3872
2. Baba D., Maita N., Jee J.G., Uchimura Y., Saitoh H., Sugasawa K., Hanaoka F., Tochio H., Hiroaki H., and Shirakawa M. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435 (2005) 979-982
3. Bernier-Villamor V., Sampson D.A., Matunis M.J., and Lima C.D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108 (2002) 345-356
4. Chang C.C., Lin D.Y., Fang H.I., Chen R.H., and Shih H.M. Daxx mediates the small ubiquitin-like modifier-dependent transcriptional repression of Smad4. J. Biol. Chem. 280 (2005) 10164-10173
5. Cheng J., Bawa T., Lee P., Gong L., and Yeh E.T. Role of desumoylation in the development of prostate cancer. Neoplasia 8 (2006) 667-676
6. Chupreta S., Holmstrom S., Subramanian L., and Iniguez-Lluhi J.A. A small conserved surface in SUMO is the critical structural determinant of its transcriptional inhibitory properties. Mol. Cell. Biol. 25 (2005) 4272-4282
7. Condemine W., Takahashi Y., Zhu J., Puvion-Dutilleul F., Guegan S., Janin A., and de The H. Characterization of endogenous human promyelocytic leukemia isoforms. Cancer Res. 66 (2006) 6192-6198
8. Gill G. Post-translational modification by the small ubiquitin-related modifier SUMO has big effects on transcription factor activity. Curr. Opin. Genet. Dev. 13 (2003) 108-113
9. Gill G. Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 15 (2005) 536-541
10. Girdwood D., Bumpass D., Vaughan O.A., Thain A., Anderson L.A., Snowden A.W., Garcia-Wilson E., Perkins N.D., and Hay R.T. P300 transcriptional repression is mediated by SUMO modification. Mol. Cell 11 (2003) 1043-1054
11. Guo A., Salomoni P., Luo J., Shih A., Zhong S., Gu W., and Paolo Pandolfi P. The function of PML in p53-dependent apoptosis. Nat. Cell Biol. 2 (2000) 730-736
12. Hay R.T. SUMO: a history of modification. Mol. Cell 18 (2005) 1-12
13. Holmstrom S., Van Antwerp M.E., and Iniguez-Lluhi J.A. Direct and distinguishable inhibitory roles for SUMO isoforms in the control of transcriptional synergy. Proc. Natl. Acad. Sci. USA 100 (2003) 15758-15763
14. Iniguez-Lluhi J.A., and Pearce D. A common motif within the negative regulatory regions of multiple factors inhibits their transcriptional synergy. Mol. Cell. Biol. 20 (2000) 6040-6050
15. Ishov A.M., Sotnikov A.G., Negorev D., Vladimirova O.V., Neff N., Kamitani T., Yeh E.T., Strauss III J.F., and Maul G.G. PML is critical for ND10 formation and recruits the PML-interacting protein Daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147 (1999) 221-234
16. Ishov A.M., Vladimirova O.V., and Maul G.G. Heterochromatin and ND10 are cell-cycle regulated and phosphorylation-dependent alternate nuclear sites of the transcription repressor Daxx and SWI/SNF protein ATRX. J. Cell Sci. 117 (2004) 3807-3820
17. Jang M.S., Ryu S.W., and Kim E. Modification of Daxx by small ubiquitin-related modifier-1. Biochem. Biophys. Res. Commun. 295 (2002) 495-500
18. Jensen K., Shiels C., and Freemont P.S. PML protein isoforms and the RBCC/TRIM motif. Oncogene 20 (2001) 7223-7233
19. Johnson E.S. Protein modification by sumo. Annu. Rev. Biochem. 73 (2004) 355-382
20. Kuo H.Y., Chang C.C., Jeng J.C., Hu H.M., Lin D.Y., Maul G.G., Kwok R.P., and Shih H.M. SUMO modification negatively modulates the transcriptional activity of CREB-binding protein via the recruitment of Daxx. Proc. Natl. Acad. Sci. USA 102 (2005) 16973-16978
21. Lallemand-Breitenbach V., Zhu J., Puvion F., Koken M., Honore N., Doubeikovsky A., Duprez E., Pandolfi P.P., Puvion E., Freemont P., and de The H. Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor alpha degradation. J. Exp. Med. 193 (2001) 1361-1371
22. Lehembre F., Muller S., Pandolfi P.P., and Dejean A. Regulation of Pax3 transcriptional activity by SUMO-1-modified PML. Oncogene 20 (2001) 1-9
23. Li H., Leo C., Zhu J., Wu X., O'Neil J., Park E.J., and Chen J.D. Sequestration and inhibition of Daxx-mediated transcriptional repression by PML. Mol. Cell. Biol. 20 (2000) 1784-1796
24. Lin D.Y., and Shih H.M. Essential role of the 58-kDa microspherule protein in the modulation of Daxx-dependent transcriptional repression as revealed by nucleolar sequestration. J. Biol. Chem. 277 (2002) 25446-25456
25. Lin D., Tatham M.H., Yu B., Kim S., Hay R.T., and Chen Y. Identification of a substrate recognition site on Ubc9. J. Biol. Chem. 277 (2002) 21740-21748
26. Lin D.Y., Lai M.Z., Ann D.K., and Shih H.M. Promyelocytic leukemia protein (PML) functions as a glucocorticoid receptor co-activator by sequestering Daxx to the PML oncogenic domains (PODs) to enhance its transactivation potential. J. Biol. Chem. 278 (2003) 15958-15965
27. Lin D.Y., Fang H.I., Ma A.H., Huang Y.S., Pu Y.S., Jenster G., Kung H.J., and Shih H.M. Negative modulation of androgen receptor transcriptional activity by Daxx. Mol. Cell. Biol. 24 (2004) 10529-10541
28. Melchior F., Schergaut M., and Pichler A. SUMO: ligases, isopeptidases and nuclear pores. Trends Biochem. Sci. 28 (2003) 612-618
29. Minty A., Dumont X., Kaghad M., and Caput D. Covalent modification of p73alpha by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J. Biol. Chem. 275 (2000) 36316-36323
30. Muller S., Matunis M.J., and Dejean A. Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17 (1998) 61-70
31. Owerbach D., McKay E.M., Yeh E.T., Gabbay K.H., and Bohren K.M. A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem. Biophys. Res. Commun. 337 (2005) 517-520
32. Reverter D., and Lima C.D. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435 (2005) 687-692
33. Rosendorff A., Sakakibara S., Lu S., Kieff E., Xuan Y., DiBacco A., Shi Y., Shi Y., and Gill G. NXP-2 association with SUMO-2 depends on lysines required for transcriptional repression. Proc. Natl. Acad. Sci. USA 103 (2006) 5308-5313
34. Ryu S.W., Chae S.K., and Kim E. Interaction of Daxx, a Fas binding protein, with sentrin and Ubc9. Biochem. Biophys. Res. Commun. 279 (2000) 6-10
35. Sampson D.A., Wang M., and Matunis M.J. The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276 (2001) 21664-21669
36. Song J., Durrin L.K., Wilkinson T.A., Krontiris T.G., and Chen Y. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. USA 101 (2004) 14373-14378
37. Song J., Zhang Z., Hu W., and Chen Y. Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J. Biol. Chem. 280 (2005) 40122-40129
38. Takahashi H., Hatakeyama S., Saitoh H., and Nakayama K.I. Noncovalent SUMO-1 binding activity of thymine DNA glycosylase (TDG) is required for its SUMO-1 modification and colocalization with the promyelocytic leukemia protein. J. Biol. Chem. 280 (2005) 5611-5621
39. Tian S., Poukka H., Palvimo J.J., and Janne O.A. Small ubiquitin-related modifier-1 (SUMO-1) modification of the glucocorticoid receptor. Biochem. J. 367 (2002) 907-911
40. Wang J.C., Derynck M.K., Nonaka D.F., Khodabakhsh D.B., Haqq C., and Yamamoto K.R. Chromatin immunoprecipitation (ChIP) scanning identifies primary glucocorticoid receptor target genes. Proc. Natl. Acad. Sci. USA 101 (2004) 15603-15608
41. Weger S., Hammer E., and Engstler M. The DNA topoisomerase I binding protein topors as a novel cellular target for SUMO-1 modification: characterization of domains necessary for subcellular localization and sumolation. Exp. Cell Res. 290 (2003) 13-27
42. Yang S.H., and Sharrocks A.D. SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell 13 (2004) 611-617
43. Zhong S., Muller S., Ronchetti S., Freemont P.S., Dejean A., and Pandolfi P.P. Role of SUMO-1-modified PML in nuclear body formation. Blood 95 (2000) 2748-2752
44. Zhu J., Zhou J., Peres L., Riaucoux F., Honore N., Kogan S., and de The H. A sumoylation site in PML/RARA is essential for leukemic transformation. Cancer Cell 7 (2005) 143-153