The UBC9 E2 sumo conjugating enzyme binds the PR-Set7 histone methyltransferase to facilitate target gene repression

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Spektor, Tanya M ^a   Congdon, Lauren M ^a   Veerappan, Chendhore S ^a   Rice, Judd C ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE METHYLTRANSFERASE; PR SET7 HISTONE METHYLTRANSFERASE; SUMO 1 PROTEIN; SUMO PROTEIN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME 9 E2; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; HISTONE LYSINE METHYLTRANSFERASE; LYSINE; MESSENGER RNA; REPRESSOR PROTEIN; SETD8 PROTEIN, HUMAN; SMALL INTERFERING RNA; SUMO1 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME UBC9; UBIQUITIN-CONJUGATING ENZYME UBC9;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE TARGETING; GENETIC IDENTIFICATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PROTEIN PROTEIN INTERACTION; SUMOYLATION; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; CELL CULTURE; CHEMISTRY; CYTOLOGY; DNA MICROARRAY; DRUG ANTAGONISM; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENETICS; HUMAN GENOME; IMMUNOPRECIPITATION; KIDNEY; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; TWO HYBRID SYSTEM; WESTERN BLOTTING;

AMINO ACID SEQUENCE; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, HUMAN; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; KIDNEY; LYSINE; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, AMINO ACID; SUMO-1 PROTEIN; SUMOYLATION; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN-CONJUGATING ENZYMES;

EID: 79960911178     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022785     Document Type: Article

References (40)

1. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ, (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
2. Strahl BD, Allis CD, (2000) The language of covalent histone modifications. Nature 403: 41-45.
3. Couture JF, Collazo E, Brunzelle JS, Trievel RC, (2005) Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase. Genes Dev 19: 1455-1465.
4. Fang J, Feng Q, Ketel CS, Wang H, Cao R, et al. (2002) Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr Biol 12: 1086-1099.
5. Nishioka K, Rice JC, Sarma K, Erdjument-Bromage H, Werner J, et al. (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell 9: 1201-1213.
6. Xiao B, Jing C, Kelly G, Walker PA, Muskett FW, et al. (2005) Specificity and mechanism of the histone methyltransferase Pr-Set7. Genes Dev 19: 1444-1454.
7. Houston SI, McManus KJ, Adams MM, Sims JK, Carpenter PB, et al. (2008) Catalytic function of the PR-Set7 histone H4 lysine 20 monomethyltransferase is essential for mitotic entry and genomic stability. J Biol Chem 283: 19478-19488.
8. Huen MS, Sy SM, van Deursen JM, Chen J, (2008) Direct interaction between SET8 and proliferating cell nuclear antigen couples H4-K20 methylation with DNA replication. J Biol Chem 283: 11073-11077.
9. Oda H, Okamoto I, Murphy N, Chu J, Price SM, et al. (2009) Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol Cell Biol 29: 2278-2295.
10. Sakaguchi A, Steward R, (2007) Aberrant monomethylation of histone H4 lysine 20 activates the DNA damage checkpoint in Drosophila melanogaster. J Cell Biol 176: 155-162.
11. Abbas T, Shibata E, Park J, Jha S, Karnani N, et al. (2010) CRL4(Cdt2) regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol Cell 40: 9-21.
12. Centore RC, Havens CG, Manning AL, Li JM, Flynn RL, et al. (2010) CRL4(Cdt2)-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol Cell 40: 22-33.
13. Oda H, Hubner MR, Beck DB, Vermeulen M, Hurwitz J, et al. (2010) Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol Cell 40: 364-376.
14. Tardat M, Brustel J, Kirsh O, Lefevbre C, Callanan M, et al. (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat Cell Biol 12: 1086-1093.
15. Wu S, Wang W, Kong X, Congdon LM, Yokomori K, et al. (2010) Dynamic regulation of the PR-Set7 histone methyltransferase is required for normal cell cycle progression. Genes Dev 24: 2531-2542.
16. Sims JK, Houston SI, Magazinnik T, Rice JC, (2006) A trans-tail histone code defined by monomethylated H4 Lys-20 and H3 Lys-9 demarcates distinct regions of silent chromatin. J Biol Chem 281: 12760-12766.
17. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
18. Talasz H, Lindner HH, Sarg B, Helliger W, (2005) Histone H4-lysine 20 monomethylation is increased in promoter and coding regions of active genes and correlates with hyperacetylation. J Biol Chem 280: 38814-38822.
19. Vakoc CR, Sachdeva MM, Wang H, Blobel GA, (2006) Profile of histone lysine methylation across transcribed mammalian chromatin. Mol Cell Biol 26: 9185-9195.
20. Gareau JR, Lima CD, (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11: 861-871.
21. Lin D, Tatham MH, Yu B, Kim S, Hay RT, et al. (2002) Identification of a substrate recognition site on Ubc9. J Biol Chem 277: 21740-21748.
22. Yunus AA, Lima CD, (2006) Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway. Nat Struct Mol Biol 13: 491-499.
23. Sampson DA, Wang M, Matunis MJ, (2001) The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J Biol Chem 276: 21664-21669.
24. Fernandez-Miranda G, de Castro IP, Carmena M, Aguirre-Portoles C, Ruchaud S, et al. (2010) SUMOylation modulates the function of Aurora-B kinase. J Cell Sci 123: 2823-2833.
25. Kirsh O, Seeler JS, Pichler A, Gast A, Muller S, et al. (2002) The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J 21: 2682-2691.
26. Congdon LM, Houston SI, Veerappan CS, Spektor TM, Rice JC, (2010) PR-Set7-mediated monomethylation of histone H4 lysine 20 at specific genomic regions induces transcriptional repression. J Cell Biochem 110: 609-619.
27. Sims JK, Rice JC, (2008) PR-Set7 establishes a repressive trans-tail histone code that regulates differentiation. Mol Cell Biol 28: 4459-4468.
28. Zeng L, Yap KL, Ivanov AV, Wang X, Mujtaba S, et al. (2008) Structural insights into human KAP1 PHD finger-bromodomain and its role in gene silencing. Nat Struct Mol Biol 15: 626-633.
29. Kim JH, Kim B, Cai L, Choi HJ, Ohgi KA, et al. (2005) Transcriptional regulation of a metastasis suppressor gene by Tip60 and beta-catenin complexes. Nature 434: 921-926.
30. Bernier-Villamor V, Sampson DA, Matunis MJ, Lima CD, (2002) Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108: 345-356.
31. Tatham MH, Chen Y, Hay RT, (2003) Role of two residues proximal to the active site of Ubc9 in substrate recognition by the Ubc9.SUMO-1 thiolester complex. Biochemistry 42: 3168-3179.
32. Yang M, Hsu CT, Ting CY, Liu LF, Hwang J, (2006) Assembly of a polymeric chain of SUMO1 on human topoisomerase I in vitro. J Biol Chem 281: 8264-8274.
33. Pichler A, Gast A, Seeler JS, Dejean A, Melchior F, (2002) The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108: 109-120.
34. Shin JA, Choi ES, Kim HS, Ho JC, Watts FZ, et al. (2005) SUMO modification is involved in the maintenance of heterochromatin stability in fission yeast. Mol Cell 19: 817-828.
35. Kalakonda N, Fischle W, Boccuni P, Gurvich N, Hoya-Arias R, et al. (2008) Histone H4 lysine 20 monomethylation promotes transcriptional repression by L3MBTL1. Oncogene 27: 4293-4304.
36. Girdwood D, Bumpass D, Vaughan OA, Thain A, Anderson LA, et al. (2003) P300 transcriptional repression is mediated by SUMO modification. Mol Cell 11: 1043-1054.
37. Kim JH, Choi HJ, Kim B, Kim MH, Lee JM, et al. (2006) Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis. Nat Cell Biol 8: 631-639.
38. Yang SH, Sharrocks AD, (2004) SUMO promotes HDAC-mediated transcriptional repression. Mol Cell 13: 611-617.
39. Rice JC, Briggs SD, Ueberheide B, Barber CM, Shabanowitz J, et al. (2003) Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 12: 1591-1598.
40. Ren J, Gao X, Jin C, Zhu M, Wang X, et al. (2009) Systematic study of protein sumoylation: Development of a site-specific predictor of SUMOsp 2.0. Proteomics 9: 3409-3412.