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Ligase/protein transport PDB id
1kps
Jmol
Contents
Protein chains
159 a.a. *
156 a.a. *
Ligands
SO4 ×4
Waters ×585
* Residue conservation analysis
PDB id:
1kps
Name: Ligase/protein transport
Title: Structural basis for e2-mediated sumo conjugation revealed by a complex between ubiquitin conjugating enzyme ubc9 and rangap1
Structure: Ubiquitin-like protein sumo-1 conjugating enzyme. Chain: a, c. Synonym: ubc9, sumo-1-protein ligase, ubiquitin carrier protein. Engineered: yes. Ran-gtpase activating protein 1. Chain: b, d. Synonym: rangap1. Engineered: yes
Source: Homo sapiens. Human. Organism_taxid: 9606. Gene: ubc9. Expressed in: escherichia coli. Expression_system_taxid: 562. Mus musculus. House mouse. Organism_taxid: 10090.
Biol. unit: Tetramer (from PQS)
Resolution:
2.50Å     R-factor:   0.223     R-free:   0.300
Authors: V.Bernier-Villamor,D.A.Sampson,M.J.Matunis,C.D.Lima
Key ref:
V.Bernier-Villamor et al. (2002). Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell, 108, 345-356. PubMed id: 11853669 DOI: 10.1016/S0092-8674(02)00630-X
Date:
02-Jan-02     Release date:   13-Feb-02    
PROCHECK
Go to PROCHECK summary
 Headers
 References

Protein chains
Pfam   ArchSchema ?
P63279  (UBC9_HUMAN) -  SUMO-conjugating enzyme UBC9
Seq:
Struc: 		158 a.a.
159 a.a.
Protein chains
Pfam   ArchSchema ?
P46061  (RAGP1_MOUSE) -  Ran GTPase-activating protein 1
Seq:
Struc: 		 
Seq:
Struc: 		589 a.a.
156 a.a.
Key:    PfamA domain  Secondary structure  CATH domain

 Gene Ontology (GO) functional annotation 
  GO annot!
  Cellular component     cytoplasm   4 terms 
  Biological process     cell cycle   13 terms 
  Biochemical function     nucleotide binding     11 terms  

 

 
DOI no: 10.1016/S0092-8674(02)00630-X Cell 108:345-356 (2002)
PubMed id: 11853669  
 
 
Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1.
V.Bernier-Villamor, D.A.Sampson, M.J.Matunis, C.D.Lima.
 
  ABSTRACT  
 
E2 enzymes catalyze attachment of ubiquitin and ubiquitin-like proteins to lysine residues directly or through E3-mediated reactions. The small ubiquitin-like modifier SUMO regulates nuclear transport, stress response, and signal transduction in eukaryotes and is essential for cell-cycle progression in yeast. In contrast to most ubiquitin conjugation, the SUMO E2 enzyme Ubc9 is sufficient for substrate recognition and lysine modification of known SUMO targets. Crystallographic analysis of a complex between mammalian Ubc9 and a C-terminal domain of RanGAP1 at 2.5 A reveals structural determinants for recognition of consensus SUMO modification sequences found within SUMO-conjugated proteins. Structure-based mutagenesis and biochemical analysis of Ubc9 and RanGAP1 reveal distinct motifs required for substrate binding and SUMO modification of p53, IkappaBalpha, and RanGAP1.
 
  Selected figure(s)  
 
Figure 3.
Figure 3. Ribbon and Stereo Diagrams for Ubc9-RanGAP1.(A and B) Orthogonal ribbon representations with helices lettered and strands numbered, as in Figure 2. Ubc9 Cys93 and RanGAP1 Leu525, Lys526, and Glu528 are in solid bonds. N and C termini are denoted in italics.(C) Stereo image of the complex, as in (A). 		Figure 5.
Figure 5. Models for Ubc9 Surfaces Utilized in Substrate, SUMO, E2, and E3 Binding(A) Surface and bond representations for Ubc9 and the RanGAP1 SUMO tetrapeptide motif, respectively. Ubc9 Asp127 (red), Cys93 (green), and Tyr87 (pink) are indicated on the Ubc9 surface. The location of the channel discussed in the text is indicated by a yellow arrow.(B) Orthogonal view of (A). RanGAP1 Lys526 Nε atom is visible beyond the yellow arrow.(C–E) Orthogonal Ubc9 surface representations in complex with RanGAP1, Mms2, E6AP, and Cbl. The RanGAP1 SUMO motif is represented by solid bonds, RanGAP1(420–589)p as a red worm, the Cbl ring finger as a light blue worm, the E6AP Hect domain as a dark blue worm, and Mms2 as a green worm. Surface area buried in respective complexes is shown as a red surface (RanGAP1), a green surface (Mms2), and a blue surface (E6AP and Cbl, combined). E2s from each complex were aligned to Ubc9 by least-squares minimization on Cα atoms. Figure 5 and Figure 7 were prepared with GRASP (Nicholls et al., 1991).
 
  The above figures are reprinted by permission from Cell Press: Cell (2002, 108, 345-356) copyright 2002.  
  Figures were selected by the author.  

Literature references that cite this PDB file's key reference

  PubMed id Reference
21139563 M.Grünwald, and F.Bono (2011).
Structure of Importin13-Ubc9 complex: nuclear import and release of a key regulator of sumoylation.
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PDB code: 2xwu
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20676127 D.Ythier, D.Larrieu, R.Binet, O.Binda, C.Brambilla, S.Gazzeri, and R.Pedeux (2010).
Sumoylation of ING2 regulates the transcription mediated by Sin3A.
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20396627 G.Brahemi, A.M.Burger, A.D.Westwell, and A.Brancale (2010).
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21079245 H.Ryu, M.Furuta, D.Kirkpatrick, S.P.Gygi, and Y.Azuma (2010).
PIASy-dependent SUMOylation regulates DNA topoisomerase IIalpha activity.
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21102611 J.R.Gareau, and C.D.Lima (2010).
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20224423 J.S.Rougier, M.Albesa, and H.Abriel (2010).
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21209884 J.Wang, A.M.Taherbhoy, H.W.Hunt, S.N.Seyedin, D.W.Miller, D.J.Miller, D.T.Huang, and B.A.Schulman (2010).
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20704751 M.Sadowski, and B.Sarcevic (2010).
Mechanisms of mono- and poly-ubiquitination: Ubiquitination specificity depends on compatibility between the E2 catalytic core and amino acid residues proximal to the lysine.
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20194622 M.Sadowski, R.Suryadinata, X.Lai, J.Heierhorst, and B.Sarcevic (2010).
Molecular basis for lysine specificity in the yeast ubiquitin-conjugating enzyme Cdc34.
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A mechanistic view of the role of E3 in sumoylation.
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20855607 N.Elrouby, and G.Coupland (2010).
Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes.
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20544217 Y.C.Shin, B.Y.Liu, J.Y.Tsai, J.T.Wu, L.K.Chang, and S.C.Chang (2010).
Biochemical characterization of the small ubiquitin-like modifiers of Chlamydomonas reinhardtii.
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20332821 Y.Wang, F.Lin, and Z.H.Qin (2010).
The role of post-translational modifications of huntingtin in the pathogenesis of Huntington's disease.
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Purification of SUMO conjugating enzymes and kinetic analysis of substrate conjugation.
  Methods Mol Biol, 497, 167-186.  
19748360 A.A.Yunus, and C.D.Lima (2009).
Structure of the Siz/PIAS SUMO E3 ligase Siz1 and determinants required for SUMO modification of PCNA.
  Mol Cell, 35, 669-682.  
19643821 A.Romanenko, A.Kakehashi, K.Morimura, H.Wanibuchi, M.Wei, A.Vozianov, and S.Fukushima (2009).
Urinary bladder carcinogenesis induced by chronic exposure to persistent low-dose ionizing radiation after Chernobyl accident.
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  19638400 C.Figueroa-Romero, J.A.Iñiguez-Lluhí, J.Stadler, C.R.Chang, D.Arnoult, P.J.Keller, Y.Hong, C.Blackstone, and E.L.Feldman (2009).
SUMOylation of the mitochondrial fission protein Drp1 occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle.
  FASEB J, 23, 3917-3927.  
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Identification of SUMO-binding motifs by NMR.
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Preparation of SUMO proteases and kinetic analysis using endogenous substrates.
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19684601 F.Mohideen, A.D.Capili, P.M.Bilimoria, T.Yamada, A.Bonni, and C.D.Lima (2009).
A molecular basis for phosphorylation-dependent SUMO conjugation by the E2 UBC9.
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19240082 H.A.Blomster, V.Hietakangas, J.Wu, P.Kouvonen, S.Hautaniemi, and L.Sistonen (2009).
Novel proteomics strategy brings insight into the prevalence of SUMO-2 target sites.
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20064473 H.B.Kamadurai, J.Souphron, D.C.Scott, D.M.Duda, D.J.Miller, D.Stringer, R.C.Piper, and B.A.Schulman (2009).
Insights into ubiquitin transfer cascades from a structure of a UbcH5B approximately ubiquitin-HECT(NEDD4L) complex.
  Mol Cell, 36, 1095-1102.  
19721078 H.H.Hsiao, E.Meulmeester, B.T.Frank, F.Melchior, and H.Urlaub (2009).
"ChopNSpice," a mass spectrometric approach that allows identification of endogenous small ubiquitin-like modifier-conjugated peptides.
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19887645 M.Mo, S.B.Fleming, and A.A.Mercer (2009).
Cell cycle deregulation by a poxvirus partial mimic of anaphase-promoting complex subunit 11.
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19285941 S.Zhu, J.Goeres, K.M.Sixt, M.Békés, X.D.Zhang, G.S.Salvesen, and M.J.Matunis (2009).
Protection from isopeptidase-mediated deconjugation regulates paralog-selective sumoylation of RanGAP1.
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Defining an Embedded Code for Protein Ubiquitination.
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SUMOylation and deSUMOylation at a glance.
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19186998 Z.Xu, H.Y.Chan, W.L.Lam, K.H.Lam, L.S.Lam, T.B.Ng, and S.W.Au (2009).
SUMO proteases: redox regulation and biological consequences.
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18313922 B.Palancade, and V.Doye (2008).
Sumoylating and desumoylating enzymes at nuclear pores: underpinning their unexpected duties?
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18628979 E.M.Riising, R.Boggio, S.Chiocca, K.Helin, and D.Pasini (2008).
The polycomb repressive complex 2 is a potential target of SUMO modifications.
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18538659 E.Meulmeester, M.Kunze, H.H.Hsiao, H.Urlaub, and F.Melchior (2008).
Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25.
  Mol Cell, 30, 610-619.  
18715992 H.Ullah, E.L.Scappini, A.F.Moon, L.V.Williams, D.L.Armstrong, and L.C.Pedersen (2008).
Structure of a signal transduction regulator, RACK1, from Arabidopsis thaliana.
  Protein Sci, 17, 1771-1780.
PDB code: 3dm0
18155241 H.Windecker, and H.D.Ulrich (2008).
Architecture and assembly of poly-SUMO chains on PCNA in Saccharomyces cerevisiae.
  J Mol Biol, 376, 221-231.  
18391405 J.L.Knight, Z.Zhou, E.Gallicchio, D.M.Himmel, R.A.Friesner, E.Arnold, and R.M.Levy (2008).
Exploring structural variability in X-ray crystallographic models using protein local optimization by torsion-angle sampling.
  Acta Crystallogr D Biol Crystallogr, 64, 383-396.  
18708356 J.Zhu, S.Zhu, C.M.Guzzo, N.A.Ellis, K.S.Sung, C.Y.Choi, and M.J.Matunis (2008).
Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification.
  J Biol Chem, 283, 29405-29415.  
18691969 P.Knipscheer, A.Flotho, H.Klug, J.V.Olsen, W.J.van Dijk, A.Fish, E.S.Johnson, M.Mann, T.K.Sixma, and A.Pichler (2008).
Ubc9 sumoylation regulates SUMO target discrimination.
  Mol Cell, 31, 371-382.
PDB code: 2vrr
18562626 S.R.Holmstrom, S.Chupreta, A.Y.So, and J.A.Iñiguez-Lluhí (2008).
SUMO-mediated inhibition of glucocorticoid receptor synergistic activity depends on stable assembly at the promoter but not on DAXX.
  Mol Endocrinol, 22, 2061-2075.  
18493050 Y.Wang, I.Ladunga, A.R.Miller, K.M.Horken, T.Plucinak, D.P.Weeks, and C.P.Bailey (2008).
The small ubiquitin-like modifier (SUMO) and SUMO-conjugating system of Chlamydomonas reinhardtii.
  Genetics, 179, 177-192.  
18492068 Z.Tang, C.M.Hecker, A.Scheschonka, and H.Betz (2008).
Protein interactions in the sumoylation cascade: lessons from X-ray structures.
  FEBS J, 275, 3003-3015.  
17466333 A.D.Capili, and C.D.Lima (2007).
Structure and analysis of a complex between SUMO and Ubc9 illustrates features of a conserved E2-Ubl interaction.
  J Mol Biol, 369, 608-618.
PDB code: 2pe6
17919899 A.D.Capili, and C.D.Lima (2007).
Taking it step by step: mechanistic insights from structural studies of ubiquitin/ubiquitin-like protein modification pathways.
  Curr Opin Struct Biol, 17, 726-735.  
17803214 A.Heifetz, S.Pal, and G.R.Smith (2007).
Protein-protein docking: progress in CAPRI rounds 6-12 using a combination of methods: the introduction of steered solvated molecular dynamics.
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17418786 B.P.Somesh, S.Sigurdsson, H.Saeki, H.Erdjument-Bromage, P.Tempst, and J.Q.Svejstrup (2007).
Communication between distant sites in RNA polymerase II through ubiquitylation factors and the polymerase CTD.
  Cell, 129, 57-68.  
17646165 C.C.Chou, C.Chang, J.H.Liu, L.F.Chen, C.D.Hsiao, and H.Chen (2007).
Small ubiquitin-like modifier modification regulates the DNA binding activity of glial cell missing Drosophila homolog a.
  J Biol Chem, 282, 27239-27249.  
17446168 C.F.Woeller, D.D.Anderson, D.M.Szebenyi, and P.J.Stover (2007).
Evidence for small ubiquitin-like modifier-dependent nuclear import of the thymidylate biosynthesis pathway.
  J Biol Chem, 282, 17623-17631.  
17475278 D.M.Duda, R.C.van Waardenburg, L.A.Borg, S.McGarity, A.Nourse, M.B.Waddell, M.A.Bjornsti, and B.A.Schulman (2007).
Structure of a SUMO-binding-motif mimic bound to Smt3p-Ubc9p: conservation of a non-covalent ubiquitin-like protein-E2 complex as a platform for selective interactions within a SUMO pathway.
  J Mol Biol, 369, 619-630.
PDB code: 2eke
17911097 H.Yi, J.L.Friedman, and P.A.Ferreira (2007).
The cyclophilin-like domain of Ran-binding protein-2 modulates selectively the activity of the ubiquitin-proteasome system and protein biogenesis.
  J Biol Chem, 282, 34770-34778.  
17093186 J.L.Spidel, C.B.Wilson, R.C.Craven, and J.W.Wills (2007).
Genetic Studies of the beta-hairpin loop of Rous sarcoma virus capsid protein.
  J Virol, 81, 1288-1296.  
17643372 J.Wang, W.Hu, S.Cai, B.Lee, J.Song, and Y.Chen (2007).
The intrinsic affinity between E2 and the Cys domain of E1 in ubiquitin-like modifications.
  Mol Cell, 27, 228-237.
PDB code: 2px9
17803212 K.Wiehe, B.Pierce, W.W.Tong, H.Hwang, J.Mintseris, and Z.Weng (2007).
The performance of ZDOCK and ZRANK in rounds 6-11 of CAPRI.
  Proteins, 69, 719-725.  
17265167 M.W.Chiu, H.M.Shih, T.H.Yang, and Y.L.Yang (2007).
The type 2 dengue virus envelope protein interacts with small ubiquitin-like modifier-1 (SUMO-1) conjugating enzyme 9 (Ubc9).
  J Biomed Sci, 14, 429-444.  
18000527 R.Geiss-Friedlander, and F.Melchior (2007).
Concepts in sumoylation: a decade on.
  Nat Rev Mol Cell Biol, 8, 947-956.  
17965193 S.Lorenzen, and Y.Zhang (2007).
Monte Carlo refinement of rigid-body protein docking structures with backbone displacement and side-chain optimization.
  Protein Sci, 16, 2716-2725.  
17987030 S.Martin, K.A.Wilkinson, A.Nishimune, and J.M.Henley (2007).
Emerging extranuclear roles of protein SUMOylation in neuronal function and dysfunction.
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  20103862 Y.Chen (2007).
The enzymes in ubiquitin-like post-translational modifications.
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16820290 Y.H.Oh, M.Y.Hong, Z.Jin, T.Lee, M.K.Han, S.Park, and H.S.Kim (2007).
Chip-based analysis of SUMO (small ubiquitin-like modifier) conjugation to a target protein.
  Biosens Bioelectron, 22, 1260-1267.  
17336575 Y.L.Chang, C.J.Huang, J.Y.Chan, P.Y.Liu, H.P.Chang, and S.M.Huang (2007).
Regulation of nuclear receptor and coactivator functions by the carboxyl terminus of ubiquitin-conjugating enzyme 9.
  Int J Biochem Cell Biol, 39, 1035-1046.  
16732283 A.A.Yunus, and C.D.Lima (2006).
Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway.
  Nat Struct Mol Biol, 13, 491-499.
PDB codes: 2grn 2gro 2grp 2grq 2grr
16563226 C.Riquelme, K.K.Barthel, and X.Liu (2006).
SUMO-1 modification of MEF2A regulates its transcriptional activity.
  J Cell Mol Med, 10, 132-144.  
17000875 D.Mukhopadhyay, F.Ayaydin, N.Kolli, S.H.Tan, T.Anan, A.Kametaka, Y.Azuma, K.D.Wilkinson, and M.Dasso (2006).
SUSP1 antagonizes formation of highly SUMO2/3-conjugated species.
  J Cell Biol, 174, 939-949.  
17099700 D.Reverter, and C.D.Lima (2006).
Structural basis for SENP2 protease interactions with SUMO precursors and conjugated substrates.
  Nat Struct Mol Biol, 13, 1060-1068.
PDB codes: 2io0 2io1 2io2 2io3
16602682 J.A.Wohlschlegel, E.S.Johnson, S.I.Reed, and J.R.Yates (2006).
Improved identification of SUMO attachment sites using C-terminal SUMO mutants and tailored protease digestion strategies.
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16428449 J.Anckar, V.Hietakangas, K.Denessiouk, D.J.Thiele, M.S.Johnson, and L.Sistonen (2006).
Inhibition of DNA binding by differential sumoylation of heat shock factors.
  Mol Cell Biol, 26, 955-964.  
16478538 J.Kang, C.B.Gocke, and H.Yu (2006).
Phosphorylation-facilitated sumoylation of MEF2C negatively regulates its transcriptional activity.
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16681758 K.Okino, H.Nagai, H.Nakayama, D.Doi, K.Yoneyama, H.Konishi, and T.Takeshita (2006).
Inactivation of Crk SH3 domain-binding guanine nucleotide-releasing factor (C3G) in cervical squamous cell carcinoma.
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17099698 L.Shen, M.H.Tatham, C.Dong, A.Zagórska, J.H.Naismith, and R.T.Hay (2006).
SUMO protease SENP1 induces isomerization of the scissile peptide bond.
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PDB codes: 2iy0 2iy1
16857984 L.Song, S.Bhattacharya, A.A.Yunus, C.D.Lima, and C.Schindler (2006).
Stat1 and SUMO modification.
  Blood, 108, 3237-3244.  
16518696 M.J.Lewis, L.F.Saltibus, D.D.Hau, W.Xiao, and L.Spyracopoulos (2006).
Structural basis for non-covalent interaction between ubiquitin and the ubiquitin conjugating enzyme variant human MMS2.
  J Biomol NMR, 34, 89.
PDB code: 1zgu
16319071 M.S.Macauley, W.J.Errington, M.Schärpf, C.D.Mackereth, A.G.Blaszczak, B.J.Graves, and L.P.McIntosh (2006).
Beads-on-a-string, characterization of ETS-1 sumoylated within its flexible N-terminal sequence.
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16601690 M.Wang, D.Cheng, J.Peng, and C.M.Pickart (2006).
Molecular determinants of polyubiquitin linkage selection by an HECT ubiquitin ligase.
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16753028 O.Kerscher, R.Felberbaum, and M.Hochstrasser (2006).
Modification of proteins by ubiquitin and ubiquitin-like proteins.
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16757944 P.Knipscheer, and T.K.Sixma (2006).
Divide and conquer: the E2 active site.
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16782883 R.C.van Waardenburg, D.M.Duda, C.S.Lancaster, B.A.Schulman, and M.A.Bjornsti (2006).
Distinct functional domains of Ubc9 dictate cell survival and resistance to genotoxic stress.
  Mol Cell Biol, 26, 4958-4969.
PDB code: 2gjd
16356933 S.Grégoire, A.M.Tremblay, L.Xiao, Q.Yang, K.Ma, J.Nie, Z.Mao, Z.Wu, V.Giguère, and X.J.Yang (2006).
Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation.
  J Biol Chem, 281, 4423-4433.  
17036045 S.H.Yang, A.Galanis, J.Witty, and A.D.Sharrocks (2006).
An extended consensus motif enhances the specificity of substrate modification by SUMO.
  EMBO J, 25, 5083-5093.  
16973431 X.J.Yang, and S.Grégoire (2006).
A recurrent phospho-sumoyl switch in transcriptional repression and beyond.
  Mol Cell, 23, 779-786.  
16966324 Y.H.Hsu, K.P.Sarker, I.Pot, A.Chan, S.J.Netherton, and S.Bonni (2006).
Sumoylated SnoN represses transcription in a promoter-specific manner.
  J Biol Chem, 281, 33008-33018.  
16738318 Z.Gong, 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.  
15723079 A.Pichler, P.Knipscheer, E.Oberhofer, W.J.van Dijk, R.Körner, J.V.Olsen, S.Jentsch, F.Melchior, and T.K.Sixma (2005).
SUMO modification of the ubiquitin-conjugating enzyme E2-25K.
  Nat Struct Mol Biol, 12, 264-269.
PDB codes: 2bep 2bf8
15561718 C.B.Gocke, H.Yu, and J.Kang (2005).
Systematic identification and analysis of mammalian small ubiquitin-like modifier substrates.
  J Biol Chem, 280, 5004-5012.  
15857832 C.Degerny, D.Monte, C.Beaudoin, E.Jaffray, L.Portois, R.T.Hay, Y.de Launoit, and J.L.Baert (2005).
SUMO modification of the Ets-related transcription factor ERM inhibits its transcriptional activity.
  J Biol Chem, 280, 24330-24338.  
15931224 D.Reverter, and C.D.Lima (2005).
Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex.
  Nature, 435, 687-692.
PDB code: 1z5s
15694336 D.T.Huang, A.Paydar, M.Zhuang, M.B.Waddell, J.M.Holton, and B.A.Schulman (2005).
Structural basis for recruitment of Ubc12 by an E2 binding domain in NEDD8's E1.
  Mol Cell, 17, 341-350.
PDB code: 1y8x
15601841 E.A.Andrews, J.Palecek, J.Sergeant, E.Taylor, A.R.Lehmann, and F.Z.Watts (2005).
Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage.
  Mol Cell Biol, 25, 185-196.  
16224784 H.Ding, Y.Yang, J.Zhang, J.Wu, H.Liu, and Y.Shi (2005).
Structural basis for SUMO-E2 interaction revealed by a complex model using docking approach in combination with NMR data.
  Proteins, 61, 1050-1058.
PDB code: 1z5q
15817450 H.R.Jacquiau, R.C.van Waardenburg, R.J.Reid, M.H.Woo, H.Guo, E.S.Johnson, and M.A.Bjornsti (2005).
Defects in SUMO (small ubiquitin-related modifier) conjugation and deconjugation alter cell sensitivity to DNA topoisomerase I-induced DNA damage.
  J Biol Chem, 280, 23566-23575.  
15590687 J.T.Hannich, A.Lewis, M.B.Kroetz, S.J.Li, H.Heide, A.Emili, and M.Hochstrasser (2005).
Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae.
  J Biol Chem, 280, 4102-4110.  
15592428 M.H.Kagey, T.A.Melhuish, S.E.Powers, and D.Wotton (2005).
Multiple activities contribute to Pc2 E3 function.
  EMBO J, 24, 108-119.  
15999109 M.J.Matunis, and C.M.Pickart (2005).
Beginning at the end with SUMO.
  Nat Struct Mol Biol, 12, 565-566.  
15679615 R.Laan, W.M.Baarends, E.Wassenaar, H.P.Roest, J.H.Hoeijmakers, and J.A.Grootegoed (2005).
Expression and possible functions of DNA lesion bypass proteins in spermatogenesis.
  Int J Androl, 28, 1.  
15808504 R.T.Hay (2005).
SUMO: a history of modification.
  Mol Cell, 18, 1.  
15743823 S.Grégoire, and X.J.Yang (2005).
Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors.
  Mol Cell Biol, 25, 2273-2287.  
15820677 S.Rajan, L.D.Plant, M.L.Rabin, M.H.Butler, and S.A.Goldstein (2005).
Sumoylation silences the plasma membrane leak K+ channel K2P1.
  Cell, 121, 37-47.  
15933717 Y.Azuma, A.Arnaoutov, T.Anan, and M.Dasso (2005).
PIASy mediates SUMO-2 conjugation of Topoisomerase-II on mitotic chromosomes.
  EMBO J, 24, 2172-2182.  
16162816 Y.Morita, C.Kanei-Ishii, T.Nomura, and S.Ishii (2005).
TRAF7 sequesters c-Myb to the cytoplasm by stimulating its sumoylation.
  Mol Biol Cell, 16, 5433-5444.  
16300471 Y.Y.Mo, and S.J.Moschos (2005).
Targeting Ubc9 for cancer therapy.
  Expert Opin Ther Targets, 9, 1203-1216.  
15175327 A.C.Vertegaal, S.C.Ogg, E.Jaffray, M.S.Rodriguez, R.T.Hay, J.S.Andersen, M.Mann, and A.I.Lamond (2004).
A proteomic study of SUMO-2 target proteins.
  J Biol Chem, 279, 33791-33798.  
14990696 A.G.Castillo, L.J.Kong, L.Hanley-Bowdoin, and E.R.Bejarano (2004).
Interaction between a geminivirus replication protein and the plant sumoylation system.
  J Virol, 78, 2758-2769.  
15312912 A.N.Hegde (2004).
Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity.
  Prog Neurobiol, 73, 311-357.  
15378033 A.Pichler, P.Knipscheer, H.Saitoh, T.K.Sixma, and F.Melchior (2004).
The RanBP2 SUMO E3 ligase is neither HECT- nor RING-type.
  Nat Struct Mol Biol, 11, 984-991.  
14747994 B.M.Kus, C.E.Caldon, R.Andorn-Broza, and A.M.Edwards (2004).
Functional interaction of 13 yeast SCF complexes with a set of yeast E2 enzymes in vitro.
  Proteins, 54, 455-467.  
15062086 C.Dominguez, A.M.Bonvin, G.S.Winkler, F.M.van Schaik, H.T.Timmers, and R.Boelens (2004).
Structural model of the UbcH5B/CNOT4 complex revealed by combining NMR, mutagenesis, and docking approaches.
  Structure, 12, 633-644.
PDB code: 1ur6
15296745 D.Reverter, and C.D.Lima (2004).
A basis for SUMO protease specificity provided by analysis of human Senp2 and a Senp2-SUMO complex.
  Structure, 12, 1519-1531.
PDB codes: 1tgz 1th0
15361859 D.T.Huang, D.W.Miller, R.Mathew, R.Cassell, J.M.Holton, M.F.Roussel, and B.A.Schulman (2004).
A unique E1-E2 interaction required for optimal conjugation of the ubiquitin-like protein NEDD8.
  Nat Struct Mol Biol, 11, 927-935.
PDB code: 1tt5
  15209380 D.W.Girdwood, M.H.Tatham, and R.T.Hay (2004).
SUMO and transcriptional regulation.
  Semin Cell Dev Biol, 15, 201-210.  
15189146 E.S.Johnson (2004).
Protein modification by SUMO.
  Annu Rev Biochem, 73, 355-382.  
14673145 J.Hemelaar, A.Borodovsky, B.M.Kessler, D.Reverter, J.Cook, N.Kolli, T.Gan-Erdene, K.D.Wilkinson, G.Gill, C.D.Lima, H.L.Ploegh, and H.Ovaa (2004).
Specific and covalent targeting of conjugating and deconjugating enzymes of ubiquitin-like proteins.
  Mol Cell Biol, 24, 84-95.  
15388847 J.Song, L.K.Durrin, T.A.Wilkinson, T.G.Krontiris, and Y.Chen (2004).
Identification of a SUMO-binding motif that recognizes SUMO-modified proteins.
  Proc Natl Acad Sci U S A, 101, 14373-14378.  
15028714 M.Liang, F.Melchior, X.H.Feng, and X.Lin (2004).
Regulation of Smad4 sumoylation and transforming growth factor-beta signaling by protein inhibitor of activated STAT1.
  J Biol Chem, 279, 22857-22865.  
15449058 M.Novatchkova, R.Budhiraja, G.Coupland, F.Eisenhaber, and A.Bachmair (2004).
SUMO conjugation in plants.
  Planta, 220, 1-8.  
15355965 M.S.Macauley, W.J.Errington, M.Okon, M.Schärpf, C.D.Mackereth, B.A.Schulman, and L.P.McIntosh (2004).
Structural and dynamic independence of isopeptide-linked RanGAP1 and SUMO-1.
  J Biol Chem, 279, 49131-49137.  
15082759 M.T.Vassileva, and M.J.Matunis (2004).
SUMO modification of heterogeneous nuclear ribonucleoproteins.
  Mol Cell Biol, 24, 3623-3632.  
15341722 P.J.Winn, T.L.Religa, J.N.Battey, A.Banerjee, and R.C.Wade (2004).
Determinants of functionality in the ubiquitin conjugating enzyme family.
  Structure, 12, 1563-1574.  
15272016 T.L.Chung, H.H.Hsiao, Y.Y.Yeh, H.L.Shia, Y.L.Chen, P.H.Liang, A.H.Wang, K.H.Khoo, and S.Shoei-Lung Li (2004).
In vitro modification of human centromere protein CENP-C fragments by small ubiquitin-like modifier (SUMO) protein: definitive identification of the modification sites by tandem mass spectrometry analysis of the isopeptides.
  J Biol Chem, 279, 39653-39662.  
  12944097 B.R.Wong, F.Parlati, K.Qu, S.Demo, T.Pray, J.Huang, D.G.Payan, and M.K.Bennett (2003).
Drug discovery in the ubiquitin regulatory pathway.
  Drug Discov Today, 8, 746-754.  
12826404 D.C.Schwartz, and M.Hochstrasser (2003).
A superfamily of protein tags: ubiquitin, SUMO and related modifiers.
  Trends Biochem Sci, 28, 321-328.  
12941945 G.R.Bylebyl, I.Belichenko, and E.S.Johnson (2003).
The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast.
  J Biol Chem, 278, 44113-44120.  
12740394 H.He, Y.Dang, F.Dai, Z.Guo, J.Wu, X.She, Y.Pei, Y.Chen, W.Ling, C.Wu, S.Zhao, J.O.Liu, and L.Yu (2003).
Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B.
  J Biol Chem, 278, 29278-29287.  
12679040 M.H.Kagey, T.A.Melhuish, and D.Wotton (2003).
The polycomb protein Pc2 is a SUMO E3.
  Cell, 113, 127-137.  
12740389 P.S.Lee, C.Chang, D.Liu, and R.Derynck (2003).
Sumoylation of Smad4, the common Smad mediator of transforming growth factor-beta family signaling.
  J Biol Chem, 278, 27853-27863.  
14517261 P.Y.Wu, M.Hanlon, M.Eddins, C.Tsui, R.S.Rogers, J.P.Jensen, M.J.Matunis, A.M.Weissman, A.M.Weisman, A.M.Weissman, C.Wolberger, C.P.Wolberger, and C.M.Pickart (2003).
A conserved catalytic residue in the ubiquitin-conjugating enzyme family.
  EMBO J, 22, 5241-5250.  
12764129 R.S.Rogers, C.M.Horvath, and M.J.Matunis (2003).
SUMO modification of STAT1 and its role in PIAS-mediated inhibition of gene activation.
  J Biol Chem, 278, 30091-30097.  
12524449 T.J.Siepmann, R.N.Bohnsack, Z.Tokgöz, O.V.Baboshina, and A.L.Haas (2003).
Protein interactions within the N-end rule ubiquitin ligation pathway.
  J Biol Chem, 278, 9448-9457.  
12615929 Y.Hirano, S.Murata, K.Tanaka, M.Shimizu, and R.Sato (2003).
Sterol regulatory element-binding proteins are negatively regulated through SUMO-1 modification independent of the ubiquitin/26 S proteasome pathway.
  J Biol Chem, 278, 16809-16819.  
  12005425 A.P.VanDemark, and C.P.Hill (2002).
SUMO wrestling with specificity.
  Structure, 10, 281-282.  
  12057190 C.D.Lima (2002).
Bridging the gap between SCF and ubiquitin transfer.
  Structure, 10, 741-742.  
12226657 C.Hoege, B.Pfander, G.L.Moldovan, G.Pyrowolakis, and S.Jentsch (2002).
RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO.
  Nature, 419, 135-141.  
12192048 H.Zhang, H.Saitoh, and M.J.Matunis (2002).
Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex.
  Mol Cell Biol, 22, 6498-6508.  
12072434 J.J.Eloranta, and H.C.Hurst (2002).
Transcription factor AP-2 interacts with the SUMO-conjugating enzyme UBC9 and is sumolated in vivo.
  J Biol Chem, 277, 30798-30804.  
12354763 K.P.Bencsath, M.S.Podgorski, V.R.Pagala, C.A.Slaughter, and B.A.Schulman (2002).
Identification of a multifunctional binding site on Ubc9p required for Smt3p conjugation.
  J Biol Chem, 277, 47938-47945.  
11931752 M.Hochstrasser (2002).
New structural clues to substrate specificity in the "ubiquitin system".
  Mol Cell, 9, 453-454.  
12368356 N.Madani, R.Millette, E.J.Platt, M.Marin, S.L.Kozak, D.B.Bloch, and D.Kabat (2002).
Implication of the lymphocyte-specific nuclear body protein Sp140 in an innate response to human immunodeficiency virus type 1.
  J Virol, 76, 11133-11138.  
12393906 Y.Miyauchi, S.Yogosawa, R.Honda, T.Nishida, and H.Yasuda (2002).
Sumoylation of Mdm2 by protein inhibitor of activated STAT (PIAS) and RanBP2 enzymes.
  J Biol Chem, 277, 50131-50136.  
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