Structural basis for SUMO-E2 interaction revealed by a complex model using docking approach in combination with NMR data

Proteins: Structure, Function and Genetics

Volumn 61, Issue 4, 2005, Pages 1050-1058

  Ding, Husheng ^a   Yang, Yuedong ^a   Zhang, Jiahai ^a   Wu, Jihui ^a   Liu, Haiyan ^a,b   Shi, Yunyu ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

AIRs; Binding interface; Chemical shift perturbation; Compatibility; Electrostatic potential; Flexibility; HADDOCK; Hydrogen bonds; Interaction mode; Transient complex

Indexed keywords

PROTEIN UBC9; SUMO PROTEIN;

ARTICLE; BINDING SITE; ENERGY; HUMAN; HYDROGEN BOND; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION;

BINDING SITES; CALORIMETRY; ELECTROSTATICS; KINETICS; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; THERMODYNAMICS; UBIQUITIN-CONJUGATING ENZYMES;

EID: 28644450786     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20695     Document Type: Article

References (56)

1. Johnson ES. Protein modification by SUMO. Annu Rev Biochem 2004;73:355-382.
2. Seeler JS, Dejean A. Nuclear and unclear functions of SUMO. Nat Rev Mol Cell Biol 2003;4:690-699.
3. Muller S, Hoege C, Pyrowolakis G, Jentsch S. SUMO, ubiquitin's mysterious cousin. Nat Rev Mol Cell Biol 2001;2:202-210.
4. Kwek SS, Derry J, Tyner AL, Shen Z, Gudkov AV. Functional analysis and intracellular localization of p53 modified by SUMO-1. Oncogene 2001;20:2587-2599.
5. Muller S, Berger M, Lehembre F, Seeler JS, Haupt Y, Dejean A. c-Jun and p53 activity is modulated by SUMO-1 modification. J Biol Chem 2000;275:13321-13329.
6. Desterro JM, Rodriguez MS, Hay RT. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 1998;2:233-239.
7. Seeler JS, Marchio A, Losson R, Desterro JM, Hay RT, Chambon P, Dejean A. Common properties of nuclear body protein SP100 and TIF1alpha chromatin factor: role of SUMO modification. Mol Cell Biol 2001;21:3314-3324.
8. Zhong S, Muller S, Ronchetti S, Freemont PS, Dejean A, Pandolfi PP. Role of SUMO-1-modified PML in nuclear body formation. Blood 2000;95:2748-2752.
9. Joseph J, Tan SH, Karpova TS, McNally JG, Dasso M. SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J Cell Biol 2002;156:595-602.
10. Mao Y, Sun M, Desai SD, Liu LF. SUMO-1 conjugation to topoisomerase I: A possible repair response to topoisomerase-mediated DNA damage. Proc Natl Acad Sci USA 2000;97:4046-4051.
11. Azuma Y, Arnaoutov A, Dasso M. SUMO-2/3 regulates topoisomerase II in mitosis. J Cell Biol 2003;163:477-487.
12. Gill G. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev 2004;18:2046-2059.
13. Chen Y. Molecular mechanism of sumoylation. In: Wilson V, editior. Sumoylation: molecular biology and biochemistry. Texas: Horizon Scientific Press; 2004. p 89-112
14. Su HL, Li SS. Molecular features of human ubiquitin-like SUMO genes and their encoded proteins. Gene 2002;296:65-73.
15. Bohren KM, Nadkarni V, Song JH, Gabbay KH, Owerbach D. A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J Biol Chem 2004;279:27233-27238.
16. Saitoh H, Hinchey J. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 2000;275:6252-6258.
17. Zhou W, Ryan JJ, Zhou H. Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J Biol Chem 2004;279:32262-32268.
18. Wormald S, Hilton DJ. Inhibitors of cytokine signal transduction. J Biol Chem 2004;279:821-824.
19. Gill G. Post-translational modification by the small ubiquitin-related modifier SUMO has big effects on transcription factor activity. Curr Opin Genet Dev 2003;13:108-113.
20. Muller S, Ledl A, Schmidt D. SUMO: a regulator of gene expression and genome integrity. Oncogene 2004;23:1998-2008.
21. Swaminathan S, Kiendl F, Korner R, Lupetti R, Hengst L, Melchior F. RanGAP1*SUMO1 is phosphorylated at the onset of mitosis and remains associated with RanBP2 upon NPC disassembly. J Cell Biol 2004;164:965-971.
22. Regad T, Chelbi-Alix MK. Role and fate of PML nuclear bodies in response to interferon and viral infections. Oncogene 2001;20:7274-7286.
23. Melchior F, Schergaut M, Pichler A. SUMO: ligases, isopeptidases and nuclear pores. Trends Biochem Sci 2003;28:612-618.
24. Tatham MH, Jaffray E, Vaughan OA, Desterro JM, Botting CH, Naismith JH, Hay RT. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J Biol Chem 2001;276:35368-35374.
25. Fu C, Ahmed K, Ding H, Ding X, Lan J, Yang Z, Miao Y, Zhu Y, Shi Y, Zhu J, Huang H, Yao X. Stabilization of PML nuclear localization by conjugation and oligomerization of SUMO-3. Oncogene 2005;24:5401-5413.
26. Bayer P, Arndt A, Metzger S, Mahajan R, Melchior F, Jaenicke R, Becker J. Structure determination of the small ubiquitin-related modifier SUMO-1. J Mol Biol 1998;280:275-286.
27. Jin C, Shiyanova T, Shen Z, Liao X. Heteronuclear nuclear magnetic resonance assignments, structure and dynamics of SUMO-1, a human ubiquitin-like protein. Int J Biol Macromol 2001;28:227-234.
28. Huang WC, Ko TP, Li SS, Wang AH. Crystal structures of the human SUMO-2 protein at 1.6 A and 1.2 A resolution: implication on the functional differences of SUMO proteins. Eur J Biochem 2004;271:4114-4122.
29. Ding H, Xu Y, Chen Q, Dai H, Tang Y, Wu J, Shi Y. Solution structure of human SUMO-3 C47S and its binding surface for Ubc9. Biochemistry 2005;44:2790-2799.
30. Sheng W, Liao X. Solution structure of a yeast ubiquitin-like protein Smt3: the role of structurally less defined sequences in protein-protein recognitions. Protein Sci 2002;11:1482-1491.
31. Tong H, Hateboer G, Perrakis A, Bernards R, Sixma TK. Crystal structure of murine/human Ubc9 provides insight into the variability of the ubiquitin-conjugating system. J Biol Chem 1997;272:21381-21387.
32. Giraud MF, Desterro JM, Naismith JH. Structure of ubiquitin-conjugating enzyme 9 displays significant differences with other ubiquitin-conjugating enzymes which may reflect its specificity for sumo rather than ubiquitin. Acta Crystallogr D Biol Crystallogr 1998;54:891-898.
33. Bencsath KP, Podgorski MS, Pagala VE, Slaughter CA, Schulman BA. Identification of a multifunctional binding site on Ubc9p required for Smt3p conjugation. J Biol Chem 2002;277:47938-47945.
34. Lin D, Tatham MH, Yu B, Kim S, Hay RT, Chen Y. Identification of a substrate recognition site on Ubc9. J Biol Chem 2002;277:21740-21748.
35. Tatham MH, Chen Y, Hay RT. Role of two residues proximal to the active site of Ubc9 in substrate recognition by the Ubc9. SUMO-1 thiolester complex. Biochemistry 2003;42:3168-3179.
36. Lois LM, Lima CD. Structures of the SUMO El provide mechanistic insights into SUMO activation and E2 recruitment to E1. Embo J2005;24:439-451.
37. Macauley MS, Errington WJ, Okon M, Scharpf M, Mackereth CD, Schulman BA, McIntosh LP. Structural and dynamic independence of isopeptide-linked RanGAP1 and SUMO-1. J Biol Chem 2004;279:49131-49137.
38. Bernier-Villamor V, Sampson DA, Matunis MJ, Lima CD. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin- conjugating enzyme Ubc9 and Ran-GAP1. Cell 2002;108:345-356.
39. Halperin I, Ma B, Wolfson H, Nussinov R. Principles of docking: An overview of search algorithms and a guide to scoring functions. Proteins 2002;47:409-443.
40. van Dijk AD, Boelens R, Bonvin AM. Data-driven docking for the study of biomolecular complexes. Febs J 2005;272:293-312.
41. Dominguez C, Boelens R, Bonvin AM. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 2003;125:1731-1737.
42. Tatham MH, Kim S, Yu B, Jaffray E, Song J, Zheng J, Rodriguez MS, Hay RT, Chen Y. Role of an N-terminal site of Ubc9 in SUMO-1, -2, and -3 binding and conjugation. Biochemistry 2003;42:9959-9969.
43. Hubbard, SJ, and Thornton, JM. NACCESS. London: University College London; 1993
44. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54:905-921.
45. Linge JP, Williams MA, Spronk CA, Bonvin AM, Nilges M. Refinement of protein structures in explicit solvent. Proteins 2003;50:496-506.
46. Jorgensen WL, Tirado-Rives J. The OPLS potential function for proteins. Energy minimizations for crystals of cyclic peptides and crambin. J Am Chem Soc 1988;110:1657-1666.
47. Daura, X, Gademann, K, Jaun, B, Seebach, D, van Gunsteren, WF, Mark, AE. Peptide folding: When simulation meets experiment. Angew Chem Int Ed 1999;38:236-240
48. McDonald IK, Thornton JM. Satisfying hydrogen bonding potential in proteins. J Mol Biol 1994;238:777-793.
49. Lo Conte L, Chothia C, Janin J. The atomic structure of protein-protein recognition sites. J Mol Biol 1999;285:2177-2198
50. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 1996;8:477-486.
51. Kraulis PJ. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Cryst 1991;24:946-950.
52. Merritt EA, Bacon DJ. Raster3D - photorealistic molecular graphics. Methods Enzymol 1997;277:505-524.
53. Koradi R, Billeter M, Wuthrich, K. Molmol: a program for display and analysis of macromolecular structure. J Mol Graph 1996;14:51-55.
54. Liu Q, Jin C, Liao X, Shen Z, Chen DJ, Chen Y. The binding interface between an E2 (UBC9) and a ubiquitin homologue (UBL1). J Biol Chem 1999;274:16979-16987.
55. Liu Q, Yuan YC, Shen B, Chen DJ, Chen Y. Conformational flexibility of a ubiquitin conjugation enzyme (E2). Biochemistry 1999;38:1415-1425.
56. Burgen AS, Roberts GC, Feeney J. Binding of flexible ligands to macromolecules. Nature 1975;253:753-755.