Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway

Nature Structural and Molecular Biology

Volumn 13, Issue 6, 2006, Pages 491-499

  Yunus, Ali A ^a   Lima, Christopher D ^a  

^a NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE; MUTANT PROTEIN; NUP358 PROTEIN; PROTEIN; PROTEIN P53; PROTEIN UBC9; RANBP2 PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CATALYSIS; CHEMICAL ANALYSIS; CONJUGATION; GENETIC COMPLEMENTATION; KINETICS; MUTATION; PREDICTION; PRIORITY JOURNAL; STRUCTURE ANALYSIS; WILD TYPE; X RAY ANALYSIS;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; KINETICS; LYSINE; MUTAGENESIS; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; SUMO-1 PROTEIN; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES;

EID: 33744911377     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1104     Document Type: Article

References (45)

1. Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (1998).
2. Johnson, E.S. Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382 (2004).
3. Melchior, F. SUMO-nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16, 591-626 (2000).
4. Hochstrasser, M. Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30, 405-439 (1996).
5. Laney, J.D. & Hochstrasser, M. Substrate targeting in the ubiquitin system. Cell 97, 427-430 (1999).
6. Muller, S., Hoege, C., Pyrowolakis, G. & Jentsch, S. SUMO, ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell Biol. 2, 202-210 (2001).
7. Melchior, F., Schergaut, M. & Pichler, A. SUMO: ligases, isopeptidases and nuclear pores. Trends Biochem. Sci. 28, 612-618 (2003).
8. Bernier-Villamor, V., Sampson, D.A., Matunis, M.J. & Lima, C.D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345-356 (2002).
9. Lin, D. et al. Identification of a substrate recognition site on Ubc9. J. Biol. Chem. 277, 21740-21748 (2002).
10. Pichler, A. et al. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 12, 264-269 (2005).
11. Johnson, E.S. & Gupta, A.A. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106, 735-744 (2001).
12. Takahashi, Y., Toh-e, A. & Kikuchi, Y. A novel factor required for the SUM01/Smt3 conjugation of yeast septins. Gene 275, 223-231 (2001).
13. Kahyo, T., Nishida, T. & Yasuda, H. Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell 8, 713-718 (2001).
14. Reverter, D. & Lima, C.D. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435, 687-692 (2005).
15. Pichler, A., Gast, A., Seeler, J.S., Dejean, A. & Melchior, F. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108, 109-120 (2002).
16. Pichler, A., Knipscheer, P., Saitoh, H., Sixma, T.K. & Melchior, F. The RanBP2 SUMO E3 ligase is neither HECT- nor RING-type. Nat. Struct. Mol. Biol. 11, 984-991 (2004).
17. Kagey, M.H., Melhuish, TA. & Wotton, D. The polycomb protein Pc2 is a SUMO E3. Cell 113, 127-137 (2003).
18. Tatham, M.H., 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 42, 3168-3179 (2003).
19. Yunus, A. & Lima, C. Purification and activity assays for Ubc9, the ubiquitin-conjugating enzyme for the small ubiquitin-like modifier SUMO. Methods Enzymol. 398, 74-87 (2005).
20. Fabrega, C., Shen, V., Shuman, S. & Lima, C. D. Structure of an mRNA capping enzyme bound to the phosphorylated carboxy-terminal domain of RNA polymerase II. Mol. Cell 11, 1549-1561 (2003).
21. Seufert, W., Futcher, B. & Jentsch, S. Role of a ubiquitin- conjugating enzyme in degradation of S- and M-phase cyclins. Nature 373, 78-81 (1995).
22. Wu, P.Y. et al. A conserved catalytic residue in the ubiquitin- conjugating enzyme family. EMBO J. 22, 5241-5250 (2003).
23. Alexov, E.G. & Gunner, M.R. Incorporating protein conformational flexibility into the calculation of pH-dependent protein properties. Biophys. J. 72, 2075-2093 (1997).
24. Alexov, E.G. & Gunner, M.R. Calculated protein and proton motions coupled to electron transfer: electron transfer from QA- to QB in bacterial photosynthetic reaction centers. Biochemistry 38, 8253-8270 (1999).
25. Fersht, A. The pH dependence of enzyme catalysis. in Structure and Mechanism in Protein Science 169-189 (W.H. Freeman and Company, New York, 2000).
26. Tolbert, B.S. et al. The active site cysteine of ubiquitin-conjugating enzymes has a significantly elevated pKa: functional implications. Biochemistry 44, 16385-16391 (2005).
27. Sarcevic, B., Mawson, A., Baker, R.T. & Sutherland, R.L. Regulation of the ubiquitin-conjugating enzyme hHR6A by CDK-mediated phosphorylation. EMBO J. 21, 2009-2018 (2002).
28. VanDemark, A.P., Hofmann, R.M., Tsui, C., Pickart, C.M. & Wolberger, C. Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell 105, 711-720 (2001).
29. Zheng, N., Wang, P., Jeffrey, P.D. & Pavletich, N.P. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 102, 533-539 (2000).
30. Schulman, B.A. et al. Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408, 381-386 (2000).
31. Stebbins, C.E., Kaelin, W.G., Jr. & Pavletich, N.P. Structure of the VHL-ElonginC-ElonginB complex: implications for VHL tumor suppressor function. Science 284, 455-461 (1999).
32. Wu, G. et al. Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase. Mol. Cell 11, 1445-1456 (2003).
33. Zheng, N. et al. Structure of the Cul1-Rbx1-Skp1-F box Skp2 SCF ubiquitin ligase complex. Nature 416, 703-709 (2002).
34. Orlicky, S., Tang, X., Willems, A., Tyers, M. & Sicheri, F. Structural basis for phosphodependent substrate selection and orientation by the SCF-Cdc4 ubiquitin ligase. Cell 112, 243-256 (2003).
35. Lois, L.M. & Lima, C.D. Structures of the SUMO El provide mechanistic insights into SUMO activation and E2 recruitment to El. EMBO J. 24, 439-451 (2005).
36. Mossessova, E. & Lima, C.D. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5, 865-876 (2000).
37. Lois, L.M., Lima, C.D. & Chua, N.H. Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. Plant Cell 15, 1347-1359 (2003).
38. Sampson, D.A., Wang, M. & 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, 21664-21669 (2001).
39. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
40. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
41. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-9 (1991).
42. Brunger, AT. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
43. Strickland, S., Palmer, G. & Massey, V. Determination of dissociation constants and specific rate constants of enzyme-substrate (or protein-ligand) interactions from rapid reaction kinetic data. J. Biol. Chem. 250, 4048-4052 (1975).
44. DeLano, W.L. The PyMOL molecular graphics system. (DeLano Scientific, San Carlos, California, USA, 2002).
45. Nicholls, A., Sharp, K.A. & Honig, B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296 (1991).