The structure of the UbcH8-ubiquitin complex shows a unique ubiquitin interaction site

Biochemistry

Volumn 48, Issue 51, 2009, Pages 12169-12179

  Serniwka, Stephanie A ^a   Shaw, Gary S ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC SITES; CHEMICAL SHIFT PERTURBATIONS; CONFORMATIONAL CHANGE; COVALENTLY BOUND; CROSS-SATURATION; DISULFIDE BONDS; E3 ENZYMES; INTERACTION SITE; KEY ENZYMES; LINKER REGION; MOLECULAR DOCKING; NEGATIVE POTENTIAL; NMR SPECTROSCOPY; ROOT-MEAN SQUARE DEVIATION; STABLE COMPLEXES; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITIN MOLECULES; UBIQUITIN-MEDIATED PROTEOLYSIS; UBIQUITINATION;

CATALYSTS; ENZYMES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

COMPLEXATION;

UBCHB ENZYME; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME E2; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DISULFIDE BOND; HUMAN; MOLECULAR DOCKING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; SURFACE PROPERTY; UBIQUITINATION;

BINDING SITES; HUMANS; KINETICS; MOLECULAR CONFORMATION; PROTEIN BINDING; UBIQUITIN C; UBIQUITIN-CONJUGATING ENZYMES;

EID: 73149098116     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901686j     Document Type: Article

References (43)

1. Hershko, A., and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
2. Ciechanover, A., Orian, A., and Schwartz, A. L. (2000) Ubiquitin-mediated proteolysis: Biological regulation via destruction. BioEssays 22, 442-451.
3. Ciechanover, A., and Brundin, P. (2003) The ubiquitin proteasome system in neurodegenerative diseases: Sometimes the chicken, sometimes the egg. Neuron 40, 427-446.
4. Nalepa, G., Rolfe, M., and Harper, J. W. (2006) Drug discovery in the ubiquitin-proteasome system. Nat. Rev. Drug Discovery 5, 596-613.
5. Zhang, Y., Gao, J., Chung, K. K., Huang, H., Dawson, V. L., and Dawson, T. M. (2000) Parkin functions as an E2-dependent ubiquitin-protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc. Natl. Acad. Sci. U.S.A. 97, 13354-13359.
6. Brzovic, P. S., Keeffe, J. R., Nishikawa, H., Miyamoto, K., Fox, D., III, Fukuda, M., Ohta, T., and Klevit, R. (2003) Binding and recognition in the assembly of an active BRCA1/BARD1 ubiquitin-ligase complex. Proc. Natl. Acad. Sci. U.S.A. 100, 5646-5651.
7. Kumar, S., Kao, W. H., and Howley, P. M. (1997) Physical interaction between specific E2 and Hect E3 enzymes determines functional cooperativity. J. Biol. Chem. 272, 13548-13554.
8. Burroughs, A. M., Jaffee, M., Iyer, L. M., and Aravind, L. (2008) Anatomy of the E2 ligase fold: Implications for enzymology and evolution of ubiquitin/Ub-like protein conjugation. J. Struct. Biol. 162, 205-218.
9. Winn, P. J., Religa, T. L., Battey, J. N., Banerjee, A., and Wade, R. C. (2004) Determinants of functionality in the ubiquitin conjugating enzyme family. Structure (Cambridge, MA, U.S.) 12, 1563-1574.
10. Winn, P. J., Zahran, M., Battey, J. N., Zhou, Y., Wade, R. C., and Banerjee, A. (2007) Structural and electrostatic properties of ubiquitination and related pathways. Front. Biosci. 12, 3419-3430.
11. Hamilton, K. S., Ellison, M. J., Barber, K. R., Williams, R. S., Huzil, J. T., McKenna, S., Ptak, C., Glover, M., and Shaw, G. S. (2001) Structure of a conjugating enzyme-ubiquitin thiolester intermediate reveals a novel role for the ubiquitin tail. Structure 9, 897-904.
12. Dev, K. K., van der Putten, H., Sommer, B., and Rovelli, G. (2003) Part I: Parkin-associated proteins and Parkinson's disease. Neuro-pharmacology 45, 1-13.
13. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., and Shimizu, N. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608.
14. Merkley, N., Barber, K. R., and Shaw, G. S. (2005) Ubiquitin manipulation by an E2 conjugating enzyme using a novel covalent intermediate. J. Biol. Chem. 280, 31732-31738.
15. 15N multidimensional NMR to study the structure and dynamics of proteins. Annu. Rev. Biophys. Biomol. Struct. 27, 357-406.
16. Golovanov, A. P., Hautbergue, G. M., Wilson, S. A., and Lian, L. Y. (2004) A simple method for improving protein solubility and long-term stability. J. Am. Chem. Soc. 126, 8933-8939.
17. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665.
18. Grzesiek, S., and Bax, A. (1992) Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114, 6291-6293.
19. Wittekind, M., and Mueller, L. (1993) HNCACB, a high sensitivity 3D NMR experiment to correlate amide proton and nitrogen resonances with the α-carbon and β-carbon resonances in proteins. J. Magn. Reson., Ser. B 101, 171-180.
20. 13C magnetization. J. Magn. Reson., Ser. B 101, 114-119.
21. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
22. Johnson, B. A., and Belvins, R. A. (1994) NMRView: A computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614.
23. Shuker, S. B., Hajduk, P. J., Meadows, R. P., and Fesik, S. W. (1996) Discovering high-affinity ligands for proteins: SAR by NMR. Science 274, 1531-1534.
24. Kupce, E., and Wagner, G. (1995) Wideband homonuclear decoupling in protein spectra. J. Magn. Reson. 109, 329-333.
25. Vijay-Kumar, S., Bugg, C. E., and Cook, W. J. (1987) Structure of ubiquitin refined at 1.8 Å resolution. J. Mol. Biol. 194, 531-544.
26. Hubbard, S. J., and Thornton, J. M. (1993) NACCESS , University College London, London.
27. Vriend, G. (1990) WHAT IF: A molecular modeling and drug design program. J. Mol. Graphics 8, 52-56.
28. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797.
29. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55.
30. DeLano, W. L. (2002) Unraveling hot spots in binding interfaces: Progress and challenges. Curr. Opin. Struct. Biol. 12, 14-20.
31. Brzovic, P. S., Lissounov, A., Christensen, D. E., Hoyt, D. W., and Klevit, R. E. (2006) A UbcH5/ubiquitin noncovalent complex is required for processive BRCA1-directed ubiquitination. Mol. Cell 21, 873-880.
32. Miura, T., Klaus, W., Gsell, B., Miyamoto, C., and Senn, H. (1999) Characterization of the binding interface between ubiquitin and class I human ubiquitin-conjugating enzyme 2b by multidimensional hetero-nuclear NMR spectroscopy in solution. J. Mol. Biol. 290, 213-228.
33. Takahashi, H., Nakanishi, T., Kami, K., Arata, Y., and Shimada, I. (2000) A novel NMR method for determining the interfaces of large protein-protein complexes. Nat. Struct. Biol. 7, 220-223.
34. Dominguez, C., Boelens, R., and Bonvin, A. M. (2003) HADDOCK: A protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125, 1731-1737.
35. Quadt-Akabayov, S. R., Chill, J. H., Levy, R., Kessler, N., and Anglister, J. (2006) Determination of the human type I interferon receptor binding site on human interferon-α2 by cross saturation and an NMR-based model of the complex. Protein Sci. 15, 2656-2668.
36. Dominguez, C., Bonvin, A. M., Winkler, G. S., van Schaik, F. M., Timmers, H. T., and Boelens, R. (2004) Structural model of the UbcH5B/CNOT4 complex revealed by combining NMR, mutagenesis, and docking approaches. Structure (Cambridge, MA, U.S.) 12, 633-644.
37. Eddins, M. J., Carlile, C. M., Gomez, K. M., Pickart, C. M., and Wolberger, C. (2006) Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 13, 915-920.
38. Zhao, C., Beaudenon, S. L., Kelley, M. L., Waddell,M. B., Yuan, W., Schulman, B. A., Huibregtse, J. M., and Krug, R. M. (2004) The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-αβ-induced ubiquitin-like protein. Proc. Natl. Acad. Sci. U.S.A. 101, 7578-7582.
39. Lee, I., and Schindelin, H. (2008) Structural insights into E1-catalyzed ubiquitin activation and transfer to conjugating enzymes. Cell 134, 268-278.
40. Huang, D. T., Hunt, H. W., Zhuang, M., Ohi, M. D., Holton, J. M., and Schulman, B. A. (2007) Basis for a ubiquitin-like protein thioester switch toggling E1-E2 affinity. Nature 445, 394-398.
41. Zheng, N., Wang, P., Jeffrey, P. D., and Pavletich, N. P. (2000) Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 102, 533-539.
42. Huang, A., de Jong, R. N., Wienk, H., Winkler, G. S., Timmers, H. T., and Boelens, R. (2009) E2-c-Cbl recognition is necessary but not sufficient for ubiquitination activity. J. Mol. Biol. 385, 507-519.
43. 13C chemical-shift data. J. Biomol. NMR 4, 171-180.