Structural basis for the RING-catalyzed synthesis of K63-linked ubiquitin chains

Nature Structural and Molecular Biology

Volumn 22, Issue 8, 2015, Pages 597-602

  Branigan, Emma ^a   Plechanovová, Anna ^a   Jaffray, Ellis G ^a   Naismith, James H ^b,c   Hay, Ronald T ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; RNF4 PROTEIN; UBE2V2 PROTEIN; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME 13; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; LIGASE; LYSINE; MULTIPROTEIN COMPLEX; NUCLEAR PROTEIN; POLYUBIQUITIN; PROTEIN BINDING; RECOMBINANT PROTEIN; RNF4 PROTEIN, RAT; TRANSCRIPTION FACTOR; UBE2N PROTEIN, HUMAN; UBE2V2 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME;

ARTICLE; BIOCHEMICAL ANALYSIS; CATALYSIS; CONJUGATE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME IMMOBILIZATION; ENZYME SUBSTRATE; HUMAN; HYDROGEN BOND; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RAT; RING FINGER MOTIF; SITE DIRECTED MUTAGENESIS; UBIQUITINATION; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR MODEL; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

RATTUS;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; LIGASES; LYSINE; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTATION; NUCLEAR PROTEINS; POLYUBIQUITIN; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 84938749159     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3052     Document Type: Article

References (40)

1. Metzger, M. B., Pruneda, J. N., Klevit, R. E. & Weissman, A. M. RING-type E3 ligases: master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochim. Biophys. Acta 1843, 47-60 (2014).
2. Scheffner, M. & Kumar, S. Mammalian HECT ubiquitin-protein ligases: biological and pathophysiological aspects. Biochim. Biophys. Acta 1843, 61-74 (2014).
3. Dou, H., Buetow, L., Sibbet, G. J., Cameron, K. & Huang, D. T. BIRC7-E2 ubiquitin conjugate structure reveals the mechanism of ubiquitin transfer by a RING dimer. Nat. Struct. Mol. Biol. 19, 876-883 (2012).
4. Plechanovová, A., Jaffray, E. G., Tatham, M. H., Naismith, J. H. & Hay, R. T. Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis. Nature 489, 115-120 (2012).
5. Pruneda, J. N. et al. Structure of an E3:E2~Ub complex reveals an allosteric mechanism shared among RING/U-box ligases. Mol. Cell 47, 933-942 (2012).
6. Berndsen, C. E. & Wolberger, C. New insights into ubiquitin E3 ligase mechanism. Nat. Struct. Mol. Biol. 21, 301-307 (2014).
7. Tatham, M. H. et al. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538-546 (2008).
8. Galanty, Y., Belotserkovskaya, R., Coates, J. & Jackson, S. P. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26, 1179-1195 (2012).
9. Guzzo, C. M. et al. RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci. Signal. 5, ra88 (2012).
10. Vyas, R. et al. RNF4 is required for DNA double-strand break repair in vivo. Cell Death Differ. 20, 490-502 (2013).
11. Yin, Y. et al. SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 26, 1196-1208 (2012).
12. Rojas-Fernandez, A. et al. SUMO chain-induced dimerization activates RNF4. Mol. Cell 53, 880-892 (2014).
13. Hofmann, R. M. & Pickart, C. M. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96, 645-653 (1999).
14. Eddins, M. J., Carlile, C. M., Gomez, K. M., Pickart, C. M. & Wolberger, C. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 13, 915-920 (2006).
15. Tatham, M. H., Plechanovova, A., Jaffray, E. G., Salmen, H. & Hay, R. T. Ube2W conjugates ubiquitin to alpha-amino groups of protein N-termini. Biochem. J. 453, 137-145 (2013).
16. Lewis, M. J., Saltibus, L. F., Hau, D. D., Xiao, W. & Spyracopoulos, L. Structural basis for non-covalent interaction between ubiquitin and the ubiquitin conjugating enzyme variant human MMS2. J. Biomol. NMR 34, 89-100 (2006).
17. McKenna, S. et al. Energetics and specificity of interactions within Ub. Uev. Ubc13 human ubiquitin conjugation complexes. Biochemistry 42, 7922-7930 (2003).
18. McKenna, S. et al. Noncovalent interaction between ubiquitin and the human DNA repair protein Mms2 is required for Ubc13-mediated polyubiquitination. J. Biol. Chem. 276, 40120-40126 (2001).
19. Moraes, T. F. et al. Crystal structure of the human ubiquitin conjugating enzyme complex, hMms2-hUbc13. Nat. Struct. Biol. 8, 669-673 (2001).
20. Spyracopoulos, L., Lewis, M. J. & Saltibus, L. F. Main chain and side chain dynamics of the ubiquitin conjugating enzyme variant human Mms2 in the free and ubiquitin-bound states. Biochemistry 44, 8770-8781 (2005).
21. 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).
22. Zhang, M. et al. Chaperoned ubiquitylation: crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol. Cell 20, 525-538 (2005).
23. Reverter, D. & Lima, C. D. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435, 687-692 (2005).
24. Scott, D. C. et al. Structure of a RING E3 trapped in action reveals ligation mechanism for the ubiquitin-like protein NEDD8. Cell 157, 1671-1684 (2014).
25. Yunus, A. A. & Lima, C. D. Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway. Nat. Struct. Mol. Biol. 13, 491-499 (2006).
26. Berndsen, C. E., Wiener, R., Yu, I. W., Ringel, A. E. & Wolberger, C. A conserved asparagine has a structural role in ubiquitin-conjugating enzymes. Nat. Chem. Biol. 9, 154-156 (2013).
27. Wu, P. Y. et al. A conserved catalytic residue in the ubiquitin-conjugating enzyme family. EMBO J. 22, 5241-5250 (2003).
28. Chang, L., Zhang, Z., Yang, J., McLaughlin, S. H. & Barford, D. Molecular architecture and mechanism of the anaphase-promoting complex. Nature 513, 388-393 (2014).
29. Plechanovová, A. et al. Mechanism of ubiquitylation by dimeric RING ligase RNF4. Nat. Struct. Mol. Biol. 18, 1052-1059 (2011).
30. Collaborative Computational Project, No. 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
31. Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82 (2006).
32. Evans, P. R. in Proc. CCP4 Study Weekend (eds. Wilson, K. S., Davies, G., Ashton, A. W. & Bailey, S. ) (CCLRC Daresbury Laboratory, 1997).
33. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
34. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
35. Winter, G. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43, 186-190 (2010).
36. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
37. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
38. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
39. Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (2007).
40. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).