Structure of the human FANCL RING-Ube2T complex reveals determinants of cognate E3-E2 selection

Structure

Volumn 22, Issue 2, 2014, Pages 337-344

  Hodson, Charlotte ^a   Purkiss, Andrew ^a   Miles, Jennifer Anne ^a   Walden, Helen ^a,b  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b MRC Protein Phosphorylation Unit   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FANCONI ANEMIA GROUP L PROTEIN; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; COMPLEX FORMATION; HUMAN; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RING FINGER MOTIF; STATIC ELECTRICITY; STRUCTURE ANALYSIS; UBIQUITINATION; FANCONI ANEMIA; PROTEIN INTERACTION; RECOGNITION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; DNA REPAIR; FANCONI ANEMIA COMPLEMENTATION GROUP L PROTEIN; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; XENOPUS LAEVIS;

EID: 84893761159     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.12.004     Document Type: Article

References (40)

1. P.V. Afonine, R.W. Grosse-Kunstleve, and P.D. Adams A robust bulk-solvent correction and anisotropic scaling procedure Acta Crystallogr. D Biol. Crystallogr. 61 2005 850 855
2. A.F. Alpi, P.E. Pace, M.M. Babu, and K.J. Patel Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI Mol. Cell 32 2008 767 777
3. B.P. Alter Fanconi's anemia and malignancies Am. J. Hematol. 53 1996 99 110
4. V. Bailly, J. Lamb, P. Sung, S. Prakash, and L. Prakash Specific complex formation between yeast RAD6 and RAD18 proteins: a potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites Genes Dev. 8 1994 811 820
5. M.L. Bentley, J.E. Corn, K.C. Dong, Q. Phung, T.K. Cheung, and A.G. Cochran Recognition of UbcH5c and the nucleosome by the Bmi1/Ring1b ubiquitin ligase complex EMBO J. 30 2011 3285 3297
6. P.S. Brzovic, and R.E. Klevit Ubiquitin transfer from the E2 perspective: why is UbcH5 so promiscuous? Cell Cycle 5 2006 2867 2873
7. B. Chen, J. Mariano, Y.C. Tsai, A.H. Chan, M. Cohen, and A.M. Weissman The activity of a human endoplasmic reticulum-associated degradation E3, gp78, requires its Cue domain, RING finger, and an E2-binding site Proc. Natl. Acad. Sci. USA 103 2006 341 346
8. A.R. Cole, L.P.C. Lewis, and H. Walden The structure of the catalytic subunit FANCL of the Fanconi anemia core complex Nat. Struct. Mol. Biol. 17 2010 294 298
9. I.W. Davis, L.W. Murray, J.S. Richardson, and D.C. Richardson MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes Nucleic Acids Res. 32 Web Server issue 2004 W615 W619
10. Delano, W.L. (2002). The PyMOL molecular graphics system. http://www.pymol.org/.
11. R.J. Deshaies, and C.A.P. Joazeiro RING domain E3 ubiquitin ligases Annu. Rev. Biochem. 78 2009 399 434
12. H. Dou, L. Buetow, G.J. Sibbet, K. Cameron, and D.T. Huang BIRC7-E2 ubiquitin conjugate structure reveals the mechanism of ubiquitin transfer by a RING dimer Nat. Struct. Mol. Biol. 19 2012 876 883
13. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
14. I. Garcia-Higuera, T. Taniguchi, S. Ganesan, M.S. Meyn, C. Timmers, J. Hejna, M. Grompe, and A.D. D'Andrea Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway Mol. Cell 7 2001 249 262
15. C. Hodson, A.R. Cole, L.P. Lewis, J.A. Miles, A. Purkiss, and H. Walden Structural analysis of human FANCL, the E3 ligase in the Fanconi anemia pathway J. Biol. Chem. 286 2011 32628 32637
16. L. Huang, E. Kinnucan, G.L. Wang, S. Beaudenon, P.M. Howley, J.M. Huibregtse, and N.P. Pavletich Structure of an E6AP-UbcH7 complex: insights into ubiquitination by the E2-E3 enzyme cascade Science 286 1999 1321 1326
17. G. Kar, O. Keskin, R. Nussinov, and A. Gursoy Human proteome-scale structural modeling of E2-E3 interactions exploiting interface motifs J. Proteome Res. 11 2012 1196 1207
18. P. Knipscheer, M. Räschle, A. Smogorzewska, M. Enoiu, T.V. Ho, O.D. Schärer, S.J. Elledge, and J.C. Walter The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair Science 326 2009 1698 1701
19. M.C. Kottemann, and A. Smogorzewska Fanconi anaemia and the repair of Watson and Crick DNA crosslinks Nature 493 2013 356 363
20. Y.J. Machida, Y. Machida, Y. Chen, A.M. Gurtan, G.M. Kupfer, A.D. D'Andrea, and A. Dutta UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation Mol. Cell 23 2006 589 596
21. G. Markson, C. Kiel, R. Hyde, S. Brown, P. Charalabous, A. Bremm, J. Semple, J. Woodsmith, S. Duley, and K. Salehi-Ashtiani et al. Analysis of the human E2 ubiquitin conjugating enzyme protein interaction network Genome Res. 19 2009 1905 1911
22. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
23. A.R. Meetei, J.P. de Winter, A.L. Medhurst, M. Wallisch, Q. Waisfisz, H.J. van de Vrugt, A.B. Oostra, Z. Yan, C. Ling, and C.E. Bishop et al. A novel ubiquitin ligase is deficient in Fanconi anemia Nat. Genet. 35 2003 165 170
24. L. Pellegrini, D.S. Yu, T. Lo, S. Anand, M. Lee, T.L. Blundell, and A.R. Venkitaraman Insights into DNA recombination from the structure of a RAD51-BRCA2 complex Nature 420 2002 287 293
25. J.W. Pflugrath The finer things in X-ray diffraction data collection Acta Crystallogr. D Biol. Crystallogr. 55 1999 1718 1725
26. C.M. Pickart, and M.J. Eddins Ubiquitin: structures, functions, mechanisms Biochim. Biophys. Acta 1695 2004 55 72
27. A. Plechanovová, E.G. Jaffray, M.H. Tatham, J.H. Naismith, and R.T. Hay Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis Nature 489 2012 115 120
28. J.N. Pruneda, P.J. Littlefield, S.E. Soss, K.A. Nordquist, W.J. Chazin, P.S. Brzovic, and R.E. Klevit Structure of an E3:E2∼Ub complex reveals an allosteric mechanism shared among RING/U-box ligases Mol. Cell 47 2012 933 942
29. Y. Sato, A. Yoshikawa, A. Yamagata, H. Mimura, M. Yamashita, K. Ookata, O. Nureki, K. Iwai, M. Komada, and S. Fukai Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains Nature 455 2008 358 362
30. Y. Sheng, J.H. Hong, R. Doherty, T. Srikumar, J. Shloush, G.V. Avvakumov, J.R. Walker, S. Xue, D. Neculai, and J.W. Wan et al. A human ubiquitin conjugating enzyme (E2)-HECT E3 ligase structure-function screen Mol. Cell. Proteomics 11 2012 329 341
31. L.M. Starita, J.N. Pruneda, R.S. Lo, D.M. Fowler, H.J. Kim, J.B. Hiatt, J. Shendure, P.S. Brzovic, S. Fields, and R.E. Klevit Activity-enhancing mutations in an E3 ubiquitin ligase identified by high-throughput mutagenesis Proc. Natl. Acad. Sci. USA 110 2013 E1263 E1272
32. C. Timmers, T. Taniguchi, J. Hejna, C. Reifsteck, L. Lucas, D. Bruun, M. Thayer, B. Cox, S. Olson, and A.D. D'Andrea et al. Positional cloning of a novel Fanconi anemia gene, FANCD2 Mol. Cell 7 2001 241 248
33. F. van den Ent, and J. Löwe RF cloning: a restriction-free method for inserting target genes into plasmids J. Biochem. Biophys. Methods 67 2006 67 74
34. S.J.L. van Wijk, and H.T.M. Timmers The family of ubiquitin-conjugating enzymes (E2s): deciding between life and death of proteins FASEB J. 24 2010 981 993
35. S.J. van Wijk, S.J. de Vries, P. Kemmeren, A. Huang, R. Boelens, A.M. Bonvin, and H.T. Timmers A comprehensive framework of E2-RING E3 interactions of the human ubiquitin-proteasome system Mol. Syst. Biol. 5 2009 295
36. D.M. Wenzel, A. Lissounov, P.S. Brzovic, and R.E. Klevit UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids Nature 474 2011 105 108
37. G.S. Winkler, and H.T. Timmers Structure-based approaches to create new E2-E3 enzyme pairs Methods Enzymol. 399 2005 355 366
38. Y.H. Ye, and M. Rape Building ubiquitin chains: E2 enzymes at work Nat. Rev. Mol. Cell Biol. 10 2009 755 764
39. Q. Yin, S.C. Lin, B. Lamothe, M. Lu, Y.C. Lo, G. Hura, L. Zheng, R.L. Rich, A.D. Campos, and D.G. Myszka et al. E2 interaction and dimerization in the crystal structure of TRAF6 Nat. Struct. Mol. Biol. 16 2009 658 666
40. N. Zheng, P. Wang, P.D. Jeffrey, and N.P. Pavletich Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases Cell 102 2000 533 539