Molecular architecture of the ankyrin SOCS box family of Cul5-dependent E3 ubiquitin ligases

Journal of Molecular Biology

Volumn 425, Issue 17, 2013, Pages 3166-3177

  Muniz, João R C ^a,c   Guo, Kunde ^a   Kershaw, Nadia J ^b   Ayinampudi, Vikram ^a   Von Delft, Frank ^a   Babon, Jeffrey J ^b   Bullock, Alex N ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

degradation; proteasome; protein protein interaction; signaling; ubiquitination

Indexed keywords

ANKYRIN; CULLIN; CULLIN 5; ELONGIN B; ELONGIN C; SUPPRESSOR OF CYTOKINE SIGNALING; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME STRUCTURE; HUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN;

EID: 84881660979     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.06.015     Document Type: Article

References (58)

1. B.A. Schulman, and J.W. Harper Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways Nat Rev Mol Cell Biol 10 2009 319 331
2. A. Hershko, and A. Ciechanover The ubiquitin system Annu Rev Biochem 67 1998 425 479
3. M.D. Petroski, and R.J. Deshaies Function and regulation of cullin-RING ubiquitin ligases Nat Rev Mol Cell Biol 6 2005 9 20
4. E.S. Zimmerman, B.A. Schulman, and N. Zheng Structural assembly of cullin-RING ubiquitin ligase complexes Curr Opin Struct Biol 20 2010 714 721
5. D.M. Duda, L.A. Borg, D.C. Scott, H.W. Hunt, M. Hammel, and B.A. Schulman Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation Cell 134 2008 995 1006
6. A. Saha, and R.J. Deshaies Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation Mol Cell 32 2008 21 31
7. N. Zheng, B.A. Schulman, L. Song, J.J. Miller, P.D. Jeffrey, and P. Wang Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex Nature 416 2002 703 709
8. B.T. Kile, B.A. Schulman, W.S. Alexander, N.A. Nicola, H.M. Martin, and D.J. Hilton The SOCS box: a tale of destruction and degradation Trends Biochem Sci 27 2002 235 241
9. E.M. Linossi, and S.E. Nicholson The SOCS box-adapting proteins for ubiquitination and proteasomal degradation IUBMB Life 64 2012 316 323
10. D.J. Hilton, R.T. Richardson, W.S. Alexander, E.M. Viney, T.A. Willson, and N.S. Sprigg Twenty proteins containing a C-terminal SOCS box form five structural classes Proc Natl Acad Sci USA 95 1998 114 119
11. T. Kamura, S. Sato, D. Haque, L. Liu, W.G. Kaelin Jr., and R.C. Conaway The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families Genes Dev 12 1998 3872 3881
12. T. Kamura, K. Maenaka, S. Kotoshiba, M. Matsumoto, D. Kohda, and R.C. Conaway VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases Genes Dev 18 2004 3055 3065
13. N. Mahrour, W.B. Redwine, L. Florens, S.K. Swanson, S. Martin-Brown, and W.D. Bradford Characterization of Cullin-box sequences that direct recruitment of Cul2-Rbx1 and Cul5-Rbx2 modules to Elongin BC-based ubiquitin ligases J Biol Chem 283 2008 8005 8013
14. M.L. Heuze, F.C. Guibal, C.A. Banks, J.W. Conaway, R.C. Conaway, and Y.E. Cayre ASB2 is an Elongin BC-interacting protein that can assemble with Cullin 5 and Rbx1 to reconstitute an E3 ubiquitin ligase complex J Biol Chem 280 2005 5468 5474
15. J. Kohroki, T. Nishiyama, T. Nakamura, and Y. Masuho ASB proteins interact with Cullin5 and Rbx2 to form E3 ubiquitin ligase complexes FEBS Lett 579 2005 6796 6802
16. J. Wang, A.G. Muntean, and J.L. Hess ECSASB2 mediates MLL degradation during hematopoietic differentiation Blood 119 2012 1151 1161
17. M.L. Heuze, I. Lamsoul, M. Baldassarre, Y. Lad, S. Leveque, and Z. Razinia ASB2 targets filamins A and B to proteasomal degradation Blood 112 2008 5130 5140
18. S. Kwon, D. Kim, J.W. Rhee, J.A. Park, D.W. Kim, and D.S. Kim ASB9 interacts with ubiquitous mitochondrial creatine kinase and inhibits mitochondrial function BMC Biol 8 2010 23
19. M.A. Debrincat, J.G. Zhang, T.A. Willson, J. Silke, L.M. Connolly, and R.J. Simpson Ankyrin repeat and suppressors of cytokine signaling box protein asb-9 targets creatine kinase B for degradation J Biol Chem 282 2007 4728 4737
20. M. Tokuoka, N. Miyoshi, T. Hitora, K. Mimori, F. Tanaka, and K. Shibata Clinical significance of ASB9 in human colorectal cancer Int J Oncol 37 2010 1105 1111
21. A.S. Chung, Y.J. Guan, Z.L. Yuan, J.E. Albina, and Y.E. Chin Ankyrin repeat and SOCS box 3 (ASB3) mediates ubiquitination and degradation of tumor necrosis factor receptor II Mol Cell Biol 25 2005 4716 4726
22. J.Y. Li, B. Chai, W. Zhang, X. Wu, C. Zhang, and D. Fritze Ankyrin repeat and SOCS box containing protein 4 (Asb-4) colocalizes with insulin receptor substrate 4 (IRS4) in the hypothalamic neurons and mediates IRS4 degradation BMC Neurosci 12 2011 95
23. S.H. Diks, M.A. Sartori da Silva, J.L. Hillebrands, R.J. Bink, H.H. Versteeg, and C. van Rooijen d-Asb11 is an essential mediator of canonical Delta-Notch signalling Nat Cell Biol 10 2008 1190 1198
24. M.A. Sartori da Silva, J.M. Tee, J. Paridaen, A. Brouwers, V. Runtuwene, and D. Zivkovic Essential role for the d-Asb11 cul5 Box domain for proper notch signaling and neural cell fate decisions in vivo PLoS One 5 2010 e14023
25. X. Fei, X. Gu, S. Fan, Z. Yang, F. Li, and C. Zhang Crystal structure of Human ASB9-2 and substrate-recognition of CKB Protein J 31 2012 275 284
26. L.K. Mosavi, D.L. Minor Jr., and Z.Y. Peng Consensus-derived structural determinants of the ankyrin repeat motif Proc Natl Acad Sci USA 99 2002 16029 16034
27. S.G. Sedgwick, and S.J. Smerdon The ankyrin repeat: a diversity of interactions on a common structural framework Trends Biochem Sci 24 1999 311 316
28. A.N. Bullock, J.E. Debreczeni, A.M. Edwards, M. Sundstrom, and S. Knapp Crystal structure of the SOCS2-elongin C-elongin B complex defines a prototypical SOCS box ubiquitin ligase Proc Natl Acad Sci USA 103 2006 7637 7642
29. A.N. Bullock, M.C. Rodriguez, J.E. Debreczeni, Z. Songyang, and S. Knapp Structure of the SOCS4-ElonginB/C complex reveals a distinct SOCS box interface and the molecular basis for SOCS-dependent EGFR degradation Structure 15 2007 1493 1504
30. J.S. Woo, J.H. Imm, C.K. Min, K.J. Kim, S.S. Cha, and B.H. Oh Structural and functional insights into the B30.2/SPRY domain EMBO J 25 2006 1353 1363
31. C.E. Stebbins, W.G. Kaelin Jr., and N.P. Pavletich Structure of the VHL-ElonginC-ElonginB complex: implications for VHL tumor suppressor function Science 284 1999 455 461
32. P. Canning, C.D. Cooper, T. Krojer, J.W. Murray, A.C. Pike, and A. Chaikuad Structural basis for Cul3 assembly with the BTB-Kelch family of E3 ubiquitin ligases J Biol Chem 288 2013 7803 7814
33. E.S. Fischer, A. Scrima, K. Bohm, S. Matsumoto, G.M. Lingaraju, and M. Faty The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation Cell 147 2011 1024 1039
34. S. Angers, T. Li, X. Yi, M.J. MacCoss, R.T. Moon, and N. Zheng Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery Nature 443 2006 590 593
35. A.X. Ji, and G.G. Prive Crystal structure of KLHL3 in complex with Cullin3 PLoS One 8 2013 e60445
36. R.A. Abagyan, M. Totrov, and D. Kuznetsov ICM: a new method for protein modeling and design: applications to docking and structure prediction from the distorted native conformation J Comput Chem 15 1994 488 506
37. A. Plechanovova, 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
38. --creatine transition-state analogue complex FEBS Lett 582 2008 3959 3965
39. B. Hao, N. Zheng, B.A. Schulman, G. Wu, J.J. Miller, and M. Pagano Structural basis of the Cks1-dependent recognition of p27(Kip1) by the SCF(Skp2) ubiquitin ligase Mol Cell 20 2005 9 19
40. G. Wu, G. Xu, B.A. Schulman, P.D. Jeffrey, J.W. Harper, and N.P. Pavletich 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 2003 1445 1456
41. J. Jin, T. Cardozo, R.C. Lovering, S.J. Elledge, M. Pagano, and J.W. Harper Systematic analysis and nomenclature of mammalian F-box proteins Genes Dev 18 2004 2573 2580
42. S. Sonnberg, B.T. Seet, T. Pawson, S.B. Fleming, and A.A. Mercer Poxvirus ankyrin repeat proteins are a unique class of F-box proteins that associate with cellular SCF1 ubiquitin ligase complexes Proc Natl Acad Sci USA 105 2008 10955 10960
43. M. Barry, N. van Buuren, K. Burles, K. Mottet, Q. Wang, and A. Teale Poxvirus exploitation of the ubiquitin-proteasome system Viruses 2 2010 2356 2380
44. J. Liu, and R. Nussinov Flexible cullins in cullin-RING E3 ligases allosterically regulate ubiquitination J Biol Chem 286 2011 40934 40942
45. M. Zhuang, M.F. Calabrese, J. Liu, M.B. Waddell, A. Nourse, and M. Hammel Structures of SPOP-substrate complexes: insights into molecular architectures of BTB-Cul3 ubiquitin ligases Mol Cell 36 2009 39 50
46. L. Nie, Y. Zhao, W. Wu, Y.Z. Yang, H.C. Wang, and X.H. Sun Notch-induced Asb2 expression promotes protein ubiquitination by forming non-canonical E3 ligase complexes Cell Res 21 2011 754 769
47. 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
48. J.N. Pruneda, P.J. Littlefield, S.E. Soss, K.A. Nordquist, W.J. Chazin, and P.S. Brzovic Structure of an E3:E2 Ub complex reveals an allosteric mechanism shared among RING/U-box ligases Mol Cell 47 2012 933 942
49. P. Savitsky, J. Bray, C.D. Cooper, B.D. Marsden, P. Mahajan, and N.A. Burgess-Brown High-throughput production of human proteins for crystallization: the SGC experience J Struct Biol 172 2010 3 13
50. T. Li, N.P. Pavletich, B.A. Schulman, and N. Zheng High-level expression and purification of recombinant SCF ubiquitin ligases Methods Enzymol 398 2005 125 142
51. Collaborative Computational Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr Sect D Biol Crystallogr 50 1994 760 763
52. 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 Crystallogr 40 2007 658 674
53. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr Sect D Biol Crystallogr 66 2010 486 501
54. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, and N. Echols PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr Sect D Biol Crystallogr 66 2010 213 221
55. A.G. Leslie The integration of macromolecular diffraction data Acta Crystallogr Sect D Biol Crystallogr 62 2006 48 57
56. T.C. Terwilliger, and J. Berendzen Automated MAD and MIR structure solution Acta Crystallogr Sect D Biol Crystallogr 55 1999 849 861
57. A. Perrakis, R. Morris, and V.S. Lamzin Automated protein model building combined with iterative structure refinement Nat Struct Biol 6 1999 458 463
58. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr Sect D Biol Crystallogr 53 1997 240 255