Adaptor protein self-assembly drives the control of a cullin-RING ubiquitin ligase

Structure

Volumn 20, Issue 7, 2012, Pages 1141-1153

  Errington, Wesley J ^a   Khan, M Qasim ^a   Bueler, Stephanie A ^b   Rubinstein, John L ^a,b   Chakrabartty, Avijit ^a,c   Privé, Gilbert G ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; OLIGOMER; SPECKLE TYPE POZ PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; PRIORITY JOURNAL; UBIQUITINATION;

AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CULLIN PROTEINS; ESCHERICHIA COLI; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PLASMIDS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; UBIQUITIN; UBIQUITINATION;

EID: 84863505152     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.04.009     Document Type: Article

References (63)

1. K.F. Ahmad, C.K. Engel, and G.G. Privé Crystal structure of the BTB domain from PLZF Proc. Natl. Acad. Sci. USA 95 1998 12123 12128 (Pubitemid 28483729)
2. K.F. Ahmad, A. Melnick, S. Lax, D. Bouchard, J. Liu, C.L. Kiang, S. Mayer, S. Takahashi, J.D. Licht, and G.G. Privé Mechanism of SMRT corepressor recruitment by the BCL6 BTB domain Mol. Cell 12 2003 1551 1564 (Pubitemid 38037022)
3. 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 (Pubitemid 44527296)
4. O. Barbash, P. Zamfirova, D.I. Lin, X. Chen, K. Yang, H. Nakagawa, F. Lu, A.K. Rustgi, and J.A. Diehl Mutations in Fbx4 inhibit dimerization of the SCF(Fbx4) ligase and contribute to cyclin D1 overexpression in human cancer Cancer Cell 14 2008 68 78 (Pubitemid 351885497)
5. Y. Bayón, A.G. Trinidad, M.L. de la Puerta, M. Del Carmen Rodríguez, J. Bogetz, A. Rojas, J.M. De Pereda, S. Rahmouni, S. Williams, and S. Matsuzawa KCTD5, a putative substrate adaptor for cullin3 ubiquitin ligases FEBS J. 275 2008 3900 3910 (Pubitemid 351990954)
6. M.F. Berger, M.S. Lawrence, F. Demichelis, Y. Drier, K. Cibulskis, A.Y. Sivachenko, A. Sboner, R. Esgueva, D. Pflueger, and C. Sougnez The genomic complexity of primary human prostate cancer Nature 470 2011 214 220
7. L.M. Boyden, M. Choi, K.A. Choate, C.J. Nelson-Williams, A. Farhi, H.R. Toka, I.R. Tikhonova, R. Bjornson, S.M. Mane, and G. Colussi Mutations in kelch-like 3 and cullin 3 cause hypertension and electrolyte abnormalities Nature 482 2012 98 102
8. A.N. Bullock, J.E. Debreczeni, A.M. Edwards, M. Sundström, 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
9. M.W. Bunce, I.V. Boronenkov, and R.A. Anderson Coordinated activation of the nuclear ubiquitin ligase Cul3-SPOP by the generation of phosphatidylinositol 5-phosphate J. Biol. Chem. 283 2008 8678 8686
10. G. Canettieri, L. Di Marcotullio, A. Greco, S. Coni, L. Antonucci, P. Infante, L. Pietrosanti, E. De Smaele, E. Ferretti, and E. Miele Histone deacetylase and Cullin3-REN(KCTD11) ubiquitin ligase interplay regulates Hedgehog signalling through Gli acetylation Nat. Cell Biol. 12 2010 132 142
11. Q. Cheng, L. Chen, Z. Li, W.S. Lane, and J. Chen ATM activates p53 by regulating MDM2 oligomerization and E3 processivity EMBO J. 28 2009 3857 3867
12. S. Cirak, F. von Deimling, S. Sachdev, W.J. Errington, R. Herrmann, C. Bönnemann, K. Brockmann, S. Hinderlich, T.H. Lindner, and A. Steinbrecher Kelch-like homologue 9 mutation is associated with an early onset autosomal dominant distal myopathy Brain 133 2010 2123 2135
13. S. Correale, L. Pirone, L. Di Marcotullio, E. De Smaele, A. Greco, D. Mazzà, M. Moretti, V. Alterio, L. Vitagliano, and S. Di Gaetano Molecular organization of the cullin E3 ligase adaptor KCTD11 Biochimie 93 2011 715 724
14. E. De Smaele, L. Di Marcotullio, M. Moretti, M. Pelloni, M.A. Occhione, P. Infante, D. Cucchi, A. Greco, L. Pietrosanti, and J. Todorovic Identification and characterization of KCASH2 and KCASH3, 2 novel Cullin3 adaptors suppressing histone deacetylase and Hedgehog activity in medulloblastoma Neoplasia 13 2011 374 385
15. I.S. Dementieva, V. Tereshko, Z.A. McCrossan, E. Solomaha, D. Araki, C. Xu, N. Grigorieff, and S.A. Goldstein Pentameric assembly of potassium channel tetramerization domain-containing protein 5 J. Mol. Biol. 387 2009 175 191
16. R.J. Deshaies, and C.A. Joazeiro RING domain E3 ubiquitin ligases Annu. Rev. Biochem. 78 2009 399 434
17. R.J. Deshaies, E.D. Emberley, and A. Saha Control of cullin-ring ubiquitin ligase activity by nedd8 Subcell. Biochem. 54 2010 41 56
18. 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
19. D.M. Duda, D.C. Scott, M.F. Calabrese, E.S. Zimmerman, N. Zheng, and B.A. Schulman Structural regulation of cullin-RING ubiquitin ligase complexes Curr. Opin. Struct. Biol. 21 2011 257 264
20. M. Furukawa, Y.J. He, C. Borchers, and Y. Xiong Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases Nat. Cell Biol. 5 2003 1001 1007 (Pubitemid 37406914)
21. E. Gallagher, M. Gao, Y.C. Liu, and M. Karin Activation of the E3 ubiquitin ligase Itch through a phosphorylation-induced conformational change Proc. Natl. Acad. Sci. USA 103 2006 1717 1722 (Pubitemid 43228759)
22. R. Geyer, S. Wee, S. Anderson, J. Yates, and D.A. Wolf BTB/POZ domain proteins are putative substrate adaptors for cullin 3 ubiquitin ligases Mol. Cell 12 2003 783 790 (Pubitemid 37222497)
23. B. Hao, S. Oehlmann, M.E. Sowa, J.W. Harper, and N.P. Pavletich Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases Mol. Cell 26 2007 131 143 (Pubitemid 46550934)
24. I. Hernández-Muñoz, A.H. Lund, P. van der Stoop, E. Boutsma, I. Muijrers, E. Verhoeven, D.A. Nusinow, B. Panning, Y. Marahrens, and M. van Lohuizen Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase Proc. Natl. Acad. Sci. USA 102 2005 7635 7640 (Pubitemid 40741023)
25. A. Hershko, and A. Ciechanover The ubiquitin system Annu. Rev. Biochem. 67 1998 425 479 (Pubitemid 28411135)
26. C. Hoege, B. Pfander, G.L. Moldovan, G. Pyrowolakis, and S. Jentsch RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO Nature 419 2002 135 141 (Pubitemid 35025438)
27. D.T. Huang, A. Paydar, M. Zhuang, M.B. Waddell, J.M. Holton, and B.A. Schulman Structural basis for recruitment of Ubc12 by an E2 binding domain in NEDD8's E1 Mol. Cell 17 2005 341 350 (Pubitemid 40193306)
28. D.T. Huang, H.W. Hunt, M. Zhuang, M.D. Ohi, J.M. Holton, and B.A. Schulman Basis for a ubiquitin-like protein thioester switch toggling E1-E2 affinity Nature 445 2007 394 398 (Pubitemid 46160903)
29. Z. Kan, B.S. Jaiswal, J. Stinson, V. Janakiraman, D. Bhatt, H.M. Stern, P. Yue, P.M. Haverty, R. Bourgon, and J. Zheng Diverse somatic mutation patterns and pathway alterations in human cancers Nature 466 2010 869 873
30. A. Kentsis, R.E. Gordon, and K.L. Borden Self-assembly properties of a model RING domain Proc. Natl. Acad. Sci. USA 99 2002 667 672 (Pubitemid 34106569)
31. J.E. Kwon, M. La, K.H. Oh, Y.M. Oh, G.R. Kim, J.H. Seol, S.H. Baek, T. Chiba, K. Tanaka, and O.S. Bang BTB domain-containing speckle-type POZ protein (SPOP) serves as an adaptor of Daxx for ubiquitination by Cul3-based ubiquitin ligase J. Biol. Chem. 281 2006 12664 12672 (Pubitemid 43855356)
32. C. Li, J. Ao, J. Fu, D.F. Lee, J. Xu, D. Lonard, and B.W. O'Malley Tumor-suppressor role for the SPOP ubiquitin ligase in signal-dependent proteolysis of the oncogenic co-activator SRC-3/AIB1 Oncogene 30 2011 4350 4364
33. M. Li, C.L. Brooks, F. Wu-Baer, D. Chen, R. Baer, and W. Gu Mono- versus polyubiquitination: differential control of p53 fate by Mdm2 Science 302 2003 1972 1975 (Pubitemid 37523506)
34. 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 (Pubitemid 41578880)
35. Y. Li, and B. Hao Structural basis of dimerization-dependent ubiquitination by the SCF(Fbx4) ubiquitin ligase J. Biol. Chem. 285 2010 13896 13906
36. A. Liu, B.M. Desai, and D.A. Stoffers Identification of PCIF1, a POZ domain protein that inhibits PDX-1 (MODY4) transcriptional activity Mol. Cell. Biol. 24 2004 4372 4383 (Pubitemid 41071007)
37. M. McMahon, N. Thomas, K. Itoh, M. Yamamoto, and J.D. Hayes Dimerization of substrate adaptors can facilitate cullin-mediated ubiquitylation of proteins by a "tethering" mechanism: a two-site interaction model for the Nrf2-Keap1 complex J. Biol. Chem. 281 2006 24756 24768 (Pubitemid 44274250)
38. A.V. Mynott, S.J. Harrop, L.J. Brown, S.N. Breit, B. Kobe, and P.M. Curmi Crystal structure of importin-α bound to a peptide bearing the nuclear localisation signal from chloride intracellular channel protein 4 FEBS J. 278 2011 1662 1675
39. P. Nash, X. Tang, S. Orlicky, Q. Chen, F.B. Gertler, M.D. Mendenhall, F. Sicheri, T. Pawson, and M. Tyers Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication Nature 414 2001 514 521 (Pubitemid 33131529)
40. Y.C. Park, V. Burkitt, A.R. Villa, L. Tong, and H. Wu Structural basis for self-association and receptor recognition of human TRAF2 Nature 398 1999 533 538
41. P. Peschard, G. Kozlov, T. Lin, I.A. Mirza, A.M. Berghuis, S. Lipkowitz, M. Park, and K. Gehring Structural basis for ubiquitin-mediated dimerization and activation of the ubiquitin protein ligase Cbl-b Mol. Cell 27 2007 474 485 (Pubitemid 47126940)
42. M.D. Petroski, and R.J. Deshaies Function and regulation of cullin-RING ubiquitin ligases Nat. Rev. Mol. Cell Biol. 6 2005 9 20 (Pubitemid 40064895)
43. C.M. Pickart Mechanisms underlying ubiquitination Annu. Rev. Biochem. 70 2001 503 533 (Pubitemid 32663902)
44. N.W. Pierce, G. Kleiger, S.O. Shan, and R.J. Deshaies Detection of sequential polyubiquitylation on a millisecond timescale Nature 462 2009 615 619
45. L. Pintard, J.H. Willis, A. Willems, J.L. Johnson, M. Srayko, T. Kurz, S. Glaser, P.E. Mains, M. Tyers, B. Bowerman, and M. Peter The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin ligase Nature 425 2003 311 316 (Pubitemid 37158408)
46. L. Pintard, A. Willems, and M. Peter Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family EMBO J. 23 2004 1681 1687 (Pubitemid 38649631)
47. M.V. Poyurovsky, C. Priest, A. Kentsis, K.L. Borden, Z.Q. Pan, N. Pavletich, and C. Prives The Mdm2 RING domain C-terminus is required for supramolecular assembly and ubiquitin ligase activity EMBO J. 26 2007 90 101 (Pubitemid 46094702)
48. A. Roy, A. Kucukural, and Y. Zhang I-TASSER: a unified platform for automated protein structure and function prediction Nat. Protoc. 5 2010 725 738
49. E. Sakata, T. Satoh, S. Yamamoto, Y. Yamaguchi, M. Yagi-Utsumi, E. Kurimoto, K. Tanaka, S. Wakatsuki, and K. Kato Crystal structure of UbcH5b∼ubiquitin intermediate: insight into the formation of the self-assembled E2∼Ub conjugates Structure 18 2010 138 147
50. D.F. Sobieszczuk, A. Poliakov, Q. Xu, and D.G. Wilkinson A feedback loop mediated by degradation of an inhibitor is required to initiate neuronal differentiation Genes Dev. 24 2010 206 218
51. J. Söding, A. Biegert, and A.N. Lupas The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 33 Web Server issue 2005 W244-8
52. P.J. Stogios, and G.G. Privé The BACK domain in BTB-kelch proteins Trends Biochem. Sci. 29 2004 634 637 (Pubitemid 39491260)
53. P.J. Stogios, G.S. Downs, J.J. Jauhal, S.K. Nandra, and G.G. Privé Sequence and structural analysis of BTB domain proteins Genome Biol. 6 2005 R82
54. P.J. Stogios, J.A. Cuesta-Seijo, L. Chen, N.C. Pomroy, and G.G. Privé Insights into strand exchange in BTB domain dimers from the crystal structures of FAZF and Miz1 J. Mol. Biol. 400 2010 983 997
55. X. Tang, S. Orlicky, Z. Lin, A. Willems, D. Neculai, D. Ceccarelli, F. Mercurio, B.H. Shilton, F. Sicheri, and M. Tyers Suprafacial orientation of the SCFCdc4 dimer accommodates multiple geometries for substrate ubiquitination Cell 129 2007 1165 1176 (Pubitemid 46891040)
56. X. Tang, S. Orlicky, T. Mittag, V. Csizmok, T. Pawson, J.D. Forman-Kay, F. Sicheri, and M. Tyers Composite low affinity interactions dictate recognition of the cyclin-dependent kinase inhibitor Sic1 by the SCFCdc4 ubiquitin ligase Proc. Natl. Acad. Sci. USA 109 2012 3287 3292
57. C. Wang, Y. Pan, and B. Wang Suppressor of fused and Spop regulate the stability, processing and function of Gli2 and Gli3 full-length activators but not their repressors Development 137 2010 2001 2009
58. L. Xu, Y. Wei, J. Reboul, P. Vaglio, T.H. Shin, M. Vidal, S.J. Elledge, and J.W. Harper BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3 Nature 425 2003 316 321 (Pubitemid 37158409)
59. Q. Yan, T. Kamura, Y. Cai, J. Jin, M. Ivan, A. Mushegian, R.C. Conaway, and J.W. Conaway Identification of Elongin C and Skp1 sequences that determine Cullin selection J. Biol. Chem. 279 2004 43019 43026 (Pubitemid 39372196)
60. Q. Zhang, Q. Shi, Y. Chen, T. Yue, S. Li, B. Wang, and J. Jiang Multiple Ser/Thr-rich degrons mediate the degradation of Ci/Gli by the Cul3-HIB/SPOP E3 ubiquitin ligase Proc. Natl. Acad. Sci. USA 106 2009 21191 21196
61. 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
62. N. Zheng, B.A. Schulman, L. Song, J.J. Miller, P.D. Jeffrey, P. Wang, C. Chu, D.M. Koepp, S.J. Elledge, and M. Pagano Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex Nature 416 2002 703 709 (Pubitemid 34429140)
63. M. Zhuang, M.F. Calabrese, J. Liu, M.B. Waddell, A. Nourse, M. Hammel, D.J. Miller, H. Walden, D.M. Duda, and S.N. Seyedin Structures of SPOP substrate complexes: insights into molecular architectures of BTB-Cul3 ubiquitin ligases Mol. Cell 36 2009 39 50