Atomic structure of the APC/C and its mechanism of protein ubiquitination

Nature

Volumn 522, Issue 7557, 2015, Pages 450-454

  Chang, Leifu ^a   Zhang, Ziguo ^a   Yang, Jing ^a   McLaughlin, Stephen H ^a   Barford, David ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; ANAPHASE PROMOTING COMPLEX SUBUNIT 1; ANAPHASE PROMOTING COMPLEX SUBUNIT 8; EARLY MITOTIC INHIBITOR 1; LYSINE; PROTEIN; RECOMBINANT PROTEIN; UBCH10 PROTEIN; UBE2S PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; UVOMORULIN; ANAPC1 PROTEIN, HUMAN; ANAPC10 PROTEIN, HUMAN; ANAPC11 PROTEIN, HUMAN; ANAPHASE PROMOTING COMPLEX SUBUNIT 10; ANAPHASE PROMOTING COMPLEX SUBUNIT 11; ANAPHASE PROMOTING COMPLEX SUBUNIT 3; APC2 PROTEIN, HUMAN; CADHERIN; CDC23 PROTEIN, HUMAN; CDC27 PROTEIN, HUMAN; CDH1 PROTEIN, HUMAN; CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN; F BOX PROTEIN; FBXO5 PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN SUBUNIT; UBE2C PROTEIN, HUMAN; UBE2S PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME;

CATALYST; CHROMOSOME; CYTOLOGY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; EXPERIMENTAL STUDY; PROTEIN; QUANTITATIVE ANALYSIS;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL CYCLE CHECKPOINT; CRYOELECTRON MICROSCOPY; ENZYME MECHANISM; HUMAN; IN VIVO STUDY; INTERPHASE; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; REACTION ANALYSIS; STATIC ELECTRICITY; STRUCTURE ANALYSIS; UBIQUITINATION; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; METABOLISM; PHOSPHORYLATION; PROTEIN SUBUNIT; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; APC1 SUBUNIT, ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; APC10 SUBUNIT, ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; APC11 SUBUNIT, ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; APC3 SUBUNIT, ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; APC8 SUBUNIT, ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; CADHERINS; CATALYTIC DOMAIN; CELL CYCLE PROTEINS; CRYOELECTRON MICROSCOPY; CYTOSKELETAL PROTEINS; F-BOX PROTEINS; HUMANS; LYSINE; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN SUBUNITS; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 84933038158     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14471     Document Type: Article

References (73)

1. Meyer, H. J. & Rape, M. Processive ubiquitin chain formation by the anaphasepromoting complex. Semin. Cell Dev. Biol. 22, 544-550 (2011).
2. Pines, J. Cubismand the cell cycle: The many faces of the APC/C. Nature Rev. Mol. Cell Biol. 12, 427-438 (2011).
3. Primorac, I. & Musacchio, A. Panta rhei: The APC/C at steady state. J. Cell Biol. 201, 177-189 (2013).
4. 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).
5. Kimata, Y., Baxter, J. E., Fry, A.M. & Yamano, H. A role for the Fizzy/Cdc20 family of proteins in activation of the APC/C distinct from substrate recruitment. Mol. Cell 32, 576-583 (2008).
6. Van Voorhis, V. A. & Morgan, D. O. Activation of the APC/C ubiquitin ligase by enhanced E2 efficiency. Curr. Biol. 24, 1556-1562 (2014).
7. Kelly, A., Wickliffe, K. E., Song, L., Fedrigo, I. & Rape, M. Ubiquitin chain elongation requires E3-dependent tracking of theemerging conjugate. Mol. Cell 56, 232-245 (2014).
8. Kramer, E. R., Scheuringer, N., Podtelejnikov, A. V., Mann, M. & Peters, J. M. Mitotic regulation of the APC activator proteins CDC20 and CDH1. Mol. Biol. Cell 11, 1555-1569 (2000).
9. Rudner, A. D. & Murray, A. W. Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoting complex. J. Cell Biol. 149, 1377-1390 (2000).
10. Jaspersen, S. L.,Charles, J. F. & Morgan, D. O. Inhibitoryphosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol. 9, 227-236 (1999).
11. Zachariae, W., Schwab, M., Nasmyth, K. & Seufert, W. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 282, 1721-1724 (1998).
12. Reimann, J. D. et al. Emi1 is a mitotic regulator that interacts with Cdc20 and inhibits the anaphase promoting complex. Cell 105, 645-655 (2001).
13. Frye, J. J. et al. Electron microscopy structure of human APC/CCDH1-EMI1 reveals multimodal mechanism of E3 ligase shutdown. Nature Struct. Mol. Biol. 20, 827-835 (2013).
14. Wang, W. & Kirschner,M.W. Emi1preferentially inhibitsubiquitin chain elongation by the anaphase-promoting complex. Nature Cell Biol. 15, 797-806 (2013).
15. Wickliffe, K. E., Lorenz, S., Wemmer, D. E., Kuriyan, J. & Rape, M. Themechanismof linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell 144, 769-781 (2011).
16. Williamson, A. et al. Identification of a physiological E2 module for the human anaphase-promoting complex. Proc. Natl Acad. Sci. USA 106, 18213-18218 (2009).
17. Wu, T. et al. UBE2S drives elongation of K11-linked ubiquitin chains by the anaphase-promoting complex. Proc. Natl Acad. Sci. USA 107, 1355-1360 (2010).
18. Sironi, L. et al. Crystal structure of the tetrameric Mad1-Mad2 core complex: implications of a 'safety belt' binding mechanism for the spindle checkpoint. EMBO J. 21, 2496-2506 (2002).
19. Izawa, D. & Pines, J. Mad2 and the APC/C compete for the same site on Cdc20 to ensure proper chromosome segregation. J. Cell Biol. 199, 27-37 (2012).
20. Thornton, B. R. et al. An architectural map of the anaphase-promoting complex. Genes Dev. 20, 449-460 (2006).
21. Matyskiela, M. E. & Morgan, D. O. Analysis of activator-binding sites on the APC/C supports a cooperative substrate-bindingmechanism. Mol.Cell34, 68-80(2009).
22. Izawa,D. & Pines, J.HowAPC/C-Cdc20 changes its substrate specificity inmitosis. Nature Cell Biol. 13, 223-233 (2011).
23. Sikorski, R. S.,Michaud,W. A.& Hieter, P. p62cdc23 of Saccharomyces cerevisiae: A nuclear tetratricopeptide repeat protein with twomutable domains. Mol. Cell. Biol. 13, 1212-1221 (1993).
24. Lukas, C. et al. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature 401, 815-818 (1999).
25. Miller, J. J. et al. Emi1 stably binds and inhibits the anaphase-promoting complex/ cyclosome as a pseudosubstrate inhibitor. Genes Dev. 20, 2410-2420 (2006).
26. Brown, N. G. et al. Mechanism of polyubiquitination by human anaphasepromoting complex: RING repurposing for ubiquitin chain assembly. Mol. Cell 56, 246-260 (2014).
27. Duda, D. M. et al. Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134, 995-1006 (2008).
28. Meyer, H. J. & Rape, M. Enhanced protein degradation by branched ubiquitin chains. Cell 157, 910-921 (2014).
29. Plechanovova, 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).
30. Dou, H., Buetow, L., Sibbet, G. J., Cameron, K. & Huang, D. T. BIRC7-E2 ubiquitin conjugate structure reveals themechanism of ubiquitin transfer by a RING dimer. Nature Struct. Mol. Biol. 19, 876-883 (2012).
31. Ozkan, E., Yu, H. & Deisenhofer, J.Mechanistic insight into the allosteric activation of a ubiquitin-conjugating enzymeby RING-type ubiquitin ligases. Proc. Natl Acad. Sci. USA 102, 18890-18895 (2005).
32. Saha, A., Lewis, S., Kleiger, G., Kuhlman, B. & Deshaies, R. J. Essential role for ubiquitin-ubiquitin-conjugating enzyme interaction in ubiquitin discharge from Cdc34 to substrate. Mol. Cell 42, 75-83 (2011).
33. 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).
34. Dou, H., Buetow, L., Sibbet, G. J., Cameron, K. & Huang, D. T. Essentiality of a non-RING element in priming donor ubiquitin for catalysis by a monomeric E3. Nature Struct. Mol. Biol. 20, 982-986 (2013).
35. 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).
36. Reverter, D. & Lima, C. D. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435, 687-692 (2005).
37. Soss, S. E., Klevit, R. E. & Chazin, W. J. Activation of UbcH5c,Ub is the result of a shift in interdomain motions of the conjugate bound to U-box E3 ligase E4B. Biochemistry 52, 2991-2999 (2013).
38. Williamson, A. et al. Regulation of ubiquitin chain initiation to control the timing of substrate degradation. Mol. Cell 42, 744-757 (2011).
39. He, J. et al. Insights into degron recognition by APC/C coactivators from the structure of an Acm1-Cdh1 complex. Mol. Cell 50, 649-660 (2013).
40. Izawa, D. & Pines, J. The mitotic checkpoint complex binds a second CDC20 to inhibit active APC/C. Nature 517, 631-634 (2015).
41. Zeng, X. et al. Pharmacologic inhibition of the anaphase-promoting complex induces a spindle checkpoint-dependent mitotic arrest in the absence of spindle damage. Cancer Cell 18, 382-395 (2010).
42. Zhang, Z. et al. Recombinant expression, reconstitution and structure of human anaphase-promoting complex (APC/C). Biochem. J. 449, 365-371 (2013).
43. Kraft, C., Vodermaier, H. C., Maurer-Stroh, S., Eisenhaber, F. & Peters, J. M. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/ C substrates. Mol. Cell 18, 543-553 (2005).
44. da Fonseca, P. C. et al. Structures of APC/C(Cdh1) with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 470, 274-278 (2011).
45. Bai, X. C., Fernandez, I. S., McMullan, G. & Scheres, S. H. Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. eLife 2, e00461 (2013).
46. Li, X. et al. Electron counting and beam-induced motion correction enable nearatomic-resolution single-particle cryo-EM. Nature Methods 10, 584-590 (2013).
47. Mindell, J.A. & Grigorieff, N. Accurate determinationof local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
48. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
49. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
50. Scheres, S. H. Semi-automated selection of cryo-EM particles in RELION-1.3. J. Struct. Biol. 189, 114-122 (2015).
51. Scheres, S. H. Beam-induced motion correction for sub-megadalton cryo-EM particles. eLife 3, e03665 (2014).
52. Rosenthal, P. B. & Henderson, R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J.Mol. Biol. 333, 721-745 (2003).
53. Scheres, S. H. & Chen, S. Prevention of overfitting in cryo-EM structure determination. Nature Methods 9, 853-854 (2012).
54. Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11, 63-65 (2014).
55. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
56. Wendt, K. S. et al. Crystal structure of the APC10/DOC1 subunit of the human anaphase-promoting complex. Nature Struct. Biol. 8, 784-788 (2001).
57. Han, D. et al. Crystal structure of the N-terminal domain of anaphase-promoting complex subunit 7. J. Biol. Chem. 284, 15137-15146 (2009).
58. Zhang, Z., Kulkarni, K., Hanrahan, S. J., Thompson, A. J. & Barford, D. The APC/C subunit Cdc16/Cut9 is a contiguous tetratricopeptide repeat superhelix with a homo-dimer interface similar to Cdc27. EMBO J. 29, 3733-3744 (2010).
59. Zhang, Z. et al.Molecular structure of the N-terminal domain of the APC/C subunit Cdc27 reveals a homo-dimeric tetratricopeptide repeat architecture. J. Mol. Biol. 397, 1316-1328 (2010).
60. Zhang, Z. et al. The four canonical tpr subunits of human APC/C form related homo-dimeric structures and stack in parallel to forma TPRsuprahelix. J. Mol.Biol. 425, 4236-4248 (2013).
61. Zheng, N. et al. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416, 703-709 (2002).
62. Roy, A., Kucukural, A. & Zhang, Y. I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols 5, 725-738 (2010).
63. He, J. et al.Thestructure of the26S proteasome subunit Rpn2reveals itsPCrepeat domain as a closed toroid of two concentric alpha-helical rings. Structure 20, 513-521 (2012).
64. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D 67, 355-367 (2011).
65. Fernandez, I. S., Bai, X. C., Murshudov, G., Scheres, S. H. & Ramakrishnan, V. Initiation of translation by cricket paralysis virus IRES requires its translocation in the ribosome. Cell 157, 823-831 (2014).
66. Yang, Z. et al. UCSF Chimera, MODELLER, and IMP: an integrated modeling system. J. Struct. Biol. 179, 269-278 (2012).
67. Collaborative. Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
68. Landau, M. et al. ConSurf 2005: The projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299-W302 (2005).
69. Holm, L., Kaariainen, S., Rosenstrom, P. & Schenkel, A. Searching protein structure databases with DaliLite v.3. Bioinformatics 24, 2780-2781 (2008).
70. Barton, G. J.ALSCRIPT: A tool to formatmultiple sequence alignments. Protein Eng. 6, 37-40 (1993).
71. Hegemann, B. et al. Systematic phosphorylation analysis of humanmitotic protein complexes. Sci. Signal. 4, rs12 (2011).
72. Kraft, C. et al. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22, 6598-6609 (2003).
73. Steen, J. A. et al. Different phosphorylation states of the anaphase promoting complex in response to antimitotic drugs: A quantitative proteomic analysis. Proc. Natl Acad. Sci. USA 105, 6069-6074 (2008).