Specificity of the anaphase-promoting complex: A single-molecule study

Science

Volumn 348, Issue 6231, 2015, Pages

  Lu, Ying ^a   Wang, Weiping ^a   Kirschner, Marc W ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; APC PROTEIN; CYCLIN A; CYCLIN B; GEMININ; SECURIN; UBIQUITIN; FLUORESCENT DYE; PROTEIN BINDING; SURVIVAL MOTOR NEURON PROTEIN;

BIOASSAY; CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; FLUORESCENCE; MOLECULAR ANALYSIS; REACTION KINETICS;

ARTICLE; BINDING AFFINITY; CHEMICAL REACTION; CONTROLLED STUDY; ENZYME ASSAY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; FEMALE; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; POSITIVE FEEDBACK; PRIORITY JOURNAL; UBIQUITINATION; ANTAGONISTS AND INHIBITORS; CELL CYCLE; CHEMISTRY; FEEDBACK SYSTEM; FLUORESCENCE; HELA CELL LINE; KINETICS; METABOLISM; PROTEIN DOMAIN;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; CELL CYCLE; CYCLIN A; CYCLIN B; FEEDBACK, PHYSIOLOGICAL; FLUORESCENCE; FLUORESCENT DYES; HELA CELLS; HUMANS; KINETICS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SMN COMPLEX PROTEINS; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITINATION;

EID: 84927555890     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1248737     Document Type: Article

References (29)

1. J. J. Hopfield, Kinetic proofreading: A new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. Natl. Acad. Sci. U.S.A. 71, 4135-4139 (1974). doi: 10.1073/pnas.71.10.4135; pmid: 4530290
2. J. Ninio, Kinetic amplification of enzyme discrimination. Biochimie 57, 587-595 (1975). doi: 10.1016/S0300-9084(75) 80139-8; pmid: 1182215
3. T. W. McKeithan, Kinetic proofreading in T-cell receptor signal transduction. Proc. Natl. Acad. Sci. U.S.A. 92, 5042-5046 (1995). doi: 10.1073/pnas.92.11.5042; pmid: 7761445
4. M. Rape, S. K. Reddy, M. W. Kirschner, The processivity of multiubiquitination by the APC determines the order of substrate degradation. Cell 124, 89-103 (2006). doi: 10.1016/j.cell.2005.10.032; pmid: 16413484
5. J. M. Peters, The anaphase-promoting complex: Proteolysis in mitosis and beyond. Mol. Cell 9, 931-943 (2002). doi: 10.1016/S1097-2765(02)00540-3; pmid: 12049731
6. C. Lindon, J. Pines, Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J. Cell Biol. 164, 233-241 (2004). doi: 10.1083/jcb.200309035; pmid: 14734534
7. M. Glotzer, A. W. Murray, M. W. Kirschner, Cyclin is degraded by the ubiquitin pathway. Nature 349, 132-138 (1991). doi: 10.1038/349132a0; pmid: 1846030
8. C. M. Pfleger, M. W. Kirschner, The KEN box: An APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev. 14, 655-665 (2000). pmid: 10733526
9. D. Barford, Structural insights into anaphase-promoting complex function and mechanism. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 3605-3624 (2011). doi: 10.1098/rstb.2011.0069; pmid: 22084387
10. Y. Merbl, M. W. Kirschner, Large-scale detection of ubiquitination substrates using cell extracts and protein microarrays. Proc. Natl. Acad. Sci. U.S.A. 106, 2543-2548 (2009). doi: 10.1073/pnas.0812892106; pmid: 19181856
11. D. S. Kirkpatrick et al., Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat. Cell Biol. 8, 700-710 (2006). doi: 10.1038/ncb1436; pmid: 16799550
12. T. Ravid, M. Hochstrasser, Autoregulation of an E2 enzyme by ubiquitin-chain assembly on its catalytic residue. Nat. Cell Biol. 9, 422-427 (2007). doi: 10.1038/ncb1558; pmid: 17310239
13. W. Li, D. Tu, A. T. Brunger, Y. Ye, A ubiquitin ligase transfers preformed polyubiquitin chains from a conjugating enzyme to a substrate. Nature 446, 333-337 (2007). doi: 10.1038/nature05542; pmid: 17310145
14. N. W. Pierce, G. Kleiger, S. O. Shan, R. J. Deshaies, Detection of sequential polyubiquitylation on a millisecond timescale. Nature 462, 615-619 (2009). doi: 10.1038/nature08595; pmid: 19956254
15. C. W. Carroll, D. O. Morgan, The Doc1 subunit is a processivity factor for the anaphase-promoting complex. Nat. Cell Biol. 4, 880-887 (2002). doi: 10.1038/ncb871; pmid: 12402045
16. A. Williamson et al., Regulation of ubiquitin chain initiation to control the timing of substrate degradation. Mol. Cell 42, 744-757 (2011). doi: 10.1016/j.molcel.2011.04.022; pmid: 21700221
17. A. Plechanovová, E. G. Jaffray, M. H. Tatham, J. H. Naismith, R. T. Hay, Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis. Nature 489, 115-120 (2012). doi: 10.1038/nature11376; pmid: 22842904
18. H. B. Kamadurai et al., Insights into ubiquitin transfer cascades from a structure of a UbcH5B approximately ubiquitin-HECT (NEDD4L) complex. Mol. Cell 36, 1095-1102 (2009). doi: 10.1016/j.molcel.2009.11.010; pmid: 20064473
19. N. G. Brown et al., Mechanism of polyubiquitination by human anaphase-promoting complex: RING repurposing for ubiquitin chain assembly. Mol. Cell 56, 246-260 (2014). doi: 10.1016/j.molcel.2014.09.009; pmid: 25306923
20. A. Kelly, K. E. Wickliffe, L. Song, I. Fedrigo, M. Rape, Ubiquitin chain elongation requires E3-dependent tracking of the emerging conjugate. Mol. Cell 56, 232-245 (2014). doi: 10.1016/j.molcel.2014.09.010; pmid: 25306918
21. H. J. Meyer, M. Rape, Processive ubiquitin chain formation by the anaphase-promoting complex. Semin. Cell Dev. Biol. 22, 544-550 (2011). doi: 10.1016/j.semcdb.2011.03.009; pmid: 21477659
22. M. Fuxreiter, P. Tompa, I. Simon, Local structural disorder imparts plasticity on linear motifs. Bioinformatics 23, 950-956 (2007). doi: 10.1093/bioinformatics/btm035; pmid: 17387114
23. Z. Liu et al., GPS-ARM: Computational analysis of the APC/C recognition motif by predicting D-boxes and KEN-boxes. PLOS ONE 7, e34370 (2012). doi: 10.1371/journal. pone.0034370; pmid: 22479614
24. L. A. Highbarger, J. A. Gerlt, G. L. Kenyon, Mechanism of the reaction catalyzed by acetoacetate decarboxylase. Importance of lysine 116 in determining the pKa of active-site lysine 115. Biochemistry 35, 41-46 (1996). doi: 10.1021/bi9518306; pmid: 8555196
25. M. J. Bessman, N. Muzyczka, M. F. Goodman, R. L. Schnaar, Studies on the biochemical basis of spontaneous mutation. II. The incorporation of a base and its analogue into DNA by wild-type, mutator and antimutator DNA polymerases. J. Mol. Biol. 88, 409-421 (1974). doi: 10.1016/0022-2836(74)90491-4; pmid: 4616089
26. K. Bohman, T. Ruusala, P. C. Jelenc, C. G. Kurland, Kinetic impairment of restrictive streptomycin-resistant ribosomes. Mol. Gen. Genet. 198, 90-99 (1984). doi: 10.1007/BF00328706; pmid: 6394968
27. H. Yamano, C. Tsurumi, J. Gannon, T. Hunt, The role of the destruction box and its neighbouring lysine residues in cyclin B for anaphase ubiquitin-dependent proteolysis in fission yeast: Defining the D-box receptor. EMBO J. 17, 5670-5678 (1998). doi: 10.1093/emboj/17.19.5670; pmid: 9755167
28. M. L. Matsumoto et al., K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell 39, 477-484 (2010). doi: 10.1016/j.molcel.2010.07.001; pmid: 20655260
29. M. Kõivomägi et al., Cascades of multisite phosphorylation control Sic1 destruction at the onset of S phase. Nature 480, 128-131 (2011). doi: 10.1038/nature10560; pmid: 21993622