Structure of an APC3–APC16 Complex: Insights into Assembly of the Anaphase-Promoting Complex/Cyclosome

Yamaguchi, Masaya; Yu, Shanshan; Qiao, Renping; Weissmann, Florian; Miller, Darcie J.; VanderLinden, Ryan; Brown, Nicholas G.; Frye, Jeremiah J.; Peters, Jan-Michael; Schulman, Brenda A.

doi:10.1016/j.jmb.2014.11.020

Structure of an APC3–APC16 Complex: Insights into Assembly of the Anaphase-Promoting Complex/Cyclosome

Journal Article · Sat Dec 06 00:00:00 EST 2014 · Journal of Molecular Biology

DOI:https://doi.org/10.1016/j.jmb.2014.11.020· OSTI ID:1177429

Yamaguchi, Masaya ^[1]; Yu, Shanshan ^[1]; Qiao, Renping ^[2]; Weissmann, Florian ^[2]; Miller, Darcie J. ^[1]; VanderLinden, Ryan ^[3]; Brown, Nicholas G. ^[1]; Frye, Jeremiah J. ^[1]; Peters, Jan-Michael ^[2]; Schulman, Brenda A. ^[4]

St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Structural Biology
Research Inst. of Molecular Pathology (IMP), Vienna (Austria). Vienna Biocenter (VBC)
Howard Hughes Medical Inst., Memphis, TN (United States). St. Jude Children's Research Hospital
St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Structural Biology; Howard Hughes Medical Inst., Memphis, TN (United States). St. Jude Children's Research Hospital

The anaphase-promoting complex/cyclosome (APC/C) is a massive E3 ligase that controls mitosis by catalyzing ubiquitination of key cell cycle regulatory proteins. The APC/C assembly contains two subcomplexes: the “Platform” centers around a cullin-RING-like E3 ligase catalytic core; the “Arc Lamp” is a hub that mediates transient association with regulators and ubiquitination substrates. The Arc Lamp contains the small subunits APC16, CDC26, and APC13, and tetratricopeptide repeat (TPR) proteins (APC7, APC3, APC6, and APC8) that homodimerize and stack with quasi-2-fold symmetry. Within the APC/C complex, APC3 serves as center for regulation. APC3's TPR motifs recruit substrate-binding coactivators, CDC20 and CDH1, via their C-terminal conserved Ile-Arg (IR) tail sequences. Human APC3 also binds APC16 and APC7 and contains a > 200-residue loop that is heavily phosphorylated during mitosis, although the basis for APC3 interactions and whether loop phosphorylation is required for ubiquitination are unclear. Here, we map the basis for human APC3 assembly with APC16 and APC7, report crystal structures of APC3Δloop alone and in complex with the C-terminal domain of APC16, and test roles of APC3's loop and IR tail binding surfaces in APC/C-catalyzed ubiquitination. The structures show how one APC16 binds asymmetrically to the symmetric APC3 dimer and, together with biochemistry and prior data, explain how APC16 recruits APC7 to APC3, show how APC3's C-terminal domain is rearranged in the full APC/C assembly, and visualize residues in the IR tail binding cleft important for coactivator-dependent ubiquitination. Overall, the results provide insights into assembly, regulation, and interactions of TPR proteins and the APC/C.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1177429

Alternate ID(s):: OSTI ID: 1367766

Journal Information:: Journal of Molecular Biology, Journal Name: Journal of Molecular Biology Journal Issue: 8 Vol. 427; ISSN 0022-2836

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (80)

Cdc16p, Cdc23p and Cdc27p form a complex essential for mitosis. Lamb, J. R.; Michaud, W. A.; Sikorski, R. S. The EMBO Journal, Vol. 13, Issue 18 https://doi.org/10.1002/j.1460-2075.1994.tb06752.x	journal	September 1994
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Phosphorylation of the Cyclosome Is Required for Its Stimulation by Fizzy/cdc20 Shteinberg, Michal; Protopopov, Yana; Listovsky, Tamar Biochemical and Biophysical Research Communications, Vol. 260, Issue 1 https://doi.org/10.1006/bbrc.1999.0884	journal	June 1999
The CDC26 gene of Saccharomyces cerevisiae is required for cell growth only at high temperature Araki, Hiroyuki; Awane, Kaoru; Ogawa, Nobuo Molecular and General Genetics MGG, Vol. 231, Issue 2 https://doi.org/10.1007/BF00279807	journal	January 1992
A 20s complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B King, Randall W.; Peters, Jan-Michael; Tugendreich, Stuart Cell, Vol. 81, Issue 2 https://doi.org/10.1016/0092-8674(95)90338-0	journal	April 1995
Structure of TPR Domain–Peptide Complexes Scheufler, Clemens; Brinker, Achim; Bourenkov, Gleb Cell, Vol. 101, Issue 2 https://doi.org/10.1016/S0092-8674(00)80830-2	journal	April 2000
Identification of a novel ubiquitin-conjugating enzyme involved in mitotic cyclin degradation Yu, Hongtao; King, Randall W.; Peters, Jan-Michael Current Biology, Vol. 6, Issue 4 https://doi.org/10.1016/S0960-9822(02)00513-4	journal	April 1996
TPR Subunits of the Anaphase-Promoting Complex Mediate Binding to the Activator Protein CDH1 Vodermaier, Hartmut C.; Gieffers, Christian; Maurer-Stroh, Sebastian Current Biology, Vol. 13, Issue 17 https://doi.org/10.1016/S0960-9822(03)00581-5	journal	September 2003
Pharmacologic Inhibition of the Anaphase-Promoting Complex Induces A Spindle Checkpoint-Dependent Mitotic Arrest in the Absence of Spindle Damage Zeng, Xing; Sigoillot, Frederic; Gaur, Shantanu Cancer Cell, Vol. 18, Issue 4 https://doi.org/10.1016/j.ccr.2010.08.010	journal	October 2010
Sequential E2s Drive Polyubiquitin Chain Assembly on APC Targets Rodrigo-Brenni, Monica C.; Morgan, David O. Cell, Vol. 130, Issue 1 https://doi.org/10.1016/j.cell.2007.05.027	journal	July 2007
Solution Structure of the E.coli TolA C-terminal Domain Reveals Conformational Changes upon Binding to the Phage g3p N-terminal Domain Deprez, Christophe; Lloubès, Roland; Gavioli, Marthe Journal of Molecular Biology, Vol. 346, Issue 4 https://doi.org/10.1016/j.jmb.2004.12.028	journal	March 2005
Molecular Structure of the N-terminal Domain of the APC/C Subunit Cdc27 Reveals a Homo-dimeric Tetratricopeptide Repeat Architecture Zhang, Ziguo; Roe, S. Mark; Diogon, Marie Journal of Molecular Biology, Vol. 397, Issue 5 https://doi.org/10.1016/j.jmb.2010.02.045	journal	April 2010
The Four Canonical TPR Subunits of Human APC/C Form Related Homo-Dimeric Structures and Stack in Parallel to Form a TPR Suprahelix Zhang, Ziguo; Chang, Leifu; Yang, Jing Journal of Molecular Biology, Vol. 425, Issue 22 https://doi.org/10.1016/j.jmb.2013.04.004	journal	November 2013
The WD40 Propeller Domain of Cdh1 Functions as a Destruction Box Receptor for APC/C Substrates Kraft, Claudine; Vodermaier, Hartmut C.; Maurer-Stroh, Sebastian Molecular Cell, Vol. 18, Issue 5 https://doi.org/10.1016/j.molcel.2005.04.023	journal	May 2005
Localization of the Coactivator Cdh1 and the Cullin Subunit Apc2 in a Cryo-Electron Microscopy Model of Vertebrate APC/C Dube, Prakash; Herzog, Franz; Gieffers, Christian Molecular Cell, Vol. 20, Issue 6 https://doi.org/10.1016/j.molcel.2005.11.008	journal	December 2005
Structural Organization of the Anaphase-Promoting Complex Bound to the Mitotic Activator Slp1 Ohi, Melanie D.; Feoktistova, Anna; Ren, Liping Molecular Cell, Vol. 28, Issue 5 https://doi.org/10.1016/j.molcel.2007.10.003	journal	December 2007
Analysis of Activator-Binding Sites on the APC/C Supports a Cooperative Substrate-Binding Mechanism Matyskiela, Mary E.; Morgan, David O. Molecular Cell, Vol. 34, Issue 1 https://doi.org/10.1016/j.molcel.2009.02.027	journal	April 2009
Insights into Degron Recognition by APC/C Coactivators from the Structure of an Acm1-Cdh1 Complex He, Jun; Chao, William C. H.; Zhang, Ziguo Molecular Cell, Vol. 50, Issue 5 https://doi.org/10.1016/j.molcel.2013.04.024	journal	June 2013
Mechanism of Polyubiquitination by Human Anaphase-Promoting Complex: RING Repurposing for Ubiquitin Chain Assembly Brown, Nicholas G.; Watson, Edmond R.; Weissmann, Florian Molecular Cell, Vol. 56, Issue 2 https://doi.org/10.1016/j.molcel.2014.09.009	journal	October 2014
Novel functions for the anaphase-promoting complex in neurobiology Puram, Sidharth V.; Bonni, Azad Seminars in Cell & Developmental Biology, Vol. 22, Issue 6 https://doi.org/10.1016/j.semcdb.2011.03.006	journal	August 2011
Structural and Functional Discussion of the Tetra-Trico-Peptide Repeat, a Protein Interaction Module Zeytuni, Natalie; Zarivach, Raz Structure, Vol. 20, Issue 3 https://doi.org/10.1016/j.str.2012.01.006	journal	March 2012
Triggering of cyclin degradation in interphase extracts of amphibian eggs by cdc2 kinase Félix, Marie-Anne; Labbé, Jean-Claude; Dorée, Marcel Nature, Vol. 346, Issue 6282 https://doi.org/10.1038/346379a0	journal	July 1990
The APC/C subunit Cdc16/Cut9 is a contiguous tetratricopeptide repeat superhelix with a homo-dimer interface similar to Cdc27 Zhang, Ziguo; Kulkarni, Kiran; Hanrahan, Sarah J. The EMBO Journal, Vol. 29, Issue 21 https://doi.org/10.1038/emboj.2010.247	journal	October 2010
Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes Neumann, Beate; Walter, Thomas; Hériché, Jean-Karim Nature, Vol. 464, Issue 7289 https://doi.org/10.1038/nature08869	journal	April 2010
Structures of APC/CCdh1 with substrates identify Cdh1 and Apc10 as the D-box co-receptor da Fonseca, Paula C. A.; Kong, Eric H.; Zhang, Ziguo Nature, Vol. 470, Issue 7333 https://doi.org/10.1038/nature09625	journal	November 2010
Structural basis for the subunit assembly of the anaphase-promoting complex Schreiber, Anne; Stengel, Florian; Zhang, Ziguo Nature, Vol. 470, Issue 7333 https://doi.org/10.1038/nature09756	journal	February 2011
Structure of the mitotic checkpoint complex Chao, William C. H.; Kulkarni, Kiran; Zhang, Ziguo Nature, Vol. 484, Issue 7393 https://doi.org/10.1038/nature10896	journal	March 2012
Molecular architecture and mechanism of the anaphase-promoting complex Chang, Leifu; Zhang, Ziguo; Yang, Jing Nature, Vol. 513, Issue 7518 https://doi.org/10.1038/nature13543	journal	July 2014
Synergistic blockade of mitotic exit by two chemical inhibitors of the APC/C Sackton, Katharine L.; Dimova, Nevena; Zeng, Xing Nature, Vol. 514, Issue 7524 https://doi.org/10.1038/nature13660	journal	August 2014
UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit Garnett, Mathew J.; Mansfeld, Jörg; Godwin, Colin Nature Cell Biology, Vol. 11, Issue 11 https://doi.org/10.1038/ncb1983	journal	October 2009
APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1 Dimova, Nevena V.; Hathaway, Nathaniel A.; Lee, Byung-Hoon Nature Cell Biology, Vol. 14, Issue 2 https://doi.org/10.1038/ncb2425	journal	January 2012
An APC/C inhibitor stabilizes cyclin B1 by prematurely terminating ubiquitination Zeng, Xing; King, Randall W. Nature Chemical Biology, Vol. 8, Issue 4 https://doi.org/10.1038/nchembio.801	journal	February 2012
Protein structure prediction on the Web: a case study using the Phyre server Kelley, Lawrence A.; Sternberg, Michael J. E. Nature Protocols, Vol. 4, Issue 3 https://doi.org/10.1038/nprot.2009.2	journal	February 2009
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
The anaphase promoting complex/cyclosome: a machine designed to destroy Peters, Jan-Michael Nature Reviews Molecular Cell Biology, Vol. 7, Issue 9 https://doi.org/10.1038/nrm1988	journal	August 2006
Cubism and the cell cycle: the many faces of the APC/C Pines, Jonathon Nature Reviews Molecular Cell Biology, Vol. 12, Issue 7 https://doi.org/10.1038/nrm3132	journal	June 2011
Crystal structure of the APC10/DOC1 subunit of the human anaphase-promoting complex Wendt, Kerstin S.; Vodermaier, Hartmut C.; Jacob, Uwe Nature Structural Biology, Vol. 8, Issue 9, p. 784-788 https://doi.org/10.1038/nsb0901-784	journal	September 2001
Insights into anaphase promoting complex TPR subdomain assembly from a CDC26–APC6 structure Wang, Jing; Dye, Billy T.; Rajashankar, Kanagalaghatta R. Nature Structural & Molecular Biology, Vol. 16, Issue 9 https://doi.org/10.1038/nsmb.1645	journal	August 2009
Substrate binding on the APC/C occurs between the coactivator Cdh1 and the processivity factor Doc1 Buschhorn, Bettina A.; Petzold, Georg; Galova, Marta Nature Structural & Molecular Biology, Vol. 18, Issue 1 https://doi.org/10.1038/nsmb.1979	journal	December 2010
APC15 mediates CDC20 autoubiquitylation by APC/CMCC and disassembly of the mitotic checkpoint complex Uzunova, Kristina; Dye, Billy T.; Schutz, Hannelore Nature Structural & Molecular Biology, Vol. 19, Issue 11 https://doi.org/10.1038/nsmb.2412	journal	September 2012
Electron microscopy structure of human APC/CCDH1–EMI1 reveals multimodal mechanism of E3 ligase shutdown Frye, Jeremiah J.; Brown, Nicholas G.; Petzold, Georg Nature Structural & Molecular Biology, Vol. 20, Issue 7 https://doi.org/10.1038/nsmb.2593	journal	May 2013
Two WXXF-based motifs in NECAPs define the specificity of accessory protein binding to AP-1 and AP-2 Ritter, Brigitte; Denisov, Alexei Yu; Philie, Jacynthe The EMBO Journal, Vol. 23, Issue 19 https://doi.org/10.1038/sj.emboj.7600378	journal	September 2004
Recombinant expression, reconstitution and structure of human anaphase-promoting complex (APC/C) Zhang, Ziguo; Yang, Jing; Kong, Eric H. Biochemical Journal, Vol. 449, Issue 2 https://doi.org/10.1042/BJ20121374	journal	December 2012
Identification of a physiological E2 module for the human anaphase-promoting complex Williamson, A.; Wickliffe, K. E.; Mellone, B. G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 43 https://doi.org/10.1073/pnas.0907887106	journal	October 2009
UBE2S drives elongation of K11-linked ubiquitin chains by the Anaphase-Promoting Complex Wu, T.; Merbl, Y.; Huo, Y. Proceedings of the National Academy of Sciences, Vol. 107, Issue 4 https://doi.org/10.1073/pnas.0912802107	journal	January 2010
Structural analysis of human Cdc20 supports multisite degron recognition by APC/C Tian, W.; Li, B.; Warrington, R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 45 https://doi.org/10.1073/pnas.1213438109	journal	October 2012
Reversible phosphorylation controls the activity of cyclosome-associated cyclin-ubiquitin ligase. Lahav-Baratz, S.; Sudakin, V.; Ruderman, J. V. Proceedings of the National Academy of Sciences, Vol. 92, Issue 20 https://doi.org/10.1073/pnas.92.20.9303	journal	September 1995
E2-C, a cyclin-selective ubiquitin carrier protein required for the destruction of mitotic cyclins. Aristarkhov, A.; Eytan, E.; Moghe, A. Proceedings of the National Academy of Sciences, Vol. 93, Issue 9 https://doi.org/10.1073/pnas.93.9.4294	journal	April 1996
Electrostatic Interactions of Hsp-organizing Protein Tetratricopeptide Domains with Hsp70 and Hsp90 Kajander, Tommi; Sachs, Jonathan N.; Goldman, Adrian Journal of Biological Chemistry, Vol. 284, Issue 37 https://doi.org/10.1074/jbc.M109.033894	journal	September 2009
Phosphorylation by Cdc28 Activates the Cdc20-Dependent Activity of the Anaphase-Promoting Complex Rudner, Adam D.; Murray, Andrew W. Journal of Cell Biology, Vol. 149, Issue 7 https://doi.org/10.1083/jcb.149.7.1377	journal	June 2000
Panta rhei: The APC/C at steady state Primorac, Ivana; Musacchio, Andrea The Journal of Cell Biology, Vol. 201, Issue 2 https://doi.org/10.1083/jcb.201301130	journal	April 2013
The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Sudakin, V.; Ganoth, D.; Dahan, A. Molecular Biology of the Cell, Vol. 6, Issue 2 https://doi.org/10.1091/mbc.6.2.185	journal	February 1995
Searching protein structure databases with DaliLite v.3 Holm, L.; Kaariainen, S.; Rosenstrom, P. Bioinformatics, Vol. 24, Issue 23 https://doi.org/10.1093/bioinformatics/btn507	journal	September 2008
Mitotic regulation of the human anaphase-promoting complex by phosphorylation Kraft, C. The EMBO Journal, Vol. 22, Issue 24 https://doi.org/10.1093/emboj/cdg627	journal	December 2003
GENETIC CONTROL OF THE CELL DIVISION CYCLE IN YEAST: V. GENETIC ANALYSIS OF cdc MUTANTS Hartwell, Leland H.; Mortimer, Robert K.; Culotti, Joseph Genetics, Vol. 74, Issue 2 https://doi.org/10.1093/genetics/74.2.267	journal	June 1973
Dali server: conservation mapping in 3D Holm, Liisa; Rosenstrï¿½m, Pï¿½ivi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq366	journal	May 2010
Scalable web services for the PSIPRED Protein Analysis Workbench Buchan, Daniel W. A.; Minneci, Federico; Nugent, Tim C. O. Nucleic Acids Research, Vol. 41, Issue W1 https://doi.org/10.1093/nar/gkt381	journal	June 2013
The anaphase-promoting complex: it's not just for mitosis any more Harper, J. W. Genes & Development, Vol. 16, Issue 17 https://doi.org/10.1101/gad.1013102	journal	September 2002
Xe-p9, a Xenopus Suc1/Cks protein, is essential for the Cdc2-dependent phosphorylation of the anaphase- promoting complex at mitosis Patra, D.; Dunphy, W. G. Genes & Development, Vol. 12, Issue 16 https://doi.org/10.1101/gad.12.16.2549	journal	August 1998
An architectural map of the anaphase-promoting complex Thornton, B. R. Genes & Development, Vol. 20, Issue 4 https://doi.org/10.1101/gad.1396906	journal	February 2006
D box and KEN box motifs in budding yeast Hsl1p are required for APC-mediated degradation and direct binding to Cdc20p and Cdh1p Burton, J. L. Genes & Development, Vol. 15, Issue 18 https://doi.org/10.1101/gad.917901	journal	September 2001
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
Production of selenomethionyl-derivatized proteins in baculovirus-infected insect cells Cronin, Ciarán N.; Lim, Kheng B.; Rogers, Joe Protein Science, Vol. 16, Issue 9 https://doi.org/10.1110/ps.072931407	journal	September 2007
Ubistatins Inhibit Proteasome-Dependent Degradation by Binding the Ubiquitin Chain Verma, R. Science, Vol. 306, Issue 5693 https://doi.org/10.1126/science.1100946	journal	October 2004
Structure of the Anaphase-Promoting Complex/Cyclosome Interacting with a Mitotic Checkpoint Complex Herzog, F.; Primorac, I.; Dube, P. Science, Vol. 323, Issue 5920 https://doi.org/10.1126/science.1163300	journal	March 2009
Systematic Analysis of Human Protein Complexes Identifies Chromosome Segregation Proteins Hutchins, J. R. A.; Toyoda, Y.; Hegemann, B. Science, Vol. 328, Issue 5978 https://doi.org/10.1126/science.1181348	journal	April 2010
Identification of Subunits of the Anaphase-Promoting Complex of Saccharomyces cerevisiae Zachariae, W.; Shin, T. H.; Galova, M. Science, Vol. 274, Issue 5290 https://doi.org/10.1126/science.274.5290.1201	journal	November 1996
Mass Spectrometric Analysis of the Anaphase-Promoting Complex from Yeast: Identification of a Subunit Related to Cullins Zachariae, W. Science, Vol. 279, Issue 5354 https://doi.org/10.1126/science.279.5354.1216	journal	February 1998
Systematic Phosphorylation Analysis of Human Mitotic Protein Complexes Hegemann, B.; Hutchins, J. R. A.; Hudecz, O. Science Signaling, Vol. 4, Issue 198 https://doi.org/10.1126/scisignal.2001993	journal	November 2011
Regulation of APC/C Activators in Mitosis and Meiosis Pesin, Jillian A.; Orr-Weaver, Terry L. Annual Review of Cell and Developmental Biology, Vol. 24, Issue 1 https://doi.org/10.1146/annurev.cellbio.041408.115949	journal	November 2008
TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences Karpenahalli, Manjunatha R.; Lupas, Andrei N.; Söding, Johannes BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-2	journal	January 2007
Meiotic control of the APC/C: similarities & differences from mitosis Cooper, Katrina F.; Strich, Randy Cell Division, Vol. 6, Issue 1 https://doi.org/10.1186/1747-1028-6-16	journal	January 2011
APC16 is a conserved subunit of the anaphase-promoting complex/cyclosome Kops, Geert J. P. L.; van der Voet, Monique; Manak, Michael S. Journal of Cell Science, Vol. 123, Issue 10 https://doi.org/10.1242/jcs.061549	journal	May 2010
emb-1 Encodes the APC16 Subunit of the Caenorhabditis elegans Anaphase-Promoting Complex Shakes, Diane C.; Allen, Anna K.; Albert, Kelsey M. Genetics, Vol. 189, Issue 2 https://doi.org/10.1534/genetics.111.131714	journal	October 2011
State of the APC/C: Organization, function, and structure McLean, Janel R.; Chaix, Denis; Ohi, Melanie D. Critical Reviews in Biochemistry and Molecular Biology, Vol. 46, Issue 2 https://doi.org/10.3109/10409238.2010.541420	journal	January 2011

Cited By (12)

Atomic-Resolution Structures of the APC/C Subunits Apc4 and the Apc5 N-Terminal Domain Cronin, Nora B.; Yang, Jing; Zhang, Ziguo Journal of Molecular Biology, Vol. 427, Issue 20 https://doi.org/10.1016/j.jmb.2015.08.023	journal	October 2015
SUMO targets the APC/C to regulate transition from metaphase to anaphase Eifler, Karolin; Cuijpers, Sabine A. G.; Willemstein, Edwin Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03486-4	journal	March 2018
Visualizing the complex functions and mechanisms of the anaphase promoting complex/cyclosome (APC/C) Alfieri, Claudio; Zhang, Suyang; Barford, David Open Biology, Vol. 7, Issue 11 https://doi.org/10.1098/rsob.170204	journal	November 2017
Insights into APC/C: from cellular function to diseases and therapeutics Zhou, Zhuan; He, Mingjing; Shah, Anil A. Cell Division, Vol. 11, Issue 1 https://doi.org/10.1186/s13008-016-0021-6	journal	March 2016
Mechanisms for the temporal regulation of substrate ubiquitination by the anaphase-promoting complex/cyclosome Bansal, Shivangee; Tiwari, Swati Cell Division, Vol. 14, Issue 1 https://doi.org/10.1186/s13008-019-0057-5	journal	December 2019
The Anaphase-Promoting Complex (APC) ubiquitin ligase affects chemosensory behavior inC. elegans Wang, Julia; Jennings, Alexandra K.; Kowalski, Jennifer R. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2013	journal	May 2016
The anaphase‐promoting complex: A key mitotic regulator associated with somatic mutations occurring in cancer Melloy, Patricia G. Genes, Chromosomes and Cancer, Vol. 59, Issue 3 https://doi.org/10.1002/gcc.22820	journal	October 2019
Molecular mechanism of APC/C activation by mitotic phosphorylation Zhang, Suyang; Chang, Leifu; Alfieri, Claudio Nature, Vol. 533, Issue 7602 https://doi.org/10.1038/nature17973	journal	April 2016
Plasmodium APC3 mediates chromosome condensation and cytokinesis during atypical mitosis in male gametogenesis Wall, Richard J.; Ferguson, David J. P.; Freville, Aline Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-23871-9	journal	April 2018
RING E3 mechanism for ubiquitin ligation to a disordered substrate visualized for human anaphase-promoting complex Brown, Nicholas G.; VanderLinden, Ryan; Watson, Edmond R. Proceedings of the National Academy of Sciences, Vol. 112, Issue 17 https://doi.org/10.1073/pnas.1504161112	journal	March 2015
Mechanism of APC/C ^CDC20 activation by mitotic phosphorylation Qiao, Renping; Weissmann, Florian; Yamaguchi, Masaya Proceedings of the National Academy of Sciences, Vol. 113, Issue 19 https://doi.org/10.1073/pnas.1604929113	journal	April 2016
biGBac enables rapid gene assembly for the expression of large multisubunit protein complexes Weissmann, Florian; Petzold, Georg; VanderLinden, Ryan Proceedings of the National Academy of Sciences, Vol. 113, Issue 19 https://doi.org/10.1073/pnas.1604935113	journal	April 2016

Similar Records

RING E3 mechanism for ubiquitin ligation to a disordered substrate visualized for human anaphase-promoting complex

Journal Article · Sun Mar 29 20:00:00 EDT 2015 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1197027

Cdh1-APC/C, cyclin B-Cdc2, and Alzheimer's disease pathology

Journal Article · Thu Jan 05 23:00:00 EST 2006 · Biochemical and Biophysical Research Communications · OSTI ID:20795847

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Structure of an APC3–APC16 Complex: Insights into Assembly of the Anaphase-Promoting Complex/Cyclosome

Citation Formats

References (80)

Cited By (12)

Similar Records

Related Subjects