RING E3 mechanism for ubiquitin ligation to a disordered substrate visualized for human anaphase-promoting complex
Abstract
For many E3 ligases, a mobile RING (Really Interesting New Gene) domain stimulates ubiquitin (Ub) transfer from a thioester-linked E2~Ub intermediate to a lysine on a remotely bound disordered substrate. One such E3 is the gigantic, multisubunit 1.2-MDa anaphase-promoting complex/cyclosome (APC), which controls cell division by ubiquitinating cell cycle regulators to drive their timely degradation. Intrinsically disordered substrates are typically recruited via their KEN-box, D-box, and/or other motifs binding to APC and a coactivator such as CDH1. On the opposite side of the APC, the dynamic catalytic core contains the cullin-like subunit APC2 and its RING partner APC11, which collaborates with the E2 UBCH10 (UBE2C) to ubiquitinate substrates. However, how dynamic RING–E2~Ub catalytic modules such as APC11–UBCH10~Ub collide with distally tethered disordered substrates remains poorly understood. In this paper, we report structural mechanisms of UBCH10 recruitment to APCCDH1 and substrate ubiquitination. Unexpectedly, in addition to binding APC11’s RING, UBCH10 is corecruited via interactions with APC2, which we visualized in a trapped complex representing an APCCDH1–UBCH10~Ub–substrate intermediate by cryo-electron microscopy, and in isolation by X-ray crystallography. To our knowledge, this is the first structural view of APC, or any cullin–RING E3, with E2 and substrate juxtaposed, and it reveals how tripartitemore »
- Authors:
-
- St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Structural Biology
- St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Structural Biology. Howard Hughes Medical Inst.
- St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Structural Biology; Univ. of Tennessee Health Sciences Center, Memphis, TN (United States). Dept. of Microbiology, Immunology, and Biochemistry
- Vienna Biocenter (VBC) (Austria). Research Inst. of Molecular Pathology (IMP)
- Max Planck Inst. for Biophysical Chemistry, Gottingen (Germany); Univ. of Gottingen (Germany). Dept. of 3D Electron Cryomicroscopy. Inst. of Microbiology and Genetics
- St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Chemical Biology and Therapeutics
- St. Jude Children's Research Hospital, Memphis, TN (United States). Hartwell Center for Bioinformatics and Biotechnology
- St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Structural Biology. Howard Hughes Medical Inst.; Univ. of Tennessee Health Sciences Center, Memphis, TN (United States). Dept. of Microbiology, Immunology, and Biochemistry
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States); St. Jude Children's Research Hospital, Memphis, TN (United States); Vienna Biocenter (VBC) (Austria); Max Planck Inst. for Biophysical Chemistry, Gottingen (Germany); Univ. of Goettingen (Germany)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Inst. of Health (NIH) (United States); Jane Coffin Childs Foundation (United States); American Cancer Society (United States); American Lebanese Syrian Associated Charities (ALSAC) (United States); Howard Hughes Medical Inst. (United States); Japan Society for the Promotion of Science (Japan); Boehringer Ingelheim (Germany); Laura Bassi Centre for Optimized Structural Studies (Austria); European Union (Belgium); Austrian Research Fund (Austria); German Research Foundation (DFG)
- OSTI Identifier:
- 1197027
- Grant/Contract Number:
- AC02-06CH11357; R37GM065930; P30CA021765; P41 GM103403; RSG CDD-120969; 227764 MitoSys; Sonderforschungsbereich 860
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 112; Journal Issue: 17; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 60 APPLIED LIFE SCIENCES; ubiquitin; anaphase-promoting complex; cullin; E3; electron microscopy
Citation Formats
Brown, Nicholas G., VanderLinden, Ryan, Watson, Edmond R., Qiao, Renping, Grace, Christy R. R., Yamaguchi, Masaya, Weissmann, Florian, Frye, Jeremiah J., Dube, Prakash, Ei Cho, Shein, Actis, Marcelo L., Rodrigues, Patrick, Fujii, Naoaki, Peters, Jan-Michael, Stark, Holger, and Schulman, Brenda A. RING E3 mechanism for ubiquitin ligation to a disordered substrate visualized for human anaphase-promoting complex. United States: N. p., 2015.
Web. doi:10.1073/pnas.1504161112.
Brown, Nicholas G., VanderLinden, Ryan, Watson, Edmond R., Qiao, Renping, Grace, Christy R. R., Yamaguchi, Masaya, Weissmann, Florian, Frye, Jeremiah J., Dube, Prakash, Ei Cho, Shein, Actis, Marcelo L., Rodrigues, Patrick, Fujii, Naoaki, Peters, Jan-Michael, Stark, Holger, & Schulman, Brenda A. RING E3 mechanism for ubiquitin ligation to a disordered substrate visualized for human anaphase-promoting complex. United States. https://doi.org/10.1073/pnas.1504161112
Brown, Nicholas G., VanderLinden, Ryan, Watson, Edmond R., Qiao, Renping, Grace, Christy R. R., Yamaguchi, Masaya, Weissmann, Florian, Frye, Jeremiah J., Dube, Prakash, Ei Cho, Shein, Actis, Marcelo L., Rodrigues, Patrick, Fujii, Naoaki, Peters, Jan-Michael, Stark, Holger, and Schulman, Brenda A. Mon .
"RING E3 mechanism for ubiquitin ligation to a disordered substrate visualized for human anaphase-promoting complex". United States. https://doi.org/10.1073/pnas.1504161112. https://www.osti.gov/servlets/purl/1197027.
@article{osti_1197027,
title = {RING E3 mechanism for ubiquitin ligation to a disordered substrate visualized for human anaphase-promoting complex},
author = {Brown, Nicholas G. and VanderLinden, Ryan and Watson, Edmond R. and Qiao, Renping and Grace, Christy R. R. and Yamaguchi, Masaya and Weissmann, Florian and Frye, Jeremiah J. and Dube, Prakash and Ei Cho, Shein and Actis, Marcelo L. and Rodrigues, Patrick and Fujii, Naoaki and Peters, Jan-Michael and Stark, Holger and Schulman, Brenda A.},
abstractNote = {For many E3 ligases, a mobile RING (Really Interesting New Gene) domain stimulates ubiquitin (Ub) transfer from a thioester-linked E2~Ub intermediate to a lysine on a remotely bound disordered substrate. One such E3 is the gigantic, multisubunit 1.2-MDa anaphase-promoting complex/cyclosome (APC), which controls cell division by ubiquitinating cell cycle regulators to drive their timely degradation. Intrinsically disordered substrates are typically recruited via their KEN-box, D-box, and/or other motifs binding to APC and a coactivator such as CDH1. On the opposite side of the APC, the dynamic catalytic core contains the cullin-like subunit APC2 and its RING partner APC11, which collaborates with the E2 UBCH10 (UBE2C) to ubiquitinate substrates. However, how dynamic RING–E2~Ub catalytic modules such as APC11–UBCH10~Ub collide with distally tethered disordered substrates remains poorly understood. In this paper, we report structural mechanisms of UBCH10 recruitment to APCCDH1 and substrate ubiquitination. Unexpectedly, in addition to binding APC11’s RING, UBCH10 is corecruited via interactions with APC2, which we visualized in a trapped complex representing an APCCDH1–UBCH10~Ub–substrate intermediate by cryo-electron microscopy, and in isolation by X-ray crystallography. To our knowledge, this is the first structural view of APC, or any cullin–RING E3, with E2 and substrate juxtaposed, and it reveals how tripartite cullin–RING–E2 interactions establish APC’s specificity for UBCH10 and harness a flexible catalytic module to drive ubiquitination of lysines within an accessible zone. Finally, we propose that multisite interactions reduce the degrees of freedom available to dynamic RING E3–E2~Ub catalytic modules, condense the search radius for target lysines, increase the chance of active-site collision with conformationally fluctuating substrates, and enable regulation.},
doi = {10.1073/pnas.1504161112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 17,
volume = 112,
place = {United States},
year = {Mon Mar 30 00:00:00 EDT 2015},
month = {Mon Mar 30 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Structures of APC/CCdh1 with substrates identify Cdh1 and Apc10 as the D-box co-receptor
journal, November 2010
- da Fonseca, Paula C. A.; Kong, Eric H.; Zhang, Ziguo
- Nature, Vol. 470, Issue 7333
E3 ligase Rad18 promotes monoubiquitination rather than ubiquitin chain formation by E2 enzyme Rad6
journal, March 2011
- Hibbert, R. G.; Huang, A.; Boelens, R.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 14
Structure of a RING E3 Trapped in Action Reveals Ligation Mechanism for the Ubiquitin-like Protein NEDD8
journal, June 2014
- Scott, Daniel C.; Sviderskiy, Vladislav O.; Monda, Julie K.
- Cell, Vol. 157, Issue 7
Activation of UbcH5c∼Ub Is the Result of a Shift in Interdomain Motions of the Conjugate Bound to U-Box E3 Ligase E4B
journal, April 2013
- Soss, Sarah E.; Klevit, Rachel E.; Chazin, Walter J.
- Biochemistry, Vol. 52, Issue 17
Identification of a physiological E2 module for the human anaphase-promoting complex
journal, October 2009
- Williamson, A.; Wickliffe, K. E.; Mellone, B. G.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 43
The zinc-binding region (ZBR) fragment of Emi2 can inhibit APC/C by targeting its association with the coactivator Cdc20 and UBE2C-mediated ubiquitylation
journal, January 2014
- Shoji, Shisako; Muto, Yutaka; Ikeda, Mariko
- FEBS Open Bio, Vol. 4, Issue 1
A Structurally Unique E2-Binding Domain Activates Ubiquitination by the ERAD E2, Ubc7p, through Multiple Mechanisms
journal, May 2013
- Metzger, Meredith B.; Liang, Yu-He; Das, Ranabir
- Molecular Cell, Vol. 50, Issue 4
Identification of a novel ubiquitin-conjugating enzyme involved in mitotic cyclin degradation
journal, April 1996
- Yu, Hongtao; King, Randall W.; Peters, Jan-Michael
- Current Biology, Vol. 6, Issue 4
Crystal structure of the PRC1 ubiquitylation module bound to the nucleosome
journal, October 2014
- McGinty, Robert K.; Henrici, Ryan C.; Tan, Song
- Nature, Vol. 514, Issue 7524
Sequential E2s Drive Polyubiquitin Chain Assembly on APC Targets
journal, July 2007
- Rodrigo-Brenni, Monica C.; Morgan, David O.
- Cell, Vol. 130, Issue 1
The WD40 Propeller Domain of Cdh1 Functions as a Destruction Box Receptor for APC/C Substrates
journal, May 2005
- Kraft, Claudine; Vodermaier, Hartmut C.; Maurer-Stroh, Sebastian
- Molecular Cell, Vol. 18, Issue 5
Mechanism of ubiquitin ligation and lysine prioritization by a HECT E3
journal, August 2013
- Kamadurai, Hari B.; Qiu, Yu; Deng, Alan
- eLife, Vol. 2
Ubiquitin Chain Elongation Requires E3-Dependent Tracking of the Emerging Conjugate
journal, October 2014
- Kelly, Aileen; Wickliffe, Katherine E.; Song, Ling
- Molecular Cell, Vol. 56, Issue 2
BIRC7–E2 ubiquitin conjugate structure reveals the mechanism of ubiquitin transfer by a RING dimer
journal, August 2012
- Dou, Hao; Buetow, Lori; Sibbet, Gary J.
- Nature Structural & Molecular Biology, Vol. 19, Issue 9
APC15 mediates CDC20 autoubiquitylation by APC/CMCC and disassembly of the mitotic checkpoint complex
journal, September 2012
- Uzunova, Kristina; Dye, Billy T.; Schutz, Hannelore
- Nature Structural & Molecular Biology, Vol. 19, Issue 11
Structure of an APC3–APC16 Complex: Insights into Assembly of the Anaphase-Promoting Complex/Cyclosome
journal, April 2015
- Yamaguchi, Masaya; Yu, Shanshan; Qiao, Renping
- Journal of Molecular Biology, Vol. 427, Issue 8
Mechanism of Polyubiquitination by Human Anaphase-Promoting Complex: RING Repurposing for Ubiquitin Chain Assembly
journal, October 2014
- Brown, Nicholas G.; Watson, Edmond R.; Weissmann, Florian
- Molecular Cell, Vol. 56, Issue 2
Structure of the Cul1–Rbx1–Skp1–F boxSkp2 SCF ubiquitin ligase complex
journal, April 2002
- Zheng, Ning; Schulman, Brenda A.; Song, Langzhou
- Nature, Vol. 416, Issue 6882
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Activation of the APC/C Ubiquitin Ligase by Enhanced E2 Efficiency
journal, July 2014
- Van Voorhis, Vanessa A.; Morgan, David O.
- Current Biology, Vol. 24, Issue 13
Structural Insights into NEDD8 Activation of Cullin-RING Ligases: Conformational Control of Conjugation
journal, September 2008
- Duda, David M.; Borg, Laura A.; Scott, Daniel C.
- Cell, Vol. 134, Issue 6
Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry
journal, November 2004
- Rape, Michael; Kirschner, Marc W.
- Nature, Vol. 432, Issue 7017
Structural regulation of cullin-RING ubiquitin ligase complexes
journal, April 2011
- Duda, David M.; Scott, Daniel C.; Calabrese, Matthew F.
- Current Opinion in Structural Biology, Vol. 21, Issue 2
The Unique N Terminus of the UbcH10 E2 Enzyme Controls the Threshold for APC Activation and Enhances Checkpoint Regulation of the APC
journal, August 2008
- Summers, Matthew K.; Pan, Borlan; Mukhyala, Kiran
- Molecular Cell, Vol. 31, Issue 4
Insights into E3 ligase activity revealed by a SUMO–RanGAP1–Ubc9–Nup358 complex
journal, June 2005
- Reverter, David; Lima, Christopher D.
- Nature, Vol. 435, Issue 7042
Emi1 stably binds and inhibits the anaphase-promoting complex/cyclosome as a pseudosubstrate inhibitor
journal, September 2006
- Miller, J. J.
- Genes & Development, Vol. 20, Issue 17
Emi1 preferentially inhibits ubiquitin chain elongation by the anaphase-promoting complex
journal, May 2013
- Wang, Weiping; Kirschner, Marc W.
- Nature Cell Biology, Vol. 15, Issue 7
Identification of a Cullin Homology Region in a Subunit of the Anaphase-Promoting Complex
journal, February 1998
- Yu, H.
- Science, Vol. 279, Issue 5354
Mass Spectrometric Analysis of the Anaphase-Promoting Complex from Yeast: Identification of a Subunit Related to Cullins
journal, February 1998
- Zachariae, W.
- Science, Vol. 279, Issue 5354
Molecular architecture and mechanism of the anaphase-promoting complex
journal, July 2014
- Chang, Leifu; Zhang, Ziguo; Yang, Jing
- Nature, Vol. 513, Issue 7518
UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit
journal, October 2009
- Garnett, Mathew J.; Mansfeld, Jörg; Godwin, Colin
- Nature Cell Biology, Vol. 11, Issue 11
A Role for the Fizzy/Cdc20 Family of Proteins in Activation of the APC/C Distinct from Substrate Recruitment
journal, November 2008
- Kimata, Yuu; Baxter, Joanne E.; Fry, Andrew M.
- Molecular Cell, Vol. 32, Issue 4
A 20s complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B
journal, April 1995
- King, Randall W.; Peters, Jan-Michael; Tugendreich, Stuart
- Cell, Vol. 81, Issue 2
Regulation of Ubiquitin Chain Initiation to Control the Timing of Substrate Degradation
journal, June 2011
- Williamson, Adam; Banerjee, Sudeep; Zhu, Xining
- Molecular Cell, Vol. 42, Issue 6
Features and development of Coot
journal, March 2010
- Emsley, P.; Lohkamp, B.; Scott, W. G.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
Substrate binding on the APC/C occurs between the coactivator Cdh1 and the processivity factor Doc1
journal, December 2010
- Buschhorn, Bettina A.; Petzold, Georg; Galova, Marta
- Nature Structural & Molecular Biology, Vol. 18, Issue 1
UBE2S drives elongation of K11-linked ubiquitin chains by the Anaphase-Promoting Complex
journal, January 2010
- Wu, T.; Merbl, Y.; Huo, Y.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 4
Insights into Degron Recognition by APC/C Coactivators from the Structure of an Acm1-Cdh1 Complex
journal, June 2013
- He, Jun; Chao, William C. H.; Zhang, Ziguo
- Molecular Cell, Vol. 50, Issue 5
Structural and Functional Analysis of the Human Mitotic-specific Ubiquitin-conjugating Enzyme, UbcH10
journal, April 2002
- Lin, Yaqiong; Hwang, William C.; Basavappa, Ravi
- Journal of Biological Chemistry, Vol. 277, Issue 24
Structural analysis of human Cdc20 supports multisite degron recognition by APC/C
journal, October 2012
- Tian, W.; Li, B.; Warrington, R.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 45
APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1
journal, January 2012
- Dimova, Nevena V.; Hathaway, Nathaniel A.; Lee, Byung-Hoon
- Nature Cell Biology, Vol. 14, Issue 2
The Processivity of Multiubiquitination by the APC Determines the Order of Substrate Degradation
journal, January 2006
- Rape, Michael; Reddy, Sashank K.; Kirschner, Marc W.
- Cell, Vol. 124, Issue 1
Structure of an E3:E2∼Ub Complex Reveals an Allosteric Mechanism Shared among RING/U-box Ligases
journal, September 2012
- Pruneda, Jonathan N.; Littlefield, Peter J.; Soss, Sarah E.
- Molecular Cell, Vol. 47, Issue 6
Mms2–Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation
journal, September 2006
- Eddins, Michael J.; Carlile, Candice M.; Gomez, Kamila M.
- Nature Structural & Molecular Biology, Vol. 13, Issue 10
The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis.
journal, February 1995
- Sudakin, V.; Ganoth, D.; Dahan, A.
- Molecular Biology of the Cell, Vol. 6, Issue 2
E2-C, a cyclin-selective ubiquitin carrier protein required for the destruction of mitotic cyclins.
journal, April 1996
- Aristarkhov, A.; Eytan, E.; Moghe, A.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 9
D box and KEN box motifs in budding yeast Hsl1p are required for APC-mediated degradation and direct binding to Cdc20p and Cdh1p
journal, September 2001
- Burton, J. L.
- Genes & Development, Vol. 15, Issue 18
Electron microscopy structure of human APC/CCDH1–EMI1 reveals multimodal mechanism of E3 ligase shutdown
journal, May 2013
- Frye, Jeremiah J.; Brown, Nicholas G.; Petzold, Georg
- Nature Structural & Molecular Biology, Vol. 20, Issue 7
Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis
journal, July 2012
- Plechanovová, Anna; Jaffray, Ellis G.; Tatham, Michael H.
- Nature, Vol. 489, Issue 7414
Localization of the Coactivator Cdh1 and the Cullin Subunit Apc2 in a Cryo-Electron Microscopy Model of Vertebrate APC/C
journal, December 2005
- Dube, Prakash; Herzog, Franz; Gieffers, Christian
- Molecular Cell, Vol. 20, Issue 6
Allosteric Activation of E2-RING Finger-Mediated Ubiquitylation by a Structurally Defined Specific E2-Binding Region of gp78
journal, June 2009
- Das, Ranabir; Mariano, Jennifer; Tsai, Yien Che
- Molecular Cell, Vol. 34, Issue 6
Identification of conjugation specificity determinants unmasks vestigial preference for ubiquitin within the NEDD8 E2
journal, February 2008
- Huang, Danny T.; Zhuang, Min; Ayrault, Olivier
- Nature Structural & Molecular Biology, Vol. 15, Issue 3
Structural assembly of cullin-RING ubiquitin ligase complexes
journal, December 2010
- Zimmerman, Erik S.; Schulman, Brenda A.; Zheng, Ning
- Current Opinion in Structural Biology, Vol. 20, Issue 6
A UbcH5/Ubiquitin Noncovalent Complex Is Required for Processive BRCA1-Directed Ubiquitination
journal, March 2006
- Brzovic, Peter S.; Lissounov, Alexei; Christensen, Devin E.
- Molecular Cell, Vol. 21, Issue 6
Rapid E2-E3 Assembly and Disassembly Enable Processive Ubiquitylation of Cullin-RING Ubiquitin Ligase Substrates
journal, November 2009
- Kleiger, Gary; Saha, Anjanabha; Lewis, Steven
- Cell, Vol. 139, Issue 5
APC2 Cullin Protein and APC11 RING Protein Comprise the Minimal Ubiquitin Ligase Module of the Anaphase-promoting Complex
journal, December 2001
- Tang, Zhanyun; Li, Bing; Bharadwaj, Rajnish
- Molecular Biology of the Cell, Vol. 12, Issue 12
The ABBA Motif Binds APC/C Activators and Is Shared by APC/C Substrates and Regulators
journal, February 2015
- Di Fiore, Barbara; Davey, Norman E.; Hagting, Anja
- Developmental Cell, Vol. 32, Issue 3
RING Domain E3 Ubiquitin Ligases
journal, June 2009
- Deshaies, Raymond J.; Joazeiro, Claudio A. P.
- Annual Review of Biochemistry, Vol. 78, Issue 1
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019
- Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman
- Nature Communications, Vol. 10, Issue 1
Rapid E2-E3 Assembly and Disassembly Enable Processive Ubiquitylation of Cullin-RING Ubiquitin Ligase Substrates
text, January 2009
- Anjanabha, Saha,; J., Deshaies, Raymond; Steven, Lewis,
- The University of North Carolina at Chapel Hill University Libraries
Mechanism of ubiquitin ligation and lysine prioritization by a HECT E3
text, January 2013
- A., Schulman, Brenda; Marcelo, Actis,; M., Lewis, Steven
- The University of North Carolina at Chapel Hill University Libraries
Crystal structure of the PRC1 ubiquitylation module bound to the nucleosome
text, January 2014
- S., Tan,; R. C., Henrici,; R. K., McGinty,
- Nature Publishing Group
Works referencing / citing this record:
Specific targeting of the deubiquitinase and E3 ligase families with engineered ubiquitin variants: Gorelik and Sidhu
journal, November 2016
- Gorelik, Maryna; Sidhu, Sachdev S.
- Bioengineering & Translational Medicine, Vol. 2, Issue 1
Detection and Analysis of Cell Cycle-Associated APC/C-Mediated Cellular Ubiquitylation In Vitro and In Vivo
book, September 2016
- Cedeño, Cesyen; La Monaca, Esther; Esposito, Mara
- Methods in Molecular Biology
E2 enzymes: more than just middle men
journal, March 2016
- Stewart, Mikaela D.; Ritterhoff, Tobias; Klevit, Rachel E.
- Cell Research, Vol. 26, Issue 4
The increasing complexity of the ubiquitin code
journal, May 2016
- Yau, Richard; Rape, Michael
- Nature Cell Biology, Vol. 18, Issue 6
Structural insights into the catalysis and regulation of E3 ubiquitin ligases
journal, August 2016
- Buetow, Lori; Huang, Danny T.
- Nature Reviews Molecular Cell Biology, Vol. 17, Issue 10
Mechanisms and functions of ribosome-associated protein quality control
journal, April 2019
- Joazeiro, Claudio A. P.
- Nature Reviews Molecular Cell Biology, Vol. 20, Issue 6
biGBac enables rapid gene assembly for the expression of large multisubunit protein complexes
journal, April 2016
- Weissmann, Florian; Petzold, Georg; VanderLinden, Ryan
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 19
Design Principles Involving Protein Disorder Facilitate Specific Substrate Selection and Degradation by the Ubiquitin-Proteasome System
journal, February 2016
- Guharoy, Mainak; Bhowmick, Pallab; Tompa, Peter
- Journal of Biological Chemistry, Vol. 291, Issue 13
RETRACTED ARTICLE: Role of oxidative stress in Retinitis pigmentosa: new involved pathways by an RNA-Seq analysis
journal, December 2018
- Donato, Luigi; Scimone, Concetta; Nicocia, Giacomo
- Cell Cycle, Vol. 18, Issue 1
Insights into APC/C: from cellular function to diseases and therapeutics
journal, March 2016
- Zhou, Zhuan; He, Mingjing; Shah, Anil A.
- Cell Division, Vol. 11, Issue 1
Mechanisms for the temporal regulation of substrate ubiquitination by the anaphase-promoting complex/cyclosome
journal, December 2019
- Bansal, Shivangee; Tiwari, Swati
- Cell Division, Vol. 14, Issue 1
Cezanne/ OTUD 7B is a cell cycle‐regulated deubiquitinase that antagonizes the degradation of APC /C substrates
journal, July 2018
- Bonacci, Thomas; Suzuki, Aussie; Grant, Gavin D.
- The EMBO Journal, Vol. 37, Issue 16
Enzymatic Logic of Ubiquitin Chain Assembly
journal, July 2019
- Deol, Kirandeep K.; Lorenz, Sonja; Strieter, Eric R.
- Frontiers in Physiology, Vol. 10
Sumoylation promotes optimal APC/C activation and timely anaphase
journal, March 2018
- Lee, Christine C.; Li, Bing; Yu, Hongtao
- eLife, Vol. 7
Molecular basis of APC/C regulation by the spindle assembly checkpoint
journal, August 2016
- Alfieri, Claudio; Chang, Leifu; Zhang, Ziguo
- Nature, Vol. 536, Issue 7617
Mechanism of APC/C CDC20 activation by mitotic phosphorylation
journal, April 2016
- Qiao, Renping; Weissmann, Florian; Yamaguchi, Masaya
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 19
Visualizing the complex functions and mechanisms of the anaphase promoting complex/cyclosome (APC/C)
journal, November 2017
- Alfieri, Claudio; Zhang, Suyang; Barford, David
- Open Biology, Vol. 7, Issue 11
Quantifying the heterogeneity of macromolecular machines by mass photometry
journal, April 2020
- Sonn-Segev, Adar; Belacic, Katarina; Bodrug, Tatyana
- Nature Communications, Vol. 11, Issue 1
Atomic-Resolution Structures of the APC/C Subunits Apc4 and the Apc5 N-Terminal Domain
journal, October 2015
- Cronin, Nora B.; Yang, Jing; Zhang, Ziguo
- Journal of Molecular Biology, Vol. 427, Issue 20
Structural Basis of BRCC36 Function in DNA Repair and Immune Regulation
journal, August 2019
- Rabl, Julius; Bunker, Richard D.; Schenk, Andreas D.
- Molecular Cell, Vol. 75, Issue 3
Ubiquitin-like Protein Conjugation: Structures, Chemistry, and Mechanism
journal, February 2017
- Cappadocia, Laurent; Lima, Christopher D.
- Chemical Reviews, Vol. 118, Issue 3
Molecular basis of APC/C regulation by the spindle assembly checkpoint
journal, August 2016
- Alfieri, Claudio; Chang, Leifu; Zhang, Ziguo
- Nature, Vol. 536, Issue 7617
Specificity and disease in the ubiquitin system
journal, February 2016
- Chaugule, Viduth K.; Walden, Helen
- Biochemical Society Transactions, Vol. 44, Issue 1
Visualizing the complex functions and mechanisms of the anaphase promoting complex/cyclosome (APC/C)
journal, November 2017
- Alfieri, Claudio; Zhang, Suyang; Barford, David
- Open Biology, Vol. 7, Issue 11
Insights into APC/C: from cellular function to diseases and therapeutics
journal, March 2016
- Zhou, Zhuan; He, Mingjing; Shah, Anil A.
- Cell Division, Vol. 11, Issue 1
Mechanisms for the temporal regulation of substrate ubiquitination by the anaphase-promoting complex/cyclosome
journal, December 2019
- Bansal, Shivangee; Tiwari, Swati
- Cell Division, Vol. 14, Issue 1
Synergistic inhibition of the APC/C by the removal of APC15 in HCT116 cells lacking UBE2C
journal, September 2016
- Garvanska, Dimitriya H.; Larsen, Marie Sofie Yoo; Nilsson, Jakob
- Biology Open, Vol. 5, Issue 10
Dual RING E3 Architectures Regulate Multiubiquitination and Ubiquitin Chain Elongation by APC/C
text, January 2016
- A., Jarvis, Marc; David, Yanishevski,; G., Brown, Nicholas
- The University of North Carolina at Chapel Hill University Libraries
The mitotic checkpoint complex (MCC): looking back and forth after 15 years
journal, January 2016
- Liu, Song-Tao; Zhang, Hang
- AIMS Molecular Science, Vol. 3, Issue 4