Structural insights into E1 recognition and the ubiquitin-conjugating activity of the E2 enzyme Cdc34

Williams, Katelyn M.; Qie, Shuo; Atkison, James H.; Salazar-Arango, Sabrina; Alan Diehl, J.; Olsen, Shaun K.

doi:10.1038/s41467-019-11061-8

Title: Structural insights into E1 recognition and the ubiquitin-conjugating activity of the E2 enzyme Cdc34

Journal Article · Wed Jul 24 00:00:00 EDT 2019 · Nature Communications

DOI:https://doi.org/10.1038/s41467-019-11061-8· OSTI ID:1557318

Williams, Katelyn M. ^[1]; Qie, Shuo ^[1]; Atkison, James H. ^[1]; Salazar-Arango, Sabrina ^[1];

^[1];

^[1]

Medical Univ. of South Carolina, Charleston, SC (United States)

Ubiquitin (Ub) signaling requires the sequential interactions and activities of three enzymes, E1, E2, and E3. Cdc34 is an E2 that plays a key role in regulating cell cycle progression and requires unique structural elements to function. The molecular basis by which Cdc34 engages its E1 and the structural mechanisms by which its unique C-terminal extension functions in Cdc34 activity are unknown. Here, we present crystal structures of Cdc34 alone and in complex with E1, and a Cdc34~Ub thioester mimetic that represents the product of Uba1-Cdc34 Ub transthiolation. These structures reveal conformational changes in Uba1 and Cdc34 and a unique binding mode that are required for transthiolation. The Cdc34~Ub structure reveals contacts between the Cdc34 C-terminal extension and Ub that stabilize Cdc34~Ub in a closed conformation and are critical for Ub discharge. Altogether, our structural, biochemical, and cell-based studies provide insights into the molecular mechanisms by which Cdc34 function in cells.

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

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH); Abney Foundation

Grant/Contract Number:: AC02-06CH11357; S10 RR029205; S10 RR027139-01; NIH R01 GM115568; R01 GM128731; NIH P01 CA098101; R01 CA093237; NIH F30 CA216921; NIH T32 CA193201; NIH T32 DE017551

OSTI ID:: 1557318

Journal Information:: Nature Communications, Vol. 10, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 26 works

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References (69)

An Allosteric Inhibitor of the Human Cdc34 Ubiquitin-Conjugating Enzyme Ceccarelli, Derek F.; Tang, Xiaojing; Pelletier, Benoit Cell, Vol. 145, Issue 7 https://doi.org/10.1016/j.cell.2011.05.039	journal	June 2011
Mechanism of Lysine 48-Linked Ubiquitin-Chain Synthesis by the Cullin-RING Ubiquitin-Ligase Complex SCF-Cdc34 Petroski, Matthew D.; Deshaies, Raymond J. Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.033	journal	December 2005
The human ubiquitin-conjugating enzyme Cdc34 controls cellular proliferation through regulation of p27Kip1 protein levels Butz, Nicole; Ruetz, Stephan; Natt, Francois Experimental Cell Research, Vol. 303, Issue 2 https://doi.org/10.1016/j.yexcr.2004.10.008	journal	February 2005
Rbx1, a Component of the VHL Tumor Suppressor Complex and SCF Ubiquitin Ligase Kamura, T. Science, Vol. 284, Issue 5414 https://doi.org/10.1126/science.284.5414.657	journal	April 1999
E2 enzyme inhibition by stabilization of a low-affinity interface with ubiquitin Huang, Hao; Ceccarelli, Derek F.; Orlicky, Stephen Nature Chemical Biology, Vol. 10, Issue 2 https://doi.org/10.1038/nchembio.1412	journal	December 2013
Small molecule therapeutics targeting F-box proteins in cancer Liu, Yuan; Mallampalli, Rama K. Seminars in Cancer Biology, Vol. 36 https://doi.org/10.1016/j.semcancer.2015.09.014	journal	February 2016
Suramin inhibits cullin-RING E3 ubiquitin ligases Wu, Kenneth; Chong, Robert A.; Yu, Qing Proceedings of the National Academy of Sciences, Vol. 113, Issue 14 https://doi.org/10.1073/pnas.1601089113	journal	March 2016
Structural Basis for Recruitment of Ubc12 by an E2 Binding Domain in NEDD8's E1 Huang, Danny T.; Paydar, Amir; Zhuang, Min Molecular Cell, Vol. 17, Issue 3 https://doi.org/10.1016/j.molcel.2004.12.020	journal	February 2005
Insights into Ubiquitin Transfer Cascades from a Structure of a UbcH5B∼Ubiquitin-HECTNEDD4L Complex Kamadurai, Hari B.; Souphron, Judith; Scott, Daniel C. Molecular Cell, Vol. 36, Issue 6 https://doi.org/10.1016/j.molcel.2009.11.010	journal	December 2009
Identification of a portable determinant of cell cycle function within the carboxyl-terminal domain of the yeast CDC34 (UBC3) ubiquitin conjugating (E2) enzyme. Kolman, C. J.; Toth, J.; Gonda, D. K. The EMBO Journal, Vol. 11, Issue 8 https://doi.org/10.1002/j.1460-2075.1992.tb05380.x	journal	August 1992
MolProbity: More and better reference data for improved all-atom structure validation: PROTEIN SCIENCE.ORG Williams, Christopher J.; Headd, Jeffrey J.; Moriarty, Nigel W. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3330	journal	November 2017
SIC1 is ubiquitinated in vitro by a pathway that requires CDC4, CDC34, and cyclin/CDK activities. Verma, R.; Feldman, R. M.; Deshaies, R. J. Molecular Biology of the Cell, Vol. 8, Issue 8 https://doi.org/10.1091/mbc.8.8.1427	journal	August 1997
The yeast cell cycle gene CDC34 encodes a ubiquitin-conjugating enzyme Goebl, M.; Yochem, J.; Jentsch, S. Science, Vol. 241, Issue 4871 https://doi.org/10.1126/science.2842867	journal	September 1988
Phosphorylation- and ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor Far1p in budding yeast Henchoz, S.; Chi, Y.; Catarin, B. Genes & Development, Vol. 11, Issue 22 https://doi.org/10.1101/gad.11.22.3046	journal	November 1997
Structure of a Conjugating Enzyme-Ubiquitin Thiolester Intermediate Reveals a Novel Role for the Ubiquitin Tail Hamilton, Katherine S.; Ellison, Michael J.; Barber, Kathryn R. Structure, Vol. 9, Issue 10 https://doi.org/10.1016/S0969-2126(01)00657-8	journal	October 2001
Structural Insights into the Conformation and Oligomerization of E2∼Ubiquitin Conjugates Page, Richard C.; Pruneda, Jonathan N.; Amick, Joseph Biochemistry, Vol. 51, Issue 20 https://doi.org/10.1021/bi300058m	journal	May 2012
Phenotype-directed analysis of genotype in early-onset, familial breast cancers Price, Gareth R.; Armes, Jane E.; Ramus, Susan J. Pathology, Vol. 38, Issue 6 https://doi.org/10.1080/00313020601024052	journal	December 2006
Insights into SCF ubiquitin ligases from the structure of the Skp1–Skp2 complex Schulman, Brenda A.; Carrano, Andrea C.; Jeffrey, Philip D. Nature, Vol. 408, Issue 6810 https://doi.org/10.1038/35042620	journal	November 2000
BIRC7–E2 ubiquitin conjugate structure reveals the mechanism of ubiquitin transfer by a RING dimer Dou, Hao; Buetow, Lori; Sibbet, Gary J. Nature Structural & Molecular Biology, Vol. 19, Issue 9 https://doi.org/10.1038/nsmb.2379	journal	August 2012
The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae Schwob, E. Cell, Vol. 79, Issue 2 https://doi.org/10.1016/0092-8674(94)90193-7	journal	October 1994
The Nedd8-conjugated ROC1-CUL1 Core Ubiquitin Ligase Utilizes Nedd8 Charged Surface Residues for Efficient Polyubiquitin Chain Assembly Catalyzed by Cdc34 Wu, Kenneth; Chen, Angus; Tan, Peilin Journal of Biological Chemistry, Vol. 277, Issue 1 https://doi.org/10.1074/jbc.M108008200	journal	October 2001
Control of cell cycle-dependent degradation of c-Ski proto-oncoprotein by Cdc34 Macdonald, Mara; Wan, Yong; Wang, Wei Oncogene, Vol. 23, Issue 33 https://doi.org/10.1038/sj.onc.1207733	journal	May 2004
Blockade of ubiquitin-conjugating enzyme CDC34 enhances anti-myeloma activity of Bortezomib/Proteasome inhibitor PS-341 Chauhan, Dharminder; Li, Guilan; Hideshima, Teru Oncogene, Vol. 23, Issue 20 https://doi.org/10.1038/sj.onc.1207458	journal	April 2004
δ-Catenin promotes prostate cancer cell growth and progression by altering cell cycle and survival gene profiles Zeng, Yan; Abdallah, Agustin; Lu, Jian-Ping Molecular Cancer, Vol. 8, Issue 1 https://doi.org/10.1186/1476-4598-8-19	journal	January 2009
Structure of the Cul1–Rbx1–Skp1–F boxSkp2 SCF ubiquitin ligase complex Zheng, Ning; Schulman, Brenda A.; Song, Langzhou Nature, Vol. 416, Issue 6882 https://doi.org/10.1038/416703a	journal	April 2002
Cell division cycle 34 is highly expressed in hepatitis C virus-positive hepatocellular carcinoma with favorable phenotypes Takagi, Keiko; Takayama, Tadatoshi; Midorikawa, Yutaka Biomedical Reports, Vol. 7, Issue 1 https://doi.org/10.3892/br.2017.912	journal	May 2017
Essential Role for Ubiquitin-Ubiquitin-Conjugating Enzyme Interaction in Ubiquitin Discharge from Cdc34 to Substrate Saha, Anjanabha; Lewis, Steven; Kleiger, Gary Molecular Cell, Vol. 42, Issue 1 https://doi.org/10.1016/j.molcel.2011.03.016	journal	April 2011
Crystal structure of a human ubiquitin E1–ubiquitin complex reveals conserved functional elements essential for activity Lv, Zongyang; Williams, Katelyn M.; Yuan, Lingmin Journal of Biological Chemistry, Vol. 293, Issue 47 https://doi.org/10.1074/jbc.RA118.003975	journal	October 2018
The mechanism of OTUB1-mediated inhibition of ubiquitination Wiener, Reuven; Zhang, Xiangbin; Wang, Tao Nature, Vol. 483, Issue 7391 https://doi.org/10.1038/nature10911	journal	February 2012
Immunochemical analysis of the turnover of ubiquitin-protein conjugates in intact cells. Relationship to the breakdown of abnormal proteins. Hershko, A.; Eytan, E.; Ciechanover, A. Journal of Biological Chemistry, Vol. 257, Issue 23 https://doi.org/10.1016/S0021-9258(19)45327-1	journal	December 1982
Degradation of B-Myb by ubiquitin-mediated proteolysis: involvement of the Cdc34-SCFp45Skp2 pathway Charrasse, S.; Carena, I.; Brondani, V. Oncogene, Vol. 19, Issue 26 https://doi.org/10.1038/sj.onc.1203618	journal	June 2000
Structural Insights into E1-Catalyzed Ubiquitin Activation and Transfer to Conjugating Enzymes Lee, Imsang; Schindelin, Hermann Cell, Vol. 134, Issue 2 https://doi.org/10.1016/j.cell.2008.05.046	journal	July 2008
Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1 Lois, Luisa Maria; Lima, Christopher D. The EMBO Journal, Vol. 24, Issue 3 https://doi.org/10.1038/sj.emboj.7600552	journal	January 2005
Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB–MoaD complex Lake, Michael W.; Wuebbens, Margot M.; Rajagopalan, K. V. Nature, Vol. 414, Issue 6861 https://doi.org/10.1038/35104586	journal	November 2001
Basis for a ubiquitin-like protein thioester switch toggling E1–E2 affinity Huang, Danny T.; Hunt, Harold W.; Zhuang, Min Nature, Vol. 445, Issue 7126 https://doi.org/10.1038/nature05490	journal	January 2007
Functional and physical characterization of the cell cycle ubiquitin-conjugating enzyme CDC34 (UBC3). Identification of a functional determinant within the tail that facilitates CDC34 self-association Ptak, C.; Prendergast, J. A.; Hodgins, R. Journal of Biological Chemistry, Vol. 269, Issue 42 https://doi.org/10.1016/S0021-9258(18)47228-6	journal	October 1994
Structure of a Ubiquitin E1-E2 Complex: Insights to E1-E2 Thioester Transfer Olsen, Shaun K.; Lima, Christopher D. Molecular Cell, Vol. 49, Issue 5 https://doi.org/10.1016/j.molcel.2013.01.013	journal	March 2013
The Acidic Tail of the Cdc34 Ubiquitin-conjugating Enzyme Functions in Both Binding to and Catalysis with Ubiquitin Ligase SCF ^Cdc4 Kleiger, Gary; Hao, Bing; Mohl, Dane A. Journal of Biological Chemistry, Vol. 284, Issue 52 https://doi.org/10.1074/jbc.M109.058529	journal	October 2009
The Human Cdc34 Carboxyl Terminus Contains a Non-covalent Ubiquitin Binding Activity That Contributes to SCF-dependent Ubiquitination Choi, Yun-Seok; Wu, Kenneth; Jeong, Kwiwan Journal of Biological Chemistry, Vol. 285, Issue 23 https://doi.org/10.1074/jbc.M109.090621	journal	March 2010
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
Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34 Seol, J. H.; Feldman, R. M. R.; Zachariae, W. Genes & Development, Vol. 13, Issue 12 https://doi.org/10.1101/gad.13.12.1614	journal	June 1999
Structure of an E3:E2∼Ub Complex Reveals an Allosteric Mechanism Shared among RING/U-box Ligases Pruneda, Jonathan N.; Littlefield, Peter J.; Soss, Sarah E. Molecular Cell, Vol. 47, Issue 6 https://doi.org/10.1016/j.molcel.2012.07.001	journal	September 2012
The molecular basis of lysine 48 ubiquitin chain synthesis by Ube2K Middleton, Adam J.; Day, Catherine L. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16793	journal	November 2015
Enhanced expression of mRNAs of antisecretory factor-1, gp96, DAD1 and CDC34 in human hepatocellular carcinomas Tanaka, Kenji; Kondoh, Nobuo; Shuda, Masahiro Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1536, Issue 1 https://doi.org/10.1016/S0925-4439(01)00026-6	journal	April 2001
Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis Plechanovová, Anna; Jaffray, Ellis G.; Tatham, Michael H. Nature, Vol. 489, Issue 7414 https://doi.org/10.1038/nature11376	journal	July 2012
Molecular mechanism of a covalent allosteric inhibitor of SUMO E1 activating enzyme Lv, Zongyang; Yuan, Lingmin; Atkison, James H. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07015-1	journal	December 2018
The Mechanism of Linkage-Specific Ubiquitin Chain Elongation by a Single-Subunit E2 Wickliffe, Katherine E.; Lorenz, Sonja; Wemmer, David E. Cell, Vol. 144, Issue 5 https://doi.org/10.1016/j.cell.2011.01.035	journal	March 2011
Ubiquitin conjugation by the yeast RAD6 and CDC34 gene products. Comparison to their putative rabbit homologs, E2(20K) AND E2(32K). Haas, A. L.; Reback, P. B.; Chau, V. Journal of Biological Chemistry, Vol. 266, Issue 8 https://doi.org/10.1016/S0021-9258(19)67761-6	journal	March 1991
Rapid E2-E3 Assembly and Disassembly Enable Processive Ubiquitylation of Cullin-RING Ubiquitin Ligase Substrates Kleiger, Gary; Saha, Anjanabha; Lewis, Steven Cell, Vol. 139, Issue 5 https://doi.org/10.1016/j.cell.2009.10.030	journal	November 2009
Novel CDC34 (UBC3) ubiquitin-conjugating enzyme mutants obtained by charge-to-alanine scanning mutagenesis. Pitluk, Z. W.; McDonough, M.; Sangan, P. Molecular and Cellular Biology, Vol. 15, Issue 3 https://doi.org/10.1128/MCB.15.3.1210	journal	March 1995
Mechanism of Lysine 48 Selectivity during Polyubiquitin Chain Formation by the Ube2R1/2 Ubiquitin-Conjugating Enzyme Hill, Spencer; Harrison, Joseph S.; Lewis, Steven M. Molecular and Cellular Biology, Vol. 36, Issue 11 https://doi.org/10.1128/MCB.00097-16	journal	April 2016
Structural insights into the mechanism and E2 specificity of the RBR E3 ubiquitin ligase HHARI Yuan, Lingmin; Lv, Zongyang; Atkison, James H. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00272-6	journal	August 2017
THE ROLE OF S. CEREVISIAE CELL DIVISION CYCLE GENES IN NUCLEAR FUSION Dutcher, Susan K.; Hartwell, Leland H. Genetics, Vol. 100, Issue 2 https://doi.org/10.1093/genetics/100.2.175	journal	February 1982
S. pombe Uba1-Ubc15 Structure Reveals a Novel Regulatory Mechanism of Ubiquitin E2 Activity Lv, Zongyang; Rickman, Kimberly A.; Yuan, Lingmin Molecular Cell, Vol. 65, Issue 4 https://doi.org/10.1016/j.molcel.2017.01.008	journal	February 2017
Molecular and structural insight into lysine selection on substrate and ubiquitin lysine 48 by the ubiquitin-conjugating enzyme Cdc34 Suryadinata, Randy; Holien, Jessica K.; Yang, George Cell Cycle, Vol. 12, Issue 11 https://doi.org/10.4161/cc.24818	journal	June 2013
Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27 Pagano, M.; Tam, S.; Theodoras, A. Science, Vol. 269, Issue 5224 https://doi.org/10.1126/science.7624798	journal	August 1995
Association of the Disordered C-terminus of CDC34 with a Catalytically Bound Ubiquitin Spratt, Donald E.; Shaw, Gary S. Journal of Molecular Biology, Vol. 407, Issue 3 https://doi.org/10.1016/j.jmb.2011.01.047	journal	April 2011
The Structure of the APPBP1-UBA3-NEDD8-ATP Complex Reveals the Basis for Selective Ubiquitin-like Protein Activation by an E1 Walden, Helen; Podgorski, Michael S.; Huang, Danny T. Molecular Cell, Vol. 12, Issue 6 https://doi.org/10.1016/s1097-2765(03)00452-0	journal	December 2003
E1-E2 Interactions in Ubiquitin and Nedd8 Ligation Pathways Tokgöz, Zeynep; Siepmann, Thomas J.; Streich, Frederick Journal of Biological Chemistry, Vol. 287, Issue 1 https://doi.org/10.1074/jbc.m111.294975	journal	November 2011
Ubiquitin-conjugating Enzyme Cdc34 and Ubiquitin Ligase Skp1-Cullin-F-box Ligase (SCF) Interact through Multiple Conformations Sandoval, Daniella; Hill, Spencer; Ziemba, Amy Journal of Biological Chemistry, Vol. 290, Issue 2 https://doi.org/10.1074/jbc.m114.615559	journal	November 2014
Domain alternation and active site remodeling are conserved structural features of ubiquitin E1 Lv, Zongyang; Yuan, Lingmin; Atkison, James H. Journal of Biological Chemistry, Vol. 292, Issue 29 https://doi.org/10.1074/jbc.m117.787622	journal	June 2017
Crystal Structure of a Fragment of Mouse Ubiquitin-activating Enzyme Szczepanowski, Roman H.; Filipek, Renata; Bochtler, Matthias Journal of Biological Chemistry, Vol. 280, Issue 23 https://doi.org/10.1074/jbc.m502583200	journal	March 2005
Cdc34-mediated Degradation of ATF5 Is Blocked by Cisplatin Wei, Yuanyan; Jiang, Jianhai; Liu, Dan Journal of Biological Chemistry, Vol. 283, Issue 27 https://doi.org/10.1074/jbc.m707879200	journal	May 2008
Structural insights into non-covalent ubiquitin activation of the cIAP1-UbcH5B∼ubiquitin complex Patel, Amrita; Sibbet, Gary J.; Huang, Danny T. Journal of Biological Chemistry, Vol. 294, Issue 4 https://doi.org/10.1074/jbc.ra118.006045	journal	December 2018
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
Cdc53p acts in concert with Cdc4p and Cdc34p to control the G1-to-S-phase transition and identifies a conserved family of proteins. Mathias, N.; Johnson, S. L.; Winey, M. Molecular and Cellular Biology, Vol. 16, Issue 12 https://doi.org/10.1128/mcb.16.12.6634	journal	December 1996
Mechanism of Lysine 48 Selectivity during Polyubiquitin Chain Formation by the Ube2R1/2 Ubiquitin-Conjugating Enzyme M., Lewis, Steven; S., Harrison, Joseph; Brian, Kuhlman, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/sn40-p981	text	January 2016
Essential Role for Ubiquitin-Ubiquitin-Conjugating Enzyme Interaction in Ubiquitin Discharge from Cdc34 to Substrate Brian, Kuhlman,; Steven, Lewis,; J., Deshaies, Raymond The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/wjgb-mn48	text	January 2011
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010

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