Heat activates the AAA+ HslUV protease by melting an axial autoinhibitory plug

Baytshtok, Vladimir; Fei, Xue; Shih, Tsai-Ting; Grant, Robert A.; Santos, Justin C.; Baker, Tania A.; Sauer, Robert T.

doi:10.1016/j.celrep.2020.108639

Heat activates the AAA+ HslUV protease by melting an axial autoinhibitory plug

Journal Article · Tue Jan 19 00:00:00 EST 2021 · Cell Reports

DOI:https://doi.org/10.1016/j.celrep.2020.108639· OSTI ID:1763080

Baytshtok, Vladimir ^[1]; Fei, Xue ^[2]; Shih, Tsai-Ting ^[2]; Grant, Robert A. ^[2]; Santos, Justin C. ^[3]; Baker, Tania A. ^[2]; Sauer, Robert T. ^[2]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Memorial Sloan Kettering Cancer Center, New York, NY (United States). Sloan Kettering Institute
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Emory University School of Medicine, Atlanta, GA (United States)

At low temperatures, protein degradation by the AAA+ HslUV protease is very slow. New crystal structures reveal that residues in the intermediate domain of the HslU₆ unfoldase can plug its axial channel, blocking productive substrate binding and subsequent unfolding, translocation, and degradation by the HslV₁₂ peptidase. Biochemical experiments with wild-type and mutant enzymes support a model in which heat-induced melting of this autoinhibitory plug activates HslUV proteolysis.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1763080

Journal Information:: Cell Reports, Journal Name: Cell Reports Journal Issue: 3 Vol. 34; ISSN 2211-1247

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (21)

The I domain of the AAA+ HslUV protease coordinates substrate binding, ATP hydrolysis, and protein degradation: The I Domain Coordinates Substrate Binding and ATP Hydrolysis Sundar, Shankar; Baker, Tania A.; Sauer, Robert T. Protein Science, Vol. 21, Issue 2 https://doi.org/10.1002/pro.2001	journal	January 2012
UCSF ChimeraX: Meeting modern challenges in visualization and analysis: UCSF ChimeraX Visualization System Goddard, Thomas D.; Huang, Conrad C.; Meng, Elaine C. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3235	journal	September 2017
P22 Arc repressor: Enhanced expression of unstable mutants by addition of polar C-terminal sequences Milla, Marcos E.; Brown, Bronwen M.; Sauer, Robert T. Protein Science, Vol. 2, Issue 12 https://doi.org/10.1002/pro.5560021219	journal	December 1993
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Crystal and Solution Structures of an HslUV Protease–Chaperone Complex Sousa, Marcelo C.; Trame, Christine B.; Tsuruta, Hiro Cell, Vol. 103, Issue 4 https://doi.org/10.1016/S0092-8674(00)00166-5	journal	November 2000
Nucleotide-Dependent Conformational Changes in a Protease-Associated ATPase HslU Wang, J.; Song, J. J.; Seong, I. S. Structure, Vol. 9, Issue 11 https://doi.org/10.1016/S0969-2126(01)00670-0	journal	November 2001
Accurate determination of local defocus and specimen tilt in electron microscopy Mindell, Joseph A.; Grigorieff, Nikolaus Journal of Structural Biology, Vol. 142, Issue 3 https://doi.org/10.1016/S1047-8477(03)00069-8	journal	June 2003
Asymmetric Nucleotide Transactions of the HslUV Protease Yakamavich, Joseph A.; Baker, Tania A.; Sauer, Robert T. Journal of Molecular Biology, Vol. 380, Issue 5 https://doi.org/10.1016/j.jmb.2008.05.070	journal	July 2008
EMAN2: An extensible image processing suite for electron microscopy Tang, Guang; Peng, Liwei; Baldwin, Philip R. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.009	journal	January 2007
RELION: Implementation of a Bayesian approach to cryo-EM structure determination Scheres, Sjors H. W. Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530 https://doi.org/10.1016/j.jsb.2012.09.006	journal	December 2012
A Structurally Dynamic Region of the HslU Intermediate Domain Controls Protein Degradation and ATP Hydrolysis Baytshtok, Vladimir; Fei, Xue; Grant, Robert A. Structure, Vol. 24, Issue 10 https://doi.org/10.1016/j.str.2016.08.012	journal	October 2016
The structures of HslU and the ATP-dependent protease HslU–HslV Bochtler, Matthias; Hartmann, Claudia; Song, Hyun Kyu Nature, Vol. 403, Issue 6771 https://doi.org/10.1038/35001629	journal	February 2000
The ATP-dependent HslVU protease from Escherichia coli is a four-ring structure resembling the proteasome Rohrwild, Markus; Pfeifer, Günter; Santarius, Ute Nature Structural Biology, Vol. 4, Issue 2 https://doi.org/10.1038/nsb0297-133	journal	February 1997
Nucleotide-dependent substrate recognition by the AAA+ HslUV protease Burton, Randall E.; Baker, Tania A.; Sauer, Robert T. Nature Structural & Molecular Biology, Vol. 12, Issue 3 https://doi.org/10.1038/nsmb898	journal	February 2005
HslV-HslU: A novel ATP-dependent protease complex in Escherichia coli related to the eukaryotic proteasome. Rohrwild, M.; Coux, O.; Huang, H. C. Proceedings of the National Academy of Sciences, Vol. 93, Issue 12 https://doi.org/10.1073/pnas.93.12.5808	journal	June 1996
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
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 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
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
AAA+ Proteases: ATP-Fueled Machines of Protein Destruction Sauer, Robert T.; Baker, Tania A. Annual Review of Biochemistry, Vol. 80, Issue 1 https://doi.org/10.1146/annurev-biochem-060408-172623	journal	July 2011

Similar Records

Covalently linked HslU hexamers support a probabilistic mechanism that links ATP hydrolysis to protein unfolding and translocation

Journal Article · Mon Feb 20 19:00:00 EST 2017 · Journal of Biological Chemistry · OSTI ID:1430301

A Structurally Dynamic Region of the HslU Intermediate Domain Controls Protein Degradation and ATP Hydrolysis

Journal Article · Wed Sep 21 20:00:00 EDT 2016 · Structure · OSTI ID:1398095

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
ATP-dependent degradation
heat shock locus
proteolytic regulation
temperature control

Heat activates the AAA+ HslUV protease by melting an axial autoinhibitory plug

Citation Formats

References (21)

Similar Records

Related Subjects