Phospho‐dependent signaling during the general stress response by the atypical response regulator and ClpXP adaptor RssB

Schwartz, Jacob; Son, Jonghyeon; Brugger, Christiane; Deaconescu, Alexandra M.

doi:10.1002/pro.4047

Title: Phospho‐dependent signaling during the general stress response by the atypical response regulator and ClpXP adaptor RssB

Journal Article · 28 February 2021 · Protein Science

DOI: https://doi.org/10.1002/pro.4047 · OSTI ID:1780164

Schwartz, Jacob ^[1]; Son, Jonghyeon ^[1]; Brugger, Christiane ^[1];

^[1]

Department of Molecular Biology, Cell Biology and Biochemistry Laboratories of Molecular Medicine Brown University Providence Rhode Island USA

Abstract In the model organism Escherichia coli and related species, the general stress response relies on tight regulation of the intracellular levels of the promoter specificity subunit RpoS. RpoS turnover is exclusively dependent on RssB, a two‐domain response regulator that functions as an adaptor that delivers RpoS to ClpXP for proteolysis. Here, we report crystal structures of the receiver domain of RssB both in its unphosphorylated form and bound to the phosphomimic BeF ₃ ⁻ . Surprisingly, we find only modest differences between these two structures, suggesting that truncating RssB may partially activate the receiver domain to a “meta‐active” state. Our structural and sequence analysis points to RssB proteins not conforming to either the Y–T coupling scheme for signaling seen in prototypical response regulators, such as CheY, or to the signaling model of the less understood FATGUY proteins.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1780164

Journal Information:: Protein Science, Journal Name: Protein Science Journal Issue: 4 Vol. 30; ISSN 0961-8368

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (40)

The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli. Muffler, A.; Fischer, D.; Altuvia, S. The EMBO Journal, Vol. 15, Issue 6 https://doi.org/10.1002/j.1460-2075.1996.tb00475.x	journal	March 1996
NMR structure of activated CheY Cho, Ho S.; Lee, Seok-Yong; Yan, Dalai Journal of Molecular Biology, Vol. 297, Issue 3 https://doi.org/10.1006/jmbi.2000.3595	journal	March 2000
Crystal structure of Escherichia coli CheY refined at 1.7-A resolution Volz, K.; Matsumura, P. Journal of Biological Chemistry, Vol. 266, Issue 23 https://doi.org/10.1016/S0021-9258(18)98646-1	journal	August 1991
Survey of the number of two-component response regulator genes in the complete and annotated genome sequences of prokaryotes Ashby, Mark K. FEMS Microbiology Letters, Vol. 231, Issue 2 https://doi.org/10.1016/S0378-1097(04)00004-7	journal	February 2004
Transient Non-native Hydrogen Bonds Promote Activation of a Signaling Protein Gardino, Alexandra K.; Villali, Janice; Kivenson, Aleksandr Cell, Vol. 139, Issue 6 https://doi.org/10.1016/j.cell.2009.11.022	journal	December 2009
Solution Structures of the Inactive and BeF3-activated Response Regulator CheY2 Riepl, Hubert; Scharf, Birgit; Schmitt, Rüdiger Journal of Molecular Biology, Vol. 338, Issue 2 https://doi.org/10.1016/j.jmb.2004.02.054	journal	April 2004
Evidence Against the “Y–T Coupling” Mechanism of Activation in the Response Regulator NtrC Villali, Janice; Pontiggia, Francesco; Clarkson, Michael W. Journal of Molecular Biology, Vol. 426, Issue 7 https://doi.org/10.1016/j.jmb.2013.12.027	journal	April 2014
Snapshots of Conformational Changes Shed Light into the NtrX Receiver Domain Signal Transduction Mechanism Fernández, Ignacio; Otero, Lisandro H.; Klinke, Sebastián Journal of Molecular Biology, Vol. 427, Issue 20 https://doi.org/10.1016/j.jmb.2015.06.010	journal	October 2015
RssB-mediated σS Activation is Regulated by a Two-Tier Mechanism via Phosphorylation and Adaptor Protein – IraD Wang, Zhihao; Zhao, Siyu; Li, Yanqing Journal of Molecular Biology, Vol. 433, Issue 3 https://doi.org/10.1016/j.jmb.2020.166757	journal	February 2021
Molecular strategies for phosphorylation-mediated regulation of response regulator activity Gao, Rong; Stock, Ann M. Current Opinion in Microbiology, Vol. 13, Issue 2 https://doi.org/10.1016/j.mib.2009.12.009	journal	April 2010
Roles of adaptor proteins in regulation of bacterial proteolysis Battesti, Aurelia; Gottesman, Susan Current Opinion in Microbiology, Vol. 16, Issue 2 https://doi.org/10.1016/j.mib.2013.01.002	journal	April 2013
Role of the PFXFATG[G/Y] Motif in the Activation of SdrG, a Response Regulator Involved in the Alphaproteobacterial General Stress Response Campagne, Sébastien; Dintner, Sebastian; Gottschlich, Lisa Structure, Vol. 24, Issue 8 https://doi.org/10.1016/j.str.2016.05.015	journal	August 2016
Regulation of RssB-dependent proteolysis in Escherichia coli : a role for acetyl phosphate in a response regulator-controlled process Bouché, Sandrine; Klauck, Eberhard; Fischer, Daniela Molecular Microbiology, Vol. 27, Issue 4 https://doi.org/10.1046/j.1365-2958.1998.00725.x	journal	February 1998
Role of the response regulator RssB in sigmaS recognition and initiation of sigmaS proteolysis in Escherichia coli Klauck, Eberhard; Lingnau, Maren; Hengge-Aronis, Regine Molecular Microbiology, Vol. 40, Issue 6 https://doi.org/10.1046/j.1365-2958.2001.02482.x	journal	June 2001
Regulatory network of acid resistance genes in Escherichia coli: Regulatory network of acid resistance genes in E. coli Masuda, Nobuhisa; Church, George M. Molecular Microbiology, Vol. 48, Issue 3 https://doi.org/10.1046/j.1365-2958.2003.03477.x	journal	April 2003
Dynamic control of Dps protein levels by ClpXP and ClpAP proteases in Escherichia coli: Regulated proteolysis of Dps protein Stephani, Kunigunde; Weichart, Dieter; Hengge, Regine Molecular Microbiology, Vol. 49, Issue 6 https://doi.org/10.1046/j.1365-2958.2003.03644.x	journal	August 2003
Phosphorylation-dependent conformational changes and domain rearrangements in Staphylococcus aureus VraR activation Leonard, P. G.; Golemi-Kotra, D.; Stock, A. M. Proceedings of the National Academy of Sciences, Vol. 110, Issue 21 https://doi.org/10.1073/pnas.1302819110	journal	May 2013
The response regulator SprE controls the stability of RpoS. Pratt, L. A.; Silhavy, T. J. Proceedings of the National Academy of Sciences, Vol. 93, Issue 6 https://doi.org/10.1073/pnas.93.6.2488	journal	March 1996
Regulation of RpoS proteolysis in Escherichia coli: The response regulator RssB is a recognition factor that interacts with the turnover element in RpoS Becker, G.; Klauck, E.; Hengge-Aronis, R. Proceedings of the National Academy of Sciences, Vol. 96, Issue 11 https://doi.org/10.1073/pnas.96.11.6439	journal	May 1999
Crystal Structures of CheY Mutants Y106W and T87I/Y106W: CheY ACTIVATION CORRELATES WITH MOVEMENT OF RESIDUE 106 Zhu, Xiangyang; Rebello, Joseph; Matsumura, Philip Journal of Biological Chemistry, Vol. 272, Issue 8 https://doi.org/10.1074/jbc.272.8.5000	journal	February 1997
A Distinct Meta-active Conformation in the 1.1-Å Resolution Structure of Wild-type ApoCheY Simonovic, Miljan; Volz, Karl Journal of Biological Chemistry, Vol. 276, Issue 31 https://doi.org/10.1074/jbc.C100295200	journal	June 2001
Trouble is coming: Signaling pathways that regulate general stress responses in bacteria Gottesman, Susan Journal of Biological Chemistry, Vol. 294, Issue 31 https://doi.org/10.1074/jbc.REV119.005593	journal	June 2019
Conformational dynamism for DNA interaction in the Salmonella RcsB response regulator Casino, Patricia; Miguel-Romero, Laura; Huesa, Juanjo Nucleic Acids Research, Vol. 46, Issue 1 https://doi.org/10.1093/nar/gkx1164	journal	November 2017
The Pfam protein families database in 2019 El-Gebali, Sara; Mistry, Jaina; Bateman, Alex Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky995	journal	October 2018
Anti-adaptors provide multiple modes for regulation of the RssB adaptor protein Battesti, A.; Hoskins, J. R.; Tong, S. Genes & Development, Vol. 27, Issue 24 https://doi.org/10.1101/gad.229617.113	journal	December 2013
Structural basis for inhibition of a response regulator of σ ^S stability by a ClpXP antiadaptor Dorich, Victoria; Brugger, Christiane; Tripathi, Arti Genes & Development, Vol. 33, Issue 11-12 https://doi.org/10.1101/gad.320168.118	journal	April 2019
The RssB response regulator directly targets sigmaS for degradation by ClpXP Zhou, Y. Genes & Development, Vol. 15, Issue 5 https://doi.org/10.1101/gad.864401	journal	March 2001
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
Two variable active site residues modulate response regulator phosphoryl group stability Thomas, Stephanie A.; Brewster, Jocelyn A.; Bourret, Robert B. Molecular Microbiology, Vol. 69, Issue 2 https://doi.org/10.1111/j.1365-2958.2008.06296.x	journal	July 2008
Modulation of Response Regulator CheY Reaction Kinetics by Two Variable Residues That Affect Conformation Straughn, Philip B.; Vass, Luke R.; Yuan, Chase Journal of Bacteriology, Vol. 202, Issue 15 https://doi.org/10.1128/JB.00089-20	journal	May 2020
Genome-Wide Transcriptional Response to Varying RpoS Levels in Escherichia coli K-12 Wong, Garrett T.; Bonocora, Richard P.; Schep, Alicia N. Journal of Bacteriology, Vol. 199, Issue 7 https://doi.org/10.1128/JB.00755-16	journal	January 2017
Experimental Analysis of Functional Variation within Protein Families: Receiver Domain Autodephosphorylation Kinetics Page, Stephani C.; Immormino, Robert M.; Miller, Thane H. Journal of Bacteriology, Vol. 198, Issue 18 https://doi.org/10.1128/JB.00853-15	journal	July 2016
A New Perspective on Response Regulator Activation Stock, Ann M.; Guhaniyogi, Jayita Journal of Bacteriology, Vol. 188, Issue 21 https://doi.org/10.1128/JB.01268-06	journal	November 2006
IraL Is an RssB Anti-adaptor That Stabilizes RpoS during Logarithmic Phase Growth in Escherichia coli and Shigella Hryckowian, Andrew J.; Battesti, Aurelia; Lemke, Justin J. mBio, Vol. 5, Issue 3 https://doi.org/10.1128/mBio.01043-14	journal	May 2014
Allosteric Activation of Bacterial Response Regulators: the Role of the Cognate Histidine Kinase Beyond Phosphorylation Trajtenberg, Felipe; Albanesi, Daniela; Ruétalo, Natalia mBio, Vol. 5, Issue 6 https://doi.org/10.1128/mBio.02105-14	journal	November 2014
Structural Basis of Response Regulator Function Gao, Rong; Bouillet, Sophie; Stock, Ann M. Annual Review of Microbiology, Vol. 73, Issue 1 https://doi.org/10.1146/annurev-micro-020518-115931	journal	September 2019
Biological Insights from Structures of Two-Component Proteins Gao, Rong; Stock, Ann M. Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073214	journal	October 2009
Elucidating the function of the RpoS regulon Schellhorn, Herb E. Future Microbiology, Vol. 9, Issue 4 https://doi.org/10.2217/fmb.14.9	journal	April 2014
Insight into the RssB-Mediated Recognition and Delivery of σs to the AAA+ Protease, ClpXP Micevski, Dimce; Zeth, Kornelius; Mulhern, Terrence D. Biomolecules, Vol. 10, Issue 4 https://doi.org/10.3390/biom10040615	journal	April 2020

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