Structural asymmetry in a conserved signaling system that regulates division, replication, and virulence of an intracellular pathogen

Willett, Jonathan W.; Herrou, Julien; Briegel, Ariane; Rotskoff, Grant; Crosson, Sean

doi:10.1073/pnas.1503118112

Title: Structural asymmetry in a conserved signaling system that regulates division, replication, and virulence of an intracellular pathogen

Journal Article · Fri Oct 30 00:00:00 EDT 2015 · Proc. Natl. Acad. Sci. USA

DOI:https://doi.org/10.1073/pnas.1503118112· OSTI ID:1214861

Willett, Jonathan W.; Herrou, Julien; Briegel, Ariane; Rotskoff, Grant; Crosson, Sean ^[1]

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

Sponsoring Organization:: National Institutes of Health (NIH)

OSTI ID:: 1214861

Journal Information:: Proc. Natl. Acad. Sci. USA, Vol. 112, Issue (28) ; 07, 2015

Country of Publication:: United States

Language:: ENGLISH

References (67)

Structural Insight into Partner Specificity and Phosphoryl Transfer in Two-Component Signal Transduction Casino, Patricia; Rubio, Vicente; Marina, Alberto Cell, Vol. 139, Issue 2 https://doi.org/10.1016/j.cell.2009.08.032	journal	October 2009
Kinetic Characterization of the WalRKSpn (VicRK) Two-Component System of Streptococcus pneumoniae: Dependence of WalKSpn (VicK) Phosphatase Activity on Its PAS Domain Gutu, Alina D.; Wayne, Kyle J.; Sham, Lok-To Journal of Bacteriology, Vol. 192, Issue 9 https://doi.org/10.1128/JB.01690-09	journal	February 2010
Full-Length Structure of a Sensor Histidine Kinase Pinpoints Coaxial Coiled Coils as Signal Transducers and Modulators Diensthuber, Ralph P.; Bommer, Martin; Gleichmann, Tobias Structure, Vol. 21, Issue 7 https://doi.org/10.1016/j.str.2013.04.024	journal	July 2013
Clinical Manifestations of Human Brucellosis: A Systematic Review and Meta-Analysis Dean, Anna S.; Crump, Lisa; Greter, Helena PLoS Neglected Tropical Diseases, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pntd.0001929	journal	December 2012
Mechanistic Insights Revealed by the Crystal Structure of a Histidine Kinase with Signal Transducer and Sensor Domains Wang, Chen; Sang, Jiayan; Wang, Jiawei PLoS Biology, Vol. 11, Issue 2 https://doi.org/10.1371/journal.pbio.1001493	journal	February 2013
Structural plasticity and catalysis regulation of a thermosensor histidine kinase Albanesi, D.; Martin, M.; Trajtenberg, F. Proceedings of the National Academy of Sciences, Vol. 106, Issue 38 https://doi.org/10.1073/pnas.0906699106	journal	September 2009
Segmental Helical Motions and Dynamical Asymmetry Modulate Histidine Kinase Autophosphorylation Mechaly, Ariel E.; Sassoon, Nathalie; Betton, Jean-Michel PLoS Biology, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pbio.1001776	journal	January 2014
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates Svergun, D.; Barberato, C.; Koch, M. H. J. Journal of Applied Crystallography, Vol. 28, Issue 6 https://doi.org/10.1107/S0021889895007047	journal	December 1995
The new global map of human brucellosis Pappas, Georgios; Papadimitriou, Photini; Akritidis, Nikolaos The Lancet Infectious Diseases, Vol. 6, Issue 2 https://doi.org/10.1016/S1473-3099(06)70382-6	journal	February 2006
Collaboration gets the most out of software Morin, Andrew; Eisenbraun, Ben; Key, Jason eLife, Vol. 2 https://doi.org/10.7554/eLife.01456	journal	September 2013
Improved side-chain torsion potentials for the Amber ff99SB protein force field Lindorff-Larsen, Kresten; Piana, Stefano; Palmo, Kim Proteins: Structure, Function, and Bioinformatics https://doi.org/10.1002/prot.22711	journal	January 2010
Broad-Host-Range Expression Vectors with Tightly Regulated Promoters and Their Use To Examine the Influence of TraR and TraM Expression on Ti Plasmid Quorum Sensing Khan, S. R.; Gaines, J.; Roop, R. M. Applied and Environmental Microbiology, Vol. 74, Issue 16 https://doi.org/10.1128/AEM.01098-08	journal	July 2008
Cell cycle-dependent adaptor complex for ClpXP-mediated proteolysis directly integrates phosphorylation and second messenger signals Smith, Stephen C.; Joshi, Kamal K.; Zik, Justin J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 39 https://doi.org/10.1073/pnas.1407862111	journal	September 2014
A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression Iniesta, A. A.; McGrath, P. T.; Reisenauer, A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 29 https://doi.org/10.1073/pnas.0604554103	journal	July 2006
The B rucella abortus virulence regulator, LovhK, is a sensor kinase in the general stress response signalling pathway : The LovhK stress sensor kinase of Kim, Hye-Sook; Willett, Jonathan W.; Jain-Gupta, Neeta Molecular Microbiology, Vol. 94, Issue 4 https://doi.org/10.1111/mmi.12809	journal	October 2014
The ecological coherence of high bacterial taxonomic ranks Philippot, Laurent; Andersson, Siv G. E.; Battin, Tom J. Nature Reviews Microbiology, Vol. 8, Issue 7 https://doi.org/10.1038/nrmicro2367	journal	June 2010
Genetic and Biochemical Dissection of a HisKA Domain Identifies Residues Required Exclusively for Kinase and Phosphatase Activities Willett, Jonathan W.; Kirby, John R. PLoS Genetics, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pgen.1003084	journal	November 2012
GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Pronk, Sander; Páll, Szilárd; Schulz, Roland Bioinformatics, Vol. 29, Issue 7 https://doi.org/10.1093/bioinformatics/btt055	journal	February 2013
Branched Signal Wiring of an Essential Bacterial Cell-Cycle Phosphotransfer Protein Blair, Jimmy A.; Xu, Qingping; Childers, W. Seth Structure, Vol. 21, Issue 9 https://doi.org/10.1016/j.str.2013.06.024	journal	September 2013
Rewiring the Specificity of Two-Component Signal Transduction Systems Skerker, Jeffrey M.; Perchuk, Barrett S.; Siryaporn, Albert Cell, Vol. 133, Issue 6 https://doi.org/10.1016/j.cell.2008.04.040	journal	June 2008
The Brucella abortus General Stress Response System Regulates Chronic Mammalian Infection and Is Controlled by Phosphorylation and Proteolysis Kim, Hye-Sook; Caswell, Clayton C.; Foreman, Robert Journal of Biological Chemistry, Vol. 288, Issue 19 https://doi.org/10.1074/jbc.M113.459305	journal	April 2013
Two-Component Signal Transduction Stock, Ann M.; Robinson, Victoria L.; Goudreau, Paul N. Annual Review of Biochemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev.biochem.69.1.183	journal	June 2000
The Bacillus and Myxococcus Developmental Networks and Their Transcriptional Regulators Kroos, Lee Annual Review of Genetics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev.genet.41.110306.130400	journal	December 2007
Regulation of Lipid A Modifications by Salmonella typhimurium Virulence Genes phoP-phoQ Guo, L. Science, Vol. 276, Issue 5310 https://doi.org/10.1126/science.276.5310.250	journal	April 1997
System-level design of bacterial cell cycle control McAdams, Harley H.; Shapiro, Lucy FEBS Letters, Vol. 583, Issue 24 https://doi.org/10.1016/j.febslet.2009.09.030	journal	September 2009
The Crystal Structure of Beryllofluoride Spo0F in Complex with the Phosphotransferase Spo0B Represents a Phosphotransfer Pretransition State Varughese, Kottayil I.; Tsigelny, Igor; Zhao, Haiyan Journal of Bacteriology, Vol. 188, Issue 13 https://doi.org/10.1128/JB.00160-06	journal	July 2006
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Why and How Bacteria Localize Proteins Shapiro, L.; McAdams, H. H.; Losick, R. Science, Vol. 326, Issue 5957 https://doi.org/10.1126/science.1175685	journal	November 2009
The Brucella abortus Cu,Zn Superoxide Dismutase Is Required for Optimal Resistance to Oxidative Killing by Murine Macrophages and Wild-Type Virulence in Experimentally Infected Mice Gee, J. M.; Valderas, M. W.; Kovach, M. E. Infection and Immunity, Vol. 73, Issue 5 https://doi.org/10.1128/IAI.73.5.2873-2880.2005	journal	April 2005
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
The CckA-ChpT-CtrA Phosphorelay System Is Regulated by Quorum Sensing and Controls Flagellar Motility in the Marine Sponge Symbiont Ruegeria sp. KLH11 Zan, Jindong; Heindl, Jason E.; Liu, Yue PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066346	journal	June 2013
Regulation of the bacterial cell cycle by an integrated genetic circuit Biondi, Emanuele G.; Reisinger, Sarah J.; Skerker, Jeffrey M. Nature, Vol. 444, Issue 7121 https://doi.org/10.1038/nature05321	journal	November 2006
The Critical Role of the Conserved Thr ²⁴⁷ Residue in the Functioning of the Osmosensor EnvZ, a Histidine Kinase/Phosphatase, in Escherichia coli Dutta, Rinku; Yoshida, Takeshi; Inouye, Masayori Journal of Biological Chemistry, Vol. 275, Issue 49 https://doi.org/10.1074/jbc.M005872200	journal	September 2000
Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Igo, M. M.; Ninfa, A. J.; Stock, J. B. Genes & Development, Vol. 3, Issue 11 https://doi.org/10.1101/gad.3.11.1725	journal	November 1989
Nucleotide binding by the histidine kinase CheA Bilwes, Alexandrine M.; Quezada, Cindy M.; Croal, Laura R. Nature Structural Biology, Vol. 8, Issue 4, p. 353-360 https://doi.org/10.1038/86243	journal	April 2001
Systematic Dissection and Trajectory-Scanning Mutagenesis of the Molecular Interface That Ensures Specificity of Two-Component Signaling Pathways Capra, Emily J.; Perchuk, Barrett S.; Lubin, Emma A. PLoS Genetics, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pgen.1001220	journal	November 2010
myo-Inositol and D-Ribose Ligand Discrimination in an ABC Periplasmic Binding Protein Herrou, J.; Crosson, S. Journal of Bacteriology, Vol. 195, Issue 10 https://doi.org/10.1128/JB.00116-13	journal	March 2013
The evolution of chronic infection strategies in the α-proteobacteria Batut, Jacques; Andersson, Siv G. E.; O'Callaghan, David Nature Reviews Microbiology, Vol. 2, Issue 12 https://doi.org/10.1038/nrmicro1044	journal	December 2004
The Yeast YPD1/SLN1 Complex Xu, Qingping; Porter, Stace W.; West, Ann H. Structure, Vol. 11, Issue 12 https://doi.org/10.1016/j.str.2003.10.016	journal	December 2003
Phosphotransfer Profiling: Systematic Mapping of Two‐Component Signal Transduction Pathways and Phosphorelays Laub, Michael T.; Biondi, Emanuele G.; Skerker, Jeffrey M. Methods in Enzymology https://doi.org/10.1016/S0076-6879(07)23026-5	book	January 2007
Comparison of quantitative methods for cell-shape analysis Pincus, Z.; Theriot, J. A. Journal of Microscopy, Vol. 227, Issue 2 https://doi.org/10.1111/j.1365-2818.2007.01799.x	journal	August 2007
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
Specificity in Two-Component Signal Transduction Pathways Laub, Michael T.; Goulian, Mark Annual Review of Genetics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev.genet.41.042007.170548	journal	December 2007
Cell Cycle–Dependent Polar Localization of an Essential Bacterial Histidine Kinase that Controls DNA Replication and Cell Division Jacobs, Christine; Domian, Ibrahim J.; Maddock, Janine R. Cell, Vol. 97, Issue 1 https://doi.org/10.1016/S0092-8674(00)80719-9	journal	April 1999
A Homolog of the CtrA Cell Cycle Regulator Is Present and Essential in Sinorhizobium meliloti Barnett, Melanie J.; Hung, Dean Y.; Reisenauer, Ann Journal of Bacteriology, Vol. 183, Issue 10 https://doi.org/10.1128/JB.183.10.3204-3210.2001	journal	May 2001
LINCS: A linear constraint solver for molecular simulations Hess, Berk; Bekker, Henk; Berendsen, Herman J. C. Journal of Computational Chemistry, Vol. 18, Issue 12 https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L	journal	September 1997
Evolution of Two-Component Signal Transduction Systems Capra, Emily J.; Laub, Michael T. Annual Review of Microbiology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-micro-092611-150039	journal	October 2012
Interactions of the Human Pathogenic Brucella Species with Their Hosts Atluri, Vidya L.; Xavier, Mariana N.; de Jong, Maarten F. Annual Review of Microbiology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-micro-090110-102905	journal	October 2011
Conserved modular design of an oxygen sensory/signaling network with species-specific output Crosson, S.; McGrath, P. T.; Stephens, C. Proceedings of the National Academy of Sciences, Vol. 102, Issue 22 https://doi.org/10.1073/pnas.0503022102	journal	May 2005
Electron cryotomography sample preparation using the Vitrobot Iancu, Cristina V.; Tivol, William F.; Schooler, Jordan B. Nature Protocols, Vol. 1, Issue 6 https://doi.org/10.1038/nprot.2006.432	journal	January 2006
The CtrA phosphorelay integrates differentiation and communication in the marine alphaproteobacterium Dinoroseobacter shibae Wang, Hui; Ziesche, Lisa; Frank, Oliver BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-130	journal	February 2014
Global analysis of cell cycle gene expression of the legume symbiont Sinorhizobium meliloti De Nisco, Nicole J.; Abo, Ryan P.; Wu, C. Max Proceedings of the National Academy of Sciences, Vol. 111, Issue 9 https://doi.org/10.1073/pnas.1400421111	journal	February 2014
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
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Structural basis of a protein partner switch that regulates the general stress response of -proteobacteria Herrou, J.; Rotskoff, G.; Luo, Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 21 https://doi.org/10.1073/pnas.1116887109	journal	May 2012
The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis Brilli, Matteo; Fondi, Marco; Fani, Renato BMC Systems Biology, Vol. 4, Issue 1 https://doi.org/10.1186/1752-0509-4-52	journal	January 2010
Determinants of specificity in two-component signal transduction Podgornaia, Anna I.; Laub, Michael T. Current Opinion in Microbiology, Vol. 16, Issue 2 https://doi.org/10.1016/j.mib.2013.01.004	journal	April 2013
Electronic and Protein Structural Dynamics of a Photosensory Histidine Kinase Alexandre, Maxime T. A.; Purcell, Erin B.; van Grondelle, Rienk Biochemistry, Vol. 49, Issue 23 https://doi.org/10.1021/bi100527a	journal	May 2010
Asymmetry in the Autophosphorylation of the Two-Component Regulatory System Transmitter Protein Nitrogen Regulator II of Escherichia coli Jiang, Peng; Peliska, James A.; Ninfa, Alexander J. Biochemistry, Vol. 39, Issue 17 https://doi.org/10.1021/bi992921w	journal	April 2000
Two-Component Signal Transduction Pathways Regulating Growth and Cell Cycle Progression in a Bacterium: A System-Level Analysis Skerker, Jeffrey M.; Prasol, Melanie S.; Perchuk, Barrett S. PLoS Biology, Vol. 3, Issue 10 https://doi.org/10.1371/journal.pbio.0030334	journal	September 2005
Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle Laub, M. T.; Chen, S. L.; Shapiro, L. Proceedings of the National Academy of Sciences, Vol. 99, Issue 7 https://doi.org/10.1073/pnas.062065699	journal	April 2002
The MiST2 database: a comprehensive genomics resource on microbial signal transduction Ulrich, Luke E.; Zhulin, Igor B. Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp940	journal	November 2009
Polarity and cell fate asymmetry in Caulobacter crescentus Tsokos, Christos G.; Laub, Michael T. Current Opinion in Microbiology, Vol. 15, Issue 6 https://doi.org/10.1016/j.mib.2012.10.011	journal	December 2012
Polar growth in the Alphaproteobacterial order Rhizobiales Brown, P. J. B.; de Pedro, M. A.; Kysela, D. T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 5 https://doi.org/10.1073/pnas.1114476109	journal	January 2012
An Improved Cryogen for Plunge Freezing Tivol, William F.; Briegel, Ariane; Jensen, Grant J. Microscopy and Microanalysis, Vol. 14, Issue 5 https://doi.org/10.1017/S1431927608080781	journal	September 2008
Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein Marina, Alberto; Waldburger, Carey D.; Hendrickson, Wayne A. The EMBO Journal, Vol. 24, Issue 24 https://doi.org/10.1038/sj.emboj.7600886	journal	December 2005
Visualizing autophosphorylation in histidine kinases Casino, Patricia; Miguel-Romero, Laura; Marina, Alberto Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4258	journal	February 2014

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