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.; Biondi, Emanuele G.; Laub, Michael T.

doi:10.1371/journal.pbio.0030334

Title: Two-Component Signal Transduction Pathways Regulating Growth and Cell Cycle Progression in a Bacterium: A System-Level Analysis

Journal Article · Tue Sep 27 00:00:00 EDT 2005 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.0030334· OSTI ID:1627143

Skerker, Jeffrey M. ^[1]; Prasol, Melanie S. ^[1]; Perchuk, Barrett S. ^[1]; Biondi, Emanuele G. ^[1]; Laub, Michael T. ^[1]

Harvard Univ., Cambridge, MA (United States). Bauer Center for Genomics Research

Two-component signal transduction systems, comprised of histidine kinases and their response regulator substrates, are the predominant means by which bacteria sense and respond to extracellular signals. These systems allow cells to adapt to prevailing conditions by modifying cellular physiology, including initiating programs of gene expression, catalyzing reactions, or modifying protein–protein interactions. These signaling pathways have also been demonstrated to play a role in coordinating bacterial cell cycle progression and development. Here we report a system-level investigation of two-component pathways in the model organism Caulobacter crescentus. First, by a comprehensive deletion analysis we show that at least 39 of the 106 two-component genes are required for cell cycle progression, growth, or morphogenesis. These include nine genes essential for growth or viability of the organism. We then use a systematic biochemical approach, called phosphotransfer profiling, to map the connectivity of histidine kinases and response regulators. Combining these genetic and biochemical approaches, we identify a new, highly conserved essential signaling pathway from the histidine kinase CenK to the response regulator CenR, which plays a critical role in controlling cell envelope biogenesis and structure. Depletion of either cenK or cenR leads to an unusual, severe blebbing of cell envelope material, whereas constitutive activation of the pathway compromises cell envelope integrity, resulting in cell lysis and death. We propose that the CenK–CenR pathway may be a suitable target for new antibiotic development, given previous successes in targeting the bacterial cell wall. Finally, the ability of our in vitro phosphotransfer profiling method to identify signaling pathways that operate in vivo takes advantage of an observation that histidine kinases are endowed with a global kinetic preference for their cognate response regulators. We propose that this system-wide selectivity insulates two-component pathways from one another, preventing unwanted cross-talk.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Harvard Univ., Cambridge, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: FG03-01ER63219; FG02-04ER63922

OSTI ID:: 1627143

Journal Information:: PLoS Biology (Online), Vol. 3, Issue 10; ISSN 1545-7885

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (62)

Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system Batchelor, E.; Goulian, M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 2 https://doi.org/10.1073/pnas.0234782100	journal	January 2003
Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus Skerker, Jeffrey M.; Laub, Michael T. Nature Reviews Microbiology, Vol. 2, Issue 4 https://doi.org/10.1038/nrmicro864	journal	April 2004
Two-component and phosphorelay signal-transduction systems as therapeutic targets Stephenson, K. Current Opinion in Pharmacology, Vol. 2, Issue 5 https://doi.org/10.1016/S1471-4892(02)00194-7	journal	October 2002
Novel domains of the prokaryotic two-component signal transduction systems Galperin, Michael Y.; Nikolskaya, Anastasia N.; Koonin, Eugene V. FEMS Microbiology Letters, Vol. 203, Issue 1 https://doi.org/10.1111/j.1574-6968.2001.tb10814.x	journal	September 2001
Interaction of EnvZ, a sensory histidine kinase, with phosphorylated OmpR, the cognate response regulator: Interaction between phosphorylated OmpR and EnvZ Yoshida, Takeshi; Cai, Sheng jian; Inouye, Masayori Molecular Microbiology, Vol. 46, Issue 5 https://doi.org/10.1046/j.1365-2958.2002.03240.x	journal	December 2002
Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain Paul, R. Genes & Development, Vol. 18, Issue 6 https://doi.org/10.1101/gad.289504	journal	March 2004
MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus: MreB-dependent regulation of cell shape Figge, Rainer M.; Divakaruni, Arun V.; Gober, James W. Molecular Microbiology, Vol. 51, Issue 5 https://doi.org/10.1111/j.1365-2958.2003.03936.x	journal	February 2004
Functional Characterization in Vitro of All Two-component Signal Transduction Systems from Escherichia coli Yamamoto, Kaneyoshi; Hirao, Kiyo; Oshima, Taku Journal of Biological Chemistry, Vol. 280, Issue 2 https://doi.org/10.1074/jbc.M410104200	journal	November 2004
The Comprehensive Microbial Resource Peterson, J. D. Nucleic Acids Research, Vol. 29, Issue 1 https://doi.org/10.1093/nar/29.1.123	journal	January 2001
An essential, multicomponent signal transduction pathway required for cell cycle regulation in Caulobacter Wu, J.; Ohta, N.; Newton, A. Proceedings of the National Academy of Sciences, Vol. 95, Issue 4 https://doi.org/10.1073/pnas.95.4.1443	journal	February 1998
Targeting protein homodimerization: A novel drug discovery system Furuta, Eiji; Yamamoto, Kaneyoshi; Tatebe, Daisuke FEBS Letters, Vol. 579, Issue 10 https://doi.org/10.1016/j.febslet.2005.02.056	journal	March 2005
Quantitative phenotypic analysis of yeast deletion mutants using a highly parallel molecular bar–coding strategy Shoemaker, Daniel D.; Lashkari, Deval A.; Morris, Don Nature Genetics, Vol. 14, Issue 4 https://doi.org/10.1038/ng1296-450	journal	December 1996
petR, located upstream of the fbcFBC operon encoding the cytochrome bc ₁ complex, is homologous to bacterial response regulators and necessary for photosynthetic and respiratory growth of Rhodobacter capsulatus Tokito, Mariko K.; Daldal, Fevzi Molecular Microbiology, Vol. 6, Issue 12 https://doi.org/10.1111/j.1365-2958.1992.tb00889.x	journal	June 1992
Defective cell wall synthesis in Streptococcus pneumoniae R6 depleted for the essential PcsB putative murein hydrolase or the VicR (YycF) response regulator: Defective cell wall synthesis in pcsB mutants Ng, Wai-Leung; Kazmierczak, Krystyna M.; Winkler, Malcolm E. Molecular Microbiology, Vol. 53, Issue 4 https://doi.org/10.1111/j.1365-2958.2004.04196.x	journal	July 2004
The Complete Genome Sequence of Escherichia coli K-12 Blattner, F. R. Science, Vol. 277, Issue 5331 https://doi.org/10.1126/science.277.5331.1453	journal	September 1997
Isolation and Characterization of Inhibitors of the Essential Histidine Kinase, YycG in Bacillus subtilis and Staphylococcus aureus Watanabe, Takafumi; Hashimoto, Yoshiki; Yamamoto, Kaneyoshi The Journal of Antibiotics, Vol. 56, Issue 12 https://doi.org/10.7164/antibiotics.56.1045	journal	January 2003
Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. Evinger, M.; Agabian, N. Journal of Bacteriology, Vol. 132, Issue 1 https://doi.org/10.1128/JB.132.1.294-301.1977	journal	January 1977
Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis Hess, J. Fred; Oosawa, Kenji; Kaplan, Nachum Cell, Vol. 53, Issue 1 https://doi.org/10.1016/0092-8674(88)90489-8	journal	April 1988
Role in Cell Permeability of an Essential Two-Component System in Staphylococcus aureus Martin, Patrick K.; Li, Tong; Sun, DongXu Journal of Bacteriology, Vol. 181, Issue 12 https://doi.org/10.1128/JB.181.12.3666-3673.1999	journal	June 1999
Transduction of envelope stress in Escherichia coli by the Cpx two-component system. Raivio, T. L.; Silhavy, T. J. Journal of Bacteriology, Vol. 179, Issue 24 https://doi.org/10.1128/jb.179.24.7724-7733.1997	journal	December 1997
SIGNAL TRANSDUCTION: Signaling Specificity in Yeast Elion, E. A. Science, Vol. 307, Issue 5710 https://doi.org/10.1126/science.1109500	journal	February 2005
Functional profiling of the Saccharomyces cerevisiae genome Giaever, Guri; Chu, Angela M.; Ni, Li Nature, Vol. 418, Issue 6896 https://doi.org/10.1038/nature00935	journal	July 2002
The Biochemical Basis of an All-or-None Cell Fate Switch in Xenopus Oocytes Ferrell Jr., J. E. Science, Vol. 280, Issue 5365 https://doi.org/10.1126/science.280.5365.895	journal	May 1998
Complete genome sequence of Caulobacter crescentus Nierman, W. C.; Feldblyum, T. V.; Laub, M. T. Proceedings of the National Academy of Sciences, Vol. 98, Issue 7 https://doi.org/10.1073/pnas.061029298	journal	March 2001
Precise amounts of a novel member of a phosphotransferase superfamily are essential for growth and normal morphology in Caulobacter crescentus Fuchs, T.; Wiget, P.; Osteras, M. Molecular Microbiology, Vol. 39, Issue 3 https://doi.org/10.1046/j.1365-2958.2001.02238.x	journal	February 2001
Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates Loog, Mart; Morgan, David O. Nature, Vol. 434, Issue 7029 https://doi.org/10.1038/nature03329	journal	March 2005
Signal Transduction and Cell Cycle Checkpoints in Developmental Regulation ofCaulobacter Ohta, Noriko; Grebe, Thorsten W.; Newton, Austin Prokaryotic Development https://doi.org/10.1128/9781555818166.ch17	book	April 2014
Differential Localization of Two Histidine Kinases Controlling Bacterial Cell Differentiation Wheeler, Robert T.; Shapiro, Lucy Molecular Cell, Vol. 4, Issue 5 https://doi.org/10.1016/S1097-2765(00)80379-2	journal	November 1999
A novel bacterial tyrosine kinase essential for cell division and differentiation Wu, J.; Ohta, N.; Zhao, J. -L. Proceedings of the National Academy of Sciences, Vol. 96, Issue 23 https://doi.org/10.1073/pnas.96.23.13068	journal	November 1999
Glutamate at the Site of Phosphorylation of Nitrogen-regulatory Protein NTRC Mimics Aspartyl-Phosphate and Activates the Protein Klose, Karl E.; Weiss, David S.; Kustu, Sydney Journal of Molecular Biology, Vol. 232, Issue 1 https://doi.org/10.1006/jmbi.1993.1370	journal	July 1993
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
Synergistic Kinetic Interactions between Components of the Phosphorelay Controlling Sporulation in Bacillus subtilis ^† Grimshaw, Charles E.; Huang, Shaoming; Hanstein, Conrad G. Biochemistry, Vol. 37, Issue 5 https://doi.org/10.1021/bi971917m	journal	February 1998
An essential single domain response regulator required for normal cell division and differentiation in Caulobacter crescentus. Hecht, G. B.; Lane, T.; Ohta, N. The EMBO Journal, Vol. 14, Issue 16 https://doi.org/10.1002/j.1460-2075.1995.tb00063.x	journal	August 1995
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
Kinetic Comparison of the Specificity of the Vancomycin Resistance Kinase VanS for Two Response Regulators, VanR and PhoB ^† Fisher, Stewart L.; Kim, Soo-Ki; Wanner, Barry L. Biochemistry, Vol. 35, Issue 15 https://doi.org/10.1021/bi9525435	journal	January 1996
Optimization of specificity in a cellular protein interaction network by negative selection Zarrinpar, Ali; Park, Sang-Hyun; Lim, Wendell A. Nature, Vol. 426, Issue 6967 https://doi.org/10.1038/nature02178	journal	December 2003
Making informed decisions: regulatory interactions between two-component systems Bijlsma, Jetta J. E.; Groisman, Eduardo A. Trends in Microbiology, Vol. 11, Issue 8 https://doi.org/10.1016/S0966-842X(03)00176-8	journal	August 2003
Temporal and Spatial Regulation in Prokaryotic Cell Cycle Progression and Development Ryan, Kathleen R.; Shapiro, Lucy Annual Review of Biochemistry, Vol. 72, Issue 1 https://doi.org/10.1146/annurev.biochem.72.121801.161824	journal	June 2003
Caulobacter crescentus Requires RodA and MreB for Stalk Synthesis and Prevention of Ectopic Pole Formation Wagner, Jennifer K.; Galvani, Cheryl D.; Brun, Yves V. Journal of Bacteriology, Vol. 187, Issue 2 https://doi.org/10.1128/JB.187.2.544-553.2005	journal	January 2005
A Bacterial Cell-Cycle Regulatory Network Operating in Time and Space McAdams, H. H. Science, Vol. 301, Issue 5641 https://doi.org/10.1126/science.1087694	journal	September 2003
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
Principles of MAP Kinase Signaling Specificity in Saccharomyces cerevisiae Schwartz, Monica A.; Madhani, Hiten D. Annual Review of Genetics, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.genet.39.073003.112634	journal	December 2004
The HWE Histidine Kinases, a New Family of Bacterial Two-Component Sensor Kinases with Potentially Diverse Roles in Environmental Signaling Karniol, Baruch; Vierstra, Richard D. Journal of Bacteriology, Vol. 186, Issue 2 https://doi.org/10.1128/JB.186.2.445-453.2004	journal	January 2004
Global Analysis of the Genetic Network Controlling a Bacterial Cell Cycle Laub, M. T.; McAdams, H. H.; Feldblyum, T. Science, Vol. 290, Issue 5499 https://doi.org/10.1126/science.290.5499.2144	journal	December 2000
A bacterial environmental sensor that functions as a protein kinase and stimulates transcriptional activation. Igo, M. M.; Ninfa, A. J.; Silhavy, T. J. Genes & Development, Vol. 3, Issue 5 https://doi.org/10.1101/gad.3.5.598	journal	May 1989
Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus: PleD control of polar development Aldridge, Phillip; Paul, Ralf; Goymer, Patrick Molecular Microbiology, Vol. 47, Issue 6 https://doi.org/10.1046/j.1365-2958.2003.03401.x	journal	March 2003
Turning off flagellum rotation requires the pleiotropic gene pleD: pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus Sommer, J. M.; Newton, A. Journal of Bacteriology, Vol. 171, Issue 1 https://doi.org/10.1128/jb.171.1.392-401.1989	journal	January 1989
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Datsenko, K. A.; Wanner, B. L. Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645 https://doi.org/10.1073/pnas.120163297	journal	May 2000
A search for amino acid substitutions that universally activate response regulators: Activating substitutions in response regulators Smith, Jenny G.; Latiolais, Jamie A.; Guanga, Gerald P. Molecular Microbiology, Vol. 51, Issue 3 https://doi.org/10.1046/j.1365-2958.2003.03882.x	journal	December 2003
Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus Meisenzahl, A. C.; Shapiro, L.; Jenal, U. Journal of Bacteriology, Vol. 179, Issue 3 https://doi.org/10.1128/jb.179.3.592-600.1997	journal	February 1997
Reconstitution of the bacterial chemotaxis signal transduction system from purified components Ninfa, E. G.; Stock, A.; Mowbray, S. Journal of Biological Chemistry, Vol. 266, Issue 15 https://doi.org/10.1016/S0021-9258(18)92886-3	journal	May 1991
Pseudoreversion analysis indicates a direct role of cell division genes in polar morphogenesis and differentiation in Caulobacter crescentus. Sommer, J. M.; Newton, A. Genetics, Vol. 129, Issue 3 https://doi.org/10.1093/genetics/129.3.623	journal	November 1991
PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae Wach, Achim Yeast, Vol. 12, Issue 3 https://doi.org/10.1002/(sici)1097-0061(19960315)12:3<259::aid-yea901>3.0.co;2-c	journal	March 1996
Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism Pawlowski, K.; Klosse, U.; de Bruijn, F. J. Molecular and General Genetics MGG, Vol. 231, Issue 1 https://doi.org/10.1007/bf00293830	journal	December 1991
Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay Burbulys, David; Trach, Kathleen A.; Hoch, James A. Cell, Vol. 64, Issue 3 https://doi.org/10.1016/0092-8674(91)90238-t	journal	February 1991
An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa Schweizer, Herbert P.; Hoang, Tung T. Gene, Vol. 158, Issue 1 https://doi.org/10.1016/0378-1119(95)00055-b	journal	January 1995
The Era of Pathway Quantification Koshland, Daniel E. Science, Vol. 280, Issue 5365 https://doi.org/10.1126/science.280.5365.852	journal	May 1998
Two-Component Signal Transduction as a Target for Microbial Anti-Infective Therapy Barrett, John F.; Hoch, James A. Antimicrobial Agents and Chemotherapy, Vol. 42, Issue 7 https://doi.org/10.1128/aac.42.7.1529	journal	July 1998
Rate of major protein synthesis during the cell cycle of Caulobacter crescentus Iba, H.; Fukuda, A.; Okada, Y. Journal of Bacteriology, Vol. 135, Issue 2 https://doi.org/10.1128/jb.135.2.647-655.1978	journal	August 1978
A Two-Component Signal Transduction System Essential for Growth of Bacillus subtilis: Implications for Anti-Infective Therapy Fabret, Céline; Hoch, James A. Journal of Bacteriology, Vol. 180, Issue 23 https://doi.org/10.1128/jb.180.23.6375-6383.1998	journal	December 1998
Digging with Experimental Pick and Computational Shovel: a New Addition to the Histidine Kinase Superfamily Zhulin, Igor B. Journal of Bacteriology, Vol. 186, Issue 2 https://doi.org/10.1128/jb.186.2.267-269.2004	journal	January 2004

Cited By (115)

Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes Davidson, Phillip; Eutsey, Rory; Redler, Brendan Carnegie Mellon University https://doi.org/10.1184/r1/7264163.v1	text	January 2018
Hit the right spots: cell cycle control by phosphorylated guanosines in alphaproteobacteria Hallez, Régis; Delaby, Marie; Sanselicio, Stefano Nature Reviews Microbiology, Vol. 15, Issue 3 https://doi.org/10.1038/nrmicro.2016.183	journal	January 2017
Design of protein-interaction specificity gives selective bZIP-binding peptides Grigoryan, Gevorg; Reinke, Aaron W.; Keating, Amy E. Nature, Vol. 458, Issue 7240 https://doi.org/10.1038/nature07885	journal	April 2009
Reconstruction of biochemical networks in microorganisms Feist, Adam M.; Herrgård, Markus J.; Thiele, Ines Nature Reviews Microbiology, Vol. 7, Issue 2 https://doi.org/10.1038/nrmicro1949	journal	December 2008
Two Proteins Form a Heteromeric Bacterial Self-Recognition Complex in Which Variable Subdomains Determine Allele-Restricted Binding Cardarelli, Lia; Saak, Christina; Gibbs, Karine A. mBio, Vol. 6, Issue 3 https://doi.org/10.1128/mbio.00251-15	journal	July 2015
The two-component signalling networks of Mycobacterium tuberculosis display extensive cross-talk in vitro Agrawal, Ruchi; Pandey, Akancha; Rajankar, Mayooreshwar P. Biochemical Journal, Vol. 469, Issue 1 https://doi.org/10.1042/bj20150268	journal	June 2015
A matter of life and death: cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway Dubrac, Sarah; Bisicchia, Paola; Devine, Kevin M. Molecular Microbiology, Vol. 70, Issue 6 https://doi.org/10.1111/j.1365-2958.2008.06483.x	journal	December 2008
A gated relaxation oscillator mediated by FrzX controls morphogenetic movements in Myxococcus xanthus Guzzo, Mathilde; Murray, Seán M.; Martineau, Eugénie Nature Microbiology, Vol. 3, Issue 8 https://doi.org/10.1038/s41564-018-0203-x	journal	July 2018
Crosstalk and the evolvability of intracellular communication Rowland, Michael A.; Greenbaum, Joseph M.; Deeds, Eric J. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms16009	journal	July 2017
Direct and adaptor-mediated substrate recognition by an essential AAA+ protease Chien, P.; Perchuk, B. S.; Laub, M. T. Proceedings of the National Academy of Sciences, Vol. 104, Issue 16 https://doi.org/10.1073/pnas.0701776104	journal	April 2007
Regulation of signaling directionality revealed by 3D snapshots of a kinase:regulator complex in action Trajtenberg, Felipe; Imelio, Juan A.; Machado, Matías R. eLife, Vol. 5 https://doi.org/10.7554/elife.21422	journal	December 2016
Pneumococcal Metabolic Adaptation and Colonization Are Regulated by the Two-Component Regulatory System 08 Gómez-Mejia, Alejandro; Gámez, Gustavo; Hirschmann, Stephanie mSphere, Vol. 3, Issue 3 https://doi.org/10.1128/msphere.00165-18	journal	May 2018
FrzZ, a dual CheY-like response regulator, functions as an output for the Frz chemosensory pathway of Myxococcus xanthus Inclán, Yuki F.; Vlamakis, Hera C.; Zusman, David R. Molecular Microbiology, Vol. 65, Issue 1 https://doi.org/10.1111/j.1365-2958.2007.05774.x	journal	July 2007
First genomic insights into members of a candidate bacterial phylum responsible for wastewater bulking Sekiguchi, Yuji; Ohashi, Akiko; Parks, Donovan H. PeerJ, Vol. 3 https://doi.org/10.7717/peerj.740	journal	January 2015
Draft genome sequence and annotation of Lactobacillus acetotolerans BM-LA14527, a beer-spoilage bacteria Liu, Junyan; Li, Lin; Peters, Brian M. FEMS Microbiology Letters, Vol. 363, Issue 18 https://doi.org/10.1093/femsle/fnw201	journal	August 2016
Evidence of Cross-Regulation in Two Closely Related Pyruvate-Sensing Systems in Uropathogenic Escherichia coli Steiner, Bradley D.; Eberly, Allison R.; Hurst, Melanie N. The Journal of Membrane Biology, Vol. 251, Issue 1 https://doi.org/10.1007/s00232-018-0014-2	journal	January 2018
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 Two Chemotaxis Clusters in Caulobacter crescentus Play Different Roles in Chemotaxis and Biofilm Regulation Berne, Cécile; Brun, Yves V. Journal of Bacteriology, Vol. 201, Issue 18 https://doi.org/10.1128/jb.00071-19	journal	May 2019
A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus : Regulation of stalk biogenesis in Biondi, Emanuele G.; Skerker, Jeffrey M.; Arif, Muhammad Molecular Microbiology, Vol. 59, Issue 2 https://doi.org/10.1111/j.1365-2958.2005.04970.x	journal	November 2005
Regulated proteolysis of a transcription factor complex is critical to cell cycle progression in Caulobacter crescentus: Cell cycle regulated proteolysis in Caulobacter Gora, Kasia G.; Cantin, Amber; Wohlever, Matthew Molecular Microbiology, Vol. 87, Issue 6 https://doi.org/10.1111/mmi.12166	journal	February 2013
Isolation and characterisation of the epothilone gene cluster with flanks from high alkalotolerant strain Sorangium cellulosum (So0157-2) Li, Zhi-Feng; Zhu, Li-Ping; Gu, Jing-yan World Journal of Microbiology and Biotechnology, Vol. 33, Issue 7 https://doi.org/10.1007/s11274-017-2301-y	journal	June 2017
Complex two-component signaling regulates the general stress response in Alphaproteobacteria Kaczmarczyk, Andreas; Hochstrasser, Ramon; Vorholt, Julia A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 48 https://doi.org/10.1073/pnas.1410095111	journal	November 2014
The orphan histidine protein kinase SgmT is a c‐di‐GMP receptor and regulates composition of the extracellular matrix together with the orphan DNA binding response regulator DigR in Myxococcus xanthus Petters, Tobias; Zhang, Xin; Nesper, Jutta Molecular Microbiology, Vol. 84, Issue 1 https://doi.org/10.1111/j.1365-2958.2012.08015.x	journal	March 2012
Pervasive degeneracy and epistasis in a protein-protein interface Podgornaia, Anna I.; Laub, Michael T. Science, Vol. 347, Issue 6222 https://doi.org/10.1126/science.1257360	journal	February 2015
A Link between Dimerization and Autophosphorylation of the Response Regulator PhoB Creager-Allen, Rachel L.; Silversmith, Ruth E.; Bourret, Robert B. Journal of Biological Chemistry, Vol. 288, Issue 30 https://doi.org/10.1074/jbc.m113.471763	journal	July 2013
Pneumococcal metabolic adaptation and colonization is regulated by the two-component regulatory system 08 Gómez-Mejia, Alejandro; Gámez, Gustavo; Hirschmann, Stephanie mSphere https://doi.org/10.1101/300095	posted_content	April 2018
Intrinsic limits of information transmission in biochemical signalling motifs Suderman, Ryan; Deeds, Eric J. Interface Focus, Vol. 8, Issue 6 https://doi.org/10.1098/rsfs.2018.0039	journal	October 2018
Dissecting the Specificity of Protein-Protein Interaction in Bacterial Two-Component Signaling: Orphans and Crosstalks Procaccini, Andrea; Lunt, Bryan; Szurmant, Hendrik PLoS ONE, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pone.0019729	journal	May 2011
The Two-Component Signal Transduction System ArlRS Regulates Staphylococcus epidermidis Biofilm Formation in an ica-Dependent Manner Wu, Yang; Wang, Jiaxue; Xu, Tao PLoS ONE, Vol. 7, Issue 7 https://doi.org/10.1371/journal.pone.0040041	journal	July 2012
Regulation of bacterial surface attachment by a network of sensory transduction proteins Reyes Ruiz, Leila M.; Fiebig, Aretha; Crosson, Sean PLOS Genetics https://doi.org/10.1101/554154	journal	February 2019
A two-component system, an anti-sigma factor and two paralogous ECF sigma factors are involved in the control of general stress response in Caulobacter crescentus: C. crescentus general stress response Lourenço, Rogério F.; Kohler, Christian; Gomes, Suely L. Molecular Microbiology, Vol. 80, Issue 6 https://doi.org/10.1111/j.1365-2958.2011.07668.x	journal	May 2011
The viable but nonculturable state induction and genomic analyses of Lactobacillus casei BM-LC14617, a beer-spoilage bacterium Liu, Junyan; Li, Lin; Peters, Brian M. MicrobiologyOpen, Vol. 6, Issue 5 https://doi.org/10.1002/mbo3.506	journal	July 2017
Gene networks that compensate for crosstalk with crosstalk Müller, Isaak E.; Rubens, Jacob R.; Jun, Tomi Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12021-y	journal	September 2019
Connecting the Sequence-Space of Bacterial Signaling Proteins to Phenotypes Using Coevolutionary Landscapes Cheng, R. R.; Nordesjö, O.; Hayes, R. L. Molecular Biology and Evolution, Vol. 33, Issue 12 https://doi.org/10.1093/molbev/msw188	journal	September 2016
Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria Badrinarayanan, Anjana; Le, Tung B. K.; Laub, Michael T. Journal of Cell Biology, Vol. 210, Issue 3 https://doi.org/10.1083/jcb.201505019	journal	August 2015
A Close-up View of the VraSR Two-component System: A MEDIATOR OF STAPHYLOCOCCUS AUREUS RESPONSE TO CELL WALL DAMAGE Belcheva, Antoaneta; Golemi-Kotra, Dasantila Journal of Biological Chemistry, Vol. 283, Issue 18 https://doi.org/10.1074/jbc.m710010200	journal	March 2008
Two-Component System Cross-Regulation Integrates Bacillus anthracis Response to Heme and Cell Envelope Stress Mike, Laura A.; Choby, Jacob E.; Brinkman, Paul R. PLoS Pathogens, Vol. 10, Issue 3 https://doi.org/10.1371/journal.ppat.1004044	journal	March 2014
The asymmetric distribution of the essential histidine kinase PdhS indicates a differentiation event in Brucella abortus Hallez, Régis; Mignolet, Johann; Van Mullem, Vincent The EMBO Journal, Vol. 26, Issue 5 https://doi.org/10.1038/sj.emboj.7601577	journal	February 2007
The DivJ, CbrA and PleC system controls DivK phosphorylation and symbiosis in Sinorhizobium meliloti: The cell cycle kinase DivJ in Sinorhizobium meliloti Pini, Francesco; Frage, Benjamin; Ferri, Lorenzo Molecular Microbiology https://doi.org/10.1111/mmi.12347	journal	August 2013
Accurate prediction of protein–protein interactions from sequence alignments using a Bayesian method Burger, Lukas; van Nimwegen, Erik Molecular Systems Biology, Vol. 4, Issue 1 https://doi.org/10.1038/msb4100203	journal	January 2008
Regulation of carbohydrate degradation pathways in Pseudomonas involves a versatile set of transcriptional regulators Udaondo, Zulema; Ramos, Juan-Luis; Segura, Ana Microbial Biotechnology, Vol. 11, Issue 3 https://doi.org/10.1111/1751-7915.13263	journal	April 2018
Precise transcription timing by a second-messenger drives a bacterial G1/S cell cycle transition Kaczmarczyk, Andreas; Hempel, Antje M.; von Arx, Christoph Nature Communications https://doi.org/10.1101/675330	posted_content	January 2019
Transcriptional regulatory module analysis reveals that bridge proteins reconcile multiple signals in extracellular electron transfer pathways Ding, Dewu; Shu, Chuanjun; Sun, Xiao Proteins: Structure, Function, and Bioinformatics, Vol. 88, Issue 1 https://doi.org/10.1002/prot.25789	journal	August 2019
Analysis of the Activity and Regulon of the Two-Component Regulatory System Composed by Cjj81176_1484 and Cjj81176_1483 of Campylobacter jejuni Luethy, Paul M.; Huynh, Steven; Parker, Craig T. Journal of Bacteriology, Vol. 197, Issue 9 https://doi.org/10.1128/jb.02564-14	journal	February 2015
Sensory deprivation in Staphylococcus aureus Villanueva, Maite; García, Begoña; Valle, Jaione Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-02949-y	journal	February 2018
Engineering robust control of two-component system phosphotransfer using modular scaffolds Whitaker, W. R.; Davis, S. A.; Arkin, A. P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 44 https://doi.org/10.1073/pnas.1209230109	journal	October 2012
Multi-environment QTL mapping reveals genetic architecture of fruit cracking in a tomato RIL Solanum lycopersicum × S. pimpinellifolium population Capel, Carmen; Yuste-Lisbona, Fernando J.; López-Casado, Gloria Theoretical and Applied Genetics, Vol. 130, Issue 1 https://doi.org/10.1007/s00122-016-2809-9	journal	October 2016
Involvement of AtoSC two-component system in Escherichia coli flagellar regulon Theodorou, Marina C.; Theodorou, Evaggelos C.; Kyriakidis, Dimitrios A. Amino Acids, Vol. 43, Issue 2 https://doi.org/10.1007/s00726-011-1140-7	journal	November 2011
Fast and Accurate Multivariate Gaussian Modeling of Protein Families: Predicting Residue Contacts and Protein-Interaction Partners Baldassi, Carlo; Zamparo, Marco; Feinauer, Christoph PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0092721	journal	March 2014
Cross-talk and specificity in two-component signal transduction pathways Agrawal, Ruchi; Sahoo, Bikash Kumar; Saini, Deepak Kumar Future Microbiology, Vol. 11, Issue 5 https://doi.org/10.2217/fmb-2016-0001	journal	May 2016
Gene Expression Profiling in Viable but Nonculturable (VBNC) Cells of Pseudomonas syringae pv. syringae Postnikova, Olga A.; Shao, Jonathan; Mock, Norton M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01419	journal	December 2015
Contribution of the Cpx envelope stress system to metabolism and virulence regulation in Salmonella enterica serovar Typhimurium Subramaniam, Sivaraman; Müller, Volker S.; Hering, Nina A. PLOS ONE, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pone.0211584	journal	February 2019
Multiple communication mechanisms between sensor kinases are crucial for virulence in Pseudomonas aeruginosa Francis, Vanessa I.; Waters, Elaine M.; Finton-James, Sutharsan E. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04640-8	journal	June 2018
Performance Characteristics for Sensors and Circuits Used to Program E. coli Tabor, Jeffrey J.; Groban, Eli S.; Voigt, Christopher A. Systems Biology and Biotechnology of Escherichia coli https://doi.org/10.1007/978-1-4020-9394-4_19	book	January 2009
Engineering transcription factors with novel DNA-binding specificity using comparative genomics Desai, Tasha A.; Rodionov, Dmitry A.; Gelfand, Mikhail S. Nucleic Acids Research, Vol. 37, Issue 8 https://doi.org/10.1093/nar/gkp079	journal	March 2009
RavA/RavR two-component system regulates Xanthomonas campestris pathogenesis and c-di-GMP turnover Tao, Jun; Li, Chunxia; Luo, Chao FEMS Microbiology Letters, Vol. 358, Issue 1 https://doi.org/10.1111/1574-6968.12529	journal	August 2014
Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli Siryaporn, Albert; Goulian, Mark Molecular Microbiology, Vol. 70, Issue 2 https://doi.org/10.1111/j.1365-2958.2008.06426.x	journal	October 2008
Bioinformatics and Experimental Analysis of Proteins of Two-Component Systems in Myxococcus xanthus Shi, Xingqi; Wegener-Feldbrügge, Sigrun; Huntley, Stuart Journal of Bacteriology, Vol. 190, Issue 2 https://doi.org/10.1128/jb.01502-07	journal	January 2008
Comparative Genome Characterization of a Petroleum-Degrading Bacillus subtilis Strain DM2 Li, Shi-Weng; Liu, Meng-Yuan; Yang, Rui-Qi International Journal of Genomics, Vol. 2019 https://doi.org/10.1155/2019/7410823	journal	May 2019
Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes Davidson, Philip; Eutsey, Rory; Redler, Brendan PLOS Genetics, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pgen.1007470	journal	September 2018
Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming Cheng, Shou-Ting; Wang, Fang-Fang; Qian, Wei PLOS Pathogens, Vol. 15, Issue 8 https://doi.org/10.1371/journal.ppat.1007952	journal	August 2019
Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication Lori, Christian; Ozaki, Shogo; Steiner, Samuel Macmillan https://doi.org/10.5451/unibas-ep37801	text	January 2015
Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication Lori, C.; Ozaki, S.; Steiner, S. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14473	journal	May 2015
Rules for biological regulation based on error minimization Shinar, G.; Dekel, E.; Tlusty, T. Proceedings of the National Academy of Sciences, Vol. 103, Issue 11 https://doi.org/10.1073/pnas.0506610103	journal	March 2006
Structural asymmetry in a conserved signaling system that regulates division, replication, and virulence of an intracellular pathogen Willett, Jonathan W.; Herrou, Julien; Briegel, Ariane Proceedings of the National Academy of Sciences, Vol. 112, Issue 28 https://doi.org/10.1073/pnas.1503118112	journal	June 2015
Genome-wide prediction of prokaryotic two-component system networks using a sequence-based meta-predictor Kara, Altan; Vickers, Martin; Swain, Martin BMC Bioinformatics, Vol. 16, Issue 1 https://doi.org/10.1186/s12859-015-0741-7	journal	September 2015
Diversity of two-component systems: insights into the signal transduction mechanism by the Staphylococcus aureus two-component system GraSR Muzamal, Uzma; Gomez, Daniel; Kapadia, Fenika F1000Research, Vol. 3 https://doi.org/10.12688/f1000research.5512.1	journal	January 2014
Regulation of bacterial surface attachment by a network of sensory transduction proteins Reyes Ruiz, Leila M.; Fiebig, Aretha; Crosson, Sean PLOS Genetics, Vol. 15, Issue 5 https://doi.org/10.1371/journal.pgen.1008022	journal	May 2019
Acidic pH triggers the phosphorylation of the response regulator NtrX in alphaproteobacteria Fernández, Ignacio; Sycz, Gabriela; Goldbaum, Fernando Alberto PLOS ONE, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pone.0194486	journal	April 2018
A Link between Dimerization and Autophosphorylation of the Response Regulator PhoB E., Silversmith, Ruth; L., Creager-Allen, Rachel; B., Bourret, Robert The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/8cp1-r786	text	January 2013
Emergence and Modular Evolution of a Novel Motility Machinery in Bacteria Jennifer, Luciano,; Rym, Agrebi,; V., Le Gall, Anne ETH Zurich https://doi.org/10.3929/ethz-b-000094291	text	January 2011
Cyclic di-GMP differentially tunes a bacterial flagellar motor through a novel class of CheY-like regulators Nesper, Jutta; Hug, Isabelle; Kato, Setsu eLife Sciences Publications https://doi.org/10.5451/unibas-ep57179	text	January 2017
Emergence and Modular Evolution of a Novel Motility Machinery in Bacteria Luciano, Jennifer; Agrebi, Rym; Le Gall, Anne Valérie PLoS Genetics, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pgen.1002268	journal	September 2011
Designing bacterial signaling interactions with coevolutionary landscapes Cheng, Ryan R.; Haglund, Ellinor; Tiee, Nicholas S. PLOS ONE, Vol. 13, Issue 8 https://doi.org/10.1371/journal.pone.0201734	journal	August 2018
Post-transcriptional gene regulation by an Hfq-independent small RNA in Caulobacter crescentus Fröhlich, Kathrin S.; Förstner, Konrad U.; Gitai, Zemer Nucleic Acids Research https://doi.org/10.1093/nar/gky765	journal	August 2018
Diversity of two-component systems: insights into the signal transduction mechanism by the Staphylococcus aureus two-component system GraSR Muzamal, Uzma; Gomez, Daniel; Kapadia, Fenika F1000Research, Vol. 3 https://doi.org/10.12688/f1000research.5512.2	journal	January 2014
The orphan histidine protein kinase SgmT is a c-di-GMP receptor and regulates composition of the extracellular matrix together with the orphan DNA binding response regulator DigR in Myxococcus xanthus Petters, Tobias; Zhang, Xin; Nesper, Jutta Blackwell https://doi.org/10.5451/unibas-ep21870	text	January 2012
Rules for biological regulation based on error minimization Shinar, Guy; Dekel, Erez; Tlusty, Tsvi arXiv https://doi.org/10.48550/arxiv.1007.4521	text	January 2010
Adaptive Mutations that Prevent Crosstalk Enable the Expansion of Paralogous Signaling Protein Families Capra, Emily J.; Perchuk, Barrett S.; Skerker, Jeffrey M. Cell, Vol. 150, Issue 1 https://doi.org/10.1016/j.cell.2012.05.033	journal	July 2012
An Adaptor Hierarchy Regulates Proteolysis during a Bacterial Cell Cycle Joshi, Kamal Kishore; Bergé, Matthieu; Radhakrishnan, Sunish Kumar Cell, Vol. 163, Issue 2 https://doi.org/10.1016/j.cell.2015.09.030	journal	October 2015
Molecular Mechanisms of Two-Component Signal Transduction Zschiedrich, Christopher P.; Keidel, Victoria; Szurmant, Hendrik Journal of Molecular Biology, Vol. 428, Issue 19 https://doi.org/10.1016/j.jmb.2016.08.003	journal	September 2016
Structural Basis of a Rationally Rewired Protein-Protein Interface Critical to Bacterial Signaling Podgornaia, Anna I.; Casino, Patricia; Marina, Alberto Structure, Vol. 21, Issue 9 https://doi.org/10.1016/j.str.2013.07.005	journal	September 2013
Design and Implementation of a Biomolecular Concentration Tracker Hsiao, Victoria; de los Santos, Emmanuel L. C.; Whitaker, Weston R. ACS Synthetic Biology, Vol. 4, Issue 2 https://doi.org/10.1021/sb500024b	journal	April 2014
Cyclic GMP stimulates lymphocyte nucleic acid synthesis Weinstein, Y.; Chambers, D. A.; Bourne, H. R. Nature, Vol. 251, Issue 5473 https://doi.org/10.1038/251352a0	journal	September 1974
Evolving a robust signal transduction pathway from weak cross‐talk Siryaporn, Albert; Perchuk, Barrett S.; Laub, Michael T. Molecular Systems Biology, Vol. 6, Issue 1 https://doi.org/10.1038/msb.2010.105	journal	January 2010
Deconstructing a multiple antibiotic resistance regulation through the quantification of its input function Rodrigo, Guillermo; Bajić, Djordje; Elola, Ignacio npj Systems Biology and Applications, Vol. 3, Issue 1 https://doi.org/10.1038/s41540-017-0031-2	journal	October 2017
Mapping the ‘Two-component system’ network in rice Sharan, Ashutosh; Soni, Praveen; Nongpiur, Ramsong Chantre Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-08076-w	journal	August 2017
Two overlapping two-component systems in Xanthomonas oryzae pv. oryzae contribute to full fitness in rice by regulating virulence factors expression Zheng, Dehong; Yao, Xiaoyan; Duan, Meng Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep22768	journal	March 2016
Tiny cells meet big questions: a closer look at bacterial cell biology Goley, Erin D. Molecular Biology of the Cell, Vol. 24, Issue 8 https://doi.org/10.1091/mbc.e12-11-0788	journal	April 2013
Extended N-terminal region of the essential phosphorelay signaling protein Ypd1 fromCryptococcus neoformanscontributes to structural stability, phosphostability and binding of calcium ions Kennedy, Emily N.; Menon, Smita K.; West, Ann H. FEMS Yeast Research, Vol. 16, Issue 6 https://doi.org/10.1093/femsyr/fow068	journal	August 2016
Novel regulatory cascades controlling expression of nitrogen-fixation genes in Geobacter sulfurreducens Ueki, Toshiyuki; Lovley, Derek R. Nucleic Acids Research, Vol. 38, Issue 21 https://doi.org/10.1093/nar/gkq652	journal	July 2010
Reciprocal control of motility and biofilm formation by the PdhS2 two-component sensor kinase of Agrobacterium tumefaciens Heindl, Jason E.; Crosby, Daniel; Brar, Sukhdev Microbiology, Vol. 165, Issue 2 https://doi.org/10.1099/mic.0.000758	journal	February 2019
Guiding the design of bacterial signaling interactions using a coevolutionary landscape Cheng, R. R.; Haglund, E.; Tiee, N. Research Gate https://doi.org/10.1101/116947	journal	June 2017
Inferring interaction partners from protein sequences using mutual information Bitbol, Anne-Florence PLOS Computational Biology https://doi.org/10.1101/378042	posted_content	January 2018
CrdS and CrdA Comprise a Two-Component System That Is Cooperatively Regulated by the Che3 Chemosensory System in Myxococcus xanthus Willett, Jonathan W.; Kirby, John R. mBio, Vol. 2, Issue 4 https://doi.org/10.1128/mbio.00110-11	journal	August 2011
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
Growth Phase-Dependent Proteomes of the Malaysian IsolatedLactococcus lactisDairy Strain M4 Using Label-Free Qualitative Shotgun Proteomics Analysis Yap, Theresa Wan Chen; Rabu, Amir; Abu Bakar, Farah Diba The Scientific World Journal, Vol. 2014 https://doi.org/10.1155/2014/642891	journal	January 2014
Emergence and maintenance of functional modules in signaling pathways Soyer, Orkun S. BMC Evolutionary Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2148-7-205	journal	January 2007
Systems level analysis of two-component signal transduction systems in Erwinia amylovora: Role in virulence, regulation of amylovoran biosynthesis and swarming motility Zhao, Youfu; Wang, Dongping; Nakka, Sridevi BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-245	journal	January 2009
The genetic organisation of prokaryotic two-component system signalling pathways Williams, Robert HN; Whitworth, David E. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-720	journal	December 2010
Impact of the Staphylococcus epidermidis LytSR two-component regulatory system on murein hydrolase activity, pyruvate utilization and global transcriptional profile Zhu, Tao; Lou, Qiang; Wu, Yang BMC Microbiology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2180-10-287	journal	November 2010
Systematic mapping of two component response regulators to gene targets in a model sulfate reducing bacterium Rajeev, Lara; Luning, Eric G.; Dehal, Paramvir S. Genome Biology, Vol. 12, Issue 10 https://doi.org/10.1186/gb-2011-12-10-r99	journal	January 2011
Engineered microbial biosensors based on bacterial two-component systems as synthetic biotechnology platforms in bioremediation and biorefinery Ravikumar, Sambandam; Baylon, Mary Grace; Park, Si Jae Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0675-z	journal	April 2017
Keeping Signals Straight: How Cells Process Information and Make Decisions Laub, Michael T. PLOS Biology, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pbio.1002519	journal	July 2016
The Evolution of Two-Component Systems in Bacteria Reveals Different Strategies for Niche Adaptation Alm, Eric; Huang, Katherine; Arkin, Adam PLoS Computational Biology, Vol. 2, Issue 11 https://doi.org/10.1371/journal.pcbi.0020143	journal	January 2006
Enzyme Sequestration as a Tuning Point in Controlling Response Dynamics of Signalling Networks Feng, Song; Ollivier, Julien F.; Soyer, Orkun S. PLOS Computational Biology, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pcbi.1004918	journal	May 2016
Analysis of the Legionella longbeachae Genome and Transcriptome Uncovers Unique Strategies to Cause Legionnaires' Disease Cazalet, Christel; Gomez-Valero, Laura; Rusniok, Christophe PLoS Genetics, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pgen.1000851	journal	February 2010
DNA Binding of the Cell Cycle Transcriptional Regulator GcrA Depends on N6-Adenosine Methylation in Caulobacter crescentus and Other Alphaproteobacteria Fioravanti, Antonella; Fumeaux, Coralie; Mohapatra, Saswat S. PLoS Genetics, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pgen.1003541	journal	May 2013
Identification, Functional Characterization and Regulon Prediction of a Novel Two Component System Comprising BAS0540-BAS0541 of Bacillus anthracis Gopalani, Monisha; Dhiman, Alisha; Rahi, Amit PLOS ONE, Vol. 11, Issue 7 https://doi.org/10.1371/journal.pone.0158895	journal	July 2016
Comparative Analysis ofWolbachiaGenomes Reveals Streamlining and Divergence of Minimalist Two-Component Systems Christensen, Steen; Serbus, Laura Renee G3 Genes\|Genomes\|Genetics, Vol. 5, Issue 5 https://doi.org/10.1534/g3.115.017137	journal	May 2015
Computational Exploration of Putative LuxR Solos in Archaea and Their Functional Implications in Quorum Sensing Rajput, Akanksha; Kumar, Manoj Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00798	journal	May 2017
Identification of Modules With Similar Gene Regulation and Metabolic Functions Based on Co-expression Data Galán-Vásquez, Edgardo; Perez-Rueda, Ernesto Frontiers in Molecular Biosciences, Vol. 6 https://doi.org/10.3389/fmolb.2019.00139	journal	December 2019
Inference of biomolecular interactions from sequence data Johannes, Burger, Lukas University of Basel https://doi.org/10.5451/unibas-005184854	text	January 2010
NosP Signaling Modulates the NO/H-NOX-Mediated Multicomponent c-Di-GMP Network and Biofilm Formation in Shewanella oneidensis Lisa-Marie, Nisbett,; Lucas, Binnenkade,; Bezalel, Bacon, American Chemical Society https://doi.org/10.5451/unibas-ep83582	text	January 2019
Disruption of the BMEI0066 gene attenuates the virulence of Brucella melitensis and decreases its stress tolerance Zhang, Xinglin; Ren, Jie; Li, Na International Journal of Biological Sciences https://doi.org/10.7150/ijbs.5.570	journal	January 2009

Similar Records

The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis

Journal Article · Wed Jun 29 00:00:00 EDT 2022 · PLoS Genetics · OSTI ID:1627143

Lakey, Bryan D.; Myers, Kevin S.; Alberge, François; +5 more

Systematic Dissection and Trajectory-Scanning Mutagenesis of the Molecular Interface That Ensures Specificity of Two-Component Signaling Pathways

Journal Article · Wed Nov 24 00:00:00 EST 2010 · PLoS Genetics · OSTI ID:1627143

Capra, Emily J.; Perchuk, Barrett S.; Lubin, Emma A.; +3 more

Arm-in-Arm Response Regulator Dimers Promote Intermolecular Signal Transduction

Journal Article · Mon Feb 01 00:00:00 EST 2016 · Journal of Bacteriology · OSTI ID:1627143

Baker, Anna W.; Satyshur, Kenneth A.; Moreno Morales, Neydis; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biochemistry & molecular biology
Life sciences & biomedicine - other topics
Regulator genes
Histidine
Caulobacter crescentus
Xylose
Cell cycle and cell division
Phosphorylation
Cloning
Signal transduction

Title: Two-Component Signal Transduction Pathways Regulating Growth and Cell Cycle Progression in a Bacterium: A System-Level Analysis

Citation Formats

References (62)

Cited By (115)

Similar Records

Related Subjects