DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Conformational Coupling between Receptor and Kinase Binding Sites through a Conserved Salt Bridge in a Signaling Complex Scaffold Protein

Abstract

Bacterial chemotaxis is one of the best studied signal transduction pathways. CheW is a scaffold protein that mediates the association of the chemoreceptors and the CheA kinase in a ternary signaling complex. The effects of replacing conserved Arg62 of CheW with other residues suggested that the scaffold protein plays a more complex role than simply binding its partner proteins. Although R62A CheW had essentially the same affinity for chemoreceptors and CheA, cells expressing the mutant protein are impaired in chemotaxis. Using a combination of molecular dynamics simulations (MD), NMR spectroscopy, and circular dichroism (CD), we addressed the role of Arg62. Here we show that Arg62 forms a salt bridge with another highly conserved residue, Glu38. Although this interaction is unimportant for overall protein stability, it is essential to maintain the correct alignment of the chemoreceptor and kinase binding sites of CheW. Computational and experimental data suggest that the role of the salt bridge in maintaining the alignment of the two partner binding sites is fundamental to the function of the signaling complex but not to its assembly. We conclude that a key feature of CheW is to maintain the specific geometry between the two interaction sites required for its functionmore » as a scaffold.« less

Authors:
 [1];  [2];  [2];  [2];  [3];  [2];  [4]
  1. Univ. of Tennessee, Knoxville, TN (United States). Joint Inst. for Computational Sciences; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Physics
  2. Univ. of California, Santa Barbara, CA (United States). Dept. of Chemistry and Biochemistry
  3. Univ. of Tennessee, Knoxville, TN (United States). Dept. Biochemistry and Cell and Molecular Biology; Univ. of Tennessee, Knoxville, TN (United States). Center for Molecular Biophysics
  4. Univ. of Tennessee, Knoxville, TN (United States). Joint Inst. for Computational Sciences; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH)
OSTI Identifier:
1627232
Grant/Contract Number:  
AC05-00OR22725; GM07225; GM059544
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Computational Biology (Online)
Additional Journal Information:
Journal Name: PLoS Computational Biology (Online); Journal Volume: 9; Journal Issue: 11; Journal ID: ISSN 1553-7358
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biochemistry & Molecular Biology; Mathematical & Computational Biology

Citation Formats

Ortega, Davi R., Mo, Guoya, Lee, Kwangwoon, Zhou, Hongjun, Baudry, Jerome, Dahlquist, Frederick W., and Zhulin, Igor B. Conformational Coupling between Receptor and Kinase Binding Sites through a Conserved Salt Bridge in a Signaling Complex Scaffold Protein. United States: N. p., 2013. Web. doi:10.1371/journal.pcbi.1003337.
Ortega, Davi R., Mo, Guoya, Lee, Kwangwoon, Zhou, Hongjun, Baudry, Jerome, Dahlquist, Frederick W., & Zhulin, Igor B. Conformational Coupling between Receptor and Kinase Binding Sites through a Conserved Salt Bridge in a Signaling Complex Scaffold Protein. United States. https://doi.org/10.1371/journal.pcbi.1003337
Ortega, Davi R., Mo, Guoya, Lee, Kwangwoon, Zhou, Hongjun, Baudry, Jerome, Dahlquist, Frederick W., and Zhulin, Igor B. Thu . "Conformational Coupling between Receptor and Kinase Binding Sites through a Conserved Salt Bridge in a Signaling Complex Scaffold Protein". United States. https://doi.org/10.1371/journal.pcbi.1003337. https://www.osti.gov/servlets/purl/1627232.
@article{osti_1627232,
title = {Conformational Coupling between Receptor and Kinase Binding Sites through a Conserved Salt Bridge in a Signaling Complex Scaffold Protein},
author = {Ortega, Davi R. and Mo, Guoya and Lee, Kwangwoon and Zhou, Hongjun and Baudry, Jerome and Dahlquist, Frederick W. and Zhulin, Igor B.},
abstractNote = {Bacterial chemotaxis is one of the best studied signal transduction pathways. CheW is a scaffold protein that mediates the association of the chemoreceptors and the CheA kinase in a ternary signaling complex. The effects of replacing conserved Arg62 of CheW with other residues suggested that the scaffold protein plays a more complex role than simply binding its partner proteins. Although R62A CheW had essentially the same affinity for chemoreceptors and CheA, cells expressing the mutant protein are impaired in chemotaxis. Using a combination of molecular dynamics simulations (MD), NMR spectroscopy, and circular dichroism (CD), we addressed the role of Arg62. Here we show that Arg62 forms a salt bridge with another highly conserved residue, Glu38. Although this interaction is unimportant for overall protein stability, it is essential to maintain the correct alignment of the chemoreceptor and kinase binding sites of CheW. Computational and experimental data suggest that the role of the salt bridge in maintaining the alignment of the two partner binding sites is fundamental to the function of the signaling complex but not to its assembly. We conclude that a key feature of CheW is to maintain the specific geometry between the two interaction sites required for its function as a scaffold.},
doi = {10.1371/journal.pcbi.1003337},
journal = {PLoS Computational Biology (Online)},
number = 11,
volume = 9,
place = {United States},
year = {Thu Nov 14 00:00:00 EST 2013},
month = {Thu Nov 14 00:00:00 EST 2013}
}

Works referenced in this record:

The Principles of Nuclear Magnetism
journal, November 1961


Long-timescale molecular dynamics simulations of protein structure and function
journal, April 2009

  • Klepeis, John L.; Lindorff-Larsen, Kresten; Dror, Ron O.
  • Current Opinion in Structural Biology, Vol. 19, Issue 2
  • DOI: 10.1016/j.sbi.2009.03.004

The Role of Glycine in Protein Structure
journal, October 1943

  • Neurath, Hans
  • Journal of the American Chemical Society, Vol. 65, Issue 10
  • DOI: 10.1021/ja01250a504

Evolution and dynamics of protein interactions and networks
journal, June 2008

  • Levy, Emmanuel D.; Pereira-Leal, Jose B.
  • Current Opinion in Structural Biology, Vol. 18, Issue 3
  • DOI: 10.1016/j.sbi.2008.03.003

The Pfam protein families database
journal, December 2007

  • Finn, R. D.; Tate, J.; Mistry, J.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm960

Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

Crystal structure of scaffolding protein CheW from thermoanaerobacter tengcongensis
journal, October 2007

  • Yao, Wang; Shi, Liang; Liang, Dong-Cai
  • Biochemical and Biophysical Research Communications, Vol. 361, Issue 4
  • DOI: 10.1016/j.bbrc.2007.07.130

Inter-receptor communication through arrays of bacterial chemoreceptors
journal, January 2002

  • Gestwicki, Jason E.; Kiessling, Laura L.
  • Nature, Vol. 415, Issue 6867
  • DOI: 10.1038/415081a

Long-Range Structural and Dynamical Changes Induced by Cofactor Binding in DNA Methyltransferase M.HhaI
journal, May 2007

  • Zhou, Hongjun; Shatz, Whitney; Purdy, Matthew M.
  • Biochemistry, Vol. 46, Issue 24
  • DOI: 10.1021/bi602662e

Protein Footprinting in a Complex Milieu: Identifying the Interaction Surfaces of the Chemotaxis Adaptor Protein CheW
journal, June 2011

  • Underbakke, Eric S.; Zhu, Yimin; Kiessling, Laura L.
  • Journal of Molecular Biology, Vol. 409, Issue 4
  • DOI: 10.1016/j.jmb.2011.03.040

CheW Binding Interactions with CheA and Tar: IMPORTANCE FOR CHEMOTAXIS SIGNALING IN ESCHERICHIA COLI
journal, March 2002

  • Boukhvalova, Marina S.; Dahlquist, Frederick W.; Stewart, Richard C.
  • Journal of Biological Chemistry, Vol. 277, Issue 25
  • DOI: 10.1074/jbc.M110908200

Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins
journal, February 2012

  • Briegel, A.; Li, X.; Bilwes, A. M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 10
  • DOI: 10.1073/pnas.1115719109

A perspective on non-catalytic Src homology (SH) adaptor signalling proteins
journal, February 2012


Comparison of simple potential functions for simulating liquid water
journal, July 1983

  • Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
  • The Journal of Chemical Physics, Vol. 79, Issue 2
  • DOI: 10.1063/1.445869

Reconstruction of the chemotaxis receptor–kinase assembly
journal, April 2006

  • Park, Sang-Youn; Borbat, Peter P.; Gonzalez-Bonet, Gabriela
  • Nature Structural & Molecular Biology, Vol. 13, Issue 5
  • DOI: 10.1038/nsmb1085

A 500 ps molecular dynamics simulation study of interleukin-1β in water
journal, July 1992


Transmembrane Signaling of Chemotaxis Receptor Tar: Insights from Molecular Dynamics Simulation Studies
journal, June 2011


The identification of conserved interactions within the SH3 domain by alignment of sequences and structures
journal, January 2000

  • Larson, Stefan M.; Davidson, Alan R.; Davidson, Alan R.
  • Protein Science, Vol. 9, Issue 11
  • DOI: 10.1110/ps.9.11.2170

Transmembrane signal transduction in bacterial chemotaxis involves ligand-dependent activation of phosphate group transfer.
journal, February 1989

  • Borkovich, K. A.; Kaplan, N.; Hess, J. F.
  • Proceedings of the National Academy of Sciences, Vol. 86, Issue 4
  • DOI: 10.1073/pnas.86.4.1208

Recent developments in the MAFFT multiple sequence alignment program
journal, March 2008


All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins
journal, April 1998

  • MacKerell, A. D.; Bashford, D.; Bellott, M.
  • The Journal of Physical Chemistry B, Vol. 102, Issue 18
  • DOI: 10.1021/jp973084f

Functional interactions between receptors in bacterial chemotaxis
journal, March 2004


Role of CheW protein in coupling membrane receptors to the intracellular signaling system of bacterial chemotaxis.
journal, November 1989

  • Liu, J. D.; Parkinson, J. S.
  • Proceedings of the National Academy of Sciences, Vol. 86, Issue 22
  • DOI: 10.1073/pnas.86.22.8703

Bacterial chemoreceptors: high-performance signaling in networked arrays
journal, January 2008

  • Hazelbauer, Gerald L.; Falke, Joseph J.; Parkinson, John S.
  • Trends in Biochemical Sciences, Vol. 33, Issue 1
  • DOI: 10.1016/j.tibs.2007.09.014

Constant pressure molecular dynamics simulation: The Langevin piston method
journal, September 1995

  • Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W.
  • The Journal of Chemical Physics, Vol. 103, Issue 11
  • DOI: 10.1063/1.470648

Close-Range Electrostatic Interactions in Proteins
journal, July 2002


The Receptor–CheW Binding Interface in Bacterial Chemotaxis
journal, January 2012


Precise adaptation in bacterial chemotaxis through "assistance neighborhoods"
journal, August 2006

  • Endres, R. G.; Wingreen, N. S.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 35
  • DOI: 10.1073/pnas.0603101103

Protein Dynamism and Evolvability
journal, April 2009


Disruption of chemoreceptor signalling arrays by high levels of CheW, the receptor-kinase coupling protein
journal, March 2010


Sending Signals Dynamically
journal, April 2009


Effects of Diffusion on Free Precession in Nuclear Magnetic Resonance Experiments
journal, May 1954


Conserved Glycine Residues in the Cytoplasmic Domain of the Aspartate Receptor Play Essential Roles in Kinase Coupling and On−Off Switching
journal, May 2005

  • Coleman, Matthew D.; Bass, Randal B.; Mehan, Ryan S.
  • Biochemistry, Vol. 44, Issue 21
  • DOI: 10.1021/bi0501479

Modified Spin‐Echo Method for Measuring Nuclear Relaxation Times
journal, August 1958

  • Meiboom, S.; Gill, D.
  • Review of Scientific Instruments, Vol. 29, Issue 8
  • DOI: 10.1063/1.1716296

Analysis of the backbone dynamics of interleukin-1.beta. using two-dimensional inverse detected heteronuclear nitrogen-15-proton NMR spectroscopy
journal, August 1990

  • Clore, G. Marius; Driscoll, Paul C.; Wingfield, Paul T.
  • Biochemistry, Vol. 29, Issue 32
  • DOI: 10.1021/bi00484a006

Intramolecular motions of a zinc finger DNA-binding domain from Xfin characterized by proton-detected natural abundance carbon-13 heteronuclear NMR spectroscopy
journal, June 1991

  • Palmer, Arthur G.; Rance, Mark; Wright, Peter E.
  • Journal of the American Chemical Society, Vol. 113, Issue 12
  • DOI: 10.1021/ja00012a001

Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity
journal, August 1982

  • Lipari, Giovanni; Szabo, Attila
  • Journal of the American Chemical Society, Vol. 104, Issue 17
  • DOI: 10.1021/ja00381a009

Genetic evidence for interaction between the CheW and Tsr proteins during chemoreceptor signaling by Escherichia coli.
journal, January 1991


Universal architecture of bacterial chemoreceptor arrays
journal, September 2009

  • Briegel, A.; Ortega, D. R.; Tocheva, E. I.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 40
  • DOI: 10.1073/pnas.0905181106

Making sense of it all: bacterial chemotaxis
journal, December 2004

  • Wadhams, George H.; Armitage, Judith P.
  • Nature Reviews Molecular Cell Biology, Vol. 5, Issue 12
  • DOI: 10.1038/nrm1524

Structure of CheA, a Signal-Transducing Histidine Kinase
journal, January 1999


Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors
journal, February 2007

  • Alexander, R. P.; Zhulin, I. B.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 8
  • DOI: 10.1073/pnas.0609359104

The solution structure and interactions of CheW from Thermotoga maritima
journal, January 2002

  • Griswold, Ian J.; Zhou, Hongjun; Matison, Mikenzie
  • Nature Structural Biology, Vol. 9, Issue 2
  • DOI: 10.1038/nsb753

Receptor clustering as a cellular mechanism to control sensitivity
journal, May 1998

  • Bray, Dennis; Levin, Matthew D.; Morton-Firth, Carl J.
  • Nature, Vol. 393, Issue 6680
  • DOI: 10.1038/30018

A Relaxation-Compensated Carr−Purcell−Meiboom−Gill Sequence for Characterizing Chemical Exchange by NMR Spectroscopy
journal, March 1999

  • Loria, J. Patrick; Rance, Mark; Palmer, Arthur G.
  • Journal of the American Chemical Society, Vol. 121, Issue 10
  • DOI: 10.1021/ja983961a

Backbone Dynamics ofEscherichia coliRibonuclease HI: Correlations with Structure and Function in an Active Enzyme
journal, February 1995

  • Mandel, Arthur M.; Akke, Mikael; Palmer, III, Arthur G.
  • Journal of Molecular Biology, Vol. 246, Issue 1
  • DOI: 10.1006/jmbi.1994.0073

Solution structure of the bacterial chemotaxis adaptor protein CheW from Escherichia coli
journal, September 2007

  • Li, You; Hu, Yunfei; Fu, Wenyu
  • Biochemical and Biophysical Research Communications, Vol. 360, Issue 4
  • DOI: 10.1016/j.bbrc.2007.06.146

The MiST2 database: a comprehensive genomics resource on microbial signal transduction
journal, November 2009

  • Ulrich, Luke E.; Zhulin, Igor B.
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp940

Salt bridge stability in monomeric proteins 1 1Edited by J. M. Thornton
journal, November 1999


Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells
journal, May 2012

  • Liu, J.; Hu, B.; Morado, D. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 23
  • DOI: 10.1073/pnas.1200781109

Molecular determinants of the p K a values of Asp and Glu residues in staphylococcal nuclease: p K a Values of Asp and Glu in SNase
journal, May 2009

  • Castañeda, Carlos A.; Fitch, Carolyn A.; Majumdar, Ananya
  • Proteins: Structure, Function, and Bioinformatics, Vol. 77, Issue 3
  • DOI: 10.1002/prot.22470

Nuclear Spin Relaxation in Ellipsoids Undergoing Rotational Brownian Motion
journal, August 1962

  • Woessner, D. E.
  • The Journal of Chemical Physics, Vol. 37, Issue 3
  • DOI: 10.1063/1.1701390

The Solution Structure and Interactions of CheW from Thermotoga maritima
dataset, January 2002

  • Griswold, Ian J.; Zhou, Hongjun; Matison, Mikenzie
  • Biological Magnetic Resonance Bank
  • DOI: 10.13018/bmr4984

Receptor sensitivity in bacterial chemotaxis
journal, December 2001

  • Sourjik, V.; Berg, H. C.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 1
  • DOI: 10.1073/pnas.011589998

Algorithmic Challenges in Computational Molecular Biophysics
journal, May 1999

  • Schlick, Tamar; Skeel, Robert D.; Brunger, Axel T.
  • Journal of Computational Physics, Vol. 151, Issue 1
  • DOI: 10.1006/jcph.1998.6182

Profile hidden Markov models
journal, October 1998


Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results
journal, August 1982

  • Lipari, Giovanni; Szabo, Attila
  • Journal of the American Chemical Society, Vol. 104, Issue 17
  • DOI: 10.1021/ja00381a010

Origins and Diversification of a Complex Signal Transduction System in Prokaryotes
journal, June 2010


Molecular mechanism of transmembrane signaling by the aspartate receptor: a model.
journal, March 1996

  • Chervitz, S. A.; Falke, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 6
  • DOI: 10.1073/pnas.93.6.2545

A Piston Model for Transmembrane Signaling of the Aspartate Receptor
journal, September 1999


Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

NMRPipe: A multidimensional spectral processing system based on UNIX pipes
journal, November 1995

  • Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW.
  • Journal of Biomolecular NMR, Vol. 6, Issue 3
  • DOI: 10.1007/bf00197809

ANSIG: A program for the assignment of protein 1H 2D NMR spectra by interactive computer graphics
journal, October 1989


Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway
journal, September 1992


Solution structure of the bacterial chemotaxis adaptor protein CheW from Escherichia coli
journal, September 2007

  • Li, You; Hu, Yunfei; Fu, Wenyu
  • Biochemical and Biophysical Research Communications, Vol. 360, Issue 4
  • DOI: 10.1016/j.bbrc.2007.06.146

Crystal structure of scaffolding protein CheW from thermoanaerobacter tengcongensis
journal, October 2007

  • Yao, Wang; Shi, Liang; Liang, Dong-Cai
  • Biochemical and Biophysical Research Communications, Vol. 361, Issue 4
  • DOI: 10.1016/j.bbrc.2007.07.130

A perspective on non-catalytic Src homology (SH) adaptor signalling proteins
journal, February 2012


The Receptor–CheW Binding Interface in Bacterial Chemotaxis
journal, January 2012


Evolution and dynamics of protein interactions and networks
journal, June 2008

  • Levy, Emmanuel D.; Pereira-Leal, Jose B.
  • Current Opinion in Structural Biology, Vol. 18, Issue 3
  • DOI: 10.1016/j.sbi.2008.03.003

Long-timescale molecular dynamics simulations of protein structure and function
journal, April 2009

  • Klepeis, John L.; Lindorff-Larsen, Kresten; Dror, Ron O.
  • Current Opinion in Structural Biology, Vol. 19, Issue 2
  • DOI: 10.1016/j.sbi.2009.03.004

Bacterial chemoreceptors: high-performance signaling in networked arrays
journal, January 2008

  • Hazelbauer, Gerald L.; Falke, Joseph J.; Parkinson, John S.
  • Trends in Biochemical Sciences, Vol. 33, Issue 1
  • DOI: 10.1016/j.tibs.2007.09.014

The folding and stability of titin immunoglobulin-like modules, with implications for the mechanism of elasticity
journal, December 1995


Conserved Glycine Residues in the Cytoplasmic Domain of the Aspartate Receptor Play Essential Roles in Kinase Coupling and On−Off Switching
journal, May 2005

  • Coleman, Matthew D.; Bass, Randal B.; Mehan, Ryan S.
  • Biochemistry, Vol. 44, Issue 21
  • DOI: 10.1021/bi0501479

All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins
journal, April 1998

  • MacKerell, A. D.; Bashford, D.; Bellott, M.
  • The Journal of Physical Chemistry B, Vol. 102, Issue 18
  • DOI: 10.1021/jp973084f

Inter-receptor communication through arrays of bacterial chemoreceptors
journal, January 2002

  • Gestwicki, Jason E.; Kiessling, Laura L.
  • Nature, Vol. 415, Issue 6867
  • DOI: 10.1038/415081a

Functional interactions between receptors in bacterial chemotaxis
journal, March 2004


Making sense of it all: bacterial chemotaxis
journal, December 2004

  • Wadhams, George H.; Armitage, Judith P.
  • Nature Reviews Molecular Cell Biology, Vol. 5, Issue 12
  • DOI: 10.1038/nrm1524

The solution structure and interactions of CheW from Thermotoga maritima
journal, January 2002

  • Griswold, Ian J.; Zhou, Hongjun; Matison, Mikenzie
  • Nature Structural Biology, Vol. 9, Issue 2
  • DOI: 10.1038/nsb753

Bacterial chemotaxis and the question of gain
journal, January 2002


Precise adaptation in bacterial chemotaxis through "assistance neighborhoods"
journal, August 2006

  • Endres, R. G.; Wingreen, N. S.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 35
  • DOI: 10.1073/pnas.0603101103

Ancient chemoreceptors retain their flexibility
journal, February 2007

  • Parkinson, John S.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 8
  • DOI: 10.1073/pnas.0700278104

Universal architecture of bacterial chemoreceptor arrays
journal, September 2009

  • Briegel, A.; Ortega, D. R.; Tocheva, E. I.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 40
  • DOI: 10.1073/pnas.0905181106

Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins
journal, February 2012

  • Briegel, A.; Li, X.; Bilwes, A. M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 10
  • DOI: 10.1073/pnas.1115719109

Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells
journal, May 2012

  • Liu, J.; Hu, B.; Morado, D. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 23
  • DOI: 10.1073/pnas.1200781109

Role of CheW protein in coupling membrane receptors to the intracellular signaling system of bacterial chemotaxis.
journal, November 1989

  • Liu, J. D.; Parkinson, J. S.
  • Proceedings of the National Academy of Sciences, Vol. 86, Issue 22
  • DOI: 10.1073/pnas.86.22.8703

Molecular mechanism of transmembrane signaling by the aspartate receptor: a model.
journal, March 1996

  • Chervitz, S. A.; Falke, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 6
  • DOI: 10.1073/pnas.93.6.2545

Profile hidden Markov models
journal, October 1998


The Pfam protein families database
journal, December 2007

  • Finn, R. D.; Tate, J.; Mistry, J.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm960

The MiST2 database: a comprehensive genomics resource on microbial signal transduction
journal, November 2009

  • Ulrich, Luke E.; Zhulin, Igor B.
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp940

The identification of conserved interactions within the SH3 domain by alignment of sequences and structures
journal, January 2000

  • Larson, Stefan M.; Davidson, Alan R.; Davidson, Alan R.
  • Protein Science, Vol. 9, Issue 11
  • DOI: 10.1110/ps.9.11.2170

Protein Dynamism and Evolvability
journal, April 2009


Origins and Diversification of a Complex Signal Transduction System in Prokaryotes
journal, June 2010


Genetic evidence for interaction between the CheW and Tsr proteins during chemoreceptor signaling by Escherichia coli.
journal, January 1991


Works referencing / citing this record:

Coupling chemosensory array formation and localization
journal, October 2017


Conformational sampling of CpxA: Connecting HAMP motions to the histidine kinase function
journal, November 2018


CryoEM and computer simulations reveal a novel kinase conformational switch in bacterial chemotaxis signaling
journal, November 2015

  • Cassidy, C. Keith; Himes, Benjamin A.; Alvarez, Frances J.
  • eLife, Vol. 4
  • DOI: 10.7554/elife.08419

Assigning chemoreceptors to chemosensory pathways in Pseudomonas aeruginosa
journal, November 2017

  • Ortega, Davi R.; Fleetwood, Aaron D.; Krell, Tino
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 48
  • DOI: 10.1073/pnas.1708842114

CryoEM and computer simulations reveal a novel kinase conformational switch in bacterial chemotaxis signaling
journal, November 2015

  • Cassidy, C. Keith; Himes, Benjamin A.; Alvarez, Frances J.
  • eLife, Vol. 4
  • DOI: 10.7554/elife.08419