Atypical Response Regulator ChxR from Chlamydia trachomatis Is Structurally Poised for DNA Binding

Barta, Michael L.; Hickey, John M.; Anbanandam, Asokan; Dyer, Kevin; Hammel, Michal; Hefty, P. Scott

doi:10.1371/journal.pone.0091760

Title: **Atypical Response Regulator ChxR from Chlamydia trachomatis Is Structurally Poised for DNA Binding**

Journal Article · Wed Mar 19 00:00:00 EDT 2014 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0091760· OSTI ID:1627685

Barta, Michael L. ^[1]; Hickey, John M. ^[1]; Anbanandam, Asokan ^[1]; Dyer, Kevin ^[2]; Hammel, Michal ^[2]; Hefty, P. Scott ^[1]

University of Kansas, Lawrence, KS (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

ChxR is an atypical two-component signal transduction response regulator (RR) of the OmpR/PhoB subfamily encoded by the obligate intracellular bacterial pathogen Chlamydia trachomatis. Despite structural homology within both receiver and effector domains to prototypical subfamily members, ChxR does not require phosphorylation for dimer formation, DNA binding or transcriptional activation. Thus, we hypothesized that ChxR is in a conformation optimal for DNA binding with limited interdomain interactions. To address this hypothesis, the NMR solution structure of the ChxR effector domain was determined and used in combination with the previously reported ChxR receiver domain structure to generate a full-length dimer model based upon SAXS analysis. Small-angle scattering of ChxR supported a dimer with minimal interdomain interactions and effector domains in a conformation that appears to require only subtle reorientation for optimal major/ minor groove DNA interactions. SAXS modeling also supported that the effector domains were in a head-to-tail conformation, consistent with ChxR recognizing tandem DNA repeats. The effector domain structure was leveraged to identify key residues that were critical for maintaining protein - nucleic acid interactions. In combination with prior analysis of the essential location of specific nucleotides for ChxR recognition of DNA, a model of the full-length ChxR dimer bound to its cognate cis-acting element was generated.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC02-05CH11231; AIR01079083

OSTI ID:: 1627685

Journal Information:: PLoS ONE, Vol. 9, Issue 3; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (76)

The DNA-binding domain of OmpR: crystal structures of a winged helix transcription factor Martínez-Hackert, Erik; Stock, Ann M. Structure, Vol. 5, Issue 1 https://doi.org/10.1016/S0969-2126(97)00170-6	journal	January 1997
Structure of a Glomulin-RBX1-CUL1 Complex: Inhibition of a RING E3 Ligase through Masking of Its E2-Binding Surface Duda, David M.; Olszewski, Jennifer L.; Tron, Adriana E. Molecular Cell, Vol. 47, Issue 3 https://doi.org/10.1016/j.molcel.2012.05.044	journal	August 2012
Expression, purification, crystallization and preliminary X-ray analysis of the DNA-binding domain of a Chlamydia trachomatis OmpR/PhoB-subfamily response regulator homolog, ChxR Hickey, John M.; Hefty, P. Scott; Lamb, Audrey L. Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 65, Issue 8 https://doi.org/10.1107/S1744309109025184	journal	July 2009
Structural insights into the interaction of IL-33 with its receptors Liu, X.; Hammel, M.; He, Y. Proceedings of the National Academy of Sciences, Vol. 110, Issue 37 https://doi.org/10.1073/pnas.1308651110	journal	August 2013
The structure of a transcription activation subcomplex reveals how σ ⁷⁰ is recruited to PhoB promoters : Structure of a transcription activation subcomplex Blanco, Alexandre G.; Canals, Albert; Bernués, Jordi The EMBO Journal, Vol. 30, Issue 18 https://doi.org/10.1038/emboj.2011.271	journal	August 2011
Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering Bernadó, Pau; Svergun, Dmitri I. Mol. BioSyst., Vol. 8, Issue 1 https://doi.org/10.1039/C1MB05275F	journal	January 2012
Development of a Transformation System for Chlamydia trachomatis: Restoration of Glycogen Biosynthesis by Acquisition of a Plasmid Shuttle Vector Wang, Yibing; Kahane, Simona; Cutcliffe, Lesley T. PLoS Pathogens, Vol. 7, Issue 9 https://doi.org/10.1371/journal.ppat.1002258	journal	September 2011
Allosteric inhibition of complement function by a staphylococcal immune evasion protein Chen, Hui; Ricklin, Daniel; Hammel, Michal Proceedings of the National Academy of Sciences, Vol. 107, Issue 41 https://doi.org/10.1073/pnas.1003750107	journal	September 2010
DNA Binding of PhoB and its Interaction with RNA Polymerase Makino, Kozo; Amemura, Mitsuko; Kawamoto, Takeshi Journal of Molecular Biology, Vol. 259, Issue 1 https://doi.org/10.1006/jmbi.1996.0298	journal	May 1996
Structural basis for viral 5′-PPP-RNA recognition by human IFIT proteins Abbas, Yazan M.; Pichlmair, Andreas; Górna, Maria W. Nature, Vol. 494, Issue 7435 https://doi.org/10.1038/nature11783	journal	January 2013
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
Structure of the Response Regulator PhoP from Mycobacterium tuberculosis Reveals a Dimer through the Receiver Domain Menon, Smita; Wang, Shuishu Biochemistry, Vol. 50, Issue 26 https://doi.org/10.1021/bi2005575	journal	July 2011
Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution Koch, Michel H. J.; Vachette, Patrice; Svergun, Dmitri I. Quarterly Reviews of Biophysics, Vol. 36, Issue 2 https://doi.org/10.1017/S0033583503003871	journal	May 2003
The Structural Basis of Signal Transduction for the Response Regulator PrrA from Mycobacterium tuberculosis Nowak, Elzbieta; Panjikar, Santosh; Konarev, Peter Journal of Biological Chemistry, Vol. 281, Issue 14 https://doi.org/10.1074/jbc.M512004200	journal	January 2006
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
Residues Required for Bacillus subtilis PhoP DNA Binding or RNA Polymerase Interaction: Alanine Scanning of PhoP Effector Domain Transactivation Loop and α Helix 3 Chen, Yinghua; Abdel-Fattah, Wael R.; Hulett, F. Marion Journal of Bacteriology, Vol. 186, Issue 5 https://doi.org/10.1128/JB.186.5.1493-1502.2004	journal	March 2004
Escherichia coli positive regulator OmpR has a large loop structure at the putative RNA polymerase interaction site Kondo, Hidemasa; Nakagawa, Atsushi; Nishihira, Jun Nature Structural & Molecular Biology, Vol. 4, Issue 1 https://doi.org/10.1038/nsb0197-28	journal	January 1997
Role of the sigma 70 subunit of RNA polymerase in transcriptional activation by activator protein PhoB in Escherichia coli. Makino, K.; Amemura, M.; Kim, S. K. Genes & Development, Vol. 7, Issue 1 https://doi.org/10.1101/gad.7.1.149	journal	January 1993
Backbone dynamics of proteins as studied by nitrogen-15 inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease Kay, Lewis E.; Torchia, Dennis A.; Bax, Ad Biochemistry, Vol. 28, Issue 23 https://doi.org/10.1021/bi00449a003	journal	November 1989
X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution Putnam, Christopher D.; Hammel, Michal; Hura, Greg L. Quarterly Reviews of Biophysics, Vol. 40, Issue 3 https://doi.org/10.1017/S0033583507004635	journal	August 2007
Enhancement of RNA polymerase binding to promoters by a transcriptional activator, OmpR, in Escherichia coli: its positive and negative effects on transcription. Tsung, K.; Brissette, R. E.; Inouye, M. Proceedings of the National Academy of Sciences, Vol. 87, Issue 15 https://doi.org/10.1073/pnas.87.15.5940	journal	August 1990
Accurate SAXS Profile Computation and its Assessment by Contrast Variation Experiments Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Biophysical Journal, Vol. 105, Issue 4 https://doi.org/10.1016/j.bpj.2013.07.020	journal	August 2013
Super-Resolution in Solution X-Ray Scattering and Its Applications to Structural Systems Biology Rambo, Robert P.; Tainer, John A. Annual Review of Biophysics, Vol. 42, Issue 1 https://doi.org/10.1146/annurev-biophys-083012-130301	journal	May 2013
A common dimerization interface in bacterial response regulators KdpE and TorR Toro-Roman, Alejandro; Wu, Ti; Stock, Ann M. Protein Science, Vol. 14, Issue 12 https://doi.org/10.1110/ps.051722805	journal	December 2005
Mechanism of Activation for Transcription Factor PhoB Suggested by Different Modes of Dimerization in the Inactive and Active States Bachhawat, Priti; Swapna, G. V. T.; Montelione, Gaetano T. Structure, Vol. 13, Issue 9 https://doi.org/10.1016/j.str.2005.06.006	journal	September 2005
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
ChxR is a transcriptional activator in Chlamydia Koo, I. C.; Walthers, D.; Hefty, P. S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 3 https://doi.org/10.1073/pnas.0509690103	journal	January 2006
Growth Phase-Dependent Regulation of Target Gene Promoters for Binding of the Essential Orphan Response Regulator HP1043 of Helicobacter pylori Delany, Isabel; Spohn, Gunther; Rappuoli, Rino Journal of Bacteriology, Vol. 184, Issue 17 https://doi.org/10.1128/JB.184.17.4800-4810.2002	journal	September 2002
ESPript: analysis of multiple sequence alignments in PostScript Gouet, P.; Courcelle, E.; Stuart, D. Bioinformatics, Vol. 15, Issue 4 https://doi.org/10.1093/bioinformatics/15.4.305	journal	April 1999
The Structure of a Full-length Response Regulator from Mycobacterium tuberculosis in a Stabilized Three-dimensional Domain-swapped, Activated State King-Scott, Jack; Nowak, Elzbieta; Mylonas, Efstratios Journal of Biological Chemistry, Vol. 282, Issue 52 https://doi.org/10.1074/jbc.M705081200	journal	December 2007
Conditional Gene Expression in Chlamydia trachomatis Using the Tet System Wickstrum, Jason; Sammons, Lindsay R.; Restivo, Keasha N. PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0076743	journal	October 2013
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) Hura, Greg L.; Menon, Angeli L.; Hammel, Michal Nature Methods, Vol. 6, Issue 8 https://doi.org/10.1038/nmeth.1353	journal	July 2009
Validation of macromolecular flexibility in solution by small-angle X-ray scattering (SAXS) Hammel, Michal European Biophysics Journal, Vol. 41, Issue 10 https://doi.org/10.1007/s00249-012-0820-x	journal	May 2012
The Immunoglobulin-like Domains 1 and 2 of the Protein Tyrosine Phosphatase LAR Adopt an Unusual Horseshoe-like Conformation Biersmith, Bridget H.; Hammel, Michal; Geisbrecht, Erika R. Journal of Molecular Biology, Vol. 408, Issue 4 https://doi.org/10.1016/j.jmb.2011.03.013	journal	May 2011
Site-Specific, Insertional Inactivation of incA in Chlamydia trachomatis Using a Group II Intron Johnson, Cayla M.; Fisher, Derek J. PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0083989	journal	December 2013
Domain Orientation in the Inactive Response Regulator Mycobacterium tuberculosis MtrA Provides a Barrier to Activation ^† ^, ^‡ Friedland, Natalia; Mack, Timothy R.; Yu, Minmin Biochemistry, Vol. 46, Issue 23 https://doi.org/10.1021/bi602546q	journal	June 2007
Structure of the DNA-Binding Domain of the Response Regulator PhoP from Mycobacterium tuberculosis ^, Wang, Shuishu; Engohang-Ndong, Jean; Smith, Issar Biochemistry, Vol. 46, Issue 51 https://doi.org/10.1021/bi700970a	journal	December 2007
Generation of targeted Chlamydia trachomatis null mutants Kari, L.; Goheen, M. M.; Randall, L. B. Proceedings of the National Academy of Sciences, Vol. 108, Issue 17 https://doi.org/10.1073/pnas.1102229108	journal	April 2011
Structure-Function Studies of DNA Binding Domain of Response Regulator KdpE Reveals Equal Affinity Interactions at DNA Half-Sites Narayanan, Anoop; Paul, Lake N.; Tomar, Sakshi PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0030102	journal	January 2012
Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level Luscombe, N. M. Nucleic Acids Research, Vol. 29, Issue 13 https://doi.org/10.1093/nar/29.13.2860	journal	July 2001
Crystal structure analysis of a complete turn of B-DNA Wing, Richard; Drew, Horace; Takano, Tsunehiro Nature, Vol. 287, Issue 5784 https://doi.org/10.1038/287755a0	journal	October 1980
Amino Acids Important for DNA Recognition by the Response Regulator OmpR Rhee, Jee Eun; Sheng, Wanyun; Morgan, Leslie K. Journal of Biological Chemistry, Vol. 283, Issue 13 https://doi.org/10.1074/jbc.M705550200	journal	March 2008
Phosphorylation-independent activation of the atypical response regulator NblR Ruiz, Diego; Salinas, Paloma; Lopez-Redondo, Maria Luisa Microbiology, Vol. 154, Issue 10 https://doi.org/10.1099/mic.0.2008/020677-0	journal	October 2008
FoXS: a web server for rapid computation and fitting of SAXS profiles Schneidman-Duhovny, D.; Hammel, M.; Sali, A. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq461	journal	May 2010
Structural Analysis of the Domain Interface in DrrB, a Response Regulator of the OmpR/PhoB Subfamily Robinson, V. L.; Wu, T.; Stock, A. M. Journal of Bacteriology, Vol. 185, Issue 14 https://doi.org/10.1128/JB.185.14.4186-4194.2003	journal	July 2003
AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR Laskowski, RomanA.; Rullmann, J. AntoonC.; MacArthur, MalcolmW. Journal of Biomolecular NMR, Vol. 8, Issue 4 https://doi.org/10.1007/BF00228148	journal	December 1996
Restoring Low Resolution Structure of Biological Macromolecules from Solution Scattering Using Simulated Annealing Svergun, D. I. Biophysical Journal, Vol. 76, Issue 6, p. 2879-2886 https://doi.org/10.1016/S0006-3495(99)77443-6	journal	June 1999
Comprehensive macromolecular conformations mapped by quantitative SAXS analyses Hura, Greg L.; Budworth, Helen; Dyer, Kevin N. Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2453	journal	April 2013
TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts Shen, Yang; Delaglio, Frank; Cornilescu, Gabriel Journal of Biomolecular NMR, Vol. 44, Issue 4 https://doi.org/10.1007/s10858-009-9333-z	journal	June 2009
Backbone Dynamics of a Free and a Phosphopeptide-Complexed Src Homology 2 Domain Studied by 15N NMR Relaxation Farrow, Neil A.; Muhandiram, Ranjith; Singer, Alex U. Biochemistry, Vol. 33, Issue 19 https://doi.org/10.1021/bi00185a040	journal	May 1994
An atypical receiver domain controls the dynamic polar localization of the Myxococcus xanthus social motility protein FrzS Fraser, James S.; Merlie, John P.; Echols, Nathaniel Molecular Microbiology, Vol. 65, Issue 2 https://doi.org/10.1111/j.1365-2958.2007.05785.x	journal	July 2007
The Protein Data Bank. A Computer-Based Archival File for Macromolecular Structures Bernstein, Frances C.; Koetzle, Thomas F.; Williams, Graheme J. B. European Journal of Biochemistry, Vol. 80, Issue 2 https://doi.org/10.1111/j.1432-1033.1977.tb11885.x	journal	November 1977
Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients Sattler, M. Progress in Nuclear Magnetic Resonance Spectroscopy, Vol. 34, Issue 2 https://doi.org/10.1016/S0079-6565(98)00025-9	journal	March 1999
Version 1.2 of the Crystallography and NMR system Brunger, Axel T. Nature Protocols, Vol. 2, Issue 11 https://doi.org/10.1038/nprot.2007.406	journal	October 2007
Structural characterization of proteins and complexes using small-angle X-ray solution scattering Mertens, Haydyn D. T.; Svergun, Dmitri I. Journal of Structural Biology, Vol. 172, Issue 1 https://doi.org/10.1016/j.jsb.2010.06.012	journal	October 2010
NMRPipe: A multidimensional spectral processing system based on UNIX pipes Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW. Journal of Biomolecular NMR, Vol. 6, Issue 3 https://doi.org/10.1007/BF00197809	journal	November 1995
Structural comparison of the PhoB and OmpR DNA-binding/transactivation domains and the arrangement of PhoB molecules on the phosphate box Okamura, Hideyasu; Hanaoka, Shingo; Nagadoi, Aritaka Journal of Molecular Biology, Vol. 295, Issue 5 https://doi.org/10.1006/jmbi.1999.3379	journal	February 2000
Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law Rambo, Robert P.; Tainer, John A. Biopolymers, Vol. 95, Issue 8 https://doi.org/10.1002/bip.21638	journal	April 2011
Structure and flexibility within proteins as identified through small angle X-ray scattering Pelikan, M.; Hura, G.; Hammel, M. General Physiology and Biophysics, Vol. 28, Issue 2 https://doi.org/10.4149/gpb_2009_02_174	journal	January 2009
Genome Sequence of an Obligate Intracellular Pathogen of Humans: Chlamydia trachomatis Stephens, R. S. Science, Vol. 282, Issue 5389 https://doi.org/10.1126/science.282.5389.754	journal	October 1998
LGA: a method for finding 3D similarities in protein structures Zemla, A. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg571	journal	July 2003
Accurate assessment of mass, models and resolution by small-angle scattering Rambo, Robert P.; Tainer, John A. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12070	journal	April 2013
Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: Applications to the molecular systems and geometric objects Rocchia, Walter; Sridharan, Sundaram; Nicholls, Anthony Journal of Computational Chemistry, Vol. 23, Issue 1 https://doi.org/10.1002/jcc.1161	journal	November 2001
Structural Analysis and Solution Studies of the Activated Regulatory Domain of the Response Regulator ArcA: A Symmetric Dimer Mediated by the α4-β5-α5 Face Toro-Roman, Alejandro; Mack, Timothy R.; Stock, Ann M. Journal of Molecular Biology, Vol. 349, Issue 1 https://doi.org/10.1016/j.jmb.2005.03.059	journal	May 2005
The Atypical Response Regulator Protein ChxR Has Structural Characteristics and Dimer Interface Interactions That Are Unique within the OmpR/PhoB Subfamily Hickey, John M.; Lovell, Scott; Battaile, Kevin P. Journal of Biological Chemistry, Vol. 286, Issue 37 https://doi.org/10.1074/jbc.M111.220574	journal	July 2011
Tandem DNA Recognition by PhoB, a Two-Component Signal Transduction Transcriptional Activator Blanco, Alexandre G.; Sola, Maria; Gomis-Rüth, F. Xavier Structure, Vol. 10, Issue 5 https://doi.org/10.1016/S0969-2126(02)00761-X	journal	May 2002
Expression and Targeting of Secreted Proteins from Chlamydia trachomatis Bauler, L. D.; Hackstadt, T. Journal of Bacteriology, Vol. 196, Issue 7 https://doi.org/10.1128/JB.01290-13	journal	January 2014
Evidence of Intradomain and Interdomain Flexibility in an OmpR/PhoB Homolog from Thermotoga maritima Buckler, David R.; Zhou, Yuchen; Stock, Ann M. Structure, Vol. 10, Issue 2 https://doi.org/10.1016/s0969-2126(01)00706-7	journal	February 2002
Structure/function relationships in OmpR and other winged-helix transcription factors Kenney, L. Current Opinion in Microbiology, Vol. 5, Issue 2 https://doi.org/10.1016/s1369-5274(02)00310-7	journal	April 2002
Regulation of Response Regulator Autophosphorylation through Interdomain Contacts Barbieri, Christopher M.; Mack, Timothy R.; Robinson, Victoria L. Journal of Biological Chemistry, Vol. 285, Issue 42 https://doi.org/10.1074/jbc.m110.157164	journal	August 2010
Structure of an Atypical Orphan Response Regulator Protein Supports a New Phosphorylation-independent Regulatory Mechanism Hong, Eunmi; Lee, Hyang Mi; Ko, Hyunsook Journal of Biological Chemistry, Vol. 282, Issue 28 https://doi.org/10.1074/jbc.m609104200	journal	May 2007
Structural Analysis of the DNA-binding Domain of the Helicobacter pylori Response Regulator ArsR Gupta, Shobhana S.; Borin, Brendan N.; Cover, Timothy L. Journal of Biological Chemistry, Vol. 284, Issue 10 https://doi.org/10.1074/jbc.m804592200	journal	March 2009
Chlamydia: Old Ideas Crushed, New Mysteries Bared Hatch, Thomas Science, Vol. 282, Issue 5389 https://doi.org/10.1126/science.282.5389.638	journal	October 1998
The Atypical OmpR/PhoB Response Regulator ChxR from Chlamydia trachomatis Forms Homodimers In Vivo and Binds a Direct Repeat of Nucleotide Sequences Hickey, J. M.; Weldon, L.; Hefty, P. S. Journal of Bacteriology, Vol. 193, Issue 2 https://doi.org/10.1128/jb.00833-10	journal	November 2010
Phosphorylation-Independent Activity of Atypical Response Regulators of Helicobacter pylori Schär, Jennifer; Sickmann, Albert; Beier, Dagmar Journal of Bacteriology, Vol. 187, Issue 9 https://doi.org/10.1128/jb.187.9.3100-3109.2005	journal	May 2005

Cited By (2)

Chlamydia cell biology and pathogenesis Elwell, Cherilyn; Mirrashidi, Kathleen; Engel, Joanne Nature Reviews Microbiology, Vol. 14, Issue 6 https://doi.org/10.1038/nrmicro.2016.30	journal	April 2016
To ∼P or Not to ∼P? Non-canonical activation by two-component response regulators: Non-canonical RR activation Desai, Stuti K.; Kenney, Linda J. Molecular Microbiology, Vol. 103, Issue 2 https://doi.org/10.1111/mmi.13532	journal	October 2016

Similar Records

The Atypical Response Regulator Protein ChxR Has Structural Characteristics and Dimer Interface Interactions That Are Unique within the OmpR/PhoB Subfamily

Journal Article · Wed May 29 00:00:00 EDT 2013 · J. Biol. Chem. · OSTI ID:1627685

Hickey, John M.; Lovell, Scott; Battaile, Kevin P.; +3 more

Regulation of Response Regulator Autophosphorylation through Interdomain Contacts

Journal Article · Fri Jan 01 00:00:00 EST 2010 · Journal of Biological Chemistry · OSTI ID:1627685

Barbieri, C; Mack, T; Robinson, V; +2 more

Structure of the Response Regulator PhoP from Mycobacterium tuberculosis Reveals a Dimer Through the Receiver Domain

Journal Article · Sat Dec 31 00:00:00 EST 2011 · Biochemistry (Eaton) · OSTI ID:1627685

Menon, S; Wang, S

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
small-angle scattering
protein structure
phosphorylation
DNAS structure
DNA-binding
proteins
dimers
NMR spectroscopy
root structure

Title: Atypical Response Regulator ChxR from Chlamydia trachomatis Is Structurally Poised for DNA Binding

Citation Formats

References (76)

Cited By (2)

Similar Records

Related Subjects

Title: **Atypical Response Regulator ChxR from Chlamydia trachomatis Is Structurally Poised for DNA Binding**