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Title: Tuning site-specific dynamics to drive allosteric activation in a pneumococcal zinc uptake regulator

Abstract

MarR (multiple antibiotic resistance repressor) family proteins are bacterial repressors that regulate transcription in response to a wide range of chemical signals. Although specific features of MarR family function have been described, the role of atomic motions in MarRs remains unexplored thus limiting insights into the evolution of allostery in this ubiquitous family of repressors. Here, we provide the first experimental evidence that internal dynamics play a crucial functional role in MarR proteins. Streptococcus pneumoniae AdcR (adhesin-competence repressor) regulates ZnII homeostasis and ZnII functions as an allosteric activator of DNA binding. ZnII coordination triggers a transition from somewhat independent domains to a more compact structure. We identify residues that impact allosteric activation on the basis of ZnII-induced perturbations of atomic motions over a wide range of timescales. These findings appear to reconcile the distinct allosteric mechanisms proposed for other MarRs and highlight the importance of conformational dynamics in biological regulation.

Authors:
ORCiD logo [1];  [2];  [1];  [1];  [1]; ORCiD logo [3]
  1. Department of Chemistry, Indiana University, Bloomington, United States
  2. Department of Chemistry, Indiana University, Bloomington, United States; Graduate Program in Biochemistry, Indiana University, Bloomington, United States
  3. Department of Chemistry, Indiana University, Bloomington, United States; Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, United States
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
NIHOTHER
OSTI Identifier:
1502254
Resource Type:
Journal Article
Journal Name:
eLife
Additional Journal Information:
Journal Volume: 7; Journal Issue: 10, 2018; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
ENGLISH

Citation Formats

Capdevila, Daiana A., Huerta, Fidel, Edmonds, Katherine A., Le, My Tra, Wu, Hongwei, and Giedroc, David P. Tuning site-specific dynamics to drive allosteric activation in a pneumococcal zinc uptake regulator. United States: N. p., 2018. Web. doi:10.7554/eLife.37268.
Capdevila, Daiana A., Huerta, Fidel, Edmonds, Katherine A., Le, My Tra, Wu, Hongwei, & Giedroc, David P. Tuning site-specific dynamics to drive allosteric activation in a pneumococcal zinc uptake regulator. United States. doi:10.7554/eLife.37268.
Capdevila, Daiana A., Huerta, Fidel, Edmonds, Katherine A., Le, My Tra, Wu, Hongwei, and Giedroc, David P. Wed . "Tuning site-specific dynamics to drive allosteric activation in a pneumococcal zinc uptake regulator". United States. doi:10.7554/eLife.37268.
@article{osti_1502254,
title = {Tuning site-specific dynamics to drive allosteric activation in a pneumococcal zinc uptake regulator},
author = {Capdevila, Daiana A. and Huerta, Fidel and Edmonds, Katherine A. and Le, My Tra and Wu, Hongwei and Giedroc, David P.},
abstractNote = {MarR (multiple antibiotic resistance repressor) family proteins are bacterial repressors that regulate transcription in response to a wide range of chemical signals. Although specific features of MarR family function have been described, the role of atomic motions in MarRs remains unexplored thus limiting insights into the evolution of allostery in this ubiquitous family of repressors. Here, we provide the first experimental evidence that internal dynamics play a crucial functional role in MarR proteins. Streptococcus pneumoniae AdcR (adhesin-competence repressor) regulates ZnII homeostasis and ZnII functions as an allosteric activator of DNA binding. ZnII coordination triggers a transition from somewhat independent domains to a more compact structure. We identify residues that impact allosteric activation on the basis of ZnII-induced perturbations of atomic motions over a wide range of timescales. These findings appear to reconcile the distinct allosteric mechanisms proposed for other MarRs and highlight the importance of conformational dynamics in biological regulation.},
doi = {10.7554/eLife.37268},
journal = {eLife},
issn = {2050-084X},
number = 10, 2018,
volume = 7,
place = {United States},
year = {2018},
month = {10}
}

Works referenced in this record:

Allosteric inhibition through suppression of transient conformational states
journal, May 2013

  • Tzeng, Shiou-Ru; Kalodimos, Charalampos G.
  • Nature Chemical Biology, Vol. 9, Issue 7
  • DOI: 10.1038/nchembio.1250

The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative
journal, April 2002

  • Fuangthong, M.; Helmann, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 10
  • DOI: 10.1073/pnas.102483199

Ni(II) coordination to mixed sites modulates DNA binding of HpNikR via a long-range effect
journal, March 2012

  • West, A. L.; Evans, S. E.; Gonzalez, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 15
  • DOI: 10.1073/pnas.1120283109

The role of conformational entropy in molecular recognition by calmodulin
journal, April 2010

  • Marlow, Michael S.; Dogan, Jakob; Frederick, Kendra K.
  • Nature Chemical Biology, Vol. 6, Issue 5
  • DOI: 10.1038/nchembio.347

Molecular Mechanisms of Ligand-Mediated Attenuation of DNA Binding by MarR Family Transcriptional Regulators
journal, August 2010

  • Perera, I. C.; Grove, A.
  • Journal of Molecular Cell Biology, Vol. 2, Issue 5
  • DOI: 10.1093/jmcb/mjq021

Resonance assignments of the metal sensor CzrA in the apo-, Zn2- and DNA-bound (42 kDa) states
journal, July 2007

  • Arunkumar, Alphonse I.; Pennella, Mario A.; Kong, Xiangming
  • Biomolecular NMR Assignments, Vol. 1, Issue 1
  • DOI: 10.1007/s12104-007-9027-y

Critical biophysical properties in the Pseudomonas aeruginosa efflux gene regulator MexR are targeted by mutations conferring multidrug resistance
journal, January 2010

  • Andrésen, Cecilia; Jalal, Shah; Aili, Daniel
  • Protein Science, Vol. 19, Issue 4
  • DOI: 10.1002/pro.343

DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering
journal, January 2009

  • Franke, Daniel; Svergun, Dmitri I.
  • Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346
  • DOI: 10.1107/S0021889809000338

An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus
journal, September 2006

  • Chen, Peng R.; Bae, Taeok; Williams, Wade A.
  • Nature Chemical Biology, Vol. 2, Issue 11
  • DOI: 10.1038/nchembio820

Regulation of virulence by members of the MarR/SlyA family
journal, April 2006


Protein activity regulation by conformational entropy
journal, July 2012

  • Tzeng, Shiou-Ru; Kalodimos, Charalampos G.
  • Nature, Vol. 488, Issue 7410
  • DOI: 10.1038/nature11271

Histidine switch controlling pH-dependent protein folding and DNA binding in a transcription factor at the core of synthetic network devices
journal, January 2016

  • Deochand, D. K.; Perera, I. C.; Crochet, R. B.
  • Molecular BioSystems, Vol. 12, Issue 8
  • DOI: 10.1039/C6MB00304D

Structural characterization of the DNA-binding mechanism underlying the copper(II)-sensing MarR transcriptional regulator
journal, January 2017

  • Zhu, Rongfeng; Hao, Ziyang; Lou, Hubing
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 22, Issue 5
  • DOI: 10.1007/s00775-017-1442-7

Faithful estimation of dynamics parameters from CPMG relaxation dispersion measurements
journal, May 2006

  • Kovrigin, Evgenii L.; Kempf, James G.; Grey, Michael J.
  • Journal of Magnetic Resonance, Vol. 180, Issue 1
  • DOI: 10.1016/j.jmr.2006.01.010

Involvement of the adc Operon and Manganese Homeostasis in Streptococcus gordonii Biofilm Formation
journal, May 2003


Structural study of TcaR and its complexes with multiple antibiotics from Staphylococcus epidermidis
journal, April 2010

  • Chang, Y. -M.; Jeng, W. -Y.; Ko, T. -P.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 19
  • DOI: 10.1073/pnas.0913302107

Regulation of Metabolic Pathways by MarR Family Transcription Factors
journal, January 2017


Role of the semi-conserved histidine residue in the light-sensing domain of LitR, a MerR-type photosensory transcriptional regulator
journal, August 2016

  • Takano, Hideaki; Mise, Kou; Maruyama, Takafumi
  • Microbiology, Vol. 162, Issue 8
  • DOI: 10.1099/mic.0.000321

Coordinated Regulation of Virulence during Systemic Infection of Salmonella enterica Serovar Typhimurium
journal, February 2009


Crystal Structure of the Transcriptional Regulator Rv0678 of Mycobacterium tuberculosis
journal, April 2014

  • Radhakrishnan, Abhijith; Kumar, Nitin; Wright, Catherine C.
  • Journal of Biological Chemistry, Vol. 289, Issue 23
  • DOI: 10.1074/jbc.M113.538959

MarR family transcription factors: dynamic variations on a common scaffold
journal, July 2017


Thermal Offset Viscosities of Liquid H 2 O, D 2 O, and T 2 O
journal, March 1999

  • Cho, C. H.; Urquidi, J.; Singh, S.
  • The Journal of Physical Chemistry B, Vol. 103, Issue 11
  • DOI: 10.1021/jp9842953

The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli
journal, November 2013

  • Hao, Ziyang; Lou, Hubing; Zhu, Rongfeng
  • Nature Chemical Biology, Vol. 10, Issue 1
  • DOI: 10.1038/nchembio.1380

Conformational entropy in molecular recognition by proteins
journal, July 2007

  • Frederick, Kendra King; Marlow, Michael S.; Valentine, Kathleen G.
  • Nature, Vol. 448, Issue 7151
  • DOI: 10.1038/nature05959

Measurement of 15N relaxation rates in perdeuterated proteins by TROSY-based methods
journal, June 2012


Molecular Basis of Ligand-Dependent Regulation of NadR, the Transcriptional Repressor of Meningococcal Virulence Factor NadA
journal, April 2016


Phylogenetic distribution of DNA-binding transcription factors in bacteria and archaea
journal, December 2004


Slow Dynamics in Folded and Unfolded States of an SH3 Domain
journal, November 2001

  • Tollinger, Martin; Skrynnikov, Nikolai R.; Mulder, Frans A. A.
  • Journal of the American Chemical Society, Vol. 123, Issue 46
  • DOI: 10.1021/ja011300z

Structure of an OhrR-ohrA Operator Complex Reveals the DNA Binding Mechanism of the MarR Family
journal, October 2005


Entropy redistribution controls allostery in a metalloregulatory protein
journal, March 2017

  • Capdevila, Daiana A.; Braymer, Joseph J.; Edmonds, Katherine A.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 17
  • DOI: 10.1073/pnas.1620665114

HYDRONMR: Prediction of NMR Relaxation of Globular Proteins from Atomic-Level Structures and Hydrodynamic Calculations
journal, November 2000

  • Garcı́a de la Torre, J.; Huertas, M. L.; Carrasco, B.
  • Journal of Magnetic Resonance, Vol. 147, Issue 1
  • DOI: 10.1006/jmre.2000.2170

On the relationship between NMR-derived amide order parameters and protein backbone entropy changes: Measurement of Protein Backbone Entropy by NMR
journal, March 2015

  • Sharp, Kim A.; O'Brien, Evan; Kasinath, Vignesh
  • Proteins: Structure, Function, and Bioinformatics, Vol. 83, Issue 5
  • DOI: 10.1002/prot.24789

One-component systems dominate signal transduction in prokaryotes
journal, February 2005

  • Ulrich, Luke E.; Koonin, Eugene V.; Zhulin, Igor B.
  • Trends in Microbiology, Vol. 13, Issue 2
  • DOI: 10.1016/j.tim.2004.12.006

Mutation-Induced Population Shift in the MexR Conformational Ensemble Disengages DNA Binding: A Novel Mechanism for MarR Family Derepression
journal, August 2016

  • Anandapadamanaban, Madhanagopal; Pilstål, Robert; Andresen, Cecilia
  • Structure, Vol. 24, Issue 8
  • DOI: 10.1016/j.str.2016.06.008

Structural Insights into the Redox-Sensing Mechanism of MarR-Type Regulator AbfR
journal, January 2017

  • Liu, Guijie; Liu, Xing; Xu, Hongjiao
  • Journal of the American Chemical Society, Vol. 139, Issue 4
  • DOI: 10.1021/jacs.6b11438

MarR family transcription factors
journal, February 2013


Cooperativity and flexibility in enzyme evolution
journal, February 2018

  • Pabis, Anna; Risso, Valeria A.; Sanchez-Ruiz, Jose M.
  • Current Opinion in Structural Biology, Vol. 48
  • DOI: 10.1016/j.sbi.2017.10.020

Hydrogen Sulfide and Reactive Sulfur Species Impact Proteome S -Sulfhydration and Global Virulence Regulation in Staphylococcus aureus
journal, September 2017


Structure and Flexibility Adaptation in Nonspecific and Specific Protein-DNA Complexes
journal, July 2004


Allosteric histidine switch for regulation of intracellular zinc(II) fluctuation
journal, December 2017

  • Zhu, Rongfeng; Song, Yanqun; Liu, Haiping
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 52
  • DOI: 10.1073/pnas.1708563115

Backbone and sterospecific methyl side chain resonance assignments of the homodimeric zinc sensor AdcR (32 kDa) in the apo- and Zn(II)-bound states
journal, November 2012


Functional Role of Solvent Entropy and Conformational Entropy of Metal Binding in a Dynamically Driven Allosteric System
journal, June 2018

  • Capdevila, Daiana A.; Edmonds, Katherine A.; Campanello, Gregory C.
  • Journal of the American Chemical Society, Vol. 140, Issue 29
  • DOI: 10.1021/jacs.8b02129

The Crystal Structure of the Transcriptional Regulator HucR from Deinococcus radiodurans Reveals a Repressor Preconfigured for DNA Binding
journal, June 2006

  • Bordelon, Tee; Wilkinson, Steven P.; Grove, Anne
  • Journal of Molecular Biology, Vol. 360, Issue 1
  • DOI: 10.1016/j.jmb.2006.05.005

Direct Observation of the Ion-Pair Dynamics at a Protein–DNA Interface by NMR Spectroscopy
journal, February 2013

  • Anderson, Kurtis M.; Esadze, Alexandre; Manoharan, Mariappan
  • Journal of the American Chemical Society, Vol. 135, Issue 9
  • DOI: 10.1021/ja312314b

Application of iterative soft thresholding for fast reconstruction of NMR data non-uniformly sampled with multidimensional Poisson Gap scheduling
journal, February 2012

  • Hyberts, Sven G.; Milbradt, Alexander G.; Wagner, Andreas B.
  • Journal of Biomolecular NMR, Vol. 52, Issue 4
  • DOI: 10.1007/s10858-012-9611-z

NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy
journal, December 2014


Crystal Structure of the Zinc-Dependent MarR Family Transcriptional Regulator AdcR in the Zn(II)-Bound State
journal, December 2011

  • Guerra, Alfredo J.; Dann, Charles E.; Giedroc, David P.
  • Journal of the American Chemical Society, Vol. 133, Issue 49
  • DOI: 10.1021/ja2080532

Structural mechanism of transcription regulation of the Staphylococcus aureus multidrug efflux operon mepRA by the MarR family repressor MepR
journal, November 2013

  • Birukou, Ivan; Seo, Susan M.; Schindler, Bryan D.
  • Nucleic Acids Research, Vol. 42, Issue 4
  • DOI: 10.1093/nar/gkt1215

On prokaryotic intelligence: Strategies for sensing the environment
journal, February 2010


Protein cysteine phosphorylation of SarA/MgrA family transcriptional regulators mediates bacterial virulence and antibiotic resistance
journal, August 2012

  • Sun, F.; Ding, Y.; Ji, Q.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 38
  • DOI: 10.1073/pnas.1205952109

Metal sensor proteins: nature's metalloregulated allosteric switches
journal, January 2007

  • Giedroc, David P.; Arunkumar, Alphonse I.
  • Dalton Transactions, Issue 29
  • DOI: 10.1039/b706769k

FoXS: a web server for rapid computation and fitting of SAXS profiles
journal, May 2010

  • Schneidman-Duhovny, D.; Hammel, M.; Sali, A.
  • Nucleic Acids Research, Vol. 38, Issue Web Server
  • DOI: 10.1093/nar/gkq461

Allosteric Inhibition of a Zinc-Sensing Transcriptional Repressor: Insights into the Arsenic Repressor (ArsR) Family
journal, April 2013

  • Campanello, Gregory C.; Ma, Zhen; Grossoehme, Nicholas E.
  • Journal of Molecular Biology, Vol. 425, Issue 7
  • DOI: 10.1016/j.jmb.2013.01.018

Dynamic activation of an allosteric regulatory protein
journal, November 2009

  • Tzeng, Shiou-Ru; Kalodimos, Charalampos G.
  • Nature, Vol. 462, Issue 7271
  • DOI: 10.1038/nature08560

Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli.
journal, March 1993


Entropy in molecular recognition by proteins
journal, June 2017

  • Caro, José A.; Harpole, Kyle W.; Kasinath, Vignesh
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 25
  • DOI: 10.1073/pnas.1621154114

Energetics of Zinc-Mediated Interactions in the Allosteric Pathways of Metal Sensor Proteins
journal, December 2012

  • Chakravorty, Dhruva K.; Parker, Trent M.; Guerra, Alfredo J.
  • Journal of the American Chemical Society, Vol. 135, Issue 1
  • DOI: 10.1021/ja309170g

15N–{1H} NOE experiment at high magnetic field strengths
journal, January 2007


Structural analysis of the regulatory mechanism of MarR protein Rv2887 in M. tuberculosis
journal, July 2017


TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts
journal, June 2009

  • Shen, Yang; Delaglio, Frank; Cornilescu, Gabriel
  • Journal of Biomolecular NMR, Vol. 44, Issue 4
  • DOI: 10.1007/s10858-009-9333-z

Adhesin competence repressor (AdcR) from Streptococcus pyogenes controls adaptive responses to zinc limitation and contributes to virulence
journal, December 2014

  • Sanson, Misu; Makthal, Nishanth; Flores, Anthony R.
  • Nucleic Acids Research, Vol. 43, Issue 1
  • DOI: 10.1093/nar/gku1304

Structural and mechanistic study of the cysteine oxidation-mediated induction of the Escherichia coli MarR regulator
journal, June 2017


The role of protein dynamics in the evolution of new enzyme function
journal, September 2016

  • Campbell, Eleanor; Kaltenbach, Miriam; Correy, Galen J.
  • Nature Chemical Biology, Vol. 12, Issue 11
  • DOI: 10.1038/nchembio.2175

Metallochaperones and metalloregulation in bacteria
journal, May 2017

  • Capdevila, Daiana A.; Edmonds, Katherine A.; Giedroc, David P.
  • Essays in Biochemistry, Vol. 61, Issue 2
  • DOI: 10.1042/EBC20160076

Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli.
journal, June 1995


Protective capacities of cell surface-associated proteins of Streptococcus suis mutants deficient in divalent cation-uptake regulators
journal, April 2009


The Static Magnetic Field Dependence of Chemical Exchange Linebroadening Defines the NMR Chemical Shift Time Scale
journal, March 2000

  • Millet, Oscar; Loria, J. Patrick; Kroenke, Christopher D.
  • Journal of the American Chemical Society, Vol. 122, Issue 12
  • DOI: 10.1021/ja993511y

How Aromatic Compounds Block DNA Binding of HcaR Catabolite Regulator
journal, April 2016

  • Kim, Youngchang; Joachimiak, Grazyna; Bigelow, Lance
  • Journal of Biological Chemistry, Vol. 291, Issue 25
  • DOI: 10.1074/jbc.M115.712067

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

The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability
journal, September 2007

  • Niesen, Frank H.; Berglund, Helena; Vedadi, Masoud
  • Nature Protocols, Vol. 2, Issue 9
  • DOI: 10.1038/nprot.2007.321

The crystal structure of MexR from Pseudomonas aeruginosa in complex with its antirepressor ArmR
journal, September 2008

  • Wilke, M. S.; Heller, M.; Creagh, A. L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 39
  • DOI: 10.1073/pnas.0805489105

Two WXXF-based motifs in NECAPs define the specificity of accessory protein binding to AP-1 and AP-2
journal, September 2004

  • Ritter, Brigitte; Denisov, Alexei Yu; Philie, Jacynthe
  • The EMBO Journal, Vol. 23, Issue 19
  • DOI: 10.1038/sj.emboj.7600378

Protein Dynamics Measurements by TROSY-Based NMR Experiments
journal, April 2000

  • Zhu, Guang; Xia, Youlin; Nicholson, Linda K.
  • Journal of Magnetic Resonance, Vol. 143, Issue 2
  • DOI: 10.1006/jmre.2000.2022

1 H, 13 C- 1 H, 1 H Dipolar Cross-correlated Spin Relaxation in Methyl Groups
journal, July 2004


Identifying Allosteric Hotspots with Dynamics: Application to Inter- and Intra-species Conservation
journal, May 2016


The ensemble nature of allostery
journal, April 2014

  • Motlagh, Hesam N.; Wrabl, James O.; Li, Jing
  • Nature, Vol. 508, Issue 7496
  • DOI: 10.1038/nature13001

The activity of CouR, a MarR family transcriptional regulator, is modulated through a novel molecular mechanism
journal, September 2015

  • Otani, Hiroshi; Stogios, Peter J.; Xu, Xiaohui
  • Nucleic Acids Research, Vol. 44, Issue 2
  • DOI: 10.1093/nar/gkv955

Ile, Leu, and Val Methyl Assignments of the 723-Residue Malate Synthase G Using a New Labeling Strategy and Novel NMR Methods
journal, November 2003

  • Tugarinov, Vitali; Kay, Lewis E.
  • Journal of the American Chemical Society, Vol. 125, Issue 45
  • DOI: 10.1021/ja030345s

Probing Slow Dynamics in High Molecular Weight Proteins by Methyl-TROSY NMR Spectroscopy:  Application to a 723-Residue Enzyme
journal, March 2004

  • Korzhnev, Dmitry M.; Kloiber, Karin; Kanelis, Voula
  • Journal of the American Chemical Society, Vol. 126, Issue 12
  • DOI: 10.1021/ja039587i

Program DYNAFIT for the Analysis of Enzyme Kinetic Data: Application to HIV Proteinase
journal, June 1996


Probing Side-Chain Dynamics in the Proteasome by Relaxation Violated Coherence Transfer NMR Spectroscopy
journal, February 2007

  • Tugarinov, Vitali; Sprangers, Remco; Kay, Lewis E.
  • Journal of the American Chemical Society, Vol. 129, Issue 6
  • DOI: 10.1021/ja067827z

Molecular Mechanisms of Antibacterial Multidrug Resistance
journal, March 2007


Structural Basis for Intrinsic Thermosensing by the Master Virulence Regulator RovA of Yersinia
journal, August 2012

  • Quade, Nick; Mendonca, Chriselle; Herbst, Katharina
  • Journal of Biological Chemistry, Vol. 287, Issue 43
  • DOI: 10.1074/jbc.M112.379156

The crystal structure of XC1739: A putative multiple antibiotic-resistance repressor (MarR) from Xanthomonas campestris at 1.8 Å resolution
journal, July 2006

  • Chin, Ko-Hsin; Tu, Zhi-Le; Li, Juo-Ning
  • Proteins: Structure, Function, and Bioinformatics, Vol. 65, Issue 1
  • DOI: 10.1002/prot.21017

Lactococcus lactis ZitR Is a Zinc-Responsive Repressor Active in the Presence of Low, Nontoxic Zinc Concentrations In Vivo
journal, February 2011

  • Llull, D.; Son, O.; Blanie, S.
  • Journal of Bacteriology, Vol. 193, Issue 8
  • DOI: 10.1128/JB.01109-10

Crystal Structures of SlyA Protein, a Master Virulence Regulator of Salmonella , in Free and DNA-bound States
journal, May 2011

  • Dolan, Kyle T.; Duguid, Erica M.; He, Chuan
  • Journal of Biological Chemistry, Vol. 286, Issue 25
  • DOI: 10.1074/jbc.M111.245258

The Metalloregulatory Zinc Site in Streptococcus pneumoniae AdcR, a Zinc-activated MarR Family Repressor
journal, October 2010

  • Reyes-Caballero, Hermes; Guerra, Alfredo J.; Jacobsen, Faith E.
  • Journal of Molecular Biology, Vol. 403, Issue 2
  • DOI: 10.1016/j.jmb.2010.08.030

Characterization of SlyA in Shigella flexneri Identifies a Novel Role in Virulence
journal, February 2016

  • Weatherspoon-Griffin, Natasha; Wing, Helen J.
  • Infection and Immunity, Vol. 84, Issue 4
  • DOI: 10.1128/IAI.00806-15