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

Capdevila, Daiana A.; Huerta, Fidel; Edmonds, Katherine A.; Le, My Tra; Wu, Hongwei; Giedroc, David P.

doi:10.7554/eLife.37268

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

Journal Article · 17 October 2018 · eLife

DOI:https://doi.org/10.7554/eLife.37268· OSTI ID:1502254

^[1]; Huerta, Fidel ^[2]; Edmonds, Katherine A. ^[1]; Le, My Tra ^[1]; Wu, Hongwei ^[1]; ^[3]

Department of Chemistry, Indiana University, Bloomington, United States
Department of Chemistry, Indiana University, Bloomington, United States; Graduate Program in Biochemistry, Indiana University, Bloomington, United States
Department of Chemistry, Indiana University, Bloomington, United States; Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, United States

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.

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

Sponsoring Organization:: NIHOTHER

OSTI ID:: 1502254

Journal Information:: eLife, Vol. 7, Issue 10, 2018; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.

Country of Publication:: United States

Language:: ENGLISH

References (92)

Allosteric inhibition through suppression of transient conformational states Tzeng, Shiou-Ru; Kalodimos, Charalampos G. Nature Chemical Biology, Vol. 9, Issue 7 https://doi.org/10.1038/nchembio.1250	journal	May 2013
The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative Fuangthong, M.; Helmann, J. D. Proceedings of the National Academy of Sciences, Vol. 99, Issue 10 https://doi.org/10.1073/pnas.102483199	journal	April 2002
Ligand-Binding Pocket Bridges DNA-Binding and Dimerization Domains of the Urate-Responsive MarR Homologue MftR from Burkholderia thailandensis Gupta, Ashish; Grove, Anne Biochemistry, Vol. 53, Issue 27 https://doi.org/10.1021/bi500219t	journal	July 2014
Ni(II) coordination to mixed sites modulates DNA binding of HpNikR via a long-range effect West, A. L.; Evans, S. E.; Gonzalez, J. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 15 https://doi.org/10.1073/pnas.1120283109	journal	March 2012
The role of conformational entropy in molecular recognition by calmodulin Marlow, Michael S.; Dogan, Jakob; Frederick, Kendra K. Nature Chemical Biology, Vol. 6, Issue 5 https://doi.org/10.1038/nchembio.347	journal	April 2010
Molecular Mechanisms of Ligand-Mediated Attenuation of DNA Binding by MarR Family Transcriptional Regulators Perera, I. C.; Grove, A. Journal of Molecular Cell Biology, Vol. 2, Issue 5 https://doi.org/10.1093/jmcb/mjq021	journal	August 2010
Resonance assignments of the metal sensor CzrA in the apo-, Zn2- and DNA-bound (42 kDa) states Arunkumar, Alphonse I.; Pennella, Mario A.; Kong, Xiangming Biomolecular NMR Assignments, Vol. 1, Issue 1 https://doi.org/10.1007/s12104-007-9027-y	journal	July 2007
Critical biophysical properties in the Pseudomonas aeruginosa efflux gene regulator MexR are targeted by mutations conferring multidrug resistance Andrésen, Cecilia; Jalal, Shah; Aili, Daniel Protein Science, Vol. 19, Issue 4 https://doi.org/10.1002/pro.343	journal	January 2010
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, Daniel; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346 https://doi.org/10.1107/S0021889809000338	journal	January 2009
An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus Chen, Peng R.; Bae, Taeok; Williams, Wade A. Nature Chemical Biology, Vol. 2, Issue 11 https://doi.org/10.1038/nchembio820	journal	September 2006
Regulation of virulence by members of the MarR/SlyA family Ellison, Damon W.; Miller, Virginia L. Current Opinion in Microbiology, Vol. 9, Issue 2 https://doi.org/10.1016/j.mib.2006.02.003	journal	April 2006
Protein activity regulation by conformational entropy Tzeng, Shiou-Ru; Kalodimos, Charalampos G. Nature, Vol. 488, Issue 7410 https://doi.org/10.1038/nature11271	journal	July 2012
Histidine switch controlling pH-dependent protein folding and DNA binding in a transcription factor at the core of synthetic network devices Deochand, D. K.; Perera, I. C.; Crochet, R. B. Molecular BioSystems, Vol. 12, Issue 8 https://doi.org/10.1039/C6MB00304D	journal	January 2016
Structural characterization of the DNA-binding mechanism underlying the copper(II)-sensing MarR transcriptional regulator Zhu, Rongfeng; Hao, Ziyang; Lou, Hubing JBIC Journal of Biological Inorganic Chemistry, Vol. 22, Issue 5 https://doi.org/10.1007/s00775-017-1442-7	journal	January 2017
Faithful estimation of dynamics parameters from CPMG relaxation dispersion measurements Kovrigin, Evgenii L.; Kempf, James G.; Grey, Michael J. Journal of Magnetic Resonance, Vol. 180, Issue 1 https://doi.org/10.1016/j.jmr.2006.01.010	journal	May 2006
Structural study of TcaR and its complexes with multiple antibiotics from Staphylococcus epidermidis Chang, Y. -M.; Jeng, W. -Y.; Ko, T. -P. Proceedings of the National Academy of Sciences, Vol. 107, Issue 19 https://doi.org/10.1073/pnas.0913302107	journal	April 2010
Regulation of Metabolic Pathways by MarR Family Transcription Factors Grove, Anne Computational and Structural Biotechnology Journal, Vol. 15 https://doi.org/10.1016/j.csbj.2017.06.001	journal	January 2017
Role of the semi-conserved histidine residue in the light-sensing domain of LitR, a MerR-type photosensory transcriptional regulator Takano, Hideaki; Mise, Kou; Maruyama, Takafumi Microbiology, Vol. 162, Issue 8 https://doi.org/10.1099/mic.0.000321	journal	August 2016
Coordinated Regulation of Virulence during Systemic Infection of Salmonella enterica Serovar Typhimurium Yoon, Hyunjin; McDermott, Jason E.; Porwollik, Steffen PLoS Pathogens, Vol. 5, Issue 2 https://doi.org/10.1371/journal.ppat.1000306	journal	February 2009
Crystal Structure of the Transcriptional Regulator Rv0678 of Mycobacterium tuberculosis Radhakrishnan, Abhijith; Kumar, Nitin; Wright, Catherine C. Journal of Biological Chemistry, Vol. 289, Issue 23 https://doi.org/10.1074/jbc.M113.538959	journal	April 2014
MarR family transcription factors: dynamic variations on a common scaffold Deochand, Dinesh K.; Grove, Anne Critical Reviews in Biochemistry and Molecular Biology, Vol. 52, Issue 6 https://doi.org/10.1080/10409238.2017.1344612	journal	July 2017
Thermal Offset Viscosities of Liquid H ₂ O, D ₂ O, and T ₂ O Cho, C. H.; Urquidi, J.; Singh, S. The Journal of Physical Chemistry B, Vol. 103, Issue 11 https://doi.org/10.1021/jp9842953	journal	March 1999
Mutational Analysis of the Multiple-Antibiotic Resistance Regulator MarR Reveals a Ligand Binding Pocket at the Interface between the Dimerization and DNA Binding Domains Duval, V.; McMurry, L. M.; Foster, K. Journal of Bacteriology, Vol. 195, Issue 15 https://doi.org/10.1128/JB.02224-12	journal	May 2013
The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli Hao, Ziyang; Lou, Hubing; Zhu, Rongfeng Nature Chemical Biology, Vol. 10, Issue 1 https://doi.org/10.1038/nchembio.1380	journal	November 2013
Conformational entropy in molecular recognition by proteins Frederick, Kendra King; Marlow, Michael S.; Valentine, Kathleen G. Nature, Vol. 448, Issue 7151 https://doi.org/10.1038/nature05959	journal	July 2007
Measurement of 15N relaxation rates in perdeuterated proteins by TROSY-based methods Lakomek, Nils-Alexander; Ying, Jinfa; Bax, Ad Journal of Biomolecular NMR, Vol. 53, Issue 3 https://doi.org/10.1007/s10858-012-9626-5	journal	June 2012
Molecular Basis of Ligand-Dependent Regulation of NadR, the Transcriptional Repressor of Meningococcal Virulence Factor NadA Liguori, Alessia; Malito, Enrico; Lo Surdo, Paola PLOS Pathogens, Vol. 12, Issue 4 https://doi.org/10.1371/journal.ppat.1005557	journal	April 2016
Phylogenetic distribution of DNA-binding transcription factors in bacteria and archaea Pérez-Rueda, Ernesto; Collado-Vides, Julio; Segovia, Lorenzo Computational Biology and Chemistry, Vol. 28, Issue 5-6 https://doi.org/10.1016/j.compbiolchem.2004.09.004	journal	December 2004
Slow Dynamics in Folded and Unfolded States of an SH3 Domain Tollinger, Martin; Skrynnikov, Nikolai R.; Mulder, Frans A. A. Journal of the American Chemical Society, Vol. 123, Issue 46 https://doi.org/10.1021/ja011300z	journal	November 2001
Structure of an OhrR-ohrA Operator Complex Reveals the DNA Binding Mechanism of the MarR Family Hong, Minsun; Fuangthong, Mayuree; Helmann, John D. Molecular Cell, Vol. 20, Issue 1 https://doi.org/10.1016/j.molcel.2005.09.013	journal	October 2005
Entropy redistribution controls allostery in a metalloregulatory protein Capdevila, Daiana A.; Braymer, Joseph J.; Edmonds, Katherine A. Proceedings of the National Academy of Sciences, Vol. 114, Issue 17 https://doi.org/10.1073/pnas.1620665114	journal	March 2017
HYDRONMR: Prediction of NMR Relaxation of Globular Proteins from Atomic-Level Structures and Hydrodynamic Calculations Garcı́a de la Torre, J.; Huertas, M. L.; Carrasco, B. Journal of Magnetic Resonance, Vol. 147, Issue 1 https://doi.org/10.1006/jmre.2000.2170	journal	November 2000
On the relationship between NMR-derived amide order parameters and protein backbone entropy changes: Measurement of Protein Backbone Entropy by NMR Sharp, Kim A.; O'Brien, Evan; Kasinath, Vignesh Proteins: Structure, Function, and Bioinformatics, Vol. 83, Issue 5 https://doi.org/10.1002/prot.24789	journal	March 2015
One-component systems dominate signal transduction in prokaryotes Ulrich, Luke E.; Koonin, Eugene V.; Zhulin, Igor B. Trends in Microbiology, Vol. 13, Issue 2 https://doi.org/10.1016/j.tim.2004.12.006	journal	February 2005
Mutation-Induced Population Shift in the MexR Conformational Ensemble Disengages DNA Binding: A Novel Mechanism for MarR Family Derepression Anandapadamanaban, Madhanagopal; Pilstål, Robert; Andresen, Cecilia Structure, Vol. 24, Issue 8 https://doi.org/10.1016/j.str.2016.06.008	journal	August 2016
Structural Insights into the Redox-Sensing Mechanism of MarR-Type Regulator AbfR Liu, Guijie; Liu, Xing; Xu, Hongjiao Journal of the American Chemical Society, Vol. 139, Issue 4 https://doi.org/10.1021/jacs.6b11438	journal	January 2017
MarR family transcription factors Grove, Anne Current Biology, Vol. 23, Issue 4 https://doi.org/10.1016/j.cub.2013.01.013	journal	February 2013
Cooperativity and flexibility in enzyme evolution Pabis, Anna; Risso, Valeria A.; Sanchez-Ruiz, Jose M. Current Opinion in Structural Biology, Vol. 48 https://doi.org/10.1016/j.sbi.2017.10.020	journal	February 2018
Hydrogen Sulfide and Reactive Sulfur Species Impact Proteome S -Sulfhydration and Global Virulence Regulation in Staphylococcus aureus Peng, Hui; Zhang, Yixiang; Palmer, Lauren D. ACS Infectious Diseases, Vol. 3, Issue 10 https://doi.org/10.1021/acsinfecdis.7b00090	journal	September 2017
Structure and Flexibility Adaptation in Nonspecific and Specific Protein-DNA Complexes Kalodimos, C. G. Science, Vol. 305, Issue 5682 https://doi.org/10.1126/science.1097064	journal	July 2004
Allosteric histidine switch for regulation of intracellular zinc(II) fluctuation Zhu, Rongfeng; Song, Yanqun; Liu, Haiping Proceedings of the National Academy of Sciences, Vol. 114, Issue 52 https://doi.org/10.1073/pnas.1708563115	journal	December 2017
Backbone and sterospecific methyl side chain resonance assignments of the homodimeric zinc sensor AdcR (32 kDa) in the apo- and Zn(II)-bound states Guerra, Alfredo J.; Giedroc, David P. Biomolecular NMR Assignments, Vol. 8, Issue 1 https://doi.org/10.1007/s12104-012-9442-6	journal	November 2012
Functional Role of Solvent Entropy and Conformational Entropy of Metal Binding in a Dynamically Driven Allosteric System Capdevila, Daiana A.; Edmonds, Katherine A.; Campanello, Gregory C. Journal of the American Chemical Society, Vol. 140, Issue 29 https://doi.org/10.1021/jacs.8b02129	journal	June 2018
The Crystal Structure of the Transcriptional Regulator HucR from Deinococcus radiodurans Reveals a Repressor Preconfigured for DNA Binding Bordelon, Tee; Wilkinson, Steven P.; Grove, Anne Journal of Molecular Biology, Vol. 360, Issue 1 https://doi.org/10.1016/j.jmb.2006.05.005	journal	June 2006
Direct Observation of the Ion-Pair Dynamics at a Protein–DNA Interface by NMR Spectroscopy Anderson, Kurtis M.; Esadze, Alexandre; Manoharan, Mariappan Journal of the American Chemical Society, Vol. 135, Issue 9 https://doi.org/10.1021/ja312314b	journal	February 2013
Application of iterative soft thresholding for fast reconstruction of NMR data non-uniformly sampled with multidimensional Poisson Gap scheduling Hyberts, Sven G.; Milbradt, Alexander G.; Wagner, Andreas B. Journal of Biomolecular NMR, Vol. 52, Issue 4 https://doi.org/10.1007/s10858-012-9611-z	journal	February 2012
SarZ Promotes the Expression of Virulence Factors and Represses Biofilm Formation by Modulating SarA and agr in Staphylococcus aureus Tamber, S.; Cheung, A. L. Infection and Immunity, Vol. 77, Issue 1 https://doi.org/10.1128/IAI.00859-08	journal	October 2008
NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy Lee, Woonghee; Tonelli, Marco; Markley, John L. Bioinformatics, Vol. 31, Issue 8 https://doi.org/10.1093/bioinformatics/btu830	journal	December 2014
Crystal Structure of the Zinc-Dependent MarR Family Transcriptional Regulator AdcR in the Zn(II)-Bound State Guerra, Alfredo J.; Dann, Charles E.; Giedroc, David P. Journal of the American Chemical Society, Vol. 133, Issue 49 https://doi.org/10.1021/ja2080532	journal	December 2011
Structural mechanism of transcription regulation of the Staphylococcus aureus multidrug efflux operon mepRA by the MarR family repressor MepR Birukou, Ivan; Seo, Susan M.; Schindler, Bryan D. Nucleic Acids Research, Vol. 42, Issue 4 https://doi.org/10.1093/nar/gkt1215	journal	November 2013
On prokaryotic intelligence: Strategies for sensing the environment Marijuán, Pedro C.; Navarro, Jorge; del Moral, Raquel Biosystems, Vol. 99, Issue 2 https://doi.org/10.1016/j.biosystems.2009.09.004	journal	February 2010
Protein cysteine phosphorylation of SarA/MgrA family transcriptional regulators mediates bacterial virulence and antibiotic resistance Sun, F.; Ding, Y.; Ji, Q. Proceedings of the National Academy of Sciences, Vol. 109, Issue 38 https://doi.org/10.1073/pnas.1205952109	journal	August 2012
Metal sensor proteins: nature's metalloregulated allosteric switches Giedroc, David P.; Arunkumar, Alphonse I. Dalton Transactions, Issue 29 https://doi.org/10.1039/b706769k	journal	January 2007
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
Allosteric Inhibition of a Zinc-Sensing Transcriptional Repressor: Insights into the Arsenic Repressor (ArsR) Family Campanello, Gregory C.; Ma, Zhen; Grossoehme, Nicholas E. Journal of Molecular Biology, Vol. 425, Issue 7 https://doi.org/10.1016/j.jmb.2013.01.018	journal	April 2013
Dynamic activation of an allosteric regulatory protein Tzeng, Shiou-Ru; Kalodimos, Charalampos G. Nature, Vol. 462, Issue 7271 https://doi.org/10.1038/nature08560	journal	November 2009
Entropy in molecular recognition by proteins Caro, José A.; Harpole, Kyle W.; Kasinath, Vignesh Proceedings of the National Academy of Sciences, Vol. 114, Issue 25 https://doi.org/10.1073/pnas.1621154114	journal	June 2017
Energetics of Zinc-Mediated Interactions in the Allosteric Pathways of Metal Sensor Proteins Chakravorty, Dhruva K.; Parker, Trent M.; Guerra, Alfredo J. Journal of the American Chemical Society, Vol. 135, Issue 1 https://doi.org/10.1021/ja309170g	journal	December 2012
15N–{1H} NOE experiment at high magnetic field strengths Gong, Qingguo; Ishima, Rieko Journal of Biomolecular NMR, Vol. 37, Issue 2 https://doi.org/10.1007/s10858-006-9125-7	journal	January 2007
Structural analysis of the regulatory mechanism of MarR protein Rv2887 in M. tuberculosis Gao, Yun-Rong; Li, De-Feng; Fleming, Joy Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-01705-4	journal	July 2017
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
Adhesin competence repressor (AdcR) from Streptococcus pyogenes controls adaptive responses to zinc limitation and contributes to virulence Sanson, Misu; Makthal, Nishanth; Flores, Anthony R. Nucleic Acids Research, Vol. 43, Issue 1 https://doi.org/10.1093/nar/gku1304	journal	December 2014
Structural and mechanistic study of the cysteine oxidation-mediated induction of the Escherichia coli MarR regulator Zhu, Rongfeng; Hao, Ziyang; Lou, Hubing Tetrahedron, Vol. 73, Issue 26 https://doi.org/10.1016/j.tet.2017.05.039	journal	June 2017
The role of protein dynamics in the evolution of new enzyme function Campbell, Eleanor; Kaltenbach, Miriam; Correy, Galen J. Nature Chemical Biology, Vol. 12, Issue 11 https://doi.org/10.1038/nchembio.2175	journal	September 2016
Metallochaperones and metalloregulation in bacteria Capdevila, Daiana A.; Edmonds, Katherine A.; Giedroc, David P. Essays in Biochemistry, Vol. 61, Issue 2 https://doi.org/10.1042/EBC20160076	journal	May 2017
Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli. Seoane, A. S.; Levy, S. B. Journal of Bacteriology, Vol. 177, Issue 12 https://doi.org/10.1128/jb.177.12.3414-3419.1995	journal	June 1995
Protective capacities of cell surface-associated proteins of Streptococcus suis mutants deficient in divalent cation-uptake regulators Aranda, J.; Garrido, M. E.; Fittipaldi, N. Microbiology, Vol. 155, Issue 5 https://doi.org/10.1099/mic.0.026278-0	journal	April 2009
The Static Magnetic Field Dependence of Chemical Exchange Linebroadening Defines the NMR Chemical Shift Time Scale Millet, Oscar; Loria, J. Patrick; Kroenke, Christopher D. Journal of the American Chemical Society, Vol. 122, Issue 12 https://doi.org/10.1021/ja993511y	journal	March 2000
How Aromatic Compounds Block DNA Binding of HcaR Catabolite Regulator Kim, Youngchang; Joachimiak, Grazyna; Bigelow, Lance Journal of Biological Chemistry, Vol. 291, Issue 25 https://doi.org/10.1074/jbc.M115.712067	journal	April 2016
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
The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability Niesen, Frank H.; Berglund, Helena; Vedadi, Masoud Nature Protocols, Vol. 2, Issue 9 https://doi.org/10.1038/nprot.2007.321	journal	September 2007
The crystal structure of MexR from Pseudomonas aeruginosa in complex with its antirepressor ArmR Wilke, M. S.; Heller, M.; Creagh, A. L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 39 https://doi.org/10.1073/pnas.0805489105	journal	September 2008
Two WXXF-based motifs in NECAPs define the specificity of accessory protein binding to AP-1 and AP-2 Ritter, Brigitte; Denisov, Alexei Yu; Philie, Jacynthe The EMBO Journal, Vol. 23, Issue 19 https://doi.org/10.1038/sj.emboj.7600378	journal	September 2004
Protein Dynamics Measurements by TROSY-Based NMR Experiments Zhu, Guang; Xia, Youlin; Nicholson, Linda K. Journal of Magnetic Resonance, Vol. 143, Issue 2 https://doi.org/10.1006/jmre.2000.2022	journal	April 2000
Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data Dosset, Patrice; Hus, Jean-Christophe; Blackledge, Martin Journal of Biomolecular NMR, Vol. 16, Issue 1, p. 23-28 https://doi.org/10.1023/A:1008305808620	journal	January 2000
Rapid structural fluctuations of the free HIV protease flaps in solution: Relationship to crystal structures and comparison with predictions of dynamics calculations Freedberg, Darón I.; Ishima, Rieko; Jacob, Jaison Protein Science, Vol. 11, Issue 2 https://doi.org/10.1110/ps.33202	journal	February 2002
¹ H, ¹³ C- ¹ H, ¹ H Dipolar Cross-correlated Spin Relaxation in Methyl Groups Tugarinov, Vitali; Kay, Lewis E. Journal of Biomolecular NMR, Vol. 29, Issue 3 https://doi.org/10.1023/B:JNMR.0000032562.07475.7f	journal	July 2004
Identifying Allosteric Hotspots with Dynamics: Application to Inter- and Intra-species Conservation Clarke, Declan; Sethi, Anurag; Li, Shantao Structure, Vol. 24, Issue 5 https://doi.org/10.1016/j.str.2016.03.008	journal	May 2016
The ensemble nature of allostery Motlagh, Hesam N.; Wrabl, James O.; Li, Jing Nature, Vol. 508, Issue 7496 https://doi.org/10.1038/nature13001	journal	April 2014
The activity of CouR, a MarR family transcriptional regulator, is modulated through a novel molecular mechanism Otani, Hiroshi; Stogios, Peter J.; Xu, Xiaohui Nucleic Acids Research, Vol. 44, Issue 2 https://doi.org/10.1093/nar/gkv955	journal	September 2015
Ile, Leu, and Val Methyl Assignments of the 723-Residue Malate Synthase G Using a New Labeling Strategy and Novel NMR Methods Tugarinov, Vitali; Kay, Lewis E. Journal of the American Chemical Society, Vol. 125, Issue 45 https://doi.org/10.1021/ja030345s	journal	November 2003
Probing Slow Dynamics in High Molecular Weight Proteins by Methyl-TROSY NMR Spectroscopy: Application to a 723-Residue Enzyme Korzhnev, Dmitry M.; Kloiber, Karin; Kanelis, Voula Journal of the American Chemical Society, Vol. 126, Issue 12 https://doi.org/10.1021/ja039587i	journal	March 2004
Program DYNAFIT for the Analysis of Enzyme Kinetic Data: Application to HIV Proteinase Kuzmič, Petr Analytical Biochemistry, Vol. 237, Issue 2 https://doi.org/10.1006/abio.1996.0238	journal	June 1996
Probing Side-Chain Dynamics in the Proteasome by Relaxation Violated Coherence Transfer NMR Spectroscopy Tugarinov, Vitali; Sprangers, Remco; Kay, Lewis E. Journal of the American Chemical Society, Vol. 129, Issue 6 https://doi.org/10.1021/ja067827z	journal	February 2007
Molecular Mechanisms of Antibacterial Multidrug Resistance Alekshun, Michael N.; Levy, Stuart B. Cell, Vol. 128, Issue 6, p. 1037-1050 https://doi.org/10.1016/j.cell.2007.03.004	journal	March 2007
Structural Basis for Intrinsic Thermosensing by the Master Virulence Regulator RovA of Yersinia Quade, Nick; Mendonca, Chriselle; Herbst, Katharina Journal of Biological Chemistry, Vol. 287, Issue 43 https://doi.org/10.1074/jbc.M112.379156	journal	August 2012
The crystal structure of XC1739: A putative multiple antibiotic-resistance repressor (MarR) from Xanthomonas campestris at 1.8 Å resolution Chin, Ko-Hsin; Tu, Zhi-Le; Li, Juo-Ning Proteins: Structure, Function, and Bioinformatics, Vol. 65, Issue 1 https://doi.org/10.1002/prot.21017	journal	July 2006
Lactococcus lactis ZitR Is a Zinc-Responsive Repressor Active in the Presence of Low, Nontoxic Zinc Concentrations In Vivo Llull, D.; Son, O.; Blanie, S. Journal of Bacteriology, Vol. 193, Issue 8 https://doi.org/10.1128/JB.01109-10	journal	February 2011
Structural Insight on the Mechanism of Regulation of the MarR Family of Proteins: High-Resolution Crystal Structure of a Transcriptional Repressor from Methanobacterium thermoautotrophicum Saridakis, Vivian; Shahinas, Dea; Xu, Xiaohui Journal of Molecular Biology, Vol. 377, Issue 3 https://doi.org/10.1016/j.jmb.2008.01.001	journal	March 2008
The Metalloregulatory Zinc Site in Streptococcus pneumoniae AdcR, a Zinc-activated MarR Family Repressor Reyes-Caballero, Hermes; Guerra, Alfredo J.; Jacobsen, Faith E. Journal of Molecular Biology, Vol. 403, Issue 2 https://doi.org/10.1016/j.jmb.2010.08.030	journal	October 2010
[12] Chemical shifts as a tool for structure determination Wishart, David S.; Sykes, Brian D. Methods in Enzymology https://doi.org/10.1016/S0076-6879(94)39014-2	book	January 1994
Characterization of SlyA in Shigella flexneri Identifies a Novel Role in Virulence Weatherspoon-Griffin, Natasha; Wing, Helen J. Infection and Immunity, Vol. 84, Issue 4 https://doi.org/10.1128/IAI.00806-15	journal	February 2016

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