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Cited by 136Bacterial Genetics and BiotechnologyMetalloenzymes and iron-sulfur proteinsTrace Elements in Health

Metallochaperones and metalloregulation in bacteria

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Capdevila, Daiana A., Edmonds, Katherine A., Giedroc, David P.·2017·Essays in Biochemistry
DOI 10.1042/ebc20160076PMC PMC5858914
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Abstract

Bacterial transition metal homoeostasis or simply ‘metallostasis’ describes the process by which cells control the intracellular availability of functionally required metal cofactors, from manganese (Mn) to zinc (Zn), avoiding both metal deprivation and toxicity. Metallostasis is an emerging aspect of the vertebrate host–pathogen interface that is defined by a ‘tug-of-war’ for biologically essential metals and provides the motivation for much recent work in this area. The host employs a number of strategies to starve the microbial pathogen of essential metals, while for others attempts to limit bacterial infections by leveraging highly competitive metals. Bacteria must be capable of adapting to these efforts to remodel the transition metal landscape and employ highly specialized metal sensing transcriptional regulators, termed metalloregulatory proteins,and metallochaperones, that allocate metals to specific destinations, to mediate this adaptive response. In this essay, we discuss recent progress in our understanding of the structural mechanisms and metal specificity of this adaptive response, focusing on energy-requiring metallochaperones that play roles in the metallocofactor active site assembly in metalloenzymes and metallosensors, which govern the systems-level response to metal limitation and intoxication.

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  • Labile cation pools are sensed by metalloregulatory systems and serve to metalate nascent metalloproteins.

    “The labile cation pools are sensed by metalloregulatory systems1,219 and serve to metalate nascent metalloproteins.3”

    From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [219]

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  1. [2]Djoko KY Ong CL Walker MJ McEwan AG 2015 The role of copper and zinc toxicity in innate immune defense against bacterial pathogens J. Biol. Chem 290 18954 18961 26055706 PMC4521016
  2. [3]Martin JE Edmonds KA Bruce KE Campanello GC Eijkelkamp BA Brazel EB 2017 The zinc efflux activator SczA protects Streptococcus pneumoniae serotype 2 D39 from intracellular zinc toxicity Mol. Microbiol 10.1111/mmi.13654 PMC5426980 28249108 · DOI · Paper page
  3. [4]Neyrolles O Mintz E Catty P 2013 Zinc and copper toxicity in host defense against pathogens: Mycobacterium tuberculosis as a model example of an emerging paradigm Front. Cell Infect. Microbiol 3 89 24350063 PMC3841717
  4. [5]Higgins KA Giedroc DP 2013 Metal Specificity of Metallosensors Encyclopedia of Inorganic and Bioinorganic Chemistry 1 16 John Wiley & Sons, Ltd Chichester, UK
  5. [6]O’Halloran TV Culotta VC 2000 Metallochaperones, an intracellular shuttle service for metal ions J. Biol. Chem 275 25057 25060 10816601
  6. [7]Foster AW Osman D Robinson NJ 2014 Metal preferences and metallation J. Biol. Chem 289 28095 28103 25160626 PMC4192464
  7. [9]Waldron KJ Rutherford JC Ford D Robinson NJ 2009 Metalloproteins and metal sensing Nature 460 823 830 19675642
  8. [10]Finney LA O’Halloran TV 2003 Transition metal speciation in the cell: Insights from the chemistry of metal ion receptor Science 300 931 936 12738850
  9. [11]Wang D Hosteen O Fierke CA 2012 ZntR-mediated transcription of zntA responds to nanomolar intracellular free zinc J. Inorg. Biochem 111 173 181 22459916 PMC3408962
  10. [12]Changela A Chen K Xue Y Holschen J Outten CE O’Halloran TV 2003 Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR Science 301 1383 1387 12958362
  11. [13]Ma Z Chandrangsu P Helmann TC Romsang A Gaballa A Helmann JD 2014 Bacillithiol is a major buffer of the labile zinc pool in Bacillus subtilis Mol. Microbiol 94 756 770 25213752 PMC4227968
  12. [14]Bell SG Vallee BL 2009 The metallothionein/thionein system: an oxidoreductive metabolic zinc link Chembiochem 10 55 62 19089881
  13. [15]Nairn BL Lonergan ZR Wang J Braymer JJ Zhang Y Calcutt MW 2016 The response of Acinetobacter baumannii to zinc starvation Cell Host Microbe 19 826 836 27281572 PMC4901392
  14. [16]Weinberg ED 1975 Nutritional immunity. Host’s attempt to withhold iron from microbial invaders JAMA 231 39 41 1243565
  15. [17]Braymer JJ Giedroc DP 2014 Recent developments in copper and zinc homeostasis in bacterial pathogens Curr. Opin. Chem. Biol 19 59 66 24463765 PMC4008645
  16. [18]Robinson NJ Winge DR 2010 Copper metallochaperones Annu. Rev. Biochem 79 537 562 20205585 PMC3986808
  17. [19]Foster AW Osman D Robinson NJ 2014 Metal preferences and metallation J. Biol. Chem 289 28095 28103 25160626 PMC4192464
  18. [20]Foster AW Pernil R Patterson CJ Scott AJP Pålsson L-O Pal R 2017 A tight tunable range for Ni(II) sensing and buffering in cells Nat. Chem. Biol 10.1038/nchembio.2310 PMC5365139 28166209 · DOI
  19. [21]Porcheron G Schouler C Dozois CM 2016 Survival games at the dinner table: regulation of Enterobacterial virulence through nutrient sensing and acquisition Curr. Opin. Microbiol 30 98 106 26871481
  20. [22]Porcheron G Garénaux A Proulx J Sabri M Dozois CM 2013 Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence Front. Cell. Infect. Microbiol 3 90 24367764 PMC3852070
  21. [24]Waldron KJ Robinson NJ 2009 How do bacterial cells ensure that metalloproteins get the correct metal? Nat. Rev. Microbiol 7 25 35 19079350
  22. [25]Haas CE Rodionov DA Kropat J Malasarn D Merchant SS de Crecy-Lagard V 2009 A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life BMC Genomics 10 470 19822009 PMC2770081
  23. [26]Lacasse MJ Zamble DB 2016 [NiFe]-hydrogenase maturation Biochemistry 55 1689 1701 26919691
  24. [27]Farrugia MA Macomber L Hausinger RP 2013 Biosynthesis of the urease metallocenter J. Biol. Chem 288 13178 13185 23539618 PMC3650357
  25. [28]Lofgren M Koutmos M Banerjee R 2013 Autoinhibition and signaling by the switch ii motif in the G-protein chaperone of a radical B12 enzyme J. Biol. Chem 288 30980 30989 23996001 PMC3829411
  26. [29]Wittinghofer A Vetter IR 2011 Structure-function relationships of the G domain, a canonical switch motif Annu. Rev. Biochem 80 943 971 21675921
  27. [30]Fong YH Wong HC Yuen MH Lau PH Chen YW Wong K-B 2013 Structure of UreG/UreF/UreH complex reveals how urease accessory proteins facilitate maturation of Helicobacter pylori urease PLoS Biol 11 e1001678 24115911 PMC3792862
  28. [31]Sydor AM Lebrette H Ariyakumaran R Cavazza C Zamble DB 2014 Relationship between Ni(II) and Zn(II) coordination and nucleotide binding by the Helicobacter pylori [NiFe]-hydrogenase and urease maturation factor HypB J. Biol. Chem 289 3828 3841 24338018 PMC3924253
  29. [33]Fu Y Chang F-MJ Giedroc DP 2014 Copper transport and trafficking at the host-bacterial pathogen interface Acc. Chem. Res 47 3605 3613 25310275 PMC4268108
  30. [35]Fu Y Bruce KE Wu H Giedroc DP 2016 The S2 Cu(I) site in CupA from Streptococcus pneumoniae is required for cellular copper resistance Metallomics 8 61 70 26346139 PMC4720546
  31. [36]Fu Y Tsui H-CTH Bruce KE Sham L-TL Higgins KA Lisher JP 2013 A new structural paradigm in copper resistance in Streptococcus pneumoniae Nat. Chem. Biol 9 177 183 23354287 PMC3578076
  32. [37]Franke S Grass G Rensing C Nies DH 2003 Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli J. Bacteriol 185 3804 3812 12813074 PMC161567
  33. [38]Chacón KN Mealman TD McEvoy MM Blackburn NJ 2014 Tracking metal ions through a Cu/Ag efflux pump assigns the functional roles of the periplasmic proteins Proc. Natl. Acad. Sci. U.S.A 111 15373 15378 25313055 PMC4217431
  34. [39]Jost M Cracan V Hubbard PA Banerjee R Drennan CL 2015 Visualization of a radical B12 enzyme with its G-protein chaperone Proc. Natl. Acad. Sci. U.S.A 112 2419 2424 25675500 PMC4345561
  35. [40]Lacasse MJ Douglas CD Zamble DB 2016 Mechanism of selective nickel transfer from HypB to HypA, Escherichia coli [NiFe]-hydrogenase accessory proteins Biochemistry 55 6821 6831 27951644
  36. [41]Douglas CD Ngu TT Kaluarachchi H Zamble DB 2013 Metal transfer within the Escherichia coli HypB-HypA complex of hydrogenase accessory proteins Biochemistry 52 6030 6039 23899293 PMC4457517
  37. [42]Leach MR Jie WZ Zamble DB 2007 The role of complex formation between the Escherichia coli hydrogenase accessory factors HypB and SlyD J. Biol. Chem 282 16177 16186 17426034
  38. [43]Kaluarachchi H Zhang JW Zamble DB 2011 Escherichia coli SlyD, more than a Ni(II) reservoir Biochemistry 50 10761 10763 22085337 PMC3253374
  39. [44]Chan Chung KC Zamble DB 2011 Protein interactions and localization of the Escherichia coli accessory protein HypA during nickel insertion to [NiFe] hydrogenase J. Biol. Chem 286 43081 43090 22016389 PMC3234881
  40. [45]Xia W Li H Sze KH Sun H 2009 Structure of a nickel chaperone, HypA, from Helicobacter pylori reveals two distinct metal binding sites J. Am. Chem. Soc 131 10031 10040 19621959
  41. [46]Herbst RW Perovic I Martin-Diaconescu V O’Brien K Chivers PT Pochapsky SS 2010 Communication between the zinc and nickel sites in dimeric HypA: metal recognition and pH sensing J. Am. Chem. Soc 132 10338 10351 20662514 PMC2934764
  42. [47]Johnson RC Hu HQ Merrell DS Maroney MJ 2015 Dynamic HypA zinc site is essential for acid viability and proper urease maturation in Helicobacter pylori Metallomics 7 674 682 25608738 PMC4390472
  43. [48]Watanabe S Kawashima T Nishitani Y Kanai T Wada T Inaba K 2015 Structural basis of a Ni acquisition cycle for [NiFe] hydrogenase by Ni-metallochaperone HypA and its enhancer Proc. Natl. Acad. Sci. U.S.A 112 7701 7706 26056269 PMC4485131
  44. [49]Xia W Li H Sun H 2014 Functional disruption of HypB, a GTPase of Helicobacter pylori, by bismuth Chem. Commun. (Camb.) 50 1611 1614 24389922
  45. [50]Maier RJ Fu C Gilbert J Moshiri F Olson J Plaut AG 1996 Hydrogen uptake hydrogenase in Helicobacter pylori FEMS Microbiol. Lett 141 71 76 8764511
  46. [51]Garner JA Cover TL 1996 Binding and internalization of the Helicobacter pylori vacuolating cytotoxin by epithelial cells Infect. Immun 64 4197 4203 8926088 PMC174356
  47. [52]Miraula M Ciurli S Zambelli B 2015 Intrinsic disorder and metal binding in UreG proteins from Archae hyperthermophiles: GTPase enzymes involved in the activation of Ni(II) dependent urease J. Biol. Inorg. Chem 20 739 755 25846143
  48. [53]Yang X Li H Lai TP Sun H 2015 UreE-UreG complex facilitates nickel transfer and preactivates GTPase of UreG in Helicobacter pylori J. Biol. Chem 290 12474 12485 25752610 PMC4432268
  49. [54]D’Urzo A Santambrogio C Grandori R Ciurli S Zambelli B 2014 The conformational response to Zn(II) and Ni(II) binding of Sporosarcina pasteurii UreG, an intrinsically disordered GTPase J. Biol. Inorg. Chem 19 1341 1354 25200810
  50. [55]Merloni A Dobrovolska O Zambelli B Agostini F Bazzani M Musiani F 2014 Molecular landscape of the interaction between the urease accessory proteins UreE and UreG Biochim. Biophys. Acta 1844 1662 1674 24982029
  51. [56]Biagi F Musiani F Ciurli S 2013 Structure of the UreD-UreF-UreG-UreE complex in Helicobacter pylori: a model study J. Biol. Inorg. Chem 18 571 577 23661161
  52. [57]Musiani F Ippoliti E Micheletti C Carloni P Ciurli S 2013 Conformational fluctuations of UreG, an intrinsically disordered enzyme Biochemistry 52 2949 2954 23560717
  53. [58]Boer JL Hausinger RP 2012 Klebsiella aerogenes UreF: identification of the UreG binding site and role in enhancing the fidelity of urease activation Biochemistry 51 2298 2308 22369361 PMC3309104
  54. [59]Benoit SL McMurry JL Hill SA Maier RJ 2012 Helicobacter pylori hydrogenase accessory protein HypA and urease accessory protein UreG compete with each other for UreE recognition Biochim. Biophys. Acta 1820 1519 1525 22698670 PMC4017372
  55. [60]Zambelli B Cremades N Neyroz P Turano P Uversky VN Ciurli S 2012 Insights in the (un)structural organization of Bacillus pasteurii UreG, an intrinsically disordered GTPase enzyme Mol. Biosyst 8 220 228 21922108
  56. [61]Zambelli B Turano P Musiani F Neyroz P Ciurli S 2009 Zn2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation Proteins 74 222 239 18767150
  57. [62]Mehta N Benoit S Maier RJ 2003 Roles of conserved nucleotide-binding domains in accessory proteins, HypB and UreG, in the maturation of nickel-enzymes required for efficient Helicobacter pylori colonization Microb. Pathog 35 229 234 14521881
  58. [63]Moncrief MBC Hausinger RP 1997 Characterization of UreG, identification of a UreD-UreF-UreG complex, and evidence suggesting that a nucleotide-binding site in UreG is required for in vivo metallocenter assembly of Klebsiella aerogenes urease J. Bacteriol 179 4081 4086 9209019 PMC179225
  59. [64]Boer JL Quiroz-Valenzuela S Anderson KL Hausinger RP 2010 Mutagenesis of Klebsiella aerogenes UreG to probe nickel binding and interactions with other urease-related proteins Biochemistry 49 5859 5869 20533838 PMC2912431
  60. [65]Bellucci M Zambelli B Musiani F Turano P Ciurli S 2009 Helicobacter pylori UreE, a urease accessory protein: specific Ni 2+- and Zn2+-binding properties and interaction with its cognate UreG Biochem. J 422 91 100 19476442
  61. [66]Zambelli B Banaszak K Merloni A Kiliszek A Rypniewski W Ciurli S 2013 Selectivity of Ni(II) and Zn(II) binding to Sporosarcina pasteurii UreE, a metallochaperone in the urease assembly: a calorimetric and crystallographic study J. Biol. Inorg. Chem 18 1005 1017 24126709
  62. [67]Hubbard PA Padovani D Labunska T Mahlstedt SA Banerjee R Drennan CL 2007 Crystal structure and mutagenesis of the metallochaperone MeaB: Insight into the causes of methylmalonic aciduria J. Biol. Chem 282 31308 31316 17728257
  63. [68]Edwards TE Baugh L Bullen J Baydo RO Witte P Thompkins K 2015 Crystal structures of Mycobacterial MeaB and MMAA-like GTPases J. Struct. Funct. Genomics 16 91 99 25832174 PMC4631608
  64. [69]Kobayashi M Shimizu S 1998 Metalloenzyme nitrile hydratase: structure, regulation, and application to biotechnology Nat. Biotechnol 16 733 736 9702770
  65. [70]Gumataotao N Lankathilaka KPW Bennett B Holz RC 2017 The iron-type nitrile hydratase activator protein is a GTPase Biochem. J 474 247 258 27807009
  66. [71]Hood MI Mortensen BL Moore JL Zhang Y Kehl-Fie TE Sugitani N 2012 Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration PLoS Pathog 8 e1003068 23236280 PMC3516566
  67. [72]Gabriel SE Miyagi F Gaballa A Helmann JD 2008 Regulation of the Bacillus subtilis yciC gene and insights into the DNA-binding specificity of the zinc-sensing metalloregulator Zur J. Bacteriol 190 3482 3488 18344368 PMC2395016
  68. [73]Rae TD Schmidt PJ Pufahl RA Culotta VC O’Halloran TV 1999 Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase Science 284 805 808 10221913
  69. [74]Sydor AM Jost M Ryan KS Turo KE Douglas CD Drennan CL 2013 Metal binding properties of Escherichia coli YjiA, a member of the metal homeostasis-associated COG0523 family of GTPases Biochemistry 52 1788 1801 24449932 PMC3596956
  70. [75]Ma Z Jacobsen FE Giedroc DP 2009 Coordination chemistry of bacterial metal transport and sensing Chem. Rev 109 4644 4681 19788177 PMC2783614
  71. [76]Fernandez-López R Ruiz R de la Cruz F Moncalián G 2015 Transcription factor-based biosensors enlightened by the analyte Front. Microbiol 6 648 26191047 PMC4486848
  72. [77]Guerra AJ Giedroc DP 2012 Metal site occupancy and allosteric switching in bacterial metal sensor proteins Arch. Biochem. Biophys 519 210 222 22178748 PMC3312040
  73. [78]Luebke JL Giedroc DP 2015 Cysteine sulfur chemistry in transcriptional regulators at the host-bacterial pathogen interface Biochemistry 54 3235 3249 25946648
  74. [79]Campanello GC Ma Z Grossoehme NE Guerra AJ Ward BP Dimarchi RD 2013 Allosteric inhibition of a zinc-sensing transcriptional repressor: insights into the arsenic repressor (ArsR) family J. Mol. Biol 425 1143 1157 23353829 PMC3602352
  75. [80]Harvie DR Andreini C Cavallaro G Meng W Connolly BA Yoshida K 2006 Predicting metals sensed by ArsR-SmtB repressors: allosteric interference by a non-effector metal Mol. Microbiol 59 1341 1356 16430705
  76. [81]Ye J Kandegedara A Martin P Rosen BP 2005 Crystal structure of the Staphylococcus aureus pI258 CadC Cd(II)/Pb(II)/Zn(II)-responsive repressor J. Bacteriol 187 4214 4221 15937183 PMC1151749
  77. [82]Busenlehner LS Pennella MA Giedroc DP 2003 The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance FEMS Microbiol. Rev 27 131 143 12829264
  78. [83]Shi W Dong J Scott RA Ksenzenko MY Rosen BP 1996 The Role of arsenic-thiol interactions in metalloregulation of the ars operon J. Biol. Chem 271 9291 9297 8621591
  79. [84]Busenlehner LS Weng T-C Penner-Hahn JE Giedroc DP 2002 Elucidation of primary (α3N) and vestigial (α5) heavy metal-binding sites in Staphylococcus aureus pI258 CadC: evolutionary implications for metal ion selectivity of ArsR/SmtB metal sensor proteins J. Mol. Biol 319 685 701 12054863
  80. [85]Liu T Golden JW Giedroc DP 2005 A zinc(II)/lead(II)/cadmium(II)-inducible operon from the cyanobacterium Anabaena is regulated by AztR, an α3N ArsR/SmtB metalloregulator Biochemistry 44 8673 8683 15952774
  81. [86]Liu T Chen X Ma Z Shokes J Hemmingsen L Scott RA 2008 A Cu(I)-sensing ArsR family metal sensor protein with a relaxed metal selectivity profile Biochemistry 47 10564 10575 18795800 PMC2599807
  82. [87]Thelwell C Robinson NJ Turner-Cavet JS 1998 An SmtB-like repressor from Synechocystis PCC 6803 regulates a zinc exporter Proc. Natl. Acad. Sci. U.S.A 95 10728 10733 9724772 PMC27963
  83. [88]VanZile ML Cosper NJ Scott Ra Giedroc DP 2000 The zinc metalloregulatory protein Synechococcus PCC7942 SmtB binds a single zinc ion per monomer with high affinity in a tetrahedral coordination geometry Biochemistry 39 11818 11829 10995250
  84. [89]Lee CW Chakravorty DK Chang FMJ Reyes-Caballero H Ye Y Merz KM Jr 2012 Solution structure of Mycobacterium tuberculosis NmtR in the apo state: insights into Ni(II)-mediated allostery Biochemistry 51 2619 2629 22394357 PMC3500661
  85. [90]Shimizu T Shen J Fang M Zhang Y Hori K Trinidad JC 2017 Sulfide-responsive transcriptional repressor SqrR functions as a master regulator of sulfide-dependent photosynthesis Proc. Natl. Acad. Sci. U.S.A 114 2355 2360 28196888 PMC5338557
  86. [91]Lee SJ Lee I-G Lee K-Y Kim D-G Eun H-J Yoon H-J 2016 Two distinct mechanisms of transcriptional regulation by the redox sensor YodB Proc. Natl. Acad. Sci. U.S.A 113 E5202 E5211 27531959 PMC5024596
  87. [92]Guimarães BG Barbosa RL Soprano AS Campos BM de Souza TA Tonoli CC 2011 Plant pathogenic bacteria utilize biofilm growth-associated repressor (BigR), a novel winged-helix redox switch, to control hydrogen sulfide detoxification under hypoxia J. Biol. Chem 286 26148 26157 21632538 PMC3138302
  88. [93]Palm GJ Khanh Chi B Waack P Gronau K Becher D Albrecht D 2012 Structural insights into the redox-switch mechanism of the MarR/DUF24-type regulator HypR Nucleic Acids Res 40 4178 4192 22238377 PMC3351151
  89. [94]Ehira S Ohmori M 2012 The redox-sensing transcriptional regulator RexT controls expression of thioredoxin A2 in the cyanobacterium Anabaena sp. strain PCC 7120 J. Biol. Chem 287 40433 40440 23027868 PMC3504758
  90. [95]Mukherjee D Datta AB Chakrabarti P 2014 Crystal structure of HlyU, the hemolysin gene transcription activator, from Vibrio cholerae N16961 and functional implications Biochim. Biophys. Acta 1844 2346 2354 25450504
  91. [96]Zhao H Volkov A Veldore VH Hoch JA Varughese KI 2010 Crystal structure of the transcriptional repressor PagR of Bacillus anthracis Microbiology 156 385 391 19926656 PMC2828352
  92. [97]Gao CH Yang M He ZG 2011 An ArsR-like transcriptional factor recognizes a conserved sequence motif and positively regulates the expression of phoP in mycobacteria Biochem. Biophys. Res. Commun 411 726 731 21782791
  93. [98]Gueuné H Durand M-J Thouand G DuBow MS 2008 The ygaVP genes of Escherichia coli form a tributyltin-inducible operon Appl. Environ. Microbiol 74 1954 1958 18245262 PMC2268312
  94. [99]Nishi K Lee H-J Park S-Y Bae SJ Lee SE Adams PD 2010 Crystal structure of the transcriptional activator HlyU from Vibrio vulnificus CMCP6 FEBS Lett 584 1097 1102 20178784
  95. [100]Arunkumar AI Campanello GC Giedroc DP 2009 Solution structure of a paradigm ArsR family zinc sensor in the DNA-bound state Proc. Natl. Acad. Sci. U.S.A 106 18177 18182 19822742 PMC2775347
  96. [101]Capdevila DA Braymer JJ Edmonds KA Wu H Giedroc DP 2017 Entropy redistribution controls allostery in a metalloregulatory protein Proc. Natl. Acad. Sci. U.S.A in press PMC5410788 28348247
  97. [102]Hobman JL 2007 MerR family transcription activators: similar designs, different specificities Mol. Microbiol 63 1275 1278 17302809
  98. [103]Huang S Liu X Wang D Chen W Hu Q Wei T 2016 Structural basis for the selective Pb(ii) recognition of metalloregulatory protein PbrR691 Inorg. Chem 55 12516 12519 27989185
  99. [104]Kidd SP Djoko KY Ng J Argente MP Jennings MP McEwan AG 2011 A novel nickel responsive MerR-like regulator, NimR, from Haemophilus influenzae Metallomics 3 1009 1018 21952667
  100. [105]Philips SJ Canalizo-Hernandez M Yildirim I Schatz GC Mondragon A O’Halloran TV 2015 Allosteric transcriptional regulation via changes in the overall topology of the core promoter Science 349 877 881 26293965 PMC4617686
  101. [106]Chen T-Y Santiago AG Jung W Krzemiński L Yang F Martell DJ 2015 Concentration- and chromosome-organization-dependent regulator unbinding from DNA for transcription regulation in living cells Nat. Commun 6 7445 26145755 PMC4507017
  102. [107]Ibáñez MM Checa SK Soncini FC 2015 A single serine residue determines selectivity to monovalent metal ions in metalloregulators of the MerR family J. Bacteriol 197 1606 1613 25691529 PMC4403664
  103. [108]Szunyogh D Szokolai H Thulstrup PW Larsen FH Gyurcsik B Christensen NJ 2015 Specificity of the metalloregulator CueR for monovalent metal ions: possible functional role of a coordinated thiol? Angew. Chem. Int. Ed. Engl 54 15756 15761 26563985
  104. [109]Takano H Mise K Maruyama T Hagiwara K Ueda K 2016 Role of the semi-conserved histidine residue in the light-sensing domain of LitR, a MerR-type photosensory transcriptional regulator Microbiology 162 1500 1509 27283316
  105. [110]Lee PE Demple B Barton JK 2009 DNA-mediated redox signaling for transcriptional activation of SoxR Proc. Natl. Acad. Sci. U.S.A 106 13164 13168 19651620 PMC2726364
  106. [111]Kobayashi K Fujikawa M Kozawa T 2014 Oxidative stress sensing by the iron-sulfur cluster in the transcription factor, SoxR J. Inorg. Biochem 133 87 91 24332474
  107. [112]Chambers JR Liao J Schurr MJ Sauer K 2014 BrlR from Pseudomonas aeruginosa is a c-di-GMP-responsive transcription factor Mol. Microbiol 92 471 487 24612375 PMC4000578
  108. [113]McEwan AG Djoko KY Chen NH Couñago RLM Kidd SP Potter AJ 2011 Novel bacterial MerR-like regulators. Their role in the response to carbonyl and nitrosative stress Adv. Microb. Physiol 58 1 22 21722790
  109. [114]Couñago RM Chen NH Chang C-W Djoko KY McEwan AG Kobe B 2016 Structural basis of thiol-based regulation of formaldehyde detoxification in H. influenzae by a MerR regulator with no sensor region Nucleic Acids Res 44 6981 6993 27307602 PMC5001606
  110. [116]Leitch S Bradley MJ Rowe JL Chivers PT Maroney MJ 2007 Nickel-specific response in the transcriptional regulator, Escherichia coli NikR J. Am. Chem. Soc 129 5085 5095 17397155
  111. [117]Higgins KA Giedroc D 2014 Insights into protein allostery in the CsoR/RcnR family of transcriptional repressors Chem. Lett 43 20 25 24695963 PMC3970791
  112. [118]Marcus SA Sidiropoulos SW Steinberg H Talaat AM 2016 CsoR is essential for maintaining copper homeostasis in Mycobacterium tuberculosis PLoS ONE 11 e0151816 26999439 PMC4801387
  113. [120]Denby KJ Iwig J Bisson C Westwood J Rolfe MD Sedelnikova SE 2016 The mechanism of a formaldehyde-sensing transcriptional regulator Sci. Rep 6 38879 27934966 PMC5146963
  114. [121]Osman D Piergentili C Chen J Sayer LN Usón I Huggins TG 2016 The Effectors and sensory sites of formaldehyde-responsive regulator FrmR and metal-sensing variant J. Biol. Chem 291 19502 19516 27474740 PMC5016687
  115. [122]Luebke JL Shen J Bruce KE Kehl-Fie TE Peng H Skaar EP 2014 The CsoR-like sulfurtransferase repressor (CstR) is a persulfide sensor in Staphylococcus aureus Mol. Microbiol 94 1343 1360 25318663 PMC4264537
  116. [123]Chang FMJ Martin JE Giedroc DP 2015 Electrostatic occlusion and quaternary structural ion pairing are key determinants of Cu(I)-mediated allostery in the copper-sensing operon repressor (CsoR) Biochemistry 54 2463 2472 25798654
  117. [124]Higgins KA Chivers PT Maroney MJ 2012 Role of the N-terminus in determining metal-specific responses in the E. coli Ni- and Co-responsive metalloregulator, RcnR J. Am. Chem. Soc 134 7081 7093 22471551 PMC3375346
  118. [125]Osman D Piergentili C Chen J Chakrabarti B Foster AW Lurie-Luke E 2015 Generating a metal-responsive transcriptional regulator to test what confers metal sensing in cells J. Biol. Chem 290 19806 19822 26109070 PMC4528141
  119. [126]Jacobs AD Chang F-MJ Morrison L Dilger JM Wysocki VH Clemmer DE 2015 Resolution of stepwise cooperativities of copper binding by the homotetrameric copper-sensitive operon repressor (CsoR): impact on structure and stability Angew. Chem. Int. Ed. Engl 54 12795 12799 26332992 PMC4673887
  120. [127]Porto TV Hough MA Worrall JAR 2015 Structural insights into conformational switching in the copper metalloregulator CsoR from Streptomyces lividans Acta Crystallogr. D Biol. Crystallogr 71 1872 1878 26327377
  121. [128]Chang FMJ Coyne HJ Cubillas C Vinuesa P Fang X Ma Z 2014 Cu(I)-mediated allosteric switching in a copper-sensing operon repressor (CsoR) J. Biol. Chem 289 19204 19217 24831014 PMC4081955
  122. [129]Portmann R Poulsen KR Wimmer R Solioz M 2006 CopY-like copper inducible repressors are putative “winged helix” proteins BioMetals 19 61 70 16502332
  123. [130]Cantini F Banci L Solioz M 2009 The copper-responsive repressor CopR of Lactococcus lactis is a “winged helix” protein Biochem. J 417 493 499 18837698
  124. [131]Pazehoski KO Cobine PA Winzor DJ Dameron CT 2011 Evidence for involvement of the C-terminal domain in the dimerization of the CopY repressor protein from Enterococcus hirae Biochem. Biophys. Res. Commun 406 183 187 21295546 PMC3071704
  125. [132]Shafeeq S Yesilkaya H Kloosterman TG Narayanan G Wandel M Andrew PW 2011 The cop operon is required for copper homeostasis and contributes to virulence in Streptococcus pneumoniae Mol. Microbiol 81 1255 1270 21736642
  126. [133]Magnani D Barré O Gerber SD Solioz M 2008 Characterization of the CopR regulon of Lactococcus lactis IL1403 J. Bacteriol 190 536 545 17993525 PMC2223693
  127. [134]Cobine PA George GN Jones CE Wickramasinghe WA Solioz M Dameron CT 2002 Copper transfer from the Cu(I) Chaperone, CopZ, to the repressor, Zn(II)CopY: metal coordination environments and protein interactions Biochemistry 41 5822 5829 11980486
  128. [135]Strausak D Solioz M 1997 CopY is a copper-inducible repressor of the Enterococcus hirae copper ATPases J. Biol. Chem 272 8932 8936 9083014
  129. [136]Fillat MF 2014 The FUR (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators Arch. Biochem. Biophys 546 41 52 24513162
  130. [139]Johnston AWB Todd JD Curson AR Lei S Nikolaidou-Katsaridou N Gelfand MS 2007 Living without Fur: the subtlety and complexity of iron-responsive gene regulation in the symbiotic bacterium Rhizobium and other α-proteobacteria BioMetals 20 501 511 17310401
  131. [140]Ahn BE Cha J Lee EJ Han AR Thompson CJ Roe JH 2006 Nur, a nickel-responsive regulator of the Fur family, regulates superoxide dismutases and nickel transport in Streptomyces coelicolor Mol. Microbiol 59 1848 1858 16553888
  132. [143]Shin J Helmann JD 2016 Molecular logic of the Zur-regulated zinc deprivation response in Bacillus subtilis Nat. Commun 7 12612 27561249 PMC5007448
  133. [144]Shin J-H Jung HJ An YJ Cho Y-B Cha S-S Roe J-H 2011 Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur Proc. Natl. Acad. Sci. U.S.A 108 5045 5050 21383173 PMC3064357
  134. [145]Stapleton B Walker LR Logan TM 2013 Zn(II) stimulation of Fe(II)-activated repression in the iron-dependent repressor from Mycobacterium tuberculosis Biochemistry 52 1927 1938 23432191
  135. [146]Merchant AT Spatafora GA 2014 A role for the DtxR family of metalloregulators in gram-positive pathogenesis Mol. Oral Microbiol 29 1 10 24034418 PMC3866218
  136. [147]Twigg PD Parthasarathy G Guerrero L Logan TM Caspar DL 2001 Disordered to ordered folding in the regulation of diphtheria toxin repressor activity Proc. Natl. Acad. Sci. U.S.A 98 11259 11264 11572979 PMC58717
  137. [148]DeWitt MA Kliegman JI Helmann JD Brennan RG Farrens DL Glasfeld A 2007 The conformations of the manganese transport regulator of Bacillus subtilis in its metal-free state J. Mol. Biol 365 1257 1265 17118401 PMC2877129
  138. [150]Pohl E Holmes RK Hol WG 1999 Crystal structure of a cobalt-activated diphtheria toxin repressor-DNA complex reveals a metal-binding SH3-like domain J. Mol. Biol 292 653 667 10497029
  139. [151]Tanaka T Shinkai A Bessho Y Kumarevel T Yokoyama S 2009 Crystal structure of the manganese transport regulatory protein from Escherichia coli Proteins 77 741 746 19701940
  140. [152]McGuire AM Cuthbert BJ Ma Z Grauer-Gray KD Brunjes Brophy M Spear KA 2013 Roles of the A and C sites in the manganese-specific activation of MntR Biochemistry 52 701 713 23298157 PMC3562352
  141. [153]Lisher JP Higgins KA Maroney MJ Giedroc DP 2013 Physical characterization of the manganese-sensing pneumococcal surface antigen repressor from Streptococcus pneumoniae Biochemistry 52 7689 7701 24067066 PMC3859839
  142. [154]Stoll KE Draper WE Kliegman JI Golynskiy MV Brew-Appiah RAT Phillips RK 2009 Characterization and structure of the manganese-responsive transcriptional regulator ScaR Biochemistry 48 10308 10320 19795834 PMC3586275
  143. [155]Golynskiy M Li S Woods VL Jr Cohen SM 2007 Conformational studies of the manganese transport regulator (MntR) from Bacillus subtilis using deuterium exchange mass spectrometry J. Biol. Inorg. Chem 12 699 709 17342524
  144. [156]Schreiter ER Wang SC Zamble DB Drennan CL 2006 NikR-operator complex structure and the mechanism of repressor activation by metal ions Proc. Natl. Acad. Sci. U.S.A 103 13676 13681 16945905 PMC1564233
  145. [157]Phillips CM Schreiter ER Guo Y Wang SC Zamble DB Drennan CL 2008 Structural basis of the metal specificity for nickel regulatory protein NikR Biochemistry 47 1938 1946 18193897 PMC5914170
  146. [158]West AL St John F Lopes PEM MacKerell AD Pozharski E Michel SLJ 2010 Holo-Ni(II)HpNikR is an asymmetric tetramer containing two different nickel-binding sites J. Am. Chem. Soc 132 14447 14456 20863122 PMC2958704
  147. [159]Musiani F Zambelli B Bazzani M Mazzei L Ciurli S 2015 Nickel-responsive transcriptional regulators Metallomics 7 1305 1318 26099858
  148. [160]Wang SC Dias AV Bloom SL Zamble DB 2004 Selectivity of metal binding and metal-induced stability of Escherichia coli NikR Biochemistry 43 10018 10028 15287729
  149. [161]Chivers PT Sauer RT 2002 NikR repressor: high-affinity nickel binding to the C-terminal domain regulates binding to operator DNA Chem. Biol 9 1141 1148 12401498
  150. [162]Krecisz S Jones MD Zamble DB 2012 Nonspecific interactions between escherichia coli NikR and DNA are critical for nickel-activated DNA binding Biochemistry 51 7873 7879 22971172
  151. [163]Phillips CM Stultz CM Drennan CL 2010 Searching for the Nik operon: how a ligand-responsive transcription factor hunts for its DNA binding site Biochemistry 49 7757 7763 20712334 PMC2934762
  152. [164]West AL Evans SE Gonzalez JM Carter LG Tsuruta H Pozharski E 2012 Ni(II) coordination to mixed sites modulates DNA binding of HpNikR via a long-range effect Proc. Natl. Acad. Sci. U.S.A 109 5633 5638 22451934 PMC3326501
  153. [165]Cui G Merz KM Jr 2008 The intrinsic dynamics and function of nickel-binding regulatory protein: insights from elastic network analysis Biophys. J 94 3769 3778 18227134 PMC2367171
  154. [166]Zambelli B Danielli A Romagnoli S Neyroz P Ciurli S Scarlato V 2008 High-affinity Ni2+ binding selectively promotes binding of Helicobacter pylori NikR to its target urease promoter J. Mol. Biol 383 1129 1143 18790698
  155. [167]Bloom SL Zamble DB 2004 Metal-selective DNA-binding response of Escherichia coli NikR Biochemistry 43 10029 10038 15287730
  156. [168]Benanti EL Chivers PT 2011 Helicobacter pylori NikR protein exhibits distinct conformations when bound to different promoters J. Biol. Chem 286 15728 15737 21393642 PMC3091181
  157. [169]Mazzei L Dobrovolska O Musiani F Zambelli B Ciurli S 2015 On the interaction of Helicobacter pylori NikR, a Ni(II)-responsive transcription factor, with the urease operator: in solution and in silico studies J. Biol. Inorg. Chem 20 1021 1037 26204982
  158. [170]Muller C Bahlawane C Aubert S Delay CM Schauer K Michaud-Soret I 2011 Hierarchical regulation of the NikR-mediated nickel response in Helicobacter pylori Nucleic Acids Res 39 7564 7575 21666253 PMC3177205
  159. [171]Cuthbertson L Nodwell JR 2013 The TetR family of regulators Microbiol. Mol. Biol. Rev 77 440 475 24006471 PMC3811609
  160. [172]Kloosterman TG van der Kooi-Pol MM Bijlsma JJE Kuipers OP 2007 The novel transcriptional regulator SczA mediates protection against Zn2+ stress by activation of the Zn2+-resistance gene czcD in Streptococcus pneumoniae Mol. Microbiol 65 1049 1063 17640279
  161. [173]Zotta T Ricciardi A Ianniello RG Parente E Reale A Rossi F 2014 Assessment of aerobic and respiratory growth in the Lactobacillus casei group PLoS ONE 9 e99189 24918811 PMC4053349
  162. [174]Sawai H Yamanaka M Sugimoto H Shiro Y Aono S 2012 Structural basis for the transcriptional regulation of heme homeostasis in Lactococcus lactis J. Biol. Chem 287 30755 30768 22798069 PMC3436319
  163. [175]Große C Schleuder G Schmole C Nies DH 2014 Survival of Escherichia coli cells on solid copper surfaces is increased by glutathione Appl. Environ. Microbiol 80 7071 7078 25192999 PMC4249004
  164. [176]Mermod M Magnani D Solioz M Stoyanov JV 2012 The copper-inducible ComR (YcfQ) repressor regulates expression of ComC (YcfR), which affects copper permeability of the outer membrane of Escherichia coli BioMetals 25 33 43 22089859
  165. [177]Guerra AJ Dann CE Giedroc DP 2011 Crystal structure of the zinc-dependent MarR family transcriptional regulator AdcR in the Zn(II)-bound state J. Am. Chem. Soc 133 19614 19617 22085181 PMC3246308
  166. [178]Llull D Son O Blanié S Briffotaux J Morello E Rogniaux H 2011 Lactococcus lactis ZitR is a zinc-responsive repressor active in the presence of low, nontoxic zinc concentrations in vivo J. Bacteriol 193 1919 1929 21317326 PMC3133029
  167. [179]Reichheld SE Yu Z Davidson AR 2009 The induction of folding cooperativity by ligand binding drives the allosteric response of tetracycline repressor Proc. Natl. Acad. Sci. U.S.A 106 22263 22268 20080791 PMC2799725
  168. [180]Perera IC Grove A 2010 Molecular mechanisms of ligand-mediated attenuation of DNA binding by MarR family transcriptional regulators J. Mol. Cell Biol 2 243 254 20716550
  169. [182]Hao Z Lou H Zhu R Zhu J Zhang D Zhao BS 2013 The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli Nat. Chem. Biol 10 21 28 24185215
  170. [183]Hong M Fuangthong M Helmann JD Brennan RG 2005 Structure of an OhrR-ohrA operator complex reveals the DNA binding mechanism of the MarR family Mol. Cell 20 131 141 16209951
  171. [184]Lim D Poole K Strynadka NC 2002 Crystal structure of the MexR repressor of the mexRAB-oprM multidrug efflux operon of Pseudomonas aeruginosa J. Biol. Chem 277 29253 29259 12034710
  172. [185]Drazic A Miura H Peschek J Le Y Bach NC Kriehuber T 2013 Methionine oxidation activates a transcription factor in response to oxidative stress Proc. Natl. Acad. Sci. U.S.A 110 9493 9498 23690622 PMC3677443
  173. [186]Otani H Stogios PJ Xu X Nocek B Li S-N Savchenko A 2016 The activity of CouR, a MarR family transcriptional regulator, is modulated through a novel molecular mechanism Nucleic Acids Res 44 595 607 26400178 PMC4737184
  174. [187]Reyes-Caballero H Guerra AJ Jacobsen FE Kazmierczak KM Cowart D Koppolu UMK 2010 The metalloregulatory zinc site in Streptococcus pneumoniae AdcR, a Zinc-activated MarR family repressor J. Mol. Biol 403 197 216 20804771 PMC2949468
  175. [188]Gupta A Grove A 2014 Ligand-binding pocket bridges DNA-binding and dimerization domains of the urate-responsive marr homologue MftR from Burkholderia thailandensis Biochemistry 53 4368 4380 24955985 PMC4100783
  176. [189]Sanson M Makthal N Flores AR Olsen RJ Musser JM Kumaraswami M 2015 Adhesin competence repressor (AdcR) from Streptococcus pyogenes controls adaptive responses to zinc limitation and contributes to virulence Nucleic Acids Res 43 418 432 25510500 PMC4288194
  177. [190]Shafeeq S Kloosterman TG Kuipers OP 2011 Transcriptional response of Streptococcus pneumoniae to Zn2+) limitation and the repressor/activator function of AdcR Metallomics 3 609 618 21603707
  178. [191]Deochand DK Perera IC Crochet RB Gilbert NC Newcomer ME Grove A 2016 Histidine switch controlling pH-dependent protein folding and DNA binding in a transcription factor at the core of synthetic network devices Mol. BioSyst 12 2417 2426 27282811 PMC4955742
  179. [192]Anandapadamanaban M Pilstål R Andresen C Trewhella J Moche M Wallner B 2016 Mutation-induced population shift in the MexR conformational ensemble disengages DNA binding: a novel mechanism for MarR family derepression Structure 24 1311 1321 27427478
  180. [193]Chakravorty DK Parker TM Guerra AJ Sherrill CD Giedroc DP Merz KM Jr 2013 Energetics of zinc-mediated interactions in the allosteric pathways of metal sensor proteins J. Am. Chem. Soc 135 30 33 23214972 PMC3544337
  181. [194]Perera IC Lee YH Wilkinson SP Grove A 2009 Mechanism for attenuation of DNA binding by MarR family transcriptional regulators by small molecule ligands J. Mol. Biol 390 1019 1029 19501097
  182. [195]Choi H-J Kim S-J Mukhopadhyay P Cho S Woo J-R Storz G 2001 Structural basis of the redox switch in the OxyR transcription factor Cell 105 103 113 11301006
  183. [196]Hillion M Antelmann H 2015 Thiol-based redox switches in prokaryotes Biol. Chem 396 415 444 25720121 PMC4438307
  184. [197]Hoffmann M-C Ali K Sonnenschein M Robrahn L Strauss D Narberhaus F 2016 Molybdate uptake by Agrobacterium tumefaciens correlates with the cellular molybdenum cofactor status Mol. Microbiol 101 809 822 27196733
  185. [198]Anderson LA Palmer T Price NC Bornemann S Boxer DH Pau RN 1997 Characterisation of the molybdenum-responsive ModE regulatory protein and its binding to the promoter region of the modABCD (molybdenum transport) operon of Escherichia coli Eur. J. Biochem 246 119 126 9210473
  186. [199]Schüttelkopf AW Boxer DH Hunter WN 2003 Crystal structure of activated ModE reveals conformational changes involving both oxyanion and DNA-binding domains J. Mol. Biol 326 761 767 12581638
  187. [200]Lerche M Dian C Round A Lönneborg R Brzezinski P Leonard GA 2016 The solution configurations of inactive and activated DntR have implications for the sliding dimer mechanism of LysR transcription factors Sci. Rep 6 19988 26817994 PMC4730206
  188. [201]Jain D 2015 Allosteric control of transcription in GntR family of transcription regulators: a structural overview IUBMB Life 67 556 563 26172911
  189. [202]Tzeng S-R Kalodimos CG 2009 Dynamic activation of an allosteric regulatory protein Nature 462 368 372 19924217
  190. [203]Zheng M Cooper DR Grossoehme NE Yu M Hung LW Cieslik M 2009 Structure of Thermotoga maritima TM0439: implications for the mechanism of bacterial GntR transcription regulators with Zn2+-binding FCD domains Acta Crystallogr. D Biol. Crystallogr 65 356 365 19307717 PMC2659884
  191. [204]Blancato VS Pagliai FA Magni C Gonzalez CF Lorca GL 2016 Functional analysis of the citrate activator CitO from Enterococcus faecalis implicates a divalent metal in ligand binding Front. Microbiol 7 101 26903980 PMC4746285
  192. [205]Gao YG Suzuki H Itou H Zhou Y Tanaka Y Wachi M 2008 Structural and functional characterization of the LldR from Corynebacterium glutamicum: a transcriptional repressor involved in L-lactate and sugar utilization Nucleic Acids Res 36 7110 7123 18988622 PMC2602784
  193. [206]Cooper DR Grelewska K Kim CY Joachimiak A Derewenda ZS 2010 The structure of DinB from Geobacillus stearothermophilus: a representative of a unique four-helix-bundle superfamily Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun 66 219 224 PMC2833023 20208147
  194. [207]Watanabe S Kita A Kobayashi K Miki K 2008 Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA Proc. Natl. Acad. Sci. U.S.A 105 4121 4126 18334645 PMC2393793
  195. [208]Sasaki D Watanabe S Matsumi R Shoji T Yasukochi A Tagashira K 2013 Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation J. Mol. Biol 425 1627 1640 23399544
  196. [209]Ji Q Zhang L Jones MB Sun F Deng X Liang H 2013 Molecular mechanism of quinone signaling mediated through S-quinonization of a YodB family repressor QsrR Proc. Natl. Acad. Sci. U.S.A 110 5010 5015 23479646 PMC3612684
  197. [210]Safo MK Ko T Musayev FN Zhao Q Wang AH Archer GL 2006 Structure of the MecI repressor from Staphylococcus aureus in complex with the cognate DNA operator of mec Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun 62 320 324 PMC2222568 16582476
  198. [211]Volbeda 2017 Crystal structures of the NO sensor NsrR reveal how its iron-sulfur cluster modulates DNA binding Nat. Commun 8 15052 28425466 PMC5411485

Cited by

Sorted by citations

Authors
Capdevila, D. A., Edmonds, K. A., & Giedroc, D. P.
Affiliations
Indiana University Bloomington (US)
ORCID
Venue
Essays in Biochemistry
Publisher
Portland Press Ltd.
Published
2017-05-09
Volume
61
Issue
2
Pages
177-200
ISSN
  • 0071-1365 (ISSN-L)
  • 1744-1358
DOI
10.1042/ebc20160076
PMC
PMC5858914
OpenAlex
W2613869516
Cited by
136
References
11
Citations by year
2026: 15 · 2025: 11 · 2024: 17 · 2023: 17 · 2022: 21 · 2021: 15 · 2020: 18 · 2019: 14 · 2018: 6 · 2017: 2
FWCI
1.41
Type
journal article
Language
en
Open access
Locations
  • Essays in Biochemistry (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health
  • National Institute of General Medical Sciences (R35GM118157)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
  • Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
Keywords
metallochaperone, metalloregulation, metalloregulatory proteins, metal sensing, metalloenzymes, metal toxicity, metal ion specificity
MeSH terms
Allosteric Regulation, Bacteria, Bacterial Proteins, Metallochaperones

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