Cited by 77Bacterial Genetics and BiotechnologyMetalloenzymes and iron-sulfur proteinsProtein Structure and Dynamics

Metal site occupancy and allosteric switching in bacterial metal sensor proteins

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Guerra, Alfredo J., Giedroc, David P.·2012·Archives of Biochemistry and Biophysics

Abstract

All prokaryotes encode a panel of metal sensor or metalloregulatory proteins that govern the expression of genes that allows an organism to quickly adapt to toxicity or deprivation of both biologically essential transition metal ions, e.g., Zn, Cu, Fe, and heavy metal pollutants. As such, metal sensor proteins can be considered arbiters of intracellular transition metal bioavailability and thus potentially control the metallation state of the metalloproteins in the cell. Metal sensor proteins are specialized allosteric proteins that regulate transcription as a result direct binding of one or two cognate metal ions, to the exclusion of all others. In most cases, the binding of the cognate metal ion induces a structural change in a protein oligomer that either activates or inhibits operator DNA binding. A quantitative measure of the degree to which a particular metal drives metalloregulation of operator DNA-binding is the allosteric coupling free energy, ΔGc. In this review, we summarize recent work directed toward understanding metal occupancy and metal selectivity of these allosteric switches in selected families of metal sensor proteins and examine the structural origins of ΔGc in the functional context a thermodynamic "set-point" model of intracellular metal homeostasis.

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  • Sensitivity is determined by the affinity of the metalloregulator for its cognate ion and the effects of DNA-binding on metal affinity.

    “Sensitivity is determined by the affinity of the metalloregulator for its cognate ion and the effects of DNA-binding on metal affinity (thermodynamic coupling), as discussed in detail elsewhere.26,30”

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Research works printed but not linked: 131

  1. [1]Reyes-Caballero H Campanello GC Giedroc DP Biophys Chem 156 2011 103 114 21511390 PMC3097251
  2. [2]Giedroc DP Arunkumar AI Dalton Trans 29 2007 3107 3120 17637984
  3. [3]Ma Z Jacobsen FE Giedroc DP Chem Rev 109 2009 4644 4681 19788177 PMC2783614
  4. [4]Busenlehner LS Pennella MA Giedroc DP FEMS Microbiol Rev 27 2003 131 143 12829264
  5. [5]Osman D Cavet JS Nat Prod Rep 27 2010 668 680 20442958
  6. [6]Mandal S Chatterjee S Dam B Roy P Das Gupta SK Microbiology 153 2007 80 91 17185537
  7. [7]Guimaraes BG Barbosa RL Soprano AS Campos BM de Souza TA Tonoli CC Leme AF Murakami MT Benedetti CE J Biol Chem 286 2011 26148 26157 21632538 PMC3138302
  8. [8]Lee JW Helmann JD Biometals 20 2007 485 499 17216355
  9. [9]Kloosterman TG van der Kooi-Pol MM Bijlsma JJ Kuipers OP Mol Microbiol 65 2007 1049 1063 17640279
  10. [10]Kloosterman TG Witwicki RM van der Kooi-Pol MM Bijlsma JJ Kuipers OP J Bacteriol 190 2008 5382 5393 18515418 PMC2493273
  11. [11]Reyes-Caballero H Guerra AJ Jacobsen FE Kazmierczak KM Cowart D Koppolu UM Scott RA Winkler ME Giedroc DP J Mol Biol 403 2010 197 216 20804771 PMC2949468
  12. [12]Jacobsen FE Kazmierczak KM Lisher JP Winkler ME Giedroc DP Metallomics 3 2011 38 41 21275153 PMC3061551
  13. [13]Shafeeq S Kloosterman TG Kuipers OP Metallomics 3 2011 609 618 21603707
  14. [14]Orth P Schnappinger D Hillen W Saenger W Hinrichs W Nat Struct Biol 7 2000 215 219 10700280
  15. [15]Kuroda M Hayashi H Ohta T Microbiol Immunol 43 1999 115 125 10229265
  16. [16]Arunkumar AI Campanello GC Giedroc DP Proc Natl Acad Sci U S A 106 2009 18177 18182 19822742 PMC2775347
  17. [17]Outten CE Outten FW O'Halloran TV J Biol Chem 274 1999 37517 37524 10608803
  18. [18]Changela A Chen K Xue Y Holschen J Outten CE O'Halloran TV Mondragon A Science 301 2003 1383 1387 12958362
  19. [19]Llull D Poquet I Appl Environ Microbiol 70 2004 5398 5406 15345426 PMC520854
  20. [20]Llull D Son O Blanie S Briffotaux J Morello E Rogniaux H Danot O Poquet I J Bacteriol 193 2011 1919 1929 21317326 PMC3133029
  21. [21]Panina EM Mironov AA Gelfand MS Proc Natl Acad Sci U S A 100 2003 9912 9917 12904577 PMC187884
  22. [22]Outten CE O'Halloran TV Science 292 2001 2488 2492 11397910
  23. [23]Waldron KJ Robinson NJ Nat Rev Microbiol 7 2009 25 35 19079350
  24. [24]Waldron KJ Rutherford JC Ford D Robinson NJ Nature 460 2009 823 830 19675642
  25. [26]Eide DJ Biochim Biophys Acta 1763 2006 711 722 16675045
  26. [27]Krezel A Maret W J Am Chem Soc 129 2007 10911 10921 17696343
  27. [28]Suhy DA Simon KD Linzer DI O'Halloran TV J Biol Chem 274 1999 9183 9192 10092590
  28. [29]Maret W J Nutr 133 2003 1460S 1462S 12730443
  29. [30]Krezel A Maret W J Biol Inorg Chem 11 2006 1049 1062 16924557
  30. [31]Bozym RA Thompson RB Stoddard AK Fierke CA ACS Chem Biol 1 2006 103 111 17163650
  31. [32]Vinkenborg JL Nicolson TJ Bellomo EA Koay MS Rutter GA Merkx M Nat Methods 6 2009 737 740 19718032 PMC6101214
  32. [33]Otvos JD Armitage IM Proc Natl Acad Sci U S A 77 1980 7094 7098 6938956 PMC350447
  33. [34]Zangger K Oz G Otvos JD Armitage IM Protein Sci 8 1999 2630 2638 10631978 PMC2144227
  34. [35]Pruteanu M Neher SB Baker TA J Bacteriol 189 2007 3017 3025 17220226 PMC1855835
  35. [36]Mettert EL Kiley PJ J Mol Biol 354 2005 220 232 16243354
  36. [37]Pruteanu M Baker TA Res Microbiol 160 2009 677 683 19747971 PMC2783568
  37. [38]Festa RA Jones MB Butler-Wu S Sinsimer D Gerads R Bishai WR Peterson SN Darwin KH Mol Microbiol 79 2011 133 148 21166899 PMC3052634
  38. [39]Stoyanov JV Mancini S Lu ZH Mourlane F Poulsen KR Wimmer R Solioz M FEMS Microbiol Lett 302 2010 69 75 19903200
  39. [40]Grossoehme NE Giedroc DP J Am Chem Soc 131 2009 17860 17870 19995076 PMC2811267
  40. [41]Ma Z Cowart DM Ward BP Arnold RJ DiMarchi RD Zhang L George GN Scott RA Giedroc DP J Am Chem Soc 131 2009 18044 18045 19928961 PMC2797707
  41. [42]Reinhart GD Methods Enzymol 380 2004 187 203 15051338
  42. [43]Singh VK Xiong A Usgaard TR Chakrabarti S Deora R Misra TK Jayaswal RK Mol Microbiol 33 1999 200 207 10411736
  43. [44]Xiong A Jayaswal RK J Bacteriol 180 1998 4024 4029 9696746 PMC107394
  44. [45]Sun Y Wong MD Rosen BP J Biol Chem 276 2001 14955 14960 11278706
  45. [46]Andrews SC Robinson AK Rodriguez-Quinones F FEMS Microbiol Rev 27 2003 215 237 12829269
  46. [47]Stoll KE Draper WE Kliegman JI Golynskiy MV Brew-Appiah RA Phillips RK Brown HK Breyer WA Jakubovics NS Jenkinson HF Brennan RG Cohen SM Glasfeld A Biochemistry 48 2009 10308 10320 19795834 PMC3586275
  47. [48]Pennella MA Arunkumar AI Giedroc DP J Mol Biol 356 2006 1124 1136 16406068
  48. [49]Busenlehner LS Weng TC Penner-Hahn JE Giedroc DP J Mol Biol 319 2002 685 701 12054863
  49. [50]Cavet JS Graham AI Meng W Robinson NJ J Biol Chem 278 2003 44560 44566 12939264
  50. [51]Wang Y Hemmingsen L Giedroc DP Biochemistry 44 2005 8976 8988 15966722
  51. [52]Ma Z Gabriel SE Helmann JD Nucl Acids Res 2011 in press PMC3241647 21821657
  52. [53]Popovych N Sun S Ebright RH Kalodimos CG Nat Struct Mol Biol 13 2006 831 838 16906160 PMC2757644
  53. [54]Lefevre JF Dayie KT Peng JW Wagner G Biochemistry 35 1996 2674 2686 8611573
  54. [55]Krizova H Zidek L Stone MJ Novotny MV Sklenar V J Biomol NMR 28 2004 369 384 14872128
  55. [56]Kern D Zuiderweg ER Curr Opin Struct Biol 13 2003 748 757 14675554
  56. [57]Akke M Curr Opin Struct Biol 12 2002 642 647 12464317
  57. [58]Englander JJ Louie G McKinnie RE Englander SW J Mol Biol 284 1998 1695 1706 9878380
  58. [59]Reyes-Caballero H Lee CW Giedroc DP Biochemistry 50 2011 7941 7952 21819125 PMC3225088
  59. [60]Ma Z Lee JW Helmann JD Nucl Acids Res 39 2011 5036 5044 21398634 PMC3130269
  60. [61]Grossoehme NE Akilesh S Guerinot ML Wilcox DE Inorg Chem 45 2006 8500 8508 17029360
  61. [62]Pohl E Holmes RK Hol WG J Mol Biol 285 1999 1145 1156 9887269
  62. [63]Pohl E Haller JC Mijovilovich A Meyer-Klaucke W Garman E Vasil ML Mol Microbiol 47 2003 903 915 12581348
  63. [64]Dian C Vitale S Leonard GA Bahlawane C Fauquant C Leduc D Muller C de Reuse H Michaud-Soret I Terradot L Mol Microbiol 79 2011 1260 1275 21208302
  64. [65]Lucarelli D Russo S Garman E Milano A Meyer-Klaucke W Pohl E J Biol Chem 282 2007 9914 9922 17213192
  65. [66]Shin JH Jung HJ An YJ Cho YB Cha SS Roe JH Proc Natl Acad Sci U S A 108 2011 5045 5050 21383173 PMC3064357
  66. [67]Guerra AJ Dann CE III Giedroc DP J Am Chem Soc 2011 in press 10.1021/ja2080532 PMC3246308 22085181 · DOI
  67. [68]Eicken C Pennella MA Chen X Koshlap KM VanZile ML Sacchettini JC Giedroc DP J Mol Biol 333 2003 683 695 14568530
  68. [69]Busenlehner LS Giedroc DP J Inorg Biochem 100 2006 1024 1034 16487591
  69. [70]VanZile ML Cosper NJ Scott RA Giedroc DP Biochemistry 39 2000 11818 11829 10995250
  70. [71]Lee S Arunkumar AI Chen X Giedroc DP J Am Chem Soc 128 2006 1937 1947 16464095
  71. [72]Maciag A Dainese E Rodriguez GM Milano A Provvedi R Pasca MR Smith I Palu G Riccardi G Manganelli R J Bacterio l 189 2007 730 740 PMC1797298 17098899
  72. [73]Diaz-Mireles E Wexler M Sawers G Bellini D Todd JD Johnston AW Microbiology 150 2004 1447 1456 15133106
  73. [74]Ahn BE Cha J Lee EJ Han AR Thompson CJ Roe JH Mol Microbiol 59 2006 1848 1858 16553888
  74. [75]An YJ Ahn BE Han AR Kim HM Chung KM Shin JH Cho YB Roe JH Cha SS Nucl Acids Res 2009 3442 3451 19336416 PMC2691836
  75. [76]Lee JW Helmann JD Nature 440 2006 363 367 16541078
  76. [77]Jacquamet L Traore DA Ferrer JL Proux O Testemale D Hazemann JL Nazarenko E El Ghazouani A Caux-Thang C Duarte V Latour JM Mol Microbiol 73 2009 20 31 19508285
  77. [78]Small SK Puri S O'Brian MR Biometals 22 2009 89 97 19093075 PMC2659648
  78. [79]Hibbing ME Fuqua C J Bacteriol 193 2011 3461 3472 21602352 PMC3133315
  79. [80]Traore DA El Ghazouani A Jacquamet L Borel F Ferrer JL Lascoux D Ravanat JL Jaquinod M Blondin G Caux-Thang C Duarte V Latour JM Nat Chem Biol 5 2009 53 59 19079268
  80. [81]Traore DA El Ghazouani A Ilango S Dupuy J Jacquamet L Ferrer JL Caux-Thang C Duarte V Latour JM Mol Microbiol 61 2006 1211 1219 16925555
  81. [82]Outten CE Tobin DA Penner-Hahn JE O'Halloran TV Biochemistry 40 2001 10417 10423 11523983
  82. [83]Carrington PE Chivers PT Al-Mjeni F Sauer RT Maroney MJ Nat Struct Biol 10 2003 126 130 12524532
  83. [84]Pennella MA Shokes JE Cosper NJ Scott RA Giedroc DP Proc Natl Acad Sci U S A 100 2003 3713 3718 12651949 PMC152987
  84. [85]Giedroc DP Mol Microbiol 73 2009 1 4 19508286 PMC2765198
  85. [86]Ma Z Cowart DM Scott RA Giedroc DP Biochemistry 48 2009 3325 3334 19249860 PMC2728441
  86. [87]Bradley MJ Chivers PT Baker NA J Mol Biol 378 2008 1155 1173 18433769 PMC2478562
  87. [88]Sindhikara DJ Roitberg AE Merz KM Jr Biochemistry 48 2009 12024 12033 19891498 PMC2795120
  88. [89]Chakravorty DK Wang B Lee CW Giedroc DP Merz KM J Am Chem Soc 2011 in press PMC3288340 22007899
  89. [90]Watanabe S Kita A Kobayashi K Miki K Proc Natl Acad Sci U S A 105 2008 4121 4126 18334645 PMC2393793
  90. [91]Liu T Ramesh A Ma Z Ward SK Zhang L George GN Talaat AM Sacchettini JC Giedroc DP Nat Chem Biol 3 2007 60 68 17143269
  91. [92]Corbett D Schuler S Glenn S Andrew PW Cavet JS Roberts IS Mol Microbiol 2011 21564342
  92. [93]Iwig JS Rowe JL Chivers PT Mol Microbiol 62 2006 252 262 16956381
  93. [94]Iwig JS Leitch S Herbst RW Maroney MJ Chivers PT J Am Chem Soc 130 2008 7592 7606 18505253 PMC2435081
  94. [95]Grossoehme N Kehl-Fie TE Ma Z Adams KW Cowart DM Scott RA Skaar EP Giedroc DP J Biol Chem 286 2011 13522 13531 21339296 PMC3075698
  95. [96]Campbell DR Chapman KE Waldron KJ Tottey S Kendall S Cavallaro G Andreini C Hinds J Stoker NG Robinson NJ Cavet JS J Biol Chem 282 2007 32298 32310 17726022 PMC3145109
  96. [97]Wu J Rosen BP J Biol Chem 268 1993 52 58 8416957
  97. [98]Morby AP Turner JS Huckle JW Robinson NJ Nucl Acids Res 21 1993 921 925 8451191 PMC309225
  98. [99]Harvie DR Andreini C Cavallaro G Meng W Connolly BA Yoshida K Fujita Y Harwood CR Radford DS Tottey S Cavet JS Robinson NJ Mol Microbiol 59 2006 1341 1356 16430705
  99. [100]Cavet JS Meng W Pennella MA Appelhoff RJ Giedroc DP Robinson NJ J Biol Chem 277 2002 38441 38448 12163508
  100. [102]Banci L Bertini I Cantini F Ciofi-Baffoni S Cavet JS Dennison C Graham AI Harvie DR Robinson NJ J Biol Chem 282 2007 30181 30188 17599915
  101. [103]Ye J Kandegedara A Martin P Rosen BP J Bacteriol 187 2005 4214 4221 15937183 PMC1151749
  102. [104]Barondeau DP Kassmann CJ Bruns CK Tainer JA Getzoff ED Biochemistry 43 2004 8038 8047 15209499
  103. [105]Sankararamakrishnan R Verma S Kumar S Proteins 58 2005 211 221 15508143
  104. [106]Chung KC Cao L Dias AV Pickering IJ George GN Zamble DB J Am Chem Soc 130 2008 14056 14057 18834129
  105. [107]West AL St John F Lopes PE MacKerell AD Jr Pozharski E Michel SL J Am Chem Soc 132 2010 14447 14456 20863122 PMC2958704
  106. [108]Schreiter ER Wang SC Zamble DB Drennan CL Proc Natl Acad Sci U S A 103 2006 13676 13681 16945905 PMC1564233
  107. [109]Phillips CM Nerenberg PS Drennan CL Stultz CM J Am Chem Soc 131 2009 10220 10228 19621966 PMC3579654
  108. [110]Phillips CM Schreiter ER Stultz CM Drennan CL Biochemistry 49 2010 7830 7838 20704276 PMC2934763
  109. [111]Borremans B Hobman JL Provoost A Brown NL van Der Lelie D J Bacteriol 183 2001 5651 5658 11544228 PMC95457
  110. [112]Chen P Greenberg B Taghavi S Romano C van der Lelie D He C Angew Chem Int Ed Engl 44 2005 2715 2719 15800869
  111. [113]Lund PA Ford SJ Brown NL J Gen Microbiol 132 Pt 2 1986 465 480 3011964
  112. [114]Ralston DM O'Halloran TV Proc Natl Acad Sci U S A 87 1990 3846 3850 2187194 PMC54000
  113. [115]Hobman JL Wilkie J Brown NL Biometals 18 2005 429 436 16158235
  114. [116]Dosanjh NS West AL Michel SL Biochemistry 48 2009 527 536 19119856
  115. [117]van Vliet AH Ernst FD Kusters JG Trends Microbiol 12 2004 489 494 15488389
  116. [118]Dosanjh NS Michel SL Curr Opin Chem Biol 10 2006 123 130 16504569
  117. [119]Ernst FD Stoof J Horrevoets WM Kuipers EJ Kusters JG van Vliet AH Infect Immun 74 2006 6821 6828 17015456 PMC1698083
  118. [120]Dosanjh NS Hammerbacher NA Michel SL Biochemistry 46 2007 2520 2529 17291009
  119. [121]Dian C Schauer K Kapp U McSweeney SM Labigne A Terradot L J Mol Biol 361 2006 715 730 16872629
  120. [122]Benini S Cianci M Ciurli S Dalton Trans 40 2011 7831 7833 21725560
  121. [123]Wen Y Feng J Scott DR Marcus EA Sachs G J Bacteriol 191 2009 449 460 18978046 PMC2620809
  122. [124]Tottey S Harvie DR Robinson NJ Acc Chem Res 38 2005 775 783 16231873
  123. [125]Kell DB Arch Toxicol 84 2010 825 889 20967426 PMC2988997
  124. [126]Burkhead JL Gray LW Lutsenko S Biometals 24 2011 455 466 21380607 PMC3106420
  125. [127]Whitmire JM Gancz H Merrell DS Curr Med Chem 14 2007 469 478 17305547
  126. [128]Flo TH Smith KD Sato S Rodriguez DJ Holmes MA Strong RK Akira S Aderem A Nature 432 2004 917 921 15531878
  127. [129]Corbin BD Seeley EH Raab A Feldmann J Miller MR Torres VJ Anderson KL Dattilo BM Dunman PM Gerads R Caprioli RM Nacken W Chazin WJ Skaar EP Science 319 2008 962 965 18276893
  128. [130]Kehl-Fie TE Chitayat S Hood MI Damo S Restrepo N Garcia C Munro KA Chazin WJ Skaar EP Cell Host Microbe 10 2011 158 164 21843872 PMC3157011
  129. [131]Nobles CL Maresso AW Metallomics 3 2011 788 796 21725569
  130. [132]Kehl-Fie TE Skaar EP Curr Opin Chem Biol 14 2010 218 224 20015678 PMC2847644
  131. [133]Wang SC Dias AV Bloom SL Zamble DB Biochemistry 43 2004 10018 10028 15287729

Cited by

Sorted by citations

Authors
Guerra, A. J., & Giedroc, D. P.
Affiliations
Indiana University Bloomington (US)
Corresponding author
Giedroc, David P.
Venue
Archives of Biochemistry and Biophysics
Publisher
Elsevier BV
Published
2012-03
Volume
519
Issue
2
Pages
210-222
ISSN
0003-9861 (ISSN-L)
OpenAlex
W2085328815
Cited by
77
References
9
Citations by year
2026: 2 · 2025: 4 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 1 · 2020: 1 · 2019: 7 · 2018: 5 · 2017: 8 · 2016: 7 · 2015: 9 · 2014: 11 · 2013: 7 · 2012: 4
FWCI
0.75
Type
journal article
Language
en
Open access
Locations
  • Archives of Biochemistry and Biophysics (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
US National Institutes of Health (GM042569)
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
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
Keywords
metalloregulation, metal ion selectivity, transition metal homeostasis, transcriptional regulation, DNA binding, metalloproteins, bacterial metal homeostasis
MeSH terms
Allosteric Regulation, Bacteria, Bacterial Proteins, DNA, Bacterial, Metals

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