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Cited by 153Bacterial Genetics and BiotechnologyTrace Elements in HealthMetal-Catalyzed Oxygenation Mechanisms

Cu Homeostasis in Bacteria: The Ins and Outs

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Andrei, Andreea, Öztürk, Yavuz, Khalfaoui-Hassani, Bahia, Rauch, Juna, Marckmann, Dorian, Trasnea, Petru-Iulian, Daldal, Fevzi, Koch, Hans-Georg·2020·Membranes
DOI 10.3390/membranes10090242PMC PMC7558416
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Abstract

Copper (Cu) is an essential trace element for all living organisms and used as cofactor in key enzymes of important biological processes, such as aerobic respiration or superoxide dismutation. However, due to its toxicity, cells have developed elaborate mechanisms for Cu homeostasis, which balance Cu supply for cuproprotein biogenesis with the need to remove excess Cu. This review summarizes our current knowledge on bacterial Cu homeostasis with a focus on Gram-negative bacteria and describes the multiple strategies that bacteria use for uptake, storage and export of Cu. We furthermore describe general mechanistic principles that aid the bacterial response to toxic Cu concentrations and illustrate dedicated Cu relay systems that facilitate Cu delivery for cuproenzyme biogenesis. Progress in understanding how bacteria avoid Cu poisoning while maintaining a certain Cu quota for cell proliferation is of particular importance for microbial pathogens because Cu is utilized by the host immune system for attenuating pathogen survival in host cells.

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  • The thiolate coordination chemistry of Hg2+ provides a model for how Hg2+ can transfer between resistance proteins MerT, MerR, and MerA and foreshadowed the similar pathway for Cu+ transfer between chaperones and client proteins.

    “This provides a model for how Hg2+ can transfer between resistance proteins that function in transport (MerT), sensing (MerR), and reduction (MerA) and foreshadowed the similar pathway described for the transfer of Cu+ between chaperones and client proteins.196,211”

    From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [196]

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  1. [1]Argüello J.M. Raimunda D. Padilla-Benavides T. Mechanisms of copper homeostasis in bacteria Front. Cell. Infect. Microbiol. 2013 3 73 10.3389/fcimb.2013.00073 24205499 PMC3817396 · DOI
  2. [3]Ibrahim Z. Petrusan A.J. Hooke P. Hinsa-Leasure S.M. Reduction of bacterial burden by copper alloys on high-touch athletic center surfaces Am. J. Infect. Control 2018 46 197 201 10.1016/j.ajic.2017.08.028 29102052 · DOI
  3. [4]Besold A.N. Culbertson E.M. Culotta V.C. The Yin and Yang of copper during infection J. Biol. Inorg. Chem. 2016 21 137 144 10.1007/s00775-016-1335-1 26790881 PMC5535265 · DOI · Paper page
  4. [5]Ladomersky E. Khan A. Shanbhag V. Cavet J.S. Chan J. Weisman G.A. Petris M.J. Host and Pathogen Copper-Transporting P-Type ATPases Function Antagonistically during Salmonella Infection Infect. Immun. 2017 85 10.1128/IAI.00351-17 28652309 PMC5563570 · DOI
  5. [6]Antoine R. Rivera-Millot A. Roy G. Jacob-Dubuisson F. Relationships Between Copper-Related Proteomes and Lifestyles in β Proteobacteria Front. Microbiol. 2019 10 2217 10.3389/fmicb.2019.02217 31608037 PMC6769254 · DOI
  6. [7]Ward S.K. Hoye E.A. Talaat A.M. The global responses of Mycobacterium tuberculosis to physiological levels of copper J. Bacteriol. 2008 190 2939 2946 10.1128/JB.01847-07 18263720 PMC2293257 · DOI
  7. [8]Ward S.K. Abomoelak B. Hoye E.A. Steinberg H. Talaat A.M. CtpV: A putative copper exporter required for full virulence of Mycobacterium tuberculosis Mol. Microbiol. 2010 77 1096 1110 10.1111/j.1365-2958.2010.07273.x 20624225 PMC2965804 · DOI
  8. [9]Wolschendorf F. Ackart D. Shrestha T.B. Hascall-Dove L. Nolan S. Lamichhane G. Wang Y. Bossmann S.H. Basaraba R.J. Niederweis M. Copper resistance is essential for virulence of Mycobacterium tuberculosis Proc. Natl. Acad. Sci. USA 2011 108 1621 1626 10.1073/pnas.1009261108 21205886 PMC3029754 · DOI · Paper page
  9. [10]Price E.E. Boyd J.M. Genetic Regulation of Metal Ion Homeostasis in Staphylococcus aureus Trends Microbiol. 2020 10.1016/j.tim.2020.04.004 PMC7494629 32381454 · DOI
  10. [11]Begg S.L. The role of metal ions in the virulence and viability of bacterial pathogens Biochem. Soc. Trans. 2019 47 77 87 10.1042/BST20180275 30626704 · DOI
  11. [12]Li C. Li Y. Ding C. The Role of Copper Homeostasis at the Host-Pathogen Axis: From Bacteria to Fungi Int. J. Mol. Sci. 2019 20 175 10.3390/ijms20010175 30621285 PMC6337107 · DOI · Paper page
  12. [13]Dupont C.L. Grass G. Rensing C. Copper toxicity and the origin of bacterial resistance—New insights and applications Met. Integr. Biometal Sci. 2011 3 1109 1118 10.1039/c1mt00107h 21984219 · DOI
  13. [14]Shi X. Darwin K.H. Copper homeostasis in Mycobacterium tuberculosis Met. Integr. Biometal Sci. 2015 7 929 934 10.1039/C4MT00305E 25614981 PMC4465026 · DOI
  14. [15]Braymer J.J. Giedroc D.P. Recent developments in copper and zinc homeostasis in bacterial pathogens Curr. Opin. Chem. Biol. 2014 19 59 66 10.1016/j.cbpa.2013.12.021 24463765 PMC4008645 · DOI · Paper page
  15. [16]Foster A.W. Osman D. Robinson N.J. Metal preferences and metallation J. Biol. Chem. 2014 289 28095 28103 10.1074/jbc.R114.588145 25160626 PMC4192464 · DOI
  16. [17]Gaetke L.M. Chow C.K. Copper toxicity, oxidative stress, and antioxidant nutrients Toxicology 2003 189 147 163 10.1016/S0300-483X(03)00159-8 12821289 · DOI
  17. [18]Stewart L.J. Thaqi D. Kobe B. McEwan A.G. Waldron K.J. Djoko K.Y. Handling of nutrient copper in the bacterial envelope Met. Integr. Biometal Sci. 2019 11 50 63 10.1039/C8MT00218E 30334058 · DOI · Paper page
  18. [19]Durand A. Azzouzi A. Bourbon M.L. Steunou A.S. Liotenberg S. Maeshima A. Astier C. Argentini M. Saito S. Ouchane S. c-Type Cytochrome Assembly Is a Key Target of Copper Toxicity within the Bacterial Periplasm mBio 2015 6 e01007 e01015 10.1128/mBio.01007-15 26396241 PMC4600104 · DOI
  19. [20]Steunou A.S. Durand A. Bourbon M.L. Babot M. Tambosi R. Liotenberg S. Ouchane S. Cadmium and Copper Cross-Tolerance. Cu+ Alleviates Cd2+ Toxicity, and Both Cations Target Heme and Chlorophyll Biosynthesis Pathway in Rubrivivax gelatinosus Front. Microbiol. 2020 11 893 10.3389/fmicb.2020.00893 32582041 PMC7283390 · DOI
  20. [21]Hiniker A. Collet J.F. Bardwell J.C. Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC J. Biol. Chem. 2005 280 33785 33791 10.1074/jbc.M505742200 16087673 · DOI
  21. [22]Decker H. Terwilliger N. Cops and robbers: Putative evolution of copper oxygen-binding proteins J. Exp. Biol. 2000 203 1777 1782 10821735
  22. [23]Ekici S. Yang H. Koch H.-G. Daldal F. Novel transporter required for biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulatus mBio 2012 3 10.1128/mBio.00293-11 22294680 PMC3266609 · DOI
  23. [24]Banci L. Bertini I. Cantini F. Ciofi-Baffoni S. Cellular copper distribution: A mechanistic systems biology approach Cell. Mol. Life Sci. CMLS 2010 67 2563 2589 10.1007/s00018-010-0330-x 20333435 PMC11115773 · DOI
  24. [25]Rensing C. McDevitt S.F. The copper metallome in prokaryotic cells Met. Ions. Life Sci. 2013 12 417 450 10.1007/978-94-007-5561-1_12 23595679 · DOI
  25. [26]Aguirre G. Pilon M. Copper Delivery to Chloroplast Proteins and its Regulation Front. Plant Sci. 2015 6 1250 10.3389/fpls.2015.01250 26793223 PMC4709454 · DOI
  26. [27]Canonica F. Klose D. Ledermann R. Sauer M.M. Abicht H.K. Quade N. Gossert A.D. Chesnov S. Fischer H.M. Jeschke G. Structural basis and mechanism for metallochaperone-assisted assembly of the Cu(A) center in cytochrome oxidase Sci. Adv. 2019 5 eaaw8478 10.1126/sciadv.aaw8478 31392273 PMC6669012 · DOI
  27. [28]Ekici S. Pawlik G. Lohmeyer E. Koch H.-G. Daldal F. Biogenesis of cbb(3)-type cytochrome c oxidase in Rhodobacter capsulatus Biochim. Biophys. Acta 2012 1817 898 910 10.1016/j.bbabio.2011.10.011 22079199 PMC3304015 · DOI
  28. [29]Kudva R. Denks K. Kuhn P. Vogt A. Muller M. Koch H.G. Protein translocation across the inner membrane of Gram-negative bacteria: The Sec and Tat dependent protein transport pathways Res. Microbiol. 2013 164 505 534 10.1016/j.resmic.2013.03.016 23567322 · DOI · Paper page
  29. [30]Stolle P. Hou B. Brüser T. The Tat Substrate CueO Is Transported in an Incomplete Folding State J. Biol. Chem. 2016 291 13520 13528 10.1074/jbc.M116.729103 27129241 PMC4919438 · DOI
  30. [31]Koch H.G. Winterstein C. Saribas A.S. Alben J.O. Daldal F. Roles of the ccoGHIS gene products in the biogenesis of the cbb(3)-type cytochrome c oxidase J. Mol. Biol. 2000 297 49 65 10.1006/jmbi.2000.3555 10704306 · DOI
  31. [32]Kulajta C. Thumfart J.O. Haid S. Daldal F. Koch H.G. Multi-step assembly pathway of the cbb3-type cytochrome c oxidase complex J. Mol. Biol. 2006 355 989 1004 10.1016/j.jmb.2005.11.039 16343536 · DOI
  32. [33]Khalfaoui-Hassani B. Verissimo A.F. Shroff N.P. Ekici S. Trasnea P.-I. Utz M. Koch H.-G. Daldal F. Biogenesis of Cytochrome c Complexes: From Insertion of Redox Cofactors to Assembly of Different Subunits Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling Cramer W.A. Kallas T. Springer Dordrecht, The Netherlands 2016 527 554
  33. [34]Richter O.M. Ludwig B. Cytochrome c oxidase—Structure, function, and physiology of a redox-driven molecular machine Rev. Physiol. Biochem. Pharmacol. 2003 147 47 74 10.1007/s10254-003-0006-0 12783267 · DOI
  34. [35]Ross M.O. Rosenzweig A.C. A tale of two methane monooxygenases J. Biol. Inorg. Chem. JBIC Publ. Soc. Biol. Inorg. Chem. 2017 22 307 319 10.1007/s00775-016-1419-y PMC5352483 27878395 · DOI
  35. [36]Roberts S.A. Weichsel A. Grass G. Thakali K. Hazzard J.T. Tollin G. Rensing C. Montfort W.R. Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli Proc. Natl. Acad. Sci. USA 2002 99 2766 2771 10.1073/pnas.052710499 11867755 PMC122422 · DOI
  36. [37]Horrell S. Kekilli D. Strange R.W. Hough M.A. Recent structural insights into the function of copper nitrite reductases Met. Integr. Biometal Sci. 2017 9 1470 1482 10.1039/C7MT00146K 28702572 · DOI
  37. [38]Palm-Espling M.E. Niemiec M.S. Wittung-Stafshede P. Role of metal in folding and stability of copper proteins in vitro Biochim. Biophys. Acta 2012 1823 1594 1603 10.1016/j.bbamcr.2012.01.013 22306006 · DOI
  38. [39]Fenlon L.A. Slauch J.M. Cytoplasmic Copper Detoxification in Salmonella Can Contribute to SodC Metalation but Is Dispensable during Systemic Infection J. Bacteriol. 2017 199 e00437-17 10.1128/JB.00437-17 28924031 PMC5686607 · DOI
  39. [40]Zhang L. Wüst A. Prasser B. Müller C. Einsle O. Functional assembly of nitrous oxide reductase provides insights into copper site maturation Proc. Natl. Acad. Sci. USA 2019 116 12822 12827 10.1073/pnas.1903819116 31189605 PMC6601269 · DOI
  40. [41]Buffoni F. Ignesti G. The copper-containing amine oxidases: Biochemical aspects and functional role Mol. Genet. Metab. 2000 71 559 564 10.1006/mgme.2000.3098 11136547 · DOI
  41. [42]Hermann B. Kern M. La Pietra L. Simon J. Einsle O. The octahaem MccA is a haem c-copper sulfite reductase Nature 2015 520 706 709 10.1038/nature14109 25642962 · DOI
  42. [43]Kanteev M. Goldfeder M. Fishman A. Structure-function correlations in tyrosinases Protein Sci. Publ. Protein Soc. 2015 24 1360 1369 10.1002/pro.2734 26104241 PMC4570531 · DOI
  43. [44]McGuirl M.A. Bollinger J.A. Cosper N. Scott R.A. Dooley D.M. Expression, purification, and characterization of NosL, a novel Cu(I) protein of the nitrous oxide reductase (nos) gene cluster J. Biol. Inorg. Chem. JBIC Publ. Soc. Biol. Inorg. Chem. 2001 6 189 195 10.1007/s007750000190 11293413 · DOI
  44. [45]Bennett S.P. Soriano-Laguna M.J. Bradley J.M. Svistunenko D.A. Richardson D.J. Gates A.J. Le Brun N.E. NosL is a dedicated copper chaperone for assembly of the Cu(Z) center of nitrous oxide reductase Chem. Sci. 2019 10 4985 4993 10.1039/C9SC01053J 31183047 PMC6530538 · DOI
  45. [46]Lohmeyer E. Schröder S. Pawlik G. Trasnea P.-I. Peters A. Daldal F. Koch H.-G. The ScoI homologue SenC is a copper binding protein that interacts directly with the cbb3-type cytochrome oxidase in Rhodobacter capsulatus Biochim. Biophys. Acta 2012 1817 2005 2015 10.1016/j.bbabio.2012.06.621 22771512 PMC3432722 · DOI
  46. [47]Trasnea P.I. Andrei A. Marckmann D. Utz M. Khalfaoui-Hassani B. Selamoglu N. Daldal F. Koch H.G. A Copper Relay System Involving Two Periplasmic Chaperones Drives cbb3-Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus ACS Chem. Biol. 2018 13 1388 1396 10.1021/acschembio.8b00293 29613755 PMC5959785 · DOI
  47. [48]Serventi F. Youard Z.A. Murset V. Huwiler S. Buhler D. Richter M. Luchsinger R. Fischer H.M. Brogioli R. Niederer M. Copper starvation-inducible protein for cytochrome oxidase biogenesis in Bradyrhizobium japonicum J. Biol. Chem. 2012 287 38812 38823 10.1074/jbc.M112.406173 23012364 PMC3493923 · DOI
  48. [49]Canonica F. Hennecke H. Glockshuber R. Biochemical pathway for the biosynthesis of the Cu(A) center in bacterial cytochrome c oxidase FEBS Lett. 2019 593 2977 2989 10.1002/1873-3468.13587 31449676 · DOI
  49. [50]Abicht H.K. Scharer M.A. Quade N. Ledermann R. Mohorko E. Capitani G. Hennecke H. Glockshuber R. How periplasmic thioredoxin TlpA reduces bacterial copper chaperone ScoI and cytochrome oxidase subunit II (CoxB) prior to metallation J. Biol. Chem. 2014 289 32431 32444 10.1074/jbc.M114.607127 25274631 PMC4239598 · DOI
  50. [51]Banci L. Bertini I. Ciofi-Baffoni S. Katsari E. Katsaros N. Kubicek K. Mangani S. A copper(I) protein possibly involved in the assembly of CuA center of bacterial cytochrome c oxidase Proc. Natl. Acad. Sci. USA 2005 102 3994 3999 10.1073/pnas.0406150102 15753304 PMC554794 · DOI
  51. [52]Trasnea P.-I. Utz M. Khalfaoui-Hassani B. Lagies S. Daldal F. Koch H.-G. Cooperation between two periplasmic copper chaperones is required for full activity of the cbb3-type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus Mol. Microbiol. 2016 100 345 361 10.1111/mmi.13321 26718481 PMC4878679 · DOI
  52. [53]Thompson A.K. Gray J. Liu A. Hosler J.P. The roles of Rhodobacter sphaeroides copper chaperones PCu(A)C and Sco (PrrC) in the assembly of the copper centers of the aa(3)-type and the cbb(3)-type cytochrome c oxidases Biochim. Biophys. Acta 2012 1817 955 964 10.1016/j.bbabio.2012.01.003 22248670 PMC3336013 · DOI
  53. [54]Rubino J.T. Franz K.J. Coordination chemistry of copper proteins: How nature handles a toxic cargo for essential function J. Inorg. Biochem. 2012 107 129 143 10.1016/j.jinorgbio.2011.11.024 22204943 · DOI
  54. [55]Arguello J.M. Gonzalez-Guerrero M. Raimunda D. Bacterial transition metal P(1B)-ATPases: Transport mechanism and roles in virulence Biochemistry 2011 50 9940 9949 10.1021/bi201418k 21999638 PMC3224801 · DOI
  55. [56]Mattle D. Zhang L. Sitsel O. Pedersen L.T. Moncelli M.R. Tadini-Buoninsegni F. Gourdon P. Rees D.C. Nissen P. Meloni G. A sulfur-based transport pathway in Cu+-ATPases EMBO Rep. 2015 16 728 740 10.15252/embr.201439927 25956886 PMC4467857 · DOI
  56. [57]Gourdon P. Liu X.Y. Skjorringe T. Morth J.P. Moller L.B. Pedersen B.P. Nissen P. Crystal structure of a copper-transporting PIB-type ATPase Nature 2011 475 59 64 10.1038/nature10191 21716286 · DOI
  57. [58]Osman D. Cavet J.S. Copper homeostasis in bacteria Adv. Appl. Microbiol. 2008 65 217 247 10.1016/s0065-2164(08)00608-4 19026867 · DOI
  58. [59]Schweigel-Röntgen M. The families of zinc (SLC30 and SLC39) and copper (SLC31) transporters Curr. Top. Membr. 2014 73 321 355 10.1016/b978-0-12-800223-0.00009-8 24745988 · DOI
  59. [60]Dancis A. Yuan D.S. Haile D. Askwith C. Eide D. Moehle C. Kaplan J. Klausner R.D. Molecular characterization of a copper transport protein in S. cerevisiae: An unexpected role for copper in iron transport Cell 1994 76 393 402 10.1016/0092-8674(94)90345-X 8293472 · DOI · Paper page
  60. [61]Öhrvik H. Thiele D.J. The role of Ctr1 and Ctr2 in mammalian copper homeostasis and platinum-based chemotherapy J. Trace Elem. Med. Biol. 2015 31 178 182 10.1016/j.jtemb.2014.03.006 24703712 PMC4175275 · DOI
  61. [62]Petris M.J. The SLC31 (Ctr) copper transporter family Pflügers Arch. 2004 447 752 755 10.1007/s00424-003-1092-1 12827356 · DOI
  62. [63]Ren F. Logeman B.L. Zhang X. Liu Y. Thiele D.J. Yuan P. X-ray structures of the high-affinity copper transporter Ctr1 Nat. Commun. 2019 10 1386 10.1038/s41467-019-09376-7 30918258 PMC6437178 · DOI
  63. [64]Dyla M. Kjærgaard M. Poulsen H. Nissen P. Structure and Mechanism of P-Type ATPase Ion Pumps Annu. Rev. Biochem. 2020 89 583 603 10.1146/annurev-biochem-010611-112801 31874046 · DOI
  64. [65]Kanamaru K. Kashiwagi S. Mizuno T. A copper-transporting P-type ATPase found in the thylakoid membrane of the cyanobacterium Synechococcus species PCC7942 Mol. Microbiol. 1994 13 369 377 10.1111/j.1365-2958.1994.tb00430.x 7984114 · DOI
  65. [66]Tottey S. Rich P.R. Rondet S.A.M. Robinson N.J. Two Menkes-type ATPases Supply Copper for Photosynthesis inSynechocystis PCC 6803 J. Biol. Chem. 2001 276 19999 20004 10.1074/jbc.M011243200 11264284 · DOI
  66. [67]Solioz M. Chapter 11—Copper Disposition in Bacteria Clinical and Translational Perspectives on WILSON DISEASE Kerkar N. Roberts E.A. Academic Press Cambridge, MA, USA 2019 101 113
  67. [68]Solioz M. Stoyanov J.V. Copper homeostasis in Enterococcus hirae FEMS Microbiol. Rev. 2003 27 183 195 10.1016/S0168-6445(03)00053-6 12829267 · DOI
  68. [69]Badarau A. Dennison C. Thermodynamics of copper and zinc distribution in the cyanobacterium Synechocystis PCC 6803 Proc. Natl. Acad. Sci. USA 2011 108 13007 13012 10.1073/pnas.1101448108 21778408 PMC3156197 · DOI
  69. [70]Raimunda D. Gonzalez-Guerrero M. Leeber B.W. 3rd Arguello J.M. The transport mechanism of bacterial Cu+-ATPases: Distinct efflux rates adapted to different function Biometals 2011 24 467 475 10.1007/s10534-010-9404-3 21210186 PMC3092005 · DOI
  70. [71]Robinson N.J. Winge D.R. Copper metallochaperones Annu. Rev. Biochem. 2010 79 537 562 10.1146/annurev-biochem-030409-143539 20205585 PMC3986808 · DOI
  71. [72]Teitzel G.M. Geddie A. De Long S.K. Kirisits M.J. Whiteley M. Parsek M.R. Survival and Growth in the Presence of Elevated Copper: Transcriptional Profiling of Copper-Stressed Pseudomonas aeruginosa J. Bacteriol. 2006 188 7242 10.1128/JB.00837-06 17015663 PMC1636237 · DOI
  72. [73]Almárcegui R.J. Navarro C.A. Paradela A. Albar J.P. von Bernath D. Jerez C.A. New Copper Resistance Determinants in the Extremophile Acidithiobacillus ferrooxidans: A Quantitative Proteomic Analysis J. Proteome Res. 2014 13 946 960 10.1021/pr4009833 24380576 · DOI
  73. [74]Selamoglu N. Önder Ö. Öztürk Y. Khalfaoui-Hassani B. Blaby-Haas C.E. Garcia B.A. Koch H.-G. Daldal F. Comparative differential cuproproteomes of Rhodobacter capsulatus reveal novel copper homeostasis related proteins Metallomics 2020 12 572 591 10.1039/C9MT00314B 32149296 PMC7192791 · DOI
  74. [75]Lutkenhaus J.F. Role of a major outer membrane protein in Escherichia coli J. Bacteriol. 1977 131 631 637 10.1128/JB.131.2.631-637.1977 328491 PMC235472 · DOI
  75. [76]Li X.Z. Nikaido H. Williams K.E. Silver-resistant mutants of Escherichia coli display active efflux of Ag+ and are deficient in porins J. Bacteriol. 1997 179 6127 6132 10.1128/JB.179.19.6127-6132.1997 9324262 PMC179518 · DOI
  76. [77]Niederweis M. Danilchanka O. Huff J. Hoffmann C. Engelhardt H. Mycobacterial outer membranes: In search of proteins Trends Microbiol. 2010 18 109 116 10.1016/j.tim.2009.12.005 20060722 PMC2931330 · DOI
  77. [78]Alderwick L.J. Harrison J. Lloyd G.S. Birch H.L. The Mycobacterial Cell Wall—Peptidoglycan and Arabinogalactan Cold Spring Harbor Perspect. Med. 2015 5 a021113 10.1101/cshperspect.a021113 PMC4526729 25818664 · DOI
  78. [79]Speer A. Rowland J.L. Haeili M. Niederweis M. Wolschendorf F. Porins Increase Copper Susceptibility of Mycobacterium tuberculosis J. Bacteriol. 2013 195 5133 10.1128/JB.00763-13 24013632 PMC3811576 · DOI
  79. [80]Faller M. Niederweis M. Schulz G.E. The Structure of a Mycobacterial Outer-Membrane Channel Science 2004 303 1189 10.1126/science.1094114 14976314 · DOI
  80. [81]Niederweis M. Ehrt S. Heinz C. Klöcker U. Karosi S. Swiderek K.M. Riley L.W. Benz R. Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis Mol. Microbiol. 1999 33 933 945 10.1046/j.1365-2958.1999.01472.x 10476028 · DOI
  81. [82]Shah S. Dalecki A.G. Malalasekera A.P. Crawford C.L. Michalek S.M. Kutsch O. Sun J. Bossmann S.H. Wolschendorf F. 8-Hydroxyquinolines Are Boosting Agents of Copper-Related Toxicity in Mycobacterium tuberculosis Antimicrob. Agents Chemother. 2016 60 5765 10.1128/AAC.00325-16 27431227 PMC5038248 · DOI
  82. [83]Carreira C. Pauleta S.R. Moura I. The catalytic cycle of nitrous oxide reductase—The enzyme that catalyzes the last step of denitrification J. Inorg. Biochem. 2017 177 423 434 10.1016/j.jinorgbio.2017.09.007 28927704 · DOI
  83. [84]Pomowski A. Zumft W.G. Kroneck P.M.H. Einsle O. N2O binding at a [4Cu:2S] copper–sulphur cluster in nitrous oxide reductase Nature 2011 477 234 237 10.1038/nature10332 21841804 · DOI
  84. [85]Mokhele K. Tang Y.J. Clark M.A. Ingraham J.L. A Pseudomonas stutzeri outer membrane protein inserts copper into N2O reductase J. Bacteriol. 1987 169 5721 10.1128/JB.169.12.5721-5726.1987 3680176 PMC214080 · DOI
  85. [86]Lee H.S. Abdelal A.H. Clark M.A. Ingraham J.L. Molecular characterization of nosA, a Pseudomonas stutzeri gene encoding an outer membrane protein required to make copper-containing N2O reductase J. Bacteriol. 1991 173 5406 10.1128/JB.173.17.5406-5413.1991 1885521 PMC208252 · DOI
  86. [87]Schalk I.J. Mislin G.L. Brillet K. Structure, function and binding selectivity and stereoselectivity of siderophore-iron outer membrane transporters Curr. Top. Membr. 2012 69 37 66 10.1016/b978-0-12-394390-3.00002-1 23046646 · DOI
  87. [88]Schalk I.J. Hannauer M. Braud A. New roles for bacterial siderophores in metal transport and tolerance Environ. Microbiol. 2011 13 2844 2854 10.1111/j.1462-2920.2011.02556.x 21883800 · DOI
  88. [89]Schalk I.J. Cunrath O. An overview of the biological metal uptake pathways in Pseudomonas aeruginosa Environ. Microbiol. 2016 18 3227 3246 10.1111/1462-2920.13525 27632589 · DOI
  89. [90]Rechnitzer H. Brzuszkiewicz E. Strittmatter A. Liesegang H. Lysnyansky I. Daniel R. Gottschalk G. Rottem S. Genomic features and insights into the biology of Mycoplasma fermentans Microbiology 2011 157 760 773 10.1099/mic.0.043208-0 21109561 · DOI
  90. [91]Lee H.S. Hancock R.E. Ingraham J.L. Properties of a Pseudomonas stutzeri outer membrane channel-forming protein (NosA) required for production of copper-containing N2O reductase J. Bacteriol. 1989 171 2096 10.1128/JB.171.4.2096-2100.1989 2467899 PMC209862 · DOI
  91. [92]Wunsch P. Herb M. Wieland H. Schiek U.M. Zumft W.G. Requirements for CuA and Cu-S Center Assembly of Nitrous Oxide Reductase Deduced from Complete Periplasmic Enzyme Maturation in the Nondenitrifier Pseudomonas putida J. Bacteriol. 2003 185 887 10.1128/JB.185.3.887-896.2003 12533464 PMC142834 · DOI
  92. [93]Chillappagari S. Miethke M. Trip H. Kuipers O.P. Marahiel M.A. Copper acquisition is mediated by YcnJ and regulated by YcnK and CsoR in Bacillus subtilis J. Bacteriol. 2009 191 2362 2370 10.1128/JB.01616-08 19168619 PMC2655523 · DOI
  93. [94]Yoneyama H. Nakae T. Protein C (OprC) of the outer membrane of Pseudomonas aeruginosa is a copper-regulated channel protein Microbiology 1996 142 2137 2144 10.1099/13500872-142-8-2137 8760927 · DOI
  94. [95]Quintana J. Novoa-Aponte L. Argüello J.M. Copper homeostasis networks in the bacterium Pseudomonas aeruginosa J. Biol. Chem. 2017 292 15691 15704 10.1074/jbc.M117.804492 28760827 PMC5612103 · DOI
  95. [96]Han Y. Wang T. Chen G. Pu Q. Liu Q. Zhang Y. Xu L. Wu M. Liang H. A Pseudomonas aeruginosa type VI secretion system regulated by CueR facilitates copper acquisition PLoS Pathog. 2019 15 e1008198 10.1371/journal.ppat.1008198 31790504 PMC6907878 · DOI
  96. [97]Bhamidimarri S.P. Young T.R. Shanmugam M. Soderholm S. Belzunces B. Baslé A. Skylaris C. Bumann D. Khalid S. van den Berg B. Acquisition of ionic copper by a bacterial outer membrane protein bioRxiv 2020 10.1101/2020.06.04.134395 PMC8610252 34762655 · DOI
  97. [98]Mermod M. Magnani D. Solioz M. Stoyanov J.V. The copper-inducible ComR (YcfQ) repressor regulates expression of ComC (YcfR), which affects copper permeability of the outer membrane of Escherichia coli Biometals 2012 25 33 43 10.1007/s10534-011-9510-x 22089859 · DOI
  98. [99]Egler M. Grosse C. Grass G. Nies D.H. Role of the Extracytoplasmic Function Protein Family Sigma Factor RpoE in Metal Resistance of Escherichia coli J. Bacteriol. 2005 187 2297 10.1128/JB.187.7.2297-2307.2005 15774872 PMC1065229 · DOI
  99. [100]Liu W. Wang Y. Jing C. Transcriptome analysis of silver, palladium, and selenium stresses in Pantoea sp. IMH Chemosphere 2018 208 50 58 10.1016/j.chemosphere.2018.05.169 29860144 · DOI
  100. [101]Zheng M. Wang X. Templeton L.J. Smulski D.R. LaRossa R.A. Storz G. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide J. Bacteriol. 2001 183 4562 4570 10.1128/JB.183.15.4562-4570.2001 11443091 PMC95351 · DOI
  101. [102]Richmond C.S. Glasner J.D. Mau R. Jin H. Blattner F.R. Genome-wide expression profiling in Escherichia coli K-12 Nucleic Acids Res. 1999 27 3821 3835 10.1093/nar/27.19.3821 10481021 PMC148645 · DOI
  102. [103]Dennison C. David S. Lee J. Bacterial copper storage proteins J. Biol. Chem. 2018 293 4616 4627 10.1074/jbc.TM117.000180 29414794 PMC5880151 · DOI
  103. [104]Pittman M.S. Robinson H.C. Poole R.K. A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm J. Biol. Chem. 2005 280 32254 32261 10.1074/jbc.M503075200 16040611 · DOI
  104. [105]Padilla-Benavides T. George Thompson A.M. McEvoy M.M. Arguello J.M. Mechanism of ATPase-mediated Cu+ export and delivery to periplasmic chaperones: The interaction of Escherichia coli CopA and CusF J. Biol. Chem. 2014 289 20492 20501 10.1074/jbc.M114.577668 24917681 PMC4110264 · DOI
  105. [106]Dennison C. The Coordination Chemistry of Copper Uptake and Storage for Methane Oxidation Chemistry 2019 25 74 86 10.1002/chem.201803444 30281847 · DOI
  106. [107]Lee J. Dennison C. Cytosolic Copper Binding by a Bacterial Storage Protein and Interplay with Copper Efflux Int. J. Mol. Sci. 2019 20 4144 10.3390/ijms20174144 PMC6747150 31450649 · DOI
  107. [108]Quistgaard E.M. Löw C. Guettou F. Nordlund P. Understanding transport by the major facilitator superfamily (MFS): Structures pave the way Nat. Rev. Mol. Cell Biol. 2016 17 123 132 10.1038/nrm.2015.25 26758938 · DOI
  108. [109]Ekici S. Turkarslan S. Pawlik G. Dancis A. Baliga N.S. Koch H.-G. Daldal F. Intracytoplasmic copper homeostasis controls cytochrome c oxidase production mBio 2014 5 e01055-13 10.1128/mBio.01055-13 24425735 PMC3903287 · DOI
  109. [110]Khalfaoui-Hassani B. Wu H. Blaby-Haas C.E. Zhang Y. Sandri F. Verissimo A.F. Koch H.G. Daldal F. Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome c Oxidases mBio 2018 9 10.1128/mBio.00065-18 PMC5829832 29487231 · DOI
  110. [111]Beaudoin J. Ekici S. Daldal F. Ait-Mohand S. Guérin B. Labbé S. Copper transport and regulation in Schizosaccharomyces pombe Biochem. Soc. Trans. 2013 41 1679 1686 10.1042/BST2013089 24256274 PMC4871122 · DOI
  111. [112]Arguello J.M. Eren E. Gonzalez-Guerrero M. The structure and function of heavy metal transport P1B-ATPases Biometals 2007 20 233 248 10.1007/s10534-006-9055-6 17219055 · DOI
  112. [113]Khalfaoui-Hassani B. Verissimo A.F. Koch H.-G. Daldal F. Uncovering the Transmembrane Metal Binding Site of the Novel Bacterial Major Facilitator Superfamily-Type Copper Importer CcoA mBio 2016 7 10.1128/mBio.01981-15 26787831 PMC4725013 · DOI
  113. [114]Zhang Y. Blaby-Haas C.E. Steimle S. Verissimo A.F. Garcia-Angulo V.A. Koch H.-G. Daldal F. Khalfaoui-Hassani B. Cu Transport by the Extended Family of CcoA-like Transporters (CalT) in Proteobacteria Sci. Rep. 2019 9 1208 10.1038/s41598-018-37988-4 30718766 PMC6362234 · DOI
  114. [115]Gutiérrez-Preciado A. Torres A.G. Merino E. Bonomi H.R. Goldbaum F.A. García-Angulo V.A. Extensive Identification of Bacterial Riboflavin Transporters and Their Distribution across Bacterial Species PLoS ONE 2015 10 e0126124 10.1371/journal.pone.0126124 25938806 PMC4418817 · DOI
  115. [116]Vitreschak A.G. Rodionov D.A. Mironov A.A. Gelfand M.S. Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation Nucleic Acids Res. 2002 30 3141 3151 10.1093/nar/gkf433 12136096 PMC135753 · DOI
  116. [117]Kenney G.E. Rosenzweig A.C. Chalkophores Annu. Rev. Biochem. 2018 87 645 676 10.1146/annurev-biochem-062917-012300 29668305 PMC6013396 · DOI
  117. [118]Anttila J. Heinonen P. Nenonen T. Pino A. Iwaï H. Kauppi E. Soliymani R. Baumann M. Saksi J. Suni N. Is coproporphyrin III a copper-acquisition compound in Paracoccus denitrificans? Biochim. Biophys. Acta 2011 1807 311 318 10.1016/j.bbabio.2010.12.014 21216223 · DOI
  118. [119]Byers B.R. Powell M.V. Lankford C.E. Iron-chelating hydroxamic acid (schizokinen) active in initiation of cell division in Bacillus megaterium J. Bacteriol. 1967 93 286 294 10.1128/JB.93.1.286-294.1967 4960152 PMC315000 · DOI
  119. [120]Song L. Zhang Y. Chen W. Gu T. Zhang S.Y. Ji Q. Mechanistic insights into staphylopine-mediated metal acquisition Proc. Natl. Acad. Sci. USA 2018 115 3942 3947 10.1073/pnas.1718382115 29581261 PMC5899449 · DOI
  120. [121]Fitch M.W. Graham D.W. Arnold R.G. Agarwal S.K. Phelps P. Speitel G.E. Georgiou G. Phenotypic characterization of copper-resistant mutants of Methylosinus trichosporium OB3b Appl. Environ. Microbiol. 1993 59 2771 10.1128/AEM.59.9.2771-2776.1993 8215352 PMC182364 · DOI
  121. [122]Kenney G.E. Rosenzweig A.C. Methanobactins: Maintaining copper homeostasis in methanotrophs and beyond J. Biol. Chem. 2018 293 4606 4615 10.1074/jbc.TM117.000185 29348173 PMC5880147 · DOI
  122. [123]Kim H.J. Graham D.W. DiSpirito A.A. Alterman M.A. Galeva N. Larive C.K. Asunskis D. Sherwood P.M.A. Methanobactin, a Copper-Acquisition Compound from Methane-Oxidizing Bacteria Science 2004 305 1612 10.1126/science.1098322 15361623 · DOI
  123. [124]Behling L.A. Hartsel S.C. Lewis D.E. DiSpirito A.A. Choi D.W. Masterson L.R. Veglia G. Gallagher W.H. NMR, mass spectrometry and chemical evidence reveal a different chemical structure for methanobactin that contains oxazolone rings J. Am. Chem. Soc. 2008 130 12604 12605 10.1021/ja804747d 18729522 PMC3617554 · DOI
  124. [125]Krentz B.D. Mulheron H.J. Semrau J.D. DiSpirito A.A. Bandow N.L. Haft D.H. Vuilleumier S. Murrell J.C. McEllistrem M.T. Hartsel S.C. A Comparison of Methanobactins from Methylosinus trichosporium OB3b and Methylocystis Strain SB2 Predicts Methanobactins Are Synthesized from Diverse Peptide Precursors Modified To Create a Common Core for Binding and Reducing Copper Ions Biochemistry 2010 49 10117 10130 10.1021/bi1014375 20961038 PMC3924600 · DOI
  125. [126]El Ghazouani A. Baslé A. Gray J. Graham D.W. Firbank S.J. Dennison C. Variations in methanobactin structure influences copper utilization by methane-oxidizing bacteria Proc. Natl. Acad. Sci. USA 2012 109 8400 8404 10.1073/pnas.1112921109 22582172 PMC3365152 · DOI
  126. [127]El Ghazouani A. Baslé A. Firbank S.J. Knapp C.W. Gray J. Graham D.W. Dennison C. Copper-Binding Properties and Structures of Methanobactins from Methylosinus trichosporium OB3b Inorg. Chem. 2011 50 1378 1391 10.1021/ic101965j 21254756 · DOI
  127. [128]Hakemian A.S. Tinberg C.E. Kondapalli K.C. Telser J. Hoffman B.M. Stemmler T.L. Rosenzweig A.C. The Copper Chelator Methanobactin from Methylosinus trichosporium OB3b Binds Copper(I) J. Am. Chem. Soc. 2005 127 17142 17143 10.1021/ja0558140 16332035 PMC2864604 · DOI
  128. [129]Semrau J.D. Jagadevan S. DiSpirito A.A. Khalifa A. Scanlan J. Bergman B.H. Freemeier B.C. Baral B.S. Bandow N.L. Vorobev A. Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs Environ. Microbiol. 2013 15 3077 3086 10.1111/1462-2920.12150 23682956 · DOI
  129. [130]Kenney G.E. Rosenzweig A.C. Genome mining for methanobactins BMC Biol. 2013 11 17 10.1186/1741-7007-11-17 23442874 PMC3621798 · DOI
  130. [131]Dassama L.M.K. Kenney G.E. Rosenzweig A.C. Methanobactins: From genome to function Metallomics 2017 9 7 20 10.1039/C6MT00208K 27905614 PMC5269455 · DOI
  131. [132]Dassama L.M.K. Kenney G.E. Ro S.Y. Zielazinski E.L. Rosenzweig A.C. Methanobactin transport machinery Proc. Natl. Acad. Sci. USA 2016 113 13027 13032 10.1073/pnas.1603578113 27807137 PMC5135309 · DOI
  132. [133]Kuroda T. Tsuchiya T. Multidrug efflux transporters in the MATE family Biochim. Biophys. Acta Proteins Proteom. 2009 1794 763 768 10.1016/j.bbapap.2008.11.012 19100867 · DOI
  133. [134]He X. Szewczyk P. Karyakin A. Evin M. Hong W.-X. Zhang Q. Chang G. Structure of a cation-bound multidrug and toxic compound extrusion transporter Nature 2010 467 991 994 10.1038/nature09408 20861838 PMC3152480 · DOI
  134. [135]Balasubramanian R. Kenney G.E. Rosenzweig A.C. Dual pathways for copper uptake by methanotrophic bacteria J. Biol. Chem. 2011 286 37313 37319 10.1074/jbc.M111.284984 21900235 PMC3199478 · DOI
  135. [136]Gu W. Farhan Ul Haque M. Baral B.S. Turpin E.A. Bandow N.L. Kremmer E. Flatley A. Zischka H. DiSpirito A.A. Semrau J.D. A TonB-Dependent Transporter Is Responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b Appl. Environ. Microbiol. 2016 82 1917 10.1128/AEM.03884-15 26773085 PMC4784032 · DOI
  136. [137]Carniel E. The Yersinia high-pathogenicity island: An iron-uptake island Microbes Infect. 2001 3 561 569 10.1016/S1286-4579(01)01412-5 11418330 · DOI · Paper page
  137. [138]Perry R.D. Fetherston J.D. Yersiniabactin iron uptake: Mechanisms and role in Yersinia pestis pathogenesis Microbes Infect. 2011 13 808 817 10.1016/j.micinf.2011.04.008 21609780 PMC3148425 · DOI
  138. [139]Chaturvedi K.S. Hung C.S. Giblin D.E. Urushidani S. Austin A.M. Dinauer M.C. Henderson J.P. Cupric Yersiniabactin Is a Virulence-Associated Superoxide Dismutase Mimic ACS Chem. Biol. 2014 9 551 561 10.1021/cb400658k 24283977 PMC3934373 · DOI
  139. [140]Chaturvedi K.S. Hung C.S. Crowley J.R. Stapleton A.E. Henderson J.P. The siderophore yersiniabactin binds copper to protect pathogens during infection Nat. Chem. Biol. 2012 8 731 736 10.1038/nchembio.1020 22772152 PMC3600419 · DOI · Paper page
  140. [142]Koh E.-I. Robinson A.E. Bandara N. Rogers B.E. Henderson J.P. Copper import in Escherichia coli by the yersiniabactin metallophore system Nat. Chem. Biol. 2017 13 1016 1021 10.1038/nchembio.2441 28759019 PMC5562518 · DOI
  141. [143]Rakin A. Saken E. Harmsen D. Heesemann J. The pesticin receptor of Yersinia enterocolitica: A novel virulence factor with dual function Mol. Microbiol. 1994 13 253 263 10.1111/j.1365-2958.1994.tb00420.x 7984105 · DOI
  142. [144]Schubert S. Rakin A. Heesemann J. The Yersinia high-pathogenicity island (HPI): Evolutionary and functional aspects Int. J. Med. Microbiol. 2004 294 83 94 10.1016/j.ijmm.2004.06.026 15493818 · DOI · Paper page
  143. [145]Boal A.K. Rosenzweig A.C. Structural biology of copper trafficking Chem. Rev. 2009 109 4760 4779 10.1021/cr900104z 19824702 PMC2768115 · DOI
  144. [146]Aliaga M.E. Lopez-Alarcon C. Bridi R. Speisky H. Redox-implications associated with the formation of complexes between copper ions and reduced or oxidized glutathione J. Inorg. Biochem. 2016 154 78 88 10.1016/j.jinorgbio.2015.08.005 26277412 · DOI
  145. [147]Hatori Y. Inouye S. Akagi R. Thiol-based copper handling by the copper chaperone Atox1 IUBMB Life 2017 69 246 254 10.1002/iub.1620 28294521 · DOI
  146. [148]Kosman D.J. The teleos of metallo-reduction and metallo-oxidation in eukaryotic iron and copper trafficking Metallomics 2018 10 370 377 10.1039/C8MT00015H 29484341 PMC5864563 · DOI
  147. [149]Matson D.M. Ariöz C. Wittung-Stafshede P. Extended functional repertoire for human copper chaperones Biomol. Concepts 2016 7 29 39 10.1515/bmc-2015-0030 26745464 · DOI
  148. [151]Knutson M.D. Steap proteins: Implications for iron and copper metabolism Nutr. Rev. 2007 65 335 340 17695374
  149. [152]Ohgami R.S. Campagna D.R. McDonald A. Fleming M.D. The Steap proteins are metalloreductases Blood 2006 108 1388 1394 10.1182/blood-2006-02-003681 16609065 PMC1785011 · DOI · Paper page
  150. [153]Wyman S. Simpson R.J. McKie A.T. Sharp P.A. Dcytb (Cybrd1) functions as both a ferric and a cupric reductase in vitro FEBS Lett. 2008 582 1901 1906 10.1016/j.febslet.2008.05.010 18498772 · DOI
  151. [154]Zhang X. Krause K.H. Xenarios I. Soldati T. Boeckmann B. Evolution of the ferric reductase domain (FRD) superfamily: Modularity, functional diversification, and signature motifs PLoS ONE 2013 8 e58126 10.1371/journal.pone.0058126 23505460 PMC3591440 · DOI
  152. [155]Attar N. Campos O.A. Vogelauer M. Cheng C. Xue Y. Schmollinger S. Salwinski L. Mallipeddi N.V. Boone B.A. Yen L. The histone H3-H4 tetramer is a copper reductase enzyme Science 2020 369 59 64 10.1126/science.aba8740 32631887 PMC7842201 · DOI
  153. [156]Rudolph J. Luger K. The secret life of histones Science 2020 369 33 10.1126/science.abc8242 32631882 · DOI
  154. [157]Marckmann D. Trasnea P.I. Schimpf J. Winterstein C. Andrei A. Schmollinger S. Blaby-Haas C.E. Friedrich T. Daldal F. Koch H.G. The cbb 3-type cytochrome oxidase assembly factor CcoG is a widely distributed cupric reductase Proc. Natl. Acad. Sci. USA 2019 116 21166 21175 10.1073/pnas.1913803116 31570589 PMC6800367 · DOI
  155. [158]Helbig K. Bleuel C. Krauss G.J. Nies D.H. Glutathione and transition-metal homeostasis in Escherichia coli J. Bacteriol. 2008 190 5431 5438 10.1128/JB.00271-08 18539744 PMC2493246 · DOI
  156. [159]Pawlik G. Kulajta C. Sachelaru I. Schroder S. Waidner B. Hellwig P. Daldal F. Koch H.G. The putative assembly factor CcoH is stably associated with the cbb3-type cytochrome oxidase J. Bacteriol. 2010 192 6378 6389 10.1128/JB.00988-10 20952576 PMC3008534 · DOI
  157. [160]Preisig O. Zufferey R. Hennecke H. The Bradyrhizobium japonicum fixGHIS genes are required for the formation of the high-affinity cbb3-type cytochrome oxidase Arch. Microbiol. 1996 165 297 305 10.1007/s002030050330 8661920 · DOI
  158. [161]Koch H.G. Hwang O. Daldal F. Isolation and characterization of Rhodobacter capsulatus mutants affected in cytochrome cbb3 oxidase activity J. Bacteriol. 1998 180 969 978 10.1128/JB.180.4.969-978.1998 9473054 PMC106979 · DOI
  159. [162]Volentini S.I. Farias R.N. Rodriguez-Montelongo L. Rapisarda V.A. Cu(II)-reduction by Escherichia coli cells is dependent on respiratory chain components Biometals 2011 24 827 835 10.1007/s10534-011-9436-3 21390523 · DOI
  160. [163]Abicht H.K. Gonskikh Y. Gerber S.D. Solioz M. Non-enzymic copper reduction by menaquinone enhances copper toxicity in Lactococcus lactis IL1403 Microbiology 2013 159 1190 1197 10.1099/mic.0.066928-0 23579688 · DOI
  161. [164]Andreazza R. Okeke B.C. Pieniz S. Brandelli A. Lambais M.R. Camargo F.A.O. Bioreduction of Cu(II) by Cell-Free Copper Reductase from a Copper Resistant Pseudomonas sp. NA Biol. Trace Elem. Res. 2011 143 1182 1192 10.1007/s12011-010-8899-3 21104339 · DOI
  162. [165]Neubert M.J. Dahlmann E.A. Ambrose A. Johnson M.D.L. Copper Chaperone CupA and Zinc Control CopY Regulation of the Pneumococcal cop Operon mSphere 2017 2 10.1128/mSphere.00372-17 29062896 PMC5646241 · DOI
  163. [166]Fu Y. Bruce K.E. Wu H. Giedroc D.P. The S2 Cu(i) site in CupA from Streptococcus pneumoniae is required for cellular copper resistance Metallomics 2016 8 61 70 10.1039/C5MT00221D 26346139 PMC4720546 · DOI
  164. [167]Sazinsky M.H. LeMoine B. Orofino M. Davydov R. Bencze K.Z. Stemmler T.L. Hoffman B.M. Arguello J.M. Rosenzweig A.C. Characterization and structure of a Zn2+ and [2Fe-2S]-containing copper chaperone from Archaeoglobus fulgidus J. Biol. Chem. 2007 282 25950 25959 10.1074/jbc.M703311200 17609202 PMC2859431 · DOI
  165. [168]Palumaa P. Copper chaperones. The concept of conformational control in the metabolism of copper FEBS Lett. 2013 587 1902 1910 10.1016/j.febslet.2013.05.019 23684646 · DOI
  166. [169]Banci L. Bertini I. Ciofi-Baffoni S. Kozyreva T. Zovo K. Palumaa P. Affinity gradients drive copper to cellular destinations Nature 2010 465 645 648 10.1038/nature09018 20463663 · DOI
  167. [170]Odermatt A. Solioz M. Two trans-acting metalloregulatory proteins controlling expression of the copper-ATPases of Enterococcus hirae J. Biol. Chem. 1995 270 4349 4354 10.1074/jbc.270.9.4349 7876197 · DOI
  168. [171]Wimmer R. Herrmann T. Solioz M. Wuthrich K. NMR structure and metal interactions of the CopZ copper chaperone J. Biol. Chem. 1999 274 22597 22603 10.1074/jbc.274.32.22597 10428839 · DOI
  169. [172]Utz M. Andrei A. Milanov M. Trasnea P.I. Marckmann D. Daldal F. Koch H.G. The Cu chaperone CopZ is required for Cu homeostasis in Rhodobacter capsulatus and influences cytochrome cbb3 oxidase assembly Mol. Microbiol. 2019 111 764 783 10.1111/mmi.14190 30582886 PMC6417943 · DOI
  170. [173]Lu Z.H. Dameron C.T. Solioz M. The Enterococcus hirae paradigm of copper homeostasis: Copper chaperone turnover, interactions, and transactions Biometals 2003 16 137 143 12572673
  171. [174]Peuser V. Glaeser J. Klug G. The RSP_2889 gene product of Rhodobacter sphaeroides is a CueR homologue controlling copper-responsive genes Microbiology 2011 157 3306 3313 10.1099/mic.0.051607-0 21903751 · DOI
  172. [175]Drees S.L. Klinkert B. Helling S. Beyer D.F. Marcus K. Narberhaus F. Lubben M. One gene, two proteins: Coordinated production of a copper chaperone by differential transcript formation and translational frameshifting in Escherichia coli Mol. Microbiol. 2017 106 635 645 10.1111/mmi.13841 28925527 · DOI
  173. [176]Meydan S. Klepacki D. Karthikeyan S. Margus T. Thomas P. Jones J.E. Khan Y. Briggs J. Dinman J.D. Vázquez-Laslop N. Programmed Ribosomal Frameshifting Generates a Copper Transporter and a Copper Chaperone from the Same Gene Mol. Cell 2017 65 207 219 10.1016/j.molcel.2016.12.008 28107647 PMC5270581 · DOI
  174. [177]Kay K.L. Zhou L. Tenori L. Bradley J.M. Singleton C. Kihlken M.A. Ciofi-Baffoni S. Le Brun N.E. Kinetic analysis of copper transfer from a chaperone to its target protein mediated by complex formation Chem. Commun. 2017 53 1397 1400 10.1039/C6CC08966F 28078344 · DOI
  175. [178]Singleton C. Hearnshaw S. Zhou L. Le Brun N.E. Hemmings A.M. Mechanistic insights into Cu(I) cluster transfer between the chaperone CopZ and its cognate Cu(I)-transporting P-type ATPase, CopA Biochem. J. 2009 424 347 356 10.1042/BJ20091079 19751213 · DOI
  176. [179]Singleton C. Le Brun N.E. Atx1-like chaperones and their cognate P-type ATPases: Copper-binding and transfer Biometals 2007 20 275 289 10.1007/s10534-006-9068-1 17225061 · DOI
  177. [180]Gonzalez-Guerrero M. Arguello J.M. Mechanism of Cu+-transporting ATPases: Soluble Cu+ chaperones directly transfer Cu+ to transmembrane transport sites Proc. Natl. Acad. Sci. USA 2008 105 5992 5997 10.1073/pnas.0711446105 18417453 PMC2329688 · DOI
  178. [181]Kihlken M.A. Leech A.P. Le Brun N.E. Copper-mediated dimerization of CopZ, a predicted copper chaperone from Bacillus subtilis Biochem. J. 2002 368 729 739 10.1042/bj20021036 12238948 PMC1223043 · DOI
  179. [182]Hearnshaw S. West C. Singleton C. Zhou L. Kihlken M.A. Strange R.W. Le Brun N.E. Hemmings A.M. A tetranuclear Cu(I) cluster in the metallochaperone protein CopZ Biochemistry 2009 48 9324 9326 10.1021/bi9011995 19746989 · DOI
  180. [183]Kay K.L. Hamilton C.J. Le Brun N.E. Mass spectrometry of B. subtilis CopZ: Cu(i)-binding and interactions with bacillithiol Metallomics 2016 8 709 719 10.1039/C6MT00036C 27197762 · DOI
  181. [184]Carmel-Harel O. Storz G. Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and saccharomyces cerevisiae responses to oxidative stress Annu. Rev. Microbiol. 2000 54 439 461 10.1146/annurev.micro.54.1.439 11018134 · DOI
  182. [185]Novoa-Aponte L. Ramírez D. Argüello J.M. The interplay of the metallosensor CueR with two distinct CopZ chaperones defines copper homeostasis in Pseudomonas aeruginosa J. Biol. Chem. 2019 294 4934 4945 10.1074/jbc.RA118.006316 30718281 PMC6442026 · DOI
  183. [186]Fu Y. Tsui H.C. Bruce K.E. Sham L.T. Higgins K.A. Lisher J.P. Kazmierczak K.M. Maroney M.J. Dann C.E. 3rd Winkler M.E. A new structural paradigm in copper resistance in Streptococcus pneumoniae Nat. Chem. Biol. 2013 9 177 183 10.1038/nchembio.1168 23354287 PMC3578076 · DOI · Paper page
  184. [188]Davidi D. Longo L.M. Jabłońska J. Milo R. Tawfik D.S. A Bird’s-Eye View of Enzyme Evolution: Chemical, Physicochemical, and Physiological Considerations Chem. Rev. 2018 118 8786 8797 10.1021/acs.chemrev.8b00039 30133258 · DOI
  185. [189]Drees S.L. Beyer D.F. Lenders-Lomscher C. Lubben M. Distinct functions of serial metal-binding domains in the Escherichia coli P1B-ATPase CopA Mol. Microbiol. 2015 97 423 438 10.1111/mmi.13038 25899340 · DOI
  186. [190]Gonzalez-Guerrero M. Hong D. Arguello J.M. Chaperone-mediated Cu+ delivery to Cu+ transport ATPases: Requirement of nucleotide binding J. Biol. Chem. 2009 284 20804 20811 10.1074/jbc.M109.016329 19525226 PMC2742845 · DOI
  187. [191]Kittleson J.T. Loftin I.R. Hausrath A.C. Engelhardt K.P. Rensing C. McEvoy M.M. Periplasmic metal-resistance protein CusF exhibits high affinity and specificity for both CuI and AgI Biochemistry 2006 45 11096 11102 10.1021/bi0612622 16964970 · DOI
  188. [192]Vasák M. Advances in metallothionein structure and functions J. Trace Elem. Med. Biol. 2005 19 13 17 10.1016/j.jtemb.2005.03.003 16240666 · DOI
  189. [193]Calvo J. Jung H. Meloni G. Copper metallothioneins IUBMB Life 2017 69 236 245 10.1002/iub.1618 28296007 · DOI
  190. [194]Sato M. Bremner I. Oxygen free radicals and metallothionein Free Radic. Biol. Med. 1993 14 325 337 10.1016/0891-5849(93)90029-T 8458590 · DOI
  191. [195]Turner J.S. Robinson N.J. Cyanobacterial metallothioneins: Biochemistry and molecular genetics J. Ind. Microbiol. 1995 14 119 125 10.1007/BF01569893 7766203 · DOI
  192. [196]Blindauer C.A. Bacterial metallothioneins: Past, present, and questions for the future J. Biol. Inorg. Chem. 2011 16 1011 1024 10.1007/s00775-011-0790-y 21594652 · DOI
  193. [197]Ziller A. Fraissinet-Tachet L. Metallothionein diversity and distribution in the tree of life: A multifunctional protein Metallomics 2018 10 1549 1559 10.1039/C8MT00165K 30229264 · DOI
  194. [198]Olafson R.W. Abel K. Sim R.G. Prokaryotic metallothionein: Preliminary characterization of a blue-green alga heavy metal-binding protein Biochem. Biophys. Res. Commun. 1979 89 36 43 10.1016/0006-291X(79)90939-2 113007 · DOI
  195. [199]Blindauer C.A. Harrison M.D. Parkinson J.A. Robinson A.K. Cavet J.S. Robinson N.J. Sadler P.J. A metallothionein containing a zinc finger within a four-metal cluster protects a bacterium from zinc toxicity Proc. Natl. Acad. Sci. USA 2001 98 9593 9598 10.1073/pnas.171120098 11493688 PMC55497 · DOI
  196. [201]Vita N. Platsaki S. Baslé A. Allen S.J. Paterson N.G. Crombie A.T. Murrell J.C. Waldron K.J. Dennison C. A four-helix bundle stores copper for methane oxidation Nature 2015 525 140 143 10.1038/nature14854 26308900 PMC4561512 · DOI
  197. [202]DiSpirito A.A. Semrau J.D. Murrell J.C. Gallagher W.H. Dennison C. Vuilleumier S. Methanobactin and the Link between Copper and Bacterial Methane Oxidation Microbiol. Mol. Biol. Rev. 2016 80 387 409 10.1128/MMBR.00058-15 26984926 PMC4867365 · DOI
  198. [203]Trotsenko Y.A. Murrell J.C. Metabolic aspects of aerobic obligate methanotrophy Adv. Appl. Microbiol. 2008 63 183 229 10.1016/s0065-2164(07)00005-6 18395128 · DOI
  199. [204]Vita N. Landolfi G. Basle A. Platsaki S. Lee J. Waldron K.J. Dennison C. Bacterial cytosolic proteins with a high capacity for Cu(I) that protect against copper toxicity Sci. Rep. 2016 6 39065 10.1038/srep39065 27991525 PMC5171941 · DOI
  200. [205]Straw M.L. Chaplin A.K. Hough M.A. Paps J. Bavro V.N. Wilson M.T. Vijgenboom E. Worrall J.A.R. A cytosolic copper storage protein provides a second level of copper tolerance in Streptomyces lividans Metallomics 2018 10 180 193 10.1039/C7MT00299H 29292456 · DOI

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Cited by

Sorted by citations

Authors
Andrei, A., Öztürk, Y., Khalfaoui-Hassani, B., Rauch, J., Marckmann, D., Trasnea, P.-I., Daldal, F., & Koch, H.-G.
Affiliations
  • University of Freiburg (DE)
  • Centre National de la Recherche Scientifique (FR)
  • Institute of Science and Technology Austria (AT)
  • University of Pennsylvania (US)
Corresponding author
Koch, Hans-Georg
ORCID
Venue
Membranes
Publisher
MDPI AG
Published
2020-09-18
Volume
10
Issue
9
Pages
242
ISSN
2077-0375 (ISSN-L)
DOI
10.3390/membranes10090242
PMC
PMC7558416
OpenAlex
W3087451181
Cited by
153
References
8
Citations by year
2026: 24 · 2025: 36 · 2024: 32 · 2023: 20 · 2022: 23 · 2021: 18
FWCI
2.19
Type
journal article
Language
en
Open access
Licence
Locations
  • Membranes (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institute of Science and Technology Austria (submittedVersion, cc-by)
  • HAL (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
Funders
  • Deutsche Forschungsgemeinschaft (KO2184/8, KO2184/9, ID 4032222702/SFB1381, ID 235777276/GRK2202)
  • National Institutes of Health (GM38237)
  • U.S. Department of Energy (DE-FG02-91ER20052)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
  • Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
Keywords
copper homeostasis, copper uptake, copper storage, copper exports, copper enzymes, copper toxicity, Gram-negative bacteria, pathogenic microorganisms, host immune response

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