Competition for zinc binding in the host-pathogen interaction

Frontiers in Cellular and Infection Microbiology

Volumn 3, Issue DEC, 2013, Pages

  Cerasi, Mauro ^a   Ammendola, Serena ^a   Battistoni, Andrea ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

Author keywords

Antibacterial therapies; Host pathogen interaction; Metal cofactor; Nutritional immunity; Salmonella enterica; Zinc transporter; Zinc uptake; ZnuABC

Indexed keywords

BACTERIAL PROTEIN; CALGRANULIN; INTERLEUKIN 6; PROTEIN S 100; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RIBOSOME PROTEIN; ZINC ION; CARRIER PROTEIN; ZINC; ZINC TRANSPORTER;

BACTERIAL GROWTH; BACTERIAL VIRULENCE; BINDING AND RELATED PHENOMENA; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HUMAN; MINERAL METABOLISM; NONHUMAN; PATHOGENICITY; PROTEIN BINDING; RIBOSOME; SHORT SURVEY; ZINC BINDING; ZINC MOBILIZATION; ANTIBACTERIAL THERAPIES; BACTERIUM; HOST-PATHOGEN INTERACTION; METABOLISM; METAL COFACTOR; NUTRITIONAL IMMUNITY; REVIEW; SALMONELLA ENTERICA; ZINC UPTAKE; ZNUABC;

ANTIBACTERIAL THERAPIES; HOST-PATHOGEN INTERACTION; METAL COFACTOR; NUTRITIONAL IMMUNITY; SALMONELLA ENTERICA; ZINC TRANSPORTER; ZINC UPTAKE; ZNUABC;

BACTERIA; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; MEMBRANE TRANSPORT PROTEINS; ZINC;

EID: 84897918689     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00108     Document Type: Short Survey

References (95)

1. Ammendola, S., Pasquali, P., Pacello, F., Rotilio, G., Castor, M., Libby, S. J., et al. (2008). Regulatory and structural differences in the Cu,Zn-superoxide dismutases of Salmonella enterica and their significance for virulence. J. Biol. Chem. 283, 13688-13699. doi: 10.1074/jbc.M710499200.
2. Ammendola, S., Pasquali, P., Pistoia, C., Petrucci, P., Petrarca, P., Rotilio, G., et al. (2007). High-affinity Zn2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica. Infect. Immun. 75, 5867-5876. doi: 10.1128/IAI.00559-07.
3. Andreini, C., Banci, L., Bertini, I., and Rosato, A. (2006). Zinc through the three domains of life. J. Proteome Res. 5, 3173-3178. doi: 10.1021/pr0603699.
4. Andreini, C., Bertini, I., Cavallaro, G., Holliday, G. L., and Thornton, J. M. (2008). Metal ions in biological catalysis: from enzyme databases to general principles. J. Biol. Inorg. Chem. 13, 1205-1218. doi: 10.1007/s00775-008-0404-5.
5. Andrews, S. C., Robinson, A. K., and Rodríguez-Quiñones, F. (2003). Bacterial iron homeostasis. FEMS Microbiol. Rev. 27, 215-237. doi: 10.1016/S0168-6445(03)00055-X.
6. Banerjee, S., Wei, B., Bhattacharyya-Pakrasi, M., Pakrasi, H. B., and Smith, T. J. (2003). Structural determinants of metal specificity in the zinc transport protein ZnuA from synechocystis 6803. J. Mol. Biol. 333, 1061-1069. doi: 10.1016/j.jmb.2003.09.008.
7. Beard, S. J., Hashim, R., Membrillo-Hernandez, J., Hughes, M. N., and Poole, R. K. (1997). Zinc(II) tolerance in Escherichia coli K-12: evidence that the zntA gene (o732) encodes a cation transport ATPase. Mol. Microbiol. 25, 883-891. doi: 10.1111/j.1365-2958.1997.mmi518.x.
8. Berducci, G., Mazzetti, A. P., Rotilio, G., and Battistoni, A. (2004). Periplasmic competition for zinc uptake between the metallochaperone ZnuA and Cu, Zn superoxide dismutase. FEBS Lett. 569, 289-292. doi: 10.1016/j.febslet.2004.06.008.
9. Blaby-Haas, C. E., Furman, R., Rodionov, D. A., Artsimovitch, I., and De Crécy-Lagard, V. (2011). Role of a Zn-independent DksA in Zn homeostasis and stringent response. Mol. Microbiol. 79, 700-715. doi: 10.1111/j.1365-2958.2010.07475.x.
10. Blindauer, C. A., Harrison, M. D., Robinson, A. K., Parkinson, J. A., Bowness, P. W., Sadler, P. J., et al. (2002). Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Mol. Microbiol. 45, 1421-1432. doi: 10.1046/j.1365-2958.2002.03109.x.
11. Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., et al. (2011). Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10, 248-259. doi: 10.1016/j.chom.2011.08.006.
12. Brunjes Brophy, M., Nakashige, T. G., Gaillard, A., and Nolan, E. M. (2013). Contributions of the S100A9 C-terminal tail to high-affinity Mn(II) chelation by the host-defense protein human calprotectin. J. Am. Chem. Soc. 135, 17804-17817. doi: 10.1021/ja407147d.
13. Campbell, E. A., Greenwell, R., Anthony, J. R., Wang, S., Lim, L., Das, K., et al. (2007). A conserved structural module regulates transcriptional responses to diverse stress signals in bacteria. Mol. Cell 27, 793-805. doi: 10.1016/j.molcel.2007.07.009.
14. Campoy, S., Jara, M., Busquets, N., Perez De Rozas, A. M., Badiola, I., and Barbe, J. (2002). Role of the high-affinity zinc uptake znuABC system in Salmonella enterica serovar typhimurium virulence. Infect. Immun. 70, 4721-4725. doi: 10.1128/IAI.70.8.4721-4725.2002.
15. Castelli, S., Stella, L., Petrarca, P., Battistoni, A., Desideri, A., and Falconi, M. (2013). Zinc ion coordination as a modulating factor of the ZnuA histidine-rich loop flexibility: a molecular modeling and fluorescence spectroscopy study. Biochem. Biophys. Res. Commun. 430, 769-773. doi: 10.1016/j.bbrc.2012.11.073.
16. Chandra, B. R., Yogavel, M., and Sharma, A. (2007). Structural analysis of ABC-family periplasmic zinc binding protein provides new insights into mechanism of ligand uptake and release. J. Mol. Biol. 367, 970-982. doi: 10.1016/j.jmb.2007.01.041.
17. Chivers, P. T. (2007). A galvanizing story-protein stability and zinc homeostasis. J. Bacteriol. 189, 2953-2954. doi: 10.1128/JB.00173-07.
18. Clapp, B., Skyberg, J. A., Yang, X., Thornburg, T., Walters, N., and Pascual, D. W. (2011). Protective live oral brucellosis vaccines stimulate Th1 and th17 cell responses. Infect. Immun. 79, 4165-4174. doi: 10.1128/IAI.05080-11.
19. Colvin, R. A., Holmes, W. R., Fontaine, C. P., and Maret, W. (2010). Cytosolic zinc buffering and muffling: their role in intracellular zinc homeostasis. Metallomics 2, 306-317. doi: 10.1039/b926662c.
20. Corbett, D., Wang, J., Schuler, S., Lopez-Castejon, G., Glenn, S., Brough, D., et al. (2012). Two zinc uptake systems contribute to the full virulence of Listeria monocytogenes during growth in vitro and in vivo. Infect. Immun. 80, 14-21. doi: 10.1128/IAI.05904-11.
21. Counago, R. M., McDevitt, C. A., Ween, M. P., and Kobe, B. (2012). Prokaryotic substrate-binding proteins as targets for antimicrobial therapies. Curr. Drug Targets 13, 1400-1410. doi: 10.2174/138945012803530170.
22. Counago, R. M., Ween, M. P., Begg, S. L., Bajaj, M., Zuegg, J., O'Mara, M. L., et al. (2013). Imperfect coordination chemistry facilitates metal ion release in the Psa permease. Nat. Chem. Biol.
23. Dahiya, I., and Stevenson, R. M. (2010). The ZnuABC operon is important for Yersinia ruckeri infections of rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 33, 331-340. doi: 10.1111/j.1365-2761.2009.01125.x.
24. Damo, S. M., Kehl-Fie, T. E., Sugitani, N., Holt, M. E., Rathi, S., Murphy, W. J., et al. (2013). Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 110, 3841-3846. doi: 10.1073/pnas.1220341110.
25. Davis, L. M., Kakuda, T., and Dirita, V. J. (2009). A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J. Bacteriol. 191, 1631-1640. doi: 10.1128/JB.01394-08.
26. Desrosiers, D. C., Bearden, S. W., Mier, I. Jr., Abney, J., Paulley, J. T., Fetherston, J. D., et al. (2010). Znu is the predominant zinc importer in Yersinia pestis during in vitro growth but is not essential for virulence. Infect. Immun. 78, 5163-5177. doi: 10.1128/IAI.00732-10.
27. Dintilhac, A., Alloing, G., Granadel, C., and Claverys, J. P. (1997). Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol. Microbiol. 25, 727-739. doi: 10.1046/j.1365-2958.1997.5111879.x.
28. Eide, D. J. (2006). Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 1763, 711-722. doi: 10.1016/j.bbamcr.2006.03.005.
29. Ellison, M. L., Farrow, J. M., Parrish, W., Danell, A. S., and Pesci, E. C. (2013). The Transcriptional regulator Np20 Is the Zinc uptake regulator in Pseudomonas aeruginosa. PLoS ONE 8:e75389. doi: 10.1371/journal.pone.0075389.
30. Gabbianelli, R., Scotti, R., Ammendola, S., Petrarca, P., Nicolini, L., and Battistoni, A. (2011). Role of ZnuABC and ZinT in Escherichia coli O157:H7 zinc acquisition and interaction with epithelial cells. BMC Microbiol. 11:36. doi: 10.1186/1471-2180-11-36.
31. Gabriel, S. E., and Helmann, J. D. (2009). Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions. J. Bacteriol. 191, 6116-6122. doi: 10.1128/JB.00802-09.
32. Garmory, H. S., and Titball, R. W. (2004). ATP-binding cassette transporters are targets for the development of antibacterial vaccines and therapies. Infect. Immun. 72, 6757-6763. doi: 10.1128/IAI.72.12.6757-6763.2004.
33. Garrido, M. E., Bosch, M., Medina, R., Llagostera, M., Perez De Rozas, A. M., Badiola, I., et al. (2003). The high-affinity zinc-uptake system znuACB is under control of the iron-uptake regulator (fur) gene in the animal pathogenPasteurella multocida. FEMS Microbiol. Lett. 221, 31-37. doi: 10.1016/S0378-1097(03)00131-9.
34. Gielda, L. M., and Dirita, V. J. (2012). Zinc competition among the intestinal microbiota. MBio 3, e00171-00112. doi: 10.1128/mBio.00171-12.
35. Glaser, R., Harder, J., Lange, H., Bartels, J., Christophers, E., and Schroder, J. M. (2005). Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat. Immunol. 6, 57-64. doi: 10.1038/ni1142.
36. Gradassi, M., Pesciaroli, M., Martinelli, N., Ruggeri, J., Petrucci, P., Hassan, W. H., et al. (2013). Attenuated Salmonella enterica serovar Typhimurium lacking the ZnuABC transporter: an efficacious orally-administered mucosal vaccine against salmonellosis in pigs. Vaccine 31, 3695-3701. doi: 10.1016/j.vaccine.2013.05.105.
37. Graham, A. I., Hunt, S., Stokes, S. L., Bramall, N., Bunch, J., Cox, A. G., et al. (2009). Severe zinc depletion of Escherichia coli: roles for high affinity zinc binding by ZinT, zinc transport and zinc-independent proteins. J. Biol. Chem. 284, 18377-18389. doi: 10.1074/jbc.M109.001503.
38. Grass, G., Franke, S., Taudte, N., Nies, D. H., Kucharski, L. M., Maguire, M. E., et al. (2005). The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J. Bacteriol. 187, 1604-1611. doi: 10.1128/JB.187.5.1604-1611.2005.
39. Grass, G., Wong, M. D., Rosen, B. P., Smith, R. L., and Rensing, C. (2002). ZupT is a Zn(II) uptake system in Escherichia coli. J. Bacteriol. 184, 864-866. doi: 10.1128/JB.184.3.864-866.2002.
40. Haas, C. E., Rodionov, D. A., Kropat, J., Malasarn, D., Merchant, S. S., and 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. doi: 10.1186/1471-2164-10-470.
41. Hantke, K. (2005). Bacterial zinc uptake and regulators. Curr. Opin. Microbiol. 8, 196-202. doi: 10.1016/j.mib.2005.02.001.
42. Hensley, M. P., Tierney, D. L., and Crowder, M. W. (2011). Zn(II) binding to Escherichia coli 70S ribosomes. Biochemistry 50, 9937-9939. doi: 10.1021/bi200619w.
43. Ho, T. D., Davis, B. M., Ritchie, J. M., and Waldor, M. K. (2008). Type 2 secretion promotes enterohemorrhagic Escherichia coli adherence and intestinal colonization. Infect. Immun. 76, 1858-1865. doi: 10.1128/IAI.01688-07.
44. Hood, M. I., Mortensen, B. L., Moore, J. L., Zhang, Y., Kehl-Fie, T. E., Sugitani, N., et al. (2012). Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog. 8:e1003068. doi: 10.1371/journal.ppat.1003068.
45. Hubert, K., Devos, N., Mordhorst, I., Tans, C., Baudoux, G., Feron, C., et al. (2013). ZnuD, a potential candidate for a simple and universal Neisseria meningitidis vaccine. Infect. Immun. 81, 1915-1927. doi: 10.1128/IAI.01312-12.
46. Ilari, A., Alaleona, F., Petrarca, P., Battistoni, A., and Chiancone, E. (2011). The X-ray structure of the zinc transporter ZnuA from Salmonella enterica discloses a unique triad of zinc-coordinating histidines. J. Mol. Biol. 409, 630-641. doi: 10.1016/j.jmb.2011.04.036.
47. Ilari, A., Alaleona, F., Tria, G., Petrarca, P., Battistoni, A., Zamparelli, C., et al. (2013). The Salmonella enterica ZinT structure, zinc affinity and interaction with the high-affinity uptake protein ZnuA provide insight into the management of periplasmic zinc. Biochim. Biophys. Acta 1840, 535-544. doi: 10.1016/j.bbagen.2013.10.010.
48. Irving, H., and Williams, R. J. P. (1948). Order of stability of metal complexes. Nature 162, 746-747. doi: 10.1038/162746a0.
49. Karlinsey, J. E., Maguire, M. E., Becker, L. A., Crouch, M. L., and Fang, F. C. (2010). The phage shock protein PspA facilitates divalent metal transport and is required for virulence of Salmonella enterica sv. Typhimurium. Mol. Microbiol. 78, 669-685. doi: 10.1111/j.1365-2958.2010.07357.x.
50. Katayama, A., Tsujii, A., Wada, A., Nishino, T., and Ishihama, A. (2002). Systematic search for zinc-binding proteins in Escherichia coli. Eur. J. Biochem. 269, 2403-2413. doi: 10.1046/j.1432-1033.2002.02900.x.
51. Kehl-Fie, T. E., and Skaar, E. P. (2010). Nutritional immunity beyond iron: a role for manganese and zinc. Curr. Opin. Chem. Biol. 14, 218-224. doi: 10.1016/j.cbpa.2009.11.008.
52. Kim, S., Watanabe, K., Shirahata, T., and Watarai, M. (2004). Zinc uptake system (znuA locus) of Brucella abortus is essential for intracellular survival and virulence in mice. J. Vet. Med. Sci. 66, 1059-1063. doi: 10.1292/jvms.66.1059.
53. Kropachev, K. Y., Zharkov, D. O., and Grollman, A. P. (2006). Catalytic mechanism of Escherichia coli endonuclease VIII: roles of the intercalation loop and the zinc finger. Biochemistry 45, 12039-12049. doi: 10.1021/bi060663e.
54. Kumar, P., Sannigrahi, S., and Tzeng, Y. L. (2012). The Neisseria meningitidis ZnuD zinc receptor contributes to interactions with epithelial cells and supports heme utilization when expressed in Escherichia coli. Infect. Immun. 80, 657-667. doi: 10.1128/IAI.05208-11.
55. Lewinson, O., Lee, A. T., and Rees, D. C. (2009). A P-type ATPase importer that discriminates between essential and toxic transition metals. Proc. Natl. Acad. Sci. U.S.A. 106, 4677-4682. doi: 10.1073/pnas.0900666106.
56. Lewis, D. A., Klesney-Tait, J., Lumbley, S. R., Ward, C. K., Latimer, J. L., Ison, C. A., et al. (1999). Identification of the znuA-encoded periplasmic zinc transport protein of Haemophilus ducreyi. Infect Immun 67, 5060-5068.
57. Li, Y., Qiu, Y., Gao, H., Guo, Z., Han, Y., Song, Y., et al. (2009). Characterization of Zur-dependent genes and direct Zur targets in Yersinia pestis. BMC Microbiol. 9:128. doi: 10.1186/1471-2180-9-128.
58. Lim, C. K., Hassan, K. A., Penesyan, A., Loper, J. E., and Paulsen, I. T. (2013). The effect of zinc limitation on the transcriptome of Pseudomonas protegens Pf-5. Environ. Microbiol. 15, 702-715. doi: 10.1111/j.1462-2920.2012.02849.x.
59. Liu, J. Z., Jellbauer, S., Poe, A. J., Ton, V., Pesciaroli, M., Kehl-Fie, T. E., et al. (2012). Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11, 227-239. doi: 10.1016/j.chom.2012.01.017.
60. Liuzzi, J. P. (2005). Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc. Natl. Acad. Sci. U.S.A. 102, 6843-6848. doi: 10.1073/pnas.0502257102.
61. Loisel, E., Chimalapati, S., Bougault, C., Imberty, A., Gallet, B., Di Guilmi, A. M., et al. (2011). Biochemical characterization of the histidine triad protein PhtD as a cell surface zinc-binding protein of pneumococcus. Biochemistry 50, 3551-3558. doi: 10.1021/bi200012f.
62. Lucarelli, D., Russo, S., Garman, E., Milano, A., Meyer-Klaucke, W., and Pohl, E. (2007). Crystal Structure and function of the zinc uptake regulator FurB from Mycobacterium tuberculosis. J. of Biol. Chem. 282, 9914-9922. doi: 10.1074/jbc.M609974200.
63. McDevitt, C. A., Ogunniyi, A. D., Valkov, E., Lawrence, M. C., Kobe, B., McEwan, A. G., et al. (2011). A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog. 7:e1002357. doi: 10.1371/journal.ppat.1002357.
64. Meini, M. R., Gonzalez, L. J., and Vila, A. J. (2013). Antibiotic resistance in Zn(II)-deficient environments: metallo-beta-lactamase activation in the periplasm. Future Microbiol. 8, 947-979. doi: 10.2217/fmb.13.34.
65. Miller, W. T., Hill, K.a.W., and Schimmel, P. (1991). Evidence for a "cysteine-histidine box" metal-binding site in an Escherichia coli aminoacyl-tRNA synthetase. Biochemistry 30, 6970-6976. doi: 10.1021/bi00242a023.
66. Murphy, T. F., Brauer, A. L., Kirkham, C., Johnson, A., Koszelak-Rosenblum, M., and Malkowski, M. G. (2013). Role of the zinc uptake ABC transporter of Moraxella catarrhalis in persistence in the respiratory tract. Infect. Immun. 81, 3406-3413. doi: 10.1128/IAI.00589-13.
67. Nielubowicz, G. R., Smith, S. N., and Mobley, H. L. (2010). Zinc uptake contributes to motility and provides a competitive advantage to Proteus mirabilis during experimental urinary tract infection. Infect. Immun. 78, 2823-2833. doi: 10.1128/IAI.01220-09.
68. Nikaido, H., and Vaara, M. (1985). Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49, 1-32.
69. Ortiz De Orue Lucana, D., Wedderhoff, I., and Groves, M. R. (2012). ROS-mediated signalling in bacteria: zinc-containing Cys-X-X-Cys redox centres and iron-based oxidative stress. J. Signal Transduct. 2012, 605905. doi: 10.1155/2012/605905.
70. Outten, C. E., and O'Halloran, T. V. (2001). Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292, 2488-2492. doi: 10.1126/science.1060331.
71. Outten, C. E., Tobin, D. A., Penner-Hahn, J. E., and O'Halloran, T. V. (2001). Characterization of the metal receptor sites in Escherichia coli Zur, an ultrasensitive zinc(II) metalloregulatory protein. Biochemistry 40, 10417-10423. doi: 10.1021/bi0155448.
72. Panina, E. M. (2003). Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc. Natl. Acad. Sci. U.S.A. 100, 9912-9917. doi: 10.1073/pnas.1733691100.
73. Panina, E. M., Mironov, A. A., and Gelfand, M. S. (2003). Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc. Natl. Acad. Sci. U.S.A. 100, 9912-9917. doi: 10.1073/pnas.1733691100.
74. Pasquali, P., Ammendola, S., Pistoia, C., Petrucci, P., Tarantino, M., Valente, C., et al. (2008). Attenuated Salmonella enterica serovar Typhimurium lacking the ZnuABC transporter confers immune-based protection against challenge infections in mice. Vaccine 26, 3421-3426. doi: 10.1016/j.vaccine.2008.04.036.
75. Patzer, S. I., and Hantke, K. (1998). The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol. Microbiol. 28, 1199-1210. doi: 10.1046/j.1365-2958.1998.00883.x.
76. Pawlik, M. C., Hubert, K., Joseph, B., Claus, H., Schoen, C., and Vogel, U. (2012). The zinc-responsive regulon of Neisseria meningitidis comprises 17 genes under control of a Zur element. J. Bacteriol. 194, 6594-6603. doi: 10.1128/JB.01091-12.
77. Pesciaroli, M., Aloisio, F., Ammendola, S., Pistoia, C., Petrucci, P., Tarantino, M., et al. (2011). An attenuated Salmonella enterica serovar Typhimurium strain lacking the ZnuABC transporter induces protection in a mouse intestinal model of Salmonella infection. Vaccine 29, 1783-1790. doi: 10.1016/j.vaccine.2010.12.111.
78. Pesciaroli, M., Gradassi, M., Martinelli, N., Ruggeri, J., Pistoia, C., Raffatellu, M., et al. (2013). Salmonella Typhimurium lacking the Znuabc transporter is attenuated and immunogenic in pigs. Vaccine 31, 2868-2873. doi: 10.1016/j.vaccine.2013.04.032.
79. Petrarca, P., Ammendola, S., Pasquali, P., and Battistoni, A. (2010). The Zur-regulated ZinT protein is an auxiliary component of the high-affinity ZnuABC zinc transporter that facilitates metal recruitment during severe zinc shortage. J. Bacteriol. 192, 1553-1564. doi: 10.1128/JB.01310-09.
80. Rensing, C., Mitra, B., and Rosen, B. P. (1997). The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc. Natl. Acad. Sci. U.S.A. 94, 14326-14331. doi: 10.1073/pnas.94.26.14326.
81. Rosadini, C. V., Gawronski, J. D., Raimunda, D., Arguello, J. M., and Akerley, B. J. (2011). A novel zinc binding system, ZevAB, is critical for survival of nontypeable Haemophilus influenzae in a murine lung infection model. Infect. Immun. 79, 3366-3376. doi: 10.1128/IAI.05135-11.
82. Sabri, M., Houle, S., and Dozois, C. M. (2009). Roles of the extraintestinal pathogenic Escherichia coli ZnuACB and ZupT zinc transporters during urinary tract infection. Infect. Immun. 77, 1155-1164. doi: 10.1128/IAI.01082-08.
83. Scrutton, M. C., Wu, C. W., and Goldthwait, D. A. (1971). The presence and possible role of zinc in RNA polymerase obtained from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 68, 2497-2501. doi: 10.1073/pnas.68.10.2497.
84. Shin, J. H., Jung, H. J., An, Y. J., Cho, Y. B., Cha, S. S., and 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. doi: 10.1073/pnas.1017744108.
85. Simm, C., Luan, C. H., Weiss, E., and O'Halloran, T. (2011). High-throughput screen for identifying small molecules that target fungal zinc homeostasis. PLoS ONE 6:e25136. doi: 10.1371/journal.pone.0025136.
86. Stork, M., Bos, M. P., Jongerius, I., De Kok, N., Schilders, I., Weynants, V. E., et al. (2010). An outer membrane receptor of Neisseria meningitidis involved in zinc acquisition with vaccine potential. PLoS Pathog. 6:e1000969. doi: 10.1371/journal.ppat.1000969.
87. Subramanian Vignesh, K., Landero Figueroa, J. A., Porollo, A., Caruso, J. A., and Deepe, G. S. Jr. (2013). Granulocyte macrophage-colony stimulating factor induced zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. Immunity 39, 697-710. doi: 10.1016/j.immuni.2013.09.006.
88. Taudte, N., and Grass, G. (2010). Point mutations change specificity and kinetics of metal uptake by ZupT from Escherichia coli. Biometals 23, 643-656. doi: 10.1007/s10534-010-9319-z.
89. Waldron, K. J., and Robinson, N. J. (2009). How do bacterial cells ensure that metalloproteins get the correct metal? Nat. Rev. Microbiol. 7, 25-35. doi: 10.1038/nrmicro2057.
90. Wang, D., Hosteen, O., and Fierke, C. A. (2012). ZntR-mediated transcription of zntA responds to nanomolar intracellular free zinc. J. Inorg. Biochem. 111, 173-181. doi: 10.1016/j.jinorgbio.2012.02.008.
91. Wang, D., Hurst, T. K., Thompson, R. B., and Fierke, C. A. (2011). Genetically encoded ratiometric biosensors to measure intracellular exchangeable zinc in Escherichia coli. J. Biomed. Opt. 16, 087011. doi: 10.1117/1.3613926.
92. Wei, B., Randich, A. M., Bhattacharyya-Pakrasi, M., Pakrasi, H. B., and Smith, T. J. (2007). Possible regulatory role for the histidine-rich loop in the zinc transport protein, ZnuA. Biochemistry 46, 8734-8743. doi: 10.1021/bi700763w.
93. Yang, X., Becker, T., Walters, N., and Pascual, D. W. (2006). Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge. Infect. Immun. 74, 3874-3879. doi: 10.1128/IAI.01957-05.
94. Yatsunyk, L. A., Easton, J. A., Kim, L. R., Sugarbaker, S. A., Bennett, B., Breece, R. M., et al. (2008). Structure and metal binding properties of ZnuA, a periplasmic zinc transporter from Escherichia coli. J. Biol. Inorg. Chem. 13, 271-288. doi: 10.1007/s00775-007-0320-0.
95. Zalewski, P., Truong-Tran, A., Lincoln, S., Ward, D., Shankar, A., Coyle, P., et al. (2006). Use of a zinc fluorophore to measure labile pools of zinc in body fluids and cell-conditioned media. BioTechniques 40, 509-520. doi: 10.2144/06404RR02.