1887

Abstract

has a flea-mammal-flea transmission cycle, and is a zoonotic pathogen that causes the systemic diseases bubonic and septicaemic plague in rodents and humans, as well as pneumonic plague in humans and non-human primates. Bubonic and pneumonic plague are quite different diseases that result from different routes of infection. Manganese (Mn) acquisition is critical for the growth and pathogenesis of a number of bacteria. The Yfe/Sit and/or MntH systems are the two prominent Mn transporters in Gram-negative bacteria. Previously we showed that the Yfe system transports Fe and Mn. Here we demonstrate that a mutation in or did not significantly affect aerobic growth under Mn-deficient conditions. A double mutant did exhibit a moderate growth defect which was alleviated by supplementation with Mn. No short-term energy-dependent uptake of Mn was observed in this double mutant. Like the promoter, the promoter was repressed by both Mn and Fe via Fur. Sequences upstream of the Fur binding sequence in the promoter converted an iron-repressible promoter to one that is also repressed by Mn and Fe. To our knowledge, this is the first report identifying promoter elements needed to alter cation specificities involved in transcriptional repression. Finally, the double mutant had an ~133-fold loss of virulence in a mouse model of bubonic plague but no virulence loss in the pneumonic plague model. This suggests that Mn availability, bacterial Mn requirements or Mn transporters used by are different in the lungs (pneumonic plague) compared with systemic disease.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.053710-0
2012-03-01
2021-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/3/804.html?itemId=/content/journal/micro/10.1099/mic.0.053710-0&mimeType=html&fmt=ahah

References

  1. Anderson E. S., Paulley J. T., Gaines J. M., Valderas M. W., Martin D. W., Menscher E., Brown T. D., Burns C. S., Roop R. M. II ( 2009). The manganese transporter MntH is a critical virulence determinant for Brucella abortus 2308 in experimentally infected mice. Infect Immun 77:3466–3474 [View Article][PubMed]
    [Google Scholar]
  2. Anjem A., Varghese S., Imlay J. A. ( 2009). Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli . Mol Microbiol 72:844–858 [View Article][PubMed]
    [Google Scholar]
  3. Arirachakaran P., Benjavongkulchai E., Luengpailin S., Ajdić D., Banas J. A. ( 2007). Manganese affects Streptococcus mutans virulence gene expression. Caries Res 41:503–511 [View Article][PubMed]
    [Google Scholar]
  4. Aschner J. L., Aschner M. ( 2005). Nutritional aspects of manganese homeostasis. Mol Aspects Med 26:353–362 [View Article][PubMed]
    [Google Scholar]
  5. Aschner M., Gannon M. ( 1994). Manganese (Mn) transport across the rat blood-brain barrier: saturable and transferrin-dependent transport mechanisms. Brain Res Bull 33:345–349 [View Article][PubMed]
    [Google Scholar]
  6. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. (editors) ( 1987). Current Protocols in Molecular Biology New York: Wiley;
    [Google Scholar]
  7. Bagg A., Neilands J. B. ( 1987). Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli . Biochemistry 26:5471–5477 [View Article][PubMed]
    [Google Scholar]
  8. Bearden S. W., Perry R. D. ( 1999). The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol 32:403–414 [View Article][PubMed]
    [Google Scholar]
  9. Bearden S. W., Fetherston J. D., Perry R. D. ( 1997). Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis . Infect Immun 65:1659–1668[PubMed]
    [Google Scholar]
  10. Bearden S. W., Staggs T. M., Perry R. D. ( 1998). An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J Bacteriol 180:1135–1147[PubMed]
    [Google Scholar]
  11. Beesley E. D., Brubaker R. R., Janssen W. A., Surgalla M. J. ( 1967). Pesticins. 3. Expression of coagulase and mechanism of fibrinolysis. J Bacteriol 94:19–26[PubMed]
    [Google Scholar]
  12. Berntsson R. P.-A., Smits S. H. J., Schmitt L., Slotboom D.-J., Poolman B. ( 2010). A structural classification of substrate-binding proteins. FEBS Lett 584:2606–2617 [View Article][PubMed]
    [Google Scholar]
  13. Berry A. M., Paton J. C. ( 1996). Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae . Infect Immun 64:5255–5262[PubMed]
    [Google Scholar]
  14. Birnboim H. C., Doly J. ( 1979). A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523 [View Article][PubMed]
    [Google Scholar]
  15. Boyer E., Bergevin I., Malo D., Gros P., Cellier M. F. M. ( 2002). Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect Immun 70:6032–6042 [View Article][PubMed]
    [Google Scholar]
  16. Brubaker R. R. ( 1969). Mutation rate to nonpigmentation in Pasteurella pestis . J Bacteriol 98:1404–1406[PubMed]
    [Google Scholar]
  17. Cao J., Woodhall M. R., Alvarez J., Cartron M. L., Andrews S. C. ( 2007). EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157 : H7. Mol Microbiol 65:857–875 [View Article][PubMed]
    [Google Scholar]
  18. Champion O. L., Karlyshev A., Cooper I. A. M., Ford D. C., Wren B. W., Duffield M., Oyston P. C. F., Titball R. W. ( 2011). Yersinia pseudotuberculosis mntH functions in intracellular manganese accumulation, which is essential for virulence and survival in cells expressing functional Nramp1. Microbiology 157:1115–1122 [View Article][PubMed]
    [Google Scholar]
  19. Claverys J. P. ( 2001). A new family of high-affinity ABC manganese and zinc permeases. Res Microbiol 152:231–243 [View Article][PubMed]
    [Google Scholar]
  20. Corbin B. D., Seeley E. H., Raab A., Feldmann J., Miller M. R., Torres V. J., Anderson K. L., Dattilo B. M., Dunman P. M. & other authors ( 2008). Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319:962–965 [View Article][PubMed]
    [Google Scholar]
  21. Critchfield J. W., Keen C. L. ( 1992). Manganese+2 exhibits dynamic binding to multiple ligands in human plasma. Metabolism 41:1087–1092 [View Article][PubMed]
    [Google Scholar]
  22. Dashper S. G., Butler C. A., Lissel J. P., Paolini R. A., Hoffmann B., Veith P. D., O’Brien-Simpson N. M., Snelgrove S. L., Tsiros J. T., Reynolds E. C. ( 2005). A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J Biol Chem 280:28095–28102 [View Article][PubMed]
    [Google Scholar]
  23. Datsenko K. A., Wanner B. L. ( 2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645 [View Article][PubMed]
    [Google Scholar]
  24. Davidsson L., Lönnerdal B., Sandström B., Kunz C., Keen C. L. ( 1989). Identification of transferrin as the major plasma carrier protein for manganese introduced orally or intravenously or after in vitro addition in the rat. J Nutr 119:1461–1464[PubMed]
    [Google Scholar]
  25. Deng W., Burland V., Plunkett G. III, Boutin A., Mayhew G. F., Liss P., Perna N. T., Rose D. J., Mau B. & other authors ( 2002). Genome sequence of Yersinia pestis KIM. J Bacteriol 184:4601–4611 [View Article][PubMed]
    [Google Scholar]
  26. Desrosiers D. C., Bearden S. W., Mier I. Jr, Abney J., Paulley J. T., Fetherston J. D., Salazar J. C., Radolf J. D., Perry R. D. ( 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 [View Article][PubMed]
    [Google Scholar]
  27. Dintilhac A., Alloing G., Granadel C., 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 [View Article][PubMed]
    [Google Scholar]
  28. Fetherston J. D., Lillard J. W. Jr, Perry R. D. ( 1995). Analysis of the pesticin receptor from Yersinia pestis: role in iron-deficient growth and possible regulation by its siderophore. J Bacteriol 177:1824–1833[PubMed]
    [Google Scholar]
  29. Fetherston J. D., Kirillina O., Bobrov A. G., Paulley J. T., Perry R. D. ( 2010). The yersiniabactin transport system is critical for the pathogenesis of bubonic and pneumonic plague. Infect Immun 78:2045–2052 [View Article][PubMed]
    [Google Scholar]
  30. Fields K. A., Nilles M. L., Cowan C., Straley S. C. ( 1999). Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect Immun 67:5395–5408[PubMed]
    [Google Scholar]
  31. Forman S., Nagiec M. J., Abney J., Perry R. D., Fetherston J. D. ( 2007). Analysis of the aerobactin and ferric hydroxamate uptake systems of Yersinia pestis . Microbiology 153:2332–2341 [View Article][PubMed]
    [Google Scholar]
  32. Fraústo da Silva J. J. R., Williams R. J. P. ( 2001). The Biological Chemistry of the Elements: the Inorganic Chemistry of Life, 2nd edn. New York: Oxford University Press;
    [Google Scholar]
  33. Gong S., Bearden S. W., Geoffroy V. A., Fetherston J. D., Perry R. D. ( 2001). Characterization of the Yersinia pestis Yfu ABC inorganic iron transport system. Infect Immun 69:2829–2837 [View Article][PubMed]
    [Google Scholar]
  34. Gray R. D., Duncan A., Noble D., Imrie M., O’Reilly D. S. J., Innes J. A., Porteous D. J., Greening A. P., Boyd A. C. ( 2010). Sputum trace metals are biomarkers of inflammatory and suppurative lung disease. Chest 137:635–641 [View Article][PubMed]
    [Google Scholar]
  35. Große C., Scherer J., Koch D., Otto M., Taudte N., Grass G. ( 2006). A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli . Mol Microbiol 62:120–131 [View Article][PubMed]
    [Google Scholar]
  36. Guedon E., Helmann J. D. ( 2003). Origins of metal ion selectivity in the DtxR/MntR family of metalloregulators. Mol Microbiol 48:495–506 [View Article][PubMed]
    [Google Scholar]
  37. Hantke K. ( 1987). Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: fur not only affects iron metabolism. Mol Gen Genet 210:135–139 [View Article][PubMed]
    [Google Scholar]
  38. Hazlett K. R. O., Rusnak F., Kehres D. G., Bearden S. W., La Vake C. J., La Vake M. E., Maguire M. E., Perry R. D., Radolf J. D. ( 2003). The Treponema pallidum tro operon encodes a multiple metal transporter, a zinc-dependent transcriptional repressor, and a semi-autonomously expressed phosphoglycerate mutase. J Biol Chem 278:20687–20694 [View Article][PubMed]
    [Google Scholar]
  39. He J., Miyazaki H., Anaya C., Yu F., Yeudall W. A., Lewis J. P. ( 2006). Role of Porphyromonas gingivalis FeoB2 in metal uptake and oxidative stress protection. Infect Immun 74:4214–4223 [View Article][PubMed]
    [Google Scholar]
  40. Higuchi K., Smith J. L. ( 1961). Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to avirulence. J Bacteriol 81:605–608[PubMed]
    [Google Scholar]
  41. Ikeda J. S., Janakiraman A., Kehres D. G., Maguire M. E., Slauch J. M. ( 2005). Transcriptional regulation of sitABCD of Salmonella enterica serovar Typhimurium by MntR and Fur. J Bacteriol 187:912–922 [View Article][PubMed]
    [Google Scholar]
  42. Inglesby T. V., Dennis D. T., Henderson D. A., Bartlett J. G., Ascher M. S., Eitzen E., Fine A. D., Friedlander A. M., Hauer J. & other authors ( 2000). Plague as a biological weapon: medical and public health management. JAMA 283:2281–2290 [View Article][PubMed]
    [Google Scholar]
  43. Jakubovics N. S., Jenkinson H. F. ( 2001). Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147:1709–1718[PubMed]
    [Google Scholar]
  44. Janakiraman A., Slauch J. M. ( 2000). The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium . Mol Microbiol 35:1146–1155 [View Article][PubMed]
    [Google Scholar]
  45. Janulczyk R., Pallon J., Björck L. ( 1999). Identification and characterization of a Streptococcus pyogenes ABC transporter with multiple specificity for metal cations. Mol Microbiol 34:596–606 [View Article][PubMed]
    [Google Scholar]
  46. Janulczyk R., Ricci S., Björck L. ( 2003). MtsABC is important for manganese and iron transport, oxidative stress resistance, and virulence of Streptococcus pyogenes . Infect Immun 71:2656–2664 [View Article][PubMed]
    [Google Scholar]
  47. Kehl-Fie T. E., Skaar E. P. ( 2010). Nutritional immunity beyond iron: a role for manganese and zinc. Curr Opin Chem Biol 14:218–224 [View Article][PubMed]
    [Google Scholar]
  48. Kehres D. G., Janakiraman A., Slauch J. M., Maguire M. E. ( 2002a). SitABCD is the alkaline Mn2+ transporter of Salmonella enterica serovar Typhimurium. J Bacteriol 184:3159–3166 [View Article][PubMed]
    [Google Scholar]
  49. Kehres D. G., Janakiraman A., Slauch J. M., Maguire M. E. ( 2002b). Regulation of Salmonella enterica serovar Typhimurium mntH transcription by H2O2, Fe2+, and Mn2+.. J Bacteriol 184:3151–3158 [View Article][PubMed]
    [Google Scholar]
  50. Kirillina O., Bobrov A. G., Fetherston J. D., Perry R. D. ( 2006). Hierarchy of iron uptake systems: Yfu and Yiu are functional in Yersinia pestis . Infect Immun 74:6171–6178 [View Article][PubMed]
    [Google Scholar]
  51. Kliegman J. I., Griner S. L., Helmann J. D., Brennan R. G., Glasfeld A. ( 2006). Structural basis for the metal-selective activation of the manganese transport regulator of Bacillus subtilis . Biochemistry 45:3493–3505 [View Article][PubMed]
    [Google Scholar]
  52. Koch D., Chan A. C. K., Murphy M. E. P., Lilie H., Grass G., Nies D. H. ( 2011). Characterization of a dipartite iron uptake system from uropathogenic Escherichia coli strain F11. J Biol Chem 286:25317–25330 [View Article][PubMed]
    [Google Scholar]
  53. Lathem W. W., Price P. A., Miller V. L., Goldman W. E. ( 2007). A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315:509–513 [View Article][PubMed]
    [Google Scholar]
  54. Lim K. H. L., Jones C. E., vanden Hoven R. N., Edwards J. L., Falsetta M. L., Apicella M. A., Jennings M. P., McEwan A. G. ( 2008). Metal binding specificity of the MntABC permease of Neisseria gonorrhoeae and its influence on bacterial growth and interaction with cervical epithelial cells. Infect Immun 76:3569–3576 [View Article][PubMed]
    [Google Scholar]
  55. Lönnerdal B., Keen C. L., Hurley L. S. ( 1985). Manganese binding proteins in human and cow’s milk. Am J Clin Nutr 41:550–559[PubMed]
    [Google Scholar]
  56. Macara I. G., Hoy T. G., Harrison P. M. ( 1973). The formation of ferritin from apoferritin. Inhibition and metal ion-binding studies. Biochem J 135:785–789[PubMed]
    [Google Scholar]
  57. Marra A., Lawson S., Asundi J. S., Brigham D., Hromockyj A. E. ( 2002). In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection. Microbiology 148:1483–1491[PubMed]
    [Google Scholar]
  58. McDevitt C. A., Ogunniyi A. D., Valkov E., Lawrence M. C., Kobe B., McEwan A. G., Paton J. C. ( 2011). A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog 7:e1002357 [View Article][PubMed]
    [Google Scholar]
  59. Miller J. H. ( 1992). A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  60. Moutafchiev D., Sirakov L., Bontchev P. ( 1998). The competition between transferrins labeled with 59Fe, 65Zn, and 54Mn for the binding sites on lactating mouse mammary gland cells. Biol Trace Elem Res 61:181–191 [View Article][PubMed]
    [Google Scholar]
  61. Ouyang Z., He M., Oman T., Yang X. F., Norgard M. V. ( 2009). A manganese transporter, BB0219 (BmtA), is required for virulence by the Lyme disease spirochete, Borrelia burgdorferi . Proc Natl Acad Sci U S A 106:3449–3454 [View Article][PubMed]
    [Google Scholar]
  62. Paik S., Brown A., Munro C. L., Cornelissen C. N., Kitten T. ( 2003). The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor. J Bacteriol 185:5967–5975 [View Article][PubMed]
    [Google Scholar]
  63. Papavasiliou P. S., Cotzias G. C. ( 1961). Neutron activation analysis: the determination of manganese. J Biol Chem 236:2365–2369[PubMed]
    [Google Scholar]
  64. Papp-Wallace K. M., Maguire M. E. ( 2006). Manganese transport and the role of manganese in virulence. Annu Rev Microbiol 60:187–209 [View Article][PubMed]
    [Google Scholar]
  65. Patzer S. I., Hantke K. ( 2001). Dual repression by Fe2+-Fur and Mn2+-MntR of the mntH gene, encoding an NRAMP-like Mn2+ transporter in Escherichia coli . J Bacteriol 183:4806–4813 [View Article][PubMed]
    [Google Scholar]
  66. Perry R. D., Fetherston J. D. ( 1997). Yersinia pestis – etiologic agent of plague. Clin Microbiol Rev 10:35–66[PubMed]
    [Google Scholar]
  67. Perry R. D., Pendrak M. L., Schuetze P. ( 1990). Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis . J Bacteriol 172:5929–5937[PubMed]
    [Google Scholar]
  68. Perry R. D., Abney J., Mier I. Jr, Lee Y., Bearden S. W., Fetherston J. D. ( 2003). Regulation of the Yersinia pestis Yfe and Ybt iron transport systems. Adv Exp Med Biol 529:275–283 [View Article][PubMed]
    [Google Scholar]
  69. Perry R. D., Mier I. Jr, Fetherston J. D. ( 2007). Roles of the Yfe and Feo transporters of Yersinia pestis in iron uptake and intracellular growth. Biometals 20:699–703 [View Article][PubMed]
    [Google Scholar]
  70. Perry R. D., Bobrov A. G., Kirillina O., Fetherston J. D. ( 2012). Yersinia pestis transition metal divalent cation transporters. Adv Exp Med Biol
    [Google Scholar]
  71. Privalle C. T., Fridovich I. ( 1993). Iron specificity of the Fur-dependent regulation of the biosynthesis of the manganese-containing superoxide dismutase in Escherichia coli . J Biol Chem 268:5178–5181[PubMed]
    [Google Scholar]
  72. Rajasekaran M. B., Nilapwar S., Andrews S. C., Watson K. A. ( 2010). EfeO-cupredoxins: major new members of the cupredoxin superfamily with roles in bacterial iron transport. Biometals 23:1–17 [View Article][PubMed]
    [Google Scholar]
  73. Reed L. J., Muench H. ( 1938). A simple method for estimating fifty percent endpoints. Am J Hyg 27:493–497
    [Google Scholar]
  74. Rehnberg G. L., Hein J. F., Carter S. D., Laskey J. W. ( 1980). Chronic manganese oxide administration to preweanling rats: manganese accumulation and distribution. J Toxicol Environ Health 6:217–226 [View Article][PubMed]
    [Google Scholar]
  75. Rhodes E. R., Tomaras A. P., McGillivary G., Connerly P. L., Actis L. A. ( 2005). Genetic and functional analyses of the Actinobacillus actinomycetemcomitans AfeABCD siderophore-independent iron acquisition system. Infect Immun 73:3758–3763 [View Article][PubMed]
    [Google Scholar]
  76. Rogers H. J. ( 1973). Iron-binding catechols and virulence in Escherichia coli . Infect Immun 7:445–456[PubMed]
    [Google Scholar]
  77. Runyen-Janecky L. J., Reeves S. A., Gonzales E. G., Payne S. M. ( 2003). Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect Immun 71:1919–1928 [View Article][PubMed]
    [Google Scholar]
  78. Runyen-Janecky L., Dazenski E., Hawkins S., Warner L. ( 2006). Role and regulation of the Shigella flexneri Sit and MntH systems. Infect Immun 74:4666–4672 [View Article][PubMed]
    [Google Scholar]
  79. Sabri M., Léveillé S., Dozois C. M. ( 2006). A SitABCD homologue from an avian pathogenic Escherichia coli strain mediates transport of iron and manganese and resistance to hydrogen peroxide. Microbiology 152:745–758 [View Article][PubMed]
    [Google Scholar]
  80. Sabri M., Caza M., Proulx J., Lymberopoulos M. H., Brée A., Moulin-Schouleur M., Curtiss R. III, Dozois C. M. ( 2008). Contribution of the SitABCD, MntH, and FeoB metal transporters to the virulence of avian pathogenic Escherichia coli O78 strain χ7122. Infect Immun 76:601–611 [View Article][PubMed]
    [Google Scholar]
  81. Schmitt M. P. ( 2002). Analysis of a DtxR-like metalloregulatory protein, MntR, from Corynebacterium diphtheriae that controls expression of an ABC metal transporter by an Mn2+-dependent mechanism. J Bacteriol 184:6882–6892 [View Article][PubMed]
    [Google Scholar]
  82. Smith A. J., Ward P. N., Field T. R., Jones C. L., Lincoln R. A., Leigh J. A. ( 2003). MtuA, a lipoprotein receptor antigen from Streptococcus uberis, is responsible for acquisition of manganese during growth in milk and is essential for infection of the lactating bovine mammary gland. Infect Immun 71:4842–4849 [View Article][PubMed]
    [Google Scholar]
  83. Staggs T. M., Perry R. D. ( 1991). Identification and cloning of a fur regulatory gene in Yersinia pestis . J Bacteriol 173:417–425[PubMed]
    [Google Scholar]
  84. Surgalla M. J., Beesley E. D. ( 1969). Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis . Appl Microbiol 18:834–837[PubMed]
    [Google Scholar]
  85. Tottey S., Waldron K. J., Firbank S. J., Reale B., Bessant C., Sato K., Cheek T. R., Gray J., Banfield M. J. & other authors ( 2008). Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 455:1138–1142 [View Article][PubMed]
    [Google Scholar]
  86. Zaharik M. L., Finlay B. B. ( 2004). Mn2+ and bacterial pathogenesis. Front Biosci 9:1035–1042 [View Article][PubMed]
    [Google Scholar]
  87. Zaharik M. L., Cullen V. L., Fung A. M., Libby S. J., Kujat Choy S. L., Coburn B., Kehres D. G., Maguire M. E., Fang F. C., Finlay B. B. ( 2004). The Salmonella enterica serovar Typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1G169 murine typhoid model. Infect Immun 72:5522–5525 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.053710-0
Loading
/content/journal/micro/10.1099/mic.0.053710-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error