Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium

Infection and Immunity

Volumn 70, Issue 11, 2002, Pages 6032-6042

  Boyer, E ^a   Bergevin, I ^a   Malo, D ^a   Gros, P ^a   Cellier, Matthieu F M ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2,2' BIPYRIDINE; ABC TRANSPORTER; CARRIER PROTEIN; DIVALENT CATION; DNA; HYDROGEN PEROXIDE; IRON; MANGANESE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; GENE EXPRESSION; MACROPHAGE; MOUSE; MUTANT; NONHUMAN; PATHOGENICITY; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SALMONELLA ENTERICA; SEROTYPE;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; CULTURE MEDIA; GENES, BACTERIAL; HYDROGEN PEROXIDE; IRON; MACROPHAGES; MANGANESE; MICE; OPERON; SALMONELLA TYPHIMURIUM; VIRULENCE;

EID: 0036840469     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.70.11.6032-6042.2002     Document Type: Article

References (37)

1. Agranoff, D., I. M. Monahan, J. A. Mangan, P. D. Butcher, and S. Krishna. 1999. Mycobacterium tuberculosis expresses a novel pH-dependent divalent cation transporter belonging to the Nramp family. J. Exp. Med. 190:717-724.
2. Bartsevich, V. V., and H. B. Pakrasi. 1995. Molecular identification of an ABC transporter complex for manganese: analysis of a cyanobacterial mutant strain impaired in the photosynthetic oxygen evolution process. EMBO J. 14:1845-1853.
3. Bearden, S. W., and R. D. Perry. 1999. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32:403-414.
4. Bearden, S. W., T. M. Staggs, and R. D. Perry. 1998. An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J. Bacteriol. 180:1135-1147.
5. Beuzon, C. R., and D. W. Holden. 2001. Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect. 3:1345-1352.
6. Byers, B. R., and J. E. L. Arceneaux. 1998. Microbial iron transport: iron acquisition by pathogenic microorganisms, p. 37-66. In A. Sigel and H. Sigel (ed.), Iron transport and storage in microorganisms, plants and animals Marcel Dekker Inc., New York, N.Y.
7. Cellier, M. F., I. Bergevin, E. Boyer, and E. Richer. 2001. Polyphyletic origins of bacterial Nramp transporters, Trends Genet. 17:365-370.
8. Christianson, D. W. 1997. Structural chemistry and biology of manganese metalloenzymes. Prog. Biophys. Mol. Biol. 67:217-252.
9. Claverys, J. P. 2001. A new family of high-affinity ABC manganese and zinc permeases. Res. Microbiol. 152:231-243.
10. Dennis, J. J., and G. J. Zylstra. 1998. Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl. Environ. Microbiol. 64:2710-2715.
11. Domenech, P., A. S. Pym, M. Cellier, C. E. Barry, and S. T. Cole. 2002. Inactivation of the Mycobacterium tuberculosis Nramp orthologue (mntH) does not affect virulence in a mouse model of tuberculosis. FEMS Microbiol. Lett. 207:81-86.
12. Govoni, G., F. Canonne-Hergaux, C. G. Pfeifer, S. L. Marcus, S. D. Mills, D. J. Hackam, S. Grinstein, D. Malo, B. B. Finlay, and P. Gros. 1999. Functional expression of Nramp1 in vitro in the murine macrophage line RAW264.7. Infect. Immun. 67:2225-2232.
13. Gruenheid, S., E. Pinner, M. Desjardins, and P. Gros. 1997. Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J. Exp. Med. 185:717-730.
14. Hacker, J., and J. B. Kaper. 2000. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54:641-679.
15. Hantke, K. 1997. Ferrous iron uptake by a magnesium transport system is toxic for Escherichia coli and Salmonella typhimuruim. J. Bacteriol. 179:6201-6204.
16. Jabado, N., A. Jankowski, S. Dougaparsad, V. Picard, S. Grinstein, and P. Gros. 2000. Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J. Exp. Med. 192:1237-1248.
17. Jakubovics, N. S., and H. F. Jenkinson. 2001. Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147:1709-1718.
18. Janakiraman, A., and J. M. Slauch. 2000. The putative iron transport system sitABCD encoded on SP11 is required for full virulence of Salmonella typhimurium. Mol. Microbiol. 35:1146-1155.
19. Kammler, M., C. Schon, and K. Hantke. 1993. Characterization of the ferrous iron uptake system of Escherichia coli. J. Bacteriol. 175:6212-6219.
20. Kehres, D. G., M. L. Zaharik, B. B. Finlay, and M. E. Maguire. 2000. The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol. Microbiol. 36:1085-1100.
21. Leung, K. Y., and B. B. Finlay. 1991. Intracellular replication is essential for the virulence of Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 88:11470-11474.
22. Link, A. J., D. Phillips, and G. M. Church. 1997. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J. Bacteriol. 179:6228-6237.
23. Makui, H., E. Roig, S. T. Cole, J. D. Helmann, P. Gros, and M. F. Cellier. 2000. Identification of the Escherichia coli K-12 Nramp orthologue (mntH) as a selective divalent metal ion transporter. Mol. Microbiol. 35:1065-1078.
24. Malo, D., K. Vogan, S. Vidal, J. Hu, M. Cellier, E. Schurr, A. Fuks, N. Bumstead, K. Morgan, and P. Gros. 1994. Haplotype mapping and sequence analysis of the mouse Nramp gene predict susceptibility to infection with intracellular parasites. Genomics 23:51-451.
25. Mastroeni, P., A. Vazquez-Torres, F. C. Fang, Y. Xu, S. Khan, C. E. Hormaeche, and G. Dougan. 2000. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J. Exp. Med. 192:237-248.
26. Miller, J. H. (ed.). 1992. A laboratory manual and handbook for E. coli and related bacteria, p. 24.5-24.6. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
27. Moeck, G. S., and J. W. Coulton. 1998. TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol. Microbiol. 28:675-681.
28. Ohl, M. E., and S. I. Miller. 2001. Salmonella: a model for bacterial pathogenesis. Annu. Rev. Med. 52:259-274.
29. 2+ transporter in Escherichia coli. J. Bacteriol. 183:4806-4813.
30. Posey, J. E., and F. C. Gherardini. 2000. Lack of a role for iron in the Lyme disease pathogen. Science 288:1651-1653.
31. Que, Q., and J. D. Helmann. 2000. Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins. Mol. Microbiol. 35:1454-1468.
32. Ratledge, C., and L. G. Dover. 2000. Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 54:881-941.
33. Robson, H. G., and S. I. Vas. 1972. Resistance of inbred mice to Salmonella typhimurium. J. Infect. Dis. 126:378-386.
34. Tsolis, R. M., A. J. Baumler, F. Heffron, and I. Stojiljkovic. 1996. Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect. Immun. 64:4549-4556.
35. Velayudhan, J., N. J. Hughes, A. A. McColm, J. Bagshaw, C. L. Clayton, S. C. Andrews, and D. J. Kelly. 2000. Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol. Microbiol. 37:274-286.
36. Vidal, S., M. L. Tremblay, G. Govoni, S. Gauthier, G. Sebastiani, D. Malo, E. Skamene, M. Olivier, S. Jothy, and P. Gros. 1995. The ityllsh/bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J. Exp. Med. 182:655-666.
37. Zhou, D., W. D. Hardt, and J. E. Galan. 1999. Salmonella typhirium encodes a putative iron transport system within the centisome 63 pathogenicity island. Infect. Immun. 67:1974-1981.