Quantitative PCR-based competitive index for high-throughput screening of salmonella virulence factors

Infection and Immunity

Volumn 79, Issue 1, 2011, Pages 360-368

  Yoon, Hyunjin ^a   Gros, Phillipe ^b   Heffron, Fred ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; BACTERICIDAL ACTIVITY; HIGH THROUGHPUT SCREENING; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SALMONELLA;

ANIMALS; BACTERIAL PROTEINS; CATION TRANSPORT PROTEINS; CELLS, CULTURED; GENE DELETION; GENE EXPRESSION REGULATION; MACROPHAGES; MICE; POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; VIRULENCE FACTORS;

EID: 78650904841     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00873-10     Document Type: Article

References (64)

1. Aberle, S. W., and E. Puchhammer-Stockl. 2002. Diagnosis of herpesvirus infections of the central nervous system. J. Clin. Virol. 25(Suppl. 1):S79-S85.
2. Barton, C. H., S. H. Whitehead, and J. M. Blackwell. 1995. Nramp transfec-tion transfers Ity/Lsh/Bcg-related pleiotropic effects on macrophage activation: influence on oxidative burst and nitric oxide pathways. Mol. Med. 1:267-279.
3. Baumler, A. J., R. M. Tsolis, P. J. Valentine, T. A. Ficht, and F. Heffron. 1997. Synergistic effect of mutations in invA and lpfC on the ability of Salmonella typhimurium to cause murine typhoid. Infect. Immun. 65:2254-2259.
4. 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.
5. Blackwell, J. M., S. Searle, T. Goswami, and E. N. Miller. 2000. Understanding the multiple functions of Nramp1. Microbes Infect. 2, 317-321.
6. Bomberger, J. M., D. P. Maceachran, B. A. Coutermarsh, S. Ye, G. A. O'Toole, and B. A. Stanton. 2009. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 5:e1000382.
7. Buchmeier, N. A., and F. Heffron. 1989. Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages. Infect. Immun. 57:1-7.
8. Buchmeier, N. A., and F. Heffron. 1991. Inhibition of macrophage phago-some-lysosome fusion by Salmonella typhimurium. Infect. Immun. 59:2232-2238.
9. Bustin, S. A. 2000. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25:169-193.
10. Camilli, A., L. G. Tilney, and D. A. Portnoy. 1993. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol. Microbiol. 8:143-157.
11. Canonne-Hergaux, F., J. Calafat, E. Richer, M. Cellier, S. Grinstein, N. Borregaard, and P. Gros. 2002. Expression and subcellular localization of NRAMP1 in human neutrophil granules. Blood 100:268-275.
12. Chu, A. M., and R. W. Davis. 2008. High-throughput creation of a whole-genome collection of yeast knockout strains. Methods Mol. Biol. 416:205-220.
13. Conlan, J. W., and R. J. North. 1994. Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J. Exp. Med. 179:259-268.
14. Coombes, B. K., M. E. Wickham, N. F. Brown, S. Lemire, L. Bossi, W. W. Hsiao, F. S. Brinkman, and B. B. Finlay. 2005. Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar Typhimurium with autonomous expression from its associated phage. J. Mol. Biol. 348:817-830.
15. Datsenko, K. A., and B. L. Wanner. 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.
16. Ellermeier, C. D., A. Janakiraman, and J. M. Slauch. 2002. Construction of targeted single copy lac fusions using lambda red and FLP-mediated site-specific recombination in bacteria. Gene 290:153-161.
17. Forbes, J. R., and P. Gros. 2003. Iron, manganese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood 102:1884-1892.
18. Freter, R., P. C. O'Brien, and M. S. Macsai. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun. 34:234-240. (Pubitemid 11004969)
19. Geddes, K., F. Cruz, and F. Heffron. 2007. Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog. 3:e196.
20. Gerichter, C. B. 1960. The dissemination of Salmonella typhi, S. paratyphi A and S. paratyphi B through the organs of the white mouse by oral infection. J. Hyg. (Lond.) 58:307-319.
21. Govoni, G., and P. Gros. 1998. Macrophage NRAMP1 and its role in resistance to microbial infections. Inflamm. Res. 47:277-284.
22. 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.
23. Hafez, H. M., R. Hauck, D. Luschow, and L. McDougald. 2005. Comparison of the specificity and sensitivity of PCR, nested PCR, and real-time PCR for the diagnosis of histomoniasis. Avian Dis. 49:366-370.
24. Heid, C. A., J. Stevens, K. J. Livak, and P. M. Williams. 1996. Real-time quantitative PCR. Genome Res. 6:986-994.
25. Hensel, M., J. E. Shea, C. Gleeson, M. D. Jones, E. Dalton, and D. W. Holden. 1995. Simultaneous identification of bacterial virulence genes by negative selection. Science 269:400-403.
26. Ho, T. D., N. Figueroa-Bossi, M. Wang, S. Uzzau, L. Bossi, and J. M. Slauch. 2002. Identification of GtgE, a novel virulence factor encoded on the Gifsy-2 bacteriophage of Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:5234-5239.
27. Hormaeche, C. E. 1979. Natural resistance to Salmonella typhimurium in different inbred mouse strains. Immunology 37:311-318.
28. Huynh, C, D. L. Sacks, and N. W. Andrews. 2006. A Leishmania amazonen-sis ZIP family iron transporter is essential for parasite replication within macrophage phagolysosomes. J. Exp. Med. 203:2363-2375.
29. Kamphuis, W., A. Schneemann, L. M. van Beek, A. B. Smit, P. F. Hoyng, and E. Koya. 2001. Prostanoid receptor gene expression profile in human trabecular meshwork: a quantitative real-time PCR approach. Invest. Ophthalmol. Vis. Sci. 42:3209-3215.
30. Kesty, N. C, K. M. Mason, M. Reedy, S. E. Miller, and M. J. Kuehn. 2004. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23:4538-4549.
31. Lalmanach, A. C, and F. Lantier. 1999. Host cytokine response and resistance to Salmonella infection. Microbes Infect. 1:719-726.
32. Lalmanach, A. C, A. Montagne, P. Menanteau, and F. Lantier. 2001. Effect of the mouse Nramp1 genotype on the expression of IFN-gamma gene in early response to Salmonella infection. Microbes Infect. 3:639-644.
33. Lang, T., E. Prina, D. Sibthorpe, and J. M. Blackwell. 1997. Nramp1 trans-fection transfers Ity/Lsh/Bcg-related pleiotropic effects on macrophage activation: influence on antigen processing and presentation. Infect. Immun. 65:380-386.
34. Libby, S. J., L. G. Adams, T. A. Ficht, C. Allen, H. A. Whitford, N. A. Buchmeier, S. Bossie, and D. G. Guiney. 1997. The spv genes on the Salmonella dublin virulence plasmid are required for severe enteritis and systemic infection in the natural host. Infect. Immun. 65:1786-1792.
35. Libby, S. J., W. Goebel, A. Ludwig, N. Buchmeier, F. Bowe, F. C. Fang, D. G. Guiney, J. G. Songer, and F. Heffron. 1994. A cytolysin encoded by Salmonella is required for survival within macrophages. Proc. Natl. Acad. Sci. U.S.A. 91:489-493. (Pubitemid 24041427)
36. Liu, G., X. P. Xia, S. L. Gong, and Y. Zhao. 2006. The macrophage heterogeneity: difference between mouse peritoneal exudate and splenic F4/80 + macrophages. J. Cell. Physiol. 209:341-352.
37. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
38. Mastroeni, P., A. Grant, O. Restif, and D. Maskell. 2009. A dynamic view of the spread and intracellular distribution of Salmonella enterica. Nat. Rev. Microbiol. 7:73-80.
39. Meynell, G. G., and B. A. Stocker. 1957. Some hypotheses on the aetiology of fatal infections in partially resistant hosts and their application to mice challenged with Salmonella paratyphi-B or Salmonella typhimurium by in-traperitoneal injection. J. Gen. Microbiol. 16:38-58.
40. Mocellin, S., C. R. Rossi, P. Pilati, D. Nitti, and F. M. Marincola. 2003. Quantitative real-time PCR: a powerful ally in cancer research. Trends Mol. Med. 9:189-195.
41. Niess, J. H., S. Brand, X. Gu, L. Landsman, S. Jung, B. A. McCormick, J. M. Vyas, M. Boes, H. L. Ploegh, J. G. Fox, D. R. Littman, and H. C. Reinecker 2005. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307:254-258.
42. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
43. Plant, J., and A. A. Glynn. 1974. Natural resistance to Salmonella infection, delayed hypersensitivity and Ir genes in different strains of mice. Nature 248:345-347.
44. Ramakers, C., J. M. Ruijter, R. H. Deprez, and A. F. Moorman. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339:62-66.
45. Richter-Dahlfors, A., A. M. Buchan, and B. B. Finlay. 1997. Murine salmo-nellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186:569-580.
46. Roach, T. I., D. Chatterjee, and J. M. Blackwell. 1994. Induction of early-response genes KC and JE by mycobacterial lipoarabinomannans: regulation of KC expression in murine macrophages by Lsh/Ity/Bcg (candidate Nramp). Infect. Immun. 62:1176-1184.
47. Rubin, R. H., and L. Weinstein (ed.). 1977. Salmonellosis: microbiologic, pathologic and clinical features. Stratton Intercontinental Medical Book Corp., New York, NY.
48. Searle, S., N. A. Bright, T. I. Roach, P. G. Atkinson, C. H. Barton, R. H. Meloen, and J. M. Blackwell. 1998. Localisation of Nramp1 in macrophages: modulation with activation and infection. J. Cell Sci. 111:2855-2866.
49. Skotnikova, O. I., A. Y. Sobolev, V. V. Demkin, N. P. Nikolaeva, E. Y. Nosova, E. L. Isaeva, A. M. Moroz, and V. I. Litvinov. 2000. Application of nested-PCR technique for the diagnosis of tuberculosis. Bull. Exp. Biol. Med. 129:612-614.
50. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449:419-426.
51. Stober, C. B., S. Brode, J. K. White, J. F. Popoff, and J. M. Blackwell. 2007. Slc11a1, formerly Nramp1, is expressed in dendritic cells and influences major histocompatibility complex class II expression and antigen-presenting cell function. Infect. Immun. 75:5059-5067.
52. Taylor, R. K., V. L. Miller, D. B. Furlong, and J. J. Mekalanos. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. U.S.A. 84:2833-2837.
53. Unsworth, K. E., and D. W. Holden. 2000. Identification and analysis of bacterial virulence genes in vivo. Philos. Trans. R Soc. Lond. B Biol. Sci. 355:613-622.
54. Uzzau, S., P. A. Gulig, B. Paglietti, G. Leori, B. A. Stocker, and S. Rubino. 2000. Role of the Salmonella abortusovis virulence plasmid in the infection of BALB/c mice. FEMS Microbiol. Lett. 188:15-18.
55. Valdez, Y., G. E. Diehl, B. A. Vallance, G. A. Grassl, J. A. Guttman, N. F. Brown, C. M. Rosenberger, D. R. Littman, P. Gros, and B. B. Finlay. 2008. Nramp1 expression by dendritic cells modulates inflammatory responses during Salmonella Typhimurium infection. Cell. Microbiol. 10:1646-1661.
56. Valdez, Y., G. A. Grassl, J. A. Guttman, B. Coburn, P. Gros, B. A. Vallance, and B. B. Finlay. 2009. Nramp1 drives an accelerated inflammatory response during Salmonella-induced colitis in mice. Cell. Microbiol. 11:351-362.
57. Vidal, S., M. L. Tremblay, G. Govoni, S. Gauthier, G. Sebastiani, D. Malo, E. Skamene, M. Olivier, S. Jothy, and P. Gros. 1995. The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J. Exp. Med. 182:655-666.
58. Vidal, S. M., D. Malo, K. Vogan, E. Skamene, and P. Gros. 1993. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73:469-485.
59. Wai, S. N., B. Lindmark, T. Soderblom, A. Takade, M. Westermark, J. Oscarsson, J. Jass, A. Richter-Dahlfors, Y. Mizunoe, and B. E. Uhlin. 2003. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115:25-35.
60. Wyllie, S., P. Seu, and J. A. Goss. 2002. The natural resistance-associated macrophage protein 1 Slc11a1 (formerly Nramp1) and iron metabolism in macrophages. Microbes Infect. 4:351-359.
61. Yoon, H., J. E. McDermott, S. Porwollik, M. McClelland, and F. Heffron. 2009. Coordinated regulation of virulence during systemic infection of Salmonella enterica serovar Typhimurium. PLoS Pathog. 5:e1000306.
62. Yuan, J. S., A. Reed, F. Chen, and C. N. J. Stewart. 2006. Statistical analysis of real-time PCR data. BMC Bioinformatics 7:85.
63. Zaharik, M. L., B. A. Vallance, J. L. Puente, P. Gros, and B. B. Finlay. 2002. Host-pathogen interactions: host resistance factor Nramp1 up-regulates the expression of Salmonella pathogenicity island-2 virulence genes. Proc. Natl. Acad. Sci. U.S.A. 99:15705-15710.
64. Zwilling, B. S., D. E. Kuhn, L. Wikoff, D. Brown, and W. Lafuse. 1999. Role of iron in Nramp1-mediated inhibition of mycobacterial growth. Infect. Im-mun. 67:1386-1392.