The role of the spv genes in Salmonella pathogenesis

Frontiers in Microbiology

Volumn 2, Issue JUNE, 2011, Pages

  Guiney, Donald G ^a   Fierer, Joshua ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

ADP ribosylation; Apoptosis; CD4; Non typhoid bacteremia; Phosphothreonine lyase; Salmonella; Spv; Virulence

Indexed keywords

EID: 84860495725     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00129     Document Type: Article

References (88)

1. Abrahams, G. L., and Hensel, M. (2006). Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell. Microbiol. 8, 728-737.
2. Abrahams, G. L., Muller, P., and Hensel, M. (2006). Functional dissection of SseF, a type III effector protein involved in positioning the Salmonella-containing vacuole. Traffic 7, 950-965.
3. Allen, L. A., DeLeo, F. R., Gallois, A., Toyoshima, S., Suzuki, K., and Nauseef, W. M. (1999). Transient association of the nicotinamide adenine dinucleotide phosphate oxidase subunits p47phox and p67phox with phagosomes in neutrophils from patients with X-linked chronic granulomatous disease. Blood 93, 3521-3530.
4. Arthur, G., Nduba, V. N., Kariuki, S. M., Kimari, J., Bhatt, S. M., and Gilks, C. F. (2001). Trends in bloodstream infections among human immunodeficiency virusinfected adults admitted to a hospital in Nairobi, Kenya, during the last decade. Clin. Infect. Dis. 33, 248-256.
5. Blaser, M. J., and Feldman, R. A. (1981). From the centers for disease control. Salmonella bacteremia: reports to the Centers for Disease Control, 1968-1979. J. Infect. Dis. 143, 743-746.
6. Boyd, E. F., and Hartl, D. L. (1998). Salmonella virulence plasmid. Modular acquisition of the spv virulence region by an F-plasmid in Salmonella enterica subspecies I and insertion into the chromosome of subspecies II, IIIa, IV and VII isolates. Genetics 149, 1183-1190.
7. Browne, S. H., Hasegawa, P., Okamoto, S., Fierer, J., and Guiney, D. G. (2008). Identification of Salmonella SPI-2 secretion system components required for SpvB-mediated cytotoxicity in macrophages and virulence in mice. FEMS Immunol. Med. Microbiol. 52, 194-201.
8. Browne, S. H., Lesnick, M. L., and Guiney, D. G. (2002). Genetic requirements for Salmonella-induced cytopathology in human monocyte-derived macrophages. Infect. Immun. 70, 7126-7135.
9. Brumell, J. H., Goosney, D. L., and Finlay, B. B. (2002). SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules. Traffic 3, 407-415.
10. Celum, C. L., Chaisson, R. E., Rutherford, G. W., Barnhart, J. L., and Echenberg, D. F. (1987). Incidence of salmonellosis in patients with AIDS. J. Infect. Dis. 156, 998-1002.
11. Chen, C. Y., Buchmeier, N. A., Libby, S., Fang, F. C., Krause, M., and Guiney, D. G. (1995). Central regulatory role for the RpoS sigma factor in expression of Salmonella dublin plasmid virulence genes. J. Bacteriol. 177, 5303-5309.
12. Chen, C. Y., Eckmann, L., Libby, S. J., Fang, F. C., Okamoto, S., Kagnoff, M. F., Fierer, J., and Guiney, D. G. (1996). Expression of Salmonella typhimurium rpoS and rpoS-dependent genes in the intracellular environment of eukaryotic cells. Infect. Immun. 64, 4739-4743.
13. Coburn, B., Grassl, G. A., and Finlay, B. B. (2007). Salmonella, the host and disease: a brief review. Immunol. Cell Biol. 85, 112-118.
14. Cohen, P. S.,O'Brien,T. F., Schoenbaum, S. C., and Medeiros, A. A. (1978). The risk of endothelial infection in adults with Salmonella bacteremia. Ann. Intern. Med. 89, 931-932.
15. Deiwick, J., Salcedo, S. P., Boucrot, E., Gilliland, S. M., Henry, T., Petermann, N., Waterman, S. R., Gorvel, J. P., Holden, D. W., and Méresse, S. (2006). The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect. Immun. 74, 6965-6972.
16. elBenna, J., Ruedi, J. M., and Babior, B. M. (1994). Cytosolic guanine nucleotide-binding protein Rac2 operates in vivo as a component of the neutrophil respiratory burst oxidase. Transfer of Rac2 and the cytosolic oxidase components p47phox and p67phox to the submembranous actin cytoskeleton during oxidase activation. J. Biol. Chem. 269, 6729-6734.
17. Fang, F. C., and Fierer, J. (1991). Human infection with Salmonella dublin. Medicine 70, 198-207.
18. Fang, F. C., Krause, M., Roudier, C., Fierer, J., and Guiney, D. G. (1991). Growth regulation of a Salmonella plasmid gene essential for virulence. J. Bacteriol. 173, 6783-6789.
19. Fang, F. C., Libby, S. J., Buchmeier, N. A., Loewen, P. C., Switala, J., Harwood, J., and Guiney, D. G. (1992). The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc. Natl. Acad. Sci. U.S.A. 89, 11978-11982.
20. Fields, P. I., Swanson, R. V., Haidaris, C. G., and Heffron, F. (1986). Mutants of Salmonella typhimurium that cannot survive within the macrophage are a virulent. Proc. Natl. Acad. Sci. U.S.A. 83, 5189-5193.
21. Fierer, J. (1983). Invasive Salmonella dublin infections associated with drinking raw milk. West. J. Med. 138, 665-669.
22. Fierer, J., Eckmann, L., Fang, F., Pfeifer, C., Finlay, B. B., and Guiney, D. (1993). Expression of the Salmonella virulence plasmid gene spvB in cultured macrophages and nonphagocytic cells. Infect. Immun. 61, 5231-5236.
23. Fierer, J., and Guiney, D. G. (2001). Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J. Clin. Invest. 107, 775-780.
24. Fierer, J., Hatlen, L., Lin, J. P., Estrella, D., Mihalko, P., and Yau-Young, A. (1990). Successful treatment using gentamicin liposomes of Salmonella dublin infections in mice. Antimicrob. Agents Chemother. 34, 343-348.
25. Fierer, J., Krause, M., Tauxe, R., and Guiney, D. (1992). Salmonella typhimurium bacteremia: association with the virulence plasmid. J. Infect. Dis. 166, 639-642.
26. Fink, S. L., and Cookson, B. T. (2007). Pyroptosis and host cell death responses during Salmonella infection. Cell. Microbiol. 9, 2562-2570.
27. Foley, S. L., and Lynne, A. M. (2008). Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J. Anim. Sci. 86, E173-E187.
28. Franchi, L., Amer, A., Body-Malapel, M., Kanneganti, T. D., Ozoren, N., Jagirdar, R., Inohara, N., Vandenabeele, P., Bertin, J., Coyle, A., Grant, E. P., and Núñez, G. (2006). Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in Salmonella-infected macrophages. Nat. Immunol. 7, 576-582.
29. Galan, J. E. (2001). Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17, 53-86.
30. Gallois,A., Klein,J.R., Allen,L.A.,Jones, B. D., and Nauseef, W. M. (2001). Salmonella pathogenicity island 2-encoded type III secretion system mediates exclusion of NADPH oxidase assembly from the phagosomal membrane. J. Immunol. 166, 5741-5748.
31. Gilks, C. F., Brindle, R. J., Newnham, R. S., Watkins, W. M., Waiyaki, P. G., Were, J. B. O., Otieno, L. S., Simani, P. M., Bhatt, S. M., Lule, G. N., Okelo, G. B. A., Brindle, R. J., Newnham, R. S., Gilks, C. F., Warrell, D. A. (1990). Life-threatening bacteraemia in HIV-1 seropositive adults admitted to hospital in Nairobi, Kenya. Lancet 336, 545-549.
32. Goldberg, M. B., and Rubin, R. H. (1988). The spectrum of Salmonella infection. Infect. Dis. Clin. North Am. 2, 571-598.
33. Grob, P., and Guiney, D. G. (1996). In vitro binding of the Salmonella dublin virulence plasmid regulatory protein SpvR to the promoter regions of spvA and spvR. J. Bacteriol. 178, 1813-1820.
34. Grob, P., Kahn, D., and Guiney, D. G. (1997). Mutational characterization of promoter regions recognized by the Salmonella dublin virulence plasmid regulatory protein SpvR. J. Bacteriol. 179, 5398-5406.
35. Gruenewald, R., Blum, S., and Chan, J. (1994). Relationship between human immunodeficiency virus infection and salmonellosis in 20-to 59-year-old residents of New York City. Clin. Infect. Dis. 18, 358-363.
36. Guiney, D. G. (2005). The role of host cell death in Salmonella infections. Curr. Top. Microbiol. Immunol. 289, 131-150.
37. Guiney, D. G., Fang, F. C., Krause, M., and Libby, S. (1994). Plasmidmediated virulence genes in non-typhoid Salmonella serovars. FEMS Microbiol. Lett. 124, 1-9.
38. Guiney, D. G., Fang, F. C., Krause, M., Libby, S., Buchmeier, N. A., and Fierer, J. (1995). Biology and clinical significance of virulence plasmids in Salmonella serovars. Clin. Infect. Dis. 21(SUPPL. 2), S146-S151.
39. Guiney, D. G., and Lesnick, M. (2005). Targeting of the actin cytoskeleton during infection by Salmonella strains. Clin. Immunol. 114, 248-255.
40. Headrick, M. L., Korangy, S., Bean, N. H., Angulo, F. J., Altekruse, S. F., Potter, M. E., and Klontz, K. C. (1998). The epidemiology of raw milk-associated foodborne disease outbreaks reported in the United States, 1973 through 1992. Am. J. Public Health 88, 1219-1221.
41. Heithoff, D. M., Shimp, W. R., Lau, P. W., Badie, G., Enioutina, E. Y., Daynes, R. A., Byrne, B. A., House, J. K., and Mahan, M. J. (2008). Human Salmonella clinical isolates distinct from those of animal origin. Appl. Environ. Microbiol. 74, 1757-1766.
42. Hochmann, H., Pust, S., von Figura, G., Aktories, K., and Barth, H. (2006). Salmonella enterica SpvB ADP-ribosylates actin at position arginine-177-characterization of the catalytic domain within the SpvB protein and a comparison to binary clostridial actin-ADPribosylating toxins. Biochemistry 45, 1271-1277.
43. Hoffman, S. L., Punjabi, N. H., Rockhill, R. C., Sutomo, A., Rivai, A. R., and Pulungsih, S. P. (1984). Duodenal string-capsule culture compared with bone-marrow, blood,and rectal-swab cultures for diagnosing typhoid and paratyphoid fever. J. Infect. Dis. 149, 157-161.
44. Hsu, L. C., Park, J. M., Zhang, K., Luo, J. L., Maeda, S., Kaufman, R. J., Eckmann, L., Guiney, D. G., and Karin, M. (2004). The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 428, 341-345.
45. Jones, T. F., Ingram, L. A., Cieslak, P. R., Vugia, D. J., Tobin-D'Angelo, M., Hurd, S., Medus, C., Cronquist, A., and Angulo, F. J. (2008). Salmonellosis outcomes differ substantially by serotype. J. Infect. Dis. 198, 109-114.
46. Kim, J. M., Eckmann, L., Savidge, T. C., Lowe, D. C., Witthoft, T., and Kagnoff, M. F. (1998). Apoptosis of human intestinal epithelial cells after bacterial invasion. J. Clin. Invest. 102, 1815-1823.
47. Kingsley, R. A., Msefula, C. L., Thomson, N. R., Kariuki, S., Holt, K. E., Gordon, M. A., Harris, D., Clarke, L., Whitehead, S., Sangal, V., Marsh, K., Achtman, M., Molyneux, M. E., Cormican, M., Parkhill, J., MacLennan, C. A., Heyderman, R. S., and Dougan, G. (2009). Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res. 19, 2279-2287.
48. Knodler, L. A., and Steele-Mortimer, O. (2003). Taking possession: biogenesis of the Salmonella-containing vacuole. Traffic 4, 587-599.
49. Krause, M., Fang, F. C., el-Gedaily, A., Libby, S., and Guiney, D. G. (1995). Mutational analysis of SpvR binding to DNA in the regulation of the Salmonella plasmid virulence operon. Plasmid 34, 37-47.
50. Krause, M., Fang, F. C., and Guiney, D. G. (1992). Regulation of plasmid virulence gene expression in Salmonella dublin involves an unusual operon structure. J. Bacteriol. 174, 4482-4489.
51. Krause, M., Roudier, C., Fierer, J., Harwood, J., and Guiney, D. (1991). Molecular analysis of the virulence locus of the Salmonella dublin plasmid pSDL2. Mol. Microbiol. 5, 307-316.
52. Lara-Tejero, M., Sutterwala, F. S., Ogura, Y., Grant, E. P., Bertin, J., Coyle, A. J., Flavell, R. A., and Galán, J. E. (2006). Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203, 1407-1412.
53. Laroux, F. S., Romero, X., Wetzler, L., Engel, P., and Terhorst, C. (2005). Cutting edge: MyD88 controls phagocyte NADPH oxidase function and killing of gramnegative bacteria. J. Immunol. 175, 5596-5600.
54. Lesnick, M. L.,and Guiney, D. G. (2001). The best defense is a good offense - Salmonella deploys an ADPribosylating toxin. Trends Microbiol. 9, 2-4; discussion 4-5.
55. Lesnick, M. L., Reiner, N. E., Fierer, J., and Guiney, D. G. (2001). The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol. Microbiol. 39, 1464-1470.
56. Li, H., Xu, H., Zhou, Y., Zhang, J., Long, C., Li, S., Chen, S., Zhou, J. M., and Shao, F. (2007). The phosphothreonine lyase activity of a bacterial type III effector family. Science 315, 1000-1003.
57. Libby, S. J., Adams, L. G., Ficht, T. A., Allen, C., Whitford, H. A., Buchmeier, N. A., Bossie, S., and Guiney, D. G. (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.
58. Libby, S. J., Lesnick, M., Hasegawa, P., Kurth, M., Belcher, C., Fierer, J., and Guiney, D. G. (2002). Characterization of the spv locus in Salmonella enterica serovar Arizona. Infect. Immun. 70, 3290-3294.
59. Libby, S. J., Lesnick, M., Hasegawa, P., Weidenhammer, E., and Guiney, D. G. (2000). The Salmonella virulence plasmid spv genes are required for cytopathology in human monocytederived macrophages. Cell. Microbiol. 2, 49-58.
60. Ly, K. T., and Casanova, J. E. (2007). Mechanisms of Salmonella entry into host cells. Cell. Microbiol. 9, 2103-2111.
61. Maccready, R. A., Reardon, J. P., and Saphra, I. (1957). Salmonellosis in Massachusetts; a sixteen-year experience. N. Engl. J. Med. 256, 1121-1128.
62. Mastroeni, P., and Menager, N. (2003). Development of acquired immunity to Salmonella. J. Med. Microbiol. 52, 453-459.
63. Mastroeni, P., Vazquez-Torres, A., Fang, F. C., Xu, Y., Khan, S., Hormaeche, C. E., and Dougan, G. (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.
64. Mazurkiewicz, P., Thomas, J., Thompson, J. A., Liu, M., Arbibe, L., Sansonetti, P., and Holden, D. W. (2008). SpvC is a Salmonella effector with phosphothreoninelyase activity on host mitogen-activated protein kinases. Mol. Microbiol. 67, 1371-1383.
65. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M., and Tauxe, R. V. (1999). Food-related illness and death in the United States. Emerg. Infect. Dis. 5, 607-625.
66. Mendelowitz, D. S., Ramstedt, R., Yao, J. S., and Bergan, J. J. (1979). Abdominal aortic salmonellosis. Surgery 85, 514-519.
67. Miao, E. A., Alpuche-Aranda, C. M., Dors, M., Clark, A. E., Bader, M. W., Miller, S. I., and Aderem, A. (2006). Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7, 569-575.
68. Miao, E. A., Mao, D. P., Yudkovsky, N., Bonneau, R., Lorang, C. G., Warren, S. E., Leaf, I. A., and Aderem, A. (2010). Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. U.S.A. 107, 3076-3080.
69. Mittrucker, H. W., and Kaufmann, S. H. (2000). Immune response to infection with Salmonella typhimurium in mice. J. Leukoc. Biol. 67, 457-463.
70. Noskin, G. A., and Clarke, J. T. (1990). Salmonella arizonae bacteremia as the presenting manifestation of human immunodeficiency virus infection following rattlesnake meat ingestion. Rev. Infect. Dis. 12, 514-517.
71. Paesold, G., Guiney, D. G., Eckmann, L., and Kagnoff, M. F. (2002). Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells. Cell. Microbiol. 4, 771-781.
72. Park, J. M., Greten, F. R., Li, Z. W., and Karin, M. (2002). Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297, 2048-2051.
73. Poh, J., Odendall, C., Spanos, A., Boyle, C., Liu, M., Freemont, P., and Holden, D. W. (2007). SteC is a Salmonella kinase required for SPI-2-dependent F-actin remodelling. Cell. Microbiol. 10, 20-30.
74. Raupach, B., Peuschel, S. K., Monack, D. M., and Zychlinsky, A. (2006). Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect. Immun. 74, 4922-4926.
75. Richter-Dahlfors, A., Buchan, A. M., and Finlay, B. B. (1997). Murine salmonellosis 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.
76. Roudier, C., Fierer, J., and Guiney, D. G. (1992). Characterization of translation termination mutations in the spv operon of the Salmonella virulence plasmid pSDL2. J. Bacteriol. 174, 6418-6423.
77. Rytkonen, A., Poh, J., Garmendia, J., Boyle, C., Thompson, A., Liu, M., Freemont, P., Hinton, J. C., and Holden, D. W. (2007). SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl. Acad. Sci. U.S.A. 104, 3502-3507.
78. Saphra, I., and Winter, J. W. (1957). Clinical manifestations of salmonellosis in man; an evaluation of 7779 human infections identified at the New York Salmonella Center. N. Engl. J. Med. 256, 1128-1134.
79. Tamura, M., Itoh, K., Akita, H., Takano, K., and Oku, S. (2006). Identification of an actin-binding site in p47phox an organizer protein of NADPH oxidase. FEBS Lett. 580, 261-267.
80. Tauxe, R. V. (1997). Emerging foodborne diseases: an evolving public health challenge. Emerging Infect. Dis. 3, 425-434.
81. Valle, E., and Guiney, D. G. (2005). Characterization of Salmonellainduced cell death in human macrophage-like THP-1 cells. Infect. Immun. 73, 2835-2840.
82. Vassiloyanakopoulos,A. P.,Okamoto, S., and Fierer, J. (1998). The crucial role of polymorphonuclear leukocytes in resistance to Salmonella dublin infections in genetically susceptible and resistant mice. Proc. Natl. Acad. Sci. U.S.A. 95, 7676-7681.
83. Vazquez-Torres, A., Fantuzzi, G., Edwards, C. K. III, Dinarello, C. A., and Fang, F. C. (2001). Defective localization of the NADPH phagocyte oxidase to Salmonellacontaining phagosomes in tumor necrosis factor p55 receptordeficient macrophages. Proc. Natl. Acad. Sci. U.S.A. 98, 2561-2565.
84. Vazquez-Torres, A., Jones-Carson, J., Baumler, A. J., Falkow, S., Valdivia, R., Brown, W., Le, M., Berggren, R., Parks, W. T., and Fang, F. C. (1999). Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401, 804-808.
85. Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Holden, D. W., Lucia, S. M., Dinauer, M. C., Mastroeni, P., and Fang, F. C. (2000). Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287, 1655-1658.
86. Waterman, S. R., and Holden, D. W. (2003). Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell. Microbiol. 5, 501-511.
87. Werner, S. B., Humphrey, G. L., and Kamei, I. (1979). Association between raw milk and human Salmonella dublin infection. Br. Med. J. 2, 238-241.
88. Zhan, Y., He, D., Newburger, P. E., and Zhou, G. W. (2004). p47(phox) PX domain of NADPH oxidase targets cell membrane via moesin-mediated association with the actin cytoskeleton. J. Cell. Biochem. 92, 795-809.