A novel PhoP-regulated locus encoding the cytolysin ClyA and the secreted invasin TaiA of Salmonella enterica serovar Typhi is involved in virulence

Microbiology

Volumn 155, Issue 2, 2009, Pages 477-488

  Faucher, Sébastien P ^a,b   Forest, Chantal ^a   Béland, Maxime ^a   Daigle, France ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLYSIN; INVASIN; PHOP PROTEIN; ADHESIN; APXI TOXIN, BACTERIA; BACTERIAL PROTEIN; HEMOLYSIN; PERFORIN; PHOP PROTEIN, BACTERIA;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL INVASION; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIUM CELL; GENE DELETION; GENE FUNCTION; GENE LOCUS; GENE MUTATION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MACROPHAGE; NONHUMAN; OPERON; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN SECRETION; REGULATORY MECHANISM; SALMONELLA ENTERICA; CELL LINE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HELA CELL; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROTEIN TRANSPORT; SALMONELLA TYPHI; TYPHOID FEVER; VIRULENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI; TAIA;

ADHESINS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE; EPITHELIAL CELLS; HELA CELLS; HEMOLYSIN PROTEINS; HUMANS; MACROPHAGES; OPERON; PERFORIN; PROTEIN TRANSPORT; SALMONELLA TYPHI; TYPHOID FEVER; VIRULENCE;

EID: 62249137129     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.022988-0     Document Type: Article

References (68)

1. Abromaitis, S., Faucher, S., Beland, M., Curtiss, R., III & Daigle, F. (2005). The presence of the tet gene from cloning vectors impairs Salmonella survival in macrophages. FEMS Microbiol Lett 242, 305-312.
2. Aguirre, A., Cabeza, M. L., Spinelli, S. V., McClelland, M., Garcia Vescovi, E. & Soncini, F. C. (2006). PhoP-induced genes within Salmonella pathogenicity island 1. J Bacteriol 188, 6889-6898.
3. Altier, C. (2005). Genetic and environmental control of Salmonella invasion. J Microbiol 43, 85-92.
4. Ansong, C., Yoon, H., Norbeck, A. D., Gustin, J. K., McDermott, J. E., Mottaz, H. M., Rue, J., Adkins, J. N., Heffron, F. & Smith, R. D. (2008). Proteomics analysis of the causative agent of typhoid fever. J Proteome Res 7, 546-557.
5. Basso, H., Rharbaoui, F., Staendner, L. H., Medina, E., Garcia-Del Portillo, F. & Guzman, C. A. (2002). Characterization of a novel intracellularly activated gene from Salmonella enterica serovar Typhi. Infect Immun 70, 5404-5411.
6. Belden, W. J. & Miller, S. I. (1994). Further characterization of the PhoP regulon: identification of new PhoP-activated virulence loci. Infect Immun 62, 5095-5101.
7. Beuzon, C. R., Banks, G., Deiwick, J., Hensel, M. & Holden, D. W. (1999). pH-dependent secretion of SseB, a product of the SPI-2 type III secretion systemof Salmonella typhimurium. Mol Microbiol 33, 806-816.
8. Bijlsma, J. J. & Groisman, E. A. (2005). The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Mol Microbiol 57, 85-96.
9. Buchmeier, N., Bossie, S., Chen, C. Y., Fang, F. C., Guiney, D. G. & Libby, S. J. (1997). SlyA, a transcriptional regulator of Salmonella typhimurium, is required for resistance to oxidative stress and is expressed in the intracellular environment of macrophages. Infect Immun 65, 3725-3730.
10. Bustamante, V. H., Martinez, L. C., Santana, F. J., Knodler, L. A., Steele-Mortimer, O. & Puente, J. L. (2008). HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proc Natl Acad Sci U S A 105, 14591-14596.
11. Chen, L. M., Kaniga, K. & Galan, J. E. (1996). Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21, 1101-1115.
12. Connor, B. A. & Schwartz, E. (2005). Typhoid and paratyphoid fever in travellers. Lancet Infect Dis 5, 623-628.
13. Coombes, B. K., Brown, N. F., Valdez, Y., Brumell, J. H. & Finlay, B. B. (2004). Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J Biol Chem 279, 49804-49815.
14. Coombes, B. K., Wickham, M. E., Brown, N. F., Lemire, S., Bossi, L., Hsiao, W. W., Brinkman, F. S. & Finlay, B. B. (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. Deiwick, J., Nikolaus, T., Erdogan, S. & Hensel, M. (1999). Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31, 1759-1773.
16. Dozois, C. M., Daigle, F. & Curtiss, R., III (2003). Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc Natl Acad Sci U S A 100, 247-252.
17. Elsinghorst, E. A. (1994). Measurement of invasion by gentamicin resistance. Methods Enzymol 236, 405-420.
18. Faucher, S. P., Porwollik, S., Dozois, C. M., McClelland, M. & Daigle, F. (2006). Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc Natl Acad Sci U S A 103, 1906-1911.
19. Fields, P. I., Swanson, R. V., Haidaris, C. G. & Heffron, F. (1986). Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U S A 83, 5189-5193.
20. Fink, S. L. & Cookson, B. T. (2006). Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8, 1812-1825.
21. Galan, J. E. (1999). Interaction of Salmonella with host cells through the centisome 63 type III secretion system. Curr Opin Microbiol 2, 46-50.
22. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84, 165-174.
23. Gardy, J. L., Laird, M. R., Chen, F., Rey, S., Walsh, C. J., Ester, M. & Brinkman, F. S. (2005). PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21, 617-623.
24. Groisman, E. A. (2001). The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183, 1835-1842.
25. Grunberg-Manago, M. (1999). Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annu Rev Genet 33, 193-227.
26. Hensel, M., Shea, J. E., Waterman, S. R., Mundy, R., Nikolaus, T., Banks, G., Vazquez-Torres, A., Gleeson, C., Fang, F. C. & Holden, D. W. (1998). Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30, 163-174.
27. Hersh, D., Monack, D. M., Smith, M. R., Ghori, N., Falkow, S. & Zychlinsky, A. (1999). The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96, 2396-2401.
28. Hone, D. M., Harris, A. M., Chatfield, S., Dougan, G. & Levine, M. M. (1991). Construction of genetically defined double aro mutants of Salmonella typhi. Vaccine 9, 810-816.
29. Kaniga, K., Delor, I. & Cornelis, G. (1991). A wide host range suicide vector for improving reverse genetics in Gram negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109, 137-141.
30. Kaniga, K., Compton, M. S., Curtiss, R., III & Sundaram, P. (1998). Molecular and functional characterization of Salmonella enterica serovar Typhimurium poxA gene: effect on attenuation of virulence and protection. Infect Immun 66, 5599-5606.
31. Kuhle, V. & Hensel, M. (2004). Cellular microbiology of intracellular Salmonella enterica: functions of the type III secretion system encoded by Salmonella pathogenicity island 2. Cell Mol Life Sci 61, 2812-2826.
32. Lai, X. H., Arencibia, I., Johansson, A., Wai, S. N., Oscarsson, J., Kalfas, S., Sundqvist, K. G., Mizunoe, Y., Sjöstedt, A. & Uhlin, B. E. (2000). Cytocidal and apoptotic effects of the ClyA protein from Escherichia coli on primary and cultured monocytes and macrophages. Infect Immun 68, 4363-4367.
33. 2+-responsive PhoP-PhoQ regulon in Salmonella enterica. J Bacteriol 185, 6287-6294.
34. -ΔΔCT method. Methods 25, 402-408.
35. Lostroh, C. P. & Lee, C. A. (2001). The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect 3, 1281-1291.
36. Ludwig, A., von Rhein, C., Bauer, S., Huttinger, C. & Goebel, W. (2004). Molecular analysis of cytolysin A (ClyA) in pathogenic Escherichia coli strains. J Bacteriol 186, 5311-5320.
37. Lundberg, U., Vinatzer, U., Berdnik, D., von Gabain, A. & Baccarini, M. (1999). Growth phase-regulated induction of Salmonella-induced macrophage apoptosis correlates with transient expression of SPI-1 genes. J Bacteriol 181, 3433-3437.
38. Marcus, S. L., Brumell, J. H., Pfeifer, C. G. & Finlay, B. B. (2000). Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect 2, 145-156.
39. Monack, D. M., Mueller, A. & Falkow, S. (2004). Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol 2, 747-765.
40. Navarre, W. W., Halsey, T. A., Walthers, D., Frye, J., McClelland, M., Potter, J. L., Kenney, L. J., Gunn, J. S., Fang, F. C. & Libby, S. J. (2005). Co-regulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol Microbiol 56, 492-508.
41. Norte, V. A., Stapleton, M. R. & Green, J. (2003). PhoP-responsive expression of the Salmonella enterica serovar Typhimurium slyA gene. J Bacteriol 185, 3508-3514.
42. O'Callaghan, D. & Charbit, A. (1990). High efficiency transformation of Salmonella typhimurium and Salmonella typhi by electroporation. Mol Gen Genet 223, 156-158.
43. Ochman, H. & Groisman, E. A. (1996). Distribution of pathogenicity islands in Salmonella spp. Infect Immun 64, 5410-5412.
44. Ochman, H., Soncini, F. C., Solomon, F. & Groisman, E. A. (1996). Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci U S A 93, 7800-7804.
45. Oscarsson, J., Mizunoe, Y., Li, L., Lai, X. H., Wieslander, A. & Uhlin, B. E. (1999). Molecular analysis of the cytolytic protein ClyA (SheA) from Escherichia coli. Mol Microbiol 32, 1226-1238.
46. Oscarsson, J., Westermark, M., Lofdahl, S., Olsen, B., Palmgren, H., Mizunoe, Y., Wai, S. N. & Uhlin, B. E. (2002). Characterization of a pore-forming cytotoxin expressed by Salmonella enterica serovars Typhi and Paratyphi A. Infect Immun 70, 5759-5769.
47. Parkhill, J., Dougan, G., James, K. D., Thomson, N. R., Pickard, D., Wain, J., Churcher, C., Mungall, K. L., Bentley, S. D. & other authors (2001). Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413, 848-852.
48. Parry, C. M., Hien, T. T., Dougan, G., White, N. J. & Farrar, J. J. (2002). Typhoid fever. N Engl J Med 347, 1770-1782.
49. Parsons, D. A. & Heffron, F. (2005). sciS, an icmF homolog in Salmonella enterica serovar Typhimurium, limits intracellular replication and decreases virulence. Infect Immun 73, 4338-4345.
50. Porwollik, S., Boyd, E. F., Choy, C., Cheng, P., Florea, L., Proctor, E. & McClelland, M. (2004). Characterization of Salmonella enterica subspecies I genovars by use of microarrays. J Bacteriol 186, 5883-5898.
51. Prost, L. R. & Miller, S. I. (2008). The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell Microbiol 10, 576-582.
52. Richter-Dahlfors, A., Buchan, A. M. & 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.
53. Rosenshine, I., Ruschkowski, S. & Finlay, B. B. (1994). Inhibitors of cytoskeletal function and signal transduction to study bacterial invasion. Methods Enzymol 236, 467-476.
54. Santos, R. L., Zhang, S., Tsolis, R. M., Kingsley, R. A., Adams, L. G. & Baumler, A. J. (2001). Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 3, 1335-1344.
55. Schwan, W. R., Huang, X. Z., Hu, L. & Kopecko, D. J. (2000). Differential bacterial survival, replication, and apoptosis-inducing ability of Salmonella serovars within human and murine macrophages. Infect Immun 68, 1005-1013.
56. Shi, Y., Cromie, M. J., Hsu, F. F., Turk, J. & Groisman, E. A. (2004). PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B. Mol Microbiol 53, 229-241.
57. Snavely, M. D., Gravina, S. A., Cheung, T. T., Miller, C. G. & Maguire, M. E. (1991). Magnesium transport in Salmonella typhimurium. Regulation of mgtA and mgtB expression. J Biol Chem 266, 824-829.
58. Song, H., Kong, W., Weatherspoon, N., Qin, G., Tyler, W., Turk, J., Curtiss, R., III & Shi, Y. (2008). Modulation of the regulatory activity of bacterial two-component systems by SlyA. J Biol Chem 283, 28158-28168.
59. Spano, S., Ugalde, J. E. & Galan, J. E. (2008). Delivery of a Salmonella typhi exotoxin from a host intracellular compartment. Cell Host Microbe 3, 30-38.
60. Sukhan, A., Kubori, T., Wilson, J. & Galan, J. E. (2001). Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex. J Bacteriol 183, 1159-1167.
61. Tierrez, A. & Garcia-del Portillo, F. (2005). New concepts in Salmonella virulence: the importance of reducing the intracellular growth rate in the host. Cell Microbiol 7, 901-909.
62. Tzokov, S. B., Wyborn, N. R., Stillman, T. J., Jamieson, S., Czudnochowski, N., Artymiuk, P. J., Green, J. & Bullough, P. A. (2006). Structure of the hemolysin E (HlyE, ClyA, and SheA) channel in its membrane-bound form. J Biol Chem 281, 23042-23049.
63. Uzzau, S., Figueroa-Bossi, N., Rubino, S. & Bossi, L. (2001). Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 98, 15264-15269.
64. von Rhein, C., Hunfeld, K. P. & Ludwig, A. (2006). Serologic evidence for effective production of cytolysin A in Salmonella enterica serovars Typhi and Paratyphi A during human infection. Infect Immun 74, 6505-6508.
65. von Rhein, C., Bauer, S., Lopez Sanjurjo, E. J., Benz, R., Goebel, W. & Ludwig, A. (2009). ClyA cytolysin from Salmonella: distribution within the genus, regulation of expression by SlyA, and pore-forming characteristics. Int J Med Microbiol 299, 21-35.
66. Wai, S. N., Lindmark, B., Soderblom, T., Takade, A., Westermark, M., Oscarsson, J., Jass, J., Richter-Dahlfors, A., Mizunoe, Y. & Uhlin, B. E. (2003). Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115, 25-35.
67. Wang, R. F. & Kushner, S. R. (1991). Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100, 195-199.
68. Waterman, S. R. & Holden, D. W. (2003). Functions and effectors of the Salmonella pathogenicity island 2 Type III secretion system. Cell Microbiol 5, 501-511.