Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells

Cellular Microbiology

Volumn 4, Issue 11, 2002, Pages 771-781

  Paesold, Günther ^a   Guiney, Donald G ^a   Eckmann, Lars ^a   Kagnoff, Martin F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3;

APOPTOSIS; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CELL FATE; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENE MUTATION; GENETIC CODE; HOST CELL; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; NONHUMAN; PATHOGENICITY; PLASMID; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SALMONELLA ENTERICA; SALMONELLOSIS; SEROTYPE; WILD TYPE;

APOPTOSIS; CASPASE 3; CASPASES; CHLORAMPHENICOL; ENZYME ACTIVATION; EPITHELIAL CELLS; GENES, BACTERIAL; HT29 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; MUTATION; PLASMIDS; PROTEIN SYNTHESIS INHIBITORS; SALMONELLA; VIRULENCE; VIRULENCE FACTORS;

ANIMALIA; BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR DUBLIN;

EID: 0036854564     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-5822.2002.00233.x     Document Type: Review

References (49)

1. Abreu-Martin, M.T., Vidrich, A., Lynch, D.H., and Targan, S.R. (1995) Divergent induction of apoptosis and IL-8 secretion in HT-29 cells in response to TNF-alpha and ligation of Fas antigen. J Immunol 155: 4147-4154.
2. Beninger, P.R., Chikami, G., Tanabe, K., Roudier, C., Fierer, J., and Guiney, D.G. (1988) Physical and genetic mapping of the Salmonella dublin virulence plasmid pSDL2. Relationship to plasmids from other Salmonella strains. J Clin Invest 81: 1341-1347.
3. Beuzon, C.R., Meresse, S., Unsworth, K.E., Ruiz-Albert, J., Garvis, S., Waterman, S. R. et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
4. Bispham, J., Tripathi, B.N., Watson, P.R., and Wallis, T.S. (2001) Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves. Infect Immun 69: 367-377.
5. Brennan, M.A., and Cookson, B.T. (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38: 31-40.
6. Caldwell, A.L., and Gulig, P.A. (1991) The Salmonella typhimurium virulence plasmid encodes a positive regulator of a plasmid-encoded virulence gene. J Bacteriol 173: 7176-7185.
7. Caulin, C., Salvesen, G.S., and Oshima, R.G. (1997) Caspase cleavage of keratin 18 and reorganization of intermediate filaments during epithelial cell apoptosis. J Cell Biol 138: 1379-1394.
8. Chen, C.Y., Eckmann, L., Libby, S.J., Fang, F.C., Okamoto, S., Kagnoff, M.F. et al. (1996) Expression of Salmonella typhimurium rpoS and rpoS-dependent genes in the intracellular environment of eukaryotic cells. Infect Immun 64: 4739-4743.
9. Chikami, G.K., Fierer, J., and Guiney, D.G. (1985) Plasmid-mediated virulence in Salmonella dublin demonstrated by use of a Tn5-oriT construct. Infect Immun 50: 420-424.
10. Cirillo, D.M., Valdivia, R.H., Monack, D.M., and Falkow, S. (1998) Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30: 175-188.
11. De La Cruz, E., and Pollard, T.D. (1994) Transient kinetic analysis of rhodamine phalloidin binding to actin filaments. Biochemistry 33: 14387-14392.
12. Deiwick, J., Nikolaus, T., Erdogan, S., and Hensel, M. (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759-1773.
13. Eckmann, L., Kagnoff, M.F., and Fierer, J. (1993) Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun 61: 4569-4574.
14. Everest, P., Ketley, J., Hardy, S., Douce, G., Khan, S., Shea, J. et al. (1999) Evaluation of Salmonella typhimurium mutants in a model of experimental gastroenteritis. Infect Immun 67: 2815-2821.
15. 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.
16. Fierer, J., and Guiney, D.G. (2001) Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J Clin Invest 107: 775-780.
17. 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.
18. Galan, J.E. (1996) Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 20: 263-271.
19. 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.
20. Galyov, E.E., Wood, M.W., Rosqvist, R., Mullan, P.B., Watson, P.R., Hedges, S., and Wallis, T.S. (1997) A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 25: 903-912.
21. Hensel, M. (2000) Salmonella pathogenicity island 2. Mol Microbiol 36: 1015-1023.
22. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E., and Holden, D.W. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
23. Hensel, M., Shea, J.E., Waterman, S.R., Mundy, R., Nikolaus, T., Banks, G. et al. (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.
24. Iwanaga, T., Han, H., Adachi, K., and Fujita, T. (1993) A novel mechanism for disposing of effete epithelial cells in the small intestine of guinea pigs. Gastroenterology 105: 1089-1097.
25. Janicke, R.U., Sprengart, M.L., Wati, M.R., and Porter, A.G. (1998) Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273: 9357-9360.
26. Jesenberger, V., Procyk, K.J., Yuan, J., Reipert, S., and Baccarini, M. (2000) Salmonella-induced caspase-2 activation in macrophages: a novel mechanism in pathogen-mediated apoptosis. J Exp Med 192: 1035-1046.
27. Jung, H.C., Eckmann, L., Yang, S.K., Panja, A., Fierer, J., Morzycka-Wroblewska, E., and Kagnoff, M.F. (1995) A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 95: 55-65.
28. 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.
29. 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.
30. Leers, M.P., Kolgen, W., Bjorklund, V., Bergman, T., Tribbick, G., Persson, B. et al. (1999) Immunocytochemical detection and mapping of a cytokeratin 18 neo- epitope exposed during early apoptosis. J Pathol 187: 567-572.
31. 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.
32. 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 monocyte-derived macrophages. Cell Microbiol 2: 49-58.
33. Lundberg, U., Vinatzer, U., Berdnik, D., von Gabain, A., and 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.
34. Maloy, S.R., Steward, V.L., and Taylor, R.K. (1996) Genetic analysis of pathogenic bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Press.
35. Meresse, S., Unsworth, K.E., Habermann, A., Griffiths, G., Fang, F., Martinez-Lorenzo, M.J. et al. (2001) Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella. Cell Microbiol 3: 567-577.
36. Miao, E.A., Scherer, C.A., Tsolis, R.M., Kingsley, R.A., Adams, L.G., Baumler, A.J., and Miller, S.I. (1999) Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol Microbiol 34: 850-864.
37. Ochman, H., Soncini, F.C., Solomon, F., and Groisman, E.A. (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 93:7800-7804.
38. Ohl, M.E., and Miller, S.I. (2001) Salmonella: a model for bacterial pathogenesis. Annu Rev Med 52: 259-274.
39. Shea, J.E., Hensel, M., Gleeson, C., and Holden, D.W. (1996) Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci USA 93: 2593-2597.
40. Shea, J.E., Beuzon, C.R., Gleeson, C., Mundy, R., and Holden, D.W. (1999) Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect Immun 67: 213-219.
41. Suarez, M., and Russmann, H. (1998) Molecular mechanisms of Salmonella invasion: the type III secretion system of the pathogenicity island 1. Int Microbiol 1: 197-204.
42. Tezcan-Merdol, D., Nyman, T., Lindberg, U., Haag, F., KochNolte, F., and Rhen, M. (2001) Actin is ADP-ribosylated by the Salmonella enterica virulence- associated protein SpvB. Mol Microbiol 39: 606-619.
43. Valdivia, R.H., and Falkow, S. (1997) Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277: 2007-2011.
44. Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Holden, D.W., Lucia, S.M., Dinauer, M.C. et al. (2000) Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287: 1655-1658.
45. van der Velden, A.W., Lindgren, S.W., Worley, M.J., and Heffron, F. (2000) Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype typhimurium. Infect Immun 68: 5702-5709.
46. Wolf, B.B., and Green, D.R. (1999) Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 274: 20049-20052.
47. Woo, M., Hakem, R., Soengas, M.S., Duncan, G.S., Shahinian, A., Kagi, D. et al. (1998) Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes. Genes Dev 12: 806-819.
48. Wood, M.W., Jones, M.A., Watson, P.R., Hedges, S., Wallis, T.S., and Galyov, E.E. (1998) Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 29: 883-891.
49. Yang, S.K., Eckmann, L., Panja, A., and Kagnoff, M.F. (1997) Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 113: 1214-1223.