Pseudomonas aeruginosa induces type-III-secretion-mediated apoptosis of macrophages and epithelial cells

Infection and Immunity

Volumn 67, Issue 10, 1999, Pages 5530-5537

  Hauser, Alan R ^a,c   Engel, Joanne N ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIN; PROTEIN DERIVATIVE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIUM ISOLATE; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIUM CELL; HOST SUSCEPTIBILITY; HUMAN; HUMAN CELL; INTERNALIZATION; MACROPHAGE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; STRAIN DIFFERENCE;

EID: 0032879168     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.10.5530-5537.1999     Document Type: Article

References (42)

1. Apodaca, G., M. Bomsel, R. Lindstedt, J. Engel, D. Frank, K. Mostov, and J. Wiener-Kronish. 1995. Characterization of Pseudomonas aeruginosa-induced MDCK cell injury: glycosylation defective host cells are resistant to bacterial killing. Infect. Immun. 63:1541-1551.
2. Bjorn, M. J., O. R. Pavlovskis, M. R. Thompson, and B. H. Iglewski. 1979. Production of exoenzyme S during Pseudomonas aeruginosa infection in burned mice. Infect. Immun. 24:837-842.
3. Buja, L. M., M. L. Eigenbrodt, and E. H. Eigenbrodt. 1993. Apoptosis and necrosis: basic types and mechanisms of cell death. Arch. Pathol. Lab. Med. 117:1208-1214.
4. Chen, L. M., K. Kone, and J. E. Galan. 1996. Salmonella spp. are cytotoxic for cultured macrophages. Mol. Microbiol. 21:1101-1115.
5. Coburn, J., and D. Frank. 1999. Macrophages and epithelial cells respond differently to the Pseudomonas aeruginosa type III secretion system. Infect. Immun. 67:3151-3154.
6. Finck-Barbancon, V., J. Goranson, L. Zhu, T. Sawa, J. P. Wiener-Kronish, S. M. J. Fleiszig, C. Wu, L. Mende-Mueller, and D. Frank. 1997. ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol. Microbiol. 25:547-557.
7. Finck-Barbancon, V., T. L. Yahr, and D. W. Frank. 1998. Identification and characterization of SpcU, a chaperone required for efficient secretion of the ExoU cytotoxin. J. Bacteriol. 180:6224-6231.
8. Fleiszig, S. M. J., J. P. Wiener-Kronish, H. Miyazaki, V. Vallas, K. Mostov, D. Kanada, T. Sawa, T. S. B. Yen, and D. Frank. 1997. Pseudomonas aeruginosa-mediated cytotoxicity and invasion correlate with distinct genotypes at the loci encoding exoenzyme S. Infect. Immun. 65:579-586.
9. Fleiszig, S. M. J., T. S. Zaidi, M. J. Preston, M. Grout, D. J. Evans, and G. B. Pier. 1996. Relationship between cytotoxicity and corneal epithelial cell invasion by clinical isolates of Pseudomonas aeruginosa. Infect. Immun. 64: 2288-2294.
10. Frank, D. 1997. The exoenzyme S regulon of Pseudomonas aeruginosa. Mol. Microbiol. 26:621-629.
11. Frank, D. W., G. Nair, and H. Schweizer. 1994. Construction and characterization of chromosomal insertional mutations of the Pseudomonas aeruginosa exoenzyme S trans-regulatory locus. Infect. Immun. 62:554-563.
12. Frithz-Lindsten, E., Y. Du, R. Rosqvist, and A. Forsberg. 1997. Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol. Microbiol. 25:1125-1139.
13. Guichon, A., and A. Zychlinsky. 1997. Clinical isolates of Shigella species induce apoptosis in macrophages. J. Infect. Dis. 175:470-473.
14. Hauser, A. R., P. J. Kang, and J. Engel. 1998. PepA, a novel secreted protein of Pseudomonas aeruginosa, is necessary for cytotoxicity and virulence. Mol. Microbiol. 27:807-818.
15. Hauser, A. R., P. J. Kang, S. J. M. Fleiszig, K. Mostov, and J. Engel. 1998. Defects in type III secretion correlate with internalization of Pseudomonas aeruginosa by epithelial cells. Infect. Immun. 66:1413-1420.
16. Hersh, D., D. M. Monack, M. R. Smith, N. Ghori, S. Falkow, and A. Zychlinsky. 1999. The Salmonella invasin SipB induces macrophage apoptosis by binding caspase-1. Proc. Natl. Acad. Sci. USA 96:2396-2401.
17. Holloway, B. W., V. Krishnapillai, and A. F. Morgan. 1979. Chromosomal genetics of Pseudomonas. Microbiol. Rev. 43:73-102.
18. Iglewski, B. H., J. Sadoff, M. J. Bjorn, and E. S. Maxwell. 1978. Pseudomonas aeruginosa exoenzyme S: an adenosine diphosphate ribosyltransferase distinct from toxin A. Proc. Natl. Acad. Sci. USA 75:3211-3215.
19. Islam, D., B. Veress, P. K. Bardhan, A. A. Lindberg, and B. Christensson. 1997. In situ characterization of inflammatory responses in the rectal mucosae of patients with shigellosis. Infect. Immun. 65:739-749.
20. Kang, P. J., A. R. Hauser, G. Apodaca, S. Fleiszig, J. Wiener-Kronish, K. Mostov, and J. N. Engel. 1997. Identification of Pseudomonas aeruginosa genes required for epithelial cell injury. Mol. Microbiol. 24:1249-1262.
21. Kudoh, I., J. P. Wiener-Kronish, S. Hashimoto, J.-F. Pittet, and D. Frank. 1994. Exoproduct secretions of P. aeruginosa strains influence severity of alveolar epithelial injury. Am. J. Physiol. 267(5 Pt. 1):L551-L556.
22. Liu, P. V. 1966. The roles of various fractions of Pseudomonas aeruginosa in its pathogenesis. II. Effects of lecithinase and protease. J. Infect. Dis. 116: 112-116.
23. Majno, G., and I. Joris. 1995. Apoptosis, oncosis, and necrosis: an overview of cell death. Am. J. Pathol. 146:3-15.
24. Mills, S. D., A. Boland, M.-P. Sory, P. van der Smissen, C. Kerbourch, B. B. Finlay, and G. R. Cornells. 1997. Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc. Natl. Acad. Sci. USA 94:12638-12643.
25. Monack, D. M., J. Mecsas, N. Ghori, and S. Falkow. 1997. Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc. Natl. Acad. Sci. USA 94:10385-10390.
26. Morimoto, H., and B. Bonavida. 1992. Diphtheria toxin and Pseudomonas A toxin-mediated apoptosis: ADP-ribosylation of elongation factor-2 is required for DNA fragmentation and cell lysis and synergy with tumor necrosis factor-α. J. Immunol. 149:2089-2094.
27. Olson, J. C., E. M. McGuffie, and D. W. Frank. 1997. Effects of differential expression of the 49-kilodalton exoenzyme S by Pseudomonas aeruginosa on cultured eukaryotic cells. Infect. Immun. 65:248-256.
28. Pahl, H. L., B. Krauss, K. Schulze-Osthoff, T. Decker, E. B.-M. Traenckner, M. Vogt, C. Myers, T. Parks, P. Warring, A. Muhlbacher, A.-P. Czernilofsky, and P. Baeuerle. 1996. The immunosuppressive fungal metabolite gliotoxin specifically inhibits transcription factor NF-κB. J. Exp. Med. 183:1829-1840.
29. Palmer, L. E., S. Hobbie, J. E. Galan, and J. B. Bliska. 1998. YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNR-alpha production and downregulation of the MAP kinases p38 and JNK. Mol. Microbiol. 27:953-965.
30. Pederson, K. J., and J. T. Barbieri. 1998. Intracellular expression of the ADP-ribosyltransferase domain of Pseudomonas aeruginosa exoenzyme S is cytotoxic to eukaryotic cells. Mol. Microbiol. 30:751-759.
31. Pollack, M. 1998. Infections due to Pseudomonas species and related organisms, p. 943-950. In A. S. Fauci, E. Braunwald, K. J. Isselbacher, J. D. Wilson, J. B. Martin, D. L. Kasper, S. L. Hauser, and D. L. Longo (ed.), Harrison's principles of internal medicine, 14th ed. McGraw-Hill, New York, N.Y.
32. Salyers, A. A., and D. D. Whitt. 1994. Bacterial pathogenesis: a molecular approach. ASM Press, Washington, D.C.
33. Sawa, T., T. Yahr, M. Ohara, K. Kurahashi, M. A. Gropper, J. P. Wiener-Kronish, and D. W. Frank. 1999. Active and passive immunization with the Pseudomonas V antigen protects against type III intoxication and lung injury. Nat. Med. 5:392-398.
34. Schesser, K., A.-K. Spiik, J.-M. Dukuzumuranyi, M. F. Neurath, S. Petersson, and H. Wolf-Watz. 1998. The yopJ locus is required for Yersinia-mediated inhibition of NF-κB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol. Microbiol. 28:1067-1079.
35. Tanenbaum, S. W. 1978. Cytochalasin: biochemical and cell biological aspects. North-Holland, Amsterdam, The Netherlands.
36. Waring, P., R. D. Eichner, A. Mullbacher, and A. Sjaarda. 1988. Gliotoxin induces apoptosis in macrophages unrelated to its antiphagocytic properties. J. Biol. Chem. 263:18493-18499.
37. Whitchurch, C. B., and J. S. Mattick. 1994. Characterization of a gene, pilU, required for twitching motility but not phage sensitivity in Pseudomonas aeruginosa. Mol. Microbiol. 13:1079-1081.
38. Yahr, T. L., J. T. Barbieri, and D. W. Frank. 1996. Genetic relationship between the 53- and 49-kilodalton forms of exoenzyme S from Pseudomonas aeruginosa. J. Bacteriol. 178:1412-1419.
39. Yahr, T. L., A. J. Vallis, M. K. Hancock, J. T. Barbieri, and D. W. Frank. 1998. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc. Natl. Acad. Sci. USA 95:13899-13904.
40. Zychlinsky, A., B. Kenny, R. Menard, M.-C. Prevost, I. B. Holland, and P. J. Sansonetti. 1994. IpaB mediates macrophage apoptosis induced by Shigella flexneri. Mol. Microbiol. 11:619-627.
41. Zychlinsky, A., M.-C. Prevost, and P. J. Sansonetti. 1992. Shigella flexneri induces apoptosis in infected macrophages. Nature 358:167-169.
42. Zychlinsky, A., K. Thirumalai, J. Arondel, J. R. Cantey, A. O. Aliprantis, and P. J. Sansonetti. 1996. In vivo apoptosis in Shigella flexneri infections. Infect. Immun. 64:5357-5365.