Apoptotic response of Chang cells to infection with Pseudomonas aeruginosa strains PAK and PAO-I: Molecular ordering of the apoptosis signaling cascade and role of type IV pili

Infection and Immunity

Volumn 71, Issue 5, 2003, Pages 2665-2673

  Jendrossek, Verena ^a   Fillon, Sophie ^a   Belka, Claus ^a   Müller, Ilka ^a   Puttkammer, Beatrice ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; FAS ANTIGEN; INTERFERON; INTERLEUKIN 1BETA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

APOPTOSIS; ARTICLE; BACTERIAL STRAIN; BACTERIUM PILUS; CONJUNCTIVA EPITHELIUM; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOSOL; ENZYME ACTIVATION; ENZYME SUBSTRATE; GRAM NEGATIVE BACTERIUM; GRAM NEGATIVE INFECTION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNE RESPONSE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; WILD TYPE;

ANTIGENS, CD95; APOPTOSIS; CELL LINE; EPITHELIAL CELLS; FIMBRIAE, BACTERIAL; HUMANS; INTERLEUKIN-1; PSEUDOMONAS AERUGINOSA;

EID: 0037408254     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.5.2665-2673.2003     Document Type: Article

References (70)

1. Allewelt, M., F. T. Coleman, M. Grout, G. P. Priebe, and G. B. Pier. 2000. Acquisition of expression of the Pseudomonas aeruginosa ExoU cytotoxin leads to increased bacterial virulence in a murine model of acute pneumonia and systemic spread. Infect. Immun. 68:3998-4004.
2. Apodaca, G., M. Bomsel, R. Lindstedt, J. Engel, D. Frank, K. E. 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.
3. Belka, C., J. Rudner, S. Wesselborg, A. Stepczynska, P. Marini, A. Lepple-Wienhues, H. Faltin, M. Bamberg, W. Budach, and K. Schulze-Osthoff. 2000. Differential role of caspase-8 and BID activation during radiation- and CD95-induced apoptosis. Oncogene 19:1181-1190.
4. Bradley, D. E. 1980. A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can. J. Microbiol 26:146-154.
5. Chi, E., T. Mehl, D. Nunn, and S. Lory. 1991. Interaction of Pseudomonas aeruginosa with A549 pneumocyte cells. Infect. Immun. 59:822-828.
6. Chinnaiyan, A. M., C. G. Tepper, M. F. Seldin, K. O'Rourke, F. C. Kischkel, S. Hellbardt, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271:4961-4965.
7. Comolli, J. C., A. R. Hauser, L. Waite, C. B. Whitchurch, J. S. Mattick, and J. N. Engel. 1999. Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia. Infect. Immun. 67:3625-3630.
8. Comolli, J. C., L. L. Waite, K. E. Mostov, and J. N. Engel. 1999. Pili binding to asialo-GM1 on epithelial cells can mediate cytotoxicity or bacterial internalization by Pseudomonas aeruginosa. Infect. Immun. 67:3207-3214.
9. Cowell, B. A., D. Y. Chen, D. W. Frank, A. J. Vallis, and S. M. Fleiszig. 2000. ExoT of cytotoxic Pseudomonas aeruginosa prevents uptake by corneal epithelial cells. Infect. Immun. 68:403-406.
10. Dacheux, D., B. Toussaint, M. Richard, G. Brochier, J. Croize, and I. Attree. 2000. Pseudomonas aeruginosa cystic fibrosis isolates induce rapid, type III secretion-dependent, but ExoU-independent, oncosis of macrophages and polymorphonuclear neutrophils. Infect. Immun. 68:2916-2924.
11. DiMango, E., A. J. Ratner, R. Bryan, S. Tabibi, and A. Prince. 1998. Activation of NF-kappaB by adherent Pseudomonas aeruginosa in normal and cystic fibrosis respiratory epithelial cells. J. Clin. Investig. 101:2598-2605.
12. Doig, P., T. Todd, P. A. Sastry, K. K. Lee, R. S. Hodges, W. Paranchych, and R. T. Irvin. 1988. Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells. Infect. Immun. 56:1641-1646.
13. Epelman, S., T. F. Bruno, G. G. Neely, D. E. Woods, and C. H. Mody. 2000. Pseudomonas aeruginosa exoenzyme S induces transcriptional expression of proinflammatory cytokines and chemokines. Infect. Immun. 68:4811-4814.
14. Evans, D. J., D. W. Frank, V. Finck-Barbancon, C. Wu, and S. M. Fleiszig. 1998. Pseudomonas aeruginosa invasion and cytotoxicity are independent events, both of which involve protein tyrosine kinase activity. Infect. Immun. 66:1453-1459.
15. Farinha, M. A., B. D. Conway, L. M. Glasier, N. W. Ellert, R. T. Irvin, R. Sherburne, and W. Paranchych. 1994. Alteration of the pilin adhesin of Pseudomonas aeruginosa PAO results in normal pilus biogenesis but a loss of adherence to human pneumocyte cells and decreased virulence in mice. Infect. Immun. 62:4118-4123.
16. Feldman, M., R. Bryan, S. Rajan, L. Scheffier, S. Brunnert, H. Tang, and A. Prince. 1998. Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect. Immun. 66:43-51.
17. Ferrari, D., A. Stepczynska, M. Los, S. Wesselborg, and K. Schulze-Osthoff. 1998. Differential regulation and ATP requirement for caspase-8 and caspase-3 activation during CD95- and anticancer drug-induced apoptosis. J. Exp. Med. 188:979-984.
18. Finck-Barbancon, V., and D. W. Frank. 2001. Multiple domains are required for the toxic activity of Pseudomonas aeruginosa ExoU. J. Bacteriol. 183:4330-4344.
19. Finck-Barbancon, V., J. Goranson, L. Zhu, T. Sawa, J. P. Wiener-Kronish, S. M. Fleiszig, C. Wu, L. Mende-Mueller, and D. W. Frank. 1997. ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol. Microbiol 25:547-557.
20. Fleiszig, S. M., J. P. Wiener-Kronish, H. Miyazaki, V. Vallas, K. E. Mostov, D. Kanada, T. Sawa, T. S. Yen, and D. W. Frank. 1997. Pseudomonas aeruginosa-mediated cytotoxicity and invasion correlate with distinct genotypes at the loci encoding exoenzyme S. Infect. Immun. 65:579-586.
21. Fleiszig, S. M., T. S. Zaidi, and G. B. Pier. 1995. Pseudomonas aeruginosa invasion of and multiplication within corneal epithelial cells in vitro. Infect. Immun. 63:4072-4077.
22. 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.
23. Garrity-Ryan, L., B. Kazmierczak, R. Kowal, J. Comolli, A. Hauser, and J. N. Engel. 2000. The arginine finger domain of ExoT contributes to actin cytoskeleton disruption and inhibition of internalization of Pseudomonas aeruginosa by epithelial cells and macrophages. Infect. Immun. 68:7100-7113.
24. Grassme, H., E. Gulbins, B. Brenner, K. Ferlinz, K. Sandhoff, K. Harzer, F. Lang, and T. F. Meyer. 1997. Acidic sphingomyelinase mediates entry of N. gonorrhoeae into nonphagocytic cells. Cell 91:605-615.
25. Grassme, H., S. Kirschnek, J. Riethmueller, A. Riehle, G. von Kurthy, F. Lang, M. Weller, and E. Gulbins. 2000. CD95/CD95 ligand interactions on epithelial cells in host defense to Pseudomonas aeruginosa. Science 290:527-530.
26. Graupner, S., V. Frey, R. Hashemi, M. G. Lorenz, G. Brandes, and W. Wackernagel. 2000. Type IV pilus genes pilA and pilC of Pseudomonas stutzeri are required for natural genetic transformation, and pilA can be replaced by corresponding genes from nontransformable species. J. Bacteriol. 182:2184-2190.
27. Green, D. R., and J. C. Reed. 1998. Mitochondria and apoptosis. Science 281:1309-1312.
28. Gupta, S. K., R. S. Berk, S. Masinick, and L. D. Hazlett. 1994. Pili and lipopolysaccharide of Pseudomonas aeruginosa bind to the glycolipid asialo GM1. Infect. Immun. 62:4572-4579.
29. Halaas, O., R. Vik, A. Ashkenazi, and T. Espevik. 2000. Lipopolysaccharide induces expression of APO2 ligand/TRAIL in human monocytes and macrophages. Scand. J. Immunol 51:244-250.
30. Hauser, A. R., and J. N. Engel. 1999. Pseudomonas aeruginosa induces type-III-secretion-mediated apoptosis of macrophages and epithelial cells. Infect. Immun. 67:5530-5537.
31. Hornef, M. W., A. Roggenkamp, A. M. Geiger, M. Hogardt, C. A. Jacobi, and J. Heesemann. 2000. Triggering the ExoS regulon of Pseudomonas aeruginosa: a GFP-reporter analysis of exoenzyme (Exo) S, ExoT and ExoU synthesis. Microb. Pathog. 29:329-343.
32. Jendrossek, V., H. Grassme, I. Mueller, F. Lang, and E. Gulbins. 2001. Pseudomonas aeruginosa-induced apoptosis involves mitochondria and stress-activated protein kinases. Infect. Immun. 69:2675-2683.
33. Joza, N., S. A. Susin, E. Daugas, W. L. Stanford, S. K. Cho, C. Y. Li, T. Sasaki, A. J. Elia, H. Y. Cheng, L. Ravagnan, K. F. Ferri, N. Zamzami, A. Wakeham, R. Hakem, H. Yoshida, Y. Y. Kong, T. W. Mak, J. C. Zuniga-Pflucker, G. Kroemer, and J. M. Penninger. 2001. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410:549-554.
34. Kagami, Y., M. Ratliff, M. Surber, A. Martinez, and D. N. Nunn. 1998. Type II protein secretion by Pseudomonas aeruginosa: genetic suppression of a conditional mutation in the pilin-like component XcpT by the cytoplasmic component XcpR. Mol. Microbiol. 27:221-233.
35. Kang, P. J., A. R. Hauser, G. Apodaca, S. M. 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.
36. Kohler, T., L. K. Curty, F. Barja, C. van Delden, and J. C. Pechere. 2000. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182:5990-5996.
37. Leff, J. A., J. W. Baer, M. E. Bodman, J. M. Kirkman, P. F. Shanley, L. M. Patton, C. J. Beehler, J. M. McCord, and J. E. Repine. 1994. Interleukin-1-induced lung neutrophil accumulation and oxygen metabolite-mediated lung leak in rats. Am. J. Physiol. 266:L2-L8.
38. Leist, M., and M. Jaattela. 2001. Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell. Biol. 2:589-598.
39. Li, H., H. Zhu, C. J. Xu, and J. Yuan. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491-501.
40. Li, P., D. Nijhawan, I. Budihardjo, S. M. Srinivasula, M. Ahmad, E. S. Alnemri, and X. Wang. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479-489.
41. Lomholt, J. A., K. Poulsen, and M. Kilian. 2001. Epidemic population structure of Pseudomonas aeruginosa: evidence for a clone that is pathogenic to the eye and that has a distinct combination of virulence factors. Infect. Immun. 69:6284-6295.
42. Lu, H. M., S. T. Motley, and S. Lory. 1997. Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion. Mol. Microbiol. 25:247-259.
43. Luo, X., I. Budihardjo, H. Zou, C. Slaughter, and X. Wang. 1998. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors, Cell 94:481-490.
44. Mattick, J. S., C. B. Whitchurch, and R. A. Alm. 1996. The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa - a review. Gene 179:147-155.
45. Matute-Bello, G., C. W. Frevert, W. C. Liles, M. Nakamura, J. T. Ruzinski, K. Ballman, V. A. Wong, C. Vathanaprida, and T. R. Martin. 2001. Fas/Fas ligand system mediates epithelial injury, but not pulmonary host defenses, in response to inhaled bacteria. Infect. Immun. 69:5768-5776.
46. McIlroy, D., H. Sakahira, R. V. Talanian, and S. Nagata. 1999. Involvement of caspase 3-activated DNase in J. internucleosomal DNA cleavage induced by diverse apoptotic stimuli. Oncogene 18:4401-4408.
47. Medema, J. P., C. Scaffidi, F. C. Kischkel, A. Shevchenko, M. Mann, P. H. Krammer, and M. E. Peter. 1997. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J. 16:2794-2804.
48. Muzio, M., A. M. Chinnaiyan, F. C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J. D. Bretz, M. Zhang, R. Gentz, M. Mann, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817-827.
49. Plotkowski, M. C., A. M. Saliba, S. H. Pereira, M. P. Cervante, and O. Bajolet-Laudinat. 1994. Pseudomonas aeruginosa selective adherence to and entry into human endothelial cells. Infect. Immun. 62:5456-5463.
50. Rajan, S., G. Cacalano, R. Bryan, A. J. Ratner, C. U. Sontich, A. van Heerckeren, P. Davis, and A. Prince. 2000. Pseudomonas aeruginosa induction of apoptosis in respiratory epithelial cells: analysis of the effects of cystic fibrosis transmembrane conductance regulator dysfunction and bacterial virulence factors. Am. J. Respir. Cell Mol. Biol. 23:304-312.
51. Roncero, C., A. Darzins, and M. J. Casadaban. 1990. Pseudomonas aeruginosa transposable bacteriophages D3112 and B3 require pili and surface growth for adsorption. J. Bacteriol. 172:1899-1904.
52. Rudner, J., A. Lepple-Wienhues, W. Budach, J. Berschauer, B. Friedrich, S. Wesselborg, K. Schulze-Osthoff, and C. Belka. 2001. Wild-type, mitochondrial and ER-restricted Bcl-2 inhibit DNA damage-induced apoptosis but do not affect death receptor-induced apoptosis. J. Cell Sci. 114:4161-4172.
53. Saiman, L., K. Ishimoto, S. Lory, and A. Prince. 1990. The effect of piliation and exoproduct expression on the adherence of Pseudomonas aeruginosa to respiratory epithelial monolayers. J. Infect. Dis. 161:541-548.
54. Salvesen, G. S., and V. M. Dixit. 1999. Caspase activation: the induced-proximity model. Proc. Natl. Acad. Sci. USA 96:10964-10967.
55. Sansonetti, P. J., A. Phalipon, J. Arondel, K. Thirumalai, S. Banerjee, S. Akira, K. Takeda, and A. Zychlinsky. 2000. Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12:581-590.
56. Sawa, T., D. B. Corry, M. A. Gropper, M. Ohara, K. Kurahashi, and J. P. Wiener-Kronish. 1997. IL-10 improves lung injury and survival in Pseudomonas aeruginosa pneumonia. J. Immunol. 159:2858-2866.
57. Schultz, M. J., A. W. Rijneveld, S. Florquin, C. K. Edwards, C. A. Dinarello, and T. van der Poll. 2002. Role of interleukin-1 in the pulmonary immune response during Pseudomonas aeruginosa pneumonia. Am. J. Physiol. Lung Cell. Mol. Physiol 282:L285-L290.
58. Schulze-Osthoff, K., A. C. Bakker, B. Vanhaesebroeck, R. Beyaert, W. A. Jacob, and W. Fiers. 1992. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J. Biol. Chem. 267:5317-5323.
59. Schumann, R. R., C. Belka, D. Reuter, N. Lamping, C. J. Kirschning, J. R. Weber, and D. Pfeil. 1998. Lipopolysaccharide activates caspase-1 (interleukin-1-converting enzyme) in cultured monocytic and endothelial cells. Blood 91:577-584.
60. Strasser, A., L. O'Connor, and V. M. Dixit. 2000. Apoptosis signaling. Annu. Rev. Biochem. 69:217-245.
61. Stroh, C., and K. Schulze-Osthoff. 1998. Death by a thousand cuts: an ever increasing list of caspase substrates. Cell Death Differ. 5:997-1000.
62. Susin, S. A., H. K. Lorenzo, N. Zamzami, I. Marzo, B. E. Snow, G. M. Brothers, J. Mangion, E. Jacotot, P. Costantini, M. Loeffler, N. Larochette, D. R. Goodlett, R. Aebersold, D. P. Siderovski, J. M. Penninger, and G. Kroemer. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446.
63. Tang, H. B., E. DiMango, R. Bryan, M. Gambello, B. H. Iglewski, J. B. Goldberg, and A. Prince. 1996. Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infect. Immun. 64:37-43.
64. Thornberry, N. A., and Y. Lazebnik. 1998. Caspases: enemies within. Science 281:1312-1316.
65. Ulich, T. R., L. R. Watson, S. M. Yin, K. Z. Guo, P. Wang, H. Thang, and J. del Castillo. 1991. The intratracheal administration of endotoxin and cytokines. I. Characterization of LPS-induced IL-1 and TNF mRNA expression and the LPS-, IL-1-, and TNF-induced inflammatory infiltrate. Am. J. Pathol. 138:1485-1496.
66. Vasil, M. L. 1986. Pseudomonas aeruginosa: biology, mechanisms of virulence, epidemiology. J. Pediatr. 108:800-805.
67. Xue, M. L., M. D. Willcox, A. Lloyd, D. Wakefield, and A. Thakur. 2001. Regulatory role of IL-lbeta in the expression of IL-6 and IL-8 in human corneal epithelial cells during Pseudomonas aeruginosa colonization. Clin. Exp. Ophthalmol. 29:171-174.
68. Yamaguchi, N., I. R. Kieba, J. Korostoff, P. S. Howard, B. J. Shenker, and E. T. Lally. 2001. Maintenance of oxidative phosphorylation protects cells from Actinobacillus actinomycetemcomitans leukotoxin-induced apoptosis. Cell. Microbiol. 3:811-823.
69. Zamzami, N., P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S. A. Susin, P. X. Petit, B. Mignotte, and G. Kroemer. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:367-377.
70. Zou, H., Y. Li, X. Liu, and X. Wang. 1999. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274:11549-11556.