The arginine finger domain of ExoT contributes to actin cytoskeleton disruption and inhibition of internalization of Pseudomonas aeruginosa by epithelial cells and macrophages

Infection and Immunity

Volumn 68, Issue 12, 2000, Pages 7100-7113

  Garrity Ryan, L ^a   Kazmierczak, B ^a   Kowal, R ^a   Comolli, J ^a,c   Hauser, A ^a,d   Engel, J N ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ARGININE; BACTERIAL PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MUTANT PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ADOLESCENT; ANIMAL CELL; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CELL INVASION; CYTOSKELETON; CYTOTOXICITY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; INTERNALIZATION; LIVER; MACROPHAGE; MOUSE; MUTATION; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA;

ACTINS; ADP RIBOSE TRANSFERASES; ANIMALS; ARGININE; BACTERIAL TOXINS; BIOLOGICAL TRANSPORT; CYTOPLASM; CYTOSKELETON; EXOTOXINS; FEMALE; HELA CELLS; HUMANS; MACROPHAGES; MICE; MICE, INBRED BALB C; PSEUDOMONAS AERUGINOSA; VIRULENCE; VIRULENCE FACTORS;

EID: 0034444645     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.68.12.7100-7113.2000     Document Type: Article

References (55)

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. Black, D. B., and J. B. Bliska. 2000. The RhoGAP activity of the Yersinia cytotoxin YopE is required for antiphagocytic function and virulence. Mol. Microbiol. 37:515-527.
4. Black, D. S., and J. B. Bliska. 1997. Identification of p130Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO J. 16:2730-2744.
5. Chen, L.-M., S. Hobbie, and J. E. Galan. 1996. Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 274:2115-2118.
6. Cowell, B. A., D. Y. Chen, D. W. Frank, A. J. Vallis, and S. M. J. Fleiszig. 2000. ExoT of cytotoxic Pseudomonas aeruginosa prevents uptake by corneal epithelial cells. Infect. Immun. 68:403-406.
7. Drubin, D. G., and W. J. Nelson. 1996. Origins of cell polarity. Cell 84:335-344.
8. Evans, D. J., D. W. Frank, V. Finck-Barbançon, 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.
9. Finck-Barbançon, 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.
10. Finlay, B. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
11. Fleiszig, S. M., T. S. Zaidi, E. L. Fletcher, M. J. Preston, and G. B. Pier. 1994. Pseudomonas aeruginosa invades corneal epithelial cells during experimental infection. Infect. Immun. 62:3485-3493.
12. 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.
13. 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.
14. 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.
15. 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.
16. Fu, Y., and J. E. Galan. 1999. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401:293-297.
17. Geiser, T., B. Kazmierczak, L. Garrity-Ryan, M. Matthay, and J. Engel. Pseudomonas aeruginosa ExoT inhibits in vitro lung epithelial wound repair. Cell. Microbiol., in press.
18. Goehring, U. M., G. Schmidt, K. J. Pederson, K. Aktories, and J. T. Barbiere. 1999. The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases. J. Biol. Chem. 274:36369-36372.
19. Goosney, D. L., J. Celli, B. Kenny, and B. B. Finlay. 1999. Enteropathogenic Escherichia coli inhibits phagocytosis. Infect. Immun. 67:490-495.
20. Guan, K. L., and J. E. Dixon. 1990. Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249:553-556.
21. Hamid, N., A. Gustavsson, K. Andersson, K. McGee, C. Persson, C. E. Rudd, and M. Fallman. 1999. YopH dephosphorylates cas and fyn-binding protein in macrophages. Microb. Pathog. 27:231.
22. Hardt, W.-D., L. M. Chen, K. E. Schubel, X. R. Bustelo, and J. E. Galan. 1998. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93:815-822.
23. Hauser, A., and J. Engel. 1999. Pseudomonas aeruginosa induces type III secretion-mediated apoptosis in macrophages and epithelial cells. Infect. Immun. 67:5530-5537.
24. 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.
25. 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.
26. 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.
27. Isberg, R. R., and S. Falkow. 1985. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 317:262-264.
28. Isberg, R. R., and J. M. Leong. 1990. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60:861-871.
29. Just, I., J. Selzer, M. Wilm, C. von Eichel-Streiber, M. Mann, and K. Aktories. 1995. Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375:500-503.
30. 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.
31. Kazmierczak, B. I., T.-S. Jou, K. Mostov, and J. Engel. Rho-GTPase activity modulates Pseudomonas aeruginosa internalization by epithelial cells. Cell. Microbiol., in press.
32. Kooguchi, K., S. Hashimoto, A. Kobayashi, Y. Kitamura, I. Kudoh, J. Wiener-Kronish, and T. Sawa. 1998. Role of alveolar macrophages in initiation and regulation of inflammation in Pseudomonas aeruginosa pneumonia. Infect. Immun. 66:3164-3169.
33. Krall, R., G. Schmidt, K. Aktories, and J. T. Barbieri. 2000. Pseudomonas aeruginosa ExoT is a Rho GTPase-activating protein. Infect. Immun. 68: 6066-6068.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Lee, V. T., D. M. Anderson, and O. Schneewind. 1998. Targeting of Yersinia Yop proteins into the cytosol of HeLa cells: one-step translocation of YopE across bacterial and eukaryotic membranes is dependent on SycE chaperone. Mol. Microbiol. 28:593-601.
36. Lee, V. T., and O. Schneewind. 1999. Type III machines of pathogenic yersiniae secrete virulence factors into the extracellular milieu. Mol. Microbiol. 31:1619-1629.
37. Liu, P. V. 1966. The roles of various fractions of Pseudomonas aeruginosa in its pathogenesis: identity of the lethal toxins produced in vitro and in vivo. J. Infect. Dis. 116:481-489.
38. Pederson, K. J., A. J. Vallis, K. Aktories, D. W. Frank, and J. T. Barbieri. 1999. The amino-terminal domain of Pseudomonas aeruginosa ExoS disrupts actin filaments via small-molecular-weight GTP-binding proteins. Mol. Microbiol. 32:393-401.
39. Persson, C. N. C., H. Wolf-Watz, and M. Fallman. 1997. The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J. 16:2307-2318.
40. Pier, G. B., M. Grout, and T. S. Zaidi. 1997. Cystic fibrosis transmembrane conductance regulator is an epithelial cell receptor for clearance of Pseudomonas aeruginosa from the lung. Proc. Natl. Acad. Sci. USA 94:12088-12093.
41. Pier, G. B., M. Grout, T. S. Zaidi, J. C. Olsen, L. G. Johnson, J. R. Yankaskas, and J. B. Goldberg. 1996. Role of mutant CFTR in hypersusceptibility of cystic fibrosis patients to lung infections. Science 271:64-67.
42. Rosqvist, R., A. Forsberg, M. Rimpiläinen, T. Bergman, and H. Wolf-Watz. 1990. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol. Microbiol. 4:657-667.
43. Salyers, A. A., and D. D. Whitt. 1994. Bacterial pathogenesis: a molecular approach. ASM Press, Washington, D.C.
44. Sawa, T., D. Corry, M. Gropper, M. Ohara, K. Kurahashi, and J. Wiener-Kronish. 1997. IL-10 improves lung injury and survival in Pseudomonas aeruginosa pneumonia. J. Immunol. 159:2858-2866.
45. Sawa, T., M. Ohara, K. Kurahashi, S. Twining, D. Frank, O. Doroques, T. Long, M. Gropper, and J. Wiener-Kronish. 1998. In vitro cellular cytotoxicity predicts Pseudomonas aeruginosa virulence in lung infections. Infect. Immun. 66:3242-3249.
46. Schweizer, H. P., and T. T. Hoang. 1995. An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158: 15-22.
47. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1:784-791.
48. Taylor, R. K., V. L. Miller, D. B. Furlong, and J. J. Mekalanos. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. USA 84:2822-2837.
49. Vallis, A. J., V. Finck-Barbançon, T. L. Yahr, and D. W. Frank. 1999. Biological effects of Pseudomonas aeruginosa type III-secreted proteins on CHO cells. Infect. Immun. 67:2040-2044.
50. Vallis, A. J., T. L. Yahr, J. T. Barbieri, and D. W. Frank. 1999. Regulation of ExoS production and secretion by Pseudomonas aeruginosa in response to tissue culture conditions. Infect. Immun. 67:914-920.
51. von Pawel-Rammingen, U. M., V. Telpnev, G. Schmidt, K. Aktories, H. Wolf-Watz, and R. Rosqvist. 2000. GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol. Microbiol. 36:737-748.
52. West, S. E., H. P. Schweizer, C. Dall, A. K. Sample, and L. J. Runyen-Janecky. 1994. Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148:81-86.
53. Yahr, T., L. M. Mende-Mueller, M. B. Friese, and D. W. Frank. 1997. Identification of type III secreted products of the Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 179:7165-7168.
54. 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.
55. Zhang, B., Y. Zhang, C. C. Collins, D. I. Johnson, and Y. Zheng. 1999. A built-in arginine finger triggers the self-stimulatory GTPase-activating activity of rho family GTPases. J. Biol. Chem. 274:2609-2612.