Surface-associated Hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model

Infection and Immunity

Volumn 66, Issue 10, 1998, Pages 4602-4610

  Garduño, Rafael A ^a   Garduño, Elizabeth ^a   Hoffman, Paul S ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN; HEAT SHOCK PROTEIN 60;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; DOSE RESPONSE; ENDOSOME; HELA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LEGIONELLA PNEUMOPHILA; PRIORITY JOURNAL; STRAIN DIFFERENCE;

EID: 0031692318     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.66.10.4602-4610.1998     Document Type: Article

References (58)

1. Abu Kwaik, Y. 1996. The phagosome containing Legionella pneumophila within the protozoan Hartmanella vermiformis is surrounded by the rough endoplasmic reticulum. Appl. Environ. Microbiol. 62:2022-2028.
2. Abu Kwaik, Y., B. S. Fields, and C. Engleberg. 1994. Protein expression by the protozoan Hartmanella vermiformis upon contact with its bacterial parasite Legionella pneumophila. Infect. Immun. 62:1860-1866.
3. Andrews, H. L., J. P. Vogel, and R. R. Isberg. 1998. Identification of linked Legionella pneumophila genes essential for intracellular growth and evasion of the endocytic pathway, Infect. Immun. 66:950-958.
4. Berber, K. H., J. J. Merriam, and R. R. Isberg. 1994. Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol. Microbiol. 14:809-822.
5. Bozue, J. A., and W. Johnson. 1996. Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion. Infect. Immun. 64:668-673.
6. Butler, C. A. 1988. Molecular and biological characterization of the Legionella pneumophila major outer membrane protein. Ph.D. dissertation. Department of Microbiology and Immunology, University of Tennessee. Memphis. Tenn.
7. Butler, C. A., and P. S. Hoffman. 1990. Characterization of a major 31-kilodalton peptidoglycan-bound protein of Legionella pneumophila. J. Bacteriol. 172:2401-2407.
8. Butler, C. A., E. D. Street, T. P. Hatch, and P. S. Huffman. 1985. Disulfide-bonded outer membrane proteins in the genus Legionella. Infect. Immun. 48:14-18.
9. Cirillo, J. D., S. Falkow, and L. S. Tompkins. 1994. Growth of Legionella pneumophila in Acanthamoeba castellani enhances invasion. Infect. Immun. 62:3254-3261.
10. de Chastellier, C., and L. Thilo. 1997. Phagosome maturation and fusion with lysosomes in relation to surface property and size of the phagocytic particle. Eur. J. Cell Biol. 74:49-62.
11. Dramsi, S., I. Biswas, E. Maguin, L. Braun, P. Mastroeni, and P. Cossart. 1995. Entry of Listeria monocytogenes into hepatocytes requires expression of InlB, a surface protein of the internalin multigene family. Mol. Microbiol. 16:251-261.
12. Dreyfus, L. A. 1987. Virulence associated ingestion of Legionella pneumophila. Microb. Pathog. 3:45-52.
13. Ensgraber, M., and M. Loos. 1992. A 66-kilodalton heat shock protein of Salmonella typhimurium is responsible for binding of the bacterium to intestinal mucus. Infect. Immun. 60:3072-3078.
14. Fernandez, R. C., S. H. S. Lee, D. Haldane, R. Sumarah, and K. R. Rozee. 1989. Plaque assay for virulent Legionella pneumophila. J. Clin. Microbiol. 27:1961-1964.
15. Fernandez, R. C., S. M. Logan, S. H. S. Lee, and P. S. Hoffman. 1996. Elevated levels of Legionella pneumophila stress protein Hsp60 early in infection of human monocytes and L929 cells correlate with virulence. Infect. Immun. 64:1968-1976.
16. Fields, B. S. 1993. Legionella and protozoa: interaction of a pathogen and its natural host, p. 129-136. In J. M. Barbaree, R. F. Breiman, and A. P. Dufour (ed.), Legionella: current status and emerging perspectives. American Society of Microbiology, Washington, D.C.
17. Fields, B. S. 1996. The molecular ecology of legionellae. Trends Microbiol. 4:286-290.
18. Frisk, A., C. A. Ison, and T. Lagergård. 1998. GroEL heat shock protein of Haemophilus ducreyi: association with cell surface and capacity to bind to eukaryotic cells. Infect. Immun. 66:1252-1257.
19. Gaillard, J.-L., P. Berche, C. Frehel, E. Gouin, and P. Cossart. 1991. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 65:1127-1141.
20. Gao, L.-Y., O. S. Harb, and Y. Abu Kwaik. 1997. Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionary distant hosts, mammalian and protozoan cells. Infect. Immun. 65:4738-4746.
21. Garduño, R. A., G. Faulkner, M. A. Trevors, N. Vats, and P. S. Huffman. 1998. Immunolocalization of Hsp60 in Legionella pneumophila. J. Bacteriol, 180:505-513.
22. Garduño, R. A., F. D. Quinn, and P. S. Hoffman. 1998. HeLa cells as a model to study the invasiveness and biology of Legionella pneumophila. Can. J. Microbiol. 44:430-440.
23. Gibson, F. C., III, A. O. Tzianabos, and F. G. Rodgers. 1994. Adherence of Legionella pneumophila to U-937 cells, guinea pig alveolar macrophages, and MRC-5 cells by a novel, complement-independent binding mechanism. Can. J. Microbiol. 40:865-872.
24. Grassmé, 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. Harb, O. S., C. Venkataraman, B. J. Haack, L.-Y. Gao, and Y. Abu Kwaik. 1998. Heterogeneity in the attachment and uptake mechanisms of the Legionnaires' disease bacterium, Legionella pneumophila, by protozoan hosts. Appl. Environ. Microbiol. 64:126-132.
26. Hartmann, E., and C. Lingwood. 1997. Brief heat shock treatment induces a long-lasting alteration in the glycolipid receptor binding specificity and growth rate of Haemophilus influenzae. Infect. Immun. 65:1729-1733.
27. Helsel, L. O., W. F. Bibb, C. A. Butler, P. S. Hoffman, and R. M. McKinney. 1988. Recognition of a genus-wide antigen of Legionella by a monoclonal antibody. Curr. Microbiol. 16:201-208.
28. Hess, J., I. Gentschev, G. Szalay, C. Ladel, A. Bubert, W. Goebel, and S. H. E. Kaufmann. 1995. Listeria monocytogenes p60 supports host cell invasion by and in vivo survival of attenuated Salmonella typhimurium. Infect. Immun. 63:2047-2053.
29. Huffman, P. S. 1997. Invasion of eukaryotic cells by Legionella pneumophila: a common strategy for all hosts? Can. J. Infect. Dis. 8:139-146.
30. Hoffman, P. S., C. A. Butler, and F. D. Quinn. 1998. Cloning and temperature-dependent expression in Escherichia coli of a Legionella pneumophila gene coding for a genus-common 60-kilodalton antigen. Infect. Immun. 57:1731-1739.
31. Hoffman, P. S., L. Houston, und C. A. Butler. 1990. Legionella pneumophila htpAB heat shock operon: nucleotide sequence and expression of the 60- kilodalton antigen in L. pneumophila-infected HeLa cells. Infect. Immun. 58:3380-3387.
32. Hoffman, P. S., M. Ripley, and R. Weeratna. 1992. Cloning and nucleotide sequence of a gene (ompS) encoding the major outer membrane protein of Legionella pneumophila. J. Bacteriol. 174:914-920.
33. Huffman, P. S., J. H. Seyer, and C. A. Butler. 1992. Molecular characterization of the 28- and 31-kilodalton subunits of the Legionella pneumophila major outer membrane protein. J. Bacteriol. 174:908-913.
34. Horwitz, M. A. 1987. Characterization of an avirulent mutant of Legionella pneumophila that survive but do not multiply within human monocytes. J. Exp. Med. 166:1310-1328.
35. Huesca, M., S. Borgia, P. S. Hoffman, and C. A. Lingwood. 1996. Acidic pH changes receptor binding specificity of Helicobacter pylori: a binary adhesion model in which surface heat shock (stress) proteins mediate sulfatide recognition in gastric colonization. Infect. Immun. 64:2643-2648.
36. Isberg, R. R. 1989. Mammalian cell adhesion functions and cellular penetration of enteropathogenic Yersinia species. Mol. Microbiol. 3:1449-1453.
37. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
38. Maganti, S., M. M. Pierce, A. Hoffmaster, and F. G. Rodgers. 1998. The role of sialic acid in opsonin-dependent and opsonin-independent adhesion of Listeria monocytogenes to murine peritoneal macrophages. Infect. Immun. 66:620-626.
39. Menard, R., M.-C. Prevost, P. Gounon, P. Sansonetti, and C. Dehio. 1996. The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells. Proc. Natl. Acad. Sci. USA 93:1254-1258.
40. Michl, J., M. M. Pieczonka, J. C. Unkeless, and S. C. Silverstein. 1979. Effects of immobilized immune complexes on Fc- and complement-receptor function in resident and thioglycollate-elicited mouse peritoneal macrophages. J. Exp. Med. 150:607-621.
41. Mody, C. H., R. Paine III, M. S. Shahrabadi, R. H. Simon, E. Pearlman, B. I. Eisenstein, and G. B. Toews. 1993. Legionella pneumophila replicates within rat alveolar epithelial cells. J. Infect. Dis. 167:1138-1145.
42. Oldham, L. J., and F. G. Rodgers. 1985. Adhesion, penetration and intracellular replication of Legionella pneumophila: an in vitro model of pathogenesis. J. Gen. Microbiol. 131:697-706.
43. Pascule, A. W., J. C. Feeley, R. J. Gibson, L. G. Cordes, R. L. Meyerowitz, C. M. Patton, G. W. Gorman, C. L. Carmack, J. W. Ezzell, and J. N. Dowling. 1980, Pittsburgh pneumonia agent: direct isolation from human lung tissue. J. Infect. Dis. 141:727-732.
44. Pau, C.-P., B. B. Plikaytis, G. M. Carlone, and I. M. Warner. 1988. Purification, partial characterization, and seroreactivity of a genuswide 60-kilodalton Legionella protein antigen. J. Clin. Microbiol. 26:67-71.
45. Peterson, E. M., X. Cheng, S. Pal, and L. M. de la Maza. 1993. Effects of antibody isotype and host cell type on in vitro neutralization of Chlamydia trachomatis. Infect. Immun. 61:498-503.
46. Retzlaff, C., Y. Yamamoto, S. Okubo, P. S. Hoffman, H. Friedman, and T. W. Klein. 1996. Legionella pneumophila heat-shock protein-induced increase of interleukin-1β mRNA involves protein kinase C signalling in macrophages. Immunology 89:281-288.
47. Rowbotham, T. J. 1986. Current views on the relationships between amoebae, legionellae and man. Isr. J. Med. Sci. 22:678-689.
48. Roy, C. R., K. H. Berger, and R. R. Isberg. 1998, Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28:663-674.
49. Sadosky, A. B., L. A. Wiater, and H. A. Shuman. 1993. Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect. Immun. 61:5361-5373.
50. Segal, G., Purcell, M., and H. A. Shuman. 1998. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl. Acad. Sci. 95:1669-1674.
51. Speert, D. P., S. D. Wright, S. C. Silverstein, and B. Mah. 1988. Functional characterization of macrophage receptors for in vitro phagocytosis of unopsonized Pseudomonas aeruginosa. J. Clin. Investig. 82:872-879.
52. Spriggs, D. R. 1987. Legionella, microbial ecology, and inconspicuous consumption. J. Infect. Dis. 155:1086-1087.
53. Swanson, M. S., and R. R. Isberg. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63:3609-3620.
54. Swanson, M. S., and R. R. Isberg. 1996. Identification of Legionella pneumophila mutants that have aberrant intracellular fates. Infect. Immun. 64:2585-2594.
55. Venkataraman, C., B. J. Haack, S. Bondada, and Y. Abu Kwaik. 1997. Identification of a Gal/GalNAc lectin in the protozoan Hartmanella vermiformis as a potential receptor for attachment and invasion by the Legionnaires' disease bacterium, Legionella pneumophila. J. Exp. Med. 186:537-547.
56. Vogel, J. P., H. L. Andrews, S. K. Wong, and R. R. Isberg. 1998. Conjugative transfer by the virulence system of Legionella pneumophila. Science (Washington, D.C.) 279:873-876.
57. Weeratna, R., D. A. Stamler, P. H. Edelstein, M. Ripley, T. Marrie, D. Hoskin, and P. S. Hoffman. 1994. Human and guinea pig immune responses to Legionella pneumophila protein antigens OmpS and Hsp60. Infect. Immun. 62:3454-3462.
58. Young, R. A., and T. J. Elliot. 1989. Stress proteins, infection, and immune surveillance. Cell 59:5-8.