Cytolysin-dependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes

Cellular Microbiology

Volumn 8, Issue 1, 2006, Pages 107-119

  Henry, Rebecca ^a   Shaughnessy, Lee ^a   Loessner, Martin J ^b   Alberti Segui, Christine ^c   Higgins, Darren E ^c   Swanson, Joel A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b ETH ZURICH   (Switzerland)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYAN FLUORESCENT PROTEIN; CYTOLYSIN; IMMUNOGLOBULIN G; LISTERIOLYSIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; RAB PROTEIN; RAB7 PROTEIN; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIAL VIRULENCE; BACTERIOLYSIS; CELL COMPARTMENTALIZATION; CELL FUSION; CELL HETEROGENEITY; CELL LABELING; CELL MATURATION; CELL ORGANELLE; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; ENDOSOME; LISTERIA MONOCYTOGENES; LYSOSOME; MACROPHAGE; MEMBRANE MARKER; MOUSE; NONHUMAN; OPSONIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL COMPARTMENTATION; CYTOSOL; ENDOPEPTIDASES; GREEN FLUORESCENT PROTEINS; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; INTRACELLULAR MEMBRANES; LISTERIA MONOCYTOGENES; LUMINESCENT PROTEINS; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MACROPHAGES; MICE; MICROSCOPY, FLUORESCENCE; PHOSPHATIDYLINOSITOL PHOSPHATES; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; VACUOLES;

ANIMALIA; BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

EID: 33644824480     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2005.00604.x     Document Type: Article

References (38)

1. Alvarez-Dominguez, C., Stahl, P. D. (1999) Increased expression of Rab5a correlates directly with accelerated maturation of Listeria monocytogenes phagosomes. J Biol Chem 274: 11459-11462.
2. Alvarez-Dominguez, C., Roberts, R., Stahl, P. D. (1997) Internalized Listeria monocytogenes modulates intracellular trafficking and delays maturation of the phagosome. J Cell Sci 110: 731-743.
3. Beauregard, K. E., Lee, K. D., Collier, R. J., Swanson, J. A. (1997) pH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J Exp Med 186: 1159-1163.
4. de Chastellier, C., Berche, P. (1994) Fate of Listeria monocytogenes in murine macrophages: Evidence for simultaneous killing and survival of intracellular bacteria. Infect Immun 62: 543-553.
5. Conte, M. P., Petrone, G., Longhi, C., Valenti, P., Morelli, R., Superti, F., Seganti, L. (1996) The effects of inhibitors of vacuolar acidification on the release of Listeria monocytogenes from phagosomes of Caco-2 cells. J Med Microbiol 44: 418-424.
6. Cossart, P., Lecuit, M. (1998) Interactions of Listeria monocytogenes with mammalian cells during entry and actin-based movement: Bacterial factors, cellular ligands and signaling. EMBO J 17: 3797-3806.
7. Dancz, C. E., Haraga, A., Portnoy, D. A., Higgins, D. E. (2002) Inducible control of virulence gene expression in Listeria monocytogenes: Temporal requirement of listeriolysin O during intracellular infection. J Bacteriol 184: 5935-5945.
8. Deretic, V., Fratti, R. A. (1999) Mycobacterium tuberculosis phagosome. Mol Microbiol 31: 1603-1609.
9. Desjardins, M., Huber, L. A., Parton, R. G., Griffiths, G. (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 124: 677-688.
10. Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J. M., et al. (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19: 4577-4588.
11. Glomski, I. J., Gedde, M. M., Tsang, A. W., Swanson, J. A., Portnoy, D. A. (2002) The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J Cell Biol 156: 1029-1038.
12. Glomski, I. J., Decatur, A. L., Portnoy, D. A. (2003) Listeria monocytogenes mutants that fail to compartmentalize listeriolysin O activity are cytotoxic, avirulent, and unable to evade host extracellular defenses. Infect Immun 71: 6754-6765.
13. Gordon, A. H., Hart, P. D., Young, M. R. (1980) Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature 286: 79-80.
14. Hakansson, A., Bentley, C. C., Shakhnovic, E. A., Wessels, M. R. (2005) Cytolysin-dependent evasion of lysosomal killing. Proc Natl Acad Sci USA 102: 5192-5197.
15. Hashim, S., Mukherjee, K., Raje, M., Basu, S. K., Mukhopadhyay, A. (2000) Live Salmonella modulate expression of Rab proteins to persist in a specialized compartment and escape transport to lysosomes. J Biol Chem 275: 16281-16288.
16. Henry, R. M., Hoppe, A. D., Joshi, N., Swanson, J. A. (2004) The uniformity of phagosome maturation in macrophages. J Cell Biol 164: 185-194.
17. Higgins, D. E., Buchrieser, C., Freitg, N. E. (2005) Genetic tools for use with Listeria monocytogenes. In Gram-Positive Pathogens, 2nd edition. Fischetti, V. A., Novick, R. P., Ferretti, J. J., Portnoy, D. A., Rood, J. I. (eds). New York: American Society for Microbiology Press (in press).
18. Hoppe, A. D., Swanson, J. A. (2004) Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol Biol Cell 15: 3509-3519.
19. Jones, S., Portnoy, D. A. (1994) Intracellular growth of bacteria. Methods Enzymol 236: 463-467.
20. Lauer, P., Chow, M. Y., Loessner, M. J., Portnoy, D. A., Calendar, R. (2002) Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 184: 4177-4186.
21. Loessner, M. J., Kramer, K., Ebel, F., Scherer, S. (2002) C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol Microbiol 44: 335-349.
22. Mellman, I., Fuchs, R., Helenius, A. (1986) Acidification of the endocytic and exocytic pathways. Annu Rev Biochem 55: 663-700.
23. Myers, J. T., Tsang, A. W., Swanson, J. A. (2003) Localized reactive oxygen and nitrogen intermediates inhibit escape of Listeria monocytogenes from vacuoles in activated macrophages. J Immunol 171: 5447-5453.
24. Peters, C., von Figura, K. (1994) Biogenesis of lysosomal membranes. FEBS Lett 346: 146-150.
25. 2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature 396: 575-580.
26. Portnoy, D. A., Jacks, P. S., Hinrichs, D. J. (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.
27. Portnoy, D. A., Tweten, R. K., Kehoe, M., Bielecki, J. (1992) Capacity of listeriolysin O, streptolysin O, and perfringolysin O to mediate growth of Bacillus subtilis mamalian within cells. Infect Immun 60: 2710- 2717.
28. Portnoy, D. A., Auerbuch, V., Glomski, I. J. (2002) The cell biology of Listeria monocytogenes infection: The intersection of bacterial pathogenesis and cell-mediated immunity. J Cell Biol 158: 409- 414.
29. Prada-Delgado, A., Carrasco-Marin, E., Bokoch, G. M., Alvarez-Dominguez, C. (2001) Interferon-gamma listericidal action is mediated by novel Rab5a functions at the phagosomal environment. J Biol Chem 276: 19059-19065.
30. Prada-Delgado, A., Carrasco-Marin, E., Pena-Macarro, C., Del Cerro-Vadillo, E., Fresno-Escudero, M., Leyva-Cobian, F., Alvarez-Dominguez, C. (2005) Inhibition of Rab5a exchange activity is a key step for Listeria monocytogenes survival. Traffic 6: 252-265.
31. Pryor, P. R., Mullock, B. M., Bright, N. A., Gray, S. R., Luzio, J. P. (2000) The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J Cell Biol 149: 1053-1062.
32. Roberts, R. L., Barbieri, M. A., Ullrich, J., Stahl, P. D. (2000) Dynamics of rab5 activation in endocytosis and phagocytosis. J Leukoc Biol 68: 627-632.
33. Shen, A., Higgins, D. E. (2005) The 5′ untranslated region-mediated enhancement of intracellular listeriolysin O production is required for Listeria monocytogenes pathogenicity. Mol Microbiol 57: 1460-1473.
34. Shiloh, M. U., MacMicking, J. D., Nicholson, S., Brause, J. E., Potter, S., Marino, M., et al. (1999) Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10: 29-38.
35. Stenmark, H., Aasland, R., Driscoll, P. C. (2002) The phosphatidylinositol 3-phosphate-binding FYVE finger. FEBS Lett 513: 77-84.
36. Tweten, R. K., Parker, M. W., Johnson, A. E. (2001) The cholesterol-dependent cytolysins. Curr Top Microbiol Immunol 257: 15-33.
37. van Weert, A. W., Dunn, K. W., Gueze, H. J., Maxfield, F. R., Stoorvogel, W. (1995) Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 130: 821-834.
38. Zimmer, M. (2002) Green fluorescent protein (GFP): Applications, structure, and related photophysical behavior. Chem Rev 102: 759-781.