Division of the Salmonella-containing vacuole and depletion of acidic lysosomes in Salmonella-infected host cells are novel strategies of Salmonella enterica to avoid lysosomes

Infection and Immunity

Volumn 78, Issue 1, 2010, Pages 68-79

  Eswarappa, Sandeepa M ^a   Negi, Vidya Devi ^a   Chakraborty, Sangeeta ^a   Sagar, B K Chandrasekhar ^b   Chakravortty, Dipshikha ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOSOME ENZYME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL REPRODUCTION; BACTERIAL SURVIVAL; CELL DIVISION; CELL VACUOLE; CONTROLLED STUDY; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLOSIS; SPLEEN CELL;

ANIMALS; CELL LINE; ENDOCYTOSIS; HYDROGEN-ION CONCENTRATION; LYSOSOMES; MACROPHAGES; MICE; MUTATION; SALMONELLA ENTERICA; VACUOLES; VANADATES;

EID: 73449133763     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00668-09     Document Type: Article

References (42)

1. Abrahams, G. L., P. Muller, and M. Hensel. 2006. Functional dissection of SseF, a type III effector protein involved in positioning the salmonella-containing vacuole. Traffic 7:950-965.
2. Alexander, J., and K. Vickerman. 1975. Fusion of host cell secondary lysosomes with the parasitophorous vacuoles of Leishmania mexicana-infected macrophages. J. Protozool. 22:502-508.
3. Andersson, H., T. Baechi, M. Hoechl, and C. Richter. 1998. Autofluorescence of living cells. J. Microsc. 191:1-7.
4. Buchmeier, N. A., and F. Heffron. 1991. Inhibition of macrophage phagosomelysosome fusion by Salmonella typhimurium. Infect. Immun. 59:2232-2238.
5. Burkhardt, J. K., C. J. Echeverri, T. Nilsson, and R. B. Vallee. 1997. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139:469-484.
6. Canonico, P. G., and J. W. Bird. 1969. The use of acridine orange as a lysosomal marker in rat skeletal muscle. J. Cell Biol. 43:367-371.
7. Carrol, M. E., P. S. Jackett, V. R. Aber, and D. B. Lowrie. 1979. Phagolysosome formation, cyclic adenosine 3′:5′-monophosphate and the fate of Salmonella typhimurium within mouse peritoneal macrophages. J. Gen. Microbiol. 110:421-429.
8. Chakravortty, D., I. Hansen-Wester, and M. Hensel. 2002. Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J. Exp. Med. 195:1155-1166.
9. Deretic, V., S. Singh, S. Master, J. Harris, E. Roberts, G. Kyei, A. Davis, S. de Haro, J. Naylor, H. H. Lee, and I. Vergne. 2006. Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell Microbiol. 8:719-727.
10. Drecktrah, D., L. A. Knodler, D. Howe, and O. Steele-Mortimer. 2007. Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8:212-225.
11. Drose, S., K. U. Bindseil, E. J. Bowman, A. Siebers, A. Zeeck, and K. Altendorf. 1993. Inhibitory effect of modified bafilomycins and concanamycins on P- and V-type adenosinetriphosphatases. Biochemistry 32:3902-3906.
12. Duclos, S., and M. Desjardins. 2000. Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol. 2:365-377.
13. Eswarappa, S. M., K. K. Panguluri, M. Hensel, and D. Chakravortty. 2008. The yejABEF operon of Salmonella confers resistance to antimicrobial peptides and contributes to its virulence. Microbiology 154:666-678.
14. Garcia-del Portillo, F., and B. B. Finlay. 1995. Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J. Cell Biol. 129:81-97.
15. Garcia-del Portillo, F., C. Nunez-Hernandez, B. Eisman, and J. Ramos-Vivas. 2008. Growth control in the Salmonella-containing vacuole. Curr. Opin. Microbiol. 11:46-52.
16. Garvis, S. G., C. R. Beuzon, and D. W. Holden. 2001. A role for the PhoP/Q regulon in inhibition of fusion between lysosomes and Salmonella-containing vacuoles in macrophages. Cell Microbiol. 3:731-744.
17. Gibbons, I. R., M. P. Cosson, J. A. Evans, B. H. Gibbons, B. Houck, K. H. Martinson, W. S. Sale, and W. J. Tang. 1978. Potent inhibition of dynein adenosinetriphosphatase and of the motility of cilia and sperm flagella by vanadate. Proc. Natl. Acad. Sci. USA 75:2220-2224.
18. Guignot, J., E. Caron, C. Beuzon, C. Bucci, J. Kagan, C. Roy, and D. W. Holden. 2004. Microtubule motors control membrane dynamics of Salmonella-containing vacuoles. J. Cell Sci. 117:1033-1045.
19. Hamon, M., H. Bierne, and P. Cossart. 2006. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4:423-434.
20. Hansen-Wester, I., and M. Hensel. 2001. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 3:549-559.
21. Haraga, A., M. B. Ohlson, and S. I. Miller. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:53-66.
22. Hashim, S., K. Mukherjee, M. Raje, S. K. Basu, and A. Mukhopadhyay. 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.
23. Holden, D. W. 2002. Trafficking of the Salmonella vacuole in macrophages. Traffic 3:161-169.
24. Hu, L., and D. J. Kopecko. 1999. Campylobacter jejuni 81-176 associates with microtubules and dynein during invasion of human intestinal cells. Infect. Immun. 67:4171-4182.
25. Ishibashi, Y., and T. Arai. 1990. Specific inhibition of phagosome-lysosome fusion in murine macrophages mediated by Salmonella typhimurium infection. FEMS Microbiol. Immunol. 2:35-43.
26. Kim, K. J., S. J. Elliott, F. Di Cello, M. F. Stins, and K. S. Kim. 2003. The K1 capsule modulates trafficking of E. coli-containing vacuoles and enhances intracellular bacterial survival in human brain microvascular endothelial cells. Cell Microbiol. 5:245-252.
27. Knodler, L. A., and B. B. Finlay. 2001. Salmonella and apoptosis: to live or let die? Microbes Infect. 3:1321-1326.
28. Knodler, L. A., and O. Steele-Mortimer. 2003. Taking possession: biogenesis of the Salmonella-containing vacuole. Traffic 4:587-599.
29. Kurz, D. J., S. Decary, Y. Hong, and J. D. Erusalimsky. 2000. Senescence-associated (beta)-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J. Cell Sci. 113: 3613-3622.
30. Marsman, M., I. Jordens, C. Kuijl, L. Janssen, and J. Neefjes. 2004. Dyneinmediated vesicle transport controls intracellular Salmonella replication. Mol. Biol. Cell 15:2954-2964.
31. Monack, D. M., B. Raupach, A. E. Hromockyj, and S. Falkow. 1996. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93:9833-9838.
32. Moriyama, Y., T. Takano, and S. Ohkuma. 1982. Acridine orange as a fluorescent probe for lysosomal proton pump. J. Biochem. 92:1333-1336.
33. Ogawa, M., and C. Sasakawa. 2006. Intracellular survival of Shigella. Cell Microbiol. 8:177-184.
34. Oh, Y. K., C. Alpuche-Aranda, E. Berthiaume, T. Jinks, S. I. Miller, and J. A. Swanson. 1996. Rapid and complete fusion of macrophage lysosomes with phagosomes containing Salmonella typhimurium. Infect. Immun. 64:3877-3883.
35. Parks, D. R., V. M. Bryan, V. T. Oi, and L. A. Herzenberg. 1979. Antigenspecific identification and cloning of hybridomas with a fluorescence-activated cell sorter. Proc. Natl. Acad. Sci. USA 76:1962-1966.
36. Saftig, P., and J. Klumperman. 2009. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat. Rev. Mol. Cell Biol. 10:623-635.
37. Sansonetti, P. J. 2004. War and peace at mucosal surfaces. Nat. Rev. Immunol. 4:953-964.
38. Shea, J. E., M. Hensel, C. Gleeson, and D. W. Holden. 1996. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93:2593-2597.
39. Steele-Mortimer, O. 2008. The Salmonella-containing vacuole: moving with the times. Curr. Opin. Microbiol. 11:38-45.
40. Varadi, A., L. I. Johnson-Cadwell, V. Cirulli, Y. Yoon, V. J. Allan, and G. A. Rutter. 2004. Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynaminrelated protein-1. J. Cell Sci. 117:4389-4400.
41. Vazquez-Torres, A., Y. Xu, J. Jones-Carson, D. W. Holden, S. M. Lucia, M. C. Dinauer, P. Mastroeni, and F. C. Fang. 2000. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287: 1655-1658.
42. Zelenin, A. V. 1966. Fluorescence microscopy of lysosomes and related structures in living cells. Nature 212:425-426.