Tracking the dynamic interplay between bacterial and host factors during pathogen-induced vacuole rupture in real time

Cellular Microbiology

Volumn 12, Issue 4, 2010, Pages 545-556

  Ray, Katrina ^a,b   Bobard, Alexandre ^a   Danckaert, Anne ^a   Paz Haftel, Irit ^a   Clair, Caroline ^a,c   Ehsani, Soudeh ^a   Tang, Christoph ^b   Sansonetti, Philippe ^a   Van Nhieu, Guy Tran ^a   Enninga, Jost ^a  

^a INSTITUT PASTEUR   (France)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c CENTRE DE RECHERCHE DES CORDELIERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BIOLOGICAL MARKER; GALECTIN 3; HOST FACTOR PROTEIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN PIPB2; PROTEIN SIFA; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM; BACTERIUM TRANSDUCTION; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; FLUORESCENCE RESONANCE ENERGY TRANSFER; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; SALMONELLA;

BACTERIAL PROTEINS; GALECTIN 3; GLYCOPROTEINS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; SALMONELLA; SHIGELLA FLEXNERI; TIME FACTORS; VACUOLES;

BACTERIA (MICROORGANISMS); MAMMALIA; NEGIBACTERIA; SALMONELLA; SHIGELLA FLEXNERI;

EID: 77954289641     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01428.x     Document Type: Article

References (36)

1. Beauregard, K.E., Lee, K.D., Collier, R.J., and Swanson, J.A. (1997) pH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J Exp Med 186: 1159-1163.
2. Beuzon, C.R., Meresse, S., Unsworth, K.E., Ruiz-Albert, J., Garvis, S., Waterman, S.R., et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
3. Bish, S.E., Song, W., and Stein, D.C. (2008) Quantification of bacterial internalization by host cells using a betalactamase reporter strain: Neisseria gonorrhoeae invasion into cervical epithelial cells requires bacterial viability. Microbes Infect 10: 1182-1191.
4. Blocker, A., Gounon, P., Larquet, E., Niebuhr, K., Cabiaux, V., Parsot, C., and Sansonetti, P. (1999) The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147: 683-693.
5. Boucrot, E., Henry, T., Borg, J.P., Gorvel, J.P., and Meresse, S. (2005) The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308: 1174-1178.
6. Charpentier, X., and Oswald, E. (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186: 5486-5495.
7. Conner, S.D., and Schmid, S.L. (2003) Regulated portals of entry into the cell. Nature 422: 37-44.
8. Drecktrah, D., Knodler, L.A., Howe, D., and Steele-Mortimer, O. (2007) Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8: 212-225.
9. Dupont, N., Lacas-Gervais, S., Bertout, J., Paz, I., Freche, B., Van Nhieu, G.T., et al. (2009) Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 6: 137-149.
10. Ehsani, S., Rodrigues, C.D., and Enninga, J. (2009) Turning on the spotlight-using light to monitor and characterize bacterial effector secretion and translocation. Curr Opin Microbiol 12: 24-30.
11. Germane, K.L., Ohi, R., Goldberg, M.B., and Spiller, B.W. (2008) Structural and functional studies indicate that Shigella VirA is not a protease and does not directly destabilize microtubules. Biochemistry 47: 10241-10243.
12. Gouin, E., Gantelet, H., Egile, C., Lasa, I., Ohayon, H., Villiers, V., et al. (1999) A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J Cell Sci 112 (Part 11): 1697-1708.
13. Gruenberg, J., and van der Goot, F.G. (2006) Mechanisms of pathogen entry through the endosomal compartments. Nat Rev Mol Cell Biol 7: 495-504.
14. Henry, R., Shaughnessy, L., Loessner, M.J., Alberti-Segui, C., Higgins, D.E., and Swanson, J.A. (2006a) Cytolysindependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes. Cell Microbiol 8: 107-119.
15. Henry, T., Couillault, C., Rockenfeller, P., Boucrot, E., Dumont, A., Schroeder, N., et al. (2006b) The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc Natl Acad Sci USA 103: 13497-13502.
16. Hermant, D., Menard, R., Arricau, N., Parsot, C., and Popoff, M.Y. (1995) Functional conservation of the Salmonella and Shigella effectors of entry into epithelial cells. Mol Microbiol 17: 781-789.
17. Hume, P.J., McGhie, E.J., Hayward, R.D., and Koronakis, V. (2003) The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology. Mol Microbiol 49: 425-439.
18. Jarry, T.M., and Cheung, A.L. (2006) Staphylococcus aureus escapes more efficiently from the phagosome of a cystic fibrosis bronchial epithelial cell line than from its normal counterpart. Infect Immun 74: 2568-2577.
19. Labigne-Roussel, A.F., Lark, D., Schoolnik, G., and Falkow, S. (1984) Cloning and expression of an afimbrial adhesin (AFA-I) responsible for P blood group-independent, mannose-resistant hemagglutination from a pyelonephritic Escherichia coli strain. Infect Immun 46: 251-259.
20. Mills, E., Baruch, K., Charpentier, X., Kobi, S., and Rosenshine, I. (2008) Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe 3: 104-113.
21. Mounier, J., Popoff, M.R., Enninga, J., Frame, M.C., Sansonetti, P.J., and Van Nhieu, G.T. (2009) The IpaC carboxyterminal effector domain mediates Src-dependent actin polymerization during Shigella invasion of epithelial cells. PLoS Pathog 5: e1000271.
22. Nhieu, G.T., Enninga, J., Sansonetti, P., and Grompone, G. (2005) Tyrosine kinase signaling and type III effectors orchestrating Shigella invasion. Curr Opin Microbiol 8: 16-20.
23. Osiecki, J.C., Barker, J., Picking, W.L., Serfis, A.B., Berring, E., Shah, S., et al. (2001) IpaC from Shigella and SipC from Salmonella possess similar biochemical properties but are functionally distinct. Mol Microbiol 42: 469-481.
24. Paetzold, S., Lourido, S., Raupach, B., and Zychlinsky, A. (2007) Shigella flexneri phagosomal escape is independent of invasion. Infect Immun 75: 4826-4830.
25. Pepperkok, R., and Ellenberg, J. (2006) High-throughput fluorescence microscopy for systems biology. Nat Rev Mol Cell Biol 7: 690-696.
26. Pizarro-Cerda, J., and Cossart, P. (2006) Bacterial adhesion and entry into host cells. Cell 124: 715-727.
27. Portnoy, D.A., Auerbuch, V., and 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.
28. Rabinovich, G.A., and Gruppi, A. (2005) Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease. Parasite Immunol 27: 103-114.
29. Ramsden, A.E., Holden, D.W., and Mota, L.J. (2007) Membrane dynamics and spatial distribution of Salmonellacontaining vacuoles. Trends Microbiol 15: 516-524.
30. Raposo, G., Marks, M.S., and Cutler, D.F. (2007) Lysosomerelated organelles: driving post-Golgi compartments into specialisation. Curr Opin Cell Biol 19: 394-401.
31. Ray, K., Marteyn, B., Sansonetti, P.J., and Tang, C.M. (2009) Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat Rev Microbiol 7: 333-340.
32. Sansonetti, P.J., Ryter, A., Clerc, P., Maurelli, A.T., and Mounier, J. (1986) Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect Immun 51: 461-469.
33. Shaughnessy, L.M., Hoppe, A.D., Christensen, K.A., and Swanson, J.A. (2006) Membrane perforations inhibit lysosome fusion by altering pH and calcium in Listeria monocytogenes vacuoles. Cell Microbiol 8: 781-792.
34. Yoshida, S., Katayama, E., Kuwae, A., Mimuro, H., Suzuki, T., and Sasakawa, C. (2002) Shigella deliver an effector protein to trigger host microtubule destabilization, which promotes Rac1 activity and efficient bacterial internalization. EMBO J 21: 2923-2935.
35. Yoshida, S., Handa, Y., Suzuki, T., Ogawa, M., Suzuki, M., Tamai, A., et al. (2006) Microtubule-severing activity of Shigella is pivotal for intercellular spreading. Science 314: 985-989.
36. Zlokarnik, G., Negulescu, P.A., Knapp, T.E., Mere, L., Burres, N., Feng, L., et al. (1998) Quantitation of transcription and clonal selection of single living cells with beta-lactamase as reporter. Science 279: 84-88.