The ClpC ATPase of Listeria monocytogenes is a general stress protein required for virulence and promoting early bacterial escape from the phagosome of macrophages

Molecular Microbiology

Volumn 27, Issue 6, 1998, Pages 1235-1245

  Rouquette, Corinne ^a   De Chastellier, Chantal ^a   Nair, Shamila ^a   Berche, Patrick ^a  

^a INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL ENZYME; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 100; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CELL SURVIVAL; CONTROLLED STUDY; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; STRESS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; CELL DIVISION; HEAT-SHOCK PROTEINS; LISTERIA MONOCYTOGENES; LIVER; MACROPHAGES; MICE; MICROSCOPY, ELECTRON; MUTAGENESIS; PHAGOSOMES; SPLEEN; TEMPERATURE; VIRULENCE;

EID: 0031884730     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.00775.x     Document Type: Article

References (49)

1. Abshire, K.Z., and Neidhardt, F.C. (1993) Analysis of proteins synthesized by Salmonella typhimurium during growth within a host macrophage. J Bacteriol 175: 3734-3743.
2. Biswas, L., Gruss, A., Ehrlich, S.D., and Maguin, E. (1993) High-efficiency gene inactivation and replacement system for Gram-positive bacteria. J Bacteriol 175: 3628-3635.
3. Bohne, J., Sokolovic, Z., and Goebel, W. (1994) Transcriptional regulation of prfA and prfA-regulated virulence genes in Listeria monocytogenes. Mol Microbiol 11: 1141-1150.
4. Britton, W.J., Roche, P.W., and Winter, N. (1994) Mechanisms of persistence of mycobacteria. Trends Microbiol 2: 284-288.
5. Buchmeier, N.A., and Heffron, F. (1990) Induction of Salmonella stress proteins upon infection of macrophages. Science 248: 730-732.
6. de Chastellier, C., and Berche, P. (1994) Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria. Infect Immun 62: 543-553.
7. Elzer, P.H., Phillips, R.X., Kovach, M.E., Peterson, K.M., and Roop, II, R.M. (1994) Characterization and genetic complementation of a Brucella abortus high-temperature-requirement A (htrA) deletion mutant. Infect Immun 62: 4135-4139.
8. Gaillard, J.L., Berche, P., Mounier, J., Richard, S., and Sansonetti, P. (1987) In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun 55: 2822-2829.
9. Gaillard, J.L., Jaubert, F., and Berche, P. (1996) The in/AB locus mediates the entry of Listeria monocytogenes into hepatocytes in vivo. J Exp Med 183: 359-369.
10. Geoffroy, C., Gaillard, J.L., Alouf, J.E., and Berche, P. (1987) Purification characterization and toxicity of sulfhydryl-activated hemolysin (listeriolysin O) from Listeria monocytogenes. Infect Immun 55: 1641-1646.
11. Geoffroy, C., Raveneau, J., Beretti, J.L., Lecroisey, A., Alouf, J.E., and Berche, P. (1991) Purification and characterization of an extracellular 29-kDa phosphatidylcholine-phospholipase C from Listeria monocytogenes. Infect Immun 59: 2382-2388.
12. Gottesman, S., Squires, C., Pichersky, E., Carrington, M., Hobbs, M., Mateick, J., et al. (1990) Conservation of the regulatory unit for the ClpA ATP-dependent proteases in prokaryotes and eukaryotes. Proc Natl Acad Sci USA 87: 3513-3517.
13. Gray, M.L., and Killinger, A.H. (1966) Listeria monocytogenes and listeric infections. Bacteriol Rev 30: 309-382.
14. Hanawa, T., Yamamoto, T., and Kamiya, S. (1995) Listeria monocytogenes can grow in macrophages without the aid of proteins induced by environmental stresses. Infect Immun 63: 4595-4599.
15. Headley, V.L., and Payne, S.M. (1990) Differential protein expression by Shigella flexneri in intracellular and extracellular environments. Proc Natl Acad Sci USA 87: 4179-4183.
16. Johnson, K.I., Charles, I., Dougan, G., Pickard, D., O'Gaora, P., Costa, G., et al. (1991) The role of a stress-response protein on Salmonella typhimurium virulence. Mol Microbiol 5: 401-407.
17. Köhler, S., Teyssier, J., Cloeckaert, A., Rouot, B., and Liautard, J.P. (1996) Participation of the molecular chaperone DnaK in the intracellular growth of Brucella suis within U937-derived phagocytes. Mol Microbiol 20: 701-712.
18. Krüger, E., Völker, U., and Hecker, M. (1994) Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. J Bacteriol 176: 3360-3367.
19. Kwaik, Y.A., Eisenstein, B.I., and Engleberg, N.C. (1993) Phenotypic modulation by Legionella pneumophila upon infection of macrophages. Infect Immun 61: 1320-1329.
20. Lathigra, R.B., Butcher, P.D., Garbe, T.R., and Young, D.B. (1991) Heat shock proteins as virulence factors of pathogens. Curr Microbiol Immunol 167: 125-143.
21. Leimeister-Wächter, M., Haffner, C., Domann, E., Goebel, W., and Chakraborty, T. (1990) Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes. Proc Natl Acad Sci USA 87: 8336-8340.
22. Leismeister-Wächter, M., Domann, E., and Chakraborty, T. (1992) The expression of virulence genes in Listeria monocytogenes is thermoregulated. J Bacteriol 174: 947-952.
23. Mackaness, G.B. (1962) Cellular resistance to infection. J Exp Med 116: 381-406.
24. Maguin, E., Duwat, P., Hege, T., Ehrlich, S.D., and Gruss, A. (1992) New thermosensitive plasmid from Gram-positive bacteria. J Bacteriol 174: 5633-5638.
25. Mengaud, J., Dramsi, S., Gouin, E., Vazquez-Boland, J.A., Milon, G., and Cossart, P. (1991) Pleiotropic control of Listeria monocytogenes virulence factors by a gene that is autoregulated. Mol Microbiol 5: 2273-2283.
26. Miyamoto, H., Yoshida, S., Taniguti, H., Qin, M.H., Fujino, H., and Mizuguti, Y. (1993) Protein profiles of Legionella pneumophila Philadelphia-1 grown in macrophages and characterization of a gene encoding a novel 24 KDa Legionella protein. Microb Pathog 15: 469-484.
27. Moulder, J.N. (1985) Comparative biology of intracellular parasitism. Microbiol Rev 49: 298-337.
28. Mounier, J., Ryter, A., Coquis-Rondon, M., and Sansonetti, P.J. (1990) Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocyte-like cell line Caco-2. Infect Immun 58: 1048-1058.
29. Msadek, T., Kunst, F., and Rapoport, G. (1994) MecB of Bacillus subtilis, a member of the ClpC ATPase family, is a pleiotropic regulator controlling competence gene expression and growth at high temperature. Proc Natl Acad Sci USA 91: 5788-5792.
30. Nathan, C.F., and Hibbs, J.B. (1991) Role of nitric oxide synthesis in macrophages antimicrobial activity. Curr Opin Immunol 3: 65-70.
31. North, R.J. (1970) The relative importance of blood monocytes and fixed macrophages to the expression of cell-mediated immunity to infections. J Exp Med 132: 521-534.
32. Parsell, D.A., Sanchez, Y., Stitzel, J.D., and Lindquist, S. (1991) Hsp104 is a highly conserved protein with two essential nucleotide-binding sites. Nature 353: 270-273.
33. Rouquette, C., Bolla, J.M., and Berche, P. (1995) An iron-dependent mutant of Listeria monocytogenes of attenuated virulence. FEMS Microbiol Lett 133: 77-83.
34. Rouquette, C., Ripio, M.T., Pelligrini, E., Bolla, J.M., Tascon, R., Vazquez-Boland, J.A., et al. (1996) Identification of a ClpC ATPase required for stress tolerance and in vivo survival of Listeria monocytogenes. Mol Microbiol 21: 977-987.
35. Ryter, A., and de Chastellier, C. (1983) Phagocyte-pathogenic microbe interactions. Int Rev Cytol 85: 287-327.
36. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
37. Schirmer, E.C., Glover, J.R., Singer, M.A., and Lindquist, S. (1996) HSP-100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21: 289-296.
38. Sheehan, B., Kocks, C., Dramsi, S., Gouin, E., Klarsfeld, A.D., Mengaud, J., et al. (1994) Molecular and genetic determinants of the Listeria monocytogenes infectious process. Curr Topics Microbiol 192: 187-216.
39. Small, P.L.C., Ramakishanan, L., and Falkow, S. (1994) Remodeling schemes of intracellular pathogens. Science 263: 637-639.
40. Sokolovic, Z., Fuchs, A., and Goebel, W. (1990) Synthesis of species-specific stress proteins by virulent strains of Listeria monocytogenes. Infect Immun 58: 3582-3587.
41. Sokolovic, Z., Riedel, J., Wuenscher, M., and Goebel, W. (1993) Surface-associated, prfA-regulated proteins of Listeria monocytogenes synthesized under stress conditions. Mol Microbiol 8: 219-227.
42. Squires, C., and Squires, C.L. (1992) The CIp proteins: proteolysis regulators and molecular chaperones? J Bacteriol 174: 1081-1085.
43. Tilney, L.G., and Portnoy, D.A. (1989) Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109: 1597-1608.
44. Trieu-Cuot, P., Carlier, C., Poyart-Salmeron, C., and Courvalin, P. (1990) A pair of mobilizable shuttle vectors conferring resistance to spectinomycin for molecular cloning in Escherichia coli and in Gram-positive bacteria. Nucleic Acids Res 18: 4296.
45. 50. Plasmid 28: 272-276.
46. Tulkens, P., and Trouet, A. (1978) The uptake and intracellular accumulation of aminoglycoside antibiotics in lysosomes of culture fibroblasts. Biochem Pharmacol 27: 415-424.
47. Vicente, M.F., Baquero, F., and Perez-Diaz, J.C. (1985) Cloning and expression of the Listeria monocytogenes haemolysin in E. coli. FEMS Microbiol Lett 30: 77-79.
48. Visick, J.E., and Clarke, S. (1995) Repair, refold, recycle: how bacteria can deal with spontaneous and environmental damage to proteins. Mol Microbiol 16: 835-845.
49. Yamamoto, T., Hanawa, T., and Ogata, S. (1994) Induction of Yersinia enterocolitica stress proteins by phagocytosis with macrophage. Microbiol Immunol 38: 295-300.