This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by de Chastellier, C
Right arrow Articles by Berche, P
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by de Chastellier, C
Right arrow Articles by Berche, P

 Previous Article  |  Next Article 

Infection and Immunity, February 1994, p. 543-553, Vol. 62, No. 2
0019-9567/1994/$04.00+0     DOI:

research-article

Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria.

C de Chastellier and P Berche

Laboratoire de Microbiologie, Faculté de Médecine Necker-Enfants Malades, Paris, France.

ABSTRACT

The intracellular survival of the ubiquitous pathogen Listeria monocytogenes was studied in primary cultures of bone marrow-derived mouse macrophages. Bacteria were able to grow rapidly in these cells, with an apparent multiplication rate of about 40 min. Electron microscopy demonstrated that intracellular bacterial replication was the consequence of simultaneous intracellular killing and replication of bacteria in the same cells. Within the first hour following phagocytosis, most bacteria were destroyed in the phagosomal compartment to which they were confined. This was due to early transfer of hydrolytic enzymes to phagosomes, undoubtedly via phagosome-lysosome (P-L) fusion, as demonstrated by a quantitative analysis after staining for a lysosomal marker, acid phosphatase. One hour after infection, about 14% of the bacteria were free in the cytoplasm, in which they multiplied and induced actin polymerization and spreading to adjacent macrophages, as in epithelial cells. By using the 3-(2,4-dinitroanilino)-3'-amino-N-methyldipropylamine staining procedure, direct evidence is presented that all phagosomes were acidified immediately after phagocytosis, thus indicating that intraphagosomal bacteria were exposed to an acidic environment that might favor vacuolar lysis by listeriolysin O. Intracellular growth in macrophages, therefore, appears to be the result of a competition between the expression of the hydrolytic activity of these cells following P-L fusion and the capacity of L. monocytogenes to escape from the acidified phagosomal compartment before P-L fusion has occurred. The finding that concomitant intracellular killing and survival of L. monocytogenes occurs in the same macrophages might explain the high immunogenicity observed in vivo with live bacteria, as opposed to killed bacteria.

Infection and Immunity, February 1994, p. 543-553, Vol. 62, No. 2
0019-9567/1994/$04.00+0     DOI:




This article has been cited by other articles:

  • Meibom, K. L., Forslund, A.-L., Kuoppa, K., Alkhuder, K., Dubail, I., Dupuis, M., Forsberg, A., Charbit, A. (2009). Hfq, a Novel Pleiotropic Regulator of Virulence-Associated Genes in Francisella tularensis. Infect. Immun. 77: 1866-1880 [Abstract] [Full Text]  
  • Bigot, A., Raynaud, C., Dubail, I., Dupuis, M., Hossain, H., Hain, T., Chakraborty, T., Charbit, A. (2009). lmo1273, a novel gene involved in Listeria monocytogenes virulence. Microbiology 155: 891-902 [Abstract] [Full Text]  
  • Poirier, K., Faucher, S. P., Beland, M., Brousseau, R., Gannon, V., Martin, C., Harel, J., Daigle, F. (2008). Escherichia coli O157:H7 Survives within Human Macrophages: Global Gene Expression Profile and Involvement of the Shiga Toxins. Infect. Immun. 76: 4814-4822 [Abstract] [Full Text]  
  • Grayo, S., Join-Lambert, O., Desroches, M. C., Le Monnier, A. (2008). Comparison of the In Vitro Efficacies of Moxifloxacin and Amoxicillin against Listeria monocytogenes. Antimicrob. Agents Chemother. 52: 1697-1702 [Abstract] [Full Text]  
  • Bigot, A., Botton, E., Dubail, I., Charbit, A. (2006). A Homolog of Bacillus subtilis Trigger Factor in Listeria monocytogenes Is Involved in Stress Tolerance and Bacterial Virulence.. Appl. Environ. Microbiol. 72: 6623-6631 [Abstract] [Full Text]  
  • Li, Z., Zhao, X., Zhou, C., Gu, B., Frankel, F. R. (2006). A truncated Bacillus subtilis dal gene with a 3' ssrA gene tag regulates the growth and virulence of racemase-deficient Listeria monocytogenes.. Microbiology 152: 3091-3102 [Abstract] [Full Text]  
  • Aziz, A., Vanhille, L., Mohideen, P., Kelly, L. M., Otto, C., Bakri, Y., Mossadegh, N., Sarrazin, S., Sieweke, M. H. (2006). Development of Macrophages with Altered Actin Organization in the Absence of MafB.. Mol. Cell. Biol. 26: 6808-6818 [Abstract] [Full Text]  
  • Kubota, K. (2006). A novel functional T cell hybridoma recognizes macrophage cell death induced by bacteria: a possible role for innate lymphocytes in bacterial infection.. J. Immunol. 176: 7576-7588 [Abstract] [Full Text]  
  • Cerro-Vadillo, E. d., Madrazo-Toca, F., Carrasco-Marin, E., Fernandez-Prieto, L., Beck, C., Leyva-Cobian, F., Saftig, P., Alvarez-Dominguez, C. (2006). Cutting Edge: A Novel Nonoxidative Phagosomal Mechanism Exerted by Cathepsin-D Controls Listeria monocytogenes Intracellular Growth. J. Immunol. 176: 1321-1325 [Abstract] [Full Text]  
  • Wilson, R. L., Brown, L. L., Kirkwood-Watts, D., Warren, T. K., Lund, S. A., King, D. S., Jones, K. F., Hruby, D. E. (2006). Listeria monocytogenes 10403S HtrA Is Necessary for Resistance to Cellular Stress and Virulence. Infect. Immun. 74: 765-768 [Abstract] [Full Text]  
  • Bigot, A., Pagniez, H., Botton, E., Frehel, C., Dubail, I., Jacquet, C., Charbit, A., Raynaud, C. (2005). Role of FliF and FliI of Listeria monocytogenes in Flagellar Assembly and Pathogenicity. Infect. Immun. 73: 5530-5539 [Abstract] [Full Text]  
  • Li, Z., Zhao, X., Higgins, D. E., Frankel, F. R. (2005). Conditional Lethality Yields a New Vaccine Strain of Listeria monocytogenes for the Induction of Cell-Mediated Immunity. Infect. Immun. 73: 5065-5073 [Abstract] [Full Text]  
  • Bringer, M.-A., Barnich, N., Glasser, A.-L., Bardot, O., Darfeuille-Michaud, A. (2005). HtrA Stress Protein Is Involved in Intramacrophagic Replication of Adherent and Invasive Escherichia coli Strain LF82 Isolated from a Patient with Crohn's Disease. Infect. Immun. 73: 712-721 [Abstract] [Full Text]  
  • Naglik, J. R., Challacombe, S. J., Hube, B. (2003). Candida albicans Secreted Aspartyl Proteinases in Virulence and Pathogenesis. Microbiol. Mol. Biol. Rev. 67: 400-428 [Abstract] [Full Text]  
  • Cotter, P. D., Hill, C. (2003). Surviving the Acid Test: Responses of Gram-Positive Bacteria to Low pH. Microbiol. Mol. Biol. Rev. 67: 429-453 [Abstract] [Full Text]  
  • Autret, N., Raynaud, C., Dubail, I., Berche, P., Charbit, A. (2003). Identification of the agr Locus of Listeria monocytogenes: Role in Bacterial Virulence. Infect. Immun. 71: 4463-4471 [Abstract] [Full Text]  
  • Lety, M.-A., Frehel, C., Beretti, J.-l., Berche, P., Charbit, A. (2003). Modification of the signal sequence cleavage site of listeriolysin O does not affect protein secretion but impairs the virulence of Listeria monocytogenes. Microbiology 149: 1249-1255 [Abstract] [Full Text]  
  • Frehel, C., Lety, M.-A., Autret, N., Beretti, J.-l., Berche, P., Charbit, A. (2003). Capacity of ivanolysin O to replace listeriolysin O in phagosomal escape and in vivo survival of Listeria monocytogenes. Microbiology 149: 611-620 [Abstract] [Full Text]  
  • Edelson, B. T., Unanue, E. R. (2002). MyD88-Dependent but Toll-Like Receptor 2-Independent Innate Immunity to Listeria: No Role for Either in Macrophage Listericidal Activity. J. Immunol. 169: 3869-3875 [Abstract] [Full Text]  
  • Conte, M. P., Petrone, G., Di Biase, A. M., Longhi, C., Penta, M., Tinari, A., Superti, F., Fabozzi, G., Visca, P., Seganti, L. (2002). Effect of Acid Adaptation on the Fate of Listeria monocytogenes in THP-1 Human Macrophages Activated by Gamma Interferon. Infect. Immun. 70: 4369-4378 [Abstract] [Full Text]  
  • Webster, P. (2002). Early Intracellular Events During Internalization of Listeria monocytogenes by J774 Cells. J. Histochem. Cytochem. 50: 503-518 [Abstract] [Full Text]  
  • Borezee, E., Pellegrini, E., Beretti, J.-L., Berche, P. (2001). SvpA, a novel surface virulence-associated protein required for intracellular survival of Listeria monocytogenes. Microbiology 147: 2913-2923 [Abstract] [Full Text]  
  • Musso, T., Badolato, R., Ravarino, D., Stornello, S., Panzanelli, P., Merlino, C., Savoia, D., Cavallo, R., Ponzi, A. N., Zucca, M. (2001). Interaction of Bartonella henselae with the Murine Macrophage Cell Line J774: Infection and Proinflammatory Response. Infect. Immun. 69: 5974-5980 [Abstract] [Full Text]  
  • Poyart, C., Pellegrini, E., Gaillot, O., Boumaila, C., Baptista, M., Trieu-Cuot, P. (2001). Contribution of Mn-Cofactored Superoxide Dismutase (SodA) to the Virulence of Streptococcus agalactiae. Infect. Immun. 69: 5098-5106 [Abstract] [Full Text]  
  • Vazquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., Wehland, J., Kreft, J. (2001). Listeria Pathogenesis and Molecular Virulence Determinants. Clin. Microbiol. Rev. 14: 584-640 [Abstract] [Full Text]  
  • Nair, S., Milohanic, E., Berche, P. (2000). ClpC ATPase Is Required for Cell Adhesion and Invasion of Listeria monocytogenes. Infect. Immun. 68: 7061-7068 [Abstract] [Full Text]  
  • Borezee, E., Pellegrini, E., Berche, P. (2000). OppA of Listeria monocytogenes, an Oligopeptide-Binding Protein Required for Bacterial Growth at Low Temperature and Involved in Intracellular Survival. Infect. Immun. 68: 7069-7077 [Abstract] [Full Text]  
  • Gentry-Weeks, C. R., Karkhoff-Schweizer, R., Pikis, A., Estay, M., Keith, J. M. (1999). Survival of Enterococcus faecalis in Mouse Peritoneal Macrophages. Infect. Immun. 67: 2160-2165 [Abstract] [Full Text]  
  • Tanabe, Y., Xiong, H., Nomura, T., Arakawa, M., Mitsuyama, M. (1999). Induction of Protective T Cells against Listeria monocytogenes in Mice by Immunization with a Listeriolysin O-Negative Avirulent Strain of Bacteria and Liposome-Encapsulated Listeriolysin O. Infect. Immun. 67: 568-575 [Abstract] [Full Text]  
  • Bannam, T., Goldfine, H. (1999). Mutagenesis of Active-Site Histidines of Listeria monocytogenes Phosphatidylinositol-Specific Phospholipase C: Effects on Enzyme Activity and Biological Function. Infect. Immun. 67: 182-186 [Abstract] [Full Text]  
  • Ohya, S., Tanabe, Y., Makino, M., Nomura, T., Xiong, H., Arakawa, M., Mitsuyama, M. (1998). The Contributions of Reactive Oxygen Intermediates and Reactive Nitrogen Intermediates to Listericidal Mechanisms Differ in Macrophages Activated Pre- and Postinfection. Infect. Immun. 66: 4043-4049 [Abstract] [Full Text]  
  • 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. JEM 186: 1159-1163 [Abstract] [Full Text]  
  • Alvarez-Dominguez, C, Roberts, R, Stahl, P. (1997). Internalized Listeria monocytogenes modulates intracellular trafficking and delays maturation of the phagosome. J. Cell Sci. 110: 731-743 [Abstract]  
  • Alvarez-Dominguez, C., Barbieri, A. M., Beron, W., Wandinger-Ness, A., Stahl, P. D. (1996). Phagocytosed Live Listeria monocytogenes Influences Rab5-regulated in Vitro Phagosome-Endosome Fusion. J. Biol. Chem. 271: 13834-13843 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»