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 Jones, S
Right arrow Articles by Portnoy, D A
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Jones, S
Right arrow Articles by Portnoy, D A

 Previous Article  |  Next Article 

Infection and Immunity, December 1994, p. 5608-5613, Vol. 62, No. 12
0019-9567/1994/$04.00+0     DOI:

research-article

Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O.

S Jones and D A Portnoy

Department of Microbiology, University of Pennsylvania School of Medicine, Philadelphia 19104-6076.

ABSTRACT

Listeriolysin O (LLO) is a pore-forming cytolysin that enables Listeria monocytogenes to escape from a host cell vacuole. The structural gene for the related cytolysin perfringolysin O (pfo) was cloned downstream from the promoter for hly, the gene encoding LLO, both on a plasmid and on the L. monocytogenes chromosome. Both strains secreted active PFO, although regulation was not identical to that of LLO. The chromosomal PFO-expressing strain was characterized for intracellular growth and cell-to-cell spread. It escaped from a host cell vacuole with 64% efficiency compared with the wild type as determined by immunofluorescent staining of bacteria for F-actin, a marker for entry into the cytoplasm. In addition, it replicated intracellularly with a doubling time similar to that of the wild type for 5 h, after which growth was aborted because of a cytotoxic effect on the host cell and influx of extracellular gentamicin. The chromosomal PFO strain was able to plaque in mouse L2 fibroblasts, but it did so at 20% efficiency compared with the wild type and the plaques were significantly smaller. Both strains expressing PFO were completely avirulent in mice. These results indicate that PFO can mediate escape from a host cell vacuole but cannot complement an hly deletion strain for virulence.


Infection and Immunity, December 1994, p. 5608-5613, Vol. 62, No. 12
0019-9567/1994/$04.00+0     DOI:




This article has been cited by other articles:

  • Alonzo, F. III, Port, G. C., Cao, M., Freitag, N. E. (2009). The Posttranslocation Chaperone PrsA2 Contributes to Multiple Facets of Listeria monocytogenes Pathogenesis. Infect. Immun. 77: 2612-2623 [Abstract] [Full Text]  
  • Zemansky, J., Kline, B. C., Woodward, J. J., Leber, J. H., Marquis, H., Portnoy, D. A. (2009). Development of a mariner-Based Transposon and Identification of Listeria monocytogenes Determinants, Including the Peptidyl-Prolyl Isomerase PrsA2, That Contribute to Its Hemolytic Phenotype. J. Bacteriol. 191: 3950-3964 [Abstract] [Full Text]  
  • Bou Ghanem, E. N., McElroy, D. S., D'Orazio, S. E. F. (2009). Multiple Mechanisms Contribute to the Robust Rapid Gamma Interferon Response by CD8+ T Cells during Listeria monocytogenes Infection. Infect. Immun. 77: 1492-1501 [Abstract] [Full Text]  
  • Lieberman, L. A., Higgins, D. E. (2009). A Small-Molecule Screen Identifies the Antipsychotic Drug Pimozide as an Inhibitor of Listeria monocytogenes Infection. Antimicrob. Agents Chemother. 53: 756-764 [Abstract] [Full Text]  
  • Kleba, B., Stephens, R. S. (2008). Chlamydial Effector Proteins Localized to the Host Cell Cytoplasmic Compartment. Infect. Immun. 76: 4842-4850 [Abstract] [Full Text]  
  • Drevets, D. A., Schawang, J. E., Dillon, M. J., Lerner, M. R., Bronze, M. S., Brackett, D. J. (2008). Innate Responses to Systemic Infection by Intracellular Bacteria Trigger Recruitment of Ly-6Chigh Monocytes to the Brain. J. Immunol. 181: 529-536 [Abstract] [Full Text]  
  • Port, G. C., Freitag, N. E. (2007). Identification of Novel Listeria monocytogenes Secreted Virulence Factors following Mutational Activation of the Central Virulence Regulator, PrfA. Infect. Immun. 75: 5886-5897 [Abstract] [Full Text]  
  • Schnupf, P., Zhou, J., Varshavsky, A., Portnoy, D. A. (2007). Listeriolysin O Secreted by Listeria monocytogenes into the Host Cell Cytosol Is Degraded by the N-End Rule Pathway. Infect. Immun. 75: 5135-5147 [Abstract] [Full Text]  
  • Yoshimura, K., Laird, L. S., Chia, C. Y., Meckel, K. F., Slansky, J. E., Thompson, J. M., Jain, A., Pardoll, D. M., Schulick, R. D. (2007). Live Attenuated Listeria Monocytogenes Effectively Treats Hepatic Colorectal Cancer Metastases and Is Strongly Enhanced by Depletion of Regulatory T Cells. Cancer Res. 67: 10058-10066 [Abstract] [Full Text]  
  • Nomura, T., Kawamura, I., Kohda, C., Baba, H., Ito, Y., Kimoto, T., Watanabe, I., Mitsuyama, M. (2007). Irreversible loss of membrane-binding activity of Listeria-derived cytolysins in non-acidic conditions: a distinct difference from allied cytolysins produced by other Gram-positive bacteria. Microbiology 153: 2250-2258 [Abstract] [Full Text]  
  • Yeung, P. S. M., Na, Y., Kreuder, A. J., Marquis, H. (2007). Compartmentalization of the Broad-Range Phospholipase C Activity to the Spreading Vacuole Is Critical for Listeria monocytogenes Virulence. Infect. Immun. 75: 44-51 [Abstract] [Full Text]  
  • D'Orazio, S. E. F., Troese, M. J., Starnbach, M. N. (2006). Cytosolic Localization of Listeria monocytogenes Triggers an Early IFN-{gamma} Response by CD8+ T Cells That Correlates with Innate Resistance to Infection. J. Immunol. 177: 7146-7154 [Abstract] [Full Text]  
  • Hamilton, S. E., Badovinac, V. P., Khanolkar, A., Harty, J. T. (2006). Listeriolysin O-Deficient Listeria monocytogenes as a Vaccine Delivery Vehicle: Antigen-Specific CD8 T Cell Priming and Protective Immunity. J. Immunol. 177: 4012-4020 [Abstract] [Full Text]  
  • Dubail, I., Bigot, A., Lazarevic, V., Soldo, B., Euphrasie, D., Dupuis, M., Charbit, A. (2006). Identification of an Essential Gene of Listeria monocytogenes Involved in Teichoic Acid Biogenesis.. J. Bacteriol. 188: 6580-6591 [Abstract] [Full Text]  
  • Kazmierczak, M. J., Wiedmann, M., Boor, K. J. (2006). Contributions of Listeria monocytogenes {sigma}B and PrfA to expression of virulence and stress response genes during extra- and intracellular growth. Microbiology 152: 1827-1838 [Abstract] [Full Text]  
  • Lety, M.-A., Frehel, C., Raynaud, C., Dupuis, M., Charbit, A. (2006). Exploring the role of the CTL epitope region of listeriolysin O in the pathogenesis of Listeria monocytogenes.. Microbiology 152: 1287-1296 [Abstract] [Full Text]  
  • Molofsky, A. B., Byrne, B. G., Whitfield, N. N., Madigan, C. A., Fuse, E. T., Tateda, K., Swanson, M. S. (2006). Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. JEM 203: 1093-1104 [Abstract] [Full Text]  
  • Garner, M. R., Njaa, B. L., Wiedmann, M., Boor, K. J. (2006). Sigma B Contributes to Listeria monocytogenes Gastrointestinal Infection but Not to Systemic Spread in the Guinea Pig Infection Model. Infect. Immun. 74: 876-886 [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]  
  • Yoshimura, K., Jain, A., Allen, H. E., Laird, L. S., Chia, C. Y., Ravi, S., Brockstedt, D. G., Giedlin, M. A., Bahjat, K. S., Leong, M. L., Slansky, J. E., Cook, D. N., Dubensky, T. W., Pardoll, D. M., Schulick, R. D. (2006). Selective Targeting of Antitumor Immune Responses with Engineered Live-Attenuated Listeria monocytogenes. Cancer Res. 66: 1096-1104 [Abstract] [Full Text]  
  • Tweten, R. K. (2005). Cholesterol-Dependent Cytolysins, a Family of Versatile Pore-Forming Toxins. Infect. Immun. 73: 6199-6209 [Full Text]  
  • Wei, Z., Schnupf, P., Poussin, M. A., Zenewicz, L. A., Shen, H., Goldfine, H. (2005). Characterization of Listeria monocytogenes Expressing Anthrolysin O and Phosphatidylinositol-Specific Phospholipase C from Bacillus anthracis. Infect. Immun. 73: 6639-6646 [Abstract] [Full Text]  
  • Schuerch, D. W., Wilson-Kubalek, E. M., Tweten, R. K. (2005). Molecular basis of listeriolysin O pH dependence. Proc. Natl. Acad. Sci. USA 102: 12537-12542 [Abstract] [Full Text]  
  • Roberts, A., Chan, Y., Wiedmann, M. (2005). Definition of Genetically Distinct Attenuation Mechanisms in Naturally Virulence-Attenuated Listeria monocytogenes by Comparative Cell Culture and Molecular Characterization. Appl. Environ. Microbiol. 71: 3900-3910 [Abstract] [Full Text]  
  • Poussin, M. A., Goldfine, H. (2005). Involvement of Listeria monocytogenes Phosphatidylinositol-Specific Phospholipase C and Host Protein Kinase C in Permeabilization of the Macrophage Phagosome. Infect. Immun. 73: 4410-4413 [Abstract] [Full Text]  
  • Mueller, K. J., Freitag, N. E. (2005). Pleiotropic Enhancement of Bacterial Pathogenesis Resulting from the Constitutive Activation of the Listeria monocytogenes Regulatory Factor PrfA. Infect. Immun. 73: 1917-1926 [Abstract] [Full Text]  
  • Boyartchuk, V., Rojas, M., Yan, B.-S., Jobe, O., Hurt, N., Dorfman, D. M., Higgins, D. E., Dietrich, W. F., Kramnik, I. (2004). The Host Resistance Locus sst1 Controls Innate Immunity to Listeria monocytogenes Infection in Immunodeficient Mice. J. Immunol. 173: 5112-5120 [Abstract] [Full Text]  
  • Chaturongakul, S., Boor, K. J. (2004). RsbT and RsbV Contribute to {sigma}B-Dependent Survival under Environmental, Energy, and Intracellular Stress Conditions in Listeria monocytogenes. Appl. Environ. Microbiol. 70: 5349-5356 [Abstract] [Full Text]  
  • O'Brien, D. K., Melville, S. B. (2004). Effects of Clostridium perfringens Alpha-Toxin (PLC) and Perfringolysin O (PFO) on Cytotoxicity to Macrophages, on Escape from the Phagosomes of Macrophages, and on Persistence of C. perfringens in Host Tissues. Infect. Immun. 72: 5204-5215 [Abstract] [Full Text]  
  • Tvinnereim, A. R., Hamilton, S. E., Harty, J. T. (2004). Neutrophil Involvement in Cross-Priming CD8+ T Cell Responses to Bacterial Antigens. J. Immunol. 173: 1994-2002 [Abstract] [Full Text]  
  • Drevets, D. A., Dillon, M. J., Schawang, J. S., van Rooijen, N., Ehrchen, J., Sunderkotter, C., Leenen, P. J. M. (2004). The Ly-6Chigh Monocyte Subpopulation Transports Listeria monocytogenes into the Brain during Systemic Infection of Mice. J. Immunol. 172: 4418-4424 [Abstract] [Full Text]  
  • Grossman, H. L., Myers, W. R., Vreeland, V. J., Bruehl, R., Alper, M. D., Bertozzi, C. R., Clarke, J. (2004). Detection of bacteria in suspension by using a superconducting quantum interference device. Proc. Natl. Acad. Sci. USA 101: 129-134 [Abstract] [Full Text]  
  • Glomski, I. J., Decatur, A. L., Portnoy, D. A. (2003). Listeria monocytogenes Mutants That Fail To Compartmentalize Listerolysin O Activity Are Cytotoxic, Avirulent, and Unable To Evade Host Extracellular Defenses. Infect. Immun. 71: 6754-6765 [Abstract] [Full Text]  
  • Grundling, A., Gonzalez, M. D., Higgins, D. E. (2003). Requirement of the Listeria monocytogenes Broad-Range Phospholipase PC-PLC during Infection of Human Epithelial Cells. J. Bacteriol. 185: 6295-6307 [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]  
  • Greene, S. L., Freitag, N. E. (2003). Negative regulation of PrfA, the key activator of Listeria monocytogenes virulence gene expression, is dispensable for bacterial pathogenesis. Microbiology 149: 111-120 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • 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. JCB 158: 409-414 [Abstract] [Full Text]  
  • Wadsworth, S. J., Goldfine, H. (2002). Mobilization of Protein Kinase C in Macrophages Induced by Listeria monocytogenes Affects Its Internalization and Escape from the Phagosome. Infect. Immun. 70: 4650-4660 [Abstract] [Full Text]  
  • Lauer, P., Chow, M. Y. N., 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 [Abstract] [Full Text]  
  • Skoberne, M., Schenk, S., Hof, H., Geginat, G. (2002). Cross-Presentation of Listeria monocytogenes-Derived CD4 T Cell Epitopes. J. Immunol. 169: 1410-1418 [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]  
  • Dramsi, S., Cossart, P. (2002). Listeriolysin O: a genuine cytolysin optimized for an intracellular parasite. JCB 156: 943-946 [Abstract] [Full Text]  
  • 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. JCB 156: 1029-1038 [Abstract] [Full Text]  
  • Hamilton, S. E., Tvinnereim, A. R., Harty, J. T. (2001). Listeria monocytogenes Infection Overcomes the Requirement for CD40 Ligand in Exogenous Antigen Presentation to CD8+ T Cells. J. Immunol. 167: 5603-5609 [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]  
  • Kolb-Maurer, A., Pilgrim, S., Kampgen, E., McLellan, A. D., Brocker, E.-B., Goebel, W., Gentschev, I. (2001). Antibodies against Listerial Protein 60 Act as an Opsonin for Phagocytosis of Listeria monocytogenes by Human Dendritic Cells. Infect. Immun. 69: 3100-3109 [Abstract] [Full Text]  
  • Decatur, A. L., Portnoy, D. A. (2000). A PEST-Like Sequence in Listeriolysin O Essential for Listeria monocytogenes Pathogenicity. Science 290: 992-995 [Abstract] [Full Text]  
  • Goldfine, H., Wadsworth, S. J., Johnston, N. C. (2000). Activation of Host Phospholipases C and D in Macrophages after Infection with Listeria monocytogenes. Infect. Immun. 68: 5735-5741 [Abstract] [Full Text]  
  • Kolb-Maurer, A., Gentschev, I., Fries, H.-W., Fiedler, F., Brocker, E.-B., Kampgen, E., Goebel, W. (2000). Listeria monocytogenes-Infected Human Dendritic Cells: Uptake and Host Cell Response. Infect. Immun. 68: 3680-3688 [Abstract] [Full Text]  
  • Gedde, M. M., Higgins, D. E., Tilney, L. G., Portnoy, D. A. (2000). Role of Listeriolysin O in Cell-to-Cell Spread of Listeria monocytogenes. Infect. Immun. 68: 999-1003 [Abstract] [Full Text]  
  • Teitelbaum, R., Cammer, M., Maitland, M. L., Freitag, N. E., Condeelis, J., Bloom, B. R. (1999). Mycobacterial infection of macrophages results in membrane-permeable phagosomes. Proc. Natl. Acad. Sci. USA 96: 15190-15195 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Wadsworth, S. J., Goldfine, H. (1999). Listeria monocytogenes Phospholipase C-Dependent Calcium Signaling Modulates Bacterial Entry into J774 Macrophage-Like Cells. Infect. Immun. 67: 1770-1778 [Abstract] [Full Text]  
  • Freitag, N. E., Jacobs, K. E. (1999). Examination of Listeria monocytogenes Intracellular Gene Expression by Using the Green Fluorescent Protein of Aequorea victoria. Infect. Immun. 67: 1844-1852 [Abstract] [Full Text]  
  • Moors, M. A., Levitt, B., Youngman, P., Portnoy, D. A. (1999). Expression of Listeriolysin O and ActA by Intracellular and Extracellular Listeria monocytogenes. Infect. Immun. 67: 131-139 [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]  
  • Greiffenberg, L., Goebel, W., Kim, K. S., Weiglein, I., Bubert, A., Engelbrecht, F., Stins, M., Kuhn, M. (1998). Interaction of Listeria monocytogenes with Human Brain Microvascular Endothelial Cells: InlB-Dependent Invasion, Long-Term Intracellular Growth, and Spread from Macrophages to Endothelial Cells. Infect. Immun. 66: 5260-5267 [Abstract] [Full Text]  
  • Zuckert, W. R., Marquis, H., Goldfine, H. (1998). Modulation of Enzymatic Activity and Biological Function of Listeria monocytogenes Broad-Range Phospholipase C by Amino Acid Substitutions and by Replacement with the Bacillus cereus Ortholog. Infect. Immun. 66: 4823-4831 [Abstract] [Full Text]  
  • Jensen, V. B., Harty, J. T., Jones, B. D. (1998). Interactions of the Invasive Pathogens Salmonella typhimurium, Listeria monocytogenes, and Shigella flexneri with M Cells and Murine Peyer's Patches. Infect. Immun. 66: 3758-3766 [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]  
  • Hauf, N., Goebel, W., Fiedler, F., Sokolovic, Z., Kuhn, M. (1997). Listeria monocytogenes infection of P388D1 macrophages results in a biphasic NF-kappa B (RelA/p50) activation induced by lipoteichoic acid and bacterial phospholipases and mediated by Ikappa Balpha and Ikappa Bbeta  degradation. Proc. Natl. Acad. Sci. USA 94: 9394-9399 [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]  
  • Lee, K.-D., Oh, Y.-K., Portnoy, D. A., Swanson, J. A. (1996). Delivery of Macromolecules into Cytosol Using Liposomes Containing Hemolysin from Listeria monocytogenes. J. Biol. Chem. 271: 7249-7252 [Abstract] [Full Text]