Summary
Listeria monocytogenes is an invasive bacterial pathogen capable of multiplying inside many host cells, including macrophages, enterocytes and hepatocytes. There is evidence to believe that secretion of listeriolysin O, an SH-activated exotoxin, is crucial for bacterial growth in host tissues. This exotoxin is stimulated in iron-deprived medium and mostly active at low pH (5.5). Electron microscopic studies showed that intracellular bacteria rapidly disrupt the vacuole membrane of phagosomes and freely multiply inside the cytosol of infected cells, thus escaping at an early stage of infection from the cellular microbicidal mechanisms. Vacuole disruption does not occur with a nonhemolytic mutant obtained by insertion of a single copy of transposon Tn1545 in the structural gene of listeriolysin O. These results strongly suggest that listeriolysin O is a major factor promoting intracellular growth ofL. monocytogenes and that intracellular growth of virulent bacteria is initiated after escaping from the phagosomal compartment.
Zusammenfassung
Listeria monocytogenes ist ein invasiver bakterieller Erreger, der sich in zahlreichen Wirtszellen, einschließlich Makrophagen, Enterozyten und Hepatozyten vermehren kann. Nach vorliegenden Daten ist anzunehmen, daß die Sekretion des Listeriolysin O, eines SH-aktivierbaren Exotoxins, für das bakterielle Wachstum in Wirtsgeweben unerläßlich ist. Dieses Exotoxin wird in eisenfreiem Medium vermehrt sezerniert und ist bei pH 5,5 am aktivsten. Mittels elektronenmikroskopischer Studien konnte nachgewiesen werden, daß intrazelluläre Bakterien die Membran der Phagosomen-Vakuolen rasch aufbrechen und sich im Zytosol der infizierten Zellen frei vermehren. Damit entkommen sie in einem frühen Infektionsstadium den mikrobiziden Mechanismen der Zelle. Bei einer nicht-hämolysierenden Mutante, gewonnen durch Insertion einer einzigen Kopie des Transposon Tn1545 in das Strukturgen des Listeriolysin O, tritt die Zerstörung der Vakuole nicht ein. Nach diesen Ergebnissen ist es sehr wahrscheinlich, daß Listeriolysin O das intrazelluläre Wachstum vonL. monocytogenes entscheidend begünstigt, und daß das intrazelluläre Wachstum virulenter Bakterien beginnt, wenn sie aus dem phagosomalen Kompartiment entwichen sind.
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Literature
Gray, M. L., Killinger, A. H. Listeria monocytogenes and listeric infections. Bacteriol. Rev. 30 (1966) 309–382.
Humbert, G., Duval, C., Fessard, O., Meunier, M., Ledoux, A. Les listérioses en France. Résultats d'une enquête nationale (824 cas). Méd. Mal. Infect. 6 (1976) 60–70.
Audurier, A., Pardon, P., Marly, J., Lantier, F., Loulergue, J. Mesure de la virulence chez la souris de différentes bactéries appartenant au genreListeria. Ann. Immunol. (Inst. Pasteur), 132D (1981) 191–200.
MacDonald, T. T., Carter, P. B. Cell-mediated immunity to intestinal infection. Infect. Immun. 28 (1980) 516–523.
Racz, P., Tenner, K., Mero, E. ExperimentalListeria enteritis. I. An electron microscopic study of the epithelial phase in experimentalListeria infection. Lab. Invest. 26 (1972) 694–700.
Fleming, D. W., Cochi, S. L., MacDonald, K. L., Brondum, J., Hayes, P. S., Plikaytis, B. D., Holmes, M. B., Audurier, A., Broome, C. V., Reingold, A. L. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N. Engl. J. Med. 312 (1985) 404–407.
Linnan, M. J., Mascola, L., Xiao, D. L., Goulet, V., Salminen, C.: An investigation of listeriosis in southern California. In:Courtieu, A. L., Espaze, E. P., Reynaud, A. E. (eds.): Listériose,Listeria, Listeriosis, 1985–1986. Université de Nantes 1985, p. 227.
Schlech, W. F., Lavigne, P. M., Bortolussi, R. A., Allen, A. C., Haldane, E. V., Wort, A. J., Hightower, A. W., Johnson, S. E., King, S. H., Nicholls, E. S., Broome, C. V. Epidemic listeriosis-evidence for transmission by food. N. Engl. J. Med. 308 (1983) 203–206.
Gaillard, J. L., Berche, P., Mounier, J., Richard, S., Sansonetti, P. Penetration ofListeria monocytogenes into the host: a crucial step of the infectious process. Ann. Microbiol. 138 (1987) 259–264.
Gaillard, J. L., Berche, P., Mounier, J., Richard, S., Sansonetti, P.: Penetration and intracellular growth ofListeria monocytogenes in the human enterocyte-like cell line Caco-2: anin vitro model of pathogenesis. Infect. Immun. 55 (in press).
Anton, W. Kritisch-experimenteller Beitrag zur Biologie desBacterium monocytogenes. Mit besonderer Berücksichtigung seiner Beziehung zur infektiösen Mononukleose des Menschen. Zentralbl. Bakteriol. I. Abt. Orig. 131 (1934) 89–103.
Lefford, M. J., Warner, S., Amel, L. Listeria pneumonitis: influence of route of immunization on resistance to airborne infection. Infect. Immun. 25 (1979) 672–679.
Kautter, D. A., Silverman, S. J., Roessler, W. G., Drawdy, J. F. Virulence ofListeria monocytogenes for experimental animals. J. Infect. Dis. 112 (1963) 167–180.
Osebold, J. W., Inouye, T. Pathogenesis ofListeria monocytogenes infections in natural hosts. I. Rabbit studies. J. Infect. Dis. 95 (1954) 52–66.
Osebold, J. W., Inouye, T. Pathogenesis ofListeria monocytogenes infections in natural hosts. II. Sheep studies. J. Infect. Dis. 95 (1954) 67–78.
Racz, P., Kaiserling, E., Tenner, K., Wuthe, H. H. ExperimentalListeria cystitis. II. Further evidence of the epithelial phase in experimentalListeria infection. An electron microscopic study. Virchows Arch. Abt. B Zellpath. 13 (1973) 24–37.
Racz, P., Tenner, K., Szivessy, K. Electron microscopic studies in experimental keratoconjunctivitis listeriosa. I. Penetration ofListeria monocytogenes into corneal epithelial cells. Acta Microbiol. Acad. Sci. Hung. 17 (1970) 221–236.
Cossel, L., Mahnke, P. F. Electron-microscopical hepatic findings in experimental listeriosis. Beitr. Path. Anat. 138 (1968) 65–95.
North, R. J. The relative importance of blood monocytes and fixed macrophages to the expression of cell-mediated immunity to infection. J. Exp. Med. 132 (1970) 521.
Berche, P. Physiopathologie des infections neuroméningées àListeria monocytogenes. Méd. Mal. Infect. 10 (1985) 588–592.
Mackaness, G. B. Cellular resistance to infection. J. Exp. Med. 116 (1962) 381–406.
Gaillard, J. L.: Rôle de l'hémolysine dans la virulence deListeria monocytogenes. Medical Thesis, Paris (1985) 1.
Gaillard, J. L., Berche, P., Sansonetti, Ph.: The role of hemolysin in the virulence ofListeria monocytogenes. In:Courtieu, A. L., Espaze, E. P., Reynaud, A. E. (eds.): Listériose,Listeria, Listeriosis. Université de Nantes, 1986, pp. 183–187.
Gaillard, J. L., Berche, P., Sansonetti, P. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence ofListeria monocytogenes. Infect. Immun. 52 (1986) 50–55.
Kathariou, S., Metz, P., Hof, H., Goebel, W. Tn916-induced mutations in the hemolysin determinant affecting virulence ofListeria monocytogenes. J. Bacteriol. 169 (1987) 1291–1297.
Geoffroy, C., Gaillard, J. L., Alouf, J. E., Berche, P. Purification, characterization and toxicity of the sulfhydryl-activated hemolysin listeriolysin O fromListeria monocytogenes. Infect. Immun. 138 (1987) 369–371.
Alouf, J. E., Geoffroy, C. Structure activity relationships in sulfhydryl-activated toxins. In:Alouf, J. E., Fehrenbach, F. J., Freer, J. H., Jeljaszewicz, J. (eds.): Bacterial protein toxins. Academic Press, London 1984, pp. 165–171.
Bernheimer, A. W. Sulfhydryl-activated toxins. In:Bernheimer, A. W. (ed.): Mechanisms in bacterial toxinology. John Wiley and Sons, Inc., New York 1976, pp. 85–97.
Armstrong, B. A., Sword, C. P. Electron microscopy ofListeria monocytogenes-infected mouse spleen. J. Bacteriol. 91 (1966) 1346–1355.
Sword, C. P. Mechanisms of pathogenesis inListeria monocytogenes. I. Influence of Iron. J. Bacteriol. 92 (1966) 536–542.
Cowart, R. E., Foster, B. G. The role of iron in the production of hemolysin byListeria monocytogenes. Curr. Microbiol. 6 (1981) 287–290.
Kingdon, G. C., Sword, C. P. Effects ofListeria monocytogenes hemolysin on phagocytic cells and lysosomes. Infect. Immun. 1 (1970) 356–362.
Cowart, R. E., Foster, B. G. Differential effects of iron on the growth ofListeria monocytogenes: minimum requirements and mechanism of acquisition. J. Infect. Dis. 151 (1985) 721–730.
Berche, P., Gaillard, J. L., Sansonetti, P. Intracellular growth ofListeria monocytogenes as a prerequisite forin vivo induction of T cell-mediated immunity. J. Immunol. 138 (1987) 2266–2271.
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Berche, P., Gaillard, J.L. & Richard, S. Invasiveness and intracellular growth of Listeria monocytogenes. Infection 16 (Suppl 2), S145–S148 (1988). https://doi.org/10.1007/BF01639738
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DOI: https://doi.org/10.1007/BF01639738