Abstract
The entry of rickettsiae into eukaryotic cells is mediated by an induced phagocytosis, but rickettsiae have never been observed in a closed phagocytic vacuole. In this study, Rickettsia conorii entry into Vero cells was observed by transmission electron microscopy during a period of 3 to 20 min after bacterium-cell contact. The entry occurred within 3 min after bacterium-cell contact, and R. conorii was observed in the process of engulfment, within a phagocytic vacuole, or free in the cytosol. Escape from the phagosome is a very rapid step since phagosome lysis was only occasionally observed. By 12 min, 90% of bacteria were internalized and half were free in the cytosol. This report confirms that rickettsiae penetrate nonphagocytic cells by induced phagocytosis and is the first demonstration of rickettsiae within a complete phagocytic vacuole.
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- Clerc P., Sansonetti P. J. Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect Immun. 1987 Nov;55(11):2681–2688. doi: 10.1128/iai.55.11.2681-2688.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cossart P., Vicente M. F., Mengaud J., Baquero F., Perez-Diaz J. C., Berche P. Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect Immun. 1989 Nov;57(11):3629–3636. doi: 10.1128/iai.57.11.3629-3636.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Falkow S., Isberg R. R., Portnoy D. A. The interaction of bacteria with mammalian cells. Annu Rev Cell Biol. 1992;8:333–363. doi: 10.1146/annurev.cb.08.110192.002001. [DOI] [PubMed] [Google Scholar]
- Gaillard J. L., Berche P., Mounier J., Richard S., Sansonetti P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun. 1987 Nov;55(11):2822–2829. doi: 10.1128/iai.55.11.2822-2829.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Geoffroy C., Gaillard J. L., Alouf J. E., Berche P. Purification, characterization, and toxicity of the sulfhydryl-activated hemolysin listeriolysin O from Listeria monocytogenes. Infect Immun. 1987 Jul;55(7):1641–1646. doi: 10.1128/iai.55.7.1641-1646.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- High N., Mounier J., Prévost M. C., Sansonetti P. J. IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole. EMBO J. 1992 May;11(5):1991–1999. doi: 10.1002/j.1460-2075.1992.tb05253.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li H., Walker D. H. Characterization of rickettsial attachment to host cells by flow cytometry. Infect Immun. 1992 May;60(5):2030–2035. doi: 10.1128/iai.60.5.2030-2035.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nogueira N., Cohn Z. Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. J Exp Med. 1976 Jun 1;143(6):1402–1420. doi: 10.1084/jem.143.6.1402. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Portnoy D. A., Chakraborty T., Goebel W., Cossart P. Molecular determinants of Listeria monocytogenes pathogenesis. Infect Immun. 1992 Apr;60(4):1263–1267. doi: 10.1128/iai.60.4.1263-1267.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Péter O., Raoult D., Gilot B. Isolation by a sensitive centrifugation cell culture system of 52 strains of spotted fever group rickettsiae from ticks collected in France. J Clin Microbiol. 1990 Jul;28(7):1597–1599. doi: 10.1128/jcm.28.7.1597-1599.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sansonetti P. J., Ryter A., Clerc P., Maurelli A. T., Mounier J. Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect Immun. 1986 Feb;51(2):461–469. doi: 10.1128/iai.51.2.461-469.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silverman D. J. Rickettsia rickettsii-induced cellular injury of human vascular endothelium in vitro. Infect Immun. 1984 Jun;44(3):545–553. doi: 10.1128/iai.44.3.545-553.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silverman D. J., Santucci L. A., Meyers N., Sekeyova Z. Penetration of host cells by Rickettsia rickettsii appears to be mediated by a phospholipase of rickettsial origin. Infect Immun. 1992 Jul;60(7):2733–2740. doi: 10.1128/iai.60.7.2733-2740.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silverman D. J., Wisseman C. L., Jr In vitro studies of rickettsia-host cell interactions: ultrastructural changes induced by Rickettsia rickettsii infection of chicken embryo fibroblasts. Infect Immun. 1979 Nov;26(2):714–727. doi: 10.1128/iai.26.2.714-727.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silverman D. J., Wisseman C. L., Jr, Waddell A. In vitro studies of Rickettsia-host cell interactions: ultrastructural study of Rickettsia prowazekii-infected chicken embryo fibroblasts. Infect Immun. 1980 Aug;29(2):778–790. doi: 10.1128/iai.29.2.778-790.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sporn L. A., Shi R. J., Lawrence S. O., Silverman D. J., Marder V. J. Rickettsia rickettsii infection of cultured endothelial cells induces release of large von Willebrand factor multimers from Weibel-Palade bodies. Blood. 1991 Nov 15;78(10):2595–2602. [PubMed] [Google Scholar]
- Teysseire N., Arnoux D., George F., Sampol J., Raoult D. von Willebrand factor release and thrombomodulin and tissue factor expression in Rickettsia conorii-infected endothelial cells. Infect Immun. 1992 Oct;60(10):4388–4393. doi: 10.1128/iai.60.10.4388-4393.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Teysseire N., Chiche-Portiche C., Raoult D. Intracellular movements of Rickettsia conorii and R. typhi based on actin polymerization. Res Microbiol. 1992 Nov-Dec;143(9):821–829. doi: 10.1016/0923-2508(92)90069-z. [DOI] [PubMed] [Google Scholar]
- WEISS E., DRESSLER H. R. Centrifugation and Rickettsiae and viruses onto cells and its effect on infection. Proc Soc Exp Biol Med. 1960 Apr;103:691–695. doi: 10.3181/00379727-103-25637. [DOI] [PubMed] [Google Scholar]
- Walker D. H., Firth W. T., Ballard J. G., Hegarty B. C. Role of phospholipase-associated penetration mechanism in cell injury by Rickettsia rickettsii. Infect Immun. 1983 May;40(2):840–842. doi: 10.1128/iai.40.2.840-842.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walker D. H., Firth W. T., Hegarty B. C. Injury restricted to cells infected with spotted fever group rickettsiae in parabiotic chambers. Acta Trop. 1984 Dec;41(4):307–312. [PubMed] [Google Scholar]
- Walker T. S. Rickettsial interactions with human endothelial cells in vitro: adherence and entry. Infect Immun. 1984 May;44(2):205–210. doi: 10.1128/iai.44.2.205-210.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walker T. S., Winkler H. H. Penetration of cultured mouse fibroblasts (L cells) by Rickettsia prowazeki. Infect Immun. 1978 Oct;22(1):200–208. doi: 10.1128/iai.22.1.200-208.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Winkler H. H., Daugherty R. M. Phospholipase A activity associated with the growth of Rickettsia prowazekii in L929 cells. Infect Immun. 1989 Jan;57(1):36–40. doi: 10.1128/iai.57.1.36-40.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Winkler H. H., Miller E. T. Phospholipase A activity in the hemolysis of sheep and human erythrocytes by Rickettsia prowazeki. Infect Immun. 1980 Aug;29(2):316–321. doi: 10.1128/iai.29.2.316-321.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Winkler H. H., Miller E. T. Phospholipase A and the interaction of Rickettsia prowazekii and mouse fibroblasts (L-929 cells). Infect Immun. 1982 Oct;38(1):109–113. doi: 10.1128/iai.38.1.109-113.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Winkler H. H. Rickettsia species (as organisms). Annu Rev Microbiol. 1990;44:131–153. doi: 10.1146/annurev.mi.44.100190.001023. [DOI] [PubMed] [Google Scholar]
- Wisseman C. L., Jr, Edlinger E. A., Waddell A. D., Jones M. R. Infection cycle of Rickettsia rickettsii in chicken embryo and L-929 cells in culture. Infect Immun. 1976 Oct;14(4):1052–1064. doi: 10.1128/iai.14.4.1052-1064.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Chastellier C., Berche P. Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria. Infect Immun. 1994 Feb;62(2):543–553. doi: 10.1128/iai.62.2.543-553.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]