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Infect Immun, May 1998, p. 2387-2392, Vol. 66, No. 5
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Virulent Brucella abortus Prevents
Lysosome Fusion and Is Distributed within Autophagosome-Like
Compartments
Javier
Pizarro-Cerdá,1
Edgardo
Moreno,1
Veronique
Sanguedolce,2
Jean-Louis
Mege,2 and
Jean-Pierre
Gorvel1,*
Centre d'Immunologie INSERM-CNRS de
Marseille-Luminy, 13288 Marseille Cedex 9,1 and
Centre National de Référence des Rickettsioses,
Centre Hospitalier Universitaire la Timone, 13385 Marseille,2 France
Received 3 November 1997/Returned for modification 26 January
1998/Accepted 6 February 1998
Virulent and attenuated Brucella abortus strains attach
to and penetrate nonprofessional phagocytic HeLa cells. Compared to pathogenic Brucella, the attenuated strain 19 hardly
replicates within cells. The majority of the strain 19 bacteria
colocalized with the lysosome marker cathepsin D, suggesting that
Brucella-containing phagosomes had fused with lysosomes, in
which they may have degraded. The virulent bacteria prevented
lysosome-phagosome fusion and were found distributed in the perinuclear
region within compartments resembling autophagosomes.
*
Corresponding author. Mailing address: Centre
d'Immunologie INSERM-CNRS de Marseille-Luminy, Case 906, 13288 Marseille Cedex 9, France. Phone: 33-4-91-26-94-66. Fax:
33-4-91-26-94-30. E-mail: gorvel{at}ciml.univ-mrs.fr.
Infect Immun, May 1998, p. 2387-2392, Vol. 66, No. 5
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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-
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-
Velasco, J., Bengoechea, J. A., Brandenburg, K., Lindner, B., Seydel, U., Gonzalez, D., Zahringer, U., Moreno, E., Moriyon, I.
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-
Teixeira-Gomes, A. P., Cloeckaert, A., Zygmunt, M. S.
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[Abstract]
[Full Text]
-
CESPEDES, S., ANDREWS, E., FOLCH, H., ONATE, A.
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[Abstract]
[Full Text]
-
Dorn, B. R., Dunn, W. A. Jr., Progulske-Fox, A.
(1999). Invasion of Human Coronary Artery Cells by Periodontal Pathogens. Infect. Immun.
67: 5792-5798
[Abstract]
[Full Text]
-
Freer, E., Pizarro-Cerda, J., Weintraub, A., Bengoechea, J.-A., Moriyon, I., Hultenby, K., Gorvel, J.-P., Moreno, E.
(1999). The Outer Membrane of Brucella ovis Shows Increased Permeability to Hydrophobic Probes and Is More Susceptible to Cationic Peptides than Are the Outer Membranes of Mutant Rough Brucella abortus Strains. Infect. Immun.
67: 6181-6186
[Abstract]
[Full Text]
-
McQuiston, J. R., Vemulapalli, R., Inzana, T. J., Schurig, G. G., Sriranganathan, N., Fritzinger, D., Hadfield, T. L., Warren, R. A., Snellings, N., Hoover, D., Halling, S. M., Boyle, S. M.
(1999). Genetic Characterization of a Tn5-Disrupted Glycosyltransferase Gene Homolog in Brucella abortus and Its Effect on Lipopolysaccharide Composition and Virulence. Infect. Immun.
67: 3830-3835
[Abstract]
[Full Text]
-
Porte, F., Liautard, J.-P., Kohler, S.
(1999). Early Acidification of Phagosomes Containing Brucella suis Is Essential for Intracellular Survival in Murine Macrophages. Infect. Immun.
67: 4041-4047
[Abstract]
[Full Text]
-
Forestier, C., Moreno, E., Pizarro-Cerda, J., Gorvel, J.-P.
(1999). Lysosomal Accumulation and Recycling of Lipopolysaccharide to the Cell Surface of Murine Macrophages, an In Vitro and In Vivo Study. J. Immunol.
162: 6784-6791
[Abstract]
[Full Text]
-
Pizarro-Cerda, J., Desjardins, M., Moreno, E., Akira, S., Gorvel, J.-P.
(1999). Modulation of Endocytosis in Nuclear Factor IL-6(-/-) Macrophages Is Responsible for a High Susceptibility to Intracellular Bacterial Infection. J. Immunol.
162: 3519-3526
[Abstract]
[Full Text]
-
Pizarro-Cerda, J., Meresse, S., Parton, R. G., van der Goot, G., Sola-Landa, A., Lopez-Goni, I., Moreno, E., Gorvel, J.-P.
(1998). Brucella abortus Transits through the Autophagic Pathway and Replicates in the Endoplasmic Reticulum of Nonprofessional Phagocytes. Infect. Immun.
66: 5711-5724
[Abstract]
[Full Text]
-
Guzman-Verri, C., Chaves-Olarte, E., von Eichel-Streiber, C., Lopez-Goni, I., Thelestam, M., Arvidson, S., Gorvel, J.-P., Moreno, E.
(2001). GTPases of the Rho Subfamily Are Required for Brucella abortus Internalization in Nonprofessional Phagocytes. DIRECT ACTIVATION OF Cdc42. J. Biol. Chem.
276: 44435-44443
[Abstract]
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