Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited

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Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited

DL Clemens and MA Horwitz
Department of Medicine, University of California, Los Angeles School of Medicine 90024.

We have used the cryosection immunogold technique to study the composition of the Mycobacterium tuberculosis phagosome. We have used quantitative immunogold staining to determine the distribution of several known markers of the endosomal-lysosomal pathway in human monocytes after ingestion of either M. tuberculosis, Legionella pneumophila, or polystyrene beads. Compared with the other phagocytic particles studied, the M. tuberculosis phagosome exhibits delayed clearance of major histocompatibility complex (MHC) class I molecules, relatively intense staining for MHC class II molecules and the endosomal marker transferrin receptor, and relatively weak staining for the lysosomal membrane glycoproteins, CD63, LAMP-1, and LAMP-2 and the lysosomal acid protease, cathepsin D. In contrast to M. tuberculosis, the L. pneumophila phagosome rapidly clears MHC class I molecules and excludes all endosomal-lysosomal markers studied. In contrast to both live M. tuberculosis and L. pneumophila phagosomes, phagosomes containing either polystyrene beads or heat-killed M. tuberculosis stain intensely for lysosomal membrane glycoproteins and cathepsin D. These findings suggest that (a) M. tuberculosis retards the maturation of its phagosome along the endosomal-lysosomal pathway and resides in a compartment with endosomal, as opposed to lysosomal, characteristics; and (b) the intraphagosomal pathway, i.e., the pathway followed by several intracellular parasites that inhibit phagosome-lysosome fusion, is heterogeneous.
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Hashim, S., Mukherjee, K., Raje, M., Basu, S. K., Mukhopadhyay, A. (2000). Live Salmonella Modulate Expression of Rab Proteins to Persist in a Specialized Compartment and Escape Transport to Lysosomes. J. Biol. Chem. 275: 16281-16288 [Abstract] [Full Text]
Clemens, D. L., Lee, B.-Y., Horwitz, M. A. (2000). Deviant Expression of Rab5 on Phagosomes Containing the Intracellular Pathogens Mycobacterium tuberculosis and Legionella pneumophila Is Associated with Altered Phagosomal Fate. Infect. Immun. 68: 2671-2684 [Abstract] [Full Text]
Schaible, U. E., Hagens, K., Fischer, K., Collins, H. L., Kaufmann, S. H. E. (2000). Intersection of Group I CD1 Molecules and Mycobacteria in Different Intracellular Compartments of Dendritic Cells. J. Immunol. 164: 4843-4852 [Abstract] [Full Text]
Gordon, S. B., Irving, G. R. B., Lawson, R. A., Lee, M. E., Read, R. C. (2000). Intracellular Trafficking and Killing of Streptococcus pneumoniae by Human Alveolar Macrophages Are Influenced by Opsonins. Infect. Immun. 68: 2286-2293 [Abstract] [Full Text]
Viswanathan, V. K., Edelstein, P. H., Pope, C. D., Cianciotto, N. P. (2000). The Legionella pneumophila iraAB Locus Is Required for Iron Assimilation, Intracellular Infection, and Virulence. Infect. Immun. 68: 1069-1079 [Abstract] [Full Text]
Mukherjee, K., Siddiqi, S. A., Hashim, S., Raje, M., Basu, S. K., Mukhopadhyay, A. (2000). Live Salmonella Recruits N-Ethylmaleimide-sensitive Fusion Protein on Phagosomal Membrane and Promotes Fusion with Early Endosome. J. Cell Biol. 148: 741-754 [Abstract] [Full Text]
Liles, M. R., Scheel, T. A., Cianciotto, N. P. (2000). Discovery of a Nonclassical Siderophore, Legiobactin, Produced by Strains of Legionella pneumophila. J. Bacteriol. 182: 749-757 [Abstract] [Full Text]