The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin

doi:10.1084/jem.184.4.1349

This Article

	Full Text (PDF)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Clemens, D. L.
	Articles by Horwitz, M. A.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Clemens, D. L.
	Articles by Horwitz, M. A.


Social Bookmarking

	What's this?

ARTICLES

The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin

DL Clemens and MA Horwitz
Department of Medicine, UCLA School of Medicine 90095, USA.

Previous studies have demonstrated that the Mycobacterium tuberculosis phagosome in human monocyte-derived macrophages acquires markers of early and late endosomes, but direct evidence of interaction of the M. tuberculosis phagosome with the endosomal compartment has been lacking. Using the cryosection immunogold technique, we have found that the M. tuberculosis phagosome acquires exogenously added transferrin in a time- dependent fashion. Near-maximal acquisition of transferrin occurs within 15 min, kinetics of acquisition consistent with interaction of the M. tuberculosis phagosome with early endosomes. Transferrin is chased out of the M. tuberculosis phagosome by incubation of the infected macrophages in culture medium lacking human transferrin. Phagosomes containing latex beads or heat-killed M. tuberculosis, on the other hand, do not acquire staining for transferrin. These and other findings demonstrate that M. tuberculosis arrests the maturation of its phagosome at a stage at which the phagosome interacts with early and late endosomes, but not with lysosomes. The transferrin endocytic pathway potentially provides a novel route for targeting antimicrobials to the M. tuberculosis phagosome.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Rampini, S. K., Selchow, P., Keller, C., Ehlers, S., Bottger, E. C., Sander, P. (2008). LspA inactivation in Mycobacterium tuberculosis results in attenuation without affecting phagosome maturation arrest. Microbiology 154: 2991-3001 [Abstract] [Full Text]
Huynh, K. K., Grinstein, S. (2007). Regulation of Vacuolar pH and Its Modulation by Some Microbial Species. Microbiol. Mol. Biol. Rev. 71: 452-462 [Abstract] [Full Text]
Kusner, D. J., Thompson, C. R., Melrose, N. A., Pitson, S. M., Obeid, L. M., Iyer, S. S. (2007). The Localization and Activity of Sphingosine Kinase 1 Are Coordinately Regulated with Actin Cytoskeletal Dynamics in Macrophages. J. Biol. Chem. 282: 23147-23162 [Abstract] [Full Text]
Majlessi, L., Combaluzier, B., Albrecht, I., Garcia, J. E., Nouze, C., Pieters, J., Leclerc, C. (2007). Inhibition of Phagosome Maturation by Mycobacteria Does Not Interfere with Presentation of Mycobacterial Antigens by MHC Molecules. J. Immunol. 179: 1825-1833 [Abstract] [Full Text]
MacGurn, J. A., Cox, J. S. (2007). A Genetic Screen for Mycobacterium tuberculosis Mutants Defective for Phagosome Maturation Arrest Identifies Components of the ESX-1 Secretion System. Infect. Immun. 75: 2668-2678 [Abstract] [Full Text]
Olakanmi, O., Schlesinger, L. S., Britigan, B. E. (2007). Hereditary hemochromatosis results in decreased iron acquisition and growth by Mycobacterium tuberculosis within human macrophages. J. Leukoc. Biol. 81: 195-204 [Abstract] [Full Text]
Daniel, D. S., Dai, G., Singh, C. R., Lindsey, D. R., Smith, A. K., Dhandayuthapani, S., Hunter, R. L. Jr, Jagannath, C. (2006). The Reduced Bactericidal Function of Complement C5-Deficient Murine Macrophages Is Associated with Defects in the Synthesis and Delivery of Reactive Oxygen Radicals to Mycobacterial Phagosomes. J. Immunol. 177: 4688-4698 [Abstract] [Full Text]
He, Y., Reichow, S., Ramamoorthy, S., Ding, X., Lathigra, R., Craig, J. C., Sobral, B. W. S., Schurig, G. G., Sriranganathan, N., Boyle, S. M. (2006). Brucella melitensis Triggers Time-Dependent Modulation of Apoptosis and Down-Regulation of Mitochondrion-Associated Gene Expression in Mouse Macrophages. Infect. Immun. 74: 5035-5046 [Abstract] [Full Text]
Harrison, A. J., Yu, M., Gardenborg, T., Middleditch, M., Ramsay, R. J., Baker, E. N., Lott, J. S. (2006). The Structure of MbtI from Mycobacterium tuberculosis, the First Enzyme in the Biosynthesis of the Siderophore Mycobactin, Reveals It To Be a Salicylate Synthase.. J. Bacteriol. 188: 6081-6091 [Abstract] [Full Text]
Tan, B. H., Meinken, C., Bastian, M., Bruns, H., Legaspi, A., Ochoa, M. T., Krutzik, S. R., Bloom, B. R., Ganz, T., Modlin, R. L., Stenger, S. (2006). Macrophages Acquire Neutrophil Granules for Antimicrobial Activity against Intracellular Pathogens. J. Immunol. 177: 1864-1871 [Abstract] [Full Text]
Lewinsohn, D. M., Grotzke, J. E., Heinzel, A. S., Zhu, L., Ovendale, P. J., Johnson, M., Alderson, M. R. (2006). Secreted Proteins from Mycobacterium tuberculosis Gain Access to the Cytosolic MHC Class-I Antigen-Processing Pathway. J. Immunol. 177: 437-442 [Abstract] [Full Text]
Appelberg, R. (2006). Macrophage nutriprive antimicrobial mechanisms. J. Leukoc. Biol. 79: 1117-1128 [Abstract] [Full Text]
Nepal, R. M, Mampe, S., Shaffer, B., Erickson, A. H, Bryant, P. (2006). Cathepsin L maturation and activity is impaired in macrophages harboring M. avium and M. tuberculosis. Int Immunol 18: 931-939 [Abstract] [Full Text]
Lang, M. L., Glatman-Freedman, A. (2006). Do CD1-Restricted T Cells Contribute to Antibody-Mediated Immunity against Mycobacterium tuberculosis?. Infect. Immun. 74: 803-809 [Full Text]
Cai, S., Sato, K., Shimizu, T., Yamabe, S., Hiraki, M., Sano, C., Tomioka, H. (2006). Antimicrobial activity of picolinic acid against extracellular and intracellular Mycobacterium avium complex and its combined activity with clarithromycin, rifampicin and fluoroquinolones. J Antimicrob Chemother 57: 85-93 [Abstract] [Full Text]
Toyooka, K., Takai, S., Kirikae, T. (2005). Rhodococcus equi can survive a phagolysosomal environment in macrophages by suppressing acidification of the phagolysosome. J Med Microbiol 54: 1007-1015 [Abstract] [Full Text]
Knight, S. A. B., Vilaire, G., Lesuisse, E., Dancis, A. (2005). Iron Acquisition from Transferrin by Candida albicans Depends on the Reductive Pathway. Infect. Immun. 73: 5482-5492 [Abstract] [Full Text]
Vergne, I., Chua, J., Lee, H.-H., Lucas, M., Belisle, J., Deretic, V. (2005). Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 102: 4033-4038 [Abstract] [Full Text]
Ramachandra, L., Smialek, J. L., Shank, S. S., Convery, M., Boom, W. H., Harding, C. V. (2005). Phagosomal Processing of Mycobacterium tuberculosis Antigen 85B Is Modulated Independently of Mycobacterial Viability and Phagosome Maturation. Infect. Immun. 73: 1097-1105 [Abstract] [Full Text]
Wagner, D., Maser, J., Lai, B., Cai, Z., Barry, C. E. III, Honer zu Bentrup, K., Russell, D. G., Bermudez, L. E. (2005). Elemental Analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-Containing Phagosomes Indicates Pathogen-Induced Microenvironments within the Host Cell's Endosomal System. J. Immunol. 174: 1491-1500 [Abstract] [Full Text]
Walburger, A., Koul, A., Ferrari, G., Nguyen, L., Prescianotto-Baschong, C., Huygen, K., Klebl, B., Thompson, C., Bacher, G., Pieters, J. (2004). Protein Kinase G from Pathogenic Mycobacteria Promotes Survival Within Macrophages. Science 304: 1800-1804 [Abstract] [Full Text]
Kagan, J. C., Stein, M.-P., Pypaert, M., Roy, C. R. (2004). Legionella Subvert the Functions of Rab1 and Sec22b to Create a Replicative Organelle. J. Exp. Med. 199: 1201-1211 [Abstract] [Full Text]
Pais, T. F., Appelberg, R. (2004). Induction of Mycobacterium avium growth restriction and inhibition of phagosome-endosome interactions during macrophage activation and apoptosis induction by picolinic acid plus IFN{gamma}. Microbiology 150: 1507-1518 [Abstract] [Full Text]
Olakanmi, O., Schlesinger, L. S., Ahmed, A., Britigan, B. E. (2004). The Nature of Extracellular Iron Influences Iron Acquisition by Mycobacterium tuberculosis Residing within Human Macrophages. Infect. Immun. 72: 2022-2028 [Abstract] [Full Text]
Vergne, I., Fratti, R. A., Hill, P. J., Chua, J., Belisle, J., Deretic, V. (2004). Mycobacterium tuberculosis Phagosome Maturation Arrest: Mycobacterial Phosphatidylinositol Analog Phosphatidylinositol Mannoside Stimulates Early Endosomal Fusion. Mol. Biol. Cell 15: 751-760 [Abstract] [Full Text]
Fratti, R. A., Chua, J., Deretic, V. (2003). Induction of p38 Mitogen-activated Protein Kinase Reduces Early Endosome Autoantigen 1 (EEA1) Recruitment to Phagosomal Membranes. J. Biol. Chem. 278: 46961-46967 [Abstract] [Full Text]
Roseeuw, E., Coessens, V., Balazuc, A.-M., Lagranderie, M., Chavarot, P., Pessina, A., Neri, M. G., Schacht, E., Marchal, G., Domurado, D. (2003). Synthesis, Degradation, and Antimicrobial Properties of Targeted Macromolecular Prodrugs of Norfloxacin. Antimicrob. Agents Chemother. 47: 3435-3441 [Abstract] [Full Text]
MacMicking, J. D., Taylor, G. A., McKinney, J. D. (2003). Immune Control of Tuberculosis by IFN-{gamma}-Inducible LRG-47. Science 302: 654-659 [Abstract] [Full Text]
Tobian, A. A. R., Potter, N. S., Ramachandra, L., Pai, R. K., Convery, M., Boom, W. H., Harding, C. V. (2003). Alternate Class I MHC Antigen Processing Is Inhibited by Toll-Like Receptor Signaling Pathogen-Associated Molecular Patterns: Mycobacterium tuberculosis 19-kDa Lipoprotein, CpG DNA, and Lipopolysaccharide. J. Immunol. 171: 1413-1422 [Abstract] [Full Text]
Solomon, J. M., Leung, G. S., Isberg, R. R. (2003). Intracellular Replication of Mycobacterium marinum within Dictyostelium discoideum: Efficient Replication in the Absence of Host Coronin. Infect. Immun. 71: 3578-3586 [Abstract] [Full Text]
Fratti, R. A., Chua, J., Vergne, I., Deretic, V. (2003). Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. USA 100: 5437-5442 [Abstract] [Full Text]
Wasylnka, J. A., Moore, M. M. (2003). Aspergillus fumigatus conidia survive and germinate in acidic organelles of A549 epithelial cells. J. Cell Sci. 116: 1579-1587 [Abstract] [Full Text]
Tailleux, L., Neyrolles, O., Honore-Bouakline, S., Perret, E., Sanchez, F., Abastado, J.-P., Lagrange, P. H., Gluckman, J. C., Rosenzwajg, M., Herrmann, J.-L. (2003). Constrained Intracellular Survival of Mycobacterium tuberculosis in Human Dendritic Cells. J. Immunol. 170: 1939-1948 [Abstract] [Full Text]
Borelli, V., Vita, F., Shankar, S., Soranzo, M. R., Banfi, E., Scialino, G., Brochetta, C., Zabucchi, G. (2003). Human Eosinophil Peroxidase Induces Surface Alteration, Killing, and Lysis of Mycobacterium tuberculosis. Infect. Immun. 71: 605-613 [Abstract] [Full Text]
Olakanmi, O., Schlesinger, L. S., Ahmed, A., Britigan, B. E. (2002). Intraphagosomal Mycobacterium tuberculosis Acquires Iron from Both Extracellular Transferrin and Intracellular Iron Pools. IMPACT OF INTERFERON-gamma AND HEMOCHROMATOSIS. J. Biol. Chem. 277: 49727-49734 [Abstract] [Full Text]
Russell, D. G., Mwandumba, H. C., Rhoades, E. E. (2002). Mycobacterium and the coat of many lipids. J. Cell Biol. 158: 421-426 [Abstract] [Full Text]
Fratti, R. A., Chua, J., Deretic, V. (2002). Cellubrevin Alterations and Mycobacterium tuberculosis Phagosome Maturation Arrest. J. Biol. Chem. 277: 17320-17326 [Abstract] [Full Text]
Ramachandra, L., Noss, E., Boom, W. H., Harding, C. V. (2001). Processing of Mycobacterium tuberculosis Antigen 85B Involves Intraphagosomal Formation of Peptide-Major Histocompatibility Complex II Complexes and Is Inhibited by Live Bacilli that Decrease Phagosome Maturation. J. Exp. Med. 194: 1421-1432 [Abstract] [Full Text]
Kusner, D. J., Barton, J. A. (2001). ATP Stimulates Human Macrophages to Kill Intracellular Virulent Mycobacterium tuberculosis Via Calcium-Dependent Phagosome-Lysosome Fusion. J. Immunol. 167: 3308-3315 [Abstract] [Full Text]
Fratti, R. A., Backer, J. M., Gruenberg, J., Corvera, S., Deretic, V. (2001). Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 154: 631-644 [Abstract] [Full Text]
Kisich, K. O., Heifets, L., Higgins, M., Diamond, G. (2001). Antimycobacterial Agent Based on mRNA Encoding Human {beta}-Defensin 2 Enables Primary Macrophages To Restrict Growth of Mycobacterium tuberculosis. Infect. Immun. 69: 2692-2699 [Abstract] [Full Text]
Malik, Z. A., Iyer, S. S., Kusner, D. J. (2001). Mycobacterium tuberculosis Phagosomes Exhibit Altered Calmodulin-Dependent Signal Transduction: Contribution to Inhibition of Phagosome-Lysosome Fusion and Intracellular Survival in Human Macrophages. J. Immunol. 166: 3392-3401 [Abstract] [Full Text]
Neyrolles, O., Gould, K., Gares, M.-P., Brett, S., Janssen, R., O'Gaora, P., Herrmann, J.-L., Prevost, M.-C., Perret, E., Thole, J. E. R., Young, D. (2001). Lipoprotein Access to MHC Class I Presentation During Infection of Murine Macrophages with Live Mycobacteria. J. Immunol. 166: 447-457 [Abstract] [Full Text]
Aldwell, F. E., Dicker, B. L., Da Silva Tatley, F. M., Cross, M. F., Liggett, S., Mackintosh, C. G., Griffin, J. F. T. (2000). Mycobacterium bovis-Infected Cervine Alveolar Macrophages Secrete Lymphoreactive Lipid Antigens. Infect. Immun. 68: 7003-7009 [Abstract] [Full Text]
Ullrich, H.-J., Beatty, W. L., Russell, D. G. (2000). Interaction of Mycobacterium avium-Containing Phagosomes with the Antigen Presentation Pathway. J. Immunol. 165: 6073-6080 [Abstract] [Full Text]
Groger, M., Holnthoner, W., Maurer, D., Lechleitner, S., Wolff, K., Mayr, B. B., Lubitz, W., Petzelbauer, P. (2000). Dermal Microvascular Endothelial Cells Express the 180-kDa Macrophage Mannose Receptor In Situ and In Vitro. J. Immunol. 165: 5428-5434 [Abstract] [Full Text]
Olakanmi, O., Britigan, B. E., Schlesinger, L. S. (2000). Gallium Disrupts Iron Metabolism of Mycobacteria Residing within Human Macrophages. Infect. Immun. 68: 5619-5627 [Abstract] [Full Text]
Garcia, R. C., Banfi, E., Pittis, M. G. (2000). Infection of Macrophage-Like THP-1 Cells with Mycobacterium avium Results in a Decrease in Their Ability to Phosphorylate Nucleolin. Infect. Immun. 68: 3121-3128 [Abstract] [Full Text]
Guerin, I., de Chastellier, C. (2000). Pathogenic Mycobacteria Disrupt the Macrophage Actin Filament Network. Infect. Immun. 68: 2655-2662 [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]
Malik, Z. A., Denning, G. M., Kusner, D. J. (2000). Inhibition of Ca2+ Signaling by Mycobacterium tuberculosis Is Associated with Reduced Phagosome-Lysosome Fusion and Increased Survival within Human Macrophages. J. Exp. Med. 191: 287-302 [Abstract] [Full Text]
Kusner, D. J., Adams, J. (2000). ATP-Induced Killing of Virulent Mycobacterium tuberculosis Within Human Macrophages Requires Phospholipase D. J. Immunol. 164: 379-388 [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]
Gomes, M. S., Paul, S., Moreira, A. L., Appelberg, R., Rabinovitch, M., Kaplan, G. (1999). Survival of Mycobacterium avium and Mycobacterium tuberculosis in Acidified Vacuoles of Murine Macrophages. Infect. Immun. 67: 3199-3206 [Abstract] [Full Text]
Schaible, U., Schlesinger, P., Steinberg, T., Mangel, W., Kobayashi, T, Russell, D. (1999). Parasitophorous vacuoles of Leishmania mexicana acquire macromolecules from the host cell cytosol via two independent routes. J. Cell Sci. 112: 681-693 [Abstract]
Berthet, F., Lagranderie, M., Gounon, P., Laurent-Winter, C., Ensergueix, D., Chavarot, P., Thouron, F., Maranghi, E., Pelicic, V., Portnoï, D., Marchal, G., Gicquel, B. (1998). Attenuation of Virulence by Disruption of the Mycobacterium tuberculosis erp Gene. Science 282: 759-762 [Abstract] [Full Text]
Hackam, D. J., Rotstein, O. D., Zhang, W.-j., Gruenheid, S., Gros, P., Grinstein, S. (1998). Host Resistance to Intracellular Infection: Mutation of Natural Resistance-associated Macrophage Protein 1�(Nramp1) Impairs Phagosomal Acidification. J. Exp. Med. 188: 351-364 [Abstract] [Full Text]
Schaible, U. E., Sturgill-Koszycki, S., Schlesinger, P. H., Russell, D. G. (1998). Cytokine Activation Leads to Acidification and Increases Maturation of Mycobacterium avium-Containing Phagosomes in Murine Macrophages. J. Immunol. 160: 1290-1296 [Abstract] [Full Text]
Desjardins, M., Descoteaux, A. (1997). Inhibition of Phagolysosomal Biogenesis by the Leishmania Lipophosphoglycan. J. Exp. Med. 185: 2061-2068 [Abstract] [Full Text]
Peyron, P., Maridonneau-Parini, I., Stegmann, T. (2001). Fusion of Human Neutrophil Phagosomes with Lysosomes in Vitro. INVOLVEMENT OF TYROSINE KINASES OF THE Src FAMILY AND INHIBITION BY MYCOBACTERIA. J. Biol. Chem. 276: 35512-35517 [Abstract] [Full Text]
Botelho, R. J., Hackam, D. J., Schreiber, A. D., Grinstein, S. (2000). Role of COPI in Phagosome Maturation. J. Biol. Chem. 275: 15717-15727 [Abstract] [Full Text]