Skip to main content Accessibility help
×
Hostname: page-component-848d4c4894-sjtt6 Total loading time: 0 Render date: 2024-07-03T00:27:01.708Z Has data issue: false hasContentIssue false

8 - Mycobacterium tuberculosis: mechanisms of phagocytosis and intracellular survival

Published online by Cambridge University Press:  07 August 2009

Joel D. Ernst
Affiliation:
Departments of Medicine and Microbiology New York University School of Medicine
Andrea Wolf
Affiliation:
Departments of Medicine and Microbiology New York University School of Medicine
Joel D. Ernst
Affiliation:
New York University
Olle Stendahl
Affiliation:
Linköpings Universitet, Sweden
Get access

Summary

INTRODUCTION

Mycobacterium tuberculosis, the cause of tuberculosis, has infected an estimated one-third of the world's human population and causes more deaths per year than any other single bacterial pathogen (Corbett et al. 2003). Although tuberculosis is most frequently an infection of the lungs, it can affect virtually any organ of the body (Raviglione & O'Brien 2004). In most individuals the infection remains latent without symptoms or transmission, but in approximately 10% the infection progresses to active disease and kills at least half of these. Untreated, active disease provides the opportunity for transmission of M. tuberculosis to other individuals through coughing up of the bacteria by an infected person, which provides droplet nuclei that are inhaled into the lung alveoli and establish a new infection. Tuberculosis is most common in developing countries; because T-lymphocyte-mediated cellular immunity is essential for control of the infection, the ongoing epidemic of HIV infection in regions with a high prevalence of tuberculosis is worsening an already severe problem. Moreover, the development of multiple drug resistance in M. tuberculosis has amplified the problems of treatment of tuberculosis in many parts of the world.

LIFE CYCLE OF M. TUBERCULOSIS

Although bacteria are not classically considered to have morphologically distinct stages representing phases of their life cycle as eucaryotic parasites do, it is clear that pathogenic bacteria such as M. tuberculosis adapt to distinct environmental niches by major alterations in their patterns of gene expression (Schnappinger et al. 2003).

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Armstrong, J. A., and Hart, P. D.. 1971. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 134: 713–40CrossRefGoogle ScholarPubMed
Armstrong, J. A., and Hart, P. D.. 1975. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival. J Exp Med 142: 1–16CrossRefGoogle ScholarPubMed
Astarie-Dequeker, C., N'Diaye, E. N., Cabec, V., Rittig, M. G., Prandi, J., and Maridonneau-Parini, I.. 1999. The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages. Infect Immun 67: 469–77Google ScholarPubMed
Balcewicz-Sablinska, M. K., Keane, J., Kornfeld, H., and Remold, H. G.. 1998. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol 161: 2636–41Google ScholarPubMed
Beharka, A. A., Gaynor, C. D., Kang, B. K., Voelker, D. R., McCormack, F. X., and Schlesinger, L. S.. 2002. Pulmonary surfactant protein A up-regulates activity of the mannose receptor, a pattern recognition receptor expressed on human macrophages. J Immunol 169: 3565–73CrossRefGoogle ScholarPubMed
Bodnar, K. A., Serbina, N. V., and Flynn, J. L.. 2001. Fate of Mycobacterium tuberculosis within murine dendritic cells. Infect Immun 69: 800–9CrossRefGoogle ScholarPubMed
Chackerian, A. A., Alt, J. M., Perera, T. V., Dascher, C. C., and Behar, S. M.. 2002. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect Immun 70: 4501–9CrossRefGoogle ScholarPubMed
Chua, J., and Deretic, V.. 2004. Mycobacterium tuberculosis reprograms waves of phosphatidylinositol 3-phosphate on phagosomal organelles. J Biol Chem 279: 36982–92CrossRefGoogle ScholarPubMed
Clemens, D. L., and Horwitz, M. A.. 1995. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181: 257–70CrossRefGoogle ScholarPubMed
Clemens, D. L., Lee, B. Y., and 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: 2671–84CrossRefGoogle ScholarPubMed
Corbett, E. L., Watt, C. J., Walker, N.et al. 2003. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 163: 1009–21.CrossRefGoogle ScholarPubMed
Cowley, S. C., and Elkins, K. L.. 2003. CD4+ T cells mediate IFN-gamma-independent control of Mycobacterium tuberculosis infection both in vitro and in vivo. J Immunol 171: 4689–99CrossRefGoogle ScholarPubMed
Crowle, A. J., Dahl, R., Ross, E., and May, M. H.. 1991. Evidence that vesicles containing living, virulent Mycobacterium tuberculosis or Mycobacterium avium in cultured human macrophages are not acidic. Infect Immun 59: 1823–31Google Scholar
Cywes, C., Godenir, N. L., H. C. Hoppe et al. 1996. Nonopsonic binding of Mycobacterium tuberculosis to human complement receptor type 3 expressed in Chinese hamster ovary cells. Infect Immun 64: 5373–83Google ScholarPubMed
Cywes, C., Hoppe, H. C., Daffe, M., and Ehlers, M. R.. 1997. Nonopsonic binding of Mycobacterium tuberculosis to complement receptor type 3 is mediated by capsular polysaccharides and is strain dependent. Infect Immun 65: 4258–66Google ScholarPubMed
Downing, J. F., Pasula, R., Wright, J. R., Twigg, H. L., III, and Martin, W. J., 2nd. 1995. Surfactant protein a promotes attachment of Mycobacterium tuberculosis to alveolar macrophages during infection with human immunodeficiency virus. Proc Natl Acad Sci USA 92: 4848–52CrossRefGoogle ScholarPubMed
Ernst, J. D. 1998. Macrophage receptors for Mycobacterium tuberculosis. Infect Immun 66: 1277–81Google ScholarPubMed
Ernst, J. D. 2000. Bacterial inhibition of phagocytosis. Cell Microbiol 2: 379–86CrossRefGoogle ScholarPubMed
Ezekowitz, R. A., Sastry, K., Bailly, P., and Warner, A.. 1990. Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J Exp Med 172: 1785–94CrossRefGoogle Scholar
Ferguson, J. S., Voelker, D. R., McCormack, F. X., and Schlesinger, L. S.. 1999. Surfactant protein D binds to Mycobacterium tuberculosis bacilli and lipoarabinomannan via carbohydrate-lectin interactions resulting in reduced phagocytosis of the bacteria by macrophages. J Immunol 163: 312–21Google ScholarPubMed
Ferguson, J. S., Weis, J. J., Martin, J. L., and Schlesinger, L. S.. 2004. Complement protein C3 binding to Mycobacterium tuberculosis is initiated by the classical pathway in human bronchoalveolar lavage fluid. Infect Immun 72: 2564–73CrossRefGoogle ScholarPubMed
Flynn, J. L., and Chan, J.. 2001. Immunology of tuberculosis. A Rev Immunol 19: 93–129CrossRefGoogle ScholarPubMed
Fratti, R. A., Backer, J. M., Gruenberg, J., Corvera, S., and Deretic, V.. 2001. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 154: 631–44CrossRefGoogle ScholarPubMed
Fratti, R. A., Chua, J., Vergne, I., and Deretic, V.. 2003. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci USA 100: 5437–42CrossRefGoogle ScholarPubMed
Garred, P., Harboe, M., Oettinger, T., Koch, C., and Svejgaard, A.. 1994. Dual role of mannan-binding protein in infections: another case of heterosis? Eur J Immunogenet 21: 125–31
Gatfield, J., and Pieters, J.. 2000. Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288: 1647–50CrossRefGoogle ScholarPubMed
Gaynor, C. D., McCormack, F. X., Voelker, D. R., McGowan, S. E., and Schlesinger, L. S.. 1995. Pulmonary surfactant protein A mediates enhanced phagocytosis of Mycobacterium tuberculosis by a direct interaction with human macrophages. J Immunol 155: 5343–51Google ScholarPubMed
Geijtenbeek, T. B., Vliet, S. J., Koppel, E. A.et al. 2003. Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197: 7–17CrossRefGoogle ScholarPubMed
Henderson, R. A., Watkins, S. C., and Flynn, J. L.. 1997. Activation of human dendritic cells following infection with Mycobacterium tuberculosis. J Immunol 159: 635–43Google ScholarPubMed
Hetland, G., and Wiker, H. G.. 1994. Antigen 85C on Mycobacterium bovis, BCG and M. tuberculosis promotes monocyte-CR3-mediated uptake of microbeads coated with mycobacterial products. Immunology 82: 445–9Google Scholar
Hetland, G., Wiker, H. G., Hogasen, K., Hamasur, B., Svenson, S. B., and Harboe, M.. 1998. Involvement of antilipoarabinomannan antibodies in classical complement activation in tuberculosis. Clin Diagn Lab Immunol 5: 211–18Google ScholarPubMed
Hickman, S. P., Chan, J., and Salgame, P.. 2002. Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J Immunol 168: 4636–42CrossRefGoogle ScholarPubMed
Hirsch, C. S., Ellner, J. J., Russell, D. G., and Rich, E. A.. 1994. Complement receptor-mediated uptake and tumor necrosis factor-alpha-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J Immunol 152: 743–53Google ScholarPubMed
Hu, C., Mayadas-Norton, T., Tanaka, K., Chan, J., and Salgame, P.. 2000. Mycobacterium tuberculosis infection in complement receptor 3-deficient mice. J Immunol 165: 2596–602CrossRefGoogle ScholarPubMed
Jiao, X., Lo-Man, R., Guermonprez, P.et al. 2002. Dendritic cells are host cells for mycobacteria in vivo that trigger innate and acquired immunity. J Immunol 168: 1294–301CrossRefGoogle ScholarPubMed
Kang, B. K., and Schlesinger, L. S.. 1998. Characterization of mannose receptor-dependent phagocytosis mediated by Mycobacterium tuberculosis lipoarabinomannan. Infect Immun 66: 2769–77Google ScholarPubMed
Keane, J., Remold, H. G., and Kornfeld, H.. 2000. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 164: 2016–20CrossRefGoogle ScholarPubMed
Keane, J., Shurtleff, B., and Kornfeld, H.. 2002. TNF-dependent BALB/c murine macrophage apoptosis following Mycobacterium tuberculosis infection inhibits bacillary growth in an IFN-gamma independent manner. Tuberculosis (Edinb) 82: 55–61CrossRefGoogle Scholar
Leemans, J. C., Juffermans, N. P., Florquin, S.et al. 2001. Depletion of alveolar macrophages exerts protective effects in pulmonary tuberculosis in mice. J Immunol 166: 4604–11CrossRefGoogle ScholarPubMed
Leemans, J. C., Florquin, S., Heikens, M., Pals, S. T., Neut, R., and Poll, T.. 2003. CD44 is a macrophage binding site for Mycobacterium tuberculosis that mediates macrophage recruitment and protective immunity against tuberculosis. J Clin Invest 111: 681–9CrossRefGoogle ScholarPubMed
Leemans, J. C., Thepen, T., Weijer, S.et al. 2005. Macrophages play a dual role during pulmonary tuberculosis in mice. J Infect Dis 191: 65–74CrossRefGoogle ScholarPubMed
Lopez Ramirez, G. M., Rom, W. N., Ciotoli, C.et al. 1994. Mycobacterium tuberculosis alters expression of adhesion molecules on monocytic cells. Infect Immun 62: 2515–20Google ScholarPubMed
Majeed, M., Perskvist, N., Ernst, J. D., Orselius, K., and Stendahl, O.. 1998. Roles of calcium and annexins in phagocytosis and elimination of an attenuated strain of Mycobacterium tuberculosis in human neutrophils. Microb Pathog 24: 309–20CrossRefGoogle ScholarPubMed
Malik, Z. A., Denning, G. M., and Kusner, D. J.. 2000. Inhibition of Ca(2+) signaling by Mycobacterium tuberculosis is associated with reduced phagosome-lysosome fusion and increased survival within human macrophages. J Exp Med 191: 287–302CrossRefGoogle ScholarPubMed
Malik, Z. A., Thompson, C. R., Hashimi, S., Porter, B., Iyer, S. S., and Kusner, D. J.. 2003. Cutting edge: Mycobacterium tuberculosis blocks Ca2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J Immunol 170: 2811–15CrossRefGoogle ScholarPubMed
McDonough, K. A., Kress, Y., and Bloom, B. R.. 1993. Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 61: 2763–73Google ScholarPubMed
McKinney, J. D., Honer zu Bentrup, K., Munoz-Elias, E. J.et al. 2000. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735–8CrossRefGoogle ScholarPubMed
Melo, M. D., Catchpole, I. R., Haggar, G., and Stokes, R. W.. 2000. Utilization of CD11b knockout mice to characterize the role of complement receptor 3 (CR3, CD11b/CD18) in the growth of Mycobacterium tuberculosis in macrophages. Cell Immunol 205: 13–23CrossRefGoogle ScholarPubMed
Menozzi, F. D., Bischoff, R., Fort, E., Brennan, M. J., and Locht, C.. 1998. Molecular characterization of the mycobacterial heparin-binding hemagglutinin, a mycobacterial adhesin. Proc Natl Acad Sci USA 95: 12625–30CrossRefGoogle ScholarPubMed
Mogues, T., Goodrich, M. E., Ryan, L., LaCourse, R., and North, R. J.. 2001. The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J Exp Med 193: 271–80CrossRefGoogle ScholarPubMed
Mosser, D. M., and Edelson, P. J.. 1985. The mouse macrophage receptor for C3bi (CR3) is a major mechanism in the phagocytosis of Leishmania promastigotes. J Immunol 135: 2785–9Google ScholarPubMed
Mosser, D. M., and Edelson, P. J.. 1987. The third component of complement (C3) is responsible for the intracellular survival of Leishmania major. Nature 327: 329–31CrossRefGoogle ScholarPubMed
Mueller-Ortiz, S. L., Wanger, A. R., and Norris, S. J.. 2001. Mycobacterial protein HbhA binds human complement component C3. Infect Immun 69: 7501–11CrossRefGoogle ScholarPubMed
Mueller-Ortiz, S. L., Sepulveda, E., Olsen, M. R., Jagannath, C., Wanger, A. R., and Norris, S. J.. 2002. Decreased infectivity despite unaltered C3 binding by a DeltahbhA mutant of Mycobacterium tuberculosis. Infect Immun 70: 6751–60CrossRefGoogle ScholarPubMed
Mwandumba, H. C., Russell, D. G., Nyirenda, M. H.et al. 2004. Mycobacterium tuberculosis resides in nonacidified vacuoles in endocytically competent alveolar macrophages from patients with tuberculosis and HIV infection. J Immunol 172: 4592–8CrossRefGoogle ScholarPubMed
Patki, V., Virbasius, J., Lane, W. S., Toh, B. H., Shpetner, H. S., and Corvera, S.. 1997. Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 94: 7326–30CrossRefGoogle ScholarPubMed
Perez, E., Samper, S., Bordas, Y., Guilhot, C., Gicquel, B., and Martin, C.. 2001. An essential role for phoP in Mycobacterium tuberculosis virulence. Mol Microbiol 41: 179–87CrossRefGoogle ScholarPubMed
Perskvist, N., Long, M., Stendahl, O., and Zheng, L.. 2002. Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol 168: 6358–65CrossRefGoogle ScholarPubMed
Peters, W., and Ernst, J. D.. 2003. Mechanisms of cell recruitment in the immune response to Mycobacterium tuberculosis. Microbes Infect 5: 151–8CrossRefGoogle ScholarPubMed
Peters, W., Scott, H. M., Chambers, H. F., Flynn, J. L., Charo, I. F., and Ernst, J. D.. 2001. Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 98: 7958–63CrossRefGoogle ScholarPubMed
Peters, W., Cyster, J. G., Mack, M.et al. 2004. CCR2-dependent trafficking of F4/80dim macrophages and CD11cdim/intermediate dendritic cells is crucial for T cell recruitment to lungs infected with Mycobacterium tuberculosis. J Immunol 172: 7647–53CrossRefGoogle Scholar
Pethe, K., Swenson, D. L., Alonso, S., Anderson, J., Wang, C., and Russell, D. G.. 2004. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc Natl Acad Sci USA 101: 13642–7CrossRefGoogle ScholarPubMed
Peyron, P., Bordier, C., N'Diaye, E. N., and Maridonneau-Parini, I.. 2000. Nonopsonic phagocytosis of Mycobacterium kansasii by human neutrophils depends on cholesterol and is mediated by CR3 associated with glycosylphosphatidylinositol-anchored proteins. J Immunol 165: 5186–91CrossRefGoogle ScholarPubMed
Ramanathan, V. D., Curtis, J., and Turk, J. L.. 1980. Activation of the alternative pathway of complement by mycobacteria and cord factor. Infect Immun 29: 30–5Google ScholarPubMed
Raviglione, M. C., and R. C. O'Brien. 2004. Tuberculosis. In Harrison's Principles of Internal Medicine. Kasper, D. L., Braunwald, E., Fauci, A. S.et al., editors, pp. 953–66. New York: McGraw Hill.Google Scholar
Rich, A. R. 1944. The Pathogenesis of Tuberculosis.Springfield, IL: C. C. Thomas.Google Scholar
Riendeau, C. J., and Kornfeld, H.. 2003. THP-1 cell apoptosis in response to Mycobacterial infection. Infect Immun 71: 254–9CrossRefGoogle ScholarPubMed
Russell, D. G., Dant, J., and Sturgill-Koszycki, S.. 1996. Mycobacterium avium- and Mycobacterium tuberculosis-containing vacuoles are dynamic, fusion-competent vesicles that are accessible to glycosphingolipids from the host cell plasmalemma. J Immunol 156: 4764–73Google ScholarPubMed
Sassetti, C. M., and Rubin, E. J.. 2003. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100: 12989–94CrossRefGoogle ScholarPubMed
Schaible, U. E., Sturgill-Koszycki, S., Schlesinger, P. H., and Russell, D. G.. 1998. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J Immunol 160: 1290–6Google ScholarPubMed
Schlesinger, L. S. 1993. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J Immunol 150: 2920–30Google Scholar
Schlesinger, L. S., Bellinger-Kawahara, C. G., Payne, N. R., and Horwitz, M. A.. 1990. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J Immunol 144: 2771–80Google ScholarPubMed
Schlesinger, L. S., Hull, S. R., and Kaufman, T. M.. 1994. Binding of the terminal mannosyl units of lipoarabinomannan from a virulent strain of Mycobacterium tuberculosis to human macrophages. J Immunol 152: 4070–9Google ScholarPubMed
Schlesinger, L. S., Kaufman, T. M., Iyer, S., Hull, S. R., and Marchiando, L. K.. 1996. Differences in mannose receptor-mediated uptake of lipoarabinomannan from virulent and attenuated strains of Mycobacterium tuberculosis by human macrophages. J Immunol 157: 4568–75Google ScholarPubMed
Schnappinger, D., Ehrt, S., M. I. Voskuil et al. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198: 693–704CrossRefGoogle ScholarPubMed
Schorey, J. S., Carroll, M. C., and Brown, E. J.. 1997. A macrophage invasion mechanism of pathogenic mycobacteria. Science 277: 1091–3CrossRefGoogle ScholarPubMed
Seiler, P., Aichele, P., Bandermann, S.et al. 2003. Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur J Immunol 33: 2676–86CrossRefGoogle ScholarPubMed
Shepard, C. C. 1957. Growth characteristics of tubercle bacilli and certain other mycobacteria in HeLa cells. J Exp Med 105: 39–55CrossRefGoogle ScholarPubMed
Shin, J. S., Gao, Z., and Abraham, S. N.. 2000. Involvement of cellular caveolae in bacterial entry into mast cells. Science 289: 785–8CrossRefGoogle ScholarPubMed
Simonsen, A., Lippe, R., Christoforidis, S.et al. 1998. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394: 494–8CrossRefGoogle ScholarPubMed
Simonsen, A., Gaullier, J. M., D'Arrigo, A., and Stenmark, H.. 1999. The Rab5 effector EEA1 interacts directly with syntaxin-6. J Biol Chem 274: 28857–60CrossRefGoogle ScholarPubMed
Stamm, L. M., Morisaki, J. H., Gao, L. Y.et al. 2003. Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J Exp Med 198: 1361–8CrossRefGoogle ScholarPubMed
Stokes, R. W., and Speert, D. P.. 1995. Lipoarabinomannan inhibits nonopsonic binding of Mycobacterium tuberculosis to murine macrophages. J Immunol 155: 1361–9Google ScholarPubMed
Stokes, R. W., Norris-Jones, R., Brooks, D. E., Beveridge, T. J., Doxsee, D., and Thorson, L. M.. 2004. The glycan-rich outer layer of the cell wall of Mycobacterium tuberculosis acts as an antiphagocytic capsule limiting the association of the bacterium with macrophages. Infect Immun 72: 5676–86CrossRefGoogle Scholar
Sturgill-Koszycki, S., Schlesinger, P. H., Chakraborty, P.et al. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263: 678–81CrossRefGoogle ScholarPubMed
Sturgill-Koszycki, S., Schaible, U. E., and Russell, D. G.. 1996. Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J 15: 6960–8Google Scholar
Tailleux, L., Neyrolles, O., Honore-Bouakline, S.et al. 2003a. Constrained intracellular survival of Mycobacterium tuberculosis in human dendritic cells. J Immunol 170: 1939–48CrossRefGoogle Scholar
Tailleux, L., Schwartz, O., Herrmann, J. L.et al. 2003b. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197: 121–7CrossRefGoogle Scholar
Taylor, M. E., Conary, J. T., Lennartz, M. R., Stahl, P. D., and Drickamer, K.. 1990. Primary structure of the mannose receptor contains multiple motifs resembling carbohydrate-recognition domains. J Biol Chem 265: 12156–62Google ScholarPubMed
Velasco-Velazquez, M. A., Barrera, D., Gonzalez-Arenas, A., Rosales, C., and Agramonte-Hevia, J.. 2003. Macrophage–Mycobacterium tuberculosis interactions: role of complement receptor 3. Microb Pathog 35: 125–31CrossRefGoogle ScholarPubMed
Vergne, I., Chua, J., and Deretic, V.. 2003. Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J Exp Med 198: 653–9CrossRefGoogle ScholarPubMed
Via, L. E., Deretic, D., Ulmer, R. J., Hibler, N. S., Huber, L. A., and Deretic, V.. 1997. Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 272: 13326–31CrossRefGoogle ScholarPubMed
Walburger, A., Koul, A., Ferrari, G., Nguyen, L.et al. 2004. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304: 1800–4CrossRefGoogle ScholarPubMed
Xia, Y., and Ross, G. D.. 1999. Generation of recombinant fragments of CD11b expressing the functional beta-glucan-binding lectin site of CR3 (CD11b/CD18). J Immunol 162: 7285–93Google Scholar
Xu, S., Cooper, A., Sturgill-Koszycki, S.et al. 1994. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J Immunol 153: 2568–78Google ScholarPubMed
Zimmerli, S., Edwards, S., and Ernst, J. D.. 1996a. Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages. Am J Respir Cell Mol Biol 15: 760–70CrossRefGoogle Scholar
Zimmerli, S., Majeed, M., Gustavsson, M., Stendahl, O., Sanan, D. A., and Ernst, J. D.. 1996b. Phagosome-lysosome fusion is a calcium-independent event in macrophages. J Cell Biol 132: 49–61CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×