The metabolic activity of Mycobacterium tuberculosis, assessed by use of a novel inducible GFP expression system, correlates with its capacity to inhibit phagosomal maturation and acidification in human macrophages

Molecular Microbiology

Volumn 68, Issue 4, 2008, Pages 1047-1060

  Lee, Bai Yu ^a   Clemens, Daniel L ^a   Horwitz, Marcus A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN; GREEN FLUORESCENT PROTEIN;

ACIDIFICATION; ARTICLE; BACTERIAL METABOLISM; CELL MATURATION; CONTROLLED STUDY; CORRELATION ANALYSIS; FLUORESCENCE; GENE CONSTRUCT; HUMAN; HUMAN CELL; INHIBITION KINETICS; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACIDS; ANTIGENS, CD; CELL LINE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; ISOPROPYL THIOGALACTOSIDE; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; PHAGOSOMES; PLASMIDS; PLATELET MEMBRANE GLYCOPROTEINS; RECOMBINANT PROTEINS; XANTHENES;

MYCOBACTERIUM TUBERCULOSIS;

EID: 42549158689     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06214.x     Document Type: Article

References (39)

1. Armstrong, J.A. Hart, P.D. (1971) Response of cultured macrophages to Mycobacterium tuberculosis with observations on fusion of lysosomes with phagosomes. J Exp Med 134 : 713 740.
2. Bachrach, G., Colston, M.J., Bercovier, H., Bar-Nir, D., Anderson, C. Papavinasasundaram, K.G. (2000) A new single-copy mycobacterial plasmid, pMF1, from Mycobacterium fortuitum which is compatible with the pAL5000 replicon. Microbiology 146 : 297 303.
3. Blokpoel, M.C., O'Toole, R., Smeulders, M.J. Williams, H.D. (2003) Development and application of unstable GFP variants to kinetic studies of mycobacterial gene expression. J Microbiol Methods 54 : 203 211.
4. Clemens, D.L. (1996) Characterization of the Mycobacterium tuberculosis phagosome. Trends Microbiol 4 : 113 118.
5. Clemens, D.L. Horwitz, M.A. (1995) Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181 : 257 270.
6. Clemens, D.L. Horwitz, M.A. (1996) The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J Exp Med 184 : 1349 1355.
7. Clemens, D.L., Lee, B.Y. Horwitz, M.A. (2000a) 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.
8. Clemens, D.L., Lee, B.Y. Horwitz, M.A. (2000b) Mycobacterium tuberculosis and Legionella pneumophila phagosomes exhibit arrested maturation despite acquisition of Rab7. Infect Immun 68 : 5154 5166.
9. Clemens, D.L., Lee, B.Y. Horwitz, M.A. (2002) The Mycobacterium tuberculosis phagosome in human macrophages is isolated from the host cell cytoplasm. Infect Immun 70 : 5800 5807.
10. Crowle, A.J., Dahl, R., Ross, E. 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 1831.
11. Dancz, C.E., Haraga, A., Portnoy, D.A. Higgins, D.E. (2002) Inducible control of virulence gene expression in Listeria monocytogenes: temporal requirement of listeriolysin O during intracellular infection. J Bacteriol 184 : 5935 5945.
12. Dargelos, E., Moyen, C., Dedieu, S., Veschambre, P., Poussard, S., Vuillier-Devillers, K., et al. (2002) Development of an inducible system to assess p94 (CAPN3) function in cultured muscle cells. J Biotechnol 96 : 271 279.
13. Deretic, V., Via, L.E., Fratti, R.A. Deretic, D. (1997) Mycobacterial phagosome maturation, rab proteins, and intracellular trafficking. Electrophoresis 18 : 2542 2547.
14. Desjardins, M. (1995) Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol 5 : 183 186.
15. Desjardins, M., Huber, L.A., Parton, R.G. Griffiths, G. (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 124 : 677 688.
16. Fratti, R.A., Vergne, I., Chua, J., Skidmore, J. Deretic, V. (2000) Regulators of membrane trafficking and Mycobacterium tuberculosis phagosome maturation block. Electrophoresis 21 : 3378 3385.
17. Goren, M.B., Hart, P.D., Young, M.R. Armstrong, J.A. (1976) Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis. Proc Natl Acad Sci USA 73 : 2510 2514.
18. Harth, G., Maslesa-Galic, S. Horwitz, M.A. (2004) A two-plasmid system for stable, selective-pressure-independent expression of multiple extracellular proteins in mycobacteria. Microbiology 150 : 2143 2151.
19. Howard, N.S., Gomez, J.E., Ko, C. Bishai, W.R. (1995) Color selection with a hygromycin-resistance-based Escherichia coli-mycobacterial shuttle vector. Gene 166 : 181 182.
20. Lepperdinger, G., Strobl, B. Kreil, G. (1998) HYAL2, a human gene expressed in many cells, encodes a lysosomal hyaluronidase with a novel type of specificity. J Biol Chem 273 : 22466 22470.
21. Malik, Z.A., Denning, G.M. 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 : 287 302.
22. 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.
23. McDonough, K.A., Kress, Y. Bloom, B.R. (1993) Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 61 : 2763 2773.
24. Mwandumba, H.C., Russell, D.G., Nyirenda, M.H., Anderson, J., White, S.A., Molyneux, M.E. Squire, S.B. (2004) Mycobacterium tuberculosis resides in nonacidified vacuoles in endocytically competent alveolar macrophages from patients with tuberculosis and HIV infection. J Immunol 172 : 4592 4598.
25. Myrvik, Q.N., Leake, E.S. Wright, M.J. (1984) Disruption of phagosomal membranes of normal alveolar macrophages by the H37Rv strain of Mycobacterium tuberculosis. A correlate of virulence. Am Rev Respir Dis 129 : 322 328.
26. Oh, Y.K. Straubinger, R.M. (1996) Intracellular fate of Mycobacterium avium: use of dual-label spectrofluorometry to investigate the influence of bacterial viability and opsonization on phagosomal pH and phagosome-lysosome interaction. Infect Immun 64 : 319 325.
27. Pitt, A., Mayorga, L.S., Schwartz, A.L. Stahl, P.D. (1992) Transport of phagosomal components to an endosomal compartment. J Biol Chem 267 : 126 132.
28. Russell, D.G. (1994) Immunoelectron microscopy of endosomal trafficking in macrophages infected with microbial pathogens. Methods Cell Biol 45 : 277 288.
29. Russell, D.G., Dant, J. 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 4773.
30. Stover, C.K., de la Cruz, V.F., Fuerst, T.R., Burlein, J.E., Benson, L.A., Bennett, L.T., et al. (1991) New use of BCG for recombinant vaccines. Nature 351 : 458 460.
31. Sturgill-Koszycki, S., Schlesinger, P.H., Chakraborty, P., Haddix, P.L., Collins, H.L., Fok, A.K., et al. (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263 : 678 681.
32. Szaflarski, W. Nierhaus, K.H. (2007) Question 7: optimized energy consumption for protein synthesis. Orig Life Evol Biosph 37 : 423 428.
33. Tsien, R.Y. (1998) The green fluorescent protein. Annu Rev Biochem 67 : 509 544.
34. Tullius, M.V., Harth, G. Horwitz, M.A. (2003) Glutamine synthetase (GlnA1) is essential for growth of Mycobacterium tuberculosis in human macrophages and in guinea pigs. Infect Immun 71 : 3927 3936.
35. Via, L.E., Deretic, D., Ulmer, R.J., Hibler, N.S., Huber, L.A. 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 13331.
36. Via, L.E., Fratti, R.A., McFalone, M., Pagan-Ramos, E., Deretic, D. Deretic, V. (1998) Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111 : 897 905.
37. van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., et al. (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129 : 1287 1298.
38. Wubbolts, R., Fernandez-Borja, M., Oomen, L., Verwoerd, D., Janssen, H., Calafat, J., et al. (1996) Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J Cell Biol 135 : 611 622.
39. Xu, S., Cooper, A., Sturgill-Koszycki, S., van Heyningen, T., Chatterjee, D., Orme, I., et al. (1994) Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J Immunol 153 : 2568 2578.