Cholesterol depletion in Mycobacterium avium-infected macrophages overcomes the block in phagosome maturation and leads to the reversible sequestration of viable mycobacteria in phagolysosome-derived autophagic vacuoles

Cellular Microbiology

Volumn 8, Issue 2, 2006, Pages 242-256

  de Chastellier, Chantal ^a   Thilo, Lutz ^b  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b Department of Biomedical Sciences   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; METHYL BETA CYCLODEXTRIN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BACTERICIDAL ACTIVITY; BONE MARROW CELL; CELL VACUOLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; HOST PATHOGEN INTERACTION; LYSOSOME; LYSOSOME MEMBRANE; MACROPHAGE; MOUSE; MYCOBACTERIUM AVIUM; NONHUMAN; PHAGOLYSOSOME; PHAGOSOME; PRIORITY JOURNAL;

ANIMALS; AUTOPHAGY; CHOLESTEROL; INTRACELLULAR MEMBRANES; LYSOSOMES; MACROPHAGES; MEMBRANE FUSION; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MYCOBACTERIUM AVIUM; PHAGOSOMES; VACUOLES;

ANIMALIA; CORYNEBACTERINEAE; MYCOBACTERIUM; MYCOBACTERIUM AVIUM;

EID: 33644816762     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2005.00617.x     Document Type: Article

References (62)

1. Allain, C.C., Poon, L.S., Chan, C.S., Richmond, W., and Fu, P.C. (1974) Enzymatic determination of total serum cholesterol. Clin Chem 20: 470-475.
2. Aniento, F., Emans, N., Griffiths, G., and Gruenberg, J. (1993) Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J Cell Biol 123: 1373-1387.
3. Armstrong, J.A., and D'Arcy Hart, P. (1971) Response of cultured macrophages to Mycobacterium tuberculosis with observations on fusion of lysosomes with phagosomes. J Exp Med 134: 713-740.
4. Beatty, W.L., Rhoades, E.R., Ullrich, H.J., Chatterjee, D., Heuser, J.E., and Russell, D.A. (2000) Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1: 235-247.
5. Botelho, R.J., Scott, C.C., and Grinstein, S. (2004) Phosphoinositide involvement in phagocytosis and phagosome maturation. Curr Top Microbiol Immunol 282: 1-30.
6. Brown, D.A., and London, E. (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14: 111-136.
7. Calle, E., Berciano, M.T., Fernandez, R., and Lafarga, M. (1999) Activation of the autophagy, c-FOS and ubiquitin expression, and nucleolar alterations in Schwann cells precede demyelination in tellurium-induced neuropathy. Acta Neuropathol (Berl) 97: 143-155.
8. Chamberlain, L.H., and Gould, G.W. (2002) The vesicle- and target-SNARE proteins that mediate Glut4 vesicle fusion are localized in detergent-insoluble lipid rafts present on distinct intracellular membranes. J Biol Chem 277: 49750-49754.
9. de Chastellier, C., and Thilo, L. (1997) Phagosome maturation and fusion with lysosomes in relation to surface property and size of the phagocytic particle. Eur J Cell Biol 74: 49-62.
10. de Chastellier, C., and Thilo, L. (1999) Mycobacteria and the endocytic pathway. In Advances in Cell and Molecular Biology of Membranes and Organelles. Gordon, S., and Tartakoff, A. M. (eds) Stamford, CT, USA: JAI Press, pp. 107-135.
11. de Chastellier, C., and Thilo, L. (2002) Pathogenic Mycobacterium avium remodels the phagosome membrane in macrophages within days after infection. Eur J Cell Biol 81: 17-25.
12. de Chastellier, C., Lang, T., and Thilo, L. (1995) Phagocytic processing of the macrophage endoparasite, Mycobacterium avium, in comparison to phagosomes which contain Bacillus subtilis or latex beads. Eur J Cell Biol 68: 167-182.
13. Chua, J., Vergne, I., Master, S., and Deretic, V. (2004) A tale of two lipids: Mycobacterium tuberculosis phagosome maturation arrest. Curr Opin Microbiol 7: 1-7.
14. Clemens, D.L., and Horwitz, M.A. (1995) Characterisation of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181: 257-270.
15. Clemens, D.L., and 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.
16. 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: 2671-2684.
17. Coppens, I., and Joiner, K.A. (2003) Host but not parasite cholesterol controls Toxoplasma cell entry by modulating organelle discharge. Mol Biol Cell 14: 3804-3820.
18. Deretic, V., and Fratti, R.A. (1999) Mycobacterium tuberculosis phagosome. Mol Microbiol 31: 1603-1609.
19. Dermine, J.F., Duclos, S., Garin, J., St-Louis, F., Rea, S., Parton, R.G., and Desjardins, M. (2001) Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J Biol Chem 276: 18507-18512.
20. Desjardins, M. (1995) Biogenesis of phagolysosomes: The 'kiss and run' hypothesis. Trends Cell Biol 5: 183-186.
21. Dorn, B.R., Dunn, W.A., Jr, and Progulske-Fox,, A. (2002) Bacterial interactions with the autophagic pathway. Cell Microbiol 4: 1-10.
22. Dunn, W.A., Jr (1990) Studies on the mechanisms of autophagy: Formation of the autophagic vacuole. J Cell Biol 110: 1923-1933.
23. 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: 631-644.
24. Fratti, R.A., Chua, J., and Deretic, V. (2002) Cellubrevin alterations and Mycobacterium tuberculosis phagosome maturation arrest. J Biol Chem 277: 17320-17326.
25. Fratti, R.A., Chua, J., and 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.
26. Fréhel, C., de Chastellier, C., Offredo, C., and Berche, P. (1991) Intramacrophage growth of Mycobacterium avium during infection of mice. Infect Immun 59: 2207-2214.
27. Fréhel, C., Offredo, C., and de Chastellier, C. (1997) The phagosomal environment protects virulent Mycobacterium avium from killing and destruction by clarithromycin. Infect Immun 65: 2792-2802.
28. Fréhel, C., Canonne-Hergaux, F., Gros, P., and de Chastellier, C. (2002) Effect of Nramp1 on bacterial replication and on maturation of Mycobacterium avium-containing phagosomes in bone marrow-derived mouse macrophages. Cell Microbiol 4: 541-556.
29. Gatfield, J., and Pieters, J. (2000) Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288: 1647-1650.
30. Gorvel, J.P., and de Chastellier, C. (2005) Bacteria spurned by self-absorbed cells. Nat Med 11: 18-19.
31. Griffiths, G., Quinn, P., and Warren, G. (1983) Dissection of the Golgi complex I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus. J Cell Biol 96: 835-850.
32. Harrison, R.E., Bucci, C., Vieira, O.V., Schroer, T.A., and Grinstein, S. (2003) Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: Role of Rab7 and RILP. Mol Cell Biol 23: 6494-6506.
33. Haylett,. T., and Thilo, L. (1986) Limited and selective transfer of plasma membrane glycoproteins to membrane of secondary lysosomes. J Cell Biol 103: 1249-1256.
34. Hur, E.M., Park, Y.S., Lee, B.D., Jang, I.H., Kim, H.S., Kim, T.D., et al. (2004) Sensitization of epidermal growthfactor-induced signaling by bradykinin is mediated by c-Src. Implications for a role of lipid microdomains. J Biol Chem 279: 5852-5860.
35. Kato, M., and Wickner, W. (2001) Ergosterol is required for the Sec18/ ATP-dependent priming step of homotypic vacuole fusion. EMBO J 20: 4035-4040.
36. Kirkegaard, K., Taylor, M.P., and Jackson, W.T. (2004) Cellular autophagy: Surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol 2: 301-314.
37. Koul, A., Herget, T., Klebl, B., and Ullrich, A. (2004) Interplay between mycobacteria and host signalling pathways. Nat Rev Microbiol 2: 189-202.
38. Kusner, D.J. (2005) Mechanisms of mycobacterial persistence in tuberculosis. Clin Immunol 114: 239-247.
39. Lai, E. C. (2003) Lipid rafts make for slippery platforms. J Cell Biol 162: 365-370.
40. Lang, T. (2003) Imaging SNAREs at work in 'unroofed' cells - approaches that may be of general interest for functional studies on membrane proteins. Biochem Soc Trans 31: 861-864
41. Levine, B. (2005) Eating oneself and uninvited guests: Autophagy-related pathways in cellular defense. Cell 120: 159-162.
42. Link, E., McMahon, H., Fischer von Mollard, G., Yamasaki, S., Niemann, H., Sudhof, T.C., and Jahn, R. (1993) Cleavage of cellubrevin by tetanus toxin does not affect fusion of early endosomes. J Biol Chem 268: 18423-18426.
43. 2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J Immunol 170: 2811-2815.
44. Manes, S., del Real, G., and Martinez, A.C. (2003) Pathogens: Raft hijackers. Nat Rev Immunol 3: 557-568.
45. Mizushima, N., Yamamoto, A., Hatano, M., Kobayashi, Y., Kabeya, Y., Suzuki, K., et al. (2001) Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 152: 657-668.
46. Mizushima, N., Ohsumi, Y., and Yoshimori, T. (2002) Autophagosome formation in mammalian cells. Cell Struct Funct 27: 421-429.
47. Orci, L., Halban, P., Perrelet, A., Amherdt, M., Ravazzola, M., and Anderson, R.G.W. (1994) PH-independent and -dependent cleavage of proinsulin in the same secretory vesicle. J Cell Biol 126: 1149-1156.
48. Petiot, A., Pattingre, S., Arico, S., Meley, D., and Codogno, P. (2002) Diversity of signaling controls of macroautophagy in mammalian cells. Cell Struct Funct 27: 431-441.
49. 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: 5186-5191.
50. Pietersen, R., Thilo, L., and de Chastellier, C. (2004) Mycobacterium tuberculosis and Mycobacterium avium modify the composition of the phagosomal membrane in infected macrophages by selective depletion of cell surface-derived glycoconjugates. Eur J Cell Biol 83: 153-158.
51. Russell, D. G. (2001) Mycobacterium tuberculosis: Here today, and here tomorrow. Nat Rev Mol Cell Biol 2: 569-577.
52. Simonsen, A., Lippe, R., Christoforidis, S., Gaullier, J.M., Brech, A., Callaghan, J., et al. (1998) EEA1 links PI (3) K function to Rab5 regulation of endosome fusion. Nature 394: 494-498.
53. Stoorvogel, W., Geuze, H.J., Griffith, J.M., Schwartz, A.L., and Strous, G.J. (1989) Relations between the intracellular pathways of the receptors for transferrin, asialoglycoprotein, and mannose 6-phosphate in human hepatoma cells. J Cell Biol 108: 2137-2148.
54. Stromhaug, P.E., Berg, T.O., Fengsrud, M., and Seglen, P.O. (1998) Purification and characterization of autophagosomes from rat hepatocytes. Biochem J 335: 217-224.
55. Sturgill-Koszycki, S., Schaible, N.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: 6960-6968.
56. Thilo, L., and de Chastellier, C. (2003) Phagosome biogenesis in relation to intracellular survival mechanisms of mycobacteria. In Intracellular Pathogens in Membrane Interactions and Vacuole Biogenesis. Gorvel, J. P. (ed.). New York: Kluwer Academic/Plenum, pp. 153-169.
57. Thilo, L., Stroud, E., and Haylett, T. (1995) Maturation of early endosomes and vesicular traffic to lysosomes in relation to membrane recycling. J Cell Sci 108: 1791-1803.
58. Thompson, C.R., Iyer, S.S., Melrose, N., Van Oosten, R., Johnson, K., Pitson, S.M., et al. (2005) Sphingosine kinase 1 (SK1) is recruited to nascent phagosomes in human macrophages: Inhibition of SK1 translocation by Mycobacterium tuberculosis. J Immunol 174: 3551-3561.
59. 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: 13326-13331.
60. Vieira, O.V., Botelho, R.J., Rameh, L., Brachmann, S.M., Matsuo, T., Davidson, H.W., et al. (2001) Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J Cell Biol 155: 19-25.
61. Vieira, O.V., Bucci, C., Harrison, R.E., Trimble, W.S., Lanzetti, L., Gruenberg, J., et al. (2003) Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol Cell Biol 23: 2501-2514.
62. Ward, D.M., Pevsner, J., Scullion, M.A., Vaughn, M., and Kaplan, J. (2000) Syntaxin 7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages. Mol Biol Cell 11: 2327-2333.