Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis

EMBO Journal

Volumn 15, Issue 24, 1996, Pages 6960-6968

  Sturgill Koszycki, Sheila ^a   Schaible, Ulrich E ^a,b   Russell, David G ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

Endosome; Macrophage; Mycobacterium; Phagocyte; Phagosome

Indexed keywords

CATHEPSIN D; IMMUNOGLOBULIN G; MEMBRANE PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ACIDIFICATION; ARTICLE; CONTROLLED STUDY; ENDOSOME; MYCOBACTERIUM AVIUM; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING;

EID: 0030481130     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb01088.x     Document Type: Article

References (49)

1. 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, 713-740.
2. Beron,W., Alvarez-Dominguez,C., Mayorga,L. and Stahl,P.D. (1995) Membrane trafficking along the phagocytic pathway. Trends Cell Biol., 5, 100-104.
3. Chakraborty,P., Sturgill-Koszycki,S. and Russell,D.G. (1994) Isolation and characterization of pathogen-containing phagosomes. Methods Cell Biol., 45, 261-276.
4. Chen,J.W., Cha,Y., Yuksel,K.U., Gracy,R.W. and August,J.T. (1988) Isolation and sequencing of a cDNA clone encoding lysosomal membrane glycoprotein mouse LAMP-1. Sequence similarity to proteins bearing onco-differentiation antigens. J. Biol. Chem., 263, 8754-8758.
5. Clague,M.J., Urbe,S., Aniento,F. and Gruenberg,J. (1994) Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem., 269, 21-24.
6. Clemens,D.L. and Horwitz,M.A. (1992) Membrane sorting during phagocytosis: selective exclusion of major histocompatibility complex molecules but not complement receptor CR3 during conventional and coiling phagocytosis. J. Exp. Med., 175, 1317-1326.
7. 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, 257-270.
8. Dautry-Varsat,A., Ciechanover,A. and Lodish,H.F. (1983) pH and the recycling of transferrin during receptor-mediated endocytosis. Proc. Natl Acad. Sci. USA, 80, 2258-2262.
9. de Chastellier,C., Frehel,C., Offredo,C. and Skamene,E. (1993) Implication of phagosome-lysosome fusion in restriction of Mycobacterium avium growth in bone marrow macrophages from genetically resistant mice. Infect. Immun., 61, 3775-3784.
10. de Chastellier,C., Lang,T. and Thilo,L. (1995) Phagocytic processing of the macrophage endoparasite Mycobacterium avium in comparison to phagosomes which contain Bacillus subtilus or latex beads. Eur. J. Cell Biol., 68, 167-176.
11. Delbrueck,R., Desel,C., von Figura,K. and Hille-Rehfeld,A. (1994) Proteolytic processing of cathepsin D in prelysosomal organelles. Eur. J. Cell Biol., 64, 7-14.
12. Desjardins,M. (1995) Biogenesis of phagolysosomes: the kiss and run hypothesis. Trends Cell Biol., 5, 183-186.
13. Desjardins,M., Huber,L.A., Parton,R.G. and Griffiths,G. (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol., 124, 677-688.
14. Diedrich,J.F., Staskus,K.A., Retzel,E.F. and Haase,A.T. (1990) Nucleotide sequence of a cDNA encoding mouse cathepsin D. Nucleic Acids Res., 18, 7184.
15. Fuchs,R., Ellinger,A., Pavelka,M., Mellman,I. and Klapper,H. (1994) Rat liver endocytic coated vesicles do not exhibit ATP-dependent acidification in vitro. Proc. Natl Acad. Sci. USA. 91, 4811-4815.
16. Ghosh,R.N. and Maxfield,F.R. (1995) Evidence for nonvectorial. retrograde transferrin trafficking in early endosomes of HEp2 cells. J. Cell Biol., 128, 549-561.
17. Gorvel,J.P., Chavier,P., Zerial,M. and Gruenberg,J. (1991) Rab 5 controls early endosome fusion in vitro. Cell, 64, 915-925.
18. Grinstein,S., Nanda,A., Lukacs,G. and Rotstein,O. (1992) V-ATPases in phagocytic cells. J. Exp. Biol., 172, 179-192.
19. Gruenberg,J. and Maxfield,F.R. (1995) Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol., 7, 552-563.
20. Grusby,M.J., Mitchell,S.C. and Glimcher,L.H. (1990) Molecular cloning of mouse cathepsin D. Nucleic Acids Res., 18, 4008.
21. Hart,P.D. and Armstrong,J.A. (1974) Strain virulence and the lysosomal response in macrophages infected with Mycobacterium tuberculosis. Infect. Immun., 10, 742-746.
22. Hart,P.D. and Young,M.R. (1978) Manipulations of the phagosomelysosome fusion response in cultured macrophages. Enhancement of fusion by chloroquine and other amines. Exp. Cell Res., 114, 486-490.
23. Hart,P.D. and Young,M.R. (1991) Ammonium chloride, an inhibitor of phagosome-lysosome fusion in macrophages, concurrently induces phagosome-endosome fusion, and opens a novel pathway: studies of a pathogenic mycobacterium and a nonpathogenic yeast. J. Exp. Med., 174, 881-889.
24. Hart,P.D., Armstrong,J.A., Brown,C.A. and Draper,P. (1972) Ultrastructural study of the behavior of macrophages toward parasitic mycobacteria. Infect. Immun., 5, 803-807.
25. Hart,P.D., Young,M.R., Gordon,A.H. and Sullivan,K.H. (1987) Inhibition of phagosome-lysosome fusion in macrophages by certain mycobacteria can be explained by inhibition of lysosomal movements observed after phagocytosis. J. Exp. Med., 166, 933-946.
26. Johnson,L.S., Dunn,K.W., Pytowsky,B. and McGraw,T.E. (1993) Endosome acidification and receptor trafficking; bafilomycin A1 slows receptor exit by a mechanism involving the receptor's internalization motif. Mol. Biol. Cell., 4, 1251-1266.
27. Klausner,R.D., Ashwell,G., Van Renswoude,J., Harford,J.B. and Bridges,K.R. (1983) Binding of apotransferrin in K562 cells: explanation of the transferrin cycle. Proc. Natl Acad. Sci. USA, 80, 2263-2266.
28. Larsen,L.B., Boisen,A. and Peterson,T.E. (1993) Procathepsin D cannot autoactivate to cathepsin D at acid pH. FEBS Lett., 319, 54-58.
29. Ludwig,T., Griffiths,G. and Hoflack,B. (1991) Distribution of newly synthesized lysosomal enzymes in the endocytic pathway of normal rat kidney cells. J. Cell Biol., 115, 1561-1572.
30. Mayorga,L.S., Bertini,F. and Stahl,P.D. (1991) Fusion of newly-formed phagosomes with endosomes in intact cells and in a cell-free system. J. Biol. Chem., 266, 6511-6517.
31. McDonough,K.A. and Kress,Y. (1995) Cytotoxicity for lung epithelial cells is a virulence-associated phenotype of Mycobacterium tuberculosis. Infect. Immun., 63, 4802-4811.
32. Mellman,I. (1992) The importance of being acid: the role of acidification in intracellular traffic. J. Exp. Biol., 172, 39-45.
33. Nanda,A., Gukovskaya,A., Tseng,J. and Grinstein,S. (1992) Activation of vacuolar-type proton pumps by proton kinase C. J. Biol. Chem., 267, 22740-22746.
34. Nathan,C.F. and Hibbs,J.J. (1991) Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol., 3, 65-70.
35. Oh,Y.K. and 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.
36. Orme,J.M., Furney,S.K., Skinner,P.S., Roberts,A.D., Brennan,P.J., Russell,D.G., Shiratsuchi,H., Ellner,J.J. and Weiser,W.Y. (1993) Inhibition of growth of Mycobacterium avium in murine and human mononuclear phagocytes by migration inhibitory factor. Infect. Immun., 61, 338-342.
37. Pitt,A.L., Mayorga,L.S., Stahl,P.D. and Schwartz,A.L. (1992) Alterations in the protein composition of maturing phagosomes. J. Clin. Invest., 90, 1978-1983.
38. Richo,G. and Connor,G.E. (1991) Proteolytic activation of human procathepsin D. In Dunn,B.M. (ed.), Structure and Function of Aspartic Proteinases. Plenum Press, New York, pp. 289-296.
39. Rijnboutt,S., Stoorvogel,W., Geuze,H.J. and Strous,G.J. (1992) Identification of subcellular compartments involved in biosynthetic processing of cathepsin D. J. Biol. Chem., 267, 15665-15672.
40. Rohrer,J., Schweizer,A., Russell,D.G. and Kornfeld,S. (1996) The targeting of LAMP 1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J. Cell Biol., 132, 565-576.
41. Russell,D.G. (1994) Immunoelectron microscopy of endosomal trafficking in macrophages infected with microbial pathogens. Methods Cell Biol., 45, 277-288.
42. Russell,D.G., Xu,S. and Chakraborty,P. (1992) Intracellular trafficking and the parasitophorous vacuole of Leishmania mexicana-infected macrophages. J. Cell. Sci., 103, 1193-1210.
43. 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, 4764-4773.
44. Schmid,S., Fuchs,R., Keilian,M., Helenius,A. and Mellman,I. (1989) Acidification of endosome subpopulations in wild-type Chinese hamster ovary cells and temperature-sensitive acidification-defective mutants. J. Cell Biol., 108, 1291-1300.
45. Sibley,L.D., Franzblau,S.G. and Krahenbuhl,J.L. (1987) Intracellular fate of Mycobacterium leprae in normal and activated mouse macrophages. Infect. Immun., 55, 680-685.
46. Sturgill-Koszycki,S. et al. (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science, 263, 678-681.
47. van Weert,A.W.M., Dunn,K.W., Geuze,H.J., Maxfield,F.R. and Stoorvogel,W. (1995) Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol., 130, 821-834.
48. Xie,X.-S., Crider,B.P., Ma,Y.-M. and Stone,D.K. (1994) Role of the 50-57-kDa heterodimer in the function of the clathrin-coated vesicle proton pump. J. Biol. Chem., 269, 25809-26815.
49. Xu,S., Cooper,A., Sturgill-Koszycki,S., van Heyningen,T., Chatterjee,D., Orme,I., Allen,P. and Russell,D.G. (1994) Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol., 153, 2568-2578.