Inhibition of phagolysosomal biogenesis by the Leishmania lipophosphoglycan

Journal of Experimental Medicine

Volumn 185, Issue 12, 1997, Pages 2061-2068

  Desjardins, Michel ^a,b,c   Descoteaux, Albert ^a,b,c  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b INRS INSTITUT ARMAND FRAPPIER   (Canada)

^c Fonds de la Rech en S du Quebec ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPHOSPHOGLYCAN;

AMASTIGOTE; ANIMAL CELL; ARTICLE; BIOGENESIS; CELL SURVIVAL; CELL VACUOLE; ENDOCYTOSIS; ENDOSOME; ENZYME INHIBITION; LEISHMANIA; LYSOSOME MEMBRANE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; OPSONIZATION; PRIORITY JOURNAL; PROTOZOON;

ANIMALS; CELL LINE; GLYCOSPHINGOLIPIDS; LEISHMANIA DONOVANI; MICE; PHAGOSOMES;

EID: 0031005660     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.185.12.2061     Document Type: Article

References (51)

1. Turco, S.J., and A. Descoteaux. 1992. The lipophosphoglycan of Leishmania parasites. Annu. Rev. Microbiol. 46:65-94.
2. McConville, M.J., and M.A.J. Ferguson. 1993. The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochem. J. 294:305-324.
3. Pimenta, P.F.P., S.J. Turco, M.J. McConville, P. Lawyer, P. Perkins, and D.L. Sacks. 1992. Stage-specific adhesion of Leishmania promastigotes to the sand fly midgut. Science (Wash. DC). 256:1812-1815.
4. Pimenta, P.F.P., E.M.B. Saraiva, E. Rowton, G.B. Modi, L.A. Garraway, S.M. Beverley, S.J. Turco, and D.L. Sacks. 1994. Evidence that the vectorial competence of phlebotomine sand flies for different species of Leishmania is controlled by structural polymorphisms in the surface lipophosphoglycan. Proc. Natl. Acad. Sci. USA. 91:9155-9159.
5. Butcher, B.A., S.J. Turco, B.A. Hilty, P.F. Pimenta, M. Panunzio, and D.L. Sacks. 1996. Deficiency in β1,3-galactosyl-transferase of a Leishmania major lipophosphoglycan mutant adversely influences the Leishmania-sand fly interaction. J. Biol. Chem. 271:20573-20579.
6. Culley, F.J., R.A. Harris, P.M. Kaye, K.P.W.J. McAdam, and J.G. Raynes. 1996. C-reactive protein binds to a novel ligand on Leishmania donovani and increases uptake into human macrophages. J. Immunol. 156:4691-1696.
7. Handman, E., L.F. Schnur, T.W. Spithill, and G.F. Mitchell. 1986. Passive transfer of Leishmania lipopolysaccharide confers parasite survival in macrophages. J. Immunol. 137:3608-3613.
8. McNeely, T.B., and S.J. Turco. 1990. Requirement of lipophosphoglycan for intracellular survival of Leishmania donovani within human monocytes.J. Immunol. 144:2475-2750.
9. Elhay, M., M. Kelleher, A. Bacic, M.J. McConville, D.L. Tolson, T.W. Pearson, and E. Handman. 1990. Lipophosphoglycan expression and virulence in ricin-resistant variants of Leishmania major. Mol. Biochem. Parasitol. 40:255-268.
10. Eilam, Y., J. El-On, and D.T. Spira. 1985. Leishmania major: excreted factor, calcium ions, and the survival of amastigotes. Exp. Parasitol. 59:161-168.
11. Beverley, S.M., and S.J. Turco. 1995. Identification of genes mediating lipophosphoglycan biosynthesis by functional complementation of Leishmania donovani mutants. Ann. Trop. Med. Parasitol. 89 (Suppl.):11-17.
12. Alexander, J., and K. Vickerman. 1975. Fusion of host cell secondary lysosomes with the parasitophorous vacuoles of Leishmania mexicana-infected macrophages. J. Protozool. 22: 502-508.
13. Chang, K.-P., and D.M. Dwyer. 1976. Multiplication of a human parasite (Leishmania donovani) in phagolysosomes of hamster macrophages in vitro. Science (Wash. DC). 193:678-680.
14. Antoine, J.-C., E. Prina, C. Jouanne, and P. Bongrand. 1990. Parasitophorous vacuoles of Leishmania amazonensis-infected macrophages maintain an acidic pH . Infect. Immun. 58:779-787.
15. Prina, E., J.-C. Antoine, B. Wiederanders, and H. Kirschke. 1990. Localization and activity of various lysosomal proteases in Leishmania amazonensis-infected macrophages. Infect. Immun. 58:1730-1737.
16. Russell, D.G., S. Xu, and P. Chakraborty. 1992. Intracellular trafficking and the parasitophorous vacuole of Leishmania mexicana-infected macrophages. J. Cell Science. 103:1193-1210.
17. Veras, P.S.T., C. de Chastellier, and M. Rabinovitch. 1992. Transfer of zymosan (yeast cell walls) to the parasitophorous vacuoles of macrophages infected with Leishmania amazonensis. J. Exp. Med. 176:639-646.
18. McConville, M.J., and J.M. Blackwell. 1991. Developmental changes in the glycosylated phosphatidylinositols of Leishmania donovani: characterization of the promastigote and amastigote glycolipids. J. Biol. Chem. 266:15170-15179.
19. Turco, S.J., and D.L. Sacks. 1991. Expression of a stage-specific lipophosphoglycan in Leishmania major amastigotes. Mol. Biochem. Parasitol. 45:91-100.
20. Moody, S.F., E. Handman, M.J. McConville, and A. Bacic. 1993. The structure of Leishmania major amastigote lipophosphoglycan. J. Biol. Chem. 268:18457-18466.
21. Chan, J., T. Fujira, P. Brennan, M. McNeil, S.J. Turco, J. Sibille, M. Snapper, P. Aisen, and B.R. Bloom. 1989. Microbial glycolipids: possible virulence factors that scavenge oxygen radicals. Proc. Natl. Acad. Sci. USA. 86:2453-2457.
22. Proudfoot, L., A.V. Nikolaev, G.-J. Feng, X.-Q. Wei, M.A.J. Ferguson, J.S. Brimacombe, and F.Y. Liew. 1996. Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc. Natl. Acad. Sci. USA. 93:10984-10989.
23. Miao, L., A. Stafford, S. Nir, S.J. Turco, T.D. Flanagan, and R.M. Epand. 1995. Potent inhibition of viral fusion by the lipophosphoglycan of Leishmania donovani. Biochemistry. 34:4676-4683.
24. Desjardins, M., L.A. Huber, R.G. Parton, and G. Griffiths. 1994. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with endocytic apparatus. J. Cell Biol. 124:677-688.
25. Desjardins, M. 1995. Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol. 5:183-186.
26. McNeely, T.B., D.L. Tolson, T.W. Pearson, and S.J. Turco. 1990. Characterization of Leishmania donovani variant clones using anti-lipophosphoglycan monoclonal antibodies. Glycobiology. 1:63-69.
27. Descoteaux, A., Y. Luo, S.J. Turco, and S.M. Beverley. 1995. A specialized pathway affecting virulence glycoconjugates of Leishmania. Science (Wash. DC). 269:1869-1872.
28. Rabinowitz, S., H. Horstmann, S. Gordon, and G. Griffiths. 1992. Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages. J. Cell Biol. 116:95-112.
29. Tolson, D.L., S.J. Turco, and T.W. Pearson. 1990. Expression of a repeating phosphorylated disaccharide lipophosphoglycan epitope on the surface of macrophages infected with Leishmania donovani. Infect. Immun. 58:3500-3507.
30. Bates, P.A., I. Hermes, and D.M. Dwyer. 1990. Golgi-mediated post-translational processing of secretory acid phosphatase by Leishmania donovani promastigotes. Mol. Biochem. Parasitol. 39:247-256.
31. Sturgill-Koszycki, S., P.H. Schlesinger, P. Chakraborty, P.L. Haddix, H.L. Collins, A.K. Fok, R.D. Allen, S.L. Gluck, J. Heuser, and D.G. Russell. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science (Wash. DC). 263:678-681.
32. Russell, D.G. J. Dante, and S. Sturgill-Koszycki. 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.
33. Clemens, D.L., and M.A. Horwitz. 1996. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J. Exp. Med. 184:1349-1355.
34. de Chastellier, C., T. Lang, and L. Thilo. 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.
35. Joiner, K.A., S.A. Fuhrman, H.M. Miettinen, L.H. Kasper, and I. Mellman. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science (Wash. DC). 249:641-646.
36. Small, P.L.C., L. Ramakrishnan, and S. Falkow. 1994. Remodeling schemes of intracellular pathogens. Science (Wash. DC). 263:637-639.
37. Finlay, B.B., and S. Falkow. 1989. Common themes in microbial pathogenicity. Microbiol. Rev. 53:210-230.
38. Descoteaux, A., and S.J. Turco. 1993. The lipophosphoglycan of Leishmania and macrophage protein kinase C. Parasitol. Today. 9:468-471.
39. Allen, L.-A.H., and A. Aderem. 1995. A role for MARCKS, the α isoenzyme of protein kinase C and myosin I in zymosan phagocytosis by macrophages. J. Exp. Med. 182:829-840.
40. Giorgione, J.R., S.J. Turco, and R.M. Epand. 1996. Transbilayer inhibition of protein kinase C by the lipophosphoglycan from Leishmania donovani. Proc. Natl. Acad. Sci. USA. 93: 11634-11639.
41. Rosen, A., K.F. Keenan, M. Thelen, A.C. Nairn, and A.A. Aderem. 1990. Activation of protein kinase C results in the displacement of its myristoylated, alanine-rich substrate from punctate structures in macrophage filopodia. J. Exp. Med. 172:1211-1215.
42. Allen, L.-A.H., and A. Aderem. 1995. Protein kinase C regulates MARCKS cycling between the plasma membrane and lysosomes in fibroblasts. EMBO (Eur. Mol. Biol. Organ.) J. 14: 1109-1121.
43. Descoteaux, A., G. Matlashewski, and S.J. Turco. 1992. Inhibition of macrophage protein kinase C-mediated protein phosphorylation by Leishmania donovani lipophosphoglycan. J. Immunol. 149:3008-3015.
44. Descoteaux, A., S.J. Turco, D.L., Sacks, and G. Matlashewski. 1991. Leishmania donovani lipophosphoglycan selectively inhibits signal transduction in macrophages. J. Immunol. 146: 2747-2753.
45. Descoteaux, A., and G. Matlashewski. 1989. C-fos and TNF gene expression in Leishmania donovani-infected macrophages. Mol. Cell. Biol. 9:5223-5227.
46. Olivier, M., R.W. Brownsey, and N.E. Reiner. 1992. Defective stimulus-response coupling in human monocytes infected with Leishmania donovani is associated with altered activation and translocation of protein kinase C. Proc. Natl. Acad. Sci. U.S.A. 89:7481-7485.
47. Goren, M.B., P. D'Arcy Hart, M.R. Young, and J.A. Armstrong. 1976. Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA. 73:2510-2514.
48. Spargo, B.J., L.M. Crowe, T. Ioneda, B.L. Beaman, and J.H. Crowe. 1991. Cord factor (α,α-trehalose 6,6′-dimycolate) inhibits fusion between phospholipid vesicles. Proc. Natl. Acad. Sci. USA. 88:737-740.
49. Gruenheid, S., E. Pinner, M. Desjardins, and P. Gros. 1997. Natural resistance to infection with intracellular parasites: the Nramp1 protein is recruited to the membrane of the phago some. J. Exp. Med. 185:717-730.
50. Desjardins, M., J.E. Celis, G. van Meer, H. Dieplinger, A. Jahraus, G. Griffiths, and L.A. Huber. 1994. Molecular characterization of phagosomes. J. Biol. Chem. 269:32194-32200.
51. Emans, N., N.N. Nzala, and M. Desjardins. 1996. Protein phosphorylation during phagosome maturation. FEBS Lett. 398:37-42.