Leishmania promastigotes require lipophosphoglycan to actively modulate the fusion properties of phagosomes at an early step of phagocytosis

Cellular Microbiology

Volumn 2, Issue 2, 2000, Pages 115-126

  Dermine, Jean François ^a   Scianimanico, Sandra ^a   Privé, Charles ^b   Descoteaux, Albert ^b   Desjardins, Michel ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPHOSPHOGLYCAN;

ANIMAL CELL; ARTICLE; ELECTRON MICROSCOPY; LEISHMANIA; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; MACROPHAGE ACTIVATION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; QUANTITATIVE DIAGNOSIS; SURVIVAL;

ACID PHOSPHATASE; ANIMALS; CELL LINE; ENDOSOMES; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOSPHINGOLIPIDS; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; LEISHMANIASIS; MACROPHAGES; MICE; PHAGOCYTOSIS; PHAGOSOMES;

ANIMALIA; INSECTA; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; MAMMALIA;

EID: 0034085602     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-5822.2000.00037.x     Document Type: Article

References (62)

1. Aderem, A., and Underhill, D.M. (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17: 593-623.
2. Alexander, J., and Russell, D.G. (1992) The interaction of Leishmania species with macrophages. Adv Parasitol 31: 175-254.
3. Alexander, J., and Vickerman, K. (1975) Fusion of host cell secondary lysosomes with the parasitophorous vacuoles of Leishmania mexicana-infected macrophages. J Protozool 22: 502-508.
4. Antoine, J.-C., Prina, E., Jouanne, C., and Bongrand, P. (1990) Parasitophorous vacuoles of Leishmania amazonensis-infected macrophages maintain an acidic pH. Infect Immun 58: 779-787.
5. Antoine, J.-C., Prina, E., Lang, T., and Courret, N. (1998) The biogenesis and properties of the parasitophorous vacuoles that harbour Leishmania in murine macrophages. Trends Microbiol 6: 392-401.
6. Armstrong, J.A., and Hart, P.D. (1971) Response of cultured macrophages to Mycobacterium tuberculosis with observation on fusion of lysosomes with phagosomes. J Exp Med 134: 713-740.
7. Barker, L.P., George, K.M., Falkow, S., and Small, P.L.C. (1997) Differential trafficking of live and dead Mycobacterium marinum organisms in macrophages. Infect Immun 65: 1497-1504.
8. Benchimol, M., and de Souza, W. (1981) Leishmania mexicana amazonensis: attachment to the membrane of the phagocytic vacuole of macrophages in vivo. Z Parasitenkd 66: 25-29.
9. Butcher, B.A., Turco, S.J., Hilty, B.A., Pimenta, P.F., Panunzio, M., and Sacks, D.L. (1996) Deficiency in beta 1,3-galactosyl-transferase of a Leishmania major lipophosphoglycan mutant adversely influences the Leishmania-sand fly interaction. J Biol Chem 271: 20573-20579.
10. Chang, K.P., and Dwyer, D.M. (1976) Multiplication of a human parasite (Leishmania donovani) in phagolysosomes of hamster macrophages in vitro. Science 193: 678-680.
11. 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.
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. 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.
14. Dermine, J.F., and Desjardins, M. (1999) Survival of intracellular pathogens within macrophages. Protoplasma 210: 11-24.
15. Descoteaux, A., and Matlashewski, G. (1989) c-fos and tumor necrosis factor gene expression in Leishmania donovani-infected macrophages. Mol Cell Biol 9: 5223-5227.
16. Descoteaux, A., Matlashewski, G., and Turco, S.J. (1992) Inhibition of macrophage protein kinase C-mediated protein phosphorylation by Leishmania donovani lipophosphoglycan. J Immunol 149: 3008-3015.
17. Descoteaux, A., Garraway, L.A., Ryan, K.A., Garrity, L.K., Turco, S.J., and Beverley, S.M. (1994) Identification of genes by functional complementation in protozoan parasite Leishmania. In Methods in Molecular Genetics, Vol. 1. Adolph, K.W. (ed.). San Diego: Academic Press, pp. 22-48.
18. Descoteaux, A., Luo, Y., Turco, S.J., and Beverley, S.M. (1995) A specialized pathway affecting virulence glycoconjugates of Leishmania. Science 269: 1869-1872.
19. Desjardins, M. (1995) Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol 5: 183-186.
20. Desjardins, M., and Descoteaux, A. (1997) Inhibition of phagolysosomal biogenesis by the Leishmania lipophosphoglycan. J Exp Med 185: 2061-2068.
21. Desjardins, M., and Descoteaux, A. (1999) Phagocytosis of Leishmania: interaction with the host and intracellular trafficking. In Advances in Cell and Molecular Biology of Membranes and Organelles, Vol. 6. Tartakoff, A., and Gordon, S. (eds). Greenwich, CT: JAI Press, pp. 297-316.
22. Desjardins, M.L.A., Huber, R.G., and Parton, and Griffiths, G. (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 124: 677-688.
23. Desjardins, M., Nzala, N.N., Corsini, R., and Rondeau, C. (1997) Maturation of phagosomes is accompanied by changes in their fusion properties and size-selective acquisition of solute materials from endosomes. J Cell Sci 110: 2303-2314.
24. Easterbrook, M.D., Levy, M.H., Gomez, A.M., Turco, S.J., Epand, R.M., and Rosenthal, K.L. (1995) Inhibition of HIV-1-induced syncytia formation and infectivity by lipophosphoglycan from Leishmania. J Acquir Immune Defic Syndr Hum Retrovirol 10: 496-505.
25. Feng, Y., Press, B., and Wandinger-Ness, A. (1995) Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 131: 1435-1452.
26. Ferrari, G., Langen, H., Naito, M., and Pieters, J. (1999) A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97: 435-447.
27. Finlay, B.B., and Falkow, S. (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136-169.
28. Giorgione, J.R., Turco, S.J., and Epand, R.M. (1996) Transbilayer inhibition of protein kinase C by the lipophosphoglycan from Leishmania donovani. Proc Natl Acad Sci USA 93: 11634-11639.
29. Haas, A. (1998) Reprogramming the phagocytic pathway - intracellular pathogens and their vacuoles. Mol Membr Biol 15: 103-121.
30. Huang, C., and Turco, S.J. (1993) Defective galactofuranose addition in lipophosphoglycan biosynthesis in a mutant of Leishmania donovani. J Biol Chem 268: 24060-24066.
31. Ilg, T., Stierhof, Y.-D., Wiese, M., McConville, M.J., and Overath, P. (1994) Characterization of phosphoglycan-containing secretory products of Leishmania. Parasitology 108: S63-S71.
32. Katakura, K., and Kobayashi, A. (1988) Acid phosphatase activity of virulent and avirulent clones of Leishmania donovani promastigotes. Infect Immun 56: 2856-2860.
33. Lang, T., Hellio, R., Kaye, P.M., and Antoine, J.-C. (1994) Leishmania donovani-infected macrophages: characterization of the parasitophorous vacuole and potential role of this organelle in antigen presentation. J Cell Sci 107: 2137-2150.
34. McConville, M.J., Schnur, L.F., Jaffe, C., and Schneider, P. (1995) Structure of Leishmania lipophosphoglycan: inter- and intra-specific polymorphism in Old World species. Biochem J 310: 807-818.
35. Martin, I., Turco, S.J., Epand, R.M., and Ruysschaert, J.M. (1998) Lipophosphoglycan of Leishmania donovani inhibits lipid vesicle fusion induced by the N-terminal extremity of viral fusogenic simian immunodeficiency virus protein. Eur J Biochem 258: 150-156.
36. Mauel, J., Schnyder, J., and Baggiolini, M. (1984) Intracellular parasite killing induced by electron carriers. II. Correlation between parasite killing and the induction of oxidative events in macrophages. Mol Biochem Parasitol 13: 97-110.
37. Méresse, S., Gorvel, J.-P., and Chavrier, P. (1995) The rab7 GTPase resides on a vesicular compartment connected to lysosomes. J Cell Sci 108: 3349-3358.
38. Miao, L., Stafford, A., Nir, S., Turco, S.J., Flanagan, T.D., and Epand, R.M. (1995) Potent inhibition of viral fusion by the lipophosphoglycan of Leishmania donovani. Biochemistry 34: 4676-4683.
39. Orlandi, Jr, P.A., and Turco, S.J. (1987) Structure of the lipid moiety of the Leishmania donovani lipophosphoglycan. J Biol Chem 262: 10384-10391.
40. Pizarro-Cerdá, J., Moreno, E., Sanguedolce, V., Mege, J.L., and Gorvel, J.-P. (1998) Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66: 2387-2392.
41. Pizarro-Cerdá, J., Desjardins, M., Moreno, E., Akira, S., and Gorvel, J.-P. (1999) Modulation of endocytosis in nuclear factor IL-6(-/-) macrophages is responsible for a high susceptibility to intracellular bacterial infection. J Immunol 162: 3519-3526.
42. Prina, E., Antoine, J.-C., Wiederanders, B., and Kirschke, H. (1990) Localization and activity of various lysosomal proteases in Leishmania amazonensis-infected macrophages. Infect Immun 58: 1730-1737.
43. Prina, E., Lang, T., Glaichenhaus, N., and Antoine, J.-C. (1996) Presentation of the protective parasite antigen LACK by Leishmania-infected macrophages. J Immunol 156: 4318-4327.
44. Puentes, S.M., Sacks, D.L., da Silva, R.P., and Joiner, K.A. (1988) Complement binding by two developmental stages of Leishmania major promastigotes varying in expression of a surface lipophosphoglycan. J Exp Med 167: 887-902.
45. Puentes, S.M., Da Silva, R.P., Sacks, D.L., Hammer, C.H., and Joiner, K.A. (1990) Serum resistance of metacyclic stage Leishmania major promastigotes is due to release of C5b-9. J Immunol 145: 4311-4316.
46. Rabinovitch, M., Topper, G., Cristello, P., and Rich, A. (1985) Receptor-mediated entry of peroxidases into the parasitophorous vacuoles of macrophages infected with Leishmania mexicana amazonensis. J Leukoc Biol 37: 247-261.
47. Rasmusson, B.J., Flanagan, T.D., Turco, S.J., Epand, R.M., and Petersen, N.O. (1998) Fusion of Sendai virus and individual host cells and inhibition of fusion by lipophosphoglycan measured with image correlation spectroscopy. Biochim Biophys Acta 1404: 338-352.
48. 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.
49. Ryan, K.A., Garraway, L.A., Descoteaux, A., Turco, S.J., and Beverley, S.M. (1993) Isolation of virulence genes directing surface glycosyl-phosphatidylinositol synthesis by functional complementation of Leishmania. Proc Natl Acad Sci USA 90: 8609-8613.
50. Scianimanico, S., Desrosiers, M., Dermine, J.-F., Méresse, S., Descoteaux, A., and Desjardins, M. (1999) Impaired recruitment of the small GTPase rab7 correlates with the inhibition of phagosome maturation by Leishmania donovani promastigotes. Cell Microbiol 1: 19-32.
51. Shepherd, V.L., Stahl, P.D., Bernd, P., and Rabinovitch, M. (1983) Receptor-mediated entry of beta-glucuronidase into the parasitophorous vacuoles of macrophages infected with Leishmania mexicana amazonensis. J Exp Med 157: 1471-1482.
52. Sinai, A.P., and Joiner, K.A. (1997) Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu Rev Microbiol 51: 415-462.
53. St-Denis, A., Caouras, V., Gervais, F., and Descoteaux, A. (1999) Role of PKC-α in the control of infection by intracellular pathogens in macrophages. J Immunol 163: 5505-5511.
54. Steele-Mortimer, O., Méresse, S., Gorvel, J.-P., Toh, B.H., and Finlay, B.B. (1999) Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1: 33-49.
55. Tolson, D.L., Turco, S.J., Beecroft, R.P., and Pearson, T.W. (1989) The immunochemical structure and surface arrangement of Leishmania donovani lipophosphoglycan determined using monoclonal antibodies. Mol Biochem Parasitol 35: 109-118.
56. Turco, S.J., and Descoteaux, A. (1992) The lipophosphoglycan of Leishmania parasites. Annu Rev Microbiol 46: 65-94.
57. Turco, S.J., Hull, S.R., Orlandi, Jr, P.A., Shepherd, S.D., Homans, S.W., Dwek, R.A., et al. (1987) Structure of the major carbohydrate fragment of the Leishmania donovani lipophosphoglycan. Biochemistry 26: 6233-6238.
58. Turco, S.J., Orlandi, Jr, P.A., Homans, S.W., Ferguson, M.A., Dwek, R.A., and Rademacher, T.W. (1989) Structure of the phosphosaccharide-inositol core of the Leishmania donovani lipophosphoglycan. J Biol Chem 264: 6711-6715.
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. Vitelli, R., Santillo, M., Lattero, D., Chiariello, M., Bifulco, M., Bruni, C.B., et al. (1997) Role of the small GTPase Rab7 in the late endocytic pathway. J Biol Chem 272: 4391-4397.
61. 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.
62. Zilberstein, D., and Shapira, M. (1994) The role of pH and temperature in the development of Leishmania parasites. Annu Rev Microbiol 48: 449-470.