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Formation and Modification of the Parasitophorous Vacuole Occupied by Toxoplasma Gondii

  • L. David Sibley
  • Christine Pouletty
  • John C. Boothroyd
Part of the NATO ASI Series book series (volume 78)

Abstract

Toxoplasma tachyzoites are able to actively invade and survive within specialized vacuoles in a wide range of vertebrate host cells. The parasite enters a vacuole that is derived from the plasma membrane by invagination, yet these vacuoles differ from standard phagocytic compartments in several respects. The Toxoplasma-containing vacuole, or parasitophorous vacuole (PV), resists acidification [Sibley et al., 1985b] and fusion with lysosomes [Jones and Hirsch 1972]. These vacuoles also resist fusion with vesicles containing soluble tracers for fluid phase endocytosis including Lucifer yellow [Joiner et al., 1990] and with vesicles containing permanent labels such as acridine orange that accumulate in acidic compartments [Sibley et al., 1985a]. While the PV is inert with respect to interactions with the host-cell endocytic network, events within the vacuole are dynamic. During invasion and vacuole formation, the parasite secretes a number of proteins from specialized storage organelles called rhoptries and dense granules. The contents of these secretory organelles are targetted to different sites within the vacuole including the vacuolar membrane and the intravacuolar network that forms a membranous interface within the vacuole [Sibley et al., 1986].

Keywords

Dense Granule Toxoplasma Gondii Parasitophorous Vacuole Congenital Toxoplasmosis Fluid Phase Endocytosis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Achbarou, A., Mercereau-Puijalon, O., Sadak, A., Fortier, B., Leriche, M.A., and Camus, D. [ 1991 ]. Differential targeting of dense granule proteins in the parasitophorous vacuole of Toxoplasma gondii. Parasitol. 103: 321–329.CrossRefGoogle Scholar
  2. Burg, J.L., Perlman, D., Kasper, L.H., Ware, P.L., and Boothroyd, J.C. [ 1988 ] Molecular analysis of the gene encoding the major surface antigen of Toxoplasma gondii. J. Immunol. 141: 3584–3591.PubMedGoogle Scholar
  3. Cesbron-Delauw, M.F., Guy, B. Pierce, R.J., Lenzen, G., Cesbron, J.Y. Charif, H., Lepage, P., Darcy, F., Lecocq, J.P., and Capron A. [ 1989 ]. Molecular characterization of a 23-kilodalton major antigen secreted by Toxoplasma gondii. Proc. Nat. Acad. Sci., USA 86: 7537–7541.CrossRefGoogle Scholar
  4. Charif, H., Darcy, F., Torpier, G., Cesbron-Delauw, M.F., and Capron, A. [ 1990 ]. Toxoplasma gondii: Characterization and localization of antigens secreted from tachyzoites. Exp. Parasitol. 71: 114–124.PubMedCrossRefGoogle Scholar
  5. Darcy, F., Deslee, D., Santoro, F., Charif, H., Auriault, C., Decoster, A., Duquesne, V. and Capron, A., [ 1988 ]. Induction of a protective antibody dependent response against toxoplasmosis by in vitro excreted/secreted antigens from tachyzoites of Toxoplasma gondii. Paras. Immunol. 10: 553–567.CrossRefGoogle Scholar
  6. Decoster, A., Darcy, F., and Capron A. [ 1988 ]. Recognition of Toxoplasma gondii excreted and secreted antigens by human sera from acquired and congenital toxoplasmosis: Identification of markers of acute and chronic infection. Clin. Exp. Immunol. 73: 376–382.PubMedGoogle Scholar
  7. Dubremetz, J.F., Rodriguez, C., and Ferreira E. [ 1985 ]. Toxoplasma gondii: Redistribution of monoclonal antibodies on tchyzoites during host cell invasion. Exp. Parasitol. 59: 24–32.PubMedCrossRefGoogle Scholar
  8. Joiner, K.A., Furhman, S.A., Miettinen, H.M., Kasper, L.H., and Mellman I. [ 1990 ]. Fusion competence of parasitophorous vacuoles in Fc receptor transfected fibroblasts. Science 249: 641–646.PubMedCrossRefGoogle Scholar
  9. Jones, T.C. and Hirsch J.G. [ 1972 ]. The interaction of Toxoplasma gondii and mammalian cells. II The absence of lysosomal fusion with phagocytic vacuoles containing living parasites. J. Exp. Med. 136: 1173–1194.PubMedCrossRefGoogle Scholar
  10. Kasper, L.H., Khan, LA. Ely, K.H., Beulow R., and Boothroyd J.C. [ 1992 ]. Antigen-specific [p30] mouse CD8+ T cells are cytotoxic against Toxoplasma gondii - infected peritoneal macrophages. J. Immunol. 148: 1493–1498.PubMedGoogle Scholar
  11. Leriche, M.A. and Dubremetz J.F. [ 1990 ]. Exocytosis of Toxoplasma dense granules into the parasitophorous vacuole after invasion. Parasitol. Res. 76: 359–362.Google Scholar
  12. Leriche, M.A. and Dubremetz J.F., [ 1991 ]. Characterization of the protein contents of rhoptries and dense granule of Toxoplasma gondii tachyzoites by subcellular fractionation and monoclonal antibodies. Mol. Biochem. Parasitol. 45: 249–260.PubMedCrossRefGoogle Scholar
  13. Nagel, S.D. and Boothroyd, J.C. [ 1989 ]. The major surface antigen, p30, of Toxoplasma gondii is anchored by a glycolipid. J. Biochem. 264: 5569–5574.Google Scholar
  14. Porchet-Hennere, E. and Torpier G. [ 1983 ]. Relations entre Toxoplasma et sa cellule-hote. Protistologica 19: 357–370.Google Scholar
  15. Priance, J.B., Araujo, F.G., Remington, J.S., Burg, J.L., Boothroyd, J.C. and Sharma, S. [ 1989 ]. Cloning of cDNAs encoding a 28-kilodalton antigen of Toxoplasma gondii. Mol. Biochem. Parasitol. 34: 3–14.CrossRefGoogle Scholar
  16. Sibley, L.D. [ 1989 ]. Active modification of host cell phagosomes by Toxoplasma gondii. In: Intracellular Parasitism. Ed. J. Moulder, Boca Raton, CRC. 245–257.Google Scholar
  17. Sibley, L.D. and Boothroyd J.C. [ 1991 ]. Calcium regulated secretion and modification of host-cell endocytic compartments by Toxoplasma. J. Cell Biol. 115: 5a.Google Scholar
  18. Sibley, L.D. and Krahenbuhl J.L. [ 1988 ]. Modification of host cell phagosomes by Toxoplasma gondii involves redistribution of surface proteins and secretion of a 32 kDa protein. E.J. Cell Biol. 47: 81–87.Google Scholar
  19. Sibley, L.D., Krahenbuhl, J.L., Adams, G.M.W., and Weidner, E., [1986]. Toxoplasma modifies macrophage phagosomes by secretion of a vesicular network rich in surface proteins. J. Cell Biol. 103: 867–874.Google Scholar
  20. Sibley, L.D., Krahenbuhl, J.L., and Weidner, E., [ 1985a ]. Lymphokine activation of J774G8 cells and mouse peritoneal macrophages challenged with Toxoplasma gondii. Infect. Immun. 49: 760–764.Google Scholar
  21. Sibley, L.D., Weidner E., and Krahenbuhl, J.L. [ 1985b ]. Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature (Lond.) 315: 416–419.CrossRefGoogle Scholar
  22. Yurko, M.A. and Gluck, S. (1987). Production and characterization of a monoclonal antibody to vacuolar H+ATPase of renal epithelia. J. Biochem. 32: 15770–15779.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1993

Authors and Affiliations

  • L. David Sibley
    • 1
    • 2
  • Christine Pouletty
    • 1
    • 2
  • John C. Boothroyd
    • 1
    • 2
  1. 1.Department of Molecular MicrobiologyWashington University School of Medicine St. LouisUSA
  2. 2.Department of Microbiology and ImmunologyStandford University, School of MedicineStandfordUSA

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