Parasite–host cell interactions in toxoplasmosis: New avenues for intervention?

Expert Reviews in Molecular Medicine

Volumn 3, Issue 2, 2001, Pages 1-20

  Coppens, Isabelle ^a   Joiner, Keith A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

host cell manipulation; intracellular protozoan; nutrition; parasitophorous vacuole; Toxoplasma gondii

Indexed keywords

EID: 85012561994     PISSN: 14623994     EISSN: 14623994     Source Type: Journal    
DOI: 10.1017/S1462399401002277     Document Type: Article

References (157)

1. Dubey, J.P. (1977) Toxoplasma, Hammondia, Besnotia, Sarcocystis, and other tissue cyst-forming coccidia of man and animals. In Parasitic Protozoa III (Kreier, J.P., ed.), pp. 101–237, Academic Press, New York, NY, USA
2. Krahenbuhl, J.L. and Remington, J.S. (1982) The immunology of Toxoplasma and toxoplasmosis. In Immunology of Parasitic Infections (Cohen, S. and Warren, K.S., eds), pp. 356–421, Blackwell Science, Oxford, UK
3. Dubey, J.P. and Beattie, C.P. (1988) Toxoplasmosis of Animals and Man, CRC, Boca Raton, FL, USA
4. Dubey, J.P., Lindsay, D.S. and Speer, C.A. (1998) Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev 11, 267–299, PubMed ID: 98225751
5. Jomaa, H. et al. (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285, 1573–1576, PubMed ID: 99407027
6. McFadden, G.I. and Roos, D.S. (1999) Apicomplexan plastids as drug targets. Trends Microbiol 7, 328–333, PubMed ID: 99362812
7. Jones, T.C., Yeh, S. and Hirsch, J.G. (1972) The interaction between Toxoplasma gondii and mammalian cells. I. Mechanism of entry and intracellular fate of the parasite. J Exp Med 136, 1157–1172, PubMed ID: 73030933
8. Sibley, L.D., Weidner, E. and Krahenbuhl, J.L. (1985) Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature 315, 416–419, PubMed ID: 85213866
9. Joiner, K.A. et al. (1990) Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249, 641–646, PubMed ID: 90341792
10. Mordue, D.G. et al. (1999) Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp Parasitol 92, 87–99, PubMed ID: 99296818
11. Schwab, J.C., Beckers, C.J. and Joiner, K.A. (1994) The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc Natl Acad Sci U S A 91, 509–513, PubMed ID: 94119916
12. Sibley, L.D. et al. (1995) Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J Cell Sci 108, 1669–1677, PubMed ID: 95340695
13. de Melo, E.J., de Carvalho, T.U. and de Souza, W. (1992) Penetration of Toxoplasma gondii into host cells induces changes in the distribution of the mitochondria and the endoplasmic reticulum. Cell Struct Funct 17, 311–317, PubMed ID: 93113698
14. Lindsay, D.S. et al. (1993) Association of host cell mitochondria with developing Toxoplasma gondii tissue cysts. Am J Vet Res 54, 1663–1667, PubMed ID: 94071260
15. Sinai, A.P., Webster, P. and Joiner, K.A. (1997) Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J Cell Sci 110, 2117–2128, PubMed ID: 98017833
16. Desmonts, G. and Couvreur, J. (1974) Congenital toxoplasmosis. A prospective study of 378 pregnancies. N Engl J Med 290, 1110–1116, PubMed ID: 74138485
17. Beaman, M.H. et al. (1995) Toxoplasma gondii. In Principles and Practice of Infectious Diseases (Mandell, G.L., Bennett, J.E. and Dolin, R., eds), pp. 2455–2475, Churchill Livingston, New York, NY, USA
18. Wong, S.Y. and Remington, J.S. (1993) Biology of Toxoplasma gondii. Aids 7, 299–316, PubMed ID: 93228876
19. Jacobs, L. (1956) Propagation, morphology and biology of Toxoplasma. Ann NY Acad Sci 64, 154–179
20. Radke, J.R. and White, M.W. (1998) A cell cycle model for the tachyzoite of Toxoplasma gondii using the Herpes simplex virus thymidine kinase. Mol Biochem Parasitol 94, 237–247, PubMed ID: 98418770
21. Dvorak, J.A. and Howe, C.L. (1977) Toxoplasma gondii-vertebrate cell interactions. I. The influence of bicarbonate ion, CO2, pH and host cell culture age on the invasion of vertebrate cells in vitro. J Protozool 24, 416–419, PubMed ID: 78028711
22. Youn, J.H. et al. (1991) Cell cycle-dependent entry of Toxoplasma gondii into synchronized HL-60 cells. Kisaengchunghak Chapchi 29, 121–128, PubMed ID: 92062640
23. Siverman, J.A. and Joiner, K.A. (1996) Toxoplasma-host cell interaction. In Host Response to Intracellular Pathogens (Kaufman, S.H.E., ed.), pp. 313–338, Landers, Austin, TX, USA
24. Furtado, G.C., Cao, Y. and Joiner, K.A. (1992) Laminin on Toxoplasma gondii mediates parasite binding to the beta 1 integrin receptor alpha 6 beta 1 on human foreskin fibroblasts and Chinese hamster ovary cells. Infect Immun 60, 4925–4931, PubMed ID: 93014216
25. Furtado, G.C. et al. (1992) Laminin enhances binding of Toxoplasma gondii tachyzoites to J774 murine macrophage cells. Infect Immun 60, 2337–2342, PubMed ID: 92267647
26. Carruthers, V.B. et al. (2000) Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect Immun 68, 4005–4011, PubMed ID: 20316026
27. Grimwood, J. and Smith, J.E. (1992) Toxoplasma gondii: the role of a 30-kDa surface protein in host cell invasion. Exp Parasitol 74, 106–111, PubMed ID: 92111672
28. Grimwood, J. and Smith, J.E. (1996) Toxoplasma gondii: the role of parasite surface and secreted proteins in host cell invasion. Int J Parasitol 26, 169–173, PubMed ID: 96231050
29. Mineo, J.R. et al. (1993) Antibodies to Toxoplasma gondii major surface protein (SAG-1, P30) inhibit infection of host cells and are produced in murine intestine after peroral infection. J Immunol 150, 3951–3964, PubMed ID: 93232602
30. Boothroyd, J.C. et al. (1998) The surface of Toxoplasma: more and less. Int J Parasitol 28, 3–9, PubMed ID: 98162855
31. Kimata, I. and Tanabe, K. (1982) Invasion by Toxoplasma gondii of ATP-depleted and ATP-restored chick embryo erythrocytes. J Gen Microbiol 128, 2499–2501, PubMed ID: 83110892
32. Schwartzman, J.D. and Pfefferkorn, E.R. (1983) Immunofluorescent localization of myosin at the anterior pole of the coccidian, Toxoplasma gondii. J Protozool 30, 657–661, PubMed ID: 84114527
33. Schwartzman, J.D. et al. (1985) Detection of the microtubule cytoskeleton of the coccidian Toxoplasma gondii and the hemoflagellate Leishmania donovani by monoclonal antibodies specific for beta-tubulin. J Protozool 32, 747–749, PubMed ID: 86062324
34. Werk, R. (1985) How does Toxoplasma gondii enter host cells? Rev Infect Dis 7, 449–457, PubMed ID: 85300091
35. Endo, T. et al. (1988) Detection and localization of actin in Toxoplasma gondii. Parasitol Res 75, 102–106, PubMed ID: 89184358
36. Ryning, F.W. and Remington, J.S. (1978) Effect of cytochalasin D on Toxoplasma gondii cell entry. Infect Immun 20, 739–743, PubMed ID: 78217362
37. Russell, D.G. and Sinden, R.E. (1981) The role of the cytoskeleton in the motility of coccidian sporozoites. J Cell Sci 50, 345–359, PubMed ID: 82098306
38. Dobrowolski, J.M. and Sibley, L.D. (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84, 933–939, PubMed ID: 96182653
39. Dobrowolski, J.M., Carruthers, V.B. and Sibley, L.D. (1997) Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol Microbiol 26, 163–173, PubMed ID: 98043546
40. Morrissette, N.S., Murray, J.M. and Roos, D.S. (1997) Subpellicular microtubules associate with an intramembranous particle lattice in the protozoan parasite Toxoplasma gondii. J Cell Sci 110, 35–42, PubMed ID: 97164035
41. Nichols, B.A. and Chiappino, M.L. (1987) Cytoskeleton of Toxoplasma gondii. J Protozool 34, 217–226, PubMed ID: 87225830
42. Dobrowolski, J.M., Niesman, I.R. and Sibley, L.D. (1997) Actin in the parasite Toxoplasma gondii is encoded by a single copy gene, ACT1 and exists primarily in a globular form. Cell Motil Cytoskeleton 37, 253–262, PubMed ID: 97371641
43. Poupel, O. and Tardieux, I. (1999) Toxoplasma gondii motility and host cell invasiveness are drastically impaired by jasplakinolide, a cyclic peptide stabilizing F-actin. Microbes Infect 1, 653–662, PubMed ID: 20079440
44. Heintzelman, M.B. and Schwartzman, J.D. (1997) A novel class of unconventional myosins from Toxoplasma gondii [published erratum appears in J Mol Biol 2000 Mar 31; 297(3): 829]. J Mol Biol 271, 139–146, PubMed ID: 97445175
45. Hettmann, C. et al. (2000) A dibasic motif in the tail of a class XIV apicomplexan myosin is an essential determinant of plasma membrane localization. Mol Biol Cell 11, 1385–1400, PubMed ID: 20214828
46. Achbarou, A. et al. (1991) Differential targeting of dense granule proteins in the parasitophorous vacuole of Toxoplasma gondii. Parasitology 103 Pt 3, 321–329, PubMed ID: 92140872
47. Carruthers, V.B. and Sibley, L.D. (1997) Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73, 114–123, PubMed ID: 97351942
48. Ngo, H.M., Hoppe, H.C. and Joiner, K.A. (2000) Differential sorting and post-secretory targeting of proteins in parasitic invasion. Trends Cell Biol 10, 67–72, PubMed ID: 20126820
49. Nichols, B.A., Chiappino, M.L. and O'Connor, G.R. (1983) Secretion from the rhoptries of Toxoplasma gondii during host-cell invasion. J Ultrastruct Res 83, 85–98, PubMed ID: 83216268
50. Saffer, L.D., Long Krug, S.A. and Schwartzman, J.D. (1989) The role of phospholipase in host cell penetration by Toxoplasma gondii. Am J Trop Med Hyg 40, 145–149, PubMed ID: 89148557
51. Saffer, L.D. and Schwartzman, J.D. (1991) A soluble phospholipase of Toxoplasma gondii associated with host cell penetration. J Protozool 38, 454–460, PubMed ID: 92014877
52. Ricard, J. et al. (1999) Toxoplasma gondii: role of the phosphatidylcholine-specific phospholipase C during cell invasion and intracellular development. Exp Parasitol 91, 231–237, PubMed ID: 99172325
53. Conseil, V., Soete, M. and Dubremetz, J.F. (1999) Serine protease inhibitors block invasion of host cells by Toxoplasma gondii. Antimicrob Agents Chemother 43, 1358–1361, PubMed ID: 99277993
54. Garcia-Réguet, N. et al. (2000) The microneme protein MIC3 of Toxoplasma gondii is a secretory adhesin that binds to both the surface of the host cells and the surface of the parasite. Cell Microbiol 2, 353–364
55. Robson, K.J. et al. (1988) A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 335, 79–82, PubMed ID: 88318952
56. Wan, K.L. et al. (1997) Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol Biochem Parasitol 84, 203–214, PubMed ID: 97237562
57. Carruthers, V.B., Sherman, G.D. and Sibley, L.D. (2000) The Toxoplasma adhesive protein MIC2 is proteolytically processed at multiple sites by two parasite-derived proteases. J Biol Chem 275, 14346–14353, PubMed ID: 20261559
58. Morisaki, J.H., Heuser, J.E. and Sibley, L.D. (1995) Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J Cell Sci 108, 2457–2464, PubMed ID: 95403585
59. Schwartzman, J.D. and Saffer, L.D. (1992) How Toxoplasma gondii gets in and out of host cells. Subcell Biochem 18, 333–364, PubMed ID: 93134654
60. Aikawa, M. et al. (1977) Transmission and scanning electron microscopy of host cell entry by Toxoplasma gondii. Am J Pathol 87, 285–296, PubMed ID: 77154871
61. Michel, R. et al. (1980) Formation of a close junction during invasion of erythrocytes by Toxoplasma gondii in vitro. Int J Parasitol 10, 309–313, PubMed ID: 81093050
62. Nichols, B.A. and O'Connor, G.R. (1981) Penetration of mouse peritoneal macrophages by the protozoon Toxoplasma gondii. New evidence for active invasion and phagocytosis. Lab Invest 44, 324–335, PubMed ID: 81146799
63. Chiappino, M.L., Nichols, B.A. and O'Connor, G.R. (1984) Scanning electron microscopy of Toxoplasma gondii: parasite torsion and host-cell responses during invasion. J Protozool 31, 288–292, PubMed ID: 84292093
64. Porchet-Hennere, E. and Torpier, G. (1983) Relations entre Toxoplasma et sa cellule-hote. Protistologica 19, 357–370
65. de Carvalho, L. and de Souza, W. (1989) Cytochemical localization of plasma membrane enzyme markers during interiorization of tachyzoites of Toxoplasma gondii by macrophages. J Protozool 36, 164–170, PubMed ID: 89258550
66. Sibley, L.D. et al. (1994) Invasion and intracellular survival by Toxoplasma gondii. In Strategies for Intracellular Survival of Microbes (Kaufman, S.H.E., ed.), pp. 245–264, Bailleire Tindall, London, UK
67. Mordue, D.G. et al. (1999) Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. J Exp Med 190, 1783–1792, PubMed ID: 20069886
68. Suss-Toby, E., Zimmerberg, J. and Ward, G.E. (1996) Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci U S A 93, 8413–8418, PubMed ID: 96323236
69. Pacheco-Soares, C. and De Souza, W. (2000) Labeled probes inserted in the macrophage membrane are transferred to the parasite surface and internalized during cell invasion by Toxoplasma gondii. Parasitol Res 86, 11–17, PubMed ID: 20132614
70. Foussard, F., Leriche, M.A. and Dubremetz, J.F. (1991) Characterization of the lipid content of Toxoplasma gondii rhoptries. Parasitology 102 Pt 3, 367–370, PubMed ID: 91326512
71. Coppens, I., Sinai, A.P. and Joiner, K.A. (2000) Toxoplasma gondii exploits host low-density lipoprotein receptor- mediated endocytosis for cholesterol acquisition. J Cell Biol 149, 167–180, PubMed ID: 20211644
72. Beckers, C.J. et al. (1994) The Toxoplasma gondii rhoptry protein ROP 2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and is exposed to the host cell cytoplasm. J Cell Biol 127, 947–961, PubMed ID: 95050975
73. Bonhomme, A. et al. (1999) Signaling during the invasion of host cells by Toxoplasma gondii. FEMS Microbiol Rev 23, 551–561, PubMed ID: 99454739
74. Moreno, S.N. and Zhong, L. (1996) Acidocalcisomes in Toxoplasma gondii tachyzoites. Biochem J 313, 655–659, PubMed ID: 96152555
75. Lin, L.L. et al. (1993) cPLA2 is phosphorylated and activated by MAP kinase. Cell 72, 269–278, PubMed ID: 93145328
76. Saffer, L.D. et al. (1992) Localization of a Toxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration. J Protozool 39, 526–530, PubMed ID: 93020598
77. Fourmaux, M.N. et al. (1996) Toxoplasma gondii microneme proteins: gene cloning and possible function. Curr Top Microbiol Immunol 219, 55–58, PubMed ID: 96383528
78. Dzierszinski, F. et al. (2000) Targeted disruption of the glycosylphosphatidylinositol-anchored surface antigen SAG3 gene in Toxoplasma gondii decreases host cell adhesion and drastically reduces virulence in mice. Mol Microbiol 37, 574–582, PubMed ID: 20392212
79. Schwartzman, J.D. (1986) Inhibition of a penetration-enhancing factor of Toxoplasma gondii by monoclonal antibodies specific for rhoptries. Infect Immun 51, 760–764, PubMed ID: 86138602
80. Kimata, I. and Tanabe, K. (1987) Secretion by Toxoplasma gondii of an antigen that appears to become associated with the parasitophorous vacuole membrane upon invasion of the host cell. J Cell Sci 88, 231–239, PubMed ID: 88087512
81. Soldati, D. et al. (1995) Complementation of a Toxoplasma gondii ROP1 knock-out mutant using phleomycin selection. Mol Biochem Parasitol 74, 87–97, PubMed ID: 96360465
82. Tanaka, T., Ohmura, T. and Hidaka, H. (1983) Calmodulin antagonists' binding sites on calmodulin. Pharmacology 26, 249–257, PubMed ID: 83221960
83. Carruthers, V.B. and Sibley, L.D. (1999) Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol Microbiol 31, 421–428, PubMed ID: 99157550
84. Vieira, M.C. and Moreno, S.N. (2000) Mobilization of intracellular calcium upon attachment of Toxoplasma gondii tachyzoites to human fibroblasts is required for invasion. Mol Biochem Parasitol 106, 157–162, PubMed ID: 20208022
85. Dubremetz, J.F. and Schwartzman, J.D. (1993) Subcellular organelles of Toxoplasma gondii and host cell invasion. Res Immunol 144, 31–33, PubMed ID: 93197668
86. Pezzella, N. et al. (1997) Involvement of calcium and calmodulin in Toxoplasma gondii tachyzoite invasion. Eur J Cell Biol 74, 92–101, PubMed ID: 97454989
87. Lingelbach, K. and Joiner, K.A. (1998) The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J Cell Sci 111, 1467–1475, PubMed ID: 98248433
88. Sibley, L.D. et al. (1986) Toxoplasma modifies macrophage phagosomes by secretion of a vesicular network rich in surface proteins. J Cell Biol 103, 867–874, PubMed ID: 86304565
89. Sinai, A.P. and Joiner, K.A. (1997) Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu Rev Microbiol 51, 415–462, PubMed ID: 98001521
90. Stedman, T.T. and Joiner, K.A. (1999) En route to the vacuole: tracing the secretory pathway of Toxoplasma gondii. Adv Cell Mol Biol Membr Org 6, 233–261
91. Asai, T., O'Sullivan, W.J. and Tatibana, M. (1983) A potent nucleoside triphosphate hydrolase from the parasitic protozoan Toxoplasma gondii. Purification, some properties, and activation by thiol compounds. J Biol Chem 258, 6816–6822, PubMed ID: 83213415
92. Sibley, L.D. et al. (1994) Toxoplasma gondii: secretion of a potent nucleoside triphosphate hydrolase into the parasitophorous vacuole. Exp Parasitol 79, 301–311, PubMed ID: 95046143
93. Silverman, J.A. et al. (1998) Induced activation of the Toxoplasma gondii nucleoside triphosphate hydrolase leads to depletion of host cell ATP levels and rapid exit of intracellular parasites from infected cells. J Biol Chem 273, 12352–12359, PubMed ID: 98241603
94. Nakaar, V. et al. (1999) Targeted reduction of nucleoside triphosphate hydrolase by antisense RNA inhibits Toxoplasma gondii proliferation. J Biol Chem 274, 5083–5087, PubMed ID: 99143176
95. Dubremetz, J.F. et al. (1993) Kinetics and pattern of organelle exocytosis during Toxoplasma gondii/host-cell interaction. Parasitol Res 79, 402–408, PubMed ID: 94022185
96. Lecordier, L. et al. (1993) Molecular structure of a Toxoplasma gondii dense granule antigen (GRA 5) associated with the parasitophorous vacuole membrane. Mol Biochem Parasitol 59, 143–153, PubMed ID: 93295432
97. Halonen, S.K. and Weidner, E. (1994) Overcoating of Toxoplasma parasitophorous vacuoles with host cell vimentin type intermediate filaments. J Eukaryot Microbiol 41, 65–71, PubMed ID: 94169889
98. Sinai, A.P. and Joiner, K.A. The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J Cell Biol (in revision)
99. Vance, J.E. and Shiao, Y.J. (1996) Intracellular trafficking of phospholipids: import of phosphatidylserine into mitochondria. Anticancer Res 16, 1333–1339, PubMed ID: 96273094
100. Takeuchi, T., Fujiwara, T. and Akao, S. (1980) Na+, K+-dependent ATPase activity and effect of K+ on in vitro protein synthesis and NAD pyrophosphorylase in Toxoplasma gondii. J Parasitol 66, 591–595, PubMed ID: 81027778
101. Gomez-Marin, J.E. et al. (1998) Interferon-gamma signal transduction during parasite infection: modulation of MAP kinases in the infection of human monocyte cells (THP1) by Toxoplasma gondii. Parasite Immunol 20, 631–635, PubMed ID: 99144459
102. Shaw, M.K. (1995) Mobilization of intrasporozoite Ca2+ is essential for Theileria parva sporozoite invasion of bovine lymphocytes. Eur J Cell Biol 68, 78–87, PubMed ID: 96105631
103. Bouchot, A. et al. (1999) Tachyzoite calcium changes during cell invasion by Toxoplasma gondii. Parasitol Res 85, 809–818, PubMed ID: 99422997
104. Cesbron-Delauw, M.F. et al. (1989) Molecular characterization of a 23-kilodalton major antigen secreted by Toxoplasma gondii. Proc Natl Acad Sci U S A 86, 7537–7541, PubMed ID: 90017513
105. Pingret, L. et al. (1996) Relationship between intracellular free calcium concentrations and the intracellular development of Toxoplasma gondii. J Histochem Cytochem 44, 1123–1129, PubMed ID: 96408032
106. Endo, T., Sethi, K.K. and Piekarski, G. (1982) Toxoplasma gondii: calcium ionophore A23187-mediated exit of trophozoites from infected murine macrophages. Exp Parasitol 53, 179–188, PubMed ID: 82139303
107. Stommel, E.W. et al. (1997) Toxoplasma gondii: dithiol-induced Ca2+ flux causes egress of parasites from the parasitophorous vacuole. Exp Parasitol 87, 88–97, PubMed ID: 97467675
108. Fichera, M.E. and Roos, D.S. (1997) A plastid organelle as a drug target in apicomplexan parasites. Nature 390, 407–409, PubMed ID: 98049349
109. Fichera, M.E., Bhopale, M.K. and Roos, D.S. (1995) In vitro assays elucidate peculiar kinetics of clindamycin action against Toxoplasma gondii. Antimicrob Agents Chemother 39, 1530–1537, PubMed ID: 96104895
110. Berens, R.L., Krug, E.C. and Marr, J.J. (1995) Purine and pyrimidine metabolism. In Biochemistry of Parasitic Organisms and Its Molecular Foundations (Marr, J.J. and Muller, M., eds), pp. 89–117, Academic Press, London, UK
111. Schwab, J.C. et al. (1995) Toxoplasma gondii tachyzoites possess an unusual plasma membrane adenosine transporter. Mol Biochem Parasitol 70, 59–69, PubMed ID: 95364852
112. Chiang, C.W. et al. (1999) The adenosine transporter of Toxoplasma gondii. Identification by insertional mutagenesis, cloning, and recombinant expression. J Biol Chem 274, 35255–35261, PubMed ID: 20044795
113. Perrotto, J., Keister, D.B. and Gelderman, A.H. (1971) Incorporation of precursors into Toxoplasma DNA. J Protozool 18, 470–473, PubMed ID: 72076026
114. Krug, E.C., Marr, J.J. and Berens, R.L. (1989) Purine metabolism in Toxoplasma gondii. J Biol Chem 264, 10601–10607, PubMed ID: 89278126
115. Bermudes, D. et al. (1994) Tandemly repeated genes encode nucleoside triphosphate hydrolase isoforms secreted into the parasitophorous vacuole of Toxoplasma gondii. J Biol Chem 269, 29252–29260, PubMed ID: 95050750
116. Asai, T. et al. (1995) Biochemical and molecular characterization of nucleoside triphosphate hydrolase isozymes from the parasitic protozoan Toxoplasma gondii. J Biol Chem 270, 11391–11397, PubMed ID: 95263459
117. Ngo, H.M. et al. (2000) Toxoplasma gondii: are host cell adenosine nucleotides a direct source for purine salvage? Exp Parasitol 95, 148–153, PubMed ID: 20372614
118. Donald, R.G.K. et al. (1996) Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. J Biol Chem 271, 14010–14019, PubMed ID: 96278850
119. Schwartzman, J.D. and Pfefferkorn, E.R. (1982) Toxoplasma gondii: purine synthesis and salvage in mutant host cells and parasites. Exp Parasitol 53, 77–86, PubMed ID: 82117403
120. Asai, T. et al. (1983) Enzymes of the de novo pyrimidine biosynthetic pathway in Toxoplasma gondii. Mol Biochem Parasitol 7, 89–100, PubMed ID: 83219079
121. McCabe, R.E. and Oster, S. (1989) Current recommendations and future prospects in the treatment of toxoplasmosis. Drugs 38, 973–987, PubMed ID: 90126405
122. Nagel, S.D. and Boothroyd, J.C. (1989) The major surface antigen, P30, of Toxoplasma gondii is anchored by a glycolipid. J Biol Chem 264, 5569–5574, PubMed ID: 89174601
123. Tomavo, S., Dubremetz, J.F. and Schwarz, R.T. (1992) Cell-free synthesis of glycolipid candidate precursor(s) for glycosyl-phosphatidylinositol anchors of Toxoplasma gondii surface proteins. Biochem Soc Trans 20, 166S, PubMed ID: 93012306
124. Cintra, W.M. and de Souza, W. (1985) Distribution of intramembranous particles and filipin-sterol complexes in the cell membranes of Toxoplasma gondii. Eur J Cell Biol 37, 63–69, PubMed ID: 85285128
125. Gallois, Y. et al. (1988) Membrane fluidity of Toxoplasma gondii: a fluorescence polarization study. Biol Cell 62, 11–15, PubMed ID: 88209757
126. Foussard, F. et al. (1991) Lipids and fatty acids of tachyzoites and purified pellicles of Toxoplasma gondii. Parasitol Res 77, 475–477, PubMed ID: 92020784
127. High, K.P., Joiner, K.A. and Handschumacher, R.E. (1994) Isolation, cDNA sequences, and biochemical characterization of the major cyclosporin-binding proteins of Toxoplasma gondii. J Biol Chem 269, 9105–9112, PubMed ID: 94179329
128. Uittenbogaard, A., Ying, Y. and Smart, E.J. (1998) Characterization of a cytosolic heat-shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking. J Biol Chem 273, 6525–6532, PubMed ID: 98165843
129. Pfefferkorn, E.R. (1984) Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc Natl Acad Sci U S A 81, 908–912, PubMed ID: 84144813
130. Pfefferkorn, E.R., Eckel, M. and Rebhun, S. (1986) Interferon-gamma suppresses the growth of Toxoplasma gondii in human fibroblasts through starvation for tryptophan. Mol Biochem Parasitol 20, 215–224, PubMed ID: 87014565
131. Sibley, L.D., Messina, M. and Niesman, I.R. (1994) Stable DNA transformation in the obligate intracellular parasite Toxoplasma gondii by complementation of tryptophan auxotrophy. Proc Natl Acad Sci U S A 91, 5508–5512, PubMed ID: 94261615
132. Fulton, J.D. and Spooner, D.F. (1960) Metabolic studies on Toxoplasma gondii. Exp Parasitol 9, 293–301
133. Iltzsch, M.H. et al. (1995) Structure-activity relationship for the binding of nucleoside ligands to adenosine kinase from Toxoplasma gondii. Biochem Pharmacol 49, 1501–1512, PubMed ID: 95283588
134. Heroux, A. et al. (1999) Crystal structure of Toxoplasma gondii hypoxanthine-guanine phosphoribosyltransferase with XMP, pyrophosphate, and two Mg(2+) ions bound: insights into the catalytic mechanism. Biochemistry 38, 14495–14506, PubMed ID: 20014542
135. Heroux, A. et al. (1999) Crystal structures of the Toxoplasma gondii hypoxanthine-guanine phosphoribosyltransferase-GMP and -IMP complexes: comparison of purine binding interactions with the XMP complex. Biochemistry 38, 14485–14494, PubMed ID: 20014541
136. Schumacher, M.A. et al. (1996) Crystal structures of Toxoplasma gondii HGXPRTase reveal the catalytic role of a long flexible loop. Nat Struct Biol 3, 881–887, PubMed ID: 96433078
137. Schumacher, M.A. et al. (2000) Crystal structures of Toxoplasma gondii adenosine kinase reveal a novel catalytic mechanism and prodrug binding. J Mol Biol 298, 875–893, PubMed ID: 20263887
138. Youn, J.H. et al. (1990) Effects of pyrimidine salvage inhibitors on uracil incorporation of Toxoplasma gondii. Kisaengchunghak Chapchi 28, 79–84, PubMed ID: 91104654
139. Schumacher, M.A. et al. (1998) Crystal structures of Toxoplasma gondii uracil phosphoribosyltransferase reveal the atomic basis of pyrimidine discrimination and prodrug binding. Embo J 17, 3219–3232, PubMed ID: 98292442
140. Bohne, W., Heesemann, J. and Gross, U. (1994) Reduced replication of Toxoplasma gondii is necessary for induction of bradyzoite-specific antigens: a possible role for nitric oxide in triggering stage conversion. Infect Immun 62, 1761–1767, PubMed ID: 94222542
141. Ferguson, D.J. and Hutchison, W.M. (1987) An ultrastructural study of the early development and tissue cyst formation of Toxoplasma gondii in the brains of mice. Parasitol Res 73, 483–491, PubMed ID: 88097304
142. Halonen, S.K., Weiss, L.M. and Chiu, F.C. (1998) Association of host cell intermediate filaments with Toxoplasma gondii cysts in murine astrocytes in vitro. Int J Parasitol 28, 815–823, PubMed ID: 98313748
143. Weiss, L.M. and Kim, K. (2000) The development and biology of bradyzoites of Toxoplasma gondii. Front Biosci 5, D391–405, PubMed ID: 20227955
144. Dubey, J.P. (1997) Bradyzoite-induced murine toxoplasmosis: stage conversion, pathogenesis, and tissue cyst formation in mice fed bradyzoites of different strains of Toxoplasma gondii [published erratum appears in J Eukaryot Microbiol 1998 May-Jun; 45(3): 367]. J Eukaryot Microbiol 44, 592–602, PubMed ID: 98096857
145. Jerome, M.E. et al. (1998) Toxoplasma gondii bradyzoites form spontaneously during sporozoite-initiated development. Infect Immun 66, 4838–4844, PubMed ID: 98427152
146. Smith, J.E. (1995) A ubiquitous intracellular parasite: the cellular biology of Toxoplasma gondii. Int J Parasitol 25, 1301–1309, PubMed ID: 96229271
147. Bohne, W., Holpert, M. and Gross, U. (1999) Stage differentiation of the protozoan parasite Toxoplasma gondii. Immunobiology 201, 248–254, PubMed ID: 20097149
148. Thomason, P., Traynor, D. and Kay, R. (1999) Taking the plunge. Terminal differentiation in Dictyostelium. Trends Genet 15, 15–19, PubMed ID: 99187892
149. Lujan, H.D. et al. (1996) Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proc Natl Acad Sci U S A 93, 7628–7633, PubMed ID: 96353868
150. Choi, W.Y. et al. (1994) Culture of tissue-cyst forming strain of Toxoplasma gondii and the effect of cyclic AMP and pyrimidine salvage inhibitors. Korean J Parasitol 32, 19–26, PubMed ID: 94220433
151. Yahiaoui, B. et al. (1999) Isolation and characterization of a subtractive library enriched for developmentally regulated transcripts expressed during encystation of Toxoplasma gondii. Mol Biochem Parasitol 99, 223–235, PubMed ID: 99270311
152. Kasper, L.H. (1989) Identification of stage-specific antigens of Toxoplasma gondii. Infect Immun 57, 668–672, PubMed ID: 89138631
153. Woodison, G. and Smith, J.E. (1990) Identification of the dominant cyst antigens of Toxoplasma gondii. Parasitology 100 Pt 3, 389–392, PubMed ID: 90301393
154. Zhang, Y.W. and Smith, J.E. (1995) Toxoplasma gondii: identification and characterization of a cyst molecule. Exp Parasitol 80, 228–233, PubMed 95203405
155. Denton, H. et al. (1996) Enzymes of energy metabolism in the bradyzoites and tachyzoites of Toxoplasma gondii. FEMS Microbiol Lett 137, 103–108, PubMed ID: 97089755
156. Dzierszinski, F. et al. (1999) The protozoan parasite Toxoplasma gondii expresses two functional plant-like glycolytic enzymes. Implications for evolutionary origin of apicomplexans. J Biol Chem 274, 24888–24895, PubMed ID: 99386970
157. Ajioka, J.W., Fitzpatrick, J.M. and Reitter, C.P. (2001) Toxoplasma gondii genomics: shedding light on pathogenesis and chemotherapy. Exp Rev Mol Med 6 January, http://www-ermm.cbcu.cam.ac.uk/01002204h.htm