Armed and dangerous: Toxoplasma gondii uses an arsenal of secretory proteins to infect host cells

Parasitology International

Volumn 48, Issue 1, 1999, Pages 1-10

  Carruthers, Vern B ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Intracellular; Invasion; Parasite; Protozoan; Secretion

Indexed keywords

CALCIUM CHANNEL; MEMBRANE ANTIGEN; SECRETORY PROTEIN;

BINDING AFFINITY; CELL MEMBRANE; HOST CELL; HOST PARASITE INTERACTION; NONHUMAN; PARASITE SURVIVAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN SECRETION; PROTEIN TRANSPORT; PROTOZOAL INFECTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TOXOPLASMA GONDII;

EID: 0033103170     PISSN: 13835769     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1383-5769(98)00042-7     Document Type: Note

References (68)

1. Lynfield R, Guerina NG. Toxoplasmosis. Pediatr Rev 1997;18:75-83.
2. Luft BJ, Remington JS. Toxoplasmic encephalitis in AIDS. Clin Infect Dis 1992;15:211-222.
3. Dobrowolski JM, Sibley LD. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 1996;84:933-939.
4. Dobrowolski JM, Carruthers VB, Sibley LD. Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol Microbiol 1997;26:163-173.
5. Suss-Toby E, Zimmerberg J, Ward GE. Toxoplasma invasion: The parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci USA 1996;93:8413-8418.
6. Mordue DG, Sibley LD. Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J Immunol 1997;159:4452-4459.
7. Sibley LD, Hakansson S, Carruthers VB. Gliding motility: An efficient mechanism for cell penetration. Curr Biol 1998;8:R12-14.
8. Boothroyd JC, Hehl A, Knoll LJ, Manger ID. The surface of Toxoplasma: More and less. Int J Parasitol 1998;28:3-9.
9. Cesbron-Delauw MF, Guy B, Pierce RJ et al. Molecular characterization of a 23-kDa major antigen secreted by Toxoplasma gondii. Proc Natl Acad Sci USA 1989; 86:7537-7541.
10. Sibley LD, Pfefferkorn ER, Boothroyd JC. Proposal for a uniform genetic nomenclature in Toxoplasma gondii. Parasitol Today 1991;7:327-328.
11. Sibley LD, Niesman IR, Parmley SF, Cesbron-Delauw M-F. 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 1995;108:1669-1677.
12. Ajioka JW, Boothroyd JC, Brunk BP et al. Gene discovery by EST sequencing in Toxoplasma gondii reveals sequences restricted to the apicomplexa. Genome Res 1998;8:18-28.
13. Endo T, Sethi KK, Piekarski G. Toxoplasma gondii: Calcium ionophore A23187-mediated exit of trophozoites from infected murine macrophages. Exp Parasitol 1982;53:179-188.
14. Mercier C, Cesbron-Delauw MF, Sibley LD. The amphipathic and agr; helices of the Toxoplasma protein GRA2 mediate post-secretory membrane association. J Cell Sci 1998;111:2171-2180.
15. Mercier C, Howe DK, Mordue D, Lingnau M, Sibley LD. Targeted disruption of the GRA2 locus in Toxoplasma gondii decreases acute virulence in mice. Inf Immun 1998;66:4176-4182.
16. Ossorio PN, Dubremetz J-F, Joiner KA. A soluble secretory protein of the intracellular parasite Toxoplasma gondii associates with the parasitophorous vacuole membrane through hydrophobic interactions. J Biol Chem 1994;269:15350-15357.
17. Schwab JC, Beckers CJM, Joiner KA. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc Natl Acad Sci USA 1994;91:509-513.
18. Asai T, O'Sullivan WJ, Tatibana M. A potent nucleoside triphosphate hydrolase from the parasitic protozoan Toxoplasma gondii. J Biol Chem 1983;258:6816-6822.
19. Sibley LD, Neisman IR, Asai T, Takeuchi T. Toxoplasma gondii: Secretion of a potent nucleoside triphosphate hydrolase into the parasitophorous vacuole. Exp Parasitol 1994;79:301-311.
20. Asai T, Miura S, Sibley LD, Okabayashi H, Takeuchi T. Biochemical and molecular characterization of nucleoside triphosphate hydrolase isoenzymes from the parasitic protozoan Toxoplasma gondii. J Biol Chem 1995;270:11391-11397.
21. 2+ flux causes egress of parasites from the parasitophorous vacuole. Exp Parasitol 1997;87:88-97.
22. Silverman JA, Qi H, Riehl A, Beckers C, Nakaar V, Joiner KA. 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 1998; 273:12352-12359.
23. Carruthers VB, Sibley LD. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 1997;73:114-123.
24. Ossorio PN, Schwartzman JD, Boothroyd JC. A Toxoplasma gondii rhoptry protein associated with host cell penetration has an unusual charge asymmetry. Mol Biochem Parasitol 1992;50:1-16.
25. Schwartzman JD. Inhibition of a penetration-enhancing factor of Toxoplasma gondii by monoclonal antibodies specific for rhoptries. Infect Immun 1986;51:760-764.
26. Norrby R, Lycke E. Factors enhancing the host-cell penetration of Toxoplasma gondii. J Bacteriol 1967;93: 53-58.
27. Lycke E, Norrby R, Remington J. Penetration-enhancing factor extracted from Toxoplasma gondii which increases its virulence for mice. J Bacteriol 1968;96: 785-788.
28. Kim K, Boothroyd JC. Gene replacement in Toxoplasma gondii with chloramphenicol acetyltransferase as selectable marker. Science 1993;262:911-914.
29. Soldati D, Kim K, Kampmeier J, Dubremetz J-F, Boothroyd JC. Complementation of a Toxoplasma gondii ROP1 knock-out mutant using phleomycin. Mol Biochem Parasitol 1995;74:87-97.
30. Beckers CJM, Dubremetz J-F, Mercereau-Puijalon O, Joiner KA. 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 1994;127:947-961.
31. Beckers CJ, Wakefield T, Joiner KA. The expression of Toxoplasma proteins in Neospora caninum and the identification of a gene encoding a novel rhoptry protein. Mol Biochem Parasitol 1997;89:209-223.
32. Leriche MA, Dubremetz JF. Characterization of the protein contents of rhoptries and dense granule of Toxoplasma gondii tachyzoites by subcellular fractionation and monoclonal antibodies. Mol Biochem Parasitol 1991;45:249-260.
33. Wan K-L, Blackwell JM, Ajioka JW. Toxoplasma gondii expressed sequence tags: Insight into tachyzoite gene expression. Mol Biochem Parasitol 1996;75:179-186.
34. Fourmaux MN, Achbarou A, Mercereau-Puijalon O et al. The MIC1 microneme protein of Toxoplasma gondii contains a duplicate receptor-like domain and binds to host cell surface. Mol Biochem Parasitol 1996;83: 201-210.
35. Wan KL, Carruthers VB, Sibley LD, Ajioka JW. Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol Biochem Parasitol 1997;84:203-214.
36. Carruthers VB, Sibley LD. Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol Microbiol, in press.
37. Sultan AA, Thathy V, Frevert U et al. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 1997;90:511-522.
38. Fourmaux MN, Garcia-Reguet N, Mercereau-Puijalon O, Dubremetz JF. Toxoplasma gondii microneme proteins: Gene cloning and possible function. Curr Top Microbiol Immunol 1996;219:55-58.
39. Achbarou A, Mercereau-Puijalon O, Autherman JM, Fortier B, Camus D, Dubremetz J-F. Characterization of microneme proteins of Toxoplasma gondii. Mol Biochem Parasitol 1991;47:223-234.
40. Karsten V, Qi H, Beckers CJ et al. The protozoan parasite Toxoplasma gondii targets proteins to dense granules and the vacuolar space using both conserved and unusual mechanisms. J Cell Biol 1998;141: 1323-1333.
41. Seeber F, Dubremetz JF, Boothroyd JC. Analysis of Toxoplasma gondii stably transfected with a transmembrane variant of its major surface protein, SAG1. J Cell Sci 1998;111:23-29.
42. Lecordier L, Mercier C, Torpier G et al. Molecular structure of a Toxoplasma gondii dense granule antigen (GRA 5) associated with the parasitophorous vacuole membrane. Mol Biochem Parasitol 1993;59:143-153.
43. Bermudes D, Dubremetz JF, Achbarou A, Joiner KA. Cloning of a cDNA encoding the dense granule protein GRA3 from Toxoplasma gondii. Mol Biochem Parasitol 1994;68:247-257.
44. Melevec M-N, Chardes T, Mercereau-Puijalon O et al. Molecular cloning of GRA4, a Toxoplasma gondii dense granule protein, recognized by mucosal IgA antibodies. Mol Biochem Parasitol 1992;56:227-238.
45. Mercier C, Lecordier L, Darcy F et al. Molecular characterization of a dense granule antigen (GRA2) associated with the network of the parasitophorous vacuole. Mol Biochem Parasitol 1993;58:71-82.
46. Lecordier L, Moleon-Borodowsky I, Dubremetz JF et al. Characterization of a dense granule antigen of Toxoplasma gondii (GRA6) associated to the network of the parasitophorous vacuole. Mol Biochem Parasitol 1995;70:85-94.
47. Fischer HG, Stachelhaus S, Sahm M, Meyer HE, Reichmann G. GRA7, an excretory 29-kDa Toxoplasma gondii dense granule antigen released by infected host cells. Mol Biochem Parasitol 1998;91:251-262.
48. Jacobs D, Dubremetz JF, Loyens A, Bosman F, Saman E. Identification and heterologous expression of a new dense granule protein (GRA7) from Toxoplasma gondii. Mol Biochem Parasitol 1998;91:237-249.
49. Nichols BA, Chiappino ML, O'Connor GR. Secretion from the rhoptries of Toxoplasma gondii during host-cell invasion. J Ultrastr Res 1983;83:85-98.
50. Foussard F, Leriche MA, Dubremetz JF. Characterization of the lipid content of Toxoplasma gondii rhoptries. Parasitology 1991;102:367-370.
51. Dubremetz JF. Host cell invasion by Toxoplasma gondii. Trends Microbiol 1998;6:27-30
52. Achbarou A, Mercereau-Puijalon O, Sadak A, Forteir B, Leriche MA, Camus D. Differential targeting of dense granule proteins in the parasitophorous vacuole of Toxoplasma gondii. Parasitology 1991;103:321-329.
53. Odenthal-Schnittler M, Tomavo S, Becker D, Dubremetz J-F, Schwartz RT. Evidence for n-linked glycosylation in Toxoplasma gondii. Biochem J 1993;291:713-721.
54. Diekmann-Schuppert A, Bause E, Schwartz RT. Glycosylation reactions in Plasmodium falciparum, Toxoplasma gondii, and Trypanosoma brucei brucei probed by the use of synthetic peptides. Biochim Biophys Acta 1994;1199:37-44.
55. Soldati D, Lassen A, Dubremetz J-F, Boothroyd JC. Processing of Toxoplasma ROP1 protein in nascent rhoptries. Mol Biochem Parasitol, in press.
56. Sadak A, Taghy Z, Fortier B, Dubremetz JF. Characterization of a family of rhoptry proteins of Toxoplasma gondii. Mol Biochem Parasitol 1988;29:203-211.
57. Saffer LD, Mercereau-Puijalon O, Dubermetz JF, Schwartzman JD. Localization of a Toxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration. J Protozool 1992; 39:526-530.
58. Chaturvedi S, Qi H, Coleman D, Rodriguez A, Hanson PI, Striepen B, Roos DS, Joiner KA. Constitutive calcium independent release of Toxoplasma gondii dense granules occurs through the NSF/SNAP/SNARE/Rab machinery. J Biol Chem, in press.
59. Dubremetz JF, Achbarou A, Bermudes D, Joiner KA. Kinetics and pattern of organelle exocytosis during Toxoplasma gondii host-cell interaction. Parasitol Res 1993;79:401-408.
60. Liddell S, Lally NC, Jenkins MC, Dubey JP. Isolation of the cDNA encoding a dense granule associated antigen (NCDG2) of Neospora caninum. Mol Biochem Parasitol 1998;93:153-158
61. Lally N, Jenkins M, Liddell S, Dubey JP. A dense granule protein (NCDG1) gene from Neospora caninum. Mol Biochem Parasitol 1997;87:239-243.
62. Asai T, Howe DK, Nakajima K, Nozaki T, Takeuchi T, Sibley LD. Neospora caninum: Tachyzoites express a potent type-i nucleoside triphosphate hydrolase, but lack nucleoside diphosphate hydrolase activity. Exp Parasitol, in press.
63. Tomley FM, Clarke LE, Kawazoe U, Dijkema R, Kok JJ. Sequence of the gene encoding an immunodominant micron protein of Eimeria tenella. Mol Biochem Parasitol 1991;49:277-288.
64. Pasamontes L, Hug D, Humbelin M, Weber G. Sequence of a major Eimeria maxima antigen homologous to the Eimeria tenella microneme protein Etp100. Mol Biochem Parasitol 1993;57:171-174.
65. Spano F, Putignani L, Naitza S, Puri C, Wright S, Crisanti A. Molecular cloning and expression analysis of a Ccryptosporidium parvum gene encoding a new member of the thrombospondin family. Mol Biochem Parasitol 1998;92:147-162.
66. Templeton TJ. Cloning and cross-species comparison of the thrombospondin-related anonymous protein (TRAP) gene from Plasmodium knowlesi, Plasmodium vivax and Plasmodium gallinaceum. Mol Biochem Parasitol 1997;84:13-24.
67. Trottein F, Triglia T, Cowman AF. Molecular cloning of a gene from Plasmodium falciparum that codes for a protein sharing motifs found in adhesive molecules from mammals and plasmodia. Mol Biochem Parasitol 1995;74:129-141.
68. de Carvalho, L, Souto-Padron T, de Souza W. Localization of lectin-binding sites and sugar-binding proteins in tachyzoites of Toxoplasma gondii. J Parasitol 1991;77:156-161