Toxoplasma gondii eukaryotic translation initiation factor 4A associated with tachyzoite virulence is down-regulated in the bradyzoite stage

International Journal for Parasitology

Volumn 32, Issue 10, 2002, Pages 1225-1234

  Gastens, Martin H ^a   Fischer, Hans Georg ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Developmental expression; eIF4A; Proteome; Toxoplasma gondii; Virulence

Indexed keywords

INITIATION FACTOR; TRANSLATION INITIATION FACTOR 4A; UNCLASSIFIED DRUG;

PARASITE;

AMINO ACID SEQUENCE; ARTICLE; ATTENUATION; CONTROLLED STUDY; CYTOSOL; DEVELOPMENTAL STAGE; DOWN REGULATION; GENE ISOLATION; GENETIC TRANSCRIPTION; HOMEOSTASIS; HOST; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MICROSOME; NONHUMAN; PARASITE VIRULENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEADY STATE; TOXOPLASMA GONDII;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CLONING, MOLECULAR; DOWN-REGULATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EUKARYOTIC INITIATION FACTOR-4A; GENE EXPRESSION REGULATION; GENES, PROTOZOAN; LIFE CYCLE STAGES; MICE; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; TOXOPLASMA; VIRULENCE;

EUKARYOTA; TOXOPLASMA GONDII;

EID: 0036710617     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0020-7519(02)00096-6     Document Type: Article

References (40)

1. Aloni R., Peleg D., Meyuhas O. Selective translational control and nonspecific post-transcriptional regulation of ribosomal protein gene expression during development and regeneration of rat liver. Mol. Cell. Biol. 12:1992;2203-2212.
2. Ashman K., Houthaeve T., Clayton J., Wilm M., Podtelejnikov A., Jensen O.N., Mann M. The application of robotics and mass spectrometry to the characterisation of the Drosophila melanogaster indirect flight muscle proteome. Lett. Pept. Sci. 4:1997;57-65.
3. Bohne W., Heesemann J., Gross U. Induction of bradyzoite-specific Toxoplasma gondii antigens in gamma interferon-treated mouse macrophages. Infect. Immun. 61:1993;1141-1145.
4. Bohne W., Gross U., Ferguson D.J.P., Heesemann J. Cloning and characterization of a bradyzoite-specifically expressed gene (hsp30/bag1) of Toxoplasma gondii, related to genes encoding small heat-shock proteins of plants. Mol. Microbiol. 16:1995;1221-1230.
5. Bohne W., Holpert M., Gross U. Stage differentiation of the protozoan parasite Toxoplasma gondii. Immunobiology. 201:1999;248-254.
6. Brusca J.S., Radolf J.D. Isolation of integral membrane proteins by phase partitioning with Triton X-114. Methods Enzymol. 228:1994;182-193.
7. Burg J.L., Perelman D., Kasper L.H., Ware P.L., Boothroyd J.C. Molecular analysis of the gene encoding the major surface antigen of Toxoplasma gondii. J. Immunol. 141:1988;3584-3591.
8. Church G.M., Gilbert W. Genomic sequencing. Proc. Natl. Acad. Sci. USA. 81:1984;1991-1995.
9. Daga R.R., Jimenez J. Translational control of the Cdc25 cell cycle phosphatase: a molecular mechanism coupling mitosis to cell growth. J. Cell Sci. 112:1999;3137-3146.
10. DeBenedetti A., Harris A.L. eIF4E expression in tumors: its possible role in progression of malignancies. Int. J. Biochem. Cell Biol. 31:1999;59-72.
11. DeBenedetti A., Joshi B., Graff J.R., Zimmer S.G. CHO cells transformed by the translation factor eIF4E display increased c-myc expression, but require overexpression of Max for tumorigenicity. Mol. Cell Differ. 2:1994;347-371.
12. Dzierszinski F., Popescu O., Toursel C., Slomianny C., Yahiaoui B., Tomavo S. The protozoan parasite Toxoplasma gondii expresses two functional plant-like glycolytic enzymes. Implications for evolutionary origin of apicomplexans. J. Biol. Chem. 274:1999;24888-24895.
13. Dzierszinski F., Mortuaire M., Dendouga N., Popescu O., Tomavo S. Differential expression of two plant-like enolases with distinct enzymatic and antigenic properties during stage conversion of the protozoan parasite Toxoplasma gondii. J. Mol. Biol. 309:2001;1017-1027.
14. Galloni M., Edgar B.A. Cell-autonomous and non-autonomous growth-defective mutants of Drosophila melanogaster. Development. 126:1999;2365-2375.
15. Gingras A.C., Raught B., Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:1999;913-963.
16. Gross U., Bohne W., Soête M., Dubremetz J.F. Developmental differentiation between tachyzoites and bradyzoites of Toxoplasma gondii. Parasitol. Today. 12:1996;30-33.
17. Huang S., Hershey J.W.B. Translational initiation factor expression and ribosomal protein gene expression are repressed coordinately but by different mechanisms in murine lymphosarcoma cells treated with glucocorticoids. Mol. Cell. Biol. 9:1989;3679-3684.
18. Knoll L.J., Boothroyd J.C. Isolation of developmentally regulated genes from Toxoplasma gondii by a gene trap with the positive and negative selectable marker hypoxanthine-guanine phosphoribosyltransferase. Mol. Cell. Biol. 18:1998;807-814.
19. Linder P., Slonimski P.P. An essential yeast protein, encoded by duplicated genes TIF1 and TIF2 and homologous to the mammalian translation initiation factor eIF-4A, can suppress a mitochondrial missense mutation. Proc. Natl. Acad. Sci. USA. 86:1989;2286-2290.
20. Marissen W.E., Lloyd R.E. Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol. Cell. Biol. 18:1998;7565-7574.
21. Nielsen P.J., Trachsel H. The mouse protein synthesis initiation factor 4A gene family includes two related functional genes which are differentially expressed. EMBO J. 7:1988;2097-2105.
22. Nischik N., Schade B., Dytnerska K., Dlugonska H., Reichmann G., Fischer H.G. Attenuation of mouse-virulent Toxoplasma gondii parasites is associated with a decrease in interleukin-12-inducing tachyzoite activity and reduced expression of actin, catalase and excretory proteins. Microbes Infect. 3:2001;689-699.
23. Odberg-Ferragut C., Soête M., Engels A., Samyn B., Loyens A., VanBeeumen J., Camus D., Dubremetz J.F. Molecular cloning of the Toxoplasma gondii sag4 gene encoding an 18 kDa bradyzoite specific surface protein. Mol. Biochem. Parasitol. 82:1996;237-244.
24. Parmley S.F., Yang S., Harth G., Sibley L.D., Sucharczuk A., Remington J.S. Molecular characterization of a 65-kilodalton Toxoplasma gondii antigen expressed abundantly in the matrix of tissue cysts. Mol. Biochem. Parasitol. 66:1994;283-296.
25. Pause A., Sonenberg N. Helicases and RNA unwinding in translation. Curr. Opin. Struct. Biol. 3:1993;953-959.
26. Pestova T.V., Kolupaeva V.G., Lomakin I.B., Pilipenko E.V., Shatsky I.N., Agol V.I., Hellen C.U.T. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA. 98:2001;7029-7036.
27. Prince J.B., Auer K.L., Huskinson J., Parmley S.F., Araujo F.G., Remington J.S. Cloning, expression, and cDNA sequence of surface antigen P22 from Toxoplasma gondii. Mol. Biochem. Parasitol. 43:1990;97-106.
28. Rabilloud T., Adessi C., Giraudel A., Lunnardi J. Improvement of the solubilization of proteins in two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis. 18:1997;307-316.
29. + T-cell clone. Microbes Infect. 3:2001;779-787.
30. Reichmann G., Dlugonska H., Fischer H.G. Characterization of TgROP9 (p36), a novel rhoptry protein of Toxoplasma gondii tachyzoites identified by T cell clone. Mol. Biochem. Parasitol. 119:2002;43-54.
31. Rousseau D., Kaspar R., Rosenwald I., Gehrke L., Sonenberg N. Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. Proc. Natl. Acad. Sci. USA. 93:1996;1065-1070.
32. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd Edition:1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
33. Schmid S.R., Linder P. DEAD protein family of putative RNA helicases. Mol. Microbiol. 6:1990;283-292.
34. Spano F., Crisanti A. The initiation translation factor eIF-4A of Cryptosporidium parvum is encoded by two distinct mRNA forms and shows DNA sequence polymorphism distinguishing genotype 1 and 2 isolates. J. Parasitol. 86:2000;777-782.
35. Tomavo S. The differential expression of multiple isoenzyme forms during stage conversion of Toxoplasma gondii: an adaptive developmental strategy. Int. J. Parasitol. 31:2001;1023-1031.
36. Tomavo S., Fortier B., Soête M., Ansel C., Camus D., Dubremetz J.F. Characterization of bradyzoite-specific antigens of Toxoplasma gondii. Infect. Immun. 59:1991;3750-3753.
37. II is dependent upon cellular growth status. Arch. Biochem. Biophys. 338:1997;111-120.
38. Yahiaoui B., Dzierszinski F., Bernigaud A., Slomianny C., Camus D., Tomavo S. Isolation and characterization of a subtractive library enriched for developmentally regulated transcripts expressed during encystation of Toxoplasma gondii. Mol. Biochem. Parasitol. 99:1999;223-235.
39. Yang S., Parmley S.F. A bradyzoite-specific expressed gene of Toxoplasma gondii encodes a polypeptide homologous to lactate dehydrogenase. Mol. Biochem. Parasitol. 73:1995;291-294.
40. Yang S., Parmley S.F. Toxoplasma gondii expresses two distinct lactate dehydrogenase homologous genes during its life cycle in intermediate hosts. Gene. 184:1997;1-12.