Expression quantitative trait locus mapping of Toxoplasma genes reveals multiple mechanisms for strain-specific differences in gene expression

Eukaryotic Cell

Volumn 7, Issue 8, 2008, Pages 1403-1414

  Boyle, Jon P ^a   Saeij, Jeroen P J ^a   Harada, Scott Y ^a   Ajioka, Jim W ^b   Boothroyd, John C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; CHROMOSOME MAP; DNA MICROARRAY; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; HYBRIDIZATION; METHODOLOGY; QUANTITATIVE TRAIT; QUANTITATIVE TRAIT LOCUS; SPECIES DIFFERENCE; TOXOPLASMA;

ANIMALS; CHROMOSOME MAPPING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENES, PROTOZOAN; GENOTYPE; HYBRIDIZATION, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMORPHISM, GENETIC; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE; SPECIES SPECIFICITY; TOXOPLASMA;

APICOMPLEXA; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 48949084367     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00073-08     Document Type: Article

References (41)

1. Ajioka, J. W., J. C. Boothroyd, B. P. Brunk, A. Hehl, L. Hillier, I. D. Manger, M. Marra, G. C. Overton, D. S. Roos, K. L. Wan, R. Waterston, and L. D. Sibley. 1998. Gene discovery by EST sequencing in Toxoplasma gondii reveals sequences restricted to the Apicomplexa. Genome Res. 8:18-28.
2. Aurrecoechea, C., M. Heiges, H. Wang, Z. Wang, S. Fischer, P. Rhodes, J. Miller, E. Kraemer, C. J. Stoeckert, Jr., D. S. Roos, and J. C. Kissinger. 2007. ApiDB: integrated resources for the apicomplexan bioinformatics resource center. Nucleic Acids Res. 35:D427-D430.
3. Beckers, C. J., T. Wakefield, and K. A. Joiner. 1997. The expression of Toxoplasma proteins in Neospora caninum and the identification of a gene encoding a novel rhoptry protein. Mol. Biochem. Parasitol. 89:209-223.
4. Behnke, M. S., J. B. Radke, A. T. Smith, W. J. Sullivan, Jr., and M. W. White. 2008. The transcription of bradyzoite genes in Toxoplasma gondii is controlled by autonomous promoter elements. Mol. Microbiol. 68:1502-1518.
5. Boothroyd, J. C., and J. F. Dubremetz. 2008. Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat. Rev. Microbiol. 6:79-88.
6. Boyle, J. P., B. Rajasekar, J. P. Saeij, J. W. Ajioka, M. Berriman, I. Paulsen, D. S. Roos, L. D. Sibley, M. W. White, and J. C. Boothroyd. 2006. Just one cross appears capable of dramatically altering the population biology of a eukaryotic pathogen like Toxoplasma gondii. Proc. Natl. Acad. Sci. USA 103:10514-10519.
7. Boyle, J. P., X. J. Wu, C. B. Shoemaker, and T. P. Yoshino. 2003. Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Mol. Biochem. Parasitol. 128:205-215.
8. Bradley, P. J., and L. D. Sibley. 2007. Rhoptries: an arsenal of secreted virulence factors. Curr. Opin. Microbiol. 10:582-587.
9. Bradley, P. J., C. Ward, S. J. Cheng, D. L. Alexander, S. Coller, G. H. Coombs, J. D. Dunn, D. J. Ferguson, S. J. Sanderson, J. M. Wastling, and J. C. Boothroyd. 2005. Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J. Biol. Chem. 280:34245-34258.
10. Broman, K. W., H. Wu, S. Sen, and G. A. Churchill. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889-890.
11. Carruthers, V. B., O. K. Giddings, and L. D. Sibley. 1999. Secretion of micronemal proteins is associated with Toxoplasma invasion of host cells. Cell. Microbiol. 1:225-235.
12. Cleary, M. D., C. D. Meiering, E. Jan, R. Guymon, and J. C. Boothroyd. 2005. Biosynthetic labeling of RNA with uracil phosphoribosyltransferase allows cell-specific microarray analysis of mRNA synthesis and decay. Nat. Biotechnol. 23:232-237.
13. Cleary, M. D., U. Singh, I. J. Blader, J. L. Brewer, and J. C. Boothroyd. 2002. Toxoplasma gondii asexual development: identification of developmentally regulated genes and distinct patterns of gene expression. Eukaryot. Cell 1:329-340.
14. Coppens, I., J. D. Dunn, J. D. Romano, M. Pypaert, H. Zhang, J. C. Boothroyd, and K. A. Joiner. 2006. Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125:261-274.
15. Dzierszinski, F., M. Nishi, L. Ouko, and D. S. Roos. 2004. Dynamics of Toxoplasma gondii differentiation. Eukaryot. Cell 3:992-1003.
16. El Hajj, H., E. Demey, J. Poncet, M. Lebrun, B. Wu, N. Galeotti, M. N. Fourmaux, O. Mercereau-Puijalon, H. Vial, G. Labesse, and J. F. Dubremetz. 2006. The ROP2 family of Toxoplasma gondii rhoptry proteins: proteomic and genomic characterization and molecular modeling. Proteomics 6:5773-5784.
17. El Hajj, H., M. Lebrun, S. T. Arold, H. Vial, G. Labesse, and J. F. Dubremetz. 2007. ROP18 is a rhoptry kinase controlling the intracellular proliferation of Toxoplasma gondii. PLoS Pathog. 3:e14.
18. Emanuelsson, O., S. Brunak, G. von Heijne, and H. Nielsen. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953-971.
19. Gilbert, L. A., S. Ravindran, J. M. Turetzky, J. C. Boothroyd, and P. J. Bradley. 2007. Toxoplasma gondii targets a protein phosphatase 2C to the nuclei of infected host cells. Eukaryot. Cell 6:73-83.
20. Gissot, M., K. A. Kelly, J. W. Ajioka, J. M. Greally, and K. Kim. 2007. Epigenomic modifications predict active promoters and gene structure in Toxoplasma gondii. PLoS Pathog. 3:e77.
21. Goring, H. H., J. E. Curran, M. P. Johnson, T. D. Dyer, J. Charlesworth, S. A. Cole, J. B. Jowett, L. J. Abraham, D. L. Rainwater, A. G. Comuzzie, M. C. Mahaney, L. Almasy, J. W. MacCluer, A. H. Kissebah, G. R. Collier, E. K. Moses, and J. Blangero. 2007. Discovery of expression QTLs using large-scale transcriptional profiling in human lymphocytes. Nat. Genet. 39:1208-1216.
22. Grigg, M. E., J. Ganatra, J. C. Boothroyd, and T. P. Margolis. 2001. Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J. Infect. Dis. 184:633-639.
23. Howe, D. K., and L. D. Sibley. 1995. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J. Infect. Dis. 172:1561-1566.
24. Khan, A., S. Taylor, C. Su, A. J. Mackey, J. Boyle, R. Cole, D. Glover, K. Tang, I. T. Paulsen, M. Berriman, J. C. Boothroyd, E. R. Pfefferkorn, J. P. Dubey, J. W. Ajioka, D. S. Roos, J. C. Wootton, and L. D. Sibley. 2005. Composite genome map and recombination parameters derived from three archetypal lineages of Toxoplasma gondii. Nucleic Acids Res. 33:2980-2992.
25. Li, L., J. Crabtree, S. Fischer, D. Pinney, C. J. Stoeckert, Jr., L. D. Sibley, and D. S. Roos. 2004. ApiEST-DB: analyzing clustered EST data of the apicomplexan parasites. Nucleic Acids Res. 32:D326-D328.
26. T method. Methods (Duluth) 25:402-408.
27. Mercier, C., S. Lefebvre-Van Hende, G. E. Garber, L. Lecordier, A. Capron, and M. F. Cesbron-Delauw. 1996. Common cis-acting elements critical for the expression of several genes of Toxoplasma gondii. Mol. Microbiol. 21:421-428.
28. Poupel, O., H. Boleti, S. Axisa, E. Couture-Tosi, and I. Tardieux. 2000. Toxofilin, a novel actin-binding protein from Toxoplasma gondii, sequesters actin monomers and caps actin filaments. Mol. Biol. Cell 11:355-368.
29. Radke, J. R., M. J. Gubbels, M. E. Jerome, J. B. Radke, B. Striepen, and M. W. White. 2004. Identification of a sporozoite-specific member of the Toxoplasma SAG superfamily via genetic complementation. Mol. Microbiol. 52:93-105.
30. Saeij, J. P., J. P. Boyle, S. Coller, S. Taylor, L. D. Sibley, E. T. Brooke-Powell, J. W. Ajioka, and J. C. Boothroyd. 2006. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314:1780-1783.
31. Saeij, J. P., S. Coller, J. P. Boyle, M. E. Jerome, M. W. White, and J. C. Boothroyd. 2007. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445:324-327.
32. Saksouk, N., M. M. Bhatti, S. Kieffer, A. T. Smith, K. Musset, J. Garin, W. J. Sullivan, Jr., M. F. Cesbron-Delauw, and M. A. Hakimi. 2005. Histone-modifying complexes regulate gene expression pertinent to the differentiation of the protozoan parasite Toxoplasma gondii. Mol. Cell. Biol. 25:10301-10314.
33. Sibley, L. D., and J. C. Boothroyd. 1992. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature 359:82-85.
34. Sibley, L. D., A. J. LeBlanc, E. R. Pfefferkorn, and J. C. Boothroyd. 1992. Generation of a restriction fragment length polymorphism linkage map for Toxoplasma gondii. Genetics 132:1003-1015.
35. Singh, U., J. L. Brewer, and J. C. Boothroyd. 2002. Genetic analysis of tachyzoite to bradyzoite differentiation mutants in Toxoplasma gondii reveals a hierarchy of gene induction. Mol. Microbiol. 44:721-733.
36. Soldati, D., and J. C. Boothroyd. 1995. A selector of transcription initiation in the protozoan parasite Toxoplasma gondii. Mol. Cell. Biol. 15:87-93.
37. Taylor, S., A. Barragan, C. Su, B. Fux, S. J. Fentress, K. Tang, W. L. Beatty, H. E. Hajj, M. Jerome, M. S. Behnke, M. White, J. C. Wootton, and L. D. Sibley. 2006. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314:1776-1780.
38. Trujillo, M., R. G. Donald, D. S. Roos, P. J. Greene, and D. V. Santi. 1996. Heterologous expression and characterization of the bifunctional dihydrofolate reductase-thymidylate synthase enzyme of Toxoplasma gondii. Biochemistry 35:6366-6374.
39. Ware, P. L., and L. H. Kasper. 1987. Strain-specific antigens of Toxoplasma gondii. Infect. Immun. 55:778-783.
40. Woo, Y., J. Affourtit, S. Daigle, A. Viale, K. Johnson, J. Naggert, and G. Churchill. 2004. A comparison of cDNA, oligonucleotide, and Affymetrix GeneChip gene expression microarray platforms. J. Biomol. Tech. 15:276-284.
41. Zhou, X. W., B. F. Kafsack, R. N. Cole, P. Beckett, R. F. Shen, and V. B. Carruthers. 2005. The opportunistic pathogen Toxoplasma gondii deploys a diverse legion of invasion and survival proteins. J. Biol. Chem. 280:34233-34244.