Proteomic analysis of the Theileria annulata schizont

International Journal for Parasitology

Volumn 43, Issue 2, 2013, Pages 173-180

  Witschi, M ^a   Xia, D ^b   Sanderson, S ^b   Baumgartner, M ^a   Wastling, J M ^b   Dobbelaere, D A E ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Apicomplexa; Detergent; Mass spectrometry; Proteome; Theileria; Transformation; Transmembrane domain; Triton X 114

Indexed keywords

MEMBRANE PROTEIN; TRITON X 114;

DETERGENT; GENE EXPRESSION; MASS SPECTROMETRY; PARASITE; PROTEIN; PROTEOMICS;

ARTICLE; CITRIC ACID CYCLE; GENETIC TRANSCRIPTION; GLYCOLYSIS; LIQUID CHROMATOGRAPHY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DATABASE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; SCHIZONT; TANDEM MASS SPECTROMETRY; THEILERIA ANNULATA;

ANIMALS; CATTLE; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PROTEOMICS; PROTOZOAN PROTEINS; SCHIZONTS; THEILERIA ANNULATA; THEILERIASIS;

APICOMPLEXA; BOS; BOVINAE; THEILERIA; THEILERIA ANNULATA;

EID: 84873145447     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2012.10.017     Document Type: Article

References (44)

1. Baumgartner M., Tardieux I., Ohayon H., Gounon P., Langsley G. The use of nocodazole in cell cycle analysis and parasite purification from Theileria parva-infected B cells. Microb. Infect. 1999, 1:1181-1188.
2. Bender A., van Dooren G.G., Ralph S.A., McFadden G.I., Schneider G. Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum. Mol. Biochem. Parasitol. 2003, 132:59-66.
3. Bishop R., Shah T., Pelle R., Hoyle D., Pearson T., Haines L., Brass A., Hulme H., Graham S.P., Taracha E.L., Kanga S., Lu C., Hass B., Wortman J., White O., Gardner M.J., Nene V., de Villiers E.P. Analysis of the transcriptome of the protozoan Theileria parva using MPSS reveals that the majority of genes are transcriptionally active in the schizont stage. Nucleic Acids Res. 2005, 33:5503-5511.
4. Bishop R.P., Odongo D.O., Mann D.J., Pearson T.W., Sugimoto C., Haines L.R., Glass E., Jensen K., Seitzer U., Ahmed J.S., Graham S.R., de Villiers E.P. Theileria. Genome Mapping and Genomics in Animal-Associated Microbes 2009, 191-231. Springer-Verlag Berlin, Heidelberg. V. Nene, C. Kole (Eds.).
5. Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 1981, 256:1604-1607.
6. Chaussepied M., Langsley G. Theileria-induced leukocyte transformation: an example of oncogenic addiction?. The Immune Response to Infection 2011, 537-546. ASM Press, Washington, DC. S.H.E. Kaufmann, B.T. Rouse, D.L. Sacks (Eds.).
7. Cordero E.M., Nakayasu E.S., Gentil L.G., Yoshida N., Almeida I.C., da Silveira J.F. Proteomic analysis of detergent-solubilized membrane proteins from insect-developmental forms of Trypanosoma cruzi. J. Proteome Res. 2009, 8:3642-3652.
8. Dobbelaere D., Baumgartner M. Theileria. Intracellular Niches of Microbes: A Pathogens Guide Through the Host Cell 2009, 613-632. Wiley-VCH Verlag, Weinheim. U.E. Schaible, A. Haas (Eds.).
9. Durrani Z., Weir W., Pillai S., Kinnaird J., Shiels B. Modulation of activation-associated host cell gene expression by the apicomplexan parasite Theileria annulata. Cell. Microbiol. 2012, 14:1434-1454.
10. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
11. Fleige T., Pfaff N., Gross U., Bohne W. Localisation of gluconeogenesis and tricarboxylic acid (TCA)-cycle enzymes and first functional analysis of the TCA cycle in Toxoplasma gondii. Int. J. Parasitol. 2008, 38:1121-1132.
12. Foth B.J., Ralph S.A., Tonkin C.J., Struck N.S., Fraunholz M., Roos D.S., Cowman A.F., McFadden G.I. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 2003, 299:705-708.
13. Gardner M.J., Bishop R., Shah T., de Villiers E.P., Carlton J.M., Hall N., Ren Q., Paulsen I.T., Pain A., Berriman M., Wilson R.J., Sato S., Ralph S.A., Mann D.J., Xiong Z., Shallom S.J., Weidman J., Jiang L., Lynn J., Weaver B., Shoaibi A., Domingo A.R., Wasawo D., Crabtree J., Wortman J.R., Haas B., Angiuoli S.V., Creasy T.H., Lu C., Suh B., Silva J.C., Utterback T.R., Feldblyum T.V., Pertea M., Allen J., Nierman W.C., Taracha E.L., Salzberg S.L., White O.R., Fitzhugh H.A., Morzaria S., Venter J.C., Fraser C.M., Nene V. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 2005, 309:134-137.
14. Horton P., Nakai K. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 1999, 24:34-36.
15. Hulliger L., Wilde K.H., Brown C.G., Turner L. Mode of multiplication of Theileria in cultures of bovine lymphocytic cells. Nature 1964, 203:728-730.
16. Kiama T.N., Kiaira J.K., Konji V.N., Musoke A.J. Enzymes of glucose and glycerol catabolism in in vitro-propagated Theileria parva schizonts. Vet. J. 1999, 158:221-227.
17. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
18. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
19. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int. J. Neural Syst. 1997, 8:581-599.
20. Olszewski K.L., Llinas M. Central carbon metabolism of Plasmodium parasites. Mol. Biochem. Parasitol. 2011, 175:95-103.
21. Pain A., Renauld H., Berriman M., Murphy L., Yeats C.A., Weir W., Kerhornou A., Aslett M., Bishop R., Bouchier C., Cochet M., Coulson R.M., Cronin A., de Villiers E.P., Fraser A., Fosker N., Gardner M., Goble A., Griffiths-Jones S., Harris D.E., Katzer F., Larke N., Lord A., Maser P., McKellar S., Mooney P., Morton F., Nene V., O'Neil S., Price C., Quail M.A., Rabbinowitsch E., Rawlings N.D., Rutter S., Saunders D., Seeger K., Shah T., Squares R., Squares S., Tivey A., Walker A.R., Woodward J., Dobbelaere D.A., Langsley G., Rajandream M.A., McKeever D., Shiels B., Tait A., Barrell B., Hall N. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 2005, 309:131-133.
22. Perkins D.N., Pappin D.J., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
23. Polonais V., Soldati-Favre D. Versatility in the acquisition of energy and carbon sources by the Apicomplexa. Biol. Cell 2010, 102:435-445.
24. Rickard M.D. Carbohydrate metabolism in Babesia rodhaini: investigations with 14C-labeled substrates and enzyme assays. Exp. Parasitol. 1970, 28:512-520.
25. Ruepp A., Zollner A., Maier D., Albermann K., Hani J., Mokrejs M., Tetko I., Guldener U., Mannhaupt G., Munsterkotter M., Mewes H.W. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 2004, 32:5539-5545.
26. Reid, A.J., Vermont, S.J., Cotton, J.A., Harris, D., Hill-Cawthorne, G.A., Könen-Waisman, S., Latham, S.M., Mourier, T., Norton, R., Quail, M.A., Sanders, M., Shanmugam, D., Sohal, A., Wasmuth, J.D., Brunk, B., Grigg, M.E., Howard, J.C., Parkinson, J., Roos, D.S., Trees, A.J., Berriman, M., Pain, A., Wastling, J.M. 2012. Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: Coccidia differing in host range and transmission strategy. PLoS Pathog. 8(3), e1002567. doi:10.1371/journal.ppat.1002567.
27. Sanderson S.J., Xia D., Prieto H., Yates J., Heiges M., Kissinger J.C., Bromley E., Lal K., Sinden R.E., Tomley F., Wastling J.M. Determining the protein repertoire of Cryptosporidium parvum sporozoites. Proteomics 2008, 8:1398-1414.
28. Schmuckli-Maurer J., Shiels B., Dobbelaere D.A. Stochastic induction of Theileria annulata merogony in vitro by chloramphenicol. Int. J. Parasitol. 2008, 38:1705-1715.
29. Schmuckli-Maurer J., Casanova C., Schmied S., Affentranger S., Parvanova I., Kang'a S., Nene V., Katzer F., McKeever D., Müller J., Bishop R., Pain A., Dobbelaere D.A. Expression analysis of the Theileria parva subtelomere-encoded variable secreted protein gene family. PLoS One 2009, 4(3):e4839. 10.1371/journal.pone.0004839.
30. Seitzer U., Gerber S., Beyer D., Dobschanski J., Kullmann B., Haller D., Ahmed J.S. Schizonts of Theileria annulata interact with the microtubuli network of their host cell via the membrane protein TaSP. Parasitol. Res. 2010, 106:1085-1102.
31. Shah T., de Villiers E., Nene V., Hass B., Taracha E., Gardner M.J., Sansom C., Pelle R., Bishop R. Using the transcriptome to annotate the genome revisited: application of massively parallel signature sequencing (MPSS). Gene 2006, 366:104-108.
32. Shiels B., Kinnaird J., McKellar S., Dickson J., Miled L.B., Melrose R., Brown D., Tait A. Disruption of synchrony between parasite growth and host cell division is a determinant of differentiation to the merozoite in Theileria annulata. J. Cell Sci. 1992, 101:99-107.
33. Shiels B., Langsley G., Weir W., Pain A., McKellar S., Dobbelaere D. Alteration of host cell phenotype by Theileria annulata and Theileria parva: mining for manipulators in the parasite genomes. Int. J. Parasitol. 2006, 36:9-21.
34. Skilton R.A., Bishop R.P., Wells C.W., Spooner P.R., Gobright E., Nkonge C., Musoke A.J., Macklin M., Iams K.P. Cloning and characterization of a 150 kDa microsphere antigen of Theileria parva that is immunologically cross-reactive with the polymorphic immunodominant molecule (PIM). Parasitology 1998, 117:321-330.
35. Slavic K., Straschil U., Reininger L., Doerig C., Morin C., Tewari R., Krishna S. Life cycle studies of the hexose transporter of Plasmodium species and genetic validation of their essentiality. Mol. Microbiol. 2010, 75:1402-1413.
36. Swan D.G., Stern R., McKellar S., Phillips K., Oura C.A., Karagenc T.I., Stadler L., Shiels B.R. Characterisation of a cluster of genes encoding Theileria annulata AT hook DNA-binding proteins and evidence for localisation to the host cell nucleus. J. Cell Sci. 2001, 114:2747-2754.
37. van Dooren G.G., Stimmler L.M., McFadden G.I. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol. Rev. 2006, 30:596-630.
38. Voet D., Voet j.g., Pratt C.W. Fundamentals of Biochemistry: Life at the Molecular Level 2006, Wiley, Hoboken, NJ.
39. von Schubert C., Xue G., Schmuckli-Maurer J., Woods K.L., Nigg E.A., Dobbelaere D.A. The transforming parasite Theileria co-opts host cell mitotic and central spindles to persist in continuously dividing cells. PLoS Biol. 2010, 8(9):e1000499. 10.1371/journal.pbio.1000499.
40. Wastling J.M., Xia D., Sohal A., Chaussepied M., Pain A., Langsley G. Proteomes and transcriptomes of the Apicomplexa-where's the message?. Int. J. Parasitol. 2009, 39:135-143.
41. Wastling J.M., Armstrong S.D., Krishna R., Xia D. Parasites, proteomes and systems: has Descartes' clock run out of time?. Parasitology 2012, 139:1103-1118.
42. Weir W., Karagenç T., Baird M., Tait A., Shiels B.R. Evolution and diversity of secretome genes in the apicomplexan parasite Theileria annulata. BMC Genomics 2010, 11:42.
43. Xia D., Sanderson S.J., Jones A.R., Prieto J.H., Yates J.R., Bromley E., Tomley F.M., Lal K., Sinden R.E., Brunk B.P., Roos D.S., Wastling J.M. The proteome of Toxoplasma gondii: integration with the genome provides novel insights into gene expression and annotation. Genome Biol. 2008, 9:R116.
44. Zuegge J., Ralph S., Schmuker M., McFadden G.I., Schneider G. Deciphering apicoplast targeting signals-feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene 2001, 280:19-26.