Proteomic comparison of four Eimeria tenella life-cycle stages: Unsporulated oocyst, sporulated oocyst, sporozoite and second-generation merozoite

Proteomics

Volumn 9, Issue 19, 2009, Pages 4566-4576

  Lal, Kalpana ^a   Bromley, Elizabeth ^b   Oakes, Richard ^b   Prieto, Judith Helena ^c   Sanderson, Sanya J ^d   Kurian, Dominic ^b   Hunt, Lawrence ^b   Yates III, John R ^c   Wastling, Jonathan M ^d   Sinden, Robert E ^a   Tomley, Fiona M ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Apicomplexa; Coccidia; Invasion; Metabolism; Microbiology

Indexed keywords

CELL PROTEIN; MANNITOL; PROTEOME;

ARTICLE; CELL CYCLE; CELL JUNCTION; DEVELOPMENTAL STAGE; EIMERIA TENELLA; ENERGY YIELD; GLUCONEOGENESIS; GLYCOLYSIS; LIFE CYCLE; MEROZOITE; NONHUMAN; OOCYST; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; PROTEOMICS; QUANTITATIVE ANALYSIS; SPOROGENESIS; SPOROZOITE; TWO DIMENSIONAL ELECTROPHORESIS;

ANIMALS; CHICKENS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EIMERIA TENELLA; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; LIFE CYCLE STAGES; MEROZOITES; OOCYSTS; PROTEOME; PROTEOMICS; PROTOZOAN PROTEINS; SPOROZOITES; TANDEM MASS SPECTROMETRY;

APICOMPLEXA; COCCIDIA; EIMERIA TENELLA;

EID: 70350239850     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200900305     Document Type: Article

References (64)

1. Shirley, M. W., Smith, A. L., Tomley, F. M., The biology of avian Eimeria with an emphasis on their control by vaccination. Adv. Parasitol. 2005, 60, 285-330.
2. Ferguson, D. J., Belli, S. I., Smith, N. C., Wallach, M. G., The development of the macrogamete and oocyst wall in Eimeria maxima: immuno-light and electron microscopy. Int. J. Parasitol. 2003, 33, 1329-1340.
3. Ryan, R., Shirley, M., Tomley, F., Mapping and expression of microneme genes in Eimeria tenella. Int. J. Parasitol. 2000, 30, 1493-1499. (Pubitemid 30953156)
4. Rose, M. E., Lawn, A. M., Millard, B. J., The effect of immunity on the early events in the life-cycle of Eimeria tenella in the caecal mucosa of the chicken. Parasitology 1984, 88, 199-210.
5. Lawn, A. M., Rose, M. E., Mucosal transport of Eimeria tenella in the cecum of the chicken. J. Parasitol. 1982, 68, 1117-1123.
6. Vervelde, L., Jeurissen, S. H., The role of intra-epithelial and lamina propria leucocytes during infection with Eimeria tenella. Adv. Exp. Med. Biol. 1995, 371B, 953-958.
7. McDonald, V., Rose, M. E., Eimeria tenella and E. necatrix: A third generation of schizogony is an obligatory part of the developmental cycle. J. Parasitol. 1987, 73, 617-622.
8. Periz, J., Gill, A. C., Hunt, L., Brown, P., Tomley, F. M., The microneme proteins EtMIC4 and EtMIC5 of Eimeria tenella form a novel, ultra-highmolecular mass protein complex that binds target host cells. J. Biol. Chem. 2007, 282, 16891-16898. (Pubitemid 47096591)
9. Greif, G., Entzeroth, R., Eimeria tenella: localisation of rhoptry antigens during parasite-host cell interactions by a rhoptry-specific monoclonal antibody in PCKC culture. Appl. Parasitol. 1996, 37, 253-259.
10. Bumstead, J., Tomley, F., Induction of secretion and surface capping of microneme proteins in Eimeria tenella. Mol. Biochem. Parasitol. 2000, 110, 311-321. (Pubitemid 30845531)
11. Tabares, E., Ferguson, D., Clark, J., Soon, P. E. et al., Eimeria tenella sporozoites and merozoites differentially express glycosylphosphatidylinositol- anchored variant surface proteins. Mol. Biochem. Parasitol. 2004, 135, 123-132. (Pubitemid 38470081)
12. de Venevelles, P., Chich, J. F., Faigle, W., Lombard, B. et al., Study of proteins associated with the Eimeria tenella refractile body by a proteomic approach. Int. J. Parasitol. 2006, 36, 1399-1407. (Pubitemid 44485649)
13. Klotz, C., Marhofer, R. J., Selzer, P. M., Lucius, R., Pogonka, T., Eimeria tenella: identification of secretory and surface proteins from expressed sequence tags. Exp. Parasitol. 2005, 111, 14-23. (Pubitemid 41058889)
14. Miska, K. B., Fetterer, R. H., Barfield, R. C., Analysis of transcripts expressed by Eimeria tenella oocysts using subtractive hybridization methods. J. Parasitol. 2004, 90, 1245-1252.
15. Li, L., Brunk, B. P., Kissinger, J. C., Pape, D. et al., Gene discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Res. 2003, 13, 443-454. (Pubitemid 36395402)
16. de Venevelles, P., Chich, J. F., Faigle, W., Loew, D. et al., Towards a reference map of Eimeria tenella sporozoite proteins by two-dimensional electrophoresis and mass spectrometry. Int. J. Parasitol. 2004, 34, 1321-1331. (Pubitemid 39469989)
17. Long, P. L., Millard, B. J., Joyner, L. P., Norton, C. C., A guide to laboratory techniques used in the study and diagnosis of avian coccidiosis. Folia Vet. Lat. 1976, 6, 201-217.
18. Shirley,M.W., in: Eckert J., Braun R., Shirley,M.W., Coudert P. (Ed.), Biotechnology - Guidlines on Techniques in Coccidiosis Research, Eimeria Species and Strains of Chickens European Commission DGXII, Luxembourg 1995, pp. 1-24.
19. Sanderson, S. J., Xia, D., Prieto, H., Yates, J. et al., Determining the protein repertoire of Cryptosporidium parvum sporozoites. Proteomics 2008, 8, 1398-1414.
20. Link, A. J., Eng, J., Schieltz, D. M., Carmack, E. et al., Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 1999, 17, 676-682. (Pubitemid 29316146)
21. Gatlin, C. L., Kleemann, G. R., Hays, L. G., Link, A. J., Yates, J. R., III, Protein identification at the low femtomole level from silver-stained gels using a new fritless electrospray interface for liquid chromatography-microspray and nanospray mass spectrometry. Anal. Biochem. 1998, 263, 93-101.
22. Washburn, M. P., Wolters,D., Yates 3rd J. R., Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 2001, 19, 242-247.
23. Bern, M., Goldberg, D., McDonald, W. H., Yates 3rd J. R., Automatic quality assessment of peptide tandem mass spectra. Bioinformatics 2004, 20, i49-i54. (Pubitemid 41296670)
24. Gao, J., Opiteck, G. J., Friedrichs, M. S., Dongre, A. R., Hefta, S. A., Changes in the protein expression of yeast as a function of carbon source. J. Proteome Res. 2003, 2, 643-649. (Pubitemid 38017109)
25. Liu, H., Sadygov, R. G., Yates 3rd J. R., A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 2004, 76, 4193-4201. (Pubitemid 38943698)
26. Nanduri, B., Lawrence, M. L., Vanguri, S., Burgess, S. C., Proteomic analysis using an unfinished bacterial genome: the effects of subminimum inhibitory concentrations of antibiotics on Mannheimia haemolytica virulence factor expression. Proteomics 2005, 5, 4852-4863. (Pubitemid 43016905)
27. Quevillon, E., Silventoinen, V., Pillai, S., Harte, N. et al., InterProScan: protein domains identifier. Nucleic Acids Res. 2005, 33, W116-W120.
28. Remm, M., Storm, C. E., Sonnhammer, E. L., Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J. Mol. Biol. 2001, 314, 1041-1052. (Pubitemid 34073068)
29. Ruepp, A., Zollner, A., Maier, D., Albermann, K., The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 2004, 32, 5539-5545. (Pubitemid 39545671)
30. Florens, L., Washburn, M. P., Raine, J. D., Anthony, R. M. et al., A proteomic view of the Plasmodium falciparum life cycle. Nature 2002, 419, 520-526.
31. Kall, L., Krogh, A., Sonnhammer, E. L., Advantages of combined transmembrane topology and signal peptide prediction - the Phobius web server. Nucleic Acids Res. 2007, 35, W429-W432.
32. 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. (Pubitemid 34014880)
33. Eisenhaber, B., Bork, P., Eisenhaber, F., Post-translational GPI lipid anchor modification of proteins in kingdoms of life: analysis of protein sequence data from complete genomes. Protein Eng. 2001, 14, 17-25. (Pubitemid 32318934)
34. Brameier, M., Krings, A., MacCallum, R. M., NucPred - predicting nuclear localization of proteins. Bioinformatics 2007, 23, 1159-1160. (Pubitemid 47050569)
35. 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. (Pubitemid 37352901)
36. Labbe, M., de Venevelles, P., Girard-Misguich, F., Bourdieu, C. et al., Eimeria tenella microneme protein EtMIC3: identification, localisation and role in host cell infection. Mol. Biochem. Parasitol. 2005, 140, 43-53. (Pubitemid 40203413)
37. Tomley, F. M., Billington, K. J., Bumstead, J. M., Clark, J. D., Monaghan, P., EtMIC4: a microneme protein from Eimeria tenella that contains tandem arrays of epidermal growth factor-like repeats and thrombospondin type-I repeats. Int. J. Parasitol. 2001, 31, 1303-1310. (Pubitemid 32868710)
38. Tomley, F. M., Bumstead, J. M., Billington, K. J., Dunn, P. P., Molecular cloning and characterization of a novel acidic microneme protein (Etmic-2) from the apicomplexan protozoan parasite, Eimeria tenella. Mol. Biochem. Parasitol. 1996, 79, 195-206.
39. Kawazoe, U., Tomley, F. M., Frazier, J. A., Fractionation and antigenic characterization of organelles of Eimeria tenella sporozoites. Parasitology 1992, 1, 1-9.
40. Jean, L., Grosclaude, J., Labbe, M., Tomley, F., Pery, P., Differential localisation of an Eimeria tenella aspartyl proteinase during the infection process. Int. J. Parasitol. 2000, 30, 1099-1107. (Pubitemid 30665358)
41. Fetterer, R. H., Jenkins, M. C., Miska, K. B., Barfield, R. C., Characterization of the antigen SO7 during development of Eimeria tenella. J. Parasitol. 2007, 93, 1107-1113.
42. Vermeulen, A. N., Kok, J. J., van den Boogaart, P., Dijkema, R., Claessens, J. A., Eimeria refractile body proteins contain two potentially functional characteristics: transhydrogenase and carbohydrate transport. FEMS Microbiol. Lett. 1993, 110, 223-229. (Pubitemid 223031816)
43. Kinnaird, J. H., Bumstead, J. M., Mann, D. J., Ryan, R. et al., EtCRK2, a cyclin-dependent kinase gene expressed during the sexual and asexual phases of the Eimeria tenella life cycle. Int. J. Parasitol. 2004, 34, 683-692. (Pubitemid 38521223)
44. Ferguson, D. J., Sahoo, N., Pinches, R. A., Bumstead, J. M. et al., MORN1 has a conserved role in asexual and sexual development across the apicomplexa. Eukaryot. Cell. 2008, 7, 698-711. (Pubitemid 351959904)
45. Xia, D., Sanderson, S. J., Jones, A. R., Prieto, J. H. et al., The proteome of Toxoplasma gondii: integration with the genome provides novel insights into gene expression and annotation. Genome Biol. 2008, 9, R116.
46. Alexander, D. L., Mital, J., Ward, G. E., Bradley, P., Boothroyd, J. C., Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathog. 2005, 1, e17.
47. Straub, K. W., Cheng, S. J., Sohn, C. S., Bradley, P. J., Novel components of the Apicomplexan moving junction reveal conserved and coccidia-restricted elements. Cell. Microbiol. 2009, 11, 590-603.
48. Alexander, D. L., Arastu-Kapur, S., Dubremetz, J. F., Boothroyd, J. C., Plasmodium falciparum AMA1 binds a rhoptry neck protein homologous to TgRON4, a component of the moving junction in Toxoplasma gondii. Eukaryot. Cell. 2006, 5, 1169-1173. (Pubitemid 44100714)
49. Besteiro, S., Michelin, A., Poncet, J., Dubremetz, J. F., Lebrun, M., Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLoS Pathog. 2009, 5, e1000309.
50. Xu, J. H., Qin, Z. H., Liao, Y. S., Xie, M. Q. et al., Characterization and expression of an actin-depolymerizing factor from Eimeria tenella. Parasitol. Res. 2008, 103, 263-270.
51. Fetterer, R. H., Miska, K. B., Jenkins, M. C., Barfield, R. C., A conserved 19-kDa Eimeria tenella antigen is a profilin-like protein. J. Parasitol. 2004, 90, 1321-1328.
52. Ferguson, D. J., Birch-Andersen, A., Hutchinson, W. M., Siim, J. C., Light and electron microscopy on the sporulation of the oocysts of Eimeria brunetti. II. Development into the sporocyst and formation of the sporozoite. Acta Pathol. Microbiol. Scand. B 1978, 86, 13-24. (Pubitemid 8341749)
53. Pomel, S., Luk, F. C., Beckers, C. J., Host cell egress and invasion induce marked relocations of glycolytic enzymes in Toxoplasma gondii tachyzoites. PLoS Pathog. 2008, 4, e1000188.
54. Allocco, J. J., Profous-Juchelka, H., Myers, R. W., Nare, B., Schmatz, D. M., Biosynthesis and catabolism of mannitol is developmentally regulated in the protozoan parasite Eimeria tenella. J. Parasitol. 1999, 85, 167-173. (Pubitemid 29251828)
55. Allocco,J. J., Nare,B., Myers,R. W., Feiglin,M. et al., Nitrophenide (Megasul) blocks Eimeria tenella development by inhibiting the mannitol cycle enzyme mannitol-1-phosphate dehydrogenase. J. Parasitol. 2001, 87, 1441-1448.
56. Fukata, T., Sasai, K., Arakawa, A., McDougald, L. R., Penetration of Eimeria tenella sporozoites under different oxygen concentrations in vitro. J. Parasitol. 1992, 78, 537-538.
57. Beyer, T. V., Coccidia of domestic animals. Some metabolic peculiarities of particular stages of the life cycle. J. Parasitol. 1970, 56, 28-29.
58. Labbe, M., Peroval, M., Bourdieu, C., Girard-Misguich, F., Pery, P., Eimeria tenella enolase and pyruvate kinase: A likely role in glycolysis and in others functions. Int. J. Parasitol. 2006, 36, 1443-1452. (Pubitemid 44751749)
59. Schaap, D., Arts, G., van Poppel, N. F., Vermeulen, A. N., De novo ribosome biosynthesis is transcriptionally regulated in Eimeria tenella, dependent on its life cycle stage. Mol. Biochem. Parasitol. 2005, 139, 239-248. (Pubitemid 40128219)
60. Ferguson, D. J., Campbell, S. A., Henriquez, F. L., Phan, L. et al., Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in Eimeria tenella. Int. J. Parasitol. 2007, 37, 33-51. (Pubitemid 46001399)
61. Pal-Bhowmick, I., Vora, H. K., Jarori, G. K., Sub-cellular localization and post-translational modifications of the Plasmodium yoelii enolase suggest moonlighting functions. Malar. J. 2007, 6, 45. (Pubitemid 46663078)
62. Gomes, R. A., Vicente Miranda, H., Sousa Silva, M., Graca, G. et al., Protein glycation and methylglyoxal metabolism in yeast: finding peptide needles in protein haystacks. FEMS Yeast Res. 2008, 8, 174-181.
63. Carruthers, V. B., Tomley, F. M., Microneme proteins in apicomplexans. Subcell. Biochem. 2008, 47, 33-45.
64. Sibley, L. D., Intracellular parasite invasion strategies. Science 2004, 304, 248-253.