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Eimeria tenella glucose-6-phosphate isomerase: molecular characterization and assessment as a target for anti-coccidial control

Published online by Cambridge University Press:  17 March 2010

S.-S. LOO ,
D. P. BLAKE ,
A. MOHD-ADNAN ,
R. MOHAMED  and
K.-L. WAN
S.-S. LOO
Affiliation:
School of Biosciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600UKM Bangi, SelangorDE, Malaysia Malaysia Genome Institute, UKM-MTDC Technology Centre, 43600UKM Bangi, SelangorDE, Malaysia
D. P. BLAKE
Affiliation:
Parasitology, Institute for Animal Health, Compton, BerkshireRG20 7NN, UK
A. MOHD-ADNAN
Affiliation:
School of Biosciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600UKM Bangi, SelangorDE, Malaysia Malaysia Genome Institute, UKM-MTDC Technology Centre, 43600UKM Bangi, SelangorDE, Malaysia
R. MOHAMED
Affiliation:
School of Biosciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600UKM Bangi, SelangorDE, Malaysia Malaysia Genome Institute, UKM-MTDC Technology Centre, 43600UKM Bangi, SelangorDE, Malaysia
K.-L. WAN*
Affiliation:
School of Biosciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600UKM Bangi, SelangorDE, Malaysia Malaysia Genome Institute, UKM-MTDC Technology Centre, 43600UKM Bangi, SelangorDE, Malaysia
*
*Corresponding author: School of Biosciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600UKM Bangi, SelangorDE, Malaysia. Tel: +603 8921 5997. Fax: +603 8925 2698. E-mail: klwan@ukm.my
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Summary

Limitations with current chemotherapeutic and vaccinal control of coccidiosis caused by Eimeria species continue to prompt development of novel controls, including the identification of new drug targets. Glucose-6-phosphate isomerase (G6-PI) has been proposed as a valid drug target for many protozoa, although polymorphism revealed by electrophoretic enzyme mobility has raised doubts for Eimeria. In this study we identified and sequenced the Eimeria tenella G6-PI orthologue (EtG6-PI) from the reference Houghton strain and confirmed its position within the prevailing taxonomic hierarchy, branching with the Apicomplexa and Plantae, distinct from the Animalia including the host, Gallus gallus. Comparison of the deduced 1647 bp EtG6-PI coding sequence with the 9016 bp genomic locus revealed 15 exons, all of which obey the intron-AG-/exon/-GT-intron splicing rule. Comparison with the Weybridge and Wisconsin strains revealed the presence of 33 single nucleotide polymorphisms (SNPs) and 14 insertion/deletion sites. Three SNPs were exonic and all yielded non-synonymous substitutions. Preliminary structural predictions suggest little association between the coding SNPs and key G6-PI catalytic residues or residues thought to be involved in the coordination of the G6-PI's substrate phosphate group. Thus, the significant polymorphism from its host orthologue and minimal intra-specific polymorphism suggest G6-PI remains a valid anti-coccidial drug target.

Keywords

G6-PIcoccidiosisdrug targetEimeria tenella
Type
Research Article
Information
Parasitology , Volume 137 , Issue 8 , July 2010 , pp. 1169 - 1177
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.Google Scholar
Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195–201.CrossRefGoogle ScholarPubMed
Bromley, E., Leeds, N., Clark, J., McGregor, E., Ward, M., Dunn, M. J. and Tomley, F. (2003). Defining the protein repertoire of microneme secretory organelles in the apicomplexan parasite Eimeria tenella. Proteomics 3, 1553–1561.Google Scholar
Carreno, R. A., Martin, D. S and Barta, J. R. (1999). Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences. Parasitology Research 85, 899–904.Google Scholar
Chapman, H. D. (1997). Biochemical, genetic and applied aspects of drug resistance in Eimeria parasites of the fowl. Avian Pathology 28, 221–244.CrossRefGoogle Scholar
Chapman, H. and Shirley, M. W. (2003). The Houghton strain of Eimeria tenella: a review of the type strain selected for genome sequencing. Avian Pathology 32, 115–127.CrossRefGoogle ScholarPubMed
Cordeiro, A. T., Michels, P. A., Delboni, L. F. and Thiemann, O. H. (2004). The crystal structure of glucose-6-phosphate isomerase from Leishmania mexicana reveals novel active site features. European Journal of Biochemistry 271, 2765–2772.CrossRefGoogle ScholarPubMed
Dzierszinski, F., Popescu, O., Toursel, C., Slomianny, C., Yahiaoui, B. and Tomavo, S. (1999). The protozoan parasite Toxoplasma gondii expresses two functional plant-like glycolytic enzymes. Implications for evolutionary origin of apicomplexans. The Journal of Biological Chemistry 274, 24888–24895.Google Scholar
Edgar, R. C. (2004 a). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Edgar, R. C. (2004 b). MUSCLE: a multiple sequence alignment method with reduces time and space complexity. BMC Bioinformatics 5, 113.Google Scholar
Felsenstein, J. (1989). Phylogeny Inference Package (Version 3.2). Cladistics 5, 164–166.Google Scholar
Funes, S., Davidson, E., Reyes-Prieto, A., Magallón, S., Herion, P., King, M. P. and González-Halphen, D. (2002). A green algal apicoplast ancestor. Science 298, 2115.Google Scholar
Grauvogel, C., Brinkmann, H. and Peterson, J. (2007). Evolution of the glucose-6-phosphate isomerase: the plasticity of the primary metabolism in the photosythetic eukaryotes. Molecular Biology and Evolution 24, 1611–1621.CrossRefGoogle Scholar
Hardré, R., Salmon, L. and Opperdoes, F. R. (2000). Competitive inhibition of Trypanosoma brucei phosphoglucose isomerase by D-arabinose-5-phosphate derivatives. Journal of Enzyme Inhibition 15, 509–515.Google Scholar
Jeffers, T. K. (1975). Attenuation of Eimeria tenella through selection for precociousness. Journal of Parasitology 61, 1083–1090.CrossRefGoogle ScholarPubMed
Joyner, L. P. and Norton, C. C. (1969). A comparison of two laboratory strains of Eimeria tenella. Parasitology 59, 907–913.CrossRefGoogle ScholarPubMed
Köhler, S., Delwiche, C. F., Denny, P. W., Tilney, L. G., Webster, P., Wilson, R. J., Palmer, J. D. and Roos, D. S. (1997). A plastid of probable green algal origin in apicomplexan parasites. Science 275, 1485–1489.Google Scholar
Leander, B. S., Clopton, R. E. and Keeling, P. J. (2003). Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and beta-tubulin. International Journal of Systematic Evolutionary Microbiology 53, 345–354.Google Scholar
Ling, K.-H., Loo, S.-S., Rosli, R., Mariana, N. S., Mohamed, R. and Wan, K.-L. (2007 a). In silico identification and characterization of a putative phosphatidylinositol 4-phosphate 5-kinase (PIP5K) gene in Eimeria tenella. In Silico Biology 7, 115–121.Google ScholarPubMed
Ling, K.-H., Rajandream, M.-A., Rivailler, P., Ivens, A., Yap, S.-J., Madeira, A. M. B. N., Mungall, K., Billington, K., Yee, W.-Y., Bankier, A. T., Carroll, F., Durham, A. M., Peters, N., Loo, S.-S., Mat-Isa, M. N., Novaes, J., Quail, M., Rosli, R., Mariana, N. S., Sobreira, T. J. P., Tivey, A., Wai, S.-F., White, S., Wu, X., Kerhornou, A., Blake, D., Mohamed, R., Shirley, M., Gruber, A., Berriman, M., Tomley, F., Dear, P. H. and Wan, K.-L. (2007 b). Sequencing and analysis of chromosome 1 of Eimeria tenella reveals a unique segmental organization. Genome Research 17, 311–319.CrossRefGoogle ScholarPubMed
Matrajt, M., Nishi, M., Fraunholz, M. J., Peter, O. and Roos, D. S. (2002) Amino-terminal control of transgenic protein expression levels in Toxoplasma gondii. Molecular and Biochemical Parasitology 20, 285–289.Google Scholar
Mount, S. M. (1982). A catalogue of splice junction sequences. Nucleic Acids Research 10, 459–472.Google Scholar
Ng, S.-T., Jangi, M. S., Shirley, M. W., Tomley, F. M. and Wan, K.-L. (2002). Comparative EST analyses provide insights into gene expression in two asexual developmental stages of Eimeria tenella. Experimental Parasitology 101, 168–173.Google Scholar
Page, R. D. M. (1996). TREEVIEW: An application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google Scholar
Razmjou, E., Haghighi, A., Rezaian, M., Kobayashi, S. and Nozaki, T. (2006). Genetic diversity of glucose phosphate isomerase from Entamoeba histolytica. Parasitology International 55, 307–311.Google Scholar
Seeber, F. (1997). Consensus sequence of translational initiation sites from Toxoplasma gondii genes. Parasitology Research 83, 309–311.CrossRefGoogle ScholarPubMed
Shirley, M. W. (1995). Eimeria species and strains of chickens. In Biotechnology – Guidelines on Techniques in Coccidiosis Research (ed. Eckert, J., Braun, R., Shirley, M. W. and Coudert, P.), pp. 1–24. European Commission, Luxembourg.Google Scholar
Shirley, M. W., Chapman, H. D., Kucera, J., Jeffers, T. K. and Bedrnir, P. (1989). Enzyme variation and pathogenicity of recent field isolates of Eimeria tenella. Research in Veterinary Science 46, 79–83.CrossRefGoogle ScholarPubMed
Shirley, M. W., Ivens, A., Gruber, A., Madeira, A. M. B. N., Wan, K.-L., Dear, P. H. and Tomley, F. M. (2004). The Eimeria genome projects: a sequence of events. Trends in Parasitology 20, 199–201.Google Scholar
Sun, Y.-J., Chou, C.-C., Chen, W.-S., Wu, R.-T., Meng, M. and Hsiao, C.-D. (1999). The crystal structure of a multifunctional protein: Phosphoglucose isomerase/autocrine motility factor/neuroleukin. Proceedings of the National Academy of Sciences, USA 96, 5412–5417.Google Scholar
Sutton, C. A., Shirley, M. W. and McDonald, V. (1986). Genetic recombination of markers for precocious development, arprinocid resistance, and isoenzymes of glucose phosphate isomerase in Eimeria acervulina. Journal of Parasitology 72, 965–967.Google Scholar
Wan, K.-L., Chong, S.-P., Ng, S.-T., Shirley, M. W., Tomley, F. M. and Jangi, M. S. (1999). A survey of genes in Eimeria tenella merozoites by EST sequencing. International Journal for Parasitology 29, 1885–1892.Google Scholar
Zhu, G., Keithly, J. S. and Philippe, H. (2000). What is the phylogenetics position of Cryptosporidium? International Journal of Systematic Evolutionary Microbiology 50, 1673–1681.Google Scholar