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An Eimeria vaccine candidate appears to be lactate dehydrogenase; characterization and comparative analysis

Published online by Cambridge University Press:  13 May 2004

D. SCHAAP ,
G. ARTS ,
J. KROEZE ,
R. NIESSEN ,
S. V. ROOSMALEN-VOS ,
K. SPREEUWENBERG ,
C. M. KUIPER ,
N. V. D. BEEK-VERHOEVEN ,
J. J. KOK  and
R. M. A. KNEGTEL
...Show all authors
D. SCHAAP
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands
G. ARTS
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands
J. KROEZE
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands Present address: Department of Parasitology, Leiden University Medical Centre, the Netherlands.
R. NIESSEN
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands
S. V. ROOSMALEN-VOS
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands
K. SPREEUWENBERG
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands
C. M. KUIPER
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands
N. V. D. BEEK-VERHOEVEN
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands
J. J. KOK
Affiliation:
Target Discovery Unit, Organon, PO Box 20, 5340BH Oss, the Netherlands
R. M. A. KNEGTEL
Affiliation:
Target Discovery Unit, Organon, PO Box 20, 5340BH Oss, the Netherlands Present address: Vertex Pharmaceuticals (Europe) Ltd, 88 Milton Park, Abingdon, Oxfordshire, UK.
A. N. VERMEULEN
Affiliation:
Parasitology R&D, Intervet International BV, PO Box 31, 5830AA Boxmeer, the Netherlands
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Abstract

An Eimeria acervulina protein fraction was identified which conferred partial protection against an E. acervulina challenge infection. From this fraction a 37 kDa protein was purified and its corresponding cDNA was cloned and shown to encode a lactate dehydrogenase (LDH). Full length cDNAs encoding LDH from two related species, E. tenella and E. maxima, were also cloned. The homology between the primary amino acid sequences of these three Eimeria LDH enzymes was rather low (66–80%), demonstrating an evolutionary divergence. The Plasmodium LDH crystal structure was used to generate a 3D-model structure of E. tenella LDH, which demonstrated that the many variations in the primary amino acid sequences (P. falciparum LDH and E. tenella LDH show only 47% identity) had not resulted in altered 3D-structures. Only a single LDH gene was identified in Eimeria, which was active as a homotetramer. The protein was present at similar levels throughout different parasitic stages (oocysts, sporozoites, schizonts and merozoites), but its corresponding RNA was only observed in the schizont stage, suggesting that its synthesis is restricted to the intracellular stage.

Keywords

EimeriaApicomplexalactate dehydrogenasevaccine
Type
Research Article
Information
Parasitology , Volume 128 , Issue 6 , June 2004 , pp. 603 - 616
Copyright
2004 Cambridge University Press

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References

REFERENCES

ALLEN, P. C. & FETTERER, R. H. ( 2002). Recent advances in biology and immunobiology of Eimeria species and in diagnosis and control of infection with these coccidian parasites of poultry. Clinical Microbiology Reviews 15, 58–65.CrossRefGoogle Scholar
ALLOCCO, J. J., PROFOUS-JUCHELKA, H., MYERS, R. W., NARE, B. & SCHMATZ, D. M. ( 1999). Biosynthesis and catabolism of mannitol is developmentally regulated in the protozoan parasite Eimeria tenella. Journal of Parasitology 85, 167–173.CrossRefGoogle Scholar
BORDIER, C. ( 1981). Phase separation of integral membrane proteins in Triton X-114 solution. Journal of Biological Chemistry 256, 1604–1607.Google Scholar
BUMSTEAD, J. M., DUNN, P. P. & TOMLEY, F. M. ( 1995). Nitrocellulose immunoblotting for identification and molecular gene cloning of Eimeria maxima antigens that stimulate lymphocyte proliferation. Clinical and Diagnostic Laboratory Immunology 2, 524–530.Google Scholar
CRANE, M. S., GOGGIN, B., PELLEGRINO, R. M., RAVINO, O. J., LANGE, C., KARKHANIS, Y. D., KIRK, K. E. & CHAKRABORTY, P. R. ( 1991). Cross-protection against four species of chicken coccidia with a single recombinant antigen. Infection and Immunity 59, 1271–1277.Google Scholar
COOMBS, G. H., DENTON, H., BROWN, S. M. & THONG, K. W. ( 1997). Biochemistry of the coccidia. Advances in Parasitology 39, 141–226.CrossRefGoogle Scholar
DUNN, C. R., BANFIELD, M. J., BARKER, J. J., HIGHAM, C. W., MORETON, K. M., TURGUT-BALIK, D., BRADY, R. L. & HOLBROOK, J. J. ( 1996). The structure of lactate dehydrogenase from Plasmodium falciparum reveals a new target for anti-malarial design. Nature Structural Biology 3, 912–915.CrossRefGoogle Scholar
FINE, I. H., KAPLAN, N. O. & KUFTINEC, D. ( 1963). Developmental changes of mammalian lactic dehydrogenases. Biochemistry 2, 116–121.CrossRefGoogle Scholar
GOMEZ, M. S., PIPER, R. C., HUNSAKER, L. A., ROYER, R. E., DECK, L. M., MAKLER, M. T. & VANDER JAGT, D. L. ( 1997). Substrate and cofactor specificity and selective inhibition of lactate dehydrogenase from the malarial parasite P. falciparum. Molecular and Biochemical Parasitology 90, 235–246.CrossRefGoogle Scholar
HARLOW, E. & LANE, D. ( 1988). Antibodies, a Laboratory Manual. Cold Spring Harbor Press, NY, USA.
JEFFERS, T. K. & LONG, P. L. ( 1985) Eimeria tenella: immunogenicity of arrested sporozoites in chickens. Experimental Parasitology 60, 175–180.CrossRefGoogle Scholar
JENKINS, M. C., AUGUSTINE, P. C., DANFORTH, H. D. & BARTA, J. R. ( 1991). X-irradiation of Eimeria tenella oocysts provides direct evidence that sporozoite invasion and early schizont development induce a protective immune response(s). Infection and Immunity 59, 4042–4048.Google Scholar
JENKINS, M. C., CASTLE, M. D. & DANFORTH, H. D. ( 1991). Protective immunization against the intestinal parasite Eimeria acervulina with recombinant coccidial antigen. Poultry Science 70, 539–547.CrossRefGoogle Scholar
JENKINS, M. C., DANFORTH, H. D., LILLEHOJ, H. S. & FETTERER, R. H. ( 1989). cDNA encoding an immunogenic region of a 22 kilodalton surface protein of Eimeria acervulina sporozoites. Molecular and Biochemical Parasitology 15, 153–161.CrossRefGoogle Scholar
LAURENT, F., BOURDIEU, C., KAGA, M., CHILMONCZYK, S., ZGRZEBSKI, G., YVORE, P. & PERY, P. ( 1993). Cloning and characterization of an Eimeria acervulina sporozoite gene homologous to aspartyl proteinases. Molecular and Biochemical Parasitology 62, 303–312.CrossRefGoogle Scholar
LI, S. S. ( 1990). Human and mouse lactate dehydrogenase genes A (muscle), B (heart), and C (testis): protein structure, genomic organization, regulation of expression, and molecular evolution. Progress in Clinical Biological Research 344, 75–99.Google Scholar
LONG, P. L., MILLARD, B. J., JOYNER, L. P. & NORTON, C. C. ( 1976). A guide to laboratory techniques used in the study and diagnosis of avian coccidiosis. Folia Veterinaria Latina 6, 201–217.Google Scholar
MARKERT, C. L., SHAKLEE, J. B. & WHITT, G. S. ( 1975). Evolution of a gene. Multiple genes for LDH isozymes provide a model of the evolution of gene structure, function and regulation. Science 189, 102–114.Google Scholar
McDONALD, V., ROSE, M. E. & JEFFERS, T. K. ( 1986). Eimeria tenella: immunogenicity of the first generation of schizogony. Parasitology 93, 1–7.CrossRefGoogle Scholar
McDONALD, V., WISHER, M. H., ROSE, M. E. & JEFFERS, T. K. ( 1988). Eimeria tenella: immunological diversity between asexual generations. Parasite Immunology 10, 649–660.CrossRefGoogle Scholar
MILLER, G. A., BHOGAL, B. S., McCANDLISS, R., STRAUSBERG, R. L., JESSEE, E. J., ANDERSON, A. C., FUCHS, C. K., NAGLE, J., LIKEL, M. H., STRASSER, J. M. & STRAUSBERG, S. ( 1989). Characterization and vaccine potential of a novel recombinant coccidial antigen. Infection and Immunity 57, 2014–2020.Google Scholar
NICHOLAS, K. B., NICHOLAS, H. B. Jr. & DEERFIELD, IID. W. ( 1997). GeneDoc: analysis and visualization of genetic variation. EMBNEW.News 4, 14.Google Scholar
PACHECO, N. D., VETTERLING, J. M. & DORAN, D. J. ( 1975). Ultrastructure of cytoplasmic and nuclear changes in Eimeria tenella during first-generation schizogony in cell culture. Journal of Parasitology 61, 31–42.CrossRefGoogle Scholar
REID, W. M. ( 1972). Coccidiosis. In Diseases of Poultry, 6th Edn ( ed. Hofstad, M. S. ), pp. 945–977. Iowa State University Press, Iowa, USA.
SAMBROOK, J., FRITSCH, E. F. & MANIATIS, T. ( 1989). Molecular Cloning, a Laboratory Manual, 2nd Edn. Cold Spring Harbor Press, NY, USA.
SHIRLEY, M. W. ( 1975). Enzyme variation in Eimeria species of the chicken. Parasitology 71, 369–376.CrossRefGoogle Scholar
SHIRLEY, M. W. ( 1986). New methods for the identification of species and strains of Eimeria. In Research in Avian Coccidiosis. Proceedings of the Georgia Coccidiosis Conference (ed. McDougald, L. R., Joyner, L. P. & Long, P. L.), pp. 13–35. University of Georgia, Athens.
SHIRLEY, M. W., CHAPMAN, H. D., KUCERA, J., JEFFERS, T. K. & BEDRNIR, P. ( 1989). Enzyme variation and pathogenicity of recent field isolates of Eimeria tenella. Research in Veterinary Science 46, 79–83.Google Scholar
SMITH, N., MILLER, C. M. D., PETRACCA, M. & ECKERT, J. ( 1995). Techniques for detecting immune responses of avian hosts. COST 89/820, Guidelines on Techniques in Coccidiosis Research. European Commission ( ed. Eckert, J., Braun, R., Shirley, M. W. & Coudert, P.), pp. 164–175. Office for Official Publications of the European Community, Luxemburg.
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINS, D. G. ( 1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.CrossRefGoogle Scholar
TOMLEY, F. M., CLARKE, L. E., KAWAZOE, U., DIJKEMA, R. & KOK, J. J. ( 1991). Sequence of the gene encoding an immunodominant microneme protein of Eimeria tenella. Molecular and Biochemical Parasitology 49, 277–288.CrossRefGoogle Scholar
VERMEULEN, A. N., KOK, J. J., VAN DEN BOOGAART, P., DIJKEMA, R. & CLAESSENS, J. A. ( 1993). Eimeria refractile body proteins contain two potentially functional characteristics: transhydrogenase and carbohydrate transport. FEMS Microbiology Letters 110, 223–229.CrossRefGoogle Scholar
VERMEULEN, A. N., SCHAAP, D. & SCHETTERS, T. P. ( 2001). Control of coccidiosis in chickens by vaccination. Veterinary Parasitology 100, 13–20.CrossRefGoogle Scholar
WHITE, J. L., HACKERT, M. L., BUEHNER, M., ADAMS, M. J., FORD, G. C., LENTZ, P. J. Jr., SMILEY, I. E., STEINDEL, S. J. & ROSSMANN, M. G. ( 1976). A comparison of the structures of apo dogfish M4 lactate dehydrogenase and its ternary complexes. Journal of Molecular Biology 102, 759–779.CrossRefGoogle Scholar
WILKS, H. M., HART, K. W., FEENEY, R., DUNN, C. R., MUIRHEAD, H., CHIA, W. N., BARSTOW, D. A., ATKINSON, T., CLARKE, A. R. & HOLBROOK, J. J. ( 1988). A specific, highly active malate dehydrogenase by redesign of a lactate dehydrogenase framework. Science 242, 1541–1544.CrossRefGoogle Scholar
YANG, S. & PARMLEY, S. F. ( 1997). Toxoplasma gondii expresses two distinct lactate dehydrogenase homologous genes during its life cycle in intermediate hosts. Gene 184, 1–12.CrossRefGoogle Scholar