Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T21:48:09.577Z Has data issue: false hasContentIssue false
  • English
  • Français

Sequence, expression and localization of calmodulin-domain protein kinases in Eimeria tenella and Eimeria maxima

Published online by Cambridge University Press:  06 April 2009

P. P. J. Dunn ,
J. M. Bumstead  and
F. M. Tomley
P. P. J. Dunn
Affiliation:
Institute for Animal Health, Compton, Newbury, Berkshire RG20 7NN, UK
J. M. Bumstead
Affiliation:
Institute for Animal Health, Compton, Newbury, Berkshire RG20 7NN, UK
F. M. Tomley*
Affiliation:
Institute for Animal Health, Compton, Newbury, Berkshire RG20 7NN, UK
*
*Corresponding author. Tel: + 44 1635 577276. Fax: + 44 635 577263. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

We have isolated and sequenced cDNA clones from Eimeria tenella and Eimeria maxima which encode proteins that share homology with a recently described family of calmodulin-domain protein kinases. The primary sequence data show that each of the protein kinases can be divided into 2 main functional domains – an amino-terminal catalytic domain typical of serine/threonine protein kinases and a carboxy-terminal domain homologous to calmodulin, which is capable of binding calcium ions at 4 ‘EF-hand’ motifs. Expression of the E. tenella calmodulin-domain protein kinase (EtCDPK) increased towards the end of oocyst sporulation, as judged by Northern and Western blotting, and indirect immunofluorescent antibody labelling showed that within a few minutes of adding sporozoites to target host cells in in vitro culture EtCDPK was found to be specifically associated with a filament-like structure that converges at the apical end of the parasite. Once the parasite entered the host cell EtCDPK appeared to be left on the host cell membrane at the point of entry, indicating a brief yet specific role for this molecule in the invasion of host cells by E. tenella.

Keywords

Eimeriacalmodulin-domain protein kinasesequenceinvasionPlasmodium falciparum calcium-dependent protein kinase
Type
Research Article
Information
Parasitology , Volume 113 , Issue 5 , November 1996 , pp. 439 - 448
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Banerjee, C. & Sarkar, D. (1992). Isolation and characterisation of a cyclic nucleotide-independent protein kinase from Leishmania donovani. Molecular and Biochemical Parasitology 52, 195–206.Google Scholar
Bossemeyer, D. (1995). Protein kinases – structure and function. FEES Letters 369, 57–61.CrossRefGoogle ScholarPubMed
Bumstead, J. M., Dunn, P. P. J. & 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.CrossRefGoogle ScholarPubMed
Cheung, W. Y. (1970). Cyclic 3′,5′-nucleotide phosphodiesterase. Demonstration of an activator. Biochemical and Biophysical Research Communications 38, 533–538.CrossRefGoogle Scholar
Church, G. M. & Gilbert, W. (1984). Genomic sequencing. Proceedings of the National Academy of Sciences, USA 81, 1991–1995.CrossRefGoogle ScholarPubMed
Clapham, D. E. (1995). Calcium signalling. Cell 80, 259–268.Google Scholar
Das, S., Saha, A. K., Mukhopadhyay, N. K. & Glew, R. H. (1986). A cyclic nucleotide-dependent protein kinase in Leishmania donovani. The Biochemical Journal 240, 641–649.CrossRefGoogle Scholar
Gale, J. R. M. & Parsons, M. (1993). A Trypanosoma brucei gene family encoding protein kinases with catalytic domains structurally related to Nek1 and NIMA. Molecular and Biochemical Parasitology 59, 111–122.CrossRefGoogle ScholarPubMed
Gomez, M. L., Erijman, L., Arauzo, S., Torres, H. N. & Tellezinon, M. T. (1989). Protein kinase C in Trypanosoma cruzi epimastigote forms: partial purification and characterisation. Molecular and Biochemical Parasitology 36, 101–108.CrossRefGoogle Scholar
Hanks, S. K. (1991). Eukaryotic protein kinases. Current Opinion in Structural Biology 1, 369–383.CrossRefGoogle Scholar
Hanks, S. K. & Quinn, A. M. (1991). Protein kinase catalytic domain sequence database: Identification of conserved features of primary structure and classification of family members. Methods in Enzymology 200, 38–62.CrossRefGoogle ScholarPubMed
Harmon, A. C., Yoo, B.-C. & McCaffery, C. (1994). Pseudosubstrate inhibition of CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 33, 7278–7287.CrossRefGoogle ScholarPubMed
Harper, J. F., Sussman, M. R., Schaller, G. E., Putnam-Evans, C., Charbonneau, H. & Harmon, A. C. (1991). A calcium-dependent protein kinase with a regulatory domain similar to calmodulin. Science 252, 951–954.CrossRefGoogle ScholarPubMed
Hunter, T. (1987). A thousand and one protein kinases. Cell 50, 823–829.Google Scholar
Jameson, B. A. & Wolf, H. (1988). The antigenic index: a novel algorithm for predicting antigenic determinants. CABIOS 4, 181–186.Google Scholar
Kappes, B., Yang, J., Suetterlin, B. W., Rathgeb-Szabo, K., Lindt, M. J. & Franklin, R. M. (1995). A Plasmodium falciparum protein kinase with two unusually large inserts. Molecular and Biochemical Parasitology 72, 163–177.CrossRefGoogle Scholar
Keith, K., Hide, G. & Tait, A. (1990). Characterisation of protein kinase C-like activities in Trypanosoma brucei. Molecular and Biochemical Parasitology 43, 107–116.CrossRefGoogle ScholarPubMed
Kemp, B. E. & Pearson, R. B. (1990). Protein kinase recognition sequence motifs. Trends in Biochemical Sciences 15, 342–346.CrossRefGoogle ScholarPubMed
Kretsinger, R. H. & Nockolds, C. E. (1973). Carp muscle calcium-binding protein II structure determination and general description. Journal of Biological Chemistry 248, 3313–3326.CrossRefGoogle ScholarPubMed
Logemann, J., Schell, J. & Willimitzer, L. (1987). Improved method for the isolation of RNA from plant tissues. Analytical Biochemistry 163, 16–20.CrossRefGoogle ScholarPubMed
Long, P. L., Joyner, L. N., Millard, B. J. & 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
McCallum-Deighton, N. & Holder, A. A. (1992). The role of calcium in the invasion of human erythrocytes by Plasmodium falciparum. Molecular and Biochemical Parasitology 50, 317–324.CrossRefGoogle ScholarPubMed
Ng, H. C., Singh, M. & Jeyaseelan, K. (1995). Molecular cloning of a Snf1 type protein kinase gene from Toxoplasma gondii. Biochemistry and Molecular Biology International 35, 155–165.Google Scholar
Parsons, M., Valentine, M. & Carter, V. (1993). Protein kinases in divergent eukaryotes: identification of protein kinase activities regulated during trypanosome development. Proceedings of the National Academy of Sciences, USA 90, 2656–2660.Google Scholar
Pearson, W. R. & Lipman, D. J. (1988). Improved tools for biological sequence comparison. Proceedings of the National Academy of Sciences, USA 85, 2444–2448.CrossRefGoogle ScholarPubMed
Putnam-Evans, C., Harmon, A. C. & Cormier, M. J. (1990). Purification and characterisation of a novel calcium-dependent protein kinase from soybean. Biochemistry 29, 2488–2495.Google Scholar
Putnam-Evans, C., Harmon, A. C., Palevitz, B. A., Fecheimer, M. & Cormier, M. J. (1989). Calcium-dependent protein kinase is localised with F-actin in plant cells. Cell Motility and the Cytoskeleton 12, 12–22.CrossRefGoogle Scholar
Read, L. K. & Mikkelsen, R. B. (1990). Cyclic AMP and Ca2+-dependent protein kinases in Plasmodium falciparum. Experimental Parasitology 71, 39–48.Google Scholar
Robson, K. J. H. & Jennings, M. W. (1991). The structure of the calmodulin gene of Plasmodium falciparum. Molecular and Biochemical Parasitology 46, 19–34.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning. A Laboratory Manual, 2nd Edn.Cold Spring Harbour Laboratory Press, Cold Spring Harbour, New York.Google Scholar
Schmatz, D. M., Crane, M. S. & Murray, P. K. (1984). Purification of Eimeria sporozoites by DE52 anion exchange chromatography. Journal of Protozoology 31, 181–183.CrossRefGoogle ScholarPubMed
Staden, R. (1982). Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Research 10, 4731–4751.Google Scholar
Stone, J. M. & Walker, J. C. (1995). Plant protein kinase families and signal transduction. Plant Physiology 108, 451–457.CrossRefGoogle ScholarPubMed
Wheeler-Alm, E. & Shapiro, S. Z. (1992). Evidence of a tyrosine kinase activity in the protozoan parasite Trypanosoma brucei. Journal of Protozoology 39, 413–416.Google Scholar
Zhao, Y., Franklin, R. M. & Kappes, B. (1994 a). Plasmodium falciparum calcium-dependent protein kinase phosphorylates proteins of the host erythrocytic membrane. Molecular and Biochemical Parasitology 66, 329–343.Google Scholar
Zhao, Y., Kappes, B. & Franklin, R. M. (1993). Gene structure and expression of an unusual protein kinase from Plasmodium falciparum homologous at its carboxyl terminus with EF-hand calcium-binding proteins. Journal of Biological Chemistry 268, 4347–4354.CrossRefGoogle ScholarPubMed
Zhao, Y., Kappes, B., Yang, J. & Franklin, R. M. (1992). Molecular cloning and stage-specific expression and cellular distribution of a putative protein kinase from Plasmodium falciparum. European Journal of Biochemistry 207, 305–313.Google Scholar
Zhao, Y., Pokutta, S., Maurer, P., Lindt, M. & Franklin, R. M. (1994 b). Calcium-binding properties of a calcium-dependent protein kinase from Plasmodium falciparum and the significance of individual calcium-binding sites for kinase activation. Biochemistry 33, 3714–3721.Google Scholar