Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-24T17:07:42.494Z Has data issue: false hasContentIssue false
  • English
  • Français

Oxytetracycline inhibition of mitochondrial protein synthesis in bovine lymphocytes infected with Theileria parva or stimulated by mitogen

Published online by Cambridge University Press:  06 April 2009

P. R. Spooner
P. R. Spooner
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
Get access Rights & Permissions [Opens in a new window]

Summary

Oxytetracycline (OTC) significantly inhibited cytochrome c oxidase activity in bovine lymphocytes infected with Theileria parva and in uninfected mitogen-stimulated lymphocytes. The inhibitory effect was detected in vitro within 24 h of treatment with drug concentrations as low as 1 µg/ml. Following mitogen stimulation of lymphocytes, concentrations of 3 and 10 µg/ml OTC completely inhibited an increase in cytochrome c oxidase activity for 48–72 h. This inhibitory activity was considered to be due to a direct effect on lymphoblast mitochondrial protein synthesis. As a consequence, adenosine triphosphate activity was significantly reduced in lymphocytes stimulated either by infection with T. parva sporozoites or by mitogen and then treated with OTC. The results also indicated that parasite mitochondrial protein synthesis was inhibited by OTC. The activity of OTC reported in this study could explain the suppression of disease following ‘infection and treatment’ immunization against East Coast fever and the in vitro drug-inhibition of schizont development.

Keywords

Theileria parvaEast Coast feveroxytetracyclinemitochondrial protein synthesisbovine lymphocytesimmunization
Type
Research Article
Information
Parasitology , Volume 101 , Issue 3 , December 1990 , pp. 387 - 393
Copyright
Copyright © Cambridge University Press 1990

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

Ashman, R. F. (1984). Lymphocyte activation. In Fundamental immunology (ed. Pàül, W. E.), pp. 267–300. New York: Raven Press.Google Scholar
Blum, J. J., Yayon, A., Friedman, S. & Ginsburg, H. (1984). Effects of mitochondrial protein synthesis inhibition on the incorporation of isoleucine into Plasmodium falciparum in vitro. Journal of Protozoology 31, 475–9.Google Scholar
Borst, P., Ruttenberg, G. J. C. M. & Kroon, A. M. (1967). Mitochondrial DNA. I. Preparation and properties of mitochondrial DNA from chick liver. Biochimica et Biophysica Acta 149, 140–55.Google Scholar
Brown, W. C. & Grab, D. J. (1985). Biological and biochemical characterization of bovine interleukin 2. Studies with cloned bovine T cells. Journal of Immunology 133, 3184–90.CrossRefGoogle Scholar
Brown, W. C. & Logan, K. S. (1986). Bovine T-cell clones infected with Theileria parva produce a factor with IL 2-like activity. Parasite Immunology 8, 189–92.Google Scholar
Connamacher, R. H. & Mandel, H. G. (1965). Binding of tetracycline to the 30S ribosomes and to polyuridylic acid. Biochemical and Biophysical Research Communications 20, 98–103.Google Scholar
Cooperstein, S. J. & Lazarow, A. (1951). A microspectrophotometric method for the determination of cytochrome oxidase. Journal of Biological Chemistry 189, 665–70.CrossRefGoogle ScholarPubMed
Davey, L. A., Ferber, M. T. & Kaye, B. (1985). Comparison of the serum pharmacokinetics of a long-acting and a conventional oxytetracycline injection. Veterinary Record 117, 426–9.Google Scholar
Day, L. E. (1966). Tetracycline inhibition of cell free protein synthesis. II. Effect of the binding of tetracycline to the components of the system. Journal of Bacteriology 92, 197–203.Google Scholar
De Jonge, H. R. (1973). Toxicity of tetracyclines in rat-small-intestinal epithelium and liver. Biochemical Pharmacology 22, 2659–77.Google Scholar
De Vries, H. & Kroon, A. M. (1970). On effects of chloramphenicol and oxytetracycline on the biogenesis of mammalian mitochondria. Biochimica et Biophysica Acta 204, 531–41.CrossRefGoogle ScholarPubMed
Divo, A. A., Geary, T. G. & Jensen, J. B. (1985). Oxygen-time-dependent effects of antibiotics and selected mitochondrial inhibitors on Plasmodium falciparum in culture. Antimicrobial Agents and Chemotherapy 27, 21–7.Google Scholar
Dolan, T. T. (1981). Progress in the chemotherapy of theileriosis. In Advances in the Control of Theileriosis (ed. Irvin, A. D., Cunningham, M. P. & Young, A. S.), pp. 186–208. The Hague: Martinus Nijhoff.Google Scholar
Gale, E. F. & Folkes, J. P. (1953). The assimilation of amino-acids by bacteria. 15. Actions of antibiotics on nucleic acids and protein synthesis in Staphylococcus aureus. The Biochemical Journal 53, 493–8.CrossRefGoogle Scholar
Geary, T. G. & Jensen, J. B. (1983). Effects of antibiotics on Plasmodium falciparum in vitro. American Journal of Tropical Medicine and Hygiene 32, 221–5.CrossRefGoogle ScholarPubMed
Gijzel, W. P. & Kroon, A. M. (1978). On the protection of bone marrow against toxic side-effects of tetracyclines. Journal of Molecular Medicine 3, 157–65.Google Scholar
Gijzel, W. P., Strating, M. & Kroon, A. M. (1972). The biogenesis of mitochondria during proliferation and maturation of the intestinal epithelium of the rat. Effects of oxytetracycline. cell Differentiation 1, 191–8.Google Scholar
Irvin, A. D. & Morrison, W. I. (1987). Immunopathology, immunology and immunoprophylaxis of Theileria infections. In Immune Responses in Parasite Infections: Immunology, Immunopathology and Immunoprophylaxis, Vol. 3 (ed. Soulsby, E. J. L.), pp. 223–274. Florida: CRC Press.Google Scholar
Jura, W. G. Z. O., Brown, C. G. D. & Brocklesby, D. W. (1985). Metabolic energy pathways in Theileria annulata sporozoites and their significance in sporozoite-bovine lymphocyte interactions in vitro. Veterinary Parasitology 17, 193–204.CrossRefGoogle ScholarPubMed
Kiatfuengfoo, R., Suthiphongchai, T., Prapunwattana, P. & Yuthavong, Y. (1989). Mitochondria as the site of action of tetracycline on Plasmodium falciparum. Molecular and Biochemical Parasitology 34, 109–16.CrossRefGoogle ScholarPubMed
Lalor, P. A., Morrison, W. I., Goddeeris, B. M., Jack, R. M. & Black, S. J. (1986). Monoclonal antibodies identify phenotypically and functionally distinct cell types in the bovine lymphoid system. Veterinary Immunology and Immunopathology 13, 121–40.CrossRefGoogle ScholarPubMed
Mchardy, N., Hudson, A. T. & Rae, D. G. (1980). Therapy of Theileria parva: correlation of results in culture and in cattle. In The in Vitro Cultivation of the Pathogens of Tropical Diseases (ed. Ilrad, ), pp. 149–152. Basel: Schwabe and Co.Google Scholar
Mchardy, N. & Wekesa, L. S. (1985). Buparvaquone (BW 720C): a new anti-theilerial naphthoquinone: its role in the therapy and prophylaxis of theileriosis. In Immunization against Theileriosis in Africa (ed. Irvin, A. D.), p. 88. Nairobi: ILRAD.Google Scholar
Mutugi, J. J., Young, A. S., Maritim, A. C., Linyonyi, A., Mbogos, K. & Leitch, B. L. (1988). Immunization of cattle using varying infective doses of Theileria parva lawrencei sporozoites derived from an African buffalo (Syncerus caffer) and treatment with buparvaquone. Parasitology 96, 391–402.CrossRefGoogle ScholarPubMed
Neitz, W. O. (1953). Aureomycin in Theileria parva infection. Nature, London 171, 34–5.CrossRefGoogle ScholarPubMed
Neitz, W. O. (1957). Theileriosis, gonderioses and cytauxzoonoses: A review. Onderstepoort Journal of Veterinary Research 27, 275–430.Google Scholar
Prapunwattana, P., O'sullivan, W. J. & Yuthavong, Y. (1988). Depression of Plasmodium falciparum dihydroorotate dehydrogenase activity in in vitro culture by tetracycline. Molecular and Biochemical Parasitology 27, 119–24.Google Scholar
Purnell, R. E. (1977). East Coast fever: some recent research in East Africa. Advances in Parasitology 15, 83–132.Google Scholar
Radley, D. E. (1981). Infection and treatment method of immunization against theileriosis. In Advances in the Control of Theileriosis (ed. Irvin, A. D., Cunningham, M. P. & Young, A. S.) pp. 227–237. The Hague: Martinus Nijhoff.Google Scholar
Schatz, G. & Mason, T. L. (1974). The biosynthesis of mitochondrial proteins. Current Review of Biochemistry 43, 51–87.CrossRefGoogle Scholar
Schein, E. & Voigt, W. P. (1979). Chemotherapy of bovine theileriosis with halofuginone. Acta Tropica 36, 391–4.Google ScholarPubMed
Spooner, P. R. (1987). Oxytetracycline and Theileria parva: the effects of the drug and its mechanisms of action with respect to the ‘infection and treatment’ method of immunizing cattle against East Coast fever. Ph.D. thesis, Brunel University, Uxbridge, U.K.Google Scholar
Spooner, P. R. (1990). The effects of oxytetracycline on Theileria parva in vitro. Parasitology 100, 11–17.CrossRefGoogle ScholarPubMed
Stanley, P. E. & Williams, S. G. (1969). Use of the liquid scintillation spectrometer for determining adenosine triphosphate by the luciferase enzyme. Analytical Biochemistry 29, 381–92.CrossRefGoogle ScholarPubMed
Sugimoto, C., Conrad, P. A., Ito, S., Brown, W. C. & Grab, D. J. (1988). Isolation of Theileria parva schizonts from infected lymphoblastoid cells. Acta Tropica 45, 203–16.Google ScholarPubMed
Tzagoloff, A., Macino, G. & Sebald, W. (1979). Mitochondrial genes and translation products. Annual Review of Biochemistry 48, 419–41.CrossRefGoogle ScholarPubMed
Van Den Bogert, C., Dontje, B. H. J., Wybenga, J. J. & Kroon, A. M. (1981). Arrest of in vivo proliferation of Zajdela tumor cells by inhibition of mitochondrial protein synthesis. Cancer Research 41, 1943–7.Google Scholar
Van Den Bogert, C., Lont, M., Mojert, M. & Kroon, A. M. (1983 a). Impairment of liver regeneration during inhibition of mitochondrial protein synthesis by oxytetracycline. Biochemica et Biophysica Acta 722, 393–400.Google Scholar
van den Bogert, C., Dontje, B. H. J. & Kroon, A. M. (1983 b). Arrest of in vivo growth of a solid Leydig cell tumor by prolonged inhibition of mitochondrial protein synthesis. Cancer Research 43, 2247–51.Google Scholar
Van Den Bogert, C. & Kroon, A. M. (1981 a). Tissue distribution and effects on mitochondrial protein synthesis of tetracyclines after prolonged continuous intravenous administration to rats. Biochemical Pharmacology 30, 1706–9.CrossRefGoogle ScholarPubMed
Van Den Bogert, C. & Kroon, A. M. (1981 b). Fluorometric determination of tetracyclines in small blood and tissue samples. Journal of Pharmaceutical Sciences 70, 186–9.CrossRefGoogle ScholarPubMed
Weber, G. (1980). Ultrastructural demonstration of succinic dehydrogenase and cytochrome oxidase activity in sporozoites of Babesia ovis and Theileria annulata (Apicomplexa: Piroplasmea) in salivary glands of tick vectors (Rhipicephalus bursa, Hyalomma anatolicum excavatum). Journal of Parasitology 66, 904–13.CrossRefGoogle ScholarPubMed
Weiss, H., Sebald, W. & Bucher, T. (1971). Cycloheximide resistant incorporation of amino acids into polypeptides of the cytochrome oxidase of Neurospora crassa. European Journal of Biochemistry 22, 19–26.Google Scholar
Winer, B. J. (1971). Statistical Principles in Experimental Design 2nd edn pp. 518–530. Princeton: McGraw Hill.Google Scholar