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Role of reactive oxygen species in expulsion of Nippostrongylus brasiliensis from rats

Published online by Cambridge University Press:  06 April 2009

S. Batra
Affiliation:
Divisions of Biochemistry, Central Drug Research Institute, Lucknow-226001, India
J. K. Srivastrava
Affiliation:
Divisions of Parasitology, Central Drug Research Institute, Lucknow-226001, India
S. Gupta
Affiliation:
Divisions of Parasitology, Central Drug Research Institute, Lucknow-226001, India
J. C. Katiyar
Affiliation:
Divisions of Parasitology, Central Drug Research Institute, Lucknow-226001, India
V. M. L. Srivastava*
Affiliation:
Divisions of Biochemistry, Central Drug Research Institute, Lucknow-226001, India
*
*Reprint requests to Dr V. M. L. Srivastava, Division of Biochemistry, Central Drug Research Institute, Lucknow-226001, India.

Summary

To understand the mechanism for the expulsion of Nippostrongylus brasiliensis from rats, age-dependent variations in the metabolism of reactive oxygen species in the parasite and the host intestines were examined. N. brasiliensis showed an age-dependent increase in its susceptibility to xanthine-xanthine oxidase and t−butyl hydroperoxide generated oxidants as well as to H2O2. Protection obtained with several scavengers suggested that the worms were damaged by the combined action of oxidants generated by the in vitro systems employed. The level of superoxide dismutase in the nematode and its release into the surroundings exhibited a marked depression with advancement of age. No such alteration was, however, recorded for catalase and glutathione peroxidase. An appreciable decrease in the level of reduced glutathione in older N. brasiliensis appears to render them prone to oxidant attack. The rat intestines, on the other hand, exhibited an appreciable depression in catalase and a reduced glutathione content with progress of the infection. Vitamin E levels were elevated. The release of O27 and H2O2 by the intestines was also found to be greater during later stages of the infection. The combined effect of the changes observed in N. brasiliensis and in the rat intestines may be at least partly responsible for expulsion of the nematode from the rats after day 10.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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References

REFERENCES

Aebi, H. (1984). Catalase in vitro. In Methods in Enzymology 105 (ed. Packer, L.), pp. 121–6. New York: Academic Press.Google Scholar
Babior, B. M. (1973). The respiratory burst oxidase. Trends in Biological Sciences 12, 241–3.CrossRefGoogle Scholar
Bass, D. A. & Szejda, P. (1979). Mechanisms of killing of newborn larvae of Trichinella spiralis by neutrophils and eosinophils. Journal of Clinical Investigation 64, 1558–64.CrossRefGoogle ScholarPubMed
Batra, S., Singh, S. P., Srivastava, V. M. L. & Chatterjee, R. K. (1989). Xanthine oxidase, superoxide dismutase, catalase and lipid peroxidation in Mastomys natalensis: effect of Dipetalonema viteae infection. Indian Journal of Experimental Biology 27, 1067–70.Google ScholarPubMed
Batra, S., Singh, S. P., Gupta, S., Katiyar, J. C. & Srivastava, V. M. L. (1990 a). Reactive oxygen intermediates metabolizing enzymes in Ancylostoma ceylanicum and Nippostrongylus brasiliensis. Free Radical Biology and Medicine 8, 271–4.CrossRefGoogle ScholarPubMed
Batra, S., Chatterjee, R. K. & Srivastava, V. M. L. (1990 b). Antioxidant enzymes in Acanthocheilonema vitaea and effect of antifilarial agents. Biochemical Pharmacology 40, 2363–9.CrossRefGoogle ScholarPubMed
Beauchamp, C. & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276–87.CrossRefGoogle Scholar
Befus, D. (1986). Immunity in intestinal helminth infections: present concepts and future directions. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 735–41.CrossRefGoogle Scholar
Beutler, E., Duron, O. & Kelly, B. M. (1963). Improved method for determination of blood glutathione. Journal of Laboratory and Clinical Medicine 61, 882–8.Google ScholarPubMed
Callahan, H. L., Crouch, R. K. & James, E. R. (1988). Helminth anti-oxidant enzymes: a protective mechanism against host oxidants. Parasitology Today 4, 218–26.CrossRefGoogle ScholarPubMed
Desai, I. D. (1984). Vitamin E analysis methods for animal tissues. In Methods in Enzymology 105 (ed. Packer, L.), pp. 138–47. New York: Academic Press.Google Scholar
Docampo, R. (1990). Sensitivity of parasites to free radical damage by antiparasitic drugs. Chemico-Biological Interactions 73, 127.CrossRefGoogle ScholarPubMed
Jain, M. K., Batra, S., Gupta, S., Katiyar, J. C. & Srivastava, V. M. L. (1989). Impact of Cysticercus fasciolaris infection on reactive oxygen intermediate metabolizing system in rat. Medical Science Research 17, 1051–3.Google Scholar
Kazura, J. W. & Meshnick, S. R. (1984). Scavenger enzymes and resistance to oxygen mediated damage to Trichinella spiralis. Molecular and Biochemical Parasitology 10, 110.CrossRefGoogle ScholarPubMed
Khan, S. H., Emerit, I. & Feingold, J. (1990). Superoxide and hydrogen peroxide production by macrophages of New Zealand black mice. Free Radical Biology and Medicine 8, 339–45.CrossRefGoogle ScholarPubMed
Klebanoff, S. J. (1975). Antimicrobial mechanisms in neutrophilic polymorphonuclear leukocytes. Seminars in Hematology 12, 117–42.Google ScholarPubMed
Leopold, F. & Wolfgang, A. G. (1984). Assays of glutathione peroxidase. In Methods in Enzymology 105 (ed. Packer, L.), pp. 114–21. New York: Academic Press.Google Scholar
Lowry, O. H., Rosenbrough, N. J., Farr, A. L. & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265&75.CrossRefGoogle ScholarPubMed
Misra, H. P.Fridovich, I. (1972). The univalent reduction of oxygen by reduced flavins and quinones. Journal of Biological Chemistry 247, 188–92.CrossRefGoogle ScholarPubMed
Nathan, C. A. (1983). Mechanisms of macrophage antimicrobial activity. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 620–30.CrossRefGoogle ScholarPubMed
Nathan, C. A., Nogueira, N., Juang Hasuch, C, Ellis, J. & Cohn, Z. A. (1979). Activation of macrophages in vitro and in vivo. Correlation between hydrogen peroxide release and killing of Trypanosoma cruzi. Journal of Experimental Medicine 140, 1056–68.CrossRefGoogle Scholar
Nishikimi, M., Rao, A. N. & Yagi, K. (1972). The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochemical and Biophysical Research Communications 46, 849–54.CrossRefGoogle ScholarPubMed
Ogilvie, B. M. & Jones, V. E. (1971). Nippostrongylus brasiliensis: a review of immunity and host–parasite relationship in rat. Experimental Parasitology 29, 138–77.CrossRefGoogle Scholar
Ogilvie, B. M., Mackenzie, C. D. & Love, R. J.(1977) Lymphocytes and eosinophils in the immune response of the rat to initial and subsequent infections with Nippostrongylus brasiliensis. American Journal of Tropical Medicine and Hygiene 26 (Suppl.), 61–7.CrossRefGoogle ScholarPubMed
Ovington, K. S. (1987). Nippostrongylus brasiliensis: physiological and metabolic responses of rats to primary infection. Experimental Parasitology 63, 10–10.CrossRefGoogle ScholarPubMed
Pande, V., Katiyar, J. C. & Sen, A. B. (1977). Susceptibilities of the albino rat and Mastomys natalensis to Nippostrongylus brasiliensis infection. Indian Journal of Parasitology 1, 41–41.Google Scholar
Singh, S. P., Batra, S., Gupta, S., Katiyar, J. C. & Srivastava, V. M. L. (1989). Effect of Ancylostoma ceylanicum infection in hamsters on enzymes that metabolize reactive oxygen intermediates. Medical Science Research 17, 493–5.Google Scholar
Smith, N. C. & Bryant, C. (1986). The role of host- generated free radicals in helminth infections: Nippostrongylus brasiliensis and Nematospiroides dubius compared. International Journal for Parasitology 16, 617–22.CrossRefGoogle ScholarPubMed
Smith, N. C. & Bryant, C. (1989 a). Free radical generation during primary infections with Nippostrongylus brasiliensis. Parasite Immunology 11, 147–60.CrossRefGoogle ScholarPubMed
Smith, N. C. & Bryant, C. (1989 b). The effect of antioxidants on the rejection of Nippostrongylus brasiliensis. Parasite Immunology 11, 161–7.CrossRefGoogle ScholarPubMed
Srivastava, J. K., Batra, S., Gupta, S., Katiyar, J. C. & Srivastava, V. M. L. (1992). Effect of anthelmintics on the antioxidant system of Nippostrongylus brasiliensis. Biochemical Pharmacology 43, 289–93.CrossRefGoogle ScholarPubMed
Sun, Y. & Oberley, W. (1989). The inhibition of catalase by glutathione. Free Radical Biology and Medicine 7, 595602.CrossRefGoogle ScholarPubMed
Thurman, R. G., Ley, H. G. & Scholz, R. (1972). Hepatic microsomal ethanol oxidation: hydrogen peroxide formation and the role of catalase. European Journal of Biochemistry 25, 420–30.CrossRefGoogle ScholarPubMed