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Hydrogen peroxide is the most toxic oxygen species for Onchocerca cervicalis microfilariae

Published online by Cambridge University Press:  06 April 2009

H. L. Callahan ,
R. K. Chouch  and
E. R. James
H. L. Callahan
Affiliation:
Department of Ophthalmology, Medical University of South Carolina, Charleston, SC 29425, USA
R. K. Chouch
Affiliation:
Department of Ophthalmology, Medical University of South Carolina, Charleston, SC 29425, USA
E. R. James
Affiliation:
Department of Ophthalmology, Medical University of South Carolina, Charleston, SC 29425, USA
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Summary

The toxicity of the active oxygen species hydrogen peroxide, superoxide radical, hydroxyl radical and singlet oxygen to microfilariae (mf) has been studied in vitro, using active oxygen-generating systems and scavengers/inhibitors. Mf viability was monitored by uptake of the radiolabel, [3H]2-deoxy-D-glouse. Hydrogen peroxide and singlet oxygen, but not superoxide radical or hydroxyl radical, are toxic for mf. Hydrogen peroxide was toxic for mf within 2 h at concentrations as low as 5 ¼, an amount eosinophils have been shown to release in vitro (Weiss et al. 1986). Catalase and thiourea, but not inactivated catalase, superoxide dismutase (SOD), singlet oxygen scavengers, or hydroxyl radical scavengers, protected mf. Mf have relatively high levels of endogenous SOD but no measurable glutathione peroxidase and low levels of catalase when compared with other parasites (Callahan, Crouch & James, 1988). The low levels of hydrogen peroxide-scavenging enzymes correlate well with mf sensitivity to hydrogen peroxide and the protective effect of exogenous catalase.

Keywords

oxidantshydeogen peroxidecatalaseOnchocerca cervicalis microfilariaein vitro viability assay
Type
Research Article
Information
Parasitology , Volume 100 , Issue 3 , June 1990 , pp. 407 - 415
Copyright
Copyright © Cambridge University Press 1990

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References

REFERENCES

Baudhuin, P., Beaufay, H., Rahman-LI, Y., Sellinger, O. Z., Wattiaux, R., Jacques, P. & De Duve, C. (1964). Intracellular distribution of monoamine oxidase, aspartate aminotransferase, alanine aminotransferase, D-amino acid oxidase and catalase in rat-liver tissue. The Biochemical Journal 92, 179–84.CrossRefGoogle ScholarPubMed
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–54.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
Bezman, S. A., Burtis, P. A., Izod, T. P. J. & Thayer, M. A. (1978). Photodynamic inactivation of E. coli by Rose Bengal immobilized on polystyrene beads. Photochemistry and Photobiology 28, 325–9.CrossRefGoogle ScholarPubMed
Bianco, A. E., Ham, P., El Sinnary, K. & Nelson, G. S. (1980). Large-scale recovery of Onchocerca microfilariae from naturally infected cattle and horses. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 109–10.Google Scholar
Bishop, C. T., Mirza, Z., Crapo, J. D. & Freeman, B. A. (1985). Free radical damage to cultured porcine aortic endothelial cells and lung fibroblasts: modulation by culture conditions. In Vitro Cellular and Developmental Biology 21, 229–36.CrossRefGoogle ScholarPubMed
Callahan, H. L., Crouch, R. K. & James, E. R. (1988). Helminth anti-oxidant enzymes: a protective mechanism against host oxidants? Parasitology Today 4, 218–25.CrossRefGoogle ScholarPubMed
Callahan, H. L., Wakeman, J. M., Crouch, R. K. & James, E. R. (1989). An in vitro radiolabel uptake viability assay for Onchocerca microfilariae. Journal of Parasitology 75, 142–4.CrossRefGoogle Scholar
Connor, D. H., George, G. H. & Gibson, D. W. (1985). Pathologic changes of human onchocerciasis: implications for future research. Reviews of Infectious Diseases 7, 809–19.CrossRefGoogle ScholarPubMed
Connor, D. H., Gibson, D. W., Neafie, R. C., Merighi, B. & Buck, A. A. (1983). Sowda onchocerciasis in North Yemen: a clinicopathologic study of 18 patients. American Society of Tropical Medicine and Hygiene 32, 123–37.CrossRefGoogle ScholarPubMed
Connor, D. H., Morrison, N. E., Kerdel-Vegas, F., Berkoff, H. A., Johnson, F., Tunnicliffe, R., Failing, F. C., Hale, L. N. & Lindquist, K. (1970). Onchocerciasis. Human Pathology 1, 553–79.CrossRefGoogle ScholarPubMed
Connor, D. H., Williams, P. H., Helwig, E. B. & Winslow, D. J. (1969). Dermal changes in onchocerciasis. Archives of Pathology 87, 193–200.Google ScholarPubMed
Darr, D. & Fridovich, I. (1986). Irreversible inactivation of catalase by 3-amino-1,2,4-triazole. Biochemical Pharmacology 35, 3642.CrossRefGoogle Scholar
Docampo, R. & Moreno, S. N. J. (1984). Free-radical intermediates in the antiparasitic action of drugs and phagocytic cells. In Free Radicals in Biology (ed. Pryor, W. A.), pp. 239–271. New York: Academic Press.Google Scholar
Fridovich, I. (1978). Oxygen radicals, hydrogen peroxide, and oxygen toxicity. In Free Radicals in Biology (ed. Pryor, W. A.), pp. 239–271. New York: Academic Press.Google ScholarPubMed
Garcia, M. L., Patel, L., Padan, E. & Kaback, H. R. (1982). Mechanism of lactose transport in Escherichia coli membrane vesicles: evidence for the involvement of histidine residue(s) in the response of the lac carrier to the proton electrochemical gradient. Biochemistry 21, 5800–5CrossRefGoogle Scholar
Gibson, D. W., Connor, D. H., Brown, H. L.Fuglsang, H., Anderson, J., Duke, B. O. L. & Buck, A. A. (1976). Onchocercal dermatitis: ultrastructural studies of microfilariae and host tissues, before and after treatment with diethylcarbamazine (Hetrazan). American Journal of Tropical Medicine and Hygiene 25, 74–87.CrossRefGoogle ScholarPubMed
Girotti, A. W., Thomas, J. P. & Jordan, J. E. (1986). Xanthine oxidase-catalyzed crosslinking of cell membrane proteins. Archives of Biochemistry and Biophysics 251, 639–53.CrossRefGoogle ScholarPubMed
Gleich, G. J. & Adolphson, C. R. (1986). The eosinophilic leukocyte: structure and function. Advances in Immunology 39, 177–253.CrossRefGoogle ScholarPubMed
Greene, B. M., Gbakima, A. A., Albeiz, E. J. & Taylor, H. R. (1985). Humoral and cellular immune responses to Onchocerca volvulus infection in humans. Reviews of Infectious Diseases 7, 789–95.CrossRefGoogle ScholarPubMed
Greene, B. M., Taylor, H. R. & Aikawa, M. (1981). Cellular killing of microfilariae of Onchocerca volvulus: eosinophil and neutrophil-mediated immune serum- dependent destruction. Journal of Immunology 127, 1611–18.CrossRefGoogle ScholarPubMed
Gunzler, W. A., Kramers, H. & Flohe, L. (1974). An improved coupled test procedure for glutathione peroxidase in blood. Zeitschrift für klinische Chemie und klinische Biochemie 12, 444–8.Google ScholarPubMed
Halliwell, B. & Gutteridge, J. M. C. (1986). Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Archives of Biochemistry and Biophysics 246, 501–14.CrossRefGoogle ScholarPubMed
Ham, P. J., James, E. R. & Bianco, A. E. (1982). Separation of viable and non-viable Onchocerca microfilariae using an ion exchanger. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 758–67.CrossRefGoogle ScholarPubMed
Hayes, D. J. (1989). Inhibition of filarial glucose transport as a potential target for selective chemotherapy. Journal of Cellular Biochemistry 13 (Supplyes.), E137.Google Scholar
Hoffee, P., Lai, C. Y., Pugh, E. L. & Horecker, B. L. (1967). The function of histidine residues in rabbit muscle aldolase. Proceedings of the National Academy of Sciences, USA 57, 107–13.CrossRefGoogle ScholarPubMed
Hyslop, P. A. & Sklar, L. A. (1984). A quantitative fluorimetric assay for the determination of oxidant production by polymorphonuclear leukocytes: its use in the simultaneous fluorimetric assay of cellular activation processes. Analytical Biochemistry 141, 280–6.CrossRefGoogle ScholarPubMed
Kephart, G. M., Gleich, G. J., Connor, D. H., Gibson, D. W. & Ackerman, S. J. (1984). Deposition of eosinphil granule major basic protein onto microfilariae of Onchocerca volvulus in the skin of patients treated with diethylcarbamazine. Laboratory Investigation 50, 51–61.Google Scholar
Klebanoff, S. J., Locksley, R. M., Jong, E. C. & Rosen, H. (1983). Oxidative response of phagocytes to parasite invasion. Ciba Foundation Symposium 99, 92–112.Google ScholarPubMed
Kraljic, I. & El Moshni, S. (1978). A new method for the detection of singlet oxygen in aqueous solutions. Photochemistry and Photobiology 28, 577–81.CrossRefGoogle Scholar
Kyle, M. E., Nakae, D., Sakaida, I., Miccadei, S. & Farber, J. L. (1988). Endocytosis of superoxide dismutase is required in order for the enzyme to protect hepatocytes from the cytotoxicity of hydrogen peroxide. Journal of Biological Chemistry 263, 3784–9.CrossRefGoogle ScholarPubMed
Mackenzie, C. D., Williams, J. F., Sisley, B. M., Steward, M. W. & O'day, J. (1985). Variations in host responses and the pathogenesis of human onchocerciasis. Reviews of Infectious Diseases 7, 789–95.CrossRefGoogle ScholarPubMed
Mkoji, G. M., Smith, J. M. & Prichard, R. K. (1988). Antioxidant systems in Schistosoma mansoni: evidence for their role in protection of the adult worms against oxidant killing. International Journal for Parasitology 18, 667–73.CrossRefGoogle ScholarPubMed
Murray, H. W. (1984). Macrophage activation: enhanced oxidative and antiprotozoal activity. Contemporary Topics in Immunobiology 13, 97–115.Google ScholarPubMed
Ngu, J. L. & Blackett, K. (1976). Immunological studies in onchocerciasis in Cameroon. Tropical and Geographical Medicine 28, 111–20.Google ScholarPubMed
Padan, E., Patel, L. & Kaback, H. R. (1979). Effect of diethylpyrocarbonate on lactose/proton symport in Escherichia coli membrane vesicles. Proceedings of the National Academy of Sciences, USA 76, 6221–5.CrossRefGoogle ScholarPubMed
Perez, H. D. (1985). Polymer-bound Rose Bengal as a singlet oxygen generating system. In Handbook of Methods for Oxygen Radical Research (ed. Greenwald, R. A), pp. 111–13. Boca Raton, Florida: CRC Press.Google Scholar
Poiree, J.-C., Starita-Geribaldi, M. & Sudaka, P. (1987). Diethylpyrocarbonate inhibition of sodium—glucose cotransport in kidney brush-border membrane vesicles. Biochimica et Biophysica Acta 900, 291–4.CrossRefGoogle ScholarPubMed
Rajagopalan, K. V. (1985). Purification of bovine milk xanthine oxidase. In Handbook of Methods for Oxygen Radical Research (ed. Greenwald, R. A.), pp. 21–23. Boca Raton, Florida: CRC Press.Google Scholar
Test, S. T. & Weiss, S. J. (1984). Quantitative and temporal characterization of the extracellular H2O2 pool generated by human neutrophils. Journal of Biological Chemistry 259, 399–405.CrossRefGoogle ScholarPubMed
Weiss, S. J., Test, S. T., Eckmann, C. M., Roos, D. & Regiani, S. (1986). Brominating oxidants generated by human eosinophils. Science 234, 200–3.CrossRefGoogle ScholarPubMed
Westhead, E. W. (1965). Photooxidation with Rose Bengal of a critical histidine residue in yeast enolase. Biochemistry 4, 2139–44.CrossRefGoogle Scholar
Williams, J. F., Ghalib, H. W., Mackenzie, C. D., Elkhalifa, M. Y., Ayuya, J. M. & Kron, M. A. (1987). Cell adherence to microfilariae of Onchocerca volvulus: a comparative study. Ciba Foundation Symposium 127, 146–63.Google ScholarPubMed