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Antioxidants promote establishment of trypanosome infections in tsetse

Published online by Cambridge University Press:  19 February 2007

E. T. MacLEOD ,
I. MAUDLIN ,
A. C. DARBY  and
S. C. WELBURN
E. T. MacLEOD
Affiliation:
Centre for Infectious Diseases, College of Medicine and Veterinary Medicine, The University of Edinburgh, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, UK
I. MAUDLIN
Affiliation:
Centre for Infectious Diseases, College of Medicine and Veterinary Medicine, The University of Edinburgh, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, UK
A. C. DARBY
Affiliation:
Centre for Infectious Diseases, College of Medicine and Veterinary Medicine, The University of Edinburgh, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, UK
S. C. WELBURN*
Affiliation:
Centre for Infectious Diseases, College of Medicine and Veterinary Medicine, The University of Edinburgh, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, UK
*
*Corresponding author. Tel: +44 131 650 6228. Fax: +44 131 650 7348. E-mail: sue.welburn@ed.ac.uk
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Summary

Efficient, cyclical transmission of trypanosomes through tsetse flies is central to maintenance of human sleeping sickness and nagana across sub-Saharan Africa. Infection rates in tsetse are normally very low as most parasites ingested with the fly bloodmeal die in the fly gut, displaying the characteristics of apoptotic cells. Here we show that a range of antioxidants (glutathione, cysteine, N-acetyl-cysteine, ascorbic acid and uric acid), when added to the insect bloodmeal, can dramatically inhibit cell death of Trypanosoma brucei brucei in tsetse. Both L- and D-cysteine invoked similar effects suggesting that inhibition of trypanosome death is not dependent on protein synthesis. The present work suggests that antioxidants reduce the midgut environment protecting trypanosomes from cell death induced by reactive oxygen species.

Keywords

Trypanosoma brucei bruceitrypanosomiasistsetseantioxidantapoptosis
Type
Research Article
Information
Parasitology , Volume 134 , Issue 6 , June 2007 , pp. 827 - 831
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Ameisen, J. C. (2002). On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death and Differentiation 9, 367–393.CrossRefGoogle ScholarPubMed
Ascenzi, P. and Gradoni, L. (2002). Nitric oxide limits parasite development in vectors and in invertebrate intermediate hosts. IUBMB Life 53, 121–123.Google ScholarPubMed
Buyukguzel, K., Tunaz, H., Putnam, S. M. and Stanley, D. (2002). Prostaglandin biosynthesis by midgut tissue isolated from the tobacco hornworm, Manduca sexta. Insect Biochemistry and Molecular Biology 32 435–443.CrossRefGoogle ScholarPubMed
Clark, D., Albrecht, M. and Arevalo, J. (1994). Ascorbate variations and dehydroascorbate reductase activity in Trypanosoma cruzi epimastigotes and trypomastigotes. Molecular and Biochemical Parasitology 66, 143–145.CrossRefGoogle ScholarPubMed
Chose, O., Sarde, C. O., Gerbod, D., Viscogliosi, E. and Roseto, A. (2003). Programmed cell death in parasitic protozoans that lack mitochondria. Trends in Parasitology 19, 559–564.CrossRefGoogle ScholarPubMed
Curtin, J. F., Donovan, M. and Cotter, T. G. (2002). Regulation and measurement of oxidative stress in apoptosis. Journal of Immunological Methods 265, 49–72.CrossRefGoogle ScholarPubMed
Das, M., Mukherjee, S. B. and Shaha, C. (2001). Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. Journal of Cell Science 114, 2461–2469.CrossRefGoogle ScholarPubMed
De Koning, H. and Diallinas, G. (2000). Nucleobase transporters (review). Molecular Membrane Biology 17, 75–94.Google ScholarPubMed
Debrabant, A., Lee, N., Bertholet, S., Duncan, R. and Nakhasi, H. L. (2003). Programmed cell death in trypanosomatids and other unicellular organisms. International Journal for Parasitology 33, 257–267.CrossRefGoogle ScholarPubMed
Duszenko, M., Muhlstadt, K. and Broder, A. (1992). Cysteine is an essential growth factor for Trypanosoma brucei bloodstream forms. Molecular and Biochemical Parasitology 50, 269–273.CrossRefGoogle ScholarPubMed
Duszenko, M., Figarella, K., Macleod, E. T. and Welburn, S. C. (2006). Death of a trypanosome: a selfish altruism. Trends in Parasitology 22, 536–542.CrossRefGoogle ScholarPubMed
Fairlamb, A. H., Blackburn, P. and Ulrich, P., Chait, B. T. and Cerami, A. (1985). Trypanothione: a novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids. Science 337, 1485–1487.CrossRefGoogle Scholar
Figarella, K., Uzcategui, N. L., Beck, A., Schoenfeld, C., Kubata, B. K., Lang, F. and Duszenko, M. (2006). Prostaglandin-induced programmed cell death in Trypanosoma brucei involves oxidative stress. Cell Death and Differentiation 13, 1802–1814.CrossRefGoogle ScholarPubMed
Hilliker, A. J., Duyf, B., Evans, D. and Phillips, J. P. (1992). Urate-null rosy mutants of Drosophila melanogaster are hypersensitive to oxygen stress. Proceedings of the National Academy of Sciences,USA 89, 4343–4347.CrossRefGoogle ScholarPubMed
Hoffmann, J. A. and Reichhart, J. M. (2002). Drosophila innate immunity: an evolutionary perspective. Nature Immunology 3, 121–126.CrossRefGoogle ScholarPubMed
Hurd, H. and Carter, V. (2004). The role of programmed cell death in Plasmodium-mosquito interactions. International Journal for Parasitology 34, 1459–1472.CrossRefGoogle ScholarPubMed
Kumar, S., Christophides, G. K., Cantera, R., Charles, B., Han, Y. S., Meister, S., Dimopoulos, G., Kafatos, F. C. and Barillas-Mury, C. (2003). The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proceedings of the National Academy of Sciences, USA 100, 14139–14144.CrossRefGoogle ScholarPubMed
Kwon, Y. W., Masutani, H., Nakamura, H., Ishii, Y. and Yodoi, J. (2003). Redox regulation of cell growth and cell death. Biological Chemistry 384, 991–996.CrossRefGoogle ScholarPubMed
Laragione, T., Bonetto, V., Casoni, F., Massignan, T., Bianchi, G., Gianazza, E. and Ghezzi, P. (2003). Redox regulation of surface protein thiols: identification of integrin alpha-4 as a molecular target by using redox proteomics. Proceedings of the National Academy of Sciences, USA 100, 14737–14741.CrossRefGoogle ScholarPubMed
Luckhart, S., Vodovotz, Y., Cui, L. and Rosenberg, R. (1998). The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proceedings of the National Academy of Sciences, USA 95, 5700–5705.CrossRefGoogle ScholarPubMed
Massie, H. R., Shumway, M. E., Whitney, S. J., Sternick, S. M. and Aiello, V. R. (1991). Ascorbic acid in Drosophila and changes during aging. Experimental Gerontology 26, 487–494.CrossRefGoogle ScholarPubMed
Maudlin, I. and Welburn, S. C. (1987). Lectin mediated establishment of midgut infections of Trypanosoma congolense and Trypanosoma brucei in Glossina morsitans. Tropical Medicine and Parasitology 38, 167–170.Google ScholarPubMed
Moloo, S. K. (1978). Excretion of uric acid and amino acids during diuresis in the adult female Glossina morsitans. Acta Tropica 35, 247–252.Google ScholarPubMed
Munks, R. J., Sant'Anna, M. R., Grail, W., Gibson, W., Igglesden, T., Yoshiyama, M., Lehane, S. M. and Lehane, M. J. (2005). Antioxidant gene expression in the blood-feeding fly Glossina morsitans morsitans. Insect Molecular Biology 14, 483–491.CrossRefGoogle ScholarPubMed
Ridgley, E. L., Xiong, Z. H. and Ruben, L. (1999). Reactive oxygen species activate a Ca2+-dependent cell death pathway in the unicellular organism Trypanosoma brucei brucei. The Biochemical Journal 340, 33–40.CrossRefGoogle ScholarPubMed
Souza, A. V., Petretski, J. H., Demasi, M., Bechara, E. J. and Oliveira, P. L. (1997). Urate protects a blood-sucking insect against hemin-induced oxidative stress. Free Radical Biology and Medicine 22, 209–214.CrossRefGoogle ScholarPubMed
Wang, J., Van Praagh, A., Hamilton, E., Wang, Q., Zou, B., Muranjan, M., Murphy, N. B. and Black, S. J. (2002). Serum xanthine oxidase: origin, regulation, and contribution to control of trypanosome parasitemia. Antioxidants and Redox Signalling 4, 161–178.CrossRefGoogle ScholarPubMed
Welburn, S. C., Maudlin, I. and Ellis, D. S. (1989). Rate of trypanosome killing by lectins in midguts of different species and strains of Glossina. Medical and Veterinary Entomology 3, 77–82.CrossRefGoogle ScholarPubMed
Wilkinson, S. R., Prathalingam, S. R., Taylor, M. C., Horn, D. and Kelly, J. M. (2005). Vitamin C biosynthesis in trypanosomes: a role for the glycosome. Proceedings of the National Academy of Sciences, USA 102, 11645–11650.CrossRefGoogle ScholarPubMed
Xing, R., Liu, S., Guo, Z., Yu, H., Li, C., Ji, X., Feng, J. and Li, P. (2005). The antioxidant activity of glucosamine hydrochloride in vitro. Bioorganic and Medicinal Chemistry 14, 1706–1709.CrossRefGoogle ScholarPubMed
Zangger, H., Mottram, J. C. and Fasel, N. (2002). Cell death in Leishmania induced by stress and differentiation: programmed cell death or necrosis? Cell Death and Differentiation 9, 1126–1139.CrossRefGoogle ScholarPubMed