Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-12-01T09:12:33.320Z Has data issue: false hasContentIssue false

DDT-resistance in Anopheles gambiae (Diptera: Culicidae) from Zanzibar, Tanzania, based on increased DDT-dehydrochlorinase activity of glutathione S-transferases

Published online by Cambridge University Press:  10 July 2009

La-aied Prapanthadara
Affiliation:
Department of Medical Parasitology, London School of Hygiene and Tropical Medicine, London, UK
Janet Hemingway*
Affiliation:
Department of Medical Parasitology, London School of Hygiene and Tropical Medicine, London, UK
Albert J. Ketterman
Affiliation:
Department of Medical Parasitology, London School of Hygiene and Tropical Medicine, London, UK
*
Professor J. Hemingway, Department of Pure & Applied Biology, University of Wales, Cardiff, P.O. Box 915, Cardiff, CFl 3TL, UK.

Abstract

DDT-resistant Anopheles gambiae Giles from Zanzibar, Tanzania, had increased levels of DDT-dehydrochlorination compared to a DDT-susceptible strain. Glutathione S-transferases (GSTs) are responsible for conversion of DDT to DDE in both the susceptible and resistant strains. Sequential column chromatography, including Q-Sepharose, S-hexylglutathione agarose, hydroxylapatite and phenyl Sepharose, allowed the partial purification of seven GSTs. All seven GSTs possessed different degrees of DDTase activity. There was an eight-fold increase in total DDTase activity in the resistant compared to the susceptible enzymes. Characterization with three substrates, 1-chloro-2,4-dinitrobenzene (CDNB), 1,2-dichloro-4-nitrobenzene (DCNB) and DDT, revealed the different substrate specificity for each isolated GST indicating different isoenzymes. GST Va possessed 60% of total DDTase activity suggesting that it contributed most to DDT-metabolism in this insect species. The DDTase activity of the GSTs in both strains of A. gambiae were found to be correlated with the GST activities toward DCNB. Preliminary studies on DDT-resistant and susceptible A. gambiae showed that both DDT-resistance and the increased levels of GST activity were stage specific which suggested that different GSTs may be involved in DDT-resistance in adults and larvae of A. gambiae.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 1995

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

Bhargava, M.M., Listowsky, I. & Arias, I.M. (1978) Ligandin: bilirubin binding and glutathione S-transferase activity are independent processes. Journal of Biological Chemistry 253, 41124115.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, 248254.CrossRefGoogle ScholarPubMed
Brealey, C.J., Crampton, P.L., Chadwick, P.R. & Rickett, F.E. (1984) Resistance mechanisms to DDT and trans-permethrin in Aedes aegypti. Pesticide Science 15, 121132.CrossRefGoogle Scholar
Brown, A.W.A. (1986) Insecticide resistance in mosquitoes: a pragmatic review. Journal of the American Mosquito Control Association 2, 123140.Google ScholarPubMed
Bruce, W.N. (1949) Latest report on fly control. Pest Control 17 (6), 7, 28.Google Scholar
Chadwick, P.R., Slatter, R. & Bowron, M.J. (1984) Cross-resistance to pyrethroids and other insecticides in Aedes aegypti. Pesticide Science 15, 112120.CrossRefGoogle Scholar
Clark, A.G. & Dauterman, W.C. (1982) The characterization by affinity chromatography of glutathione S-transferases from different strains of house fly. Pesticide Biochemistry and Physiology 17, 307314.CrossRefGoogle Scholar
Clark, A.G. & Shamaan, N.A. (1984) Evidence that DDT-dehydrochlorinase from the house fly is a glutathione S-transferase. Pesticide Biochemistry and Physiology 22, 249261.CrossRefGoogle Scholar
Clark, A.G., Shamaan, N.A., Sinclair, M.D. & Dauterman, W.C. (1986) Insecticide metabolism by multiple glutathione S-transferases in two strains of the house fly, Musca domestica (L). Pesticide Biochemistry and Physiology 25, 169175.CrossRefGoogle Scholar
Curtis, C.F. & Lines, J.D. (1987) Insecticides in the management of insect vectors of tropical disease. Insect Science and its Application 8. 709714.Google Scholar
Curtis, C.F., Lines, J.D. & Hill, N. (1983) DDT resistance in An. gambiae s.s. from Zanzibar: mosquito studies at the London School of Hygiene and Tropical Medicine. Progress Report No. 44, 1012.Google Scholar
Grant, D.F. & Matsumura, F. (1989) Glutathione S-transferase 1 and 2 in susceptible and insecticide resistant Aedes aegypti. Pesticide Biochemistry and Physiology 33, 132143.CrossRefGoogle Scholar
Grant, D.F., Dietze, E.C. & Hammock, B.D. (1991) Glutathione S-transferase isozymes in Aedes aegypti: purification, characterization, and isozyme-specific regulation. Insect Biochemistry 21, 421439.CrossRefGoogle Scholar
Habig, W.H., Pabst, M.J., Fleischner, G., Gatmaitan, Z., Arias, I.M. & Jakoby, W.B. (1974a) The identity of glutathione S-transferase B with ligandin, a major binding protein of liver. Proceedings of the National Academy of Sciences of the United States of America 71, 38793882.CrossRefGoogle Scholar
Habig, W.H., Pabst, M.J. & Jakoby, W.B. (1974b) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 71307139.CrossRefGoogle ScholarPubMed
Hayaoka, T. & Dauterman, W.C. (1982) Induction of glutathione S-transferase by phenobarbital and pesticides in various housefly strains and its effect on toxicity. Pesticide Biochemistry and Physiology 17, 113119.CrossRefGoogle Scholar
Hayaoka, T. & Dauterman, W.C. (1983) The effect of phenobarbital induction on glutathione conjugation of diazinon in susceptible and resistant houseflies. Pesticide Biochemistry and Physiology 19, 344349.CrossRefGoogle Scholar
Hazelton, G.A. & Lang, C.A. (1983) Glutathione S-transferase activities in the yellow-fever mosquito [Aedes aegypti (Louisville)] during growth and aging. Biochemical Journal 210, 281287.CrossRefGoogle Scholar
Hemingway, J., Malcolm, C.A., Kissoon, K.E., Boddington, R.B., Curtis, C.F. & Hill, N. (1985) The biochemistry of insecticide resistance in Anopheles sacharovi: comparative studies with a range of insecticide susceptible and resistant Anopheles and Culex species. Pesticide Biochemistry and Physiology 24, 6876.CrossRefGoogle Scholar
Herath, P.R.J., Jayawardena, K.G.I., Hemingway, J. & Harris, J. (1988) DDT resistance in Anopheles culicifacies Giles and A. subpictus Grassi (Diptera: Culicidae) from Sri Lanka: a field study on the mechanisms and changes in gene frequency after cessation of DDT spraying. Bulletin of Entomological Research 78, 717723.CrossRefGoogle Scholar
Jakoby, W.B. (1978) The glutathione S-transferase: a group of multifunctional detoxification proteins. Advances in Enzymology and Related Areas of Molecular Biology 46, 383414.Google ScholarPubMed
Kimura, T. & Brown, A.W.A. (1964) DDT-dehydrochlorinase in Aedes aegypti. Journal of Economic Entomology 57, 710716.CrossRefGoogle Scholar
Lines, J.D. & Nassor, N.S. (1991) DDT-resistance in Anopheles gambiae declines with mosquito age. Medical and Veterinary Entomology 5, 261265.CrossRefGoogle ScholarPubMed
McDonald, A.E. & Wood, R.J. (1979a) Mechanisms of DDT resistance in larvae of the mosquito Aedes aegypti L. Pesticide Science 10, 375382.CrossRefGoogle Scholar
McDonald, A.E. & Wood, R.J. (1979b) Mechanism of DDT resistance in larvae of the mosquito Aedes aegypti L.; the effect of DDT selection. Pesticide Science 10, 383388.CrossRefGoogle Scholar
Mannervik, B. (1985) The isozymes of glutathione transferase. Advances in Enzymology and Related Areas of Molecular Biology 57, 357417.Google ScholarPubMed
Mannervik, B. & Danielson, U.H. (1988) Glutathione transferases-structure and catalytic activity. CRC Critical Reviews in Biochemistry 23, 283337.CrossRefGoogle ScholarPubMed
Moorefield, H.H. & Kearns, C.W. (1957) Levels of DDT-dehydrochlorinase during metamorphosis of the resistant house fly. Journal of Economic Entomology 50, 1113.CrossRefGoogle Scholar
Motoyama, N. & Dauterman, W.C. (1975) Interstrain comparison of glutathione-dependent reactions in susceptible and resistant houseflies. Pesticide Biochemistry and Physiology 5, 480495.CrossRefGoogle Scholar
Ottea, J.A. & Plapp, F.W. Jr. (1984) Glutathione S-transferases in the house fly: biochemical and genetic changes associated with induction and insecticide resistance. Pesticide Biochemistry and Physiology 22, 203208.CrossRefGoogle Scholar
Pickett, C.B. & Lu, A.Y.H. (1989) Glutathione S-transferases: gene structure, regulation, and biological function. Annual Review of Biochemistry 58, 743764.CrossRefGoogle ScholarPubMed
Pimentel, D., Dewey, J.E. & Schwart, H.H. (1951) An increase in the duration of the life cycle of DDT-resistant strains of the housefly. Journal of Economic Entomology 44, 477481.CrossRefGoogle Scholar
Prapanthadara, L., Hemingway, J. & Ketterman, A.J. (1993) Partial purification and characterization of glutathione S-transferases involved in DDT resistance from the mosquito Anopheles gambiae. Pesticide Biochemistry and Physiology 47, 119133.CrossRefGoogle Scholar
Rathor, H.R. & Wood, R.J. (1981) In -vivo and in-vitro studies on DDT uptake and metabolism in susceptible and resistant strains of the mosquito Aedes aegypti L. Pesticide Science 12, 255264.CrossRefGoogle Scholar
Reiss, R.A. & James, A.A. (in press) A glutathione S-transferase gene of the vector mosquito, Anopheles gambiae. Insect Molecular Biology.Google Scholar
Tsukamoto, M. (1969) Biochemical genetics of insecticide resistance in the housefly. Residue Review 25, 289314.Google ScholarPubMed
Tu, C.-P.D., Weiss, M.J., Li, N.Q. & Reddy, C.C. (1983) Communication: tissue-specific expression of the rat glutathione S-transferases. Journal of Biological Chemistry 258, 46594662.CrossRefGoogle Scholar
Vander Jagt, D.L., Wilson, S.P., Dean, V.L. & Simons, P.C. (1982) Bilirubin binding to rat liver ligandins (glutathione S-transferases A and B). Journal of Biological Chemistry 257. 19972001.CrossRefGoogle Scholar
WHO (1981) Instructions for determining the susceptibility or resistance of mosquito larvae to insect development inhibitors. Geneva, World Health Organization (unpublished document WHO/VBC/81.212).Google Scholar
Wood, R.J. (1981) Insecticide resistance. Genes and mechanisms. pp. 5396, in Bishop, J.A. & Cook, L.M. (Eds) Genetic consequences of man made change. New York, Academic Press.Google Scholar