Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-16T07:28:05.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular and biochemical characterization of a sand fly population from Sri Lanka: evidence for insecticide resistance due to altered esterases and insensitive acetylcholinesterase

Published online by Cambridge University Press:  09 March 2007

S.N. Surendran ,
S.H.P.P. Karunaratne ,
Z. Adamsn ,
J. Hemingway  and
N.J. Hawkes
S.N. Surendran
Affiliation:
Department of Zoology, University of Jaffna, Jaffna, Sri Lanka
S.H.P.P. Karunaratne
Affiliation:
Department of Zoology, University of Peradeniya, Peradeniya, Sri Lanka
Z. Adamsn
Affiliation:
Entomology Department, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
J. Hemingway
Affiliation:
Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK
N.J. Hawkes*
Affiliation:
Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK
*
*Fax: 44 151 705 3369 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

With an increasing incidence of cutaneous leishmaniasis in Sri Lanka, particularly in northern provinces, insecticide-mediated vector control is under consideration. Optimizing such a strategy requires the characterization of sand fly populations in target areas with regard to species composition and extant resistance, among other parameters. Sand flies were collected by human bait and cattle-baited net traps on Delft Island, used as an illegal transit location by many refugees returning to the north of Sri Lanka from southern India where leishmaniasis is endemic. For species identification, genomic DNA was extracted and a fragment of the ribosomal 18S gene amplified. The sequence from all flies analysed matched that of Phlebotomus argentipes Annandale & Brunetti, the primary vector in India and the most likely vector in Sri Lanka. Independent morphological analysis also identified P. argentipes. To establish the current susceptibility status of vector species, data were obtained at the biochemical level, from which potential cross-resistance to alternative insecticides can be predicted. The Delft Island collection was assayed for the activities of four enzyme systems involved in insecticide resistance (acetylcholinesterase, non-specific carboxylesterases, glutathione-S-transferases and cytochrome p450 monooxygenases), establishing baselines against which subsequent collections can be evaluated. There was preliminary evidence for elevated esterases and altered acetylcholinesterase in this population, the first report of these resistance mechanisms in sand flies to our knowledge, which probably arose from the malathion-based spraying regimes of the Anti-Malarial Campaign.

Keywords

Sri LankaPhlebotomus argentipesribosomal 18S geneinsecticide resistancebiochemical assaysacetylcholinesterasecarboxylesterase
Type
Research Article
Information
Bulletin of Entomological Research , Volume 95 , Issue 4 , July 2005 , pp. 371 - 380
Copyright
Copyright © Cambridge University Press 2005

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

Alexander, B. & Maroli, M. (2003) Control of phlebotomine sandflies. Medical and Veterinary Entomology 17, 1–18.CrossRefGoogle ScholarPubMed
Aransay, A.M., Scoulica, E., Chaniotis, B. & Tselentis, Y. (1999) Typing of sandflies from Greece and Cyprus by DNA polymorphism of 18S rRNA gene. Insect Molecular Biology 8, 179–184.Google ScholarPubMed
Aransay, A.M., Scoulica, E., Tselentis, Y., Ready, P.D. (2000) Phylogenetic relationships of phlebotomine sandflies inferred from small subunit nuclear ribosomal DNA. Insect Molecular Biology 9, 157–168.CrossRefGoogle ScholarPubMed
Athukorale, D.N., Seneviratne, J.K.K., Ihalamulla, R.L., Premaratne, U.N. (1992) Locally acquired cutaneous leishmaniasis in Sri Lanka. Journal of Tropical Medicine and Hygiene 95, 432–433.Google ScholarPubMed
Berge, J.-B., Feyereisen, R. & Amichot, M. (1998) Cytochrome p450 monooxygenases and insecticide resistance in insects. Philosophical Transactions of the Royal Society of London Series B 353, 1701–1705.CrossRefGoogle ScholarPubMed
Brogdon, W.G., McAllister, J.C., Vulule, J.M. (1997) Haem peroxidase activity measured in single mosquitoes identifies individual expression of elevated oxidases for insecticide resistance. Journal of the American Mosquito Control Association 13, 233Google ScholarPubMed
Campbell, P.M., Trott, J.F., Claudianos, C., Smyth, K.-A., Russell, R.J., Oakeshott, J.G. (1997) Biochemistry of esterases associated with organophosphate resistance in Lucilia cuprina with comparisons to putative orthologues in other Diptera. Biochemical Genetics 35, 17–40.CrossRefGoogle ScholarPubMed
Carter, H.F. & Antonipulle, P. (1949) Observation on sandflies (Phlebotomus) in Delft Island, North Ceylon. Annals of Tropical Medicine and Parasitology 43, 62–73.CrossRefGoogle ScholarPubMed
Devonshire, A.L., Moores, G.D. (1982) A carboxylesterase with broad substrate specificity causes organophosphorus, carbamate and pyrethroid resistance in peach–potato aphids (Myzus persicae). Pesticide Biochemistry and Physiology 18, 235–246.CrossRefGoogle Scholar
El-Sayed, S., Hemingway, J., Lane, R.P. (1989) Susceptibility baselines for DDT metabolism and related enzyme systems in the sandfly Phlebotomus papatasi (Scopoli) (Diptera: Psychodidae). Bulletin of Entomological Research 79, 679–684.CrossRefGoogle Scholar
ffrench-Constant, R.H., Pittendrigh, B., Vaughan, A. & Anthony, N. (1998) Why are there so few resistance-associated mutations in insecticide target genes. Philosophical Transactions of the Royal Society of London (B) 353, 1685–1693.CrossRefGoogle ScholarPubMed
Field, L.M., Devonshire, A.L., Forde, B.G. (1988) Molecular evidence that insecticide resistance in peach–potato aphids (Myzus persiacae Sulz.) results from an amplification of an esterase gene. Biochemical Journal 251, 309–315.CrossRefGoogle ScholarPubMed
Fournier, D. & Mutero, A. (1994) Modification of acetylcholinesterase as a mechanism of resistance to insecticides. Comparative Biochemistry and Physiology 108, 19–31.Google 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, 421–433.CrossRefGoogle Scholar
Hemingway, J. (1998) Techniques to detect insecticide resistance mechanisms (field and laboratory manual). Document WHO/CDS/CPC/MAL/98.6 GenevaGoogle Scholar
Hemingway, J., Karunaratne, S.H.P.P. (1998) Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Medical and Veterinary Entomology 12, 1–12.CrossRefGoogle ScholarPubMed
Hemingway, J., Miyamoto, J., Herath, P.R.J. (1991) A possible novel link between organophosphorus and DDT insecticide resistance genes in Anopheles: supporting evidence from fenitrothion metabolism studies. Pesticide Biochemistry and Physiology 39, 49–56.CrossRefGoogle Scholar
Hemingway, J., Miller, J., Mumcuoglu, K.Y. (1999) Pyrethroid resistance mechanisms in the head louse Pediculus capitis from Israel; implications for control. Medical and Veterinary Entomology 13, 89–96.CrossRefGoogle ScholarPubMed
Hemingway, J., Hawkes, N.J., McCarroll, L. & Ranson, H. (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology 34, 653–665.CrossRefGoogle ScholarPubMed
Hughes, P.B., Raftos, D.A. (1985) Genetics of an esterase associated with resistance to organophosphorus insecticides in the sheep blowfly, Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae). Bulletin of Entomological Research 75, 535–544.CrossRefGoogle Scholar
Karunaratne, S.H. (1999) Insecticide cross-resistance spectra and underlying resistance mechanisms of Sri Lankan anopheline vectors of malaria. Southeast Asian Journal of Tropical Medicine and Public Health 30, 460–469.Google ScholarPubMed
Karunaratne, S.H.P.P. & Hemingway, J. (1996) Different insecticides select multiple carboxylesterase isoenzymes and different resistance levels from a single population of Culex quinquefasciatus. Pesticide Biochemistry and Physiology 54, 4–11.CrossRefGoogle Scholar
Karunaratne, S.H.P.P. & Hemingway, J. (2000) Insecticide resistance spectra and resistance mechanisms in populations of Japanese encephalitis vector mosquitoes, Culex tritaeniorhynchus and Cx. gelidus, in Sri Lanka. Medical and Veterinary Entomology 14, 430–436.CrossRefGoogle ScholarPubMed
Karunaratne, S.H.P.P. & Hemingway, J. (2001) Malathion resistance and prevalence of the malathion carboxylesterase mechanism in populations of mosquito vectors of disease in Sri Lanka. Bulletin of the World Health Organization 79, 1060–1064.Google ScholarPubMed
Karunaratne, S.H.P.P., Hemingway, J., Jayawardena, K.G.I., Dassanayaka, V. & Vaughan, A. (1995) Kinetic and molecular differences in the amplified and non-amplified esterases from insecticide resistant and susceptible Culex quinquefasciatus mosquitoes. Journal of Biological Chemistry 270, 31124–31128.CrossRefGoogle ScholarPubMed
Karunaweera, N.D., Pratlong, F., Siriwardena, H.V.Y.D., Ihalamulla, R.L., Dedet, J.P. (2003) Sri Lankan cutaneous leishmaniasis is caused by Leishmania donovani zymodeme MON-37. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 380–381.CrossRefGoogle ScholarPubMed
Lane, R.P., Pile, M.M., Amerasinghe, F.P. (1990) Anthropophagy and aggregation behaviour of the sandfly Phlebotomus argentipes in Sri Lanka. Medical and Veterinary Entomology 4, 79–88.CrossRefGoogle ScholarPubMed
Léger, N. & Pesson, B. (1993) Première mention de phlébotomes en Nouvelle-Calédonie et description de deux espèces nouvelles (Diptera Psychodidae Pblebotominae). Mémoires du Muséum National d'Histoire Naturelle A 157, 123–129.Google Scholar
Lewis, D.J. (1978) The phlebotomine sandflies (Diptera: Psychodidae) of the Oriental Region. Bulletin of the British Museum (Natural History) (Entomology) 37, 217–343.Google Scholar
Lewis, D.J., Killick-Kendrick, R. (1973) Some phlebotomid sand-flies and other Diptera of Malaysia and Sri Lanka. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 4–5.CrossRefGoogle ScholarPubMed
Nabeshima, T., Kozaki, T., Tomita, T. & Kono, Y. (2003) An amino acid substitution on the second acetylcholinesterase in the pirimicarb-resistant strains of the peach–potato aphid, Myzus persicae, Biochemical and Biophysical Research Communications 307, 15–22.CrossRefGoogle Scholar
Nabeshima, T., Mori, A., Kozaki, T., Iwata, Y., Hidoh, O., Harada, S., Kasai, S., Severson, D.W., Kono, Y. & Tomita, T. (2004) An amino acid substitution attributable to insecticide-insensitivity of acetylcholinesterase in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochemical and Biophysical Research Communications 313, 794–801.CrossRefGoogle Scholar
Naotunne, T. de S., Rajakulendran, S., Abeywickreme, W., Kulasiri, C.D., Perera, J., Premaratne, U.N., Attygalle, D., Mendis, K.N. (1990) Cutaneous leishmaniasis in Sri Lanka. An imported disease linked to the Middle East and African employment boom. Tropical and Geographical Medicine 42, 72–74.Google Scholar
Penilla, R.P., Rodriguez, A.D., Hemingway, J., Estrada, J.L.T., Jimenez, J.I.A., Rodriguez, M.H. (1996) Rotational and mosaic strategies for delaying the development of insecticide resistance in mosquitoes – baseline data for a large scale field trial in Southern Mexico. pp. 401–411in Wildey, K.B.Robinson, W.H.. (Eds) Proceedings of the 2nd International Conference on Insect Pests in the Urban Environment. BPCC Wheatons Ltd.Google Scholar
Perrotey, S., Benabdennbi, I., Haddad, N., Pesson, B. & Leger, N. (2000) Electrophoretic and morphological differentiation between two sympatric species of Adlerius: Phlebotomus brevis and Phlebotomus simici (Diptera: Psychodidae). Journal of Medical Entomology 37, 289–294.CrossRefGoogle ScholarPubMed
Prapanthadara, L., Hemingway, J., Ketterman, A.J. (1995) DDT-resistance in Anopheles gambiae Giles from Zanzibar Tanzania, based on increased DDT-dehydrochlorinase activity of glutathione S-transferases. Bulletin of Entomological Research 85, 267–274.CrossRefGoogle Scholar
Rozen, S., Skaletsky, H.J. (2000) Primer3 on the WWW for general users and for biologist programmers. pp. 365–386 in Krawetz, S.Misener, S. Bioinformatics methods and protocols: methods in molecular biology. Totowa, New Jersey, Humana Press.Google ScholarPubMed
Russell, R.J., Claudianos, C., Campbell, P.M., Horne, I., Sutherland, T.D., Oakeshott, J.G. (2004) Two major classes of target site insensitivity mutations confer resistance to organophosphate and carbamate insecticides. Pesticide Biochemistry and Physiology 79, 84–93.CrossRefGoogle Scholar
Siriwardena, H.V.Y.D., Udagedara, C.U., Karunaweera, N.D. (2003) Clinical features, risk factors and efficacy of cryotherapy in cutaneous leishmaniasis in Sri Lanka. Ceylon Medical Journal 48, 10–12.CrossRefGoogle ScholarPubMed
Valles, S.M., Strong, C.A. (2001) A microsomal esterase involved in cypermethrin resistance in the German cockroach, Blattella germanica. Pesticide Biochemistry and Physiology 71, 56–67.CrossRefGoogle Scholar
Vontas, J.G., Cosmidis, N., Loukas, M., Tsakas, S., Hejazi, M.J., Ayoutanti, A. & Hemingway, J. (2001) Altered acetylcholinesterase confers organophosphate resistance in the olive fruit fly Bactrocera oleae. Pesticide Biochemistry and Physiology 71, 124–132.CrossRefGoogle Scholar
Weill, M., Fort, P., Berthomieu, A., Dubois, M.P., Pasteur, N. & Raymond, M. (2002) A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene in Drosophila. Proceedings of the Royal Society of London Series B 269, 2007–2016.CrossRefGoogle Scholar
Weill, M., Lutfalla, G., Mogensen, K., Chandre, F., Berthomieu, A., Berticat, C., Pasteur, N., Philips, A., Fort, P. & Raymond, M. (2003) Insecticide resistance in mosquito vectors. Nature 423, 136–137.CrossRefGoogle ScholarPubMed
Ziegler, R., Whyard, S., Downe, A.E.R., Wyatt, G.R., Walker, V.K. (1987) General esterase, malathion carboxylesterase and malathion resistance in Culex tarsalis. Pesticide Biochemistry and Physiology 28, 279–285.CrossRefGoogle Scholar