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The molecular basis of two contrasting metabolic mechanisms of insecticide resistance

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Abstract

The esterase-based insecticide resistance mechanisms characterised to date predominantly involve elevation of activity through gene amplification allowing increased levels of insecticide sequestration, or point mutations within the esterase structural genes which change their substrate specificity. The amplified esterases are subject to various types of gene regulation in different insect species. In contrast, elevation of glutathione S-transferase activity involves upregulation of multiple enzymes belonging to one or more glutathione S-transferase classes or more rarely upregulation of a single enzyme. There is no evidence of insecticide resistance associated with gene amplification in this enzyme class. The biochemical and molecular basis of these two metabolically-based insecticide resistance mechanisms is reviewed.

Introduction

Resistance to organochlorine, organophosphate and carbamate insecticides is conferred by a limited number of mechanisms in all insects analysed to date. These mechanisms predominantly involve either metabolic detoxification of the insecticide before it reaches its target site, or changes in sensitivity of the target site so that it is no longer susceptible to insecticide inhibition. The most common metabolic resistance mechanisms involve esterases, glutathione S-transferases or monooxygenases (the latter has been the subject of a recent review by Scott et al., 1998). In most, but not all, instances of metabolic resistance, individual resistant insects can be detected through increased quantities of enzyme compared to their susceptible counterparts (Brown and Brogdon, 1987, Hemingway, 1989, Hemingway et al., 1995). Over the last decade the molecular basis of these resistance mechanisms has gradually been elucidated, opening up the exciting possibility of manipulation of these enzyme systems in the long term to restore insecticide susceptibility by manipulation of their expression patterns. The esterase and glutathione S-transferase (GST)-based insecticide resistance mechanisms in a range of insects present a number of contrasting ways in which metabolically-based resistance has been selected for at the molecular level.

Section snippets

Esterase-based resistance

Esterase-based resistance to organophosphorus and carbamate insecticides is common in a range of different insect pests (Field et al., 1988, Hemingway and Karunaratne, 1998). The esterases either produce broad spectrum insecticide resistance through rapid-binding and slow turnover of insecticide, i.e. sequestration, or narrow spectrum resistance through metabolism of a very restricted range of insecticides containing a common ester bond (Herath et al., 1987, Karunaratne et al., 1995). The

GST-based resistance

The glutathione S-transferases (GSTs) belong to a superfamily which currently has almost 100 sequences. There are at least 25 groups (families) of GST-like proteins, with one well supported large clade containing currently recognised mammalian, arthropod, helminth, nematode and mollusc GST classes (Snyder and Maddison, 1997). GSTs can produce resistance to a range of insecticides by conjugating reduced glutathione (GSH) to the insecticide or its primary toxic metabolic products. The majority of

Conclusions

The last decade has seen large advances in our understanding of the molecular basis of insecticide resistance. The structural genes coding for the enzymes, which are elevated in a number of insect species, have been cloned and characterized. Our understanding of how these genes are regulated will form another major advance in our understanding of such systems, moving us closer to the goal of manipulating pest insect species with the aim of restoring insecticide susceptibility.

Acknowledgements

The electron micrographs reported in this review would not have been possible without the expert technical assistance of Mrs C. Winters at the Cardiff School of Biosciences.

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