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Drosophila Melanogaster As a Powerful Tool for Studying Insect Toxicology T

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Drosophila Melanogaster As a Powerful Tool for Studying Insect Toxicology T Pesticide Biochemistry and Physiology 161 (2019) 95–103 Contents lists available at ScienceDirect Pesticide Biochemistry and Physiology journal homepage: www.elsevier.com/locate/pest Opinion paper Drosophila melanogaster as a powerful tool for studying insect toxicology T ARTICLE INFO ABSTRACT Keywords: Insecticides are valuable and widely used tools for the control of pest insects. Despite the use of synthetic Insecticide toxicity insecticides for > 50 years, we continue to have a limited understanding of the genes that influence the key steps Drosophila melanogaster of the poisoning process. Major barriers for improving our understanding of insecticide toxicity have included a Pharmacokinetics narrow range of tools and/or a large number of candidate genes that could be involved in the poisoning process. Genetics Herein, we discuss the numerous tools and resources available in Drosophila melanogaster that could be brought to bear to improve our understanding of the processes determining insecticide toxicity. These include unbiased approaches such as forward genetic screens, population genetic methods and candidate gene approaches. Examples are provided to showcase how D. melanogaster has been successfully used for insecticide toxicology studies in the past, and ideas for future studies using this valuable insect are discussed. 1. Introduction better understanding of the physiological processes that are involved in the poisoning processes in insects will enable us to develop safer and Insecticides represent one of the most powerful tools humans have more effective insecticides, gain insights into ways insecticides canbe ever developed to control crop pests, structural pests and vectors of made more selective, and identify genes that have the potential to human and animal diseases. In the USA alone, yearly expenditures on confer insecticide resistance. insecticides surpass $6 billion and > 550 million pounds are used an- In this review, we propose that using the powerful genetic model nually (Meister and Sine, 2014). It is difficult, or perhaps impossible, to organism Drosophila melanogaster, will help gain pioneering insights exactly calculate the economic and health benefits associated with in- into the physiological processes that underlie insecticide poisoning in secticide use, but they are substantial. Depending on the crop and level insects. What is known about each of the five steps of the poisoning of insect pressure in a given year, insecticides can boost crop yields by process, as well as how studies with D. melanogaster could be trans- 6–79% (Ware and Whitacre, 2004). Additionally and in most countries, formative to elucidate these steps, are discussed below. We review the insecticides are the only line of defense during an outbreak of an insect numerous tools that are available in D. melanogaster which could be vectored disease. brought to bear on questions in insect toxicology. We then propose a Surprisingly, despite the wide use of insecticides, we still under- pathway by which different types of questions could be pursued. stand very little about the genes that influence the key steps which Finally, we provide select examples to illustrate how D. melanogaster determine whether an insect will succumb (or not) to an insecticide. has already been used successfully to improve our understanding of Conceptually there are five steps involved in the interaction of an insect insect toxicology, as well as some examples of where D. melanogaster with an insecticide: 1) penetration into the insect (through the cuticle may not yield the most useful information. While D. melanogaster is or the gut), 2) dissemination through the insect body, 3) metabolism used primarily because it is a model organism, it is also a pest in some (e.g. detoxification), 4) interaction with the target site, and 5) excretion situations (Sun et al., 2019). (Fig. 1). Despite decades of insecticide toxicology research, the mole- cular, cellular and physiological pathways and processes involved in 2. Current status of our understanding of insect/insecticide each step of the poisoning process that ultimately culminate into the interactions survival or death of an treated insect are not well understood. Ad- ditionally, the physiological processes underlying the variation in sen- The first step of insecticide poisoning is penetration across thecu- sitivity to insecticides between individuals in naïve populations (i.e. ticle or gut (except for insecticides that directly target the cuticle (e.g. populations that have not been previously exposed to a specific in- boric acid) or gut (e.g. Bacillus thuringiensis Cry toxins)). It has long been secticide and are therefore susceptible (in the absence of cross-re- known that the LD50 of an insecticide administered via injection is sistance)) remain uncharacterized. Our poor understanding of the fac- usually lower than by topical application (Brooks, 1976; Liu and Yue, tors that determine the relative toxicity of an insecticide is partly due to 2001), indicating that penetration is a limiting step in the toxicity of the technical difficulties of studying the molecular mechanisms un- most insecticides. derlying insecticide toxicity in pest species, as well as a strong focus of There have been several studies on insecticide penetration through the research community on genes historically involved in insecticide the cuticle, including using radiolabeled insecticide to determine pe- resistance. However, the genetic basis of insecticide sensitivity likely netration rates and comparing the resistance levels for topical appli- extends beyond what is revealed by studying only known resistance cation versus injection, and such studies have identified decreased cu- genes. With millions of pounds of insecticides being used each year, a ticular penetration as a mechanism of resistance. Although numerous https://doi.org/10.1016/j.pestbp.2019.09.006 Received 20 August 2019; Received in revised form 17 September 2019; Accepted 18 September 2019 Available online 21 October 2019 0048-3575/ © 2019 Elsevier Inc. All rights reserved. Opinion paper Pesticide Biochemistry and Physiology 161 (2019) 95–103 penetration distribution target site metabolism excretion Oral Topical/residual Inhalation Injection Foregut Cuticle Trachea Midgut Hemolymph Metabolites Hemolymph Fat bodies Target sites Malpighian tubules Hindgut Excreted Fig. 1. Diagrammatic representation of insecticide pharmacokinetics/pharmacodynamics in an insect. studies have sought to understand the basis of this resistance, these pyrethroids and DDT (Dong et al., 2014; Scott, 2019). Overall, we have studies are mostly correlative, and thus the factors that facilitate or an excellent understanding of the effects of most major types ofin- impede penetration remain largely unknown (Brooks, 1976; Welling secticides on their target sites. and Peterson, 1985; Denecke et al., 2018). Furthermore, how in- Excretion is the fifth and final step in the pharmacokinetics ofin- secticides cross the gut epithelial barrier is an area that remains almost secticides and it is technically challenging to study because it tradi- entirely unexplored (Denecke et al., 2018). tionally requires collection of excreta, followed by extraction and A second step in the poisoning process is the dissemination of in- quantitation of the parent insecticide (separate from the metabolites). secticides throughout the insect after they have entered the hemolymph Increased excretion was not observed as a resistance mechanism until (Fig. 1). Fundamental information, such as active or passive transport, recently (Strycharz et al., 2013). Although the specific gene responsible about how insecticides cross internal membranes (e.g. neural sheath) was not ascertained, ABC transporters were implicated in the increased remains unknown. Even though these factors likely influence the ulti- excretion (Seong et al., 2016). In some cases, it is difficult to disen- mate poisoning outcome, they have received scant study, primarily tangle the processes of distribution and/or excretion. For example, two because they are technically very challenging to study. For example, recent studies using RNAi-mediated silencing and/or gene deletions studying distribution presents the obvious challenges of visualizing or investigated found that ABC transporters, particularly Mdr65, can alter detecting the spatial changes in insecticide concentration over time in a the toxicity of insecticides by changing the distribution/excretion of live insect. insecticides, (Denecke et al., 2017a; Sun et al., 2017). However, ABC A third step in the pharmacokinetics of insecticides, and one that transporters are a large family of proteins, with varying substrate spe- has been reasonably well studied, is the metabolism of insecticides by cificities, and the roles of most of these transporters in insecticide dis- various enzymes in the insect. Early studies succeeded in identifying the tribution and excretion have yet to be studied. types of enzymes involved in insecticide metabolism as primarily cy- From the above information it is clear that we have a largely in- tochrome P450s (CYPs), esterases, and glutathione S-transferases complete picture of the genes that determine the fate of an insect ex- (GSTs). However, each of these enzyme groups is comprised of nu- posed to an insecticide. This is driven primarily by a lack of tools and/ merous genes, which has made identification of the specific protein(s) or an abundance of candidate genes. We propose that using
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