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Neuroactive Insecticides: Targets, Selectivity, Resistance, and Secondary Effects EN58CH06-Casida ARI 5 December 2012 8:11 Neuroactive Insecticides: Targets, Selectivity, Resistance, and Secondary Effects John E. Casida1,∗ and Kathleen A. Durkin2 1Environmental Chemistry and Toxicology Laboratory, Department of Environmental Science, Policy, and Management, 2Molecular Graphics and Computational Facility, College of Chemistry, University of California, Berkeley, California 94720; email: [email protected], [email protected] Annu. Rev. Entomol. 2013. 58:99–117 Keywords The Annual Review of Entomology is online at acetylcholinesterase, calcium channels, GABAA receptor, nicotinic ento.annualreviews.org receptor, secondary targets, sodium channel This article’s doi: 10.1146/annurev-ento-120811-153645 Abstract Copyright c 2013 by Annual Reviews. Neuroactive insecticides are the principal means of protecting crops, people, All rights reserved livestock, and pets from pest insect attack and disease transmission. Cur- ∗ Corresponding author rently, the four major nerve targets are acetylcholinesterase for organophos- phates and methylcarbamates, the nicotinic acetylcholine receptor for neonicotinoids, the γ-aminobutyric acid receptor/chloride channel for by Public Health Information Access Project on 04/29/14. For personal use only. Annu. Rev. Entomol. 2013.58:99-117. Downloaded from www.annualreviews.org polychlorocyclohexanes and fiproles, and the voltage-gated sodium channel for pyrethroids and dichlorodiphenyltrichloroethane. Species selectivity and acquired resistance are attributable in part to structural differences in binding subsites, receptor subunit interfaces, or transmembrane regions. Additional targets are sites in the sodium channel (indoxacarb and metaflumizone), the glutamate-gated chloride channel (avermectins), the octopamine receptor (amitraz metabolite), and the calcium-activated calcium channel (diamides). Secondary toxic effects in mammals from off-target serine hydrolase inhibi- tion include organophosphate-induced delayed neuropathy and disruption of the cannabinoid system. Possible associations between pesticides and Parkinson’s and Alzheimer’s diseases are proposed but not established based on epidemiological observations and mechanistic considerations. 99 EN58CH06-Casida ARI 5 December 2012 8:11 WHY NEUROACTIVE INSECTICIDES? Insecticides are principal defenses against insect pests of crops, livestock, pets, and people. Most PCCA: insecticides are nerve poisons and have been since dichlorodiphenyltrichloroethane (DDT) and polychlorocycloalkane various polychlorocycloalkanes (PCCAs) were introduced in the 1940s, followed by organophos- Target site: enzyme, phates (OPs) in the 1950s, methylcarbamates (MCs) in the 1960s, pyrethroids in the 1970s, and receptor, or channel neonicotinoids in the 1990s (26, 138). Neurotoxicants are the major synthetic insecticides for site at which specific several reasons (28). They act rapidly to stop crop damage and disease transmission. There are binding initiates the many sensitive sites at which even a small disruption may ultimately prove to be lethal. A lipoidal physiological change sheath protects the insect nerve from ionized toxicants but not from lipophilic insecticides. Poor Cross-resistance: detoxification mechanisms in nerves provide prolonged toxicant effects. target site (or metabolic) resistance The nervous system has at least 11 targets or defined modes of action for neuroactive in- conferred by a secticides (7, 8, 23, 26, 32) (Figure 1, A–K). Primary target site selectivity between insects and common target (or people plays an important role in insecticide safety, but secondary targets must also be considered. detoxification Selection of pest populations for target site resistance and cross-resistance is delayed or circum- mechanism) vented by shifting modes of action. A diversity of targets is therefore critical for insect and in- Secondary effect: secticide management (95). This review considers the targets and species selectivity of neurotoxic toxicity from action at insecticides, the resistance mechanisms in insects, and the secondary effects in mammals, with a secondary target emphasis on research by the authors. Structures for the insecticides mentioned here are given in Ordeal poison: recent manuals or reviews (8, 95, 138). a poison given to the accused to determine guilt (dies) or innocence (lives) ACETYLCHOLINESTERASE Primary Target and Inhibitor Action The toxicity of OPs and MCs to insects and mammals is attributable to inhibition of acetyl- cholinesterase (AChE), which is responsible for the hydrolysis of acetylcholine (ACh) at synaptic regions of cholinergic nerve endings (19, 46, 74) (Figure 1). AChE inhibitors cause ACh to accu- mulate, resulting in excessive stimulation of cholinergic receptors. The MC physostigmine from calabar beans (Physostigma venenosum) was used first as an ordeal poison in West Africa and then to establish the relationships between ACh neurotransmission and AChE activity and its inhibition (20). AChE inhibition by OP and MC insecticides involves phosphorylation and carbamoylation, respectively, of serine in the esteratic site (Figures 1, 2). AChE is inhibited by MCs as the re- versible AChE–MC complex or as the methylcarbamoylated enzyme at serine that reactivates spontaneously over a short time span (75). The corresponding reaction with OPs yields the phos- by Public Health Information Access Project on 04/29/14. For personal use only. Annu. Rev. Entomol. 2013.58:99-117. Downloaded from www.annualreviews.org phorylated AChE that undergoes aging or reactivates slowly, except with an oxime reactivator such as pralidoxime (19, 46). −−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→ Figure 1 Proposed sites of neuroactive insecticide action on nerve impulses, neuromuscular transmission, and synaptic receptors adapted from Bloomquist (8), Casida & Quistad (28), and many other sources. The presynaptic nerve terminals (–, ) and the postsynaptic cell (–, ) or muscle cell () are shown. In the nicotinic and γ-aminobutyric acid (GABA) receptor/channel cross-sections (, ), four of the five subunits and one binding site are arbitrarily shown per channel. The number of commercial insecticides or prototype natural products (number of compounds) (95) that act at each site (A–K) are given in parentheses. Abbreviations: ACh, acetylcholine; DDT, dichlorodiphenyltrichloroethane; MC, methylcarbamate; nAChR, nicotinic acetylcholine receptor; OP, organophosphate; PCCA, polychlorocycloalkane. 100 Casida · Durkin EN58CH06-Casida ARI 5 December 2012 8:11 Neurotransmitters 11. AChE and nicotinic receptor/cation channel excitatory synapse ACh CH C(O)OCH CH N+(CH ) AChE A 3 2 2 3 3 ACh choline + acetate K+ ACh Excitatory ACh GABA NH2CH2CH2CH2C(O)OH ACh postsynaptic ACh ACh potential Extracellular Vesicles B Na+ Octopamine HO CHOHCH2NH2 ACh ACh ACh Action potential Intracellular OO BD– + Na Glutamate HO OH NH2 22. GABA receptor/CI– channel inhibitory synapse GABA Insecticides (number of compounds) G opens G GABA OP (65), MC (26), physotigmine: Vesicles Extracellular A AChE inhibitors Cl– F G G Nicotine, neonicotinoids (7): Inhibitory B nAChR agonists G = GABA postsynaptic potential E Intracellular Nereistoxin analogs (4): Cl– EF– Block of action potential C nAChR blocker 33. Glutamate receptor excitatory synapse Spinosyns (2): nAChR allosteric D activators Glu Fiproles (2), PCCAs (2), picrotoxin: Na+ E noncompetitive antagonists, blockers and convulsants Ca++ Excitatory postsynaptic potential Avermectins (4): activators, F modulators Glu Cl – F DDT, pyrethroids, pyrethrins, G veratridine (44): modulators 4.4 Voltage-dependent Na+ channel H Indoxacarb (1): blocker GI– I Metaflumizone (1): blocker Na+ Ca++ Ryanodine, diamides (2): activators Action J potential Glu Glu Type 1 pyrethroids by Public Health Information Access Project on 04/29/14. For personal use only. Control Type 2 pyrethroids Annu. Rev. Entomol. 2013.58:99-117. Downloaded from www.annualreviews.org action repetitive firing suppression of Vesicles Glu K Amitraz (1): mimics Glu potential action potential Glu = glutamate 5.5 Ca2+–activated Ca2+ channel 66. Octopamine receptor coupled to second messengers J ATP Mg2+ Ca2+ Ryanodine receptor OA OAOA Elevation of cyclic AMP Sarcoplasmic Ca2+ Muscle reticulum contraction OA OA K Neuroexcitation Transverse OA = octopamine Cell membrane tubule Ca2+ Voltage channel sensor www.annualreviews.org • Neuroactive Insecticides 101 EN58CH06-Casida ARI 5 December 2012 8:11 a AChE – chlorpyrifos oxonb nAChR – imidacloprid nAChR-heteropentamer AChBP-homopentamer O O Cl N P Extracellular O O Side view Cl binding domain Cl Trans- membrane BP BP E334* domain Top view Intracellular BP F295 BP BP Y337 H447* N131 Cl S203* F338 L141 L143 N Y231 W174 C227 N G121 Y118 N G120 N N+ C226 H O– O Y119 Y224 W79 + c GABAAR – fipronil d Na channel - deltamethrin Heteropentamer Homopentamer O α β 1 3 N Br L L V T A A T O L β3 L A β3 Br β3 T β3 T T L T L A NCA A NCA V L T L T A T L T α1 L γ S A β3 2 β3 O by Public Health Information Access Project on 04/29/14. For personal use only. Annu. Rev. Entomol. 2013.58:99-117. Downloaded from www.annualreviews.org F1530 L L932* C933 9' CF3 L F1534 L L T929* L T T F1538 6' T Cl Cl F1537 N T N NH2 L925* M918* 2' A A S CF A A N O 3 102 Casida · Durkin EN58CH06-Casida ARI 5 December 2012 8:11 Selectivity and Resistance Inhibitor specificity between the AChE of insects and mammals and between susceptible and tol- erant strains of insects contributes to selective toxicity and resistance
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