A spinosyn-sensitive Drosophila melanogaster nicotinic acetylcholine receptor identified through chemically induced target site resistance, resistance gene identification, and heterologous expression

Watson, Gerald B.; Chouinard, Scott W.; Cook, Kevin R.; Geng, Chaoxian; Gifford, Jim M.; Gustafson, Gary; Hasler, James M.; Larrinua, Ignacio M.; Letherer, Ted J.; Mitchell, Jon Ceander; Pak, William L.; Salgado, Vincent L.; Sparks, Thomas C.; Stilwell, Geoff

doi:10.1016/j.ibmb.2009.11.004

Cited by 130 publications

(141 citation statements)

References 24 publications

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“…In support of the positive allosteric modulation of nAChR and its ability to induce lethal actions in insects, κ-HXTX-Hv1c appears to have a mode of action similar to the excitatory insecticide spinosyn A (Salgado, 1998;Salgado and Saar, 2004;Salgado et al, 1998;Watson et al, 2010). Moreover, studies have indicated that spinosyn A (the major component of spinosad) interacts with a site on insect nAChRs that is distinct from other insecticides (Salgado and M A N U S C R I P T…”

Section: Validation Of Nachr As a Lethal Targetmentioning

confidence: 94%

Lethal effects of an insecticidal spider venom peptide involve positive allosteric modulation of insect nicotinic acetylcholine receptors

et al. 2017

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Please cite this article as: Windley, M.J., Vetter, I., Lewis, R.J., Nicholson, G.M., Lethal effects of an insecticidal spider venom peptide involve positive allosteric modulation of insect nicotinic acetylcholine receptors, Neuropharmacology (2017), doi: 10.1016/j.neuropharm.2017.04.008. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Highlights• The previously characterized BK Ca channel block is not responsible for the lethal excitatory toxicity of κ-HXTX-Hv1c • κ-HXTX-Hv1c is a positive allosteric modulator of the insect nicotinic acetylcholine receptor which acts by prolonging current decay and reversing receptor desensitization • The likely lethal target of κ-HXTX-Hv1c is the nicotinic acetylcholine receptor, acting by a mechanism similar to that of the insecticide spinosyn A. A B S T R A C Tκ-Hexatoxins (κ-HXTXs) are a family of excitotoxic insect-selective neurotoxins from Australian funnel-web spiders that are lethal to a wide range of insects, but display no toxicity towards vertebrates. The prototypic κ-HXTX-Hv1c selectively blocks native and expressed cockroach largeconductance calcium-activated potassium (BK Ca or K Ca 1.1) channels, but not their mammalian orthologs. Despite this potent and selective action on insect K Ca 1.1 channels, we found that the classical K Ca 1.1 blockers paxilline, charybdotoxin and iberiotoxin, which all block insect K Ca 1.1 channels, are not lethal in crickets. We therefore used whole-cell patch-clamp analysis of cockroach dorsal unpaired median (DUM) neurons to study the effects of κ-HXTX-Hv1c on sodium-activated (K Na ), delayed-rectifier (K DR ) and 'A-type' transient (K A ) K + channels. 1 µM κ-HXTX-Hv1c failed to significantly inhibit cockroach K Na and K DR channels, but did cause a 30 ± 7% saturating inhibition of K A channel currents, possibly via a Kv4 (Shal-like) action. However, this modest action at such a high concentration of κ-HXTX-Hv1c would indicate a different lethal target. Accordingly, we assessed the actions of κ-HXTX-Hv1c on neurotransmitter-gated ion channels in cockroach DUM neurons. We found that κ-HXTX-Hv1c failed to produce any major effects on GABA A or glutamate-Cl receptors but dramatically slowed nicotine-evoked ACh receptor (nAChR) current decay and reversed nAChR desensitization. These actions occurred without any alterations to nAChR current amplitude or the nicotine concentration-response curve, and are consistent with a positive allosteric modulation of nAChRs. κ-HXTX-Hv1c therefore represents the first venom peptide that selectively modulates insect nAChRs with a mode of action similar to the excitotoxic insecticide spino...

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Section: Validation Of Nachr As a Lethal Targetmentioning

confidence: 94%

Lethal effects of an insecticidal spider venom peptide involve positive allosteric modulation of insect nicotinic acetylcholine receptors

et al. 2017

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“…They target binding sites on nAChRs that are distinct from those at which other insecticides bind. Watson et al [40] and Perry et al [41] have provided strong evidence that the D. melanogaster Dα6 subunit [42] is targeted by spinosad. There are several examples of insect pest species where mutations in the α6 nAChR subunit are associated with high levels of resistance to spinosad.…”

Section: Spinosynsmentioning

confidence: 99%

Modes of Action, Resistance and Toxicity of Insecticides Targeting Nicotinic Acetylcholine Receptors

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Buckingham

Matsuda

et al. 2017

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Nicotinic acetylcholine receptors (nAChRs) are members of the cys-loop superfamily of ligand-gated ion channels (cys-loop LGICs) and mediate fast cholinergic synaptic transmission in the nervous system of insects. The completion of many insect genome projects has greatly enhanced our understanding of the individual subunits that make up nAChR gene families from an insect genetic model organism (Drosophila melanogaster), crop pests, disease vectors and beneficial (pollinator) species. In addition to considerable insect nAChR subunit diversity, individual subunits can be subject to alternative splicing and RNA editing and these post-transcriptional modifications can add significantly to the diversity of nAChR receptor subtypes. The actions of insecticides targeting nAChRs, notably cartap, neonicotinoids, sulfoximines, flupyradifurone, spinosyns and triflumezopyrim are reviewed. Structural studies obtained using an acetylcholine binding protein (AChBP) co-crystallised with neonicotinoids have yielded important new insights into the requirements for neonicotinoid insecticide -nAChR interactions. The persistent application of insecticides to crop pests leads to the onset of resistance and several examples of resistance to insecticides targeting nAChRs have been documented. Understanding the molecular basis of resistance can inform our understanding of the mechanism of insecticide action. It also provides an important driver for the development of new chemistry, diagnostic tests for resistance and the adoption of application strategies designed to attenuate such problems. Finally, we consider toxicity issues relating to nAChR-active insecticides, with particular reference to beneficial insect species (pollinators) as well as mammalian and avian toxicity. This review is part of the special issue "Insecticide Mode of Action: From Insect to Mammalian Toxicity"

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Section: Introductionmentioning

confidence: 99%

“…Apesar de as espinosinas serem moléculas relativamente recentes no mercado, já foram relatados na literatura diversos casos de resistência a spinosad, tais como em Frankliniella occidentalis (Pergande) (BIELZA et al, 2007a(BIELZA et al, , 2007b, Drosophila melanogaster (Meigen) WATSON et al, 2010), Spodoptera exigua (Hübner) (MOULTON et al, 2000), Tuta absoluta (Meyrick) (CAMPOS et al, 2014), Plutella xylostella (L.) (BAXTER et al, 2010; (STORER et al, 2010). Em 2014, a evolução da resistência de S. frugiperda a Cry1F também foi reportada no Brasil .…”

Section: Introductionunclassified

“…(YU, 1991(YU, , 1992(YU, , 2006 CARVALHO et al., 2013;NASCIMENTO et al, 2015). (BIELZA et al, 2007a(BIELZA et al, , 2007b, Drosophila melanogaster (Meigen) WATSON et al, 2010), Spodoptera exigua (Hübner) (MOULTON et al, 2000), Tuta absoluta (Meyrick) (CAMPOS et al, 2014), Plutella xylostella (L.) (BAXTER et al, 2010; (CARVALHO et al, 2013; YU, 1992 YU, , 1993 virescens (YOUNG et al, 2001; ROE et al, 2010), Helicoverpa armigera (Hübner) (AHMAD et al, 2003), P. xylostella (ZHAO et al, 2006) e Spodoptera exigua (Hübner) (WANG et al, 2006).Atualmente, as espinosinas são consideradas de grande importância no manejo integrado de pragas por possuírem elevada eficiência, características ambientais e toxicológicas favoráveis, um mecanismo de ação único, além de apresentarem baixa toxidez a populações de insetos benéficos (SPARKS et al, 2001). Desse modo, é necessário que se conheça os mecanismos e as bases genéticas envolvidos na resistência de insetos a 28 espinosinas, a fim de se desenvolver estratégias de manejo e de monitoramento da resistência que auxiliem a prolongar a vida útil dessa molécula inseticida.…”

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Bases genéticas e moleculares da resistência de <i>Spodoptera frugiperda</i> (J.E. Smith) (Lepidoptera: Noctuidae) a spinosad

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Aos meus queridos pais Katsuyuki e Vanda, e aos meus irmãos Isa e Dudu, pelo afeto, incentivo e ensinamentos fundamentais em minha formação pessoal e profissional, Ao meu namorado Makoto Okuno pelo companheirismo, afeto e apoio em todos os momentos, DEDICO E AGRADEÇO4 5 AGRADECIMENTOSAo Prof. Dr. Celso Omoto, pela orientação, por todos os ensinamentos, pela oportunidade de realização deste trabalho e pela confiança depositada em mim.Ao Prof. Dr. Fernando L. Cônsoli pelos conselhos, orientação, apoio e pela disponibilização do laboratório para condução do trabalho. Aos queridos amigos do Laboratório de Resistência de Artrópodes a Pesticidas(ESALQ/USP), Oderlei Bernardi, Daniel Bernardi, Renato J. Horikoshi, Antônio R.Nascimento, pela amizade, pela excelente convivência, companheirismo, conhecimentos transmitidos e auxílios prestados na condução deste trabalho. Foi uma grande satisfação poder trabalhar, aprender e conviver com vocês todos esses anos.A Eloisa Salmeron e Gislaine A. A. de Oliveira Campos, por todos os ensinamentos, pela paciência e auxílio na condução das atividades do laboratório, pelos conselhos, por toda ajuda e carinho. Muito obrigada por todo apoio e amizade durante esses anos, os quais foram imprescindíveis para minha formação. A todos os amigos e colegas do Programa de Pós-Graduação em Entomologia (ESALQ/USP) pelo agradável convívio, amizade e companheirismo.À minha família, em especial aos meus pais Vanda e Paulo e aos meus irmãos Isabela e Paulo Eduardo, pelo amor, incentivo e por sempre me auxiliarem e contribuírem para meu crescimento pessoal e profissional.Ao meu namorado Makoto Okuno, por todo amor, compreensão e apoio incondicionais. Muito obrigada pelo estimo e dedicação em me auxiliar e orientar sempre.Aos amigos com quem morei em Piracicaba, Fernanda Canassa e Marilis Shimano, obrigado pela amizade, companheirismo e apoio em todos os momentos.Aos queridos amigos Fernando Cabezas, Odimar Z. Zanardi, Ana Karolina Azevedo, Ravana Sfalcin, Eimi Arikawa pela amizade de todos esses anos, carinho e incentivo.A todos os funcionários do Departamento de Entomologia e Acarologia da ESALQ/USP, pela dedicação e aos serviços prestados.A Escola Superior de Agricultura 'Luiz de Queiroz' por todas as oportunidades concedidas e por ser um berço de conhecimento. Aos professores do Programa de Pós-Graduação em Entomologia da Escola Superiorde Agricultura "Luiz de Queiroz" (ESALQ/USP), pelos conhecimentos transmitidos.Ao Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) pela concessão da bolsa de estudo.Ao IRAC-BR pelo auxílio e apoio na coleta e manutenção de populações de Spodoptera frugiperda.À bibliotecária Eliana Maria Garcia da Biblioteca Central (ESALQ/USP), pelo auxílio na formatação deste trabalho. RESUMOBases genéticas e moleculares da resistência de Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) a spinosad O inseticida spinosad tem sido um dos mais utilizados para o controle de Spodoptera frugiperda (J. E. Smith) no Brasil, devido à sua eficácia e ao seu mec...

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A spinosyn-sensitive Drosophila melanogaster nicotinic acetylcholine receptor identified through chemically induced target site resistance, resistance gene identification, and heterologous expression

Cited by 130 publications

References 24 publications

Lethal effects of an insecticidal spider venom peptide involve positive allosteric modulation of insect nicotinic acetylcholine receptors

Lethal effects of an insecticidal spider venom peptide involve positive allosteric modulation of insect nicotinic acetylcholine receptors

Modes of Action, Resistance and Toxicity of Insecticides Targeting Nicotinic Acetylcholine Receptors

Bases genéticas e moleculares da resistência de <i>Spodoptera frugiperda</i> (J.E. Smith) (Lepidoptera: Noctuidae) a spinosad

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