An insecticide target in mechanoreceptor neurons

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Abstract

Hundreds of neurotoxic insecticides are currently in use. However, only a few direct targets have been identified. Here, using Drosophila and the insecticide flonicamid, we identified nicotinamidase (Naam) as a previous unidentified molecular target for an insecticide. Naam is expressed in chordotonal stretch-receptor neurons, and inhibition of Naam by a metabolite of flonicamid, TFNA-AM (4-trifluoromethylnicotinamide), induces accumulation of substrate nicotinamide and greatly inhibits negative geotaxis. Engineered flies harboring a point mutation in the active site show insecticide resistance and defects in gravity sensing. Bees are resistant to flonicamid because of a gene duplication, resulting in the generation of a TFNA-AM–insensitive Naam. Our results, in combination with the absence of genes encoding Naam in vertebrate genomes, suggest that TFNA-AM and potential species-specific Naam inhibitors could be developed as novel insecticides, anthelmintics, and antimicrobials for agriculture and human health.

Abstract

Nicotinamidase is a target for insecticides and potential anthelmintics and antimicrobials.

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Most cited references 43

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Increase in crop losses to insect pests in a warming climate

David S. Battisti, Scott Merrill, Raymond Huey … (2018)

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The importance of vector control for the control and elimination of vector-borne diseases

Anne Wilson, Orin Courtenay, Louise Kelly-Hope … (2020)

Vector-borne diseases (VBDs) such as malaria, dengue, and leishmaniasis exert a huge burden of morbidity and mortality worldwide, particularly affecting the poorest of the poor. The principal method by which these diseases are controlled is through vector control, which has a long and distinguished history. Vector control, to a greater extent than drugs or vaccines, has been responsible for shrinking the map of many VBDs. Here, we describe the history of vector control programmes worldwide from the late 1800s to date. Pre 1940, vector control relied on a thorough understanding of vector ecology and epidemiology, and implementation of environmental management tailored to the ecology and behaviour of local vector species. This complex understanding was replaced by a simplified dependency on a handful of insecticide-based tools, particularly for malaria control, without an adequate understanding of entomology and epidemiology and without proper monitoring and evaluation. With the rising threat from insecticide-resistant vectors, global environmental change, and the need to incorporate more vector control interventions to eliminate these diseases, we advocate for continued investment in evidence-based vector control. There is a need to return to vector control approaches based on a thorough knowledge of the determinants of pathogen transmission, which utilise a range of insecticide and non–insecticide-based approaches in a locally tailored manner for more effective and sustainable vector control.

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Soil-transmitted helminth infections

Peter Mark Jourdan, Poppy H. L. Lamberton, Alan Fenwick … (2018)

More than a quarter of the world's population is at risk of infection with the soil-transmitted helminths Ascaris lumbricoides, hookworm (Ancylostoma duodenale and Necator americanus), Trichuris trichiura, and Strongyloides stercoralis. Infected children and adults present with a range of medical and surgical conditions, and clinicians should consider the possibility of infection in individuals living in, or returning from, endemic regions. Although safe and effective drugs are donated free to endemic countries, only half of at-risk children received treatment in 2016. This Seminar describes the epidemiology, lifecycles, pathophysiology, clinical diagnosis, management, and public health control of soil-transmitted helminths. Previous work has questioned the effect of population-level deworming; however, it remains beyond doubt that treatment reduces the severe consequences of soil-transmitted helminthiasis. We highlight the need for refined diagnostic tools and effective control options to scale up public health interventions and improve clinical detection and management of these infections.

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Author and article information

Contributors

Xiaomu Qiao:

ORCID: https://orcid.org/0000-0001-9590-1319

Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Xiaoyu Zhang: Role: ConceptualizationRole: InvestigationRole: Methodology

Zhendong Zhou: Role: ConceptualizationRole: InvestigationRole: Methodology

Lei Guo:

ORCID: https://orcid.org/0000-0002-7122-3442

Role: ConceptualizationRole: InvestigationRole: Methodology

Weiping Wu: Role: ConceptualizationRole: InvestigationRole: Methodology

Suhan Ma: Role: ConceptualizationRole: InvestigationRole: Methodology

Xinzhong Zhang:

ORCID: https://orcid.org/0000-0001-7369-5761

Role: ConceptualizationRole: InvestigationRole: Methodology

Craig Montell:

ORCID: https://orcid.org/0000-0001-5637-1482

Role: ConceptualizationRole: Funding acquisitionRole: ResourcesRole: Writing - review & editing

Jia Huang:

ORCID: https://orcid.org/0000-0001-8336-1562

Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: November 2022

Publication date (Electronic, pub): 23 November 2022

Volume: 8

Issue: 47

Electronic Location Identifier: eabq3132

Affiliations

[ ¹ ]Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China.

[ ² ]Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou 310008, China.

[ ³ ]Department of Molecular, Cellular, and Developmental Biology and the Neuroscience Research Institute, University of California, Santa Barbara, Santa Barbara, CA 93106, USA.

Author notes

[* ]Corresponding author. Email: huangj@ 123456zju.edu.cn

Author information

Xiaomu Qiao https://orcid.org/0000-0001-9590-1319

Lei Guo https://orcid.org/0000-0002-7122-3442

Xinzhong Zhang https://orcid.org/0000-0001-7369-5761

Craig Montell https://orcid.org/0000-0001-5637-1482

Jia Huang https://orcid.org/0000-0001-8336-1562

Article

Publisher ID: abq3132

DOI: 10.1126/sciadv.abq3132

PMC ID: 9683716

SO-VID: d1a0bc78-877c-4dce-b4a7-ae12664183ce

Copyright © Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

History

Date received : 08 April 2022

Date accepted : 05 October 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000055, National Institute on Deafness and Other Communication Disorders;

Award ID: DC007864

Funded by: FundRef http://dx.doi.org/10.13039/100000060, National Institute of Allergy and Infectious Diseases;

Award ID: AI165575

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 32072496

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 31802019

Funded by: FundRef http://dx.doi.org/10.13039/501100004731, Natural Science Foundation of Zhejiang Province;

Award ID: LR19C140002

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Copyeditor Penchie Limbo

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An insecticide target in mechanoreceptor neurons

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Special feature: Decolonising the School Curriculum

Most cited references 43

Increase in crop losses to insect pests in a warming climate

The importance of vector control for the control and elimination of vector-borne diseases

Soil-transmitted helminth infections

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Cited by 6

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