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Molecular Mechanism of Action of Neonicotinoid Insecticides

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Toxicology".

Deadline for manuscript submissions: closed (31 May 2022) | Viewed by 33373

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Prof. Dr. Steeve Hervé Thany

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Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d’Orléans, UPRES EA 1207-USC INRA, Rue de Chartres, BP 6759, 45067 Orléans, France
Interests: neonicotinoid insecticides; insect neuronal nicotinic acetylcholine receptors; mammalian neuronal nicotinic receptors
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Dear Colleagues,

Neonicotinoid insecticides are used worldwide and have been demonstrated as toxic to beneficial insects such as honeybees. Their effectiveness is predominantly attributed to their high affinity for insect neuronal nicotinic acetylcholine receptors (nAChRs). Mammalian neuronal nAChRs are of major importance because cholinergic synaptic transmission plays a key role in rapid neurotransmission, learning and memory processes, and neurodegenerative diseases. Because of the low agonist effects of neonicotinoid insecticides on mammalian neuronal nAChRs, it has been suggested that they are relatively safe for mammals, including humans. However, several lines of evidence have demonstrated that neonicotinoid insecticides can modulate cholinergic functions through neuronal nAChRs. Major studies on the influence of neonicotinoid insecticides on cholinergic functions have been conducted using nicotine low-affinity homomeric α7 and high-affinity heteromeric α4β2 receptors, as they are the most abundant in the nervous system. It has been found that the neonicotinoids thiamethoxam and clothianidin can activate the release of dopamine in rat striatum. In some contexts, such as neurodegenerative diseases, they can disturb the neuronal distribution or induce oxidative stress, leading to neurotoxicity.

In this special issue, we aim to explore the molecular mechanism of action of neonicotinoid insecticides from chemical analyses, toxicology, to molecular and cellular levels.

Prof. Dr. Steeve Hervé Thany
Guest Editor

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Keywords

neonicotinoids
toxicity
chemistry
mode of action
nicotinic acetylcholine receptors

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Published Papers (7 papers)

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Editorial

Jump to: Research, Review

4 pages, 211 KiB

Open AccessEditorial

Molecular Mechanism of Action of Neonicotinoid Insecticides

by Steeve H. Thany

Int. J. Mol. Sci. 2023, 24(6), 5484; https://doi.org/10.3390/ijms24065484 - 13 Mar 2023

Cited by 8 | Viewed by 2717

Abstract

Since neonicotinoid insecticides were first introduced several years ago, most of them have been banned by the European Union due to their potentially adverse effects on humans and useful insects [...] Full article

(This article belongs to the Special Issue Molecular Mechanism of Action of Neonicotinoid Insecticides)

Research

Jump to: Editorial, Review

14 pages, 2464 KiB

Open AccessArticle

The Synergistic Effect of Thiamethoxam and Synapsin dsRNA Targets Neurotransmission to Induce Mortality in Aphis gossypii

by Xueting Qu, Sijia Wang, Guangze Lin, Mingshan Li, Jie Shen and Dan Wang

Int. J. Mol. Sci. 2022, 23(16), 9388; https://doi.org/10.3390/ijms23169388 - 20 Aug 2022

Cited by 9 | Viewed by 2289

Abstract

Sublethal doses of insecticides have many impacts on pest control and agroecosystems. Insects that survive a sublethal dose of insecticide could adapt their physiological and behavioral functions and resist this environmental stress, which contributes to the challenge of pest management. In this study, the sublethal effects of thiamethoxam on gene expression were measured through RNA sequencing in the melon aphid Aphis gossypii. Genes regulating energy production were downregulated, while genes related to neural function were upregulated. To further address the function of genes related to neurotransmission, RNA interference (RNAi) was implemented by transdermal delivery of dsRNA targeting synapsin (syn), a gene regulating presynaptic vesicle clustering. The gene expression of synapsin was knocked down and the mortality of aphids was increased significantly over the duration of the assay. Co-delivery of syn-dsRNA and thiamethoxam reversed the upregulation of synapsin caused by low-dose thiamethoxam and resulted in lethality to melon aphids, suggesting that the decreased presynaptic function may contribute to this synergistic lethal effect. In addition, the nanocarrier star polycation, which could bind both dsRNA and thiamethoxam, greatly improved the efficacy of lethality. These results increase our knowledge of the gene regulation induced by sublethal exposure to neonicotinoids and indicated that synapsin could be a potential RNAi target for resistance management of the melon aphid. Full article

(This article belongs to the Special Issue Molecular Mechanism of Action of Neonicotinoid Insecticides)

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12 pages, 4608 KiB

Open AccessArticle

Mode of Action of Neonicotinoid Insecticides Imidacloprid and Thiacloprid to the Cockroach Pameα7 Nicotinic Acetylcholine Receptor

by Alison Cartereau, Emiliane Taillebois, Jean-Yves Le Questel and Steeve H. Thany

Int. J. Mol. Sci. 2021, 22(18), 9880; https://doi.org/10.3390/ijms22189880 - 13 Sep 2021

Cited by 12 | Viewed by 3102

Abstract

The functional expression of the cockroach Pameα7 nicotinic acetylcholine receptor subunit has been previously studied, and was found to be able to form a homomeric receptor when expressed in Xenopus laevis oocytes. In this study, we found that the neonicotinoid insecticide imidacloprid is unable to activate the cockroach Pameα7 receptor, although thiacloprid induces low inward currents, suggesting that it is a partial agonist. In addition, the co-application or 5 min pretreatment with 10 µM imidacloprid increased nicotine current amplitudes, while the co-application or 5 min pretreatment with 10 µM thiacloprid decreased nicotine-evoked current amplitudes by 54% and 28%, respectively. This suggesting that these two representatives of neonicotinoid insecticides bind differently to the cockroach Pameα7 receptor. Interestingly, the docking models demonstrate that the orientation and interactions of the two insecticides in the cockroach Pameα7 nAChR binding pocket are very similar. Electrophysiological results have provided evidence to suggest that imidacloprid and thiacloprid could act as modulators of the cockroach Pameα7 receptors. Full article

(This article belongs to the Special Issue Molecular Mechanism of Action of Neonicotinoid Insecticides)

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18 pages, 908 KiB

Open AccessArticle

Partial Agonist Activity of Neonicotinoids on Rat Nicotinic Receptors: Consequences over Epinephrine Secretion and In Vivo Blood Pressure

by Joohee Park, Antoine Taly, Jennifer Bourreau, Frédéric De Nardi, Claire Legendre, Daniel Henrion, Nathalie C. Guérineau, Christian Legros, César Mattei and Hélène Tricoire-Leignel

Int. J. Mol. Sci. 2021, 22(10), 5106; https://doi.org/10.3390/ijms22105106 - 12 May 2021

Cited by 6 | Viewed by 2762

Abstract

Neonicotinoid insecticides are nicotine-derived molecules which exert acute neurotoxic effects over the insect central nervous system by activating nicotinic acetylcholine receptors (nAChRs). However, these receptors are also present in the mammalian central and peripheral nervous system, where the effects of neonicotinoids are faintly known. In mammals, cholinergic synapses are crucial for the control of vascular tone, blood pressure and skeletal muscle contraction. We therefore hypothesized that neonicotinoids could affect cholinergic networks in mammals and sought to highlight functional consequences of acute intoxication in rats with sub-lethal concentrations of the highly used acetamiprid (ACE) and clothianidin (CLO). In this view, we characterized their electrophysiological effects on rat

α

β

4 nAChRs, knowing that it is predominantly expressed in ganglia of the vegetative nervous system and the adrenal medulla, which initiates catecholamine secretion. Both molecules exhibited a weak agonist effect on

α

β

4 receptors. Accordingly, their influence on epinephrine secretion from rat adrenal glands was also weak at 100 μM, but it was stronger at 500 μM. Challenging ACE or CLO together with nicotine (NIC) ended up with paradoxical effects on secretion. In addition, we measured the rat arterial blood pressure (ABP) in vivo by arterial catheterization. As expected, NIC induced a significant increase in ABP. ACE and CLO did not affect the ABP in the same conditions. However, simultaneous exposure of rats to both NIC and ACE/CLO promoted an increase of ABP and induced a biphasic response. Modeling the interaction of ACE or CLO on

α

β

4 nAChR is consistent with a binding site located in the agonist pocket of the receptor. We present a transversal experimental approach of mammal intoxication with neonicotinoids at different scales, including in vitro, ex vivo, in vivo and in silico. It paves the way of the acute and chronic toxicity for this class of insecticides on mammalian organisms. Full article

(This article belongs to the Special Issue Molecular Mechanism of Action of Neonicotinoid Insecticides)

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Review

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23 pages, 5246 KiB

Open AccessReview

Chronic Effects of Imidacloprid on Honey Bee Worker Development—Molecular Pathway Perspectives

by Yun-Ru Chen, David T. W. Tzeng and En-Cheng Yang

Int. J. Mol. Sci. 2021, 22(21), 11835; https://doi.org/10.3390/ijms222111835 - 31 Oct 2021

Cited by 17 | Viewed by 4477

Abstract

Sublethal dosages of imidacloprid cause long-term destructive effects on honey bees at the individual and colony levels. In this review, the molecular effects of sublethal imidacloprid were integrated and reported. Several general effects have been observed among different reports using different approaches. Quantitative PCR approaches revealed that imidacloprid treatments during the adult stage are expressed as changes in immuneresponse, detoxification, and oxidation-reduction response in both workers and queens. In addition, transcriptomic approaches suggested that phototransduction, behavior, and somatic muscle development also were affected. Although worker larvae show a higher tolerance to imidacloprid than adults, molecular evidence reveals its potential impacts. Sublethal imidacloprid treatment during the larval stage causes gene expression changes in larvae, pupae, and adults. Transcriptome profiles suggest that the population and functions of affected differentially expressed genes, DEGs, vary among different worker ages. Furthermore, an early transcriptomic switch from nurse bees to foragers was observed, suggesting that precocious foraging activity may occur. This report comprehensively describes the molecular effects of sublethal dosages of imidacloprid on the honey bee Apis mellifera. The corresponding molecular pathways for physiological and neurological responses in imidacloprid-exposed honey bees were validated. Transcriptomic evidence suggests a global and sustained sublethal impact of imidacloprid on honey bee development. Full article

(This article belongs to the Special Issue Molecular Mechanism of Action of Neonicotinoid Insecticides)

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35 pages, 1001 KiB

Open AccessReview

Physiological Effects of Neonicotinoid Insecticides on Non-Target Aquatic Animals—An Updated Review

by Nemi Malhotra, Kelvin H.-C. Chen, Jong-Chin Huang, Hong-Thih Lai, Boontida Uapipatanakul, Marri Jmelou M. Roldan, Allan Patrick G. Macabeo, Tzong-Rong Ger and Chung-Der Hsiao

Int. J. Mol. Sci. 2021, 22(17), 9591; https://doi.org/10.3390/ijms22179591 - 4 Sep 2021

Cited by 45 | Viewed by 10349

Abstract

In this paper, we review the effects of large-scale neonicotinoid contaminations in the aquatic environment on non-target aquatic invertebrate and vertebrate species. These aquatic species are the fauna widely exposed to environmental changes and chemical accumulation in bodies of water. Neonicotinoids are insecticides that target the nicotinic type acetylcholine receptors (nAChRs) in the central nervous systems (CNS) and are considered selective neurotoxins for insects. However, studies on their physiologic impacts and interactions with non-target species are limited. In researches dedicated to exploring physiologic and toxic outcomes of neonicotinoids, studies relating to the effects on vertebrate species represent a minority case compared to invertebrate species. For aquatic species, the known effects of neonicotinoids are described in the level of organismal, behavioral, genetic and physiologic toxicities. Toxicological studies were reported based on the environment of bodies of water, temperature, salinity and several other factors. There exists a knowledge gap on the relationship between toxicity outcomes to regulatory risk valuation. It has been a general observation among studies that neonicotinoid insecticides demonstrate significant toxicity to an extensive variety of invertebrates. Comprehensive analysis of data points to a generalization that field-realistic and laboratory exposures could result in different or non-comparable results in some cases. Aquatic invertebrates perform important roles in balancing a healthy ecosystem, thus rapid screening strategies are necessary to verify physiologic and toxicological impacts. So far, much of the studies describing field tests on non-target species are inadequate and in many cases, obsolete. Considering the current literature, this review addresses important information gaps relating to the impacts of neonicotinoids on the environment and spring forward policies, avoiding adverse biological and ecological effects on a range of non-target aquatic species which might further impair the whole of the aquatic ecological web. Full article

(This article belongs to the Special Issue Molecular Mechanism of Action of Neonicotinoid Insecticides)

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37 pages, 1583 KiB

Open AccessReview

Neurotoxic Effects of Neonicotinoids on Mammals: What Is There beyond the Activation of Nicotinic Acetylcholine Receptors?—A Systematic Review

by Carmen Costas-Ferreira and Lilian R. F. Faro

Int. J. Mol. Sci. 2021, 22(16), 8413; https://doi.org/10.3390/ijms22168413 - 5 Aug 2021

Cited by 61 | Viewed by 6116

Abstract

Neonicotinoids are a class of insecticides that exert their effect through a specific action on neuronal nicotinic acetylcholine receptors (nAChRs). The success of these insecticides is due to this mechanism of action, since they act as potent agonists of insect nAChRs, presenting low affinity for vertebrate nAChRs, which reduces potential toxic risk and increases safety for non-target species. However, although neonicotinoids are considered safe, their presence in the environment could increase the risk of exposure and toxicity. On the other hand, although neonicotinoids have low affinity for mammalian nAChRs, the large quantity, variety, and ubiquity of these receptors, combined with its diversity of functions, raises the question of what effects these insecticides can produce in non-target species. In the present systematic review, we investigate the available evidence on the biochemical and behavioral effects of neonicotinoids on the mammalian nervous system. In general, exposure to neonicotinoids at an early age alters the correct neuronal development, with decreases in neurogenesis and alterations in migration, and induces neuroinflammation. In adulthood, neonicotinoids induce neurobehavioral toxicity, these effects being associated with their modulating action on nAChRs, with consequent neurochemical alterations. These alterations include decreased expression of nAChRs, modifications in acetylcholinesterase activity, and significant changes in the function of the nigrostriatal dopaminergic system. All these effects can lead to the activation of a series of intracellular signaling pathways that generate oxidative stress, neuroinflammation and, finally, neuronal death. Neonicotinoid-induced changes in nAChR function could be responsible for most of the effects observed in the different studies. Full article

(This article belongs to the Special Issue Molecular Mechanism of Action of Neonicotinoid Insecticides)

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