Functional and Evolutionary Consequences of Pyrethroid Resistance Mutations in S6 Transmembrane Segments of a Voltage-Gated Sodium Channel

Zhao, Yong; Park, Yoonseong; Adams, Michael E.

doi:10.1006/bbrc.2000.3832

Cited by 52 publications

(44 citation statements)

References 21 publications

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“…In this study, we showed that the V409M mutation, equivalent to the V421M mutation identified in the tobacco budworm sodium channel, altered the voltage-dependence of activation and inactivation of a cockroach sodium channel, Para CSMA , and reduced channel sensitivity to deltamethrin. Our results are consistent with two very recent independent reports of a similar effect of the V421M mutation on the sensitivity of Drosophila and house fly sodium channels expressed in Xenopus (Zhao et al, 2000;Lee and Soderlund, 2001). These studies provide direct evidence that sodium channel mutations from one insect species can effectively confer pyrethroid insensitivity to heterologous sodium channels.…”

Section: Discussionsupporting

confidence: 93%

Synergistic interaction between two cockroach sodium channel mutations and a tobacco budworm sodium channel mutation in reducing channel sensitivity to a pyrethroid insecticide

Liu

Tan

Valles

et al. 2002

Insect Biochemistry and Molecular Biology

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Pyrethroid insecticide resistance due to reduced nerve sensitivity, known as knockdown resistance (kdr or kdr-type), is linked to multiple point mutations in the para-homologous sodium channel genes. Previously we demonstrated that two mutations (E434K and C764R) in the German cockroach sodium channel greatly enhanced the ability of the L993F mutation (a known kdr -type mutation) to reduce sodium channel sensitivity to deltamethrin, a pyrethroid insecticide. Neither E434K nor C764R alone, however, altered sodium channel sensitivity. To examine whether E434K and C764R also enhance the effect of pyrethroid resistance-associated sodium channel mutations identified in other insects, we introduced a V to M mutation (V409M) into the cockroach sodium channel protein at the position that corresponds to the V421M mutation in the Heliothis virescens sodium channel protein. We found that the V409M mutation alone modified the gating properties of the sodium channel and reduced channel sensitivity to deltamethrin by 10-fold. Combining the V409M mutation with either the E434K or C764K alone did not reduce the V409M channel sensitivity to deltamethrin further. However, the triple mutation combination (V409M, E434K and C764R) dramatically reduced channel sensitivity by 100-fold compared with the wild-type channel. These results suggest that the E434K and C764R mutations are important modifiers of sodium channel sensitivity to pyrethroid insecticides.

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Section: Discussionsupporting

confidence: 93%

Synergistic interaction between two cockroach sodium channel mutations and a tobacco budworm sodium channel mutation in reducing channel sensitivity to a pyrethroid insecticide

Liu

Tan

Valles

et al. 2002

Insect Biochemistry and Molecular Biology

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“…The mutation combinations, RF, KF and KRF, not only reduce the channel sensitivity to deltamethrin, also cause more complete decay of the tail current possibly by increasing the rate of deactivation of the modified channels. An acceleration of tail current decay was previously observed for the house fly kdr and super-kdr mutations and the Heliothis virescens L1029H mutation (Smith et al, 1997;Vais et al, 2000;Zhao et al, 2000). However, the cockroach L993F mutation reduces the channel sensitivity to deltamethrin without acceleration of the decay of the tail current (Table 3 and Fig.…”

Section: Discussionsupporting

confidence: 58%

“…Introduction of the two house fly mutations into the Drosophila Para protein greatly decreased channel sensitivity to deltamethrin (Vais et al, 2000). The V421M and L1029H sodium channel mutations associated with pyrethroid resistance in Heliothis virescens were also confirmed to reduce sodium channel sensitivity to the pyrethroid permethrin (Zhao et al, 2000). These studies clearly established that these sodium channel mutations play a significant role in sodium channel insensitivity to pyrethroids.…”

Section: Introductionmentioning

confidence: 61%

“…6-mV) of voltage-dependence of activation (Lee et al, 1999c). A similar shift was observed when the Heliothis virescens L1029H mutation was introduced into the Drosophila Para channel (Zhao et al, 2000). However, when the housefly L1014F mutation was introduced into the Drosophila Para channel, no significant shift was observed (Vais et al, 2000).…”

Section: Discussionmentioning

confidence: 77%

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Novel sodium channel gene mutations in Blattella germanica reduce the sensitivity of expressed channels to deltamethrin

Tan

Liu

Tsai³

et al. 2002

Insect Biochemistry and Molecular Biology

104

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Pyrethroid insecticides alter the normal gating of voltage-gated sodium channels in the nervous system. Three sodium channel mutations (E434K, C764R, L993F) were recently identified in pyrethroid resistant German cockroach populations. In this report, we show that the L993F mutation decreased sodium channel sensitivity to the pyrethroid, deltamethrin, by five-fold in Xenopus oocytes. In contrast, neither E434K nor C764R alone decreased channel sensitivity to deltamethrin. However, E434K or C764R combined with L993F reduced deltamethrin sensitivity by 100-fold. Furthermore, concomitant presence of all three mutations (KRF) reduced channel sensitivity to deltamethrin by 500-fold. None of the mutations significantly affected channel gating. However, sodium current amplitudes from the mutant sodium channel carrying either E434K or C764R alone were much reduced compared to those of the wild-type channel or the channel carrying the double or triple mutations (KF, RF and KRF). These results indicated that evolution of sodium channel insensitivity in the German cockroach is achieved by sequential selection of a primary mutation L993F and two secondary mutations E434K and C764R, and concomitant presence of all three mutations dramatically reduced sodium channel sensitivity to deltamethrin.

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“…Pyrethroid resistance can reduce overall fitness (29) directly through reduced efficiency of the VGSC and associated metabolic costs (30) or indirectly through genetic hitchhiking (31). In addition, under strong selective pressures of pesticide exposure, genetic diversity may become depleted by "genetic erosion," as selection of a few adapted organisms creates genetic bottlenecks (32).…”

Section: Discussion Pyrethroid Resistance Varies Across Species Groupmentioning

confidence: 99%

Multiple origins of pyrethroid insecticide resistance across the species complex of a nontarget aquatic crustacean, Hyalella azteca

Weston

Poynton

Wellborn

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

139

153

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Use of pesticides can have substantial nonlethal impacts on nontarget species, including driving evolutionary change, often with unknown consequences for species, ecosystems, and society. Hyalella azteca, a species complex of North American freshwater amphipods, is widely used for toxicity testing of water and sediment and has frequently shown toxicity due to pyrethroid pesticides. We demonstrate that 10 populations, 3 from laboratory cultures and 7 from California water bodies, differed by at least 550-fold in sensitivity to pyrethroids. The populations sorted into four phylogenetic groups consistent with species-level divergence. By sequencing the primary pyrethroid target site, the voltage-gated sodium channel, we show that point mutations and their spread in natural populations were responsible for differences in pyrethroid sensitivity. At least one population had both mutant and WT alleles, suggesting ongoing evolution of resistance. Although nonresistant H. azteca were susceptible to the typical neurotoxic effects of pyrethroids, gene expression analysis suggests the mode of action in resistant H. azteca was not neurotoxicity but was oxidative stress sustained only at considerably higher pyrethroid concentrations. The finding that a nontarget aquatic species has acquired resistance to pesticides used only on terrestrial pests is troubling evidence of the impact of chronic pesticide transport from land-based applications into aquatic systems. Our findings have farreaching implications for continued uncritical use of H. azteca as a principal species for monitoring and environmental policy decisions.

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Functional and Evolutionary Consequences of Pyrethroid Resistance Mutations in S6 Transmembrane Segments of a Voltage-Gated Sodium Channel

Cited by 52 publications

References 21 publications

Synergistic interaction between two cockroach sodium channel mutations and a tobacco budworm sodium channel mutation in reducing channel sensitivity to a pyrethroid insecticide

Synergistic interaction between two cockroach sodium channel mutations and a tobacco budworm sodium channel mutation in reducing channel sensitivity to a pyrethroid insecticide

Novel sodium channel gene mutations in Blattella germanica reduce the sensitivity of expressed channels to deltamethrin

Multiple origins of pyrethroid insecticide resistance across the species complex of a nontarget aquatic crustacean, Hyalella azteca

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