Calcium-Activated Potassium Channels in Insect Pacemaker Neurons as Unexpected Target Site for the Novel Fumigant Dimethyl Disulfide

Gautier, Hélène; Auger, J.; Legros, Christian; Lapied, Bruno

doi:10.1124/jpet.107.128694

Cited by 25 publications

(17 citation statements)

References 35 publications

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“…It is also well established that DUM neurons are an important component of different motor networks (Burrows and Pflüger, 1995; Baudoux et al, 1998; Mentel et al, 2008; Vierk et al, 2009). Although DUM neurons may be activated by sensory stimuli (e.g., Baudoux and Burrows, 1998; Field et al, 2008; Pflüger et al, 2011; Rand et al, 2012), they are defined by the absence of common somatic synaptic inputs from presynaptic neurons and by their uncommon intrinsic property allowing adequate beating pacemaker activity (Grolleau and Lapied, 2000; Wicher et al, 2001; Defaix and Lapied, 2005; Heidel and Pflüger, 2006; Lavialle-Defaix et al, 2006; Gautier et al, 2008). One of the most important key determinants of the DUM neuron excitability is the action potential threshold.…”

Section: Discussionmentioning

confidence: 99%

Modulation of Low-Voltage-Activated Inward Current Permeable to Sodium and Calcium by DARPP-32 Drives Spontaneous Firing of Insect Octopaminergic Neurosecretory Cells

Lapied

Defaix

Stankiewicz

et al. 2017

Front. Syst. Neurosci.

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Identification of the different intracellular pathways that control phosphorylation/dephosphorylation process of ionic channels represents an exciting alternative approach for studying the ionic mechanisms underlying neuronal pacemaker activity. In the central nervous system of the cockroach Periplaneta americana, octopaminergic neurons, called dorsal unpaired median (DUM; DUM neurons), generate spontaneous repetitive action potentials. Short-term cultured adult DUM neurons isolated from the terminal abdominal ganglion (TAG) of the nerve cord were used to study the regulation of a tetrodotoxin-sensitive low-voltage-activated (LVA) channel permeable to sodium and calcium (Na/Ca), under whole cell voltage- and current-clamp conditions. A bell-shaped curve illustrating the regulation of the amplitude of the maintained current vs. [ATP]i was observed. This suggested the existence of phosphorylation mechanisms. The protein kinase A (PKA) inhibitor, H89 and elevating [cyclic adenosine 3′, 5′ monophosphate, cAMP]i, increased and decreased the current amplitude, respectively. This indicated a regulation of the current via a cAMP/PKA cascade. Furthermore, intracellular application of PP2B inhibitors, cyclosporine A, FK506 and PP1/2A inhibitor, okadaic acid decreased the current amplitude. From these results and because octopamine (OA) regulates DUM neuron electrical activity via an elevation of [cAMP]i, we wanted to know if, like in vertebrate dopaminergic neurons, OA receptor (OAR) stimulation could indirectly affect the current via PKA-mediated phosphorylation of Dopamine- and cAMP-regulated Phosphoprotein-32 (DARPP-32) known to inhibit PP1/2A. Experiments were performed using intracellular application of phospho-DARPP-32 and non-phospho-DARPP-32. Phospho-DARPP-32 strongly reduced the current amplitude whereas non-phospho-DARPP-32 did not affect the current. All together, these results confirm that DARPP-32-mediated inhibition of PP1/2A regulates the maintained sodium/calcium current, which contributes to the development of the pre-depolarizing phase of the DUM neuron pacemaker activity.

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Section: Discussionmentioning

confidence: 99%

Modulation of Low-Voltage-Activated Inward Current Permeable to Sodium and Calcium by DARPP-32 Drives Spontaneous Firing of Insect Octopaminergic Neurosecretory Cells

Lapied

Defaix

Stankiewicz

et al. 2017

Front. Syst. Neurosci.

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“…In other words, PP2B and CaM-kinase II could up-and downregulate INa2 amplitude, respectively. We next tested the effect of caffeine, known to stimulate the release of calcium from intracellular stores (Courjaret et al, 2003;Gautier et al, 2008), on INa2 while maintaining PP2B and/or CaMkinase II inactivated by applying intracellularly 100 nM cyclosporine A and/or 10 M KN-62, respectively. Under these conditions, bath application of caffeine (10 mM) produced stronger effect on INa2 amplitude in the presence of cyclosporine A added in the pipette solution (residual current was 64.0 Ϯ 2.2%, n ϭ 5, compared with 79.8 Ϯ 4.2% recorded in the absence of caffeine, n ϭ 10; Fig.…”

Section: Resultsmentioning

confidence: 99%

How Does Calcium-Dependent Intracellular Regulation of Voltage-Dependent Sodium Current Increase the Sensitivity to the Oxadiazine Insecticide Indoxacarb Metabolite Decarbomethoxylated JW062 (DCJW) in Insect Pacemaker Neurons?

Lavialle-Defaix¹,

Moignot²,

Legros³

et al. 2010

J Pharmacol Exp Ther

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Decarbomethoxylated JW062 (DCJW), the active component of the oxadiazine insecticide (S)-methyl 7-chloro-2,5-dihydro-2-[[(methoxycarbonyl)[4-(trifluoromethoxy)phenyl] amino]carbonyl] indeno[1,2-e][1,3,4]oxadiazine-4a(3H)-carboxylate (DPX-JW062)(indoxacarb), was tested on 2 inward voltage-dependent sodium currents (named INa1 and INa2) expressed in shortterm cultured dorsal unpaired median neurons of the cockroach Periplaneta americana. Under whole-cell voltageclamp conditions, application of DCJW resulted in a biphasic dose-dependent inhibition of the global sodium current amplitude illustrating the differing sensitivity of sodium channels to DCJW. INa2 was less sensitive to DCJW [half-maximal inhibitory concentration (IC 50 ) ϭ 1.6 M] compared with INa1 (IC 50 ϭ 1.7 nM). Although a previous study demonstrated that INa1 was regulated by the cAMP/protein kinase A cascade, we showed that INa2 was mainly regulated in an opposite way by the activation of calcium-calmodulin-dependent protein phosphatase 2B (PP2B) and calcium-calmodulin-dependent protein kinase II (CaM-kinase II). Furthermore, we demonstrated that activation of CaM-kinase II by intracellular calcium via the calcium-calmodulin complex affected the sensitivity of INa2 channels to DCJW. By increasing the intracellular calcium concentration and/or using 1,2-bis(oaminophenoxy)ethane-N,N,NЈ,NЈ-tetraacetic acid (BAPTA) (a calcium chelator), N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide hydrochloride (W7) (a calmodulin inhibitor), cyclosporine A (a PP2B inhibitor), and 1-[N,O-bis(5-isoquinolinesulfonyl)-N-methyl-L-tyrosyl]-4-phenylpiperazine (KN-62) (a CaM-kinase II inhibitor), we revealed that activation of CaMkinase II was involved in the modulation of the voltage dependence of steady-state inactivation and that the CaMkinase II pathway activated by elevation of the intracellular calcium concentration might render INa2 channels approximately 3000-fold more sensitive to DCJW. These results indicated that manipulating specific intracellular signaling pathways involved in the regulation of sodium channels might have fundamental consequences for the sensitivity of insects to insecticides. This finding reveals an exciting research area that could lead to improvement in the efficiency of insecticides.Voltage-dependent sodium channels are critical elements of electrical activity in excitable cells and thus are important targets of diverse neuroactive compounds, including pyrethroids and pyrazoline-type insecticides (Dong, 2007;Soderlund, 2008;Silver et al., 2009). Synthetic pyrethroid insecticides, which are derived from natural compounds (pyrethrins), have been used for more than 40 years and account for 25% of the worldwide insecticide market, because of their potent and rapid insect intoxication, low toxicity for mammals, and lim-B.M. was supported by a doctoral fellowship from the Région Pays de la Loire.Article, publication date, and citation information can be found at http://jpet.aspetjournals.org.

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“…In addition, numerous bacteria and fungi can decompose crucifer tissues and generate DMDS (Gamliel et al 2000). DMDS shows a complex mode of action through mitochondrial dysfunction and the activation of ATP-sensitive potassium channels; it is also a powerful inhibitor of cytochrome oxidase (Dugravot et al 2003;Gautier et al 2007). It was observed to have various fungistatic effects and nematicidal activities in soil environments (Chuankun et al 2004;Gu et al 2007).…”

Section: Introductionmentioning

confidence: 99%

The Effects of Biochar Amendment on Dimethyl Disulfide Emission and Efficacy Against Soil-Borne Pests

Wang

Fang

Yan

et al. 2016

Water Air Soil Pollut

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Biochar can potentially reduce fumigant emissions in agriculture. Dimethyl disulfide (DMDS) is an effective soil fumigant for controlling soil-borne pests. However, it is important to reduce DMDS emissions because the compound has an unpleasant and easily perceived sulfur odor. This study therefore aimed to determine the effects of two types of biochar amendments on DMDS bioactivity and emission, using bioassay methods and soil columns. The efficacy of DMDS for controlling root-knot nematode and Fusarium spp. was not reduced when the biochar used in this study was applied at a rate less than 2 and 0.5 % (on a weight basis), respectively. The biochar with high specific surface area (SSA 113 m −2 g −1 ) reduced the efficacy of DMDS against soil-borne pests more than the low SSA biochar (14 m −2 g −1 ). Increased doses of DMDS were able to offset decreases in the efficacy of DMDS in soils amended with biochars, except for high SSA biochar applied at a rate of 2 %. Biochar amendments applied to the soil surface at shallow depth can significantly reduce DMDS emission to the atmosphere. The results of this study will support decision-making about the practical use of biochar to reduce DMDS emissions.

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Calcium-Activated Potassium Channels in Insect Pacemaker Neurons as Unexpected Target Site for the Novel Fumigant Dimethyl Disulfide

Cited by 25 publications

References 35 publications

Modulation of Low-Voltage-Activated Inward Current Permeable to Sodium and Calcium by DARPP-32 Drives Spontaneous Firing of Insect Octopaminergic Neurosecretory Cells

Modulation of Low-Voltage-Activated Inward Current Permeable to Sodium and Calcium by DARPP-32 Drives Spontaneous Firing of Insect Octopaminergic Neurosecretory Cells

How Does Calcium-Dependent Intracellular Regulation of Voltage-Dependent Sodium Current Increase the Sensitivity to the Oxadiazine Insecticide Indoxacarb Metabolite Decarbomethoxylated JW062 (DCJW) in Insect Pacemaker Neurons?

The Effects of Biochar Amendment on Dimethyl Disulfide Emission and Efficacy Against Soil-Borne Pests

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