The sugar meal of the African malaria mosquito <i>Anopheles gambiae</i> (Giles) and how deterrent compounds interfere with it: a behavioural and neurophysiological study

Kessler, Sébastien; Vlimant, Michèle; Guérin, Patrick M.

doi:10.1242/jeb.076588

Cited by 43 publications

(51 citation statements)

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“…3A and Figs. S5A, S8A, and S9A), are identical to the long labellar sensilla described in A. aegypti (28,29) and are similar to the long labellar sensilla (trichoid) of Anopheles gambiae (30) and Culiseta inornata (31,32). Accessory cells surrounding sensory neurons immunostained for the Aedae-KR could be the trichogen or tormogen (30,33), because these cells are believed to secrete the dendrite bathing fluid (34,35).…”

Section: Discussionsupporting

confidence: 57%

“…Because A. aegypti prefer sucrose solutions of 100 mM or higher, a 300-mM sucrose solution was chosen for assays (27). Electrophysiological recordings on the long labellar sensillum of female A. gambiae showed that responses of the sucrose receptor cell reached a plateau at sucrose concentrations of 25-292 mM (10% sucrose) (30). We found that kinin analogs of diverse chemical structure inhibited the firing of neurons in response to sucrose in the female labellum (Fig.…”

Section: Discussionmentioning

confidence: 83%

“…Structural modifications of insect kinins, such as the incorporation of Aib and β-amino acids with an additional methylene group (-CH 2 -), render these peptides biostable, because they are protease resistant (8,(10)(11)(12)26). Our hypothesis is that the potent analog 1728 enters the labellar and tarsal sensilla (30) and diffuses through the aqueous sensillum lymph to activate the Aedae-KR expressed in sucrose taste neurons, thereby decreasing sucrose taste perception. We are not certain why analog 1728 elicits fast walk-, fly-, or jump-away behaviors (Movie S1) that are not observed for either analog 1729 or 1460, which also inhibit the sucrose response, although with less potency (Fig.…”

Section: Discussionmentioning

confidence: 98%

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Leucokinin mimetic elicits aversive behavior in mosquito Aedes aegypti (L.) and inhibits the sugar taste neuron

Kwon

Agha

Smith

et al. 2016

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

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Insect kinins (leucokinins) are multifunctional peptides acting as neurohormones and neurotransmitters. In females of the mosquito vector Aedes aegypti (L.), aedeskinins are known to stimulate fluid secretion from the renal organs (Malpighian tubules) and hindgut contractions by activating a G protein-coupled kinin receptor designated "Aedae-KR." We used protease-resistant kinin analogs 1728, 1729, and 1460 to evaluate their effects on sucrose perception and feeding behavior. In no-choice feeding bioassays (capillary feeder and plate assays), the analog 1728, which contains α-amino isobutyric acid, inhibited females from feeding on sucrose. It further induced quick fly-away or walk-away behavior following contact with the tarsi and the mouthparts. Electrophysiological recordings from single long labellar sensilla of the proboscis demonstrated that mixing the analog 1728 at 1 mM with sucrose almost completely inhibited the detection of sucrose. Aedae-KR was immunolocalized in contact chemosensory neurons in prothoracic tarsi and in sensory neurons and accessory cells of long labellar sensilla in the distal labellum. Silencing Aedae-KR by RNAi significantly reduced gene expression and eliminated the feeding-aversion behavior resulting from contact with the analog 1728, thus directly implicating the Aedae-KR in the aversion response. To our knowledge, this is the first report that kinin analogs modulate sucrose perception in any insect. The aversion to feeding elicited by analog 1728 suggests that synthetic molecules targeting the mosquito Aedae-KR in the labellum and tarsi should be investigated for the potential to discover novel feeding deterrents of mosquito vectors.neuropeptide GPCR | sucrose taste | sensory neuron | chemical target validation | feeding deterrent

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Section: Discussionsupporting

confidence: 57%

Section: Discussionmentioning

confidence: 83%

Section: Discussionmentioning

confidence: 98%

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Leucokinin mimetic elicits aversive behavior in mosquito Aedes aegypti (L.) and inhibits the sugar taste neuron

Kwon

Agha

Smith

et al. 2016

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

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“…In most of these cases, the presence of adenosine nucleotides, such as ATP or other similar purinergic compounds, seemed to be decisive for food acceptance (Friend, 1965;Friend and Smith, 1971;Smith and Friend, 1982;Galun et al, 1985). On the contrary, less information is available about the existence of anti-feedant compounds for haematophagous insects and their influence on food preference (Ignell et al, 2010;Kessler et al, 2013). New data in mosquitoes showed the occurrence of Drosophila orthologous gustatory receptor genes (Kent et al, 2008;Bohbot et al, 2014;Sparks et al, 2014) that might share a similar function, such as the one required for caffeine detection (Sparks et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Bitter stimuli modulates the feeding decision of a blood-sucking insect via two sensory inputs

Pontes

Minoli

Insaurralde

et al. 2014

Journal of Experimental Biology

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The gustatory system of animals is involved in food quality assessment and controls the feeding decision of an individual confronted with a potential alimentary source. Triatomines are haematophagous insects that feed on vertebrate blood. Once they reach a potential host, they walk over the host skin searching for an adequate site to pierce. Then, they insert their stylets and take a first sampling gorge to decide whether food is acceptable. Our work reveals that the presence of bitter compounds inhibits the feeding behavior of these bugs. Firstly, triatomines decreased their feeding behavior if substrates spread with quinine or caffeine were detected by external receptors localized exclusively in the antennae. Morphological inspections along with electrophysiological recordings revealed the existence of four gustatory sensilla located in the tip of the antenna that respond to both bitter tastants. The absence of these bitter detectors by antennal ablation reversed the observed feeding inhibition evoked by bitter compounds. Secondly, once triatomines pumped the first volume of food with bitter compounds (quinine, caffeine, berberine, salicin), a decrease in their feeding behavior was observed. Morphological inspections revealed the existence of eight gustatory sensilla located in the pharynx that might be responsible for the internal bitter detection. Finally, we found that a brief pre-exposure to bitter compounds negatively modulates the motivation of bugs to feed on an appetitive solution. Results presented here highlight the relevance of bitter taste perception in the modulation of the feeding behavior of a blood-sucking insect.

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“…Less is known about the effects of quinidine on insect feeding. This compound inhibits sucrose stimulated feeding in the mosquito, Anopheles gambiae, at concentrations as low as 0.1 mM with dynamics similar to that of quinine (Kessler et al, 2013). Quinidine deters honeybees in feeding choice assays with an ED 50 of 0.076 mM (Detzel & Wink, 1993).…”

Section: Figmentioning

confidence: 99%

Pharmacological analysis of the feeding response of codling moth (Cydia pomonella; Lepidoptera: Tortricidae) neonates to bitter compounds

Pszczółkowski¹

2017

Eur. J. Entomol.

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Abstract. Feeding in codling moth neonate caterpillars was inhibited by 0.67 mM and 2.24 mM concentrations of denatonium benzoate. This inhibitory effect was abolished by phospholipase C inhibitor, U-73122 and the phosphodiesterase inhibitor, Rolipram. Quinine and quinidine did not have inhibitory effects at concentrations as high as 1.64 mM and 0.43 mM, respectively. The inhibitory effect of denatonium was partially reversed in the presence of the calcium ion chelator, EGTA, at concentrations ranging from 2.5 μM to 250 μM. These results indicate that transduction of the taste of denatonium in codling moth neonates relies on signalling pathways that involve phospholipase C, phosphodiesterase and calcium ion infl ux into cells.

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The sugar meal of the African malaria mosquito Anopheles gambiae (Giles) and how deterrent compounds interfere with it: a behavioural and neurophysiological study

Cited by 43 publications

References 54 publications

Leucokinin mimetic elicits aversive behavior in mosquito Aedes aegypti (L.) and inhibits the sugar taste neuron

Leucokinin mimetic elicits aversive behavior in mosquito Aedes aegypti (L.) and inhibits the sugar taste neuron

Bitter stimuli modulates the feeding decision of a blood-sucking insect via two sensory inputs

Pharmacological analysis of the feeding response of codling moth (Cydia pomonella; Lepidoptera: Tortricidae) neonates to bitter compounds

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