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PLoS One
2011 Jan 01;66:e21785. doi: 10.1371/journal.pone.0021785.
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Functional characterization of the octenol receptor neuron on the maxillary palps of the yellow fever mosquito, Aedes aegypti.
Grant AJ
,
Dickens JC
.
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BACKGROUND: 1-Octen-3-ol (octenol) is a common attractant released by vertebrates which in combination with carbon dioxide (CO(2)) attracts hematophagous arthropods including mosquitoes. A receptor neuron contained within basiconic sensilla on the maxillary palps of adult mosquitoes responds selectively to 1-octen-3-ol. Recently, an odorant receptor (AaegOR8) known to occur on the maxillary palps was expressed in a heterologous system and demonstrated to be selectively sensitive to (R)-(-)-1-octen-3-ol, one of two enantiomeric forms. Lesser responses were elicited by stimulation with the (S)-enantiomer and various structural analogs.
METHODOLOGY/PRINCIPAL FINDINGS: Here we characterize the specificity of the octenol receptor neuron in the yellow fever mosquito, Aedes aegypti (L.), in vivo using single cell recordings. The octenol neuron is exquisitely sensitive to (R)-(-)-1-octen-3-ol; comparable responses to (S)-(+)-1-octen-3-ol were elicited only at stimulus doses over 100× that required for the (R)-enantiomer. An intermediate response closer to that elicited by the (R)-(-)-enantiomer was elicited by racemic 1-octen-3-ol. Small structural changes in (R)-(-)-1-octen-3-ol resulted in large decreases in responses. Increases in spike activity were also elicited in the octenol neuron by 2-undecanone, a known repellent; other repellents (DEET, IR3535 and picaridin) were inactive.
CONCLUSIONS/SIGNIFICANCE: The results of our electrophysiological studies of the octenol receptor neuron in vivo approximates results of a previous study of the octenol receptor (AaegOR8 with its obligate partner Aaeg\ORco) expressed heterologously in Xenopus oocytes. By comparison of our current results with those of the heterologous expression study, we conclude that specificity of the octenol receptor neuron can be explained largely by characteristics of the OR alone without other associated proteins present in vivo. Our findings show that repellents may have specific stimulatory effects on receptor neurons and support the notion of repellents as modulators of mosquito odorant receptor activity.
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21738794
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Figure 1. Chiral selectivity of the “C” neuron of maxillary palp basiconic sensilla.(A) Spontaneous activity of neurons associated with a basiconic sensillum on the maxillary palp of a female Ae. aegypti. Note the presence of three spike heights: A = largest spike is responsive to CO2, B = intermediate spike, and C = smallest amplitude spike is reliably activated by (R)-(−)-1-octen-3-ol. Response of “C” neuron is to a low dose of (R)-(−)-1-octen-3-ol. (B) Structure of enantiomers of 1-octen-3-ol: (R)-(−)-1-octen-3-ol and (S)-(+)-1-octen-3-ol. (C) Electrophysiological responses from an individual basiconic sensillum to a 1 sec exposure to increasing stimulus loads of the enantiomers of 1-octen-3-ol. Note at higher loads of (R)-(−)-1-octen-3-ol spikes from “C” neuron are not easily discerned from baseline. (D) Dose-response curves constructed from mean responses of “C” neurons to increasing stimulus loads of racemic 1-octen-3-ol (Rac-1-octen-3-ol, n = 4)), and its component enantiomers, (R)-(−)-1-octen-3-ol (n = 5), and (S)-(+)-1-octen-3-ol (n = 4). Points represented are mean ± SEM.
Figure 2. (R)-(−)-1-octen-3-ol strongly preferred over related analogs.Dose-response relationships from the “C” neuron in maxillary palp sensilla of female Ae. aegypti in response to increasing doses of (R)-(−)-1-octen-3-ol (n = 5) and structurally similar chemicals. (A) Movement of chiral center from “3” to “4” position, 1-octen-4-ol (n = 4). (B) Changes in carbon chain length: 1-hepten-3-ol (n = 4) and 1-nonen-3-ol (n = 3). (C) Change in functional group with loss of chiral center, 1-octen-3-one (n = 4). (D) Saturation of double bond, 3-octanol (n = 4). Points represented are mean ± SEM.
Figure 3. 2-Undecanone, a known repellent, activates the “C” neuron.(A) Dose-response relationship from the “C” neuron in maxillary palp sensilla of female Ae. aegypti in response to increasing doses of (R)-(−)-1-octen-3-ol (n = 5) and 2-undecanone (n = 6). (B) Electrophysiological responses from an individual basiconic sensillum on the maxillary palp of a female Ae. aegypti to a 1 sec exposure to: 1. hexane solvent, 2. 2-undecanone 5000 µg, 3. DEET 5000 µg, and 4. (R)-(−)-1-octen-3-ol 0.05 µg. (C) Mean number of spikes (±SEM; n = 5) from “C” neurons of female Ae. aegypti basiconic sensilla to stimulation with 5000 µg doses of hexanes, 2-undecanone, DEET, IR3535, picaridin and to 0.05 µg dose of (R)-(−)-1-octen-3-ol. Points represented are mean ± SEM. “A”, “B”, and “C” with arrows designate three spike classes present in recordings from the basiconic sensilla.
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