Leucokinin mimetic elicits aversive behavior in mosquito Aedes aegypti (L.) and inhibits the sugar taste neuron.
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.
Department of Entomology, Texas A&M University, College Station, TX 77843;
Hyeogsun
H
Kwon
UMR Evolution, Génomes, Comportement, Ecologie CNRS, Institut de Recherche pour le Développement, Université Paris-Sud, Université Paris-Saclay, F-91198 Gif-sur-Yvette, France;
Moutaz
M
Ali Agha
Department of Entomology, Iowa State University, Ames, IA 50011;
Ryan C
RC
Smith
Insect Control and Cotton Disease Research Unit, Southern Plains Agricultural Research Center, US Department of Agriculture, College Station, TX 77845;
Ronald J
RJ
Nachman
UMR Evolution, Génomes, Comportement, Ecologie CNRS, Institut de Recherche pour le Développement, Université Paris-Sud, Université Paris-Saclay, F-91198 Gif-sur-Yvette, France; AgroParisTech, Université Paris-Saclay, F-75005 Paris, France p-pietrantonio@tamu.edu frederic.marion-poll@agroparistech.fr.
Frédéric
F
Marion-Poll
Department of Entomology, Texas A&M University, College Station, TX 77843; p-pietrantonio@tamu.edu frederic.marion-poll@agroparistech.fr.
Patricia V
PV
Pietrantonio
D000330:Aedes / Q000502:physiology*; D000818:Animals; D003001:Cloning, Molecular; D018076:DNA, Complementary; D005260:Female; D006801:Humans; D007705:Kinins / Q000737:chemistry / Q000494:pharmacology*; D008297:Male; D018613:Microscopy, Confocal; D018716:Molecular Mimicry; D009474:Neurons / Q000502:physiology*; D013395:Sucrose; D013649:Taste
D018076:DNA, Complementary; D007705:Kinins; D013395:Sucrose
chemical target validation; feeding deterrent; neuropeptide GPCR; sensory neuron; sucrose taste