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A functional agonist of insect olfactory receptors : Behavior, physiology and structure

Batra, Srishti; Corcoran, Jacob LU ; Zhang, Dan Dan LU ; Pal, Pramit; Umesh, K. P.; Kulkarni, Renuka; Löfstedt, Christer LU ; Sowdhamini, Ramanathan and Olsson, Shannon B. (2019) In Frontiers in Cellular Neuroscience 13.
Abstract

Chemical signaling is ubiquitous and employs a variety of receptor types to detect the cacophony of molecules relevant for each living organism. Insects, our most diverse taxon, have evolved unique olfactory receptors with as little as 10% sequence identity between receptor types. We have identified a promiscuous volatile, 2-methyltetrahydro-3-furanone (coffee furanone), that elicits chemosensory and behavioral activity across multiple insect orders and receptors. In vivo and in vitro physiology showed that coffee furanone was detected by roughly 80% of the recorded neurons expressing the insect-specific olfactory receptor complex in the antenna of Drosophila melanogaster, at concentrations similar to other known, and less promiscuous,... (More)

Chemical signaling is ubiquitous and employs a variety of receptor types to detect the cacophony of molecules relevant for each living organism. Insects, our most diverse taxon, have evolved unique olfactory receptors with as little as 10% sequence identity between receptor types. We have identified a promiscuous volatile, 2-methyltetrahydro-3-furanone (coffee furanone), that elicits chemosensory and behavioral activity across multiple insect orders and receptors. In vivo and in vitro physiology showed that coffee furanone was detected by roughly 80% of the recorded neurons expressing the insect-specific olfactory receptor complex in the antenna of Drosophila melanogaster, at concentrations similar to other known, and less promiscuous, ligands. Neurons expressing specialized receptors, other chemoreceptor types, or mutants lacking the complex entirely did not respond to this compound. This indicates that coffee furanone is a promiscuous ligand for the insect olfactory receptor complex itself and did not induce non-specific cellular responses. In addition, we present homology modeling and docking studies with selected olfactory receptors that suggest conserved interaction regions for both coffee furanone and known ligands. Apart from its physiological activity, this known food additive elicits a behavioral response for several insects, including mosquitoes, flies, and cockroaches. A broad-scale behaviorally active molecule non-toxic to humans thus has significant implications for health and agriculture. Coffee furanone serves as a unique tool to unlock molecular, physiological, and behavioral relationships across this diverse receptor family and animal taxa.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Behavior, Electrophysiology, Heterologous expression, Molecular docking, Olfaction, Olfactory receptors
in
Frontiers in Cellular Neuroscience
volume
13
publisher
Frontiers
external identifiers
  • scopus:85066940024
ISSN
1662-5102
DOI
10.3389/fncel.2019.00134
language
English
LU publication?
yes
id
b63b0c51-79a9-4a3e-a8ae-0d01affe06d2
date added to LUP
2019-06-19 09:39:09
date last changed
2019-06-19 12:56:17
@article{b63b0c51-79a9-4a3e-a8ae-0d01affe06d2,
  abstract     = {<p>Chemical signaling is ubiquitous and employs a variety of receptor types to detect the cacophony of molecules relevant for each living organism. Insects, our most diverse taxon, have evolved unique olfactory receptors with as little as 10% sequence identity between receptor types. We have identified a promiscuous volatile, 2-methyltetrahydro-3-furanone (coffee furanone), that elicits chemosensory and behavioral activity across multiple insect orders and receptors. In vivo and in vitro physiology showed that coffee furanone was detected by roughly 80% of the recorded neurons expressing the insect-specific olfactory receptor complex in the antenna of Drosophila melanogaster, at concentrations similar to other known, and less promiscuous, ligands. Neurons expressing specialized receptors, other chemoreceptor types, or mutants lacking the complex entirely did not respond to this compound. This indicates that coffee furanone is a promiscuous ligand for the insect olfactory receptor complex itself and did not induce non-specific cellular responses. In addition, we present homology modeling and docking studies with selected olfactory receptors that suggest conserved interaction regions for both coffee furanone and known ligands. Apart from its physiological activity, this known food additive elicits a behavioral response for several insects, including mosquitoes, flies, and cockroaches. A broad-scale behaviorally active molecule non-toxic to humans thus has significant implications for health and agriculture. Coffee furanone serves as a unique tool to unlock molecular, physiological, and behavioral relationships across this diverse receptor family and animal taxa.</p>},
  articleno    = {134},
  author       = {Batra, Srishti and Corcoran, Jacob and Zhang, Dan Dan and Pal, Pramit and Umesh, K. P. and Kulkarni, Renuka and Löfstedt, Christer and Sowdhamini, Ramanathan and Olsson, Shannon B.},
  issn         = {1662-5102},
  keyword      = {Behavior,Electrophysiology,Heterologous expression,Molecular docking,Olfaction,Olfactory receptors},
  language     = {eng},
  month        = {04},
  publisher    = {Frontiers},
  series       = {Frontiers in Cellular Neuroscience},
  title        = {A functional agonist of insect olfactory receptors : Behavior, physiology and structure},
  url          = {http://dx.doi.org/10.3389/fncel.2019.00134},
  volume       = {13},
  year         = {2019},
}