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      Insect olfaction from model systems to disease control

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      Journal: Proceedings of the National Academy of Sciences
      Publisher: Proceedings of the National Academy of Sciences

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          Abstract

          Great progress has been made in the field of insect olfaction in recent years. Receptors, neurons, and circuits have been defined in considerable detail, and the mechanisms by which they detect, encode, and process sensory stimuli are being unraveled. We provide a guide to recent progress in the field, with special attention to advances made in the genetic model organism Drosophila. We highlight key questions that merit additional investigation. We then present our view of how recent advances may be applied to the control of disease-carrying insects such as mosquitoes, which transmit disease to hundreds of millions of people each year. We suggest how progress in defining the basic mechanisms of insect olfaction may lead to means of disrupting host-seeking and other olfactory behaviors, thereby reducing the transmission of deadly diseases.

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          Insect olfactory receptors are heteromeric ligand-gated ion channels.

          Koji Sato, Maurizio Pellegrino, Takao Nakagawa … (2008)
          In insects, each olfactory sensory neuron expresses between one and three ligand-binding members of the olfactory receptor (OR) gene family, along with the highly conserved and broadly expressed Or83b co-receptor. The functional insect OR consists of a heteromeric complex of unknown stoichiometry but comprising at least one variable odorant-binding subunit and one constant Or83b family subunit. Insect ORs lack homology to G-protein-coupled chemosensory receptors in vertebrates and possess a distinct seven-transmembrane topology with the amino terminus located intracellularly. Here we provide evidence that heteromeric insect ORs comprise a new class of ligand-activated non-selective cation channels. Heterologous cells expressing silkmoth, fruitfly or mosquito heteromeric OR complexes showed extracellular Ca2+ influx and cation-non-selective ion conductance on stimulation with odorant. Odour-evoked OR currents are independent of known G-protein-coupled second messenger pathways. The fast response kinetics and OR-subunit-dependent K+ ion selectivity of the insect OR complex support the hypothesis that the complex between OR and Or83b itself confers channel activity. Direct evidence for odorant-gated channels was obtained by outside-out patch-clamp recording of Xenopus oocyte and HEK293T cell membranes expressing insect OR complexes. The ligand-gated ion channel formed by an insect OR complex seems to be the basis for a unique strategy that insects have acquired to respond to the olfactory environment.
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            Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels.

            Dieter Wicher, Ronny Schäfer, René Bauernfeind … (2008)
            From worm to man, many odorant signals are perceived by the binding of volatile ligands to odorant receptors that belong to the G-protein-coupled receptor (GPCR) family. They couple to heterotrimeric G-proteins, most of which induce cAMP production. This second messenger then activates cyclic-nucleotide-gated ion channels to depolarize the olfactory receptor neuron, thus providing a signal for further neuronal processing. Recent findings, however, have challenged this concept of odorant signal transduction in insects, because their odorant receptors, which lack any sequence similarity to other GPCRs, are composed of conventional odorant receptors (for example, Or22a), dimerized with a ubiquitously expressed chaperone protein, such as Or83b in Drosophila. Or83b has a structure akin to GPCRs, but has an inverted orientation in the plasma membrane. However, G proteins are expressed in insect olfactory receptor neurons, and olfactory perception is modified by mutations affecting the cAMP transduction pathway. Here we show that application of odorants to mammalian cells co-expressing Or22a and Or83b results in non-selective cation currents activated by means of an ionotropic and a metabotropic pathway, and a subsequent increase in the intracellular Ca(2+) concentration. Expression of Or83b alone leads to functional ion channels not directly responding to odorants, but being directly activated by intracellular cAMP or cGMP. Insect odorant receptors thus form ligand-gated channels as well as complexes of odorant-sensing units and cyclic-nucleotide-activated non-selective cation channels. Thereby, they provide rapid and transient as well as sensitive and prolonged odorant signalling.
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              A spatial map of olfactory receptor expression in the Drosophila antenna.

              L B Vosshall, H Amrein, P S Morozov … (1999)
              Insects provide an attractive system for the study of olfactory sensory perception. We have identified a novel family of seven transmembrane domain proteins, encoded by 100 to 200 genes, that is likely to represent the family of Drosophila odorant receptors. Members of this gene family are expressed in topographically defined subpopulations of olfactory sensory neurons in either the antenna or the maxillary palp. Sensory neurons express different complements of receptor genes, such that individual neurons are functionally distinct. The isolation of candidate odorant receptor genes along with a genetic analysis of olfactory-driven behavior in insects may ultimately afford a system to understand the mechanistic link between odor recognition and behavior.
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                Author and article information

                Journal
                Title: Proceedings of the National Academy of Sciences
                Abbreviated Title: Proc Natl Acad Sci USA
                Publisher: Proceedings of the National Academy of Sciences
                ISSN (Print): 0027-8424
                ISSN (Electronic): 1091-6490
                Publication date Created: August 09 2011
                Publication date Created: August 09 2011
                Publication date (Print): August 09 2011
                Publication date (Electronic): July 11 2011
                Volume: 108
                Issue: 32
                Pages: 12987-12995
                Article
                DOI: 10.1073/pnas.1103472108
                PMC ID: 3156210
                PubMed ID: 21746926
                SO-VID: f4dba696-a42a-43ec-a8f5-01313cee2855
                Copyright © © 2011
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