The role of the coreceptor Orco in insect olfactory transduction

Abstract

Insects sense odorants with specialized odorant receptors (ORs). Each antennal olfactory receptor neuron expresses one OR with an odorant binding site together with a conserved coreceptor called Orco which does not bind odorants. Orco is necessary for localization of ORs to dendritic membranes and, thus, is essential for odorant detection. It forms a spontaneously opening cation channel, activated via phosphorylation by protein kinase C. Thereafter, Orco is also activated via cyclic adenosine monophosphate (cAMP). Orco forms homo-as well as heteromers with ORs with unknown stoichiometry. Contradictory publications suggest different mechanisms of olfactory transduction. On the one hand, evidence accumulates for the employment of more than one G protein-coupled olfactory transduction cascade in different insects. On the other hand, results from other studies suggest that the OR-Orco complex functions as an odorant-gated cation channel mediating ionotropic signal transduction. This review analyzes conflicting hypotheses concerning the role of Orco in insect olfactory transduction. In conclusion, in situ studies in hawkmoths falsify the hypothesis that Orco underlies odorant-induced ionotropic signal transduction in all insect species. Instead, Orco forms a metabotropically gated, slow cation channel which controls odorant response threshold and kinetics of the sensory neuron.

Odor induced cAMP production in Drosophila melanogaster olfactory sensory neurons

“…sensitivity, are regulated by multiple intracellular signaling cascades (Nakagawa and Vosshall, 2009;Wicher, 2015). The second messenger 3′,5′-cyclic adenosine monophosphate (cAMP) is an activating ligand for Orco channels (Wicher et al, 2008;Stengl, 2010;Stengl and Funk, 2013) and has been shown to enhance the activity of olfactory sensory neurons (OSNs) that express ORs (Olsson et al, 2011;Getahun et al, 2013). Insect OSNs possess the cellular machinery required to produce cAMP (Iourgenko and Levin, 2000;Boto et al, 2010) and disruption of this signaling cascade has been reported to affect the functional properties of OSNs (Martín et al, 2001;Gomez-Diaz et al, 2004;Deng et al, 2011).…”

Olfactory Signaling in Insects

“…17 The requirement of Orco activation for OR sensitization was already mentioned above. 60 A possible role of Orco as pacemaker channel was discussed 80 and observed for pheromone signaling in Manduca. 58 For Drosophila, this view could not be supported.…”

The Two Main Olfactory Receptor Families in Drosophila, ORs and IRs: A Comparative Approach

“…For example, in a lepidopteran, the crepuscular hawk moth, Manduca sexta , there is circadian control through octopamine (OA) over the olfactory metabotropic transduction of pheromones (Schendzielorz et al, 2015). OA could act on ORCO, which has been suggested to be a hormone-controlled pacemaker channel controlling spontaneous activity, threshold and temporal resolution of pheromone detection (Stengl, 2010; Stengl and Funk, 2013). In this species, no evidence of ORCO-based ionotropic signal transduction cascade has been found (Nolte et al, 2013, 2016).…”