Abstract
Seven-transmembrane receptors typically mediate olfactory signal transduction by coupling to G-proteins. Although insect odorant receptors have seven transmembrane domains like G-protein coupled receptors, they have an inverted membrane topology, constituting a key difference between the olfactory systems of insects and other animals. While heteromeric insect ORs form ligand-activated non-selective cation channels in recombinant expression systems, the evidence for an involvement of cyclic nucleotides and G-proteins in odor reception is inconsistent. We addressed this question in vivo by analyzing the role of G-proteins in olfactory signaling using electrophysiological recordings. We found that Gαs plays a crucial role for odorant induced signal transduction in OR83b expressing olfactory sensory neurons, but not in neurons expressing CO2 responsive proteins GR21a/GR63a. Moreover, signaling of Drosophila ORs involved Gαs also in a heterologous expression system. In agreement with these observations was the finding that elevated levels of cAMP result in increased firing rates, demonstrating the existence of a cAMP dependent excitatory signaling pathway in the sensory neurons. Together, we provide evidence that Gαs plays a role in the OR mediated signaling cascade in Drosophila.
Highlights
Mammalian odorant receptors (OR) comprise the largest family of seven-transmembrane spanning G-protein-coupled receptors which are characterized by extracellular N- and intracellular Ctermini [1]
Drosophila ORs were identified by bioinformatic strategies to contain seven transmembrane domains, recent experimental investigations have revealed that the membrane topology of Drosophila ORs is distinct from conventional G-protein-coupled receptors (GPCRs), with the N-terminus of these receptors located in the cytoplasm [13]
Since they had been categorized as GPCRs some time ago, G-protein signaling has been investigated in odor elicited activation of insect neurons, but conclusive genetic and biochemical evidence whether insect ORs couple to G-proteins is missing
Summary
Mammalian odorant receptors (OR) comprise the largest family of seven-transmembrane spanning G-protein-coupled receptors which are characterized by extracellular N- and intracellular Ctermini [1]. OR proteins are localized in the cilia of the olfactory sensory neurons where they stimulate a Gaolf/cAMP-mediated signal transduction cascade leading to neuronal depolarization [2,3]. Flies have considerably fewer OR genes than vertebrates, most of which express between 600–1300 ORs [5]. One key difference is the ubiquitously expressed insect receptor OR83b, which is conserved across insect species [7,8,9]. OR83b interacts with conventional ORs and is essential to transport them to the sensory cilia [10,11,12]. Solely ionotropic, and G-protein independent currents were described by Sato et al [14], non-selective cation currents activated by means of an ionotropic and a metabotropic pathway, with OR83b being directly activated by intracellular cAMP or cGMP, have been described in a study by Wicher et al [16]
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