1. Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans-Knöll-St 8, D-07745 Jena, Germany
2. Center for Molecular Biomedicine, Institute of Molecular Cell Biology, Friedrich Schiller University, Jena, Nonnenplan 2, D-07743 Jena, Germany
3. Center for Molecular Biomedicine, Department of Biophysics, Friedrich Schiller University Jena, Hans-Knöll-St. 2, D-07745 Jena, Germany

Correspondence to: Dieter Wicher¹ Correspondence and requests for materials should be addressed to D.W. (Email: dwicher@ice.mpg.de).

Abstract

From worm to man, many odorant signals are perceived by the binding of volatile ligands to odorant receptors¹ that belong to the G-protein-coupled receptor (GPCR) family². They couple to heterotrimeric G-proteins, most of which induce cAMP production³. 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 GPCRs⁴, are composed of conventional odorant receptors (for example, Or22a), dimerized with a ubiquitously expressed chaperone protein⁵, such as Or83b in Drosophila⁶. Or83b has a structure akin to GPCRs, but has an inverted orientation in the plasma membrane^{4, 7}. However, G proteins are expressed in insect olfactory receptor neurons⁸, and olfactory perception is modified by mutations affecting the cAMP transduction pathway⁹. 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 Ca²⁺ 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.

1. Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans-Knöll-St 8, D-07745 Jena, Germany
2. Center for Molecular Biomedicine, Institute of Molecular Cell Biology, Friedrich Schiller University, Jena, Nonnenplan 2, D-07743 Jena, Germany
3. Center for Molecular Biomedicine, Department of Biophysics, Friedrich Schiller University Jena, Hans-Knöll-St. 2, D-07745 Jena, Germany

Correspondence to: Dieter Wicher¹ Correspondence and requests for materials should be addressed to D.W. (Email: dwicher@ice.mpg.de).

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