Odorant and pheromone receptors in insects

Abstract

Since the emergence of the first living cells, survival has hinged on the ability to detect and localize chemicals in the environment. Modern animal species ranging from insects to mammals express large odorant receptor repertoires to detect the structurally diverse array of volatile molecules important for survival. Despite the essential nature of chemical detection, there is surprising diversity in the signaling mechanisms that different species use for odorant detection. In vertebrates, odorant receptors are classical G-protein coupled, seven transmembrane receptors that activate downstream effector enzymes that, in turn, produce second messengers that open ion channels. However, recent work reveals that insects have adopted different strategies to detect volatile chemicals. In Drosophila, the odorant receptors, predicted to have seven transmembrane domains, have reversed membrane topology compared to classical G-protein coupled receptors. Furthermore, insect odorant receptors appear to form odorant-gated ion channels. Pheromone detection in insects is even more unusual, utilizing soluble, extracellular receptors that undergo conformational activation. These alternate olfactory signaling strategies are discussed in terms of receptor design principles.

Keywords: odorant; odorant binding proteins; odorant receptor; olfaction; pheromone.

Figure 1

Model of vertebrate olfactory signal transduction. In the absence of odorant (left), the odorant receptor (OR) is bound to the GDP-bound form of G_olf. Activation by odorants (right) causes exchange of GDP for GTP by the alpha subunit of G_olf, which activates adenylyl cyclase (AC) to produce cAMP. cAMP binds cyclic nucleotide-gated ion channels that conduct sodium and calcium ions into the neuron. The calcium ions bind calcium-activated chloride channels that allow chloride ions to exit the neurons, further depolarizing the neuron.

Figure 2

Two possible models for odorant-gated channels. Left, possible role for G-protein mediated cyclic nucleotides in Or83b activation. Right, direct odorant gating of the Or/Or83b receptor complex. The major monovalent cation in the sensillum lymph is potassium.

Figure 3

Model for pheromone detection. The extracellular receptor LUSH binds cVA pheromone and undergoes an activating conformational shift. Activated LUSH binds SNMP and relieves SNMP-mediated inhibition of the Or67d/Or83b receptor complex, allowing cations to enter the neurons.