Ionotropic and metabotropic mechanisms in chemoreception: 'chance or design'?

Abstract

Chemosensory receptors convert an enormous diversity of chemical signals from the external world into a common language of electrical activity in the brain. Mammals and insects use several families of transmembrane receptor proteins to recognize distinct classes of volatile and non-volatile chemicals that are produced by conspecifics or other environmental sources. A comparison of the signalling mechanisms of mammalian and insect receptors has revealed an unexpected functional distinction: mammals rely almost exclusively on metabotropic ligand-binding receptors, which use second messenger signalling cascades to indirectly activate ion channels, whereas insects use ionotropic receptors, which are gated directly by chemical stimuli, thereby leading to neuronal depolarization. In this review, we consider possible reasons for this dichotomy, taking into account biophysical, cell biological, ecological and evolutionary influences on how information is extracted from chemosensory cues by these animal classes.

Figure 1

The main chemosensory organs, receptors and putative ligands in the mouse and the fruit fly. The image of the mouse head was adapted from Matsunami & Amrein (2003). FPRs, formyl peptide receptors; GRs, gustatory receptors; IRs, ionotropic receptors; ORs, odorant receptors; T1Rs, taste receptors type 1; T2Rs, taste receptors type 2; TAARs, trace amine-associated receptors; V1Rs, vomeronasal receptors type 1; V2Rs, vomeronasal receptors type 2.

Figure 2

Signalling mechanisms of mammalian and insect odorant receptors. A schematic of the molecular basis of olfactory signal transduction in the mouse and fruit fly. ACIII, type III adenylyl cyclase; ATP, adenosine triphosphate; cAMP, cyclic adenosine monophosphate; ANO2, anoctamin 2 channel; CNG, cyclic nucleotide-gated channel;.Gα_olf, olfactory G protein α-subunit; OR, odorant receptor.

Ana Florencia Silbering

Richard Benton