Coexpression of Two Functional Odor Receptors in One Neuron

Abstract

One of the most fundamental tenets in the field of olfaction is that each olfactory receptor neuron (ORN) expresses a single odorant receptor. However, the one receptor-one neuron principle is difficult to establish rigorously. Here we construct a receptor-to-neuron map for an entire olfactory organ in Drosophila and find that two receptor genes are coexpressed in one class of ORN. Both receptors are functional in an in vivo expression system, they are only 16% identical in amino acid sequence, and the genes that encode them are unlinked. Most importantly, their coexpression has been conserved for >45 million years. Expression of multiple odor receptors in a cell provides an additional degree of freedom for odor coding.

Activity plays a role in eliminating olfactory sensory neurons expressing multiple odorant receptors in the mouse septal organ

“…We observed colocalization from all probe combinations tested, suggesting that coexpression occurs randomly among these receptors. This is distinct from the previous reports in rat (Rawson et al, 2000), zebrafish (Sato et al, 2007), and Drosophila (Goldman et al, 2005), in which certain receptors are coexpressed in a subset of OSNs all the time or with a high tendency. Second, there are additional ORs (identified or unidentified) expressed in the septal organ (Kaluza et al, 2004;Tian and Ma, 2004).…”

The molecular basis of CO 2 reception in Drosophila

“…There is precedence for heterodimerization of Or proteins (26,27), but not Gr proteins. Most receptors of the Or family determine the ligand-specificity of the ORN in which they are expressed (16)(17)(18) but are believed to require Or83b as a coreceptor for efficient transport and/or stabilization at the membrane (19,26,27). Based on our results we cannot determine whether both Gr21a and Gr63a act directly in ligand binding and/or signaling, or whether one of them acts as a cofactor in a manner analogous to Or83b.…”

“…In most ORN classes, a single Or gene defines the odorant response profile (16)(17)(18). Typically, the Or gene is coexpressed with the noncanonical receptor Or83b, an atypical family member that is required for efficient localization of the canonical Or receptor to the dendrites (19).…”

Olfaction in vector-host interactions

“…Not surprisingly, the first identified insect ORs were found in Drosophila (Clyne et al 1999, Gao and Chess 1999, Vosshall et al 1999. Functional validation of the role of DORs as bona fide ORs came some time later through extensive use of numerous heterologous expression systems (Dobritsa et al 2003, Goldman et al 2005, Hallem et al 2004b, Kreher et al 2005, Wetzel et al 2001. As was the case with the majority of gene families, these initial studies in Drosophila opened the door for similar studies in disease vector insects.…”

“…With the sequencing of the Anopheles genome in 2002 (Holt et al 2002) much work has focused on An. gambiae (Goldman et al 2005, Hill et al 2002. Recent published work has begun to unravel and identify the molecular nature of the receptor proteins involved in CO 2 detection.…”