The diverse small proteins called odorant-binding proteins

Abstract

The term 'odorant-binding proteins (Obps)' is used to refer to a large family of insect proteins that are exceptional in their number, abundance and diversity. The name derives from the expression of many family members in the olfactory system of insects and their ability to bind odorants in vitro. However, an increasing body of evidence reveals a much broader role for this family of proteins. Recent results also provoke interesting questions about their mechanisms of action, both within and outside the olfactory system. Here we describe the identification of the first Obps and some cardinal properties of these proteins. We then consider their function, discussing both the prevailing orthodoxy and the increasing grounds for heterodox views. We then examine these proteins from a broader perspective and consider some intriguing questions in need of answers.

Keywords: Drosophila; antenna; insect; odorant-binding protein; olfaction.

Figure 1.

Obps are numerous and widely distributed across insects. The number of annotated Obp genes is shown for a variety of insects.

Figure 2.

Structure of an Obp. Obp1 of Aedes aegypti is visualized with six α-helices (α1–6) and three disulfide linkages (DS1–3) labelled. Adapted from [18].

Figure 3.

Expression of Obps in sensilla. (a) A typical olfactory sensillum. Auxiliary cells at the base of the sensillum are shown in blue and purple. Olfactory receptor neurons (ORNs) are in grey. Obps are synthesized and secreted into the sensillar lymph by auxiliary cells. The sensillum contains pores that allow odorants to enter and bind to olfactory receptors on the ORN dendrites. Adapted from [13,21,22]. (b) Immuno-electron microscopy of a cross-section from an Antheraea polyphemus trichoid sensillum, demonstrating the density of Obp labelling within the sensillar lymph. Scale bar, 1 µm. Adapted from [20]. (c) Immuno-electron microscopy of a longitudinal section from Drosophila trichoid sensilla labelled with anti-Obp83a. Scale bar, 1 µm. Adapted from [23]. (d) Map of highly abundant Obps expressed in antennal basiconic sensilla in Drosophila.

Figure 4.

Standard model of Obp function in olfactory sensilla. The prevailing model of Obp function is that Obps bind odorants and carry them through the sensillar lymph to odour receptors in the membranes of ORN dendrites.

Figure 5.

Results not predicted by the standard model. (a) Or22a expressed in Sf9 cells responds to a variety of odorants in the absence of an Obp. Adapted from [33]. (b) Similarity of the response profile of Or7a in the Drosophila ‘empty neuron’ (i) to the profile of Or7a in the ab4A neuron (ii) in which Or7a is endogenously expressed. The profiles are very similar despite the different roster of Obps to which the two neurons have access. Adapted from [34]. (c) A mutant ab8 sensillum depleted of abundant Obps did not show a decrease in odorant response compared to a control ab8 sensillum; in fact, the mutant response is greater for several odorants. *p < 0.05, **p < 0.01. Adapted from [21]. (d) Mutant flies lacking Obp59a exhibit a reduced preference for regions of higher humidity. ****p < 0.0001. Adapted from [35].