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Tuning Insect Odorant Receptors

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Tuning Insect Odorant Receptors PERSPECTIVE published: 05 April 2018 doi: 10.3389/fncel.2018.00094 Tuning Insect Odorant Receptors Dieter Wicher* Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology (MPG), Jena, Germany Among the insect olfactory receptors the odorant receptors (ORs) evolved in parallel to the onset of insect flight. A special property of this receptor type is the capability to adjust sensitivity of odor detection according to previous odor contacts. This article presents a current view on regulatory processes affecting the performance of ORs and proposes a model of mechanisms contributing to OR sensitization. Keywords: chemoreception, olfaction, ionotropic receptor, odorant receptor, receptor kinase, GPCR, intracellular signaling INTRODUCTION The performance of membrane proteins such as ion channels or receptors is dynamically adjusted according to changing physiological requirements. Olfactory receptors have to detect odors in a wide range of concentrations, from faint filaments at larger distance from the source to high concentrated and permanent presence near the source. In mammals, the olfactory receptors for general odors are G protein coupled receptors (GPCRs; Buck and Axel, 1991). For a comparison of vertebrate and insect olfaction see Kaupp(2010), for a recent review of insect olfactory receptors see Fleischer et al.(2018). Three types of receptor proteins detect volatile chemical information in insects. These are odorant receptors (ORs) which are restricted to insects, specific gustatory receptors (GRs) detecting carbon dioxide and receptors related to ionotropic glutamate receptors, called ionotropic receptors (IRs). The ORs evolved in parallel with the onset of insect flight (Missbach et al., 2014). Similar to GPCRs, insect ORs belong to the class of heptahelical transmembrane proteins. But compared with them, the OR proteins show an inverted orientation within the plasma membrane (Benton et al., 2006; Lundin et al., 2007; Smart et al., 2008). Edited by: Frédéric Marion-Poll, Analyzing the variation of insect OR protein amino acids during evolution revealed a model for AgroParisTech Institut des Sciences transmembrane domain arrangement that is unrelated to GPCRs (Hopf et al., 2015). et Industries du Vivant et de An insect OR is a heteromeric construct formed by an odor-specific OrX protein and an l’Environnement, France ubiquitary odorant co-receptor, Orco (Larsson et al., 2004; Neuhaus et al., 2005). Heterologous Reviewed by: coexpression of OrX and Orco proteins may in addition to the formation of ORs also lead to Philippe Lucas, Orco homomers (German et al., 2013). It remains to be shown that the ciliar OSN membrane also Institut National de la Recherche comprises both types of constructs. At least for the soma membrane the insertion of Orco but not Agronomique (INRA), France Eva Maria Neuhaus, of Or22a/b proteins was demonstrated (Benton et al., 2006). Friedrich Schiller Universität Jena, Experiments in heterologous expression systems supported the view that insect ORs primarily Germany operate as ligand-gated channels (Sato et al., 2008; Wicher et al., 2008). An odor stimulation *Correspondence: of sufficient strength produced—independent of G protein activity—an immediate transient 2C Dieter Wicher response. The ORs form non-selective cation channels which are also permeable for Ca . At least [email protected] some of these OR channels are constitutively active as their expression leads to an elevated level of free Ca2C, even in the absence of a stimulating odor. In addition to the fast ionotropic response Received: 23 November 2017 there was a slowly developing OR current which relied on G protein function (Wicher et al., 2008). Accepted: 21 March 2018 This finding raised the question whether there is also a role of metabotropic signaling in insect Published: 05 April 2018 olfaction. Citation: Intriguingly, when only Orco proteins are expressed they also form nonselective, Ca2C Wicher D (2018) Tuning Insect Odorant Receptors. permeable cation channels. These channels cannot be activated by odors but by cyclic nucleotides Front. Cell. Neurosci. 12:94. (Wicher et al., 2008). As in the case of ORs, it is presently unknown how the channels are composed doi: 10.3389/fncel.2018.00094 of, either as dimers as the heptahelical channel rhodopsin (Müller et al., 2011; Kato et al., 2012), or as Frontiers in Cellular Neuroscience| www.frontiersin.org 1 April 2018 | Volume 12 | Article 94 Wicher Tuning Insect Odorant Receptors tetramer like conventional ion channels (Doyle et al., 1998). Gs proteins in OR signal transduction was reported (Deng et al., Orco dimer constructs have properties comparable to those 2011). In addition, other studies demonstrated the importance of of channels formed by native Orco proteins (Mukunda et al., Gq proteins (Kain et al., 2008, 2009). Mutations in dgq, the gene 2014a). encoding the Drosophila Gq a subunit caused reduced responses Orco was found to be necessary for the insertion of the to odor stimulation. odor-specific receptor proteins into the plasma membrane In contrast to these findings, only tiny effects in Drosophila (Larsson et al., 2004). An important signaling system during sensillum recordings were observed when manipulating the development is the hedgehog (Hh) system (Briscoe and Thérond, activity of G proteins (Yao and Carlson, 2010). Rather mild 2013). The transport of Drosophila ORs to and within the effects of G protein inhibition on Ca2C responses were seen in dendritic cilia is regulated by the Hh pathway (Sanchez et al., heterologously expressed ORs (Smart et al., 2008). 2016). The localization of the ORs depends on the distribution of the Hh signal transducer Smoothened (Smo). Smo knockdown SECOND MESSENGER SYSTEMS flies showed reduced odor responses indicating less expression while mutants in the Smo repressor Patched (Ptc) display largely Independent of G protein-coupled signal cascades Ca2C is an enhanced odor responses. As Hh is produced in the OSNs the ubiquitous messenger that regulates the activity of proteins and tuning of OR distribution is an autoregulatory process (Sanchez links such signaling cascades. OR activation leads to Ca2C influx et al., 2016). Orco proteins possess a putative calmodulin (CaM) into OSNs. Prolonged odor stimuli lead to a Ca2C-induced binding domain that is well conserved among insect species adaptation of the odor response (Cao et al., 2016). On the other (Mukunda et al., 2014b). Robust mutations within this region of hand, CaM activity can enhance the OR response to moderate Orco proteins disrupted the OR traffic to the ciliar membrane stimuli (Mukunda et al., 2014b). (Bahk and Jones, 2016). Mutations in the cascade downstream Gs, i.e., in the adenylyl cyclase rutabaga and in the phosphodiesterase dunce affected G PROTEINS the olfaction-guided behavior (Martín et al., 2001). Especially overexpression of dunce in specific OSNs which diminished That insect ORs—in spite of their inverted membrane the cAMP level in these cells produced severe phenotypes topology—can interact with G proteins has been demonstrated (Gomez-Diaz et al., 2004). A reduced cAMP level impairs for heterologously expressed ORs. Activation of Drosophila the ability of flies to correctly detect an odor (Murmu and Or43a receptor could be monitored when it was coexpressed Martin, 2016). On the other hand, odor stimulation leads to with the promiscuous G protein a subunit G15 in Xenopus ooytes enhanced cAMP production (Miazzi et al., 2016). That this (Wetzel et al., 2001). In addition, pheromone-induced activation effect was related to ORs had been suggested by the finding of the silkmoth Bombyx mori OR-1 and 3 (Grosse-Wilde et al., that odor stimulation of ORs expressed in HEK293 cells gave 2006) and Heliothis virescens HR13 (Grosse-Wilde et al., 2007) rise to enhanced cAMP production (Wicher et al., 2008). coexpressed with G15 in T-Rex293 cells was reflected by calcium Artificially enhancing the cAMP concentration in Drosophila signals upon activation of IP3 receptors upon PLC activation OSNs by injecting the membrane-permeable 8-bromo-cAMP or via G15. the adenylyl cyclase activator forskolin into the base of sensilla In the antenna of Drosophila all subunits of heterotrimeric enhanced the odor-response and shifted the concentration- G proteins were shown to be expressed (Boto et al., 2010). dependence towards lower odor concentration (Getahun et al., According to immunohistochemical studies, Gs,Gi and Gq a 2013). Similarly, in flies expressing a light-activated adenylyl subunits could be detected in the OSNs. This also includes the cyclase in OSNs the spike activity could be enhanced by light sensilla along which Gi and Gq were found, whereas Gs staining exposure (Deng et al., 2011). was seen at the basal segment (Boto et al., 2010). Expression of The signaling cascade downstream Gq also plays a role Gs in fly sensilla was also reported, and Gs proteins were found in odorant signal processing of insects (Krieger and Breer, to be important for sensitive odor detection (Deng et al., 2011). 1999; Kain et al., 2008). In the hawkmoth Manduca sexta, In the antenna of B. mori the three a subunits Gs,Gi and Gq were pheromone stimuli are detected via PLC-dependent signaling detected (Miura et al., 2005) while in the mosquito Anopheles (review, Stengl, 2010). Short and faint pheromone presentation females only Gq was found in certain sensilla (Rützler et al., causes an immediate increase spike activity in the receptor 2006). neuron which is accompanied
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