Sensory Systems of Insects
Olfaction in insects
Insects perceive odorant mainly with sensory organs called sensilla on their antennae. Olfactory sensilla are generally characterised by bearing tiny pores on their cuticular surface and occur in a bewildering variety of shapes, of which the most common one is probably the hair. There are several olfactory receptor cells in the sensillum. Their dendrites extend into a sensillar lumen and their axons project to the first order olfactory information processing center of the brain, the antennal lobe (see also the chapter on the insect antenna). An odorant can be adsorbed on the cuticular surface of the sensillum, diffuse towards a pore and through it into the inside of the sensillum. Since the sensillum is filled with sensillum lymph, it is thought that volatile and insoluble odorants such as pheromones bind to specific odorant binding proteins (OBP), are thereby solubilized and transferred to the olfactory receptors on the dendrites of the olfactory receptor cells. Recently it has been reported for a special class of OBPs, the pheromone-binding proteins (PBP) that they are necessary for the activation of pheromone-sensitive odorant receptors. When the solubilized odorant binds to odorant receptors in the dendritic membrane of the olfactory receptor cell, the cell is depolarized and generates action potentials, which transmit the olfactory signal to the antennal lobe. In this chapter, we introduce the current knowledge concerning the molecular mechanisms of olfaction.
olfactory receptor neurons (ORNs) can roughly be classified into two types: those are responsive
to general odors such as floral odors or food-related odors and those that are
responsive to pheromone, i.e. species-specific odorants. General odorant receptor proteins (ORs) show low specificity and respond to
various odorants hence they are called generalists. They have partially
overlapping odorant response spectra. On the contrary pheromone receptor proteins show high specificity and respond to
only one ligand (a specific pheromone) hence they are called specialists.
Genera ORs are well
investigated in fruit fly, cockroach and honeybee and categorized into a number
of types based on their response spectra1-3).
Pheromone receptor genes were first identified by Sakurai et al., 200422) in the silkmoth. Silkmoth pheromone receptor neurons are only present on male antennae and females do not respond to the pheromone they release.. Sakurai et al. performed differential screening on a male cDNA library to isolate genes that were specifically and abundantly expressed on male antennae, and they obtained pheromone receptor gene candidates. One of the cDNA clone obtained showed a conspicuous homology with known insect odorant receptor genes in its amino acid sequence. This clone was named BmOR1 (Bombyx mori olfactory receptor 1) after the nomenclature for the silkmoth22). Subsequent experiments in which BmOR1 was expressed in Xenopus oocytes showed that BmOR1 specifically binds bombykol and activates a signal transduction system via BmGaq. Based on the sequences of BmOR1 and known insect odorant receptors, 29 odorant receptor-like sequences were discovered. Of these 29 sequences four genes were identified that were expressed male-specifically or male-dominantly. However, there was no receptor that responds to bombykol in the Xenopus oocyte expression system except BmOR122).
Female antennae responded to bombykol electrically when BmOR1 was expressed in female antennae by infection with a recombinant baculovirus. The study by Sakurai et al. cited above revealed the identity of the silkmoth pheromone receptor almost fifty years after Butenandt et al. resolved the chemical structure of silkmoth pheromone22).
Odorants are volatile chemical substances that have molecular weights less
than about 300 and are recognized as odor by olfactory systems of living
organisms (Touhara and Vosshall, 2009). Among them odorants that are, for
example associated with the existence of food, fire, or a predator are
called general odors (about pheromone, see chapter pheromone). Most odorants
are lipophlic and insoluble in water, thus different mechanisms of odorant
solubilization, reception, and recognition have evolved in insects and
mammals. In this section we provide an introduction to the molecular transduction
mechanisms of general odor reception in insects. (sorry but most of the
information is for Drosophila).
Odorants adsorbed on the sensillum are solubilized by a high concentration
of OBP in the sensillum lymph and transported (or do they diffuse rather?)
to the receptor proteins in the dendritic membrane. Insect OBPs were first
discovered in the silkmoth Antheraea polyphemus (Vogt and Riddiford, 1981).
Since then insect OBPs have been isolated in more than 40 species and genomic
analysis implies that the silkmoth has 44 types of OBP, Drosophil 51, Anopheles
gamgiae 57 (Maoda et al., 1993; Krieger et al., 1996; Pelosi et al., 2006).
OBPs isolated so far are categorized into four types (PBP, General odorant
binding protein; GOBP1. GOBP2, Antennal binding protein X; ABPX) (Vogt
et al., 1991, 1999; Pelosi et al., 2006). OBPs are soluble proteins of
about 15 kDa molecular weight and have six cysteine residues and three
disulfide bonds (Scaloni et al., 1999; Leal et al., 1999). Since X-ray
crystallography of silkmoth PBP was first performed, this method was also
applied to six other OBPs including Drosophila OBP (LUSH) (Sandler et al.,
2000; Pelosi et al., 2006). Based on these data, a model has been proposed
according to which the OBP-ligand complex dissociates at acidic pH, such
as found the dendritic membrane, making the odorant available for binding
to an OR.
Functional analyses of insect odorant receptors are performed by electrophysiological experiments using the Xenopus oocyte expression system, Drosophila transgenesis, or calcium imaging in the Barathra ovarian cell derived Sf9 cell expression system (Wetzel et al., 2001; Stortkuhl and Kettle, 2001; Hallmen et al., 2004; Lu et al., 2007; Anderson et al., 2009; Tanaka et al., 2009; Jordan et al., 2009). Among the insect odorant receptors, Drosophila Or43a was first analyzed in detail with respect to its functional properties. Using the Xenopus oocyte expression system it has been shown that Or43a responds to benzaldehyde and cyclohexanol (Wetzel et al., 2001). Using Or43a ectopically expressed in Drosophila antennae, the response characteristics of Or43a were investigated in vivo and it was shown that the antenna responds to benzaldehyde and cyclohexanol as well (Stortkuhl and Kettler, 2001). These two studies revealed that the odorant receptor receives and discriminates odorants.
The Carlson lab carried out a largescale functional analysis of the odorant receptor using empty neurons of Drosophila transformants (de Bruyne et al., 1999, 2001; Hallem et al., 2006). Using these methods, response measurements for 24 Drosophila odorant receptors to 110 odorants were performed to functionally characterize this set of odorant receptors (Hallem et al., 2004, 2006). Recently, using this method, the response characteristics of 50 odorant receptors of Anopheles gambiae were revealed (Carey et al., 2010). It was shown that the response characteristics of these receptors are identical with those of the ORNs and therefore, the response properties of ORNs are determined by the odorant receptors.
The identification of odorant receptors to general odors in the silkmoth is also rapidly progressing. Anderson et al. functionally identified three odorant receptors (BmOR19, BmOR45, and BmOR47) specifically expressed in females (Anderson et al., 2009). It has been shown that BmOR19 responds to linalool and BmOr45 and BmOr47 respond to benzoic acid. Linalol and benzoic acid are odorants derived from plants, therefore, it has been suggested that these receptors are related to the indentification of potential oviposition sites or male pheromone. Tanaka et al. functionally analyzed 23 odorant receptors expressed in silkmoth larvae (Tanaka et al., 2009). Of these receptors, BmOR59 was shown to specifically respond to cis-jasmone that is contained in mulberry leaves eaten by silkmoth larvae. This implies that BmOR59 activation by cis-jasmone is involved in attracting silkmoth larvae to leaves of the food plant.
Recently, peculiar molecular mechanisms have been discovered in insect odorant receptors. As mentioned above, G-proteins are present in insect antennae (Laue et al., 1997), and IP3, a second messenger activated via a trimeric G-protein, transiently increases in response to odorant (Boekhoff et al., 1993). Also, IP3-activated ion channels are known in insects. From these lines of evidence it has been hypothezised that insect olfactory transduction occurs though a trimeric G-protein-coupled receptor (Krieger and Breer, 1999). This resembles the scheme also found in vertebrates. However, the function of Or83b, a Drosophila odorant receptor family protein, indicates that olfactory signal transduction mechanisms in insects are different.
Although the amino acid sequence of Or83b is similar to other odorant receptors,
Or83b does not function as an odorant receptor. The amino acid sequences
of this protein and its homologs are well conserved across insect species
(Krieger et al., 2003; Jones et al., 2005). In Drosophila, Or83b is expressed
in almost all olfactory receptor neurons and Or83b deletion mutants do
not respond to odorants (Vosshall et al., 1999; Larsson et al., 2003).
From a study using Drosophila Or83b transformants it has been inferred
that the functions of Or83b are membrane trafficking of odorant receptors
and retention of the receptor proteins in the membrane (Benton et al.,
2006). In vitro experiments using cultured cells demonstrated that Or83b
forms heteromers with other odorant receptor proteins (Neuhaus et al.,
2005; Lundin et al., 2007). An Or83b-family protein is also found in the
silkmoth. When it is coexpressed with sex pheromone receptor protein the
response sensitivity of the receptor mechanism is increased (Nakagawa et
al., 2005). After that it was shown that the insect odorant receptor forms
a ligand-gated cation channel in conjuction with the Or83b-family protein
and does not function as a G-protein-coupled receptor (Sato et al., 2008:
Wicher et al., 2008). Thus, rather than being a classical G-protein-mediated
mechanism, odorant binding appears to gate channel activity directly in
insects, providing a chemo-electrical transduction with only two components.
In Drosophila it has been reported that a member of the ionotropic glutamate receptor family (ionotropic receptor; IR) functions as an odorant receptor other than general odorant receptors and pheromone receptors (Benton et al., 2009). The IR shares sequence homology with known NMDA, AMPA, and Kainate receptors but are devoid of a glutamate receptor site and expressed in the dendrites of sensory neurons in sensilla coeloconica. The functional analysis of recombinant Drosophila ectopically expressing this IR shows that this receptor is responsive to specific general odors including ammonia and phenylacetaldehyde. However, this type of IR has so far not been isolated and identified from other insect species.
Insects perceive pheromone through olfactory sensilla trichodea that are
specialized for pheromone binding and localized on the antennae. Pheromone
is adsorbed to the cuticle and can diffuse laterally to finally enter a
sensillum trichodeum through one of the pores on its surface and be solubilized
into the sensillar lymph. Insect sex pheromone components are highly lipophilic
and as a result, in analogy to general odorants, they are solublized by
pheromone binding proteins (PBP) and transported (Vogt, 2003). PBPs have
been isolated from many moth species and it has been confirmed that PBPs
can bind sex pheromone components (Pelosi et al., 2006). It has been thought
that binding to PBPs is the first step to sex pheromone recognition and
that PBPs bind sex pheromones specifically (Plettner et al., 2000; Bette
et al., 2002; Maida et al., 2003). However, it has been reported that PBPs
can also bind sex pheromones of other species and even general odorants
(Vampanacci et al., 2001; Grater et al., 2006). Gene expression analysis
of PBPs in sensillar tissues revealed that PBP are expressed in the antennae
of both sexes although with different expression levels (Abrahma et al.,
2005; Forstner et al., 2006; Watanabe et al., 2007; Xiu et al., 2007).
This implies that PBP does not bind sex pheromone exclusively. On the other
hand, an OBP (LUSH) appears to be involved in the reception of Drosophila
male pheromone, cis-vaccenyl acetate (cVA) (Xu et al., 2007; Laughlin et
al., 2008). In lush mutant, trichoid sensilla normally sensitive to cVA
does not respond to cVA stimulation whereas a conformational change of
LUSH induced by site-directed mutagenesis causes the sensilla to respond
to cVA. These reports suggest that the pheromone receptor recognizes a
structural change in the LUSH-sex pheromone complex and not the sex pheromone
itself. However, the relationship between PBPs and sex pheromone receptors
is still poorly understood.
Odorant receptors expressed in olfactory receptor neurons are the first candidate of the peripheral molecular mechanisms that recognize sex pheromone. The bombykol receptor of the silkmoth has been the first sex pheromone receptor isolated and identified in any animal species (Sakurai et al., 2004). Genes specifically expressed in male silkmoth antennae were isolated using differential screening methods. From these genes, candidate olfactory receptor genes were isolated by sequence analysis and were confirmed to be olfactory receptors, by electrophysiological experiments using the Xenopus oocyte expression system. The receptor for another sex pheromone component in silkmoth, bombykal, was identified in the same way (Nakagawa et al., 2005). In a hawkmoth, several candidates of sex pheromone receptors were isolated and they are specifically expressed on male antennae (Krieger et al., 2004). Recently, using aDrosophila mutant with “empty” olfactory receptor neurons devoid of their native receptors, the gene product of the pheromone receptor candidate gene HR13 of hawkmoth responds to a sex pheromone component, Z11-16:Ald (Kurtovie et al., 2007). A functional analysis of HR13 has also been done using Calcium imaging of cultured cells (Grosse-Wilde et al., 2004). Generally, insect odorant receptors identified so far respond to several odorants and thus have low ligand-specificity (Hallem et al., 2004; Carey et al., 2008). In contrast, the three moth sex pheromone receptors identified have high ligand specifity.
Recently, sex pheromone receptors of the diamondback moth (Plutella xylostella), Mythimna separate, Diaphania indica, and Ostrinia responding to major sex pheromone components have been identified (Mitsuno et al., 2008; Miura et al., 2009). It has been shown that these receptors can be classified into the same cluster to which silkmoth sex pheromone receptor belongs. Thus it is thought that sex pheromones of Lepidoptera are recognized by receptors that have the similar sequences.
Another type of protein that appears to be involved in sex pheromone reception is SNMP (sensory neuron membrane protein) (Benton et al., 2007). It is suggested that SNMP occurs in olfactory trichoid sensilla of many insect species including silkmoth (Rogers et al., 1996, 2001).Benton et al. measured the pheromone response of Drosophila snmp transgenic line and show that its response to general odorant does not change but the response to sex pheromone decreases. The same result is obtained from recombinant Drosophila that expresses the hawkmoth sex pheromone receptor HR13. The function of SNMP is thought to be a transfer of the fatty-caid-derived ligand from the PBP to the odorant receptor protein.
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