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Sensory Systems of Insects

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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.

Insects 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).

The domestic silkmoth (Bombyx mori) is the species in which the chemical structure of a pheromone was first identified16) and it has become a model organism of pheromone reception for which much information has been accumulated. Pheromone (specific) receptor neurons are housed in a type of hair sensillum, the long sensillum trichodeum, of which a large number covers the side branches of the antennae of the male silkmoth. Silkmoth pheromone is composed of bombykol, the major component [(E, Z)-10, 12-hexadecadien-1-ol], and bombykal, a minor (or accessory) component [(E, Z)-10, 12-hexadecadien-1-al]16,17). Bombykol alone is sufficient to elicit mating behavior in the male silkmoth. On the other hand bombykal raises the threshold for the induction of male mating behavior by bombykol and can thus effectively inhibit mating behavior17). Bombykol and bombykal receptor neurons are housed in pairs in the same type of trichoid sensillum. These receptor cells respond with high specificity to their pheromone ligands17, 18, 22, and 23)


Insect odorant receptor genes

Buck and Axel first isolated olfactory receptor genes in rat in 1991 and showed that the genes belong to the G-protein coupled receptor (GPCR) family19). In the following, olfactory receptor genes belonging to the GPCR family were also isolated from fish and the nematode Caenorhabditis elegans

In insects, it has been shown that the levels of second messenger inositol triphosphate (IP3) increase transiently upon olfactory stimulation in olfactory receptor neurons and their dendrites have also been shown to have ion channels opened by IP3.  These lines of evidence led to the hyopthesis that insect odorant receptors also belong to the GPCR family. Then Vosshall et al. (1999) first identified a candidate insect odorant receptor gene family, DOr (Drosophila odorant receptor), by searching for GPCR genes in the genomic DNA sequence20).

In 2000 the Drosophila genomic DNA was completely sequenced. It has been shown that the DOr family is composed of 60 genes which encode 62 receptor proteins. Of these 60 genes, 42 are expressed in adult olfactory receptor neurons. DOr putative amino acid sequences possess seven hydrophobic regions that are inferred to be transmembrane regions and they are thought to belong to GPCR family as the odorant receptors of vertebrates and C. elegans do. As they have little sequence homology with known GPCR amino acid sequences, they form a separate GPCR family. Drosophila olfactory receptor neurons express two types of receptors, one of which is Or83 that is expressed almost every olfactory receptor neuron21).

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).



Transduction Mechanisms in the reception of General Odors in Insects

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General Odors

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).


Solubilizaiton of odorants and their transport mechanisms

Insects perceive odorants through olfactory sensilla mostly located on the antennae. There is also a smaller number of olfactory sensilla on the maxillary palp and labial palp that belong to the mouth parts ([cite Altner!] Stange, 1992; de Bruyne et al., 1999; Kwon et al., 2006). An olfactory sensillum has a characteristic structure generally with numerous pores on its cuticular surface (see also Antenna). The lumen of the sensillum is filled with sensillum lymph surrounding the dendrites of olfactory receptor neurons (ORNs). ORN soma is surrounded by support cells (thecogen, thecogen, and trichogen cell) that secrete odorant binding proteins (OBP) or pheromone binding protein (PBP) (Steinbrecht et al., 1995; Shanbhag et al., 1999; Shanbhag et al., 2000). The ORN is a bipolar cell that extends its single dendrite into the sensillum and its single axon projects to the brain . The ORN is excited and can transmit an electrical signal to the brain when an odorant binds to the receptor protein in its dendritic membrane. Olfactory sensilla are categorized into several types according to their morphology and size (cite Altner and Prillinger, maybe 1988; Shanbhag et al., 1999; see also Antenna) and the odor response of each cell type can be recorded by single sensilum recording under favorable conditions in some types of sensilla (de Bruyne et al., 2001). In Drosophila the olfactory response spectra of most types of sensilla have been recorded and each type has a distinct olfactory spectrum (de Bruyne et al., 1999, 2001; Hallem et al., 2004; Yao et al., 2005; van der Goes van Naters and Calrson, 2007). Each sensillum houses two to four ORNs with different odorant receptor and the olfactory response spectrum of each sensillum represents these ORN spectra. (de Bruyne et al., 1999, 2001; Hallem et al., 2004). It has been shown that these response spectra of ORNs are derived from the ligand affinity of their olfactory receptor proteins.

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.


General odorant receptor

genes were first identified in rat (Buck and Axel., 1991), and it has been shown that they are G-protein coupled receptors (Firestein, 2001). After that the odorant receptor genes of human (Ben-Arie et al., 1994), fish (Ngai et al., 1993) and bird (Nef et al., 1996) were identified. In invertebrates, nematode odorant receptor genes that contain seven transmembrane domains were identified (Troemel et al., 1995; Sengupta et al., 1996) by genomic analysis. In insects the genomic analysis have revealed a species-specific number of candidate odorant receptor genes: 62 in the fruit fly (Drosophila melanogaster), 170 in the honeybee (Apis mellifera), 79 in the Malaria mosquito (Anopheles gambiae), 131 in the Yellow fever mosquito (Aedes aegypti), 341 in a flour beetle (Tribolium castaneum) and 66 in the silkmoth (Bombyx mori) (Clyne et al., 1999; Vosshall et al., 1999; Gao and Chess, 1999; Fox et al., 2001. 2002; Hill et al., 2002; Krieger et al., 2002, 2004; Robertson and Wanner, 2006 Wanner et al., 2007; Bohbot et al., 2007; Engsontia et al., 2008; Tanaka et al., 2009). It has been shown that insect odorant receptors are of the seven transmembrane domain types through hydrophobicity analysis. However, insect odorant receptors have little similarity with mammalian odorant receptors and do not have similarity sequences such as the DRY amino acid motif. Besides, the insect odorant receptors are different from vertebrate odorant receptors in terms of topology, which is reversed compared to vertebrates, with the C terminus intracellular and the N terminus extracellular. Insect odorant receptors lack many features that are characteristic of G-protein coupled receptors (Wistrand et al., 2006; Benton et al., 2006; Lundin et al., 2007).

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.


Atypical odorant receptors (ionotropic glutamate receptor family?)

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.

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Transduction Mechanisms of Pheromone receptors


Pheromones

In contrast to general odors, chemical substances that are released by an individual and that elicit specific behaviors or physiological changes in conspecific individuals are called pheromones (Karlson and Luscher, 1959). Pheromones are classified as sex pheromones, alarm pheromones, aggregation pheromones, or trail pheromones by their effect on conspecifics. Sex pheromones elicit mating behavior and are thus crucial for insect reproduction. Since the chemical structure of silkmoth sex pheromone, bombykol ( (E, Z)-10, 12-hexadecadien-1-ol), was first identified, the chemical structure of sex pheromones of more than 1500 species, including numerous economically important insects, has been identified and registered in databases (Pherobase; http://www.pherobase.com/; Pherolist; http://www.pherolist.slu.se/pherolist.php; Byers, 2002). Although the chemical structure of identified sex pheromone components includes a wide range of chemicals, sex pheromones of moths share some homologies among species (Byers, 2005). It is thought that these homologies are due to two common biosynthetic pathways that are shared by moths (Ando et al., 2004). In one pathway, moths synthesize the sex pheromone component from de novo fatty acids, (Type I), in the other the component is synthesized from linoleic acid or linolenic acid derived from plants (Type II). Through the former, alcohols such as bombykol as well as aldehydes and acetate are produced, the latter permits the synthesis of straight-chain carbohydrates (Ando et al., 2004). Generally, information on pheromones, pheromone-sensitive sensilla, and molecular mechanisms has in particular been obtained for sex pheromone systems in moths. Therefore, the present material is mostly representative for moths.


Solubilizaiton of pheromones and their transport mechanisms

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.


Sex pheromone receptor

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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