Chemical Senses Vol.15 no.2 pp.205-215, 1990 Odorant-binding proteins in vertebrates and insects: similarities and possible common function Paolo Pelosi and Rosario Maida Istituto di Industrie Agrarie, Universita' di Pisa, via S.Michele, 4, 56100 Pisa, Italy Abstract. Among the various chemoreception systems, pheromone perception in insects provides perhaps the best biochemical model for comparing with olfaction in vertebrates. The proteins recently identified in the two systems are reviewed and their characteristics are compared with particular reference to the soluble odorant-binding and pheromone-binding proteins that are present in large concentrations in both systems. Hypotheses about the functions of these binding proteins in modulating the olfactory signals are reported and discussed. Introduction It is now generally accepted that the first step in odor detection occurs at the peripheral level as a result of specific interactions between odorant molecules and receptor proteins on the surface of olfactory cilia (Getchell, 1986; Lancet, 1986, 1987; Anholt, 1987; Lancet and Pace, 1987). Much of the biochemical research in olfaction is, therefore, aimed at the identification, purification and characterization of olfactory receptor proteins. While evidence is accumulating regarding the presence and identity of putative membrane-bound odorant receptors, other protein species characterized as either enzymes or binding proteins have also been found within the olfactory system. All of these types of proteins have been proposed to be involved in the olfactory process. Hence olfaction may make use of at least three types of proteins: i) membrane-bound receptors; ii) odorant-degrading enzymes; and iii) soluble odorant-binding proteins. The above notions apply to olfaction in non-aquatic vertebrates, as well as to pheromone perception in insects and to chemosensory processes in other organisms. We believe that comparisons between various chemosensory systems can provide models to help us understand the biochemical events in vertebrate olfaction. The pheromone perception system in insects looks especially promising because of its simplicity and its similarities to olfactory systems in mammals and other vertebrates. In this paper we compare vertebrate olfaction with other chemosensory systems and summarize the existing data on odorant-binding proteins. We also point out the similarities between olfaction in vertebrates and pheromone perception in insects, and describe the common functions of binding proteins in the two systems. Chemoreception systems At the periphery, olfaction is based on the detection of small molecules by specific binding proteins. Hence we might presume that any system of ligand—protein interaction could be taken as a model for studying the early events of olfaction. However, even at the receptor neuron level, odor detection can be more complex than a simple 205 at Indiana Univ. School of Medicine on October 5, 2012 http://chemse.oxfordjournals.org/ Downloaded from
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Chemical Senses Vol.15 no.2 pp.205-215, 1990
Odorant-binding proteins in vertebrates and insects:similarities and possible common function
Paolo Pelosi and Rosario Maida
Istituto di Industrie Agrarie, Universita' di Pisa, via S.Michele, 4, 56100Pisa, Italy
Abstract. Among the various chemoreception systems, pheromone perception in insects provides perhapsthe best biochemical model for comparing with olfaction in vertebrates. The proteins recently identified inthe two systems are reviewed and their characteristics are compared with particular reference to the solubleodorant-binding and pheromone-binding proteins that are present in large concentrations in both systems.Hypotheses about the functions of these binding proteins in modulating the olfactory signals are reportedand discussed.
Introduction
It is now generally accepted that the first step in odor detection occurs at the peripherallevel as a result of specific interactions between odorant molecules and receptor proteinson the surface of olfactory cilia (Getchell, 1986; Lancet, 1986, 1987; Anholt, 1987;Lancet and Pace, 1987). Much of the biochemical research in olfaction is, therefore,aimed at the identification, purification and characterization of olfactory receptorproteins.
While evidence is accumulating regarding the presence and identity of putativemembrane-bound odorant receptors, other protein species characterized as eitherenzymes or binding proteins have also been found within the olfactory system. All ofthese types of proteins have been proposed to be involved in the olfactory process.Hence olfaction may make use of at least three types of proteins: i) membrane-boundreceptors; ii) odorant-degrading enzymes; and iii) soluble odorant-binding proteins.
The above notions apply to olfaction in non-aquatic vertebrates, as well as topheromone perception in insects and to chemosensory processes in other organisms.We believe that comparisons between various chemosensory systems can provide modelsto help us understand the biochemical events in vertebrate olfaction. The pheromoneperception system in insects looks especially promising because of its simplicity andits similarities to olfactory systems in mammals and other vertebrates.
In this paper we compare vertebrate olfaction with other chemosensory systems andsummarize the existing data on odorant-binding proteins. We also point out thesimilarities between olfaction in vertebrates and pheromone perception in insects, anddescribe the common functions of binding proteins in the two systems.
Chemoreception systems
At the periphery, olfaction is based on the detection of small molecules by specificbinding proteins. Hence we might presume that any system of ligand—protein interactioncould be taken as a model for studying the early events of olfaction. However, evenat the receptor neuron level, odor detection can be more complex than a simple
Amino acids, sugarsSugarsSeveral different compoundsSeveral volatile lipophilic compoundsAmino acidsOne or few volatile lipophilic compoundsSeveral volatile lipophilic compounds
odorant — receptor protein interaction. The presence of a mucus layer, for instance, cangreatly affect the concentration of odorant molecules in the immediate environmentof receptor binding sites (Getchell etal., 1984). In addition, as seen in bacterial systemsthe affinity of chemostimulants for membrane binding sites can be affected by changesin the properties of the binding sites (DeFranco and Koshland, 1980). Not allligand—protein interactions are suitable for studying the early events in olfaction,therefore; it seems more appropriate to restrict the choice of a model to a truechemoreception system where a behavioral response to chemical stimulation can alsobe measured.
Table I lists several well-studied chemosensory systems and the corresponding typesof chemical stimuli. Some systems respond to volatile air-borne chemicals, whereasothers, such as those of bacteria and fish, respond to stimuli carried in aqueous solution.The complexity of the stimuli can also be used to divide the systems into two groups:(i) those responding to a great number of substances with different chemical structures(e.g. the general olfactory system of non-aquatic vertebrates and insects, and the systemfor bitter taste perception in vertebrates); and (ii) those responding to a more limitednumber of compounds such as the chemosensory systems for pheromone perceptionin insects, and for sugar and/or amino acid perception in bacteria and fish, and sweettaste perception by other vertebrates. In this second group the study of the interactionsbetween stimulus and receptor is simplified because the chemical structures of specificstimuli are known; this is particularly true for pheromone perception in insects.
Of all the systems listed in Table I, only bacterial chemoreception is understood atthe biochemical level: binding proteins and receptors for the key stimuli were purifiedseveral years ago (Clarke and Koshland, 1979; Koshland, 1979), and multiplemethylations of the receptor proteins have been demonstrated to serve as a regulatorymechanism (DeFranco and Koshland, 1980; Hedblom and Adler, 1980). Thischemoreception system makes use of soluble binding proteins, specific for the chemicalstimulus, to carry amino acids and sugars from the outer to the inner membrane ofthe bacteria. The complexes formed by the binding proteins and ligands then bind tomembrane receptor proteins, giving rise to transduction of the signal (Koshland, 1981).Such a mechanism is very appealing as a model for olfaction; however the low specificityof the soluble binding proteins associated with olfactory systems indicate that the bacterialsystem is really not an appropriate model (Pelosi and Tirindelli, 1989).
For all the other systems in Table I, biochemical research is at a very early stage.If we want to choose a model for olfaction in non-aquatic vertebrates, we should excludesystems such as general olfaction in insects, and bitter taste; these are very complex
because of the great number of different stimuli, and because we lack knowledge ofthe corresponding mechanisms for discriminating between stimuli. In insects, the generalolfactory system responds to odors of plant origin and modulates to some extent theinteractions between the insect and its host plant (Visser, 1986). This olfactory systemis probably based on a complex code, common to many insect species and similar inseveral respects to the vertebrate olfactory code (Ma and Visser, 1978; van der Pers,1981; Visser, 1979, 1986; Lights al., 1987, 1988). Information about bitter taste islimited, but the large number of structurally different that taste bitter suggests that thecode is not simple (Beets, 1978).
The other systems share a code which is less complex and based on known chemicalstructures. Both olfaction in fishes and perception of sweet taste by other vertebratesare designed to detect constituents of the natural diet, such as amino acids and simplesugars. However some limitations also occur in biochemical studies of such systems.Since the ligands are common metabolites, experimental results may be affected byenzmes and transport proteins that interact with the same substrates (Brown and Hara,1981). Moreover, as far as the sweet taste is concerned, it is known that sugars arenot the best ligands, being detectable only at concentrations above 0.1 mM, and themost effective probes for use in biochemical studies, such as synthetic compounds andsome plant proteins, can have completely different structures (Beets, 1978; Persaudet al, 1988b).
The biochemistry of pheromone perception in insects then remains as probably themost appropriate model for comparing with that of vertebrate olfaction. This is becauseof the following features that simplify its study: (i) The code is simple; often only asingle compound will elicit a single distinctive behavior, (ii) The structure of the stimulusmolecule secreted by the female is known, and this particular molecule is usually thebest ligand for both the receptor and the binding proteins, (iii) 7n vivo' measurementsof electrophysiological and behavioral responses provide correlations with thebiochemical data that are much easier to obtain than with vertebrates: (iv) The anatomyis convenient for isolating the sensory organs, (v) Genetic studies are relatively easyto perform and specific mutants should not be difficult to obtain. It must be rememberedthat biochemical research in bacterial chemoreception was accelerated by the availabilityof specific mutants, (vi) The female antenna often provides a sort of blank since theproteins involved in sex pheromone recognition may not be present in the female.However this assumption is not always justified because the females of some speciescan smell their own pheromone.
Support for the insect model is also provided by the data obtained to date regardingthe biochemistry of both insect and mammalian olfaction. These data reveal manysimilarities in the biochemical components and point to common mechanisms of action.The main drawback when working with insects is the small amount of material available,even when using moths with large antennae. However the use of microtechniques forboth protein purification and the application of molecular biology makes such studiesfeasible.
Olfactory binding proteins
The olfactory proteins so far identified in both vertebrates and insects can be dividedinto three groups: (i) putative receptors, (ii) odorant-degrading enzymes, and (iii) soluble
•N.R. = Not reported.(a) Chen and Lancet, 1984a, 1984b; Chen et al., 1986a, 1986b; Lancet, 1986.(b) Cagan and Zeiger, 1978; Rhein and Cagan, 1980.(c) Fesenko et al, 1978, 1979, 1983, 1987, 1988; Novoselov et al., 1980.(d) Price, 1978; Goldberg et al., 1979; Price and Willey, 1988.(e) Moth = A.polyphemus. Vogt et al., 1988.
binding proteins. Since no specific olfactory receptor has yet been clearly identified,distinctions between the structures of receptors and binding proteins cannot be madeon the basis of the available data. However, we can list in the first group those proteinsthat the authors have indicated as candidates for olfactory receptors (Table II). All ofthe listed proteins are reported to be membrane bound and to occur uniquely in olfactorytissue. These proteins are all glycoproteins except possibly the two species isolated fromdog olfactory tissue, for which no evidence of this kind was provided.
Odorant binding data have been reported for some of these putative receptors, butnone of them have been used in extensive studies of structure-activity relationships(SAR) that employ a wide spectrum of odorants. A close agreement between bindingconstants and 'in vivo' olfactory data would provide the best evidence for the proposedfunction of specific receptors. Again, however, behavioral measurements are muchmore difficult with vertebrates than with insects.
Other proteins identified in the olfactory organs of both vertebrates and insects arereported to have enzymatic activity on odorants or pheromones. These enzymes aremore stable and somewhat more specific than the cytochrome P-450 enzymes that arealso very active in the nasal cavity. Table III summarizes the few data so far availablein the literature.
The idea that these enzymes could also serve as olfactory receptors is very appealingbecause it could explain the rapid regeneration of odor sensitivity, even after prolongedstimulation. However, SAR studies in both vertebrates and insects do not support thishypothesis, since olfactory receptors and odorant-degrading enzymes recognize theirsubstrates on the basis of different parameters: odor depends mainly on molecular sizeand shape, with little contribution from the nature of functional groups (Beets, 1978),whereas the enzymes act on specific functional groups and are less affected bystereochemicl parameters.
In most cases, enzymes metabolize odorants and pheromones into compounds whichare more soluble in water and therefore easier to eliminate from the system. For instance,
(1) Kasang, 1971.(2) Kasan and Kaissling, 1972.(3) Vogt et al., 1985.(4) Kaissling et al., 1985.(5) Prestwich et al., 1986.(6) Ferlcowich et al., 1973.(7) Ferkowich et al., 1980.(8) Mayer et al., 1976.(9) Kasang et al., 1974.
esters, such as hexadecadienyl acetate (HDA), are transformed into carboxylic acids,that are ionized at physiological pH; alcohols, such as bombykol, and aldehydes arealso oxidized to carboxylic acids, while ketones, such as androstanone are reduced tothe more polar corresponding alcohols.
A third group of proteins that binds odor molecules makes up a separate set sharingseveral common properties. All are soluble proteins of low molecular weight that occurin large concentrations (Table IV). The binding proteins occurring in mammals havebeen named OBP (odorant-binding protein), whereas those in insects are called PBP(pheromone-binding protein). To this list, the following less well characterized proteinscould also be added: pyrazine-binding proteins similar to bovine and rat OBP that arepresent in several mammals (Baldaccini et al., 1986); binding proteins for 5a-androst-16-en-3-one occurring in the sow (Hancock et al., 1985) and for 5a-androstan-3-one occurring in sheep (Persaud et al., 1988a); and a pheromone-bindingprotein present in the moth, Lymantria dispar (Vogt et al., 1987b).
All of the above binding proteins are present in solution and are extremely abundant.Typical concentrations for PBPs are about 10 mM in the sensillar lymph, whereas OBPsaccount for about 1 % of the total soluble protein in nasal tissue extracts of vertebrates.In addition, OBPs and PBPs also share the following similar characteristics, (i) Theirmolecular weights fall within a narrow range (15-20 kDa) and each appears to beconstituted of two identical subunits; the identity of the subunits has been establishedby amino acid sequence analysis in OBPs and in PBPs. (ii) Where the stoichiometryof binding has been measured, as in the two OBPs and in PBP(a) (see Table IV), itis reported that saturation occurs at the ratio of one molecule of ligand per protein dimer.(iii) The isoelectric points are very similar and all occur between 4.5 and 5.1. Thisaspect is not surprising, since a low isoelectric point is essential to allow high
concentrations of the protein to occur in solution at physiological pH. (iv) Both OBPsand PBPs show a broad specificity towards odorants or the corresponding pheromones.Besides 2-isobutyl-3-methoxypyrazine, OBP(r) also binds 3,7-dimethyloctanol andmethyl dihydrojasmonate (Pevsner et al., 1986), while many ligands for OBP(b) havebeen found which belong to several different classes of odorants and chemical compounds(Topazzini etai, 1985; Pelosi and Tirindelli, 1989). Further, the broad specificity ofPBPs, compared to the narrowly tuned response to the pheromone, is clearly illustratedby the observation that HDA, the pheromone of Antheraea polyphemus, is bound byPBPs of other Lepidopteran species that are insensitive to this pheromone (Kaissling,1986). Note again that the insect system provides biochemical, physiological andbehavioral data for the same species, whereas for vertebrates psychophysical data weremeasured with humans, and binding constants with cow or rat.
Possible functions of odorant-binding proteins
Despite all the information obtained on odorant-binding proteins, their role still remainsdifficult to identify. The common characteristics of OBPs and PBPs suggest that theymight have similar functions. While speculating on the role of these proteins, acomparison of olfaction in vertebrates and pheromone perception in insects might helpto evaluate the hypothesis of similar function and suggest new lines of investigation.
The mechanism employed in bacterial chemoreception suggested that OBPs couldmediate the interaction between odorants and membrane receptors. However this modelis unacceptable for olfaction in insects and vertebrates because their soluble bindingproteins exhibit a much lower specificity for different odorants than that expected forolfactory receptors. For example, the narrowly tuned responses of insects to specificpheromones, as measured electrophysiologically or behaviorally, is not complementedby the broad specificity of their soluble pheromone-binding proteins (Kaissling, 1987a).
At present it is generally believed that OBPs play an accessory role in olfaction.However, since their highest concentration occurs in the lateral nasal gland rather thanin the olfactory mucosa (Pevsner et al., 1988b), it remains possible that OBPs reallyhave no role in olfaction. Their property of binding odorants does not necessarily meanthat they contribute to the detection of odorants. Since virtually any volatile compoundof <250 mol. wt is an odorant, OBPs could fulfill the function of protecting therespiratory system from foreign chemicals, thereby augmenting the presumed actionof cytochrome P-450 enzymes. A role of OBPs in the detection of odorants would beproven only after extensive SAR studies on these proteins and on the olfactory receptors.In insects, the presence of PBPs in the sensillar lymph of olfactory hairs suggests thatthese proteins are involved in pheromone perception, because insect antennae areextremely specialized olfactory organs which, unlike the vertebrate nose, are involvedonly in olfaction, not in both olfaction and respiration. Hence the similarity betweenOBPs and PBPs points again to a role of the former proteins in olfaction.
If we want to define the function of the soluble binding proteins in the process ofodor detection in more detail, we find ourselves short of experimental evidence. Wecan only say that both OBPs and PBPs are carrier proteins similar to several other carrierproteins of comparable molecular weight, and homologous to some extent in their aminoacid sequence (Cavaggioni et al., 1987; Pevsner et al., 1988a). The high concentration
of such proteins in the olfacory organ, as well as in other parts of the body, increasesthe solubility of lipophilic compounds in an aqueous medium. Starting with theseobservations, two hypothesis appear equally reasonable: (i) the proteins carry odorantsto receptors; or, (ii) the proteins carry odorants away from receptors.
Based on our knowledge of the physiology of the system, it is difficult to choosebetween the above two hypotheses. In ideal equilibrium conditions, the above questionloses any chemical meaning since the concentrations of the odorants in the mucus andon the receptors are regulated by the relative binding constants, the concentration ofOBP, and the activity of the odorant-degrading enzymes.
In insects, it has been proposed that the anatomy of the sense organ could allow thepheromone to reach the receptor even before interacting with the PBP (Kaissling, 1986,1987a). This would leave only the second hypothesis valid, with PBP as a scavengerfor removing the pheromone in order to maintain receptor sensitivity. Even if we acceptthis mechanism in insects, we cannot conclude that a similar process occurs in vertebratesbecause of the marked differences in the anatomy of the two systems. Furthermore,since the ultrastructure of the insect olfactory half is not yet completely understood,the hypothesis that PBP carries the pheromone to the receptor remains a valid alter-native (Vogt et al., 1985).
Finally, we cannot rule out the idea that OBPs and PBPs act as filters to reduce theconcentration of odorants when they become so high that long-term receptordesensitization could occur. In insects, PBPs could also have an additional functionin reducing the amount of foreign pheromones with similar molecular structures thatcould interfere with receptor activation by the species' own pheromone. This idea issupported by the observation that specific sex pheromones can form complexes withPBPs of other related species.
From the above considerations we can conclude that the pheromone perception systemof moths provides the best model for studying the biochemistry of olfaction in vertebrates,not only with reference to soluble binding proteins and enzymes, but hopefully alsofor the identification and isolation of membrane bound receptor proteins.
Acknowledgements
We thank Dr Trevisan and the Istituto Sperimentale Zoologia Agraria, Padova, Italy,for kindly providing the silkmoth pupae used for the purification of the pheromonebinding protein. This work was supported by C.N.R. Grant No. 87.01668.06.
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