Chem. Senses 27: 435-443,
2002
© Oxford University Press 2002
Activation and Inhibition of the Transduction Process in Silkmoth Olfactory Receptor Neurons
Max-Planck-Institut für Verhaltensphysiologie, Seewiesen, D-82305 Starnberg, Germany 1 Present address: Yale University, Department of Molecular, Cellular and Developmental Biology, New Haven, CT 06520-8103, USA
Correspondence to be sent to: Blanka Pophof, Max-Planck-Institut für Verhaltensphysiologie Seewiesen, Postfach 1564, D-82305 Starnberg, Germany. e-mail: pophof{at}mpi-seewiesen.mpg.de
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Abstract |
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Electrophysiological responses of olfactory receptor neurons in both male and female silkmoths (Bombyx mori) were investigated. In both sexes, the G-protein activator sodium fluoride and 1,2-dioctanoyl-sn-glycerol, a membrane-permeable analog of the protein kinase C activator diacylglycerol, elicited nerve impulse responses similar to those elicited by weak continuous stimulation with odorants. Therefore, Gq-proteins and diacylglycerol-activated ion channels seem to be involved in the transduction process in both pheromone-sensitive neurons in males and general odorant-sensitive neurons in females. Decyl-thio-trifluoro-propanone is known to inhibit electrophysiological responses of male moths to pheromones, but has no effect in females. Application of this inhibitor reduced the frequency, but not the amplitude of elementary receptor potentials. It had no inhibitory effect on nerve impulse responses elicited by sodium fluoride or 1,2-dioctanoyl-sn-glycerol. This supports the idea that decyl-thio-trifluoro-propanone acts on a prior step of the transduction cascade, e.g. on the pheromone receptor molecules. General odorants, such as (±)-linalool and 1-heptanol, excite olfactory receptor neurons in females, but inhibit the pheromone-sensitive neurons in males. Both (±)-linalool and 1-heptanol inhibited the responses of male neurons elicited by sodium fluoride or 1,2-dioctanoyl-sn-glycerol. (±)-Linalool reduced the amplitude of elementary receptor potentials. In contrast to decyl-thio-trifluoro-propanone, (±)-linalool and 1-heptanol seem to interfere with later processes of the transduction cascade, possibly the opening of ion channels.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Olfactory reception in moths starts with the adsorption of odorant molecules on the olfactory hairs of the antenna (Kanaujia and Kaissling, 1985
). The hydrophobic odorant molecules pass the hydrophilic
sensillum lymph inside the olfactory sensilla bound to odorant-binding
proteins (Van den Berg and Ziegelberger,
1991; Kaissling,
1996,
2001). Arriving at the
dendritic membrane, they stimulate the odorant receptors localized in the
dendritic membrane of the olfactory receptor neurons. These molecules are
still unknown in moths, but in Drosophila it has been shown that
insect olfactory receptor proteins are, as in vertebrates, 7-transmembrane
G-protein-coupled receptors (Clyne et
al., 1999; Vosshall
et al., 1999). G-proteins of the class Gq/11
were localized in the membrane of moth olfactory receptor neurons (ORNs) and
the G-protein activator sodium fluoride (NaF) elicited nerve impulses in
pheromone-sensitive ORNs of male moths
(Laue et al., 1997).
The Gq-proteins probably activate PLCß
(Maida et al., 2000),
which leads to equimolar production of inositol-1,4,5-trisphosphate
(IP3) and diacylglycerol. Rapid increase of IP3 after
pheromone stimulation was observed in moth antennal homogenates
(Breer et al., 1990;
Kaissling and Boekhoff, 1993).
IP3-receptors were localized in the dendritic membrane of moth ORNs
(Laue and Steinbrecht, 1997)
and IP3-activated Ca-currents were found in cultured moth ORNs
(Stengl, 1993,
1994). In excised inside-out
patches of the dendritic membrane from silkmoth ORNs IP3 was
ineffective, whereas activators of protein kinase C (PKC), such as
diacylglycerol and phorbolester, activated ion channels
(Zufall and Hatt, 1991). The
diacylglycerol analog 1,2-dioctanoyl-sn-glycerol (DOG) elicited nerve impulses
in moth pheromone-sensitive ORNs (Maida
et al., 2000). It could activate ion channels via
increase of the activity of PKC, which activated cation currents in cultured
moth ORNs (Stengl, 1993). A
4-fold increase in PKC-activity after pheromone stimulation was measured in
antennal homogenates of male moths (Maida
et al., 2000).
Most of the above experiments were performed solely on male
pheromone-sensitive ORNs. In the male silkmoth Bombyx mori, the long
sensilla trichodea contain two ORNs responding to the female pheromone
components E,Z-10,12-hexadecadienol, bombykol
(Kaissling and Priesner, 1970)
and E,Z-10,12-hexadecadienal, bombykal
(Kaissling et al.,
1978). The long sensilla trichodea of the female contain two ORNs
responding to benzoic acid and to 2,6-dimethyl1-5-heptene-2-ol as well as
(±)-linalool (Priesner,
1979; Heinbockel and Kaissling,
1996, Van der Goes van Naters,
2001). In the present paper, the male and female ORNs were
investigated to show whether there are differences in olfactory transduction
between the reception of pheromones and of general odorants.
Some compounds, such as the general odorant (±)-linalool and the
esterase inhibitor decyl-thio-trifluoro-propanone (DTFP), are known to inhibit
the reception of pheromones in B. mori males
(Kaissling et al.,
1989; Pophof et al.,
2000). In this paper we have investigated the points at which
these and other compounds disrupt the transduction cascade. In particular, we
studied the influence of the inhibitors on the elementary receptor potentials
(ERPs), which are expected to reflect ion channel openings in response to the
excitation of the receptors by single odorant molecules
(Kaissling, 1994;
Redkozubov, 1999).
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Pupae of B. mori L. (Bombycidae) were obtained from the Istituto Sperimentale per la Zoologia Agraria (Padova, Italy), INRA—Unité nationale séricicole (LaMulatiére, France) and Worldwide Butterflies (Dorset, UK). The animals were sexed at the pupal stage and allowed to emerge at room temperature. The moths were then stored in a refrigerator at 12°C and used for experiments between the ages of 1 and 4 days.
Tip recordings were performed from single sensilla trichodea of isolated
male and female antennae using glass capillary Ag—AgCl electrodes. The
reference electrode was filled with hemolymph Ringer solution and inserted
into the antennal base; the recording electrode was filled with
sensillum-lymph Ringer solution and slipped over the cut sensillum tip
(Kaissling, 1995). The
preparation was held in a permanent airstream (1 m/s) filtered through
charcoal and humidified by percolation through distilled water.
For the application of the G-protein-activating fluoride
(Antonny et al.,
1993), the standard recording pipette was exchanged for a pipette
filled with a modified sensillumlymph Ringer solution, in which sodium
chloride was equimolarly replaced by 20 mM NaF (Sigma)
(Laue et al., 1997).
1,2-Dioctanoyl-sn-glycerol (DOG, Sigma), a membrane-permeable PKC activator,
was applied to the outer dendrite via the recording electrode, which contained
0.1 mM DOG in sensillum-lymph Ringer solution with 0.005% DMSO
(Maida et al., 2000).
This concentration of DMSO had no effect in control experiments performed on
11 male and five female ORNs. A fresh DOG solution was prepared before each
experiment from a stock solution of 20 mM DOG in sensillum-lymph Ringer with
1% DMSO, which was kept frozen.
Two methods were used to apply volatile odorants and inhibitors to the ORNs of sensilla trichodea:
- Capillary stimulation: to elicit weak continuous pheromone stimulation, we
used a capillary containing a cotton thread (2 cm long) loaded with
10-3 µg of either bombykol or bombykal (synthesized by H.-J.
Bestmann, University Nürnberg-Erlangen). The tip of the capillary
(diameter 40 µm) was positioned a few micrometers below the antennal
preparation, within the horizontal permanent airstream, and the pheromones
were allowed to evaporate. To apply high doses of the inhibitor
decly-thio-trifluoropropanone (DTFP, synthesized by A. Guerrero, Barcelona),
10 µg were loaded onto a cotton thread positioned in a capillary and a
short (200 ms) strong air puff was blown through the capillary over the
sensillum (Kaissling,
1995).
- Cartridge stimulation: to apply excitatory or inhibitory stimuli of
intermediate strength, the chemicals were loaded on pieces of filter paper (1
cm2 area) placed in glass cartridges (inner diameter 7 mm). During
stimulation the continuous airstream was passed through the
chemical-containing cartridge. Stimulus load per filter paper was: 0.1 µg
bombykol, 100 µg DTFP, 5 mg and 50 µl (±)-linalool (Sigma) and
1-heptanol (Sigma).
The signals were amplified using a custom-made amplifier with a band pass
DC to 2 kHZ. The unfiltered data were sampled off-line using the data
acquisition program SuperScope (GW Instruments). The parameters measured under
the influence of the different chemicals were the transepithelial potential,
the transepithelial resistance, the nerve impulse frequency of the single ORNs
and the amplitude of the elementary receptor potentials (ERPs). To measure the
resistance of the preparation, an alternating current (0.2 V, 1 Hz) was
injected into the sensillum
(Kodadová and Kaissling,
1996). The amplitude of an ERP was defined as the difference
between the transepithelial potential before the onset of the ERP and the
minimum potential before the nerve impulse occurred
(Figure 3A). Amplitudes of the
ERPs eliciting one or two nerve impulses and separated by at least 100 ms,
were measured. Groups of more than two nerve impulses were probably elicited
by several overlapping ERPs; the amplitudes of such events were not measured.
For statistical analysis, StatView (SAS Institute Inc.), Excel (Microsoft) and
Prism (GraphPad Software) were used. Because of the non-Gaussian distribution
of the data and great variability between the individuals, the nonparametric
Wilcoxon paired signed rank test was used to compare values measured in the
same animals before and after treatment.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Both the G-protein activator NaF (20 mM) and the diacylglycerol analog DOG (0.1 mM) elicited nerve impulse responses in a considerable proportion of male pheromonesensitive ORNs and female general odorant-sensitive ORNs of B. mori (Figures 1 and 2; Table 1). The nerve impulse activation started
1-3 min after the capillary containing the agents
contacted the sensilla. In males, neither compound had any effect on the
resistance of the preparation; they caused a slight, but significant decrease
of the transepithelial potential (Table
2). Both agents significantly increased the nerve impulse
frequency of both male ORNs (Table
2). The effects elicited by NaF and DOG in females were similar to
those in males and resembled responses to weak continuous odorant stimulation
(Figures 1 and
2).
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In males, but not in the females, the nerve impulses were accompanied by small deflections of the transepithelial potential, similar to ERPs but with larger amplitudes of 1 mV or more. Typically, this effect was more pronounced after application of DOG than after application of NaF (Figure 3). Frequency distributions of the amplitudes of spontaneous ERPs of the bombykol cell, compared with ERPs elicited by NaF and DOG, showed that under application of the activators, in addition to ERPs with normal amplitude larger depolarizations occurred (Figure 4A,C). The mean ERP amplitude of the bombykol cell increased significantly after application of DOG, but not after application of NaF (Table 3).
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The number of ERPs in the bombykal cell—either spontaneous or elicited by NaF or DOG—was lower than in the bombykol cell, which corresponds to the lower nerve impulse frequency measured in this cell type (Table 2). The distribution of ERP amplitudes in the bombykal cell was broader during application of DOG in comparison to spontaneous ERPs (Figure 4D). The increase of the mean ERP amplitude after application of DOG was in about the same range as in the bombykol cell, but was not significant due to the lower number of measurements (Table 3). Application of NaF had no apparent effect on the ERP amplitudes of the bombykal cell (Figure 4B; Table 3).
Before testing the effects of inhibitors on ORNs excited by NaF and DOG (Table 1), the modulation of responses to bombykol by (±)-linalool and 1-heptanol were tested. Of 62 tested ORNs of B. mori males, 54 (87%) were inhibited (Figure 5B) and eight (13%) excited by (±)-linalool. In all ORNs, the responses to bombykol were inhibited by (±)-linalool (Figure 5B,C). In two ORNs, (±)-linalool first caused excitation, but then, 40 min later, inhibition of the nerve impulse response (Figure 5D). After the end of (±)-linalool application, often off-responses were observed; these were stronger after previous pheromone stimulation (Figure 5C,D). In nine ORNs inhibited by (±)-linalool, 1-heptanol was also tested and had a strong inhibitory effect on the response to bombykol (Figure 5B); three ORNs were excited by (±)-linalool and 1-heptanol.
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(±)-Linalool reduced the frequency of ERPs elicited by pheromone stimulation slightly in the bombykol cell (Figure 6A) and strongly in the bombykal cell (Figure 6B). During application of (±)-linalool, frequency distributions of the ERP amplitudes showed a shift towards lower values (Figure 6A,B), which was much more apparent in the bombykol cell. The average ERP amplitude decreased significantly in the bombykol cell, but not in the bombykal cell (Table 3). After the end of (±)-linalool application the amplitude and the frequency of ERPs returned to previous values (Figure 6A,B; Table 3). In the bombykol cell, the ERP frequency increased after the end of inhibition (Figure 6A).
The vapor of decyl-thio-trifluoro propanone (DTFP) inhibited nerve impulse responses elicited in ORNs of B. mori males by pheromone stimulation (Figure 7); the frequency of the pheromone-elicited ERPs was strongly reduced in both male ORNs during application of DTFP (Figure 6C,D). Neither the distribution of ERP amplitudes (Figure 6C,D) nor their average amplitude (Table 3) were modulated by application of DTFP.
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Responses elicited by NaF or DOG were clearly not inhibited by DTFP (Table 1; Figure 7); however, they were inhibited by the application of (±)-linalool or 1-heptanol (Table 1; Figure 8b—e). In a few cases of NaF-elicited nerve impulses, these compounds had no effect; in two sensilla treated with NaF, 1-heptanol even activated nerve impulse responses (Table 1; Figure 8f). DOG-elicited nerve impulses were inhibited, in all tested cases, by both (±)-linalool and 1-heptanol (Table 1).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The olfactory transduction cascade in moths starts with the activation of receptors by odorants. The resulting activation of G-proteins leads to the activation of PLCß, followed by equimolar production of IP3 and diacylglycerol. There is experimental evidence that both of them might open ion channels (Stengl et al., 1999
)—see Figure
9. Here, the G-protein activator NaF and the diacylglycerol analog
DOG were used to activate the transduction cascade in both male and female
silkmoth ORNs. Their effects were already known for the male
pheromone-sensitive ORNs (Laue et
al., 1997; Maida et
al., 2000) and here they have been demonstrated for the first
time in the female general odorant-sensitive ORNs (Figures
1 and
2). Furthermore, the class of
Gq-proteins was found in both male and female antennal homogenates
(Laue et al., 1997).
We conclude that in moths the same transduction cascade is involved in
pheromone reception and in general odorant reception. This contrasts with the
situation in mammals, where the IP3/diacylglycerol-dependent
transduction cascade is involved in pheromone reception in the vomeronasal
organ, but cyclic nucleotides transduce the reception of general odorants in
the main olfactory epithelium (Zufall and
Munger, 2001).
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DTFP, which inhibited responses to pheromone, did not inhibit nerve impulse
responses elicited by DOG or NaF. This supports previous evidence
(Pophof et al., 2000)
that DTFP inhibits an earlier step of the transduction cascade, the activation
of the pheromone receptor molecules (Figure
9). DTFP did not modulate the amplitude of pheromone-induced ERPs,
but strongly reduced their frequency. ERPs are thought to represent a small
number of ion channel openings driven by the activation of single odorant
receptor molecules (A.V. Minor and K.-E. Kaissling, personal communication).
DTFP may merely reduce the number of activated receptor molecules.
In contrast to DTFP, (±)-linalool reduced not only the number but
also the amplitude of ERPs in the bombykol cell. Furthermore, the nerve
impulse discharges elicited by DOG and NaF were inhibited by both
(±)-linalool and 1-heptanol. This suggests that the mechanism of action
of these odorants differs from that of DTFP. They might interfere with the
lipids of the plasma membrane and reduce the number of ion-channel openings
per ERP, and they could affect ion channels directly
(Figure 9), as is known for ion
channels involved in olfactory and visual transduction of vertebrates
(Kawai and Miyachi, 2000).
In B. mori females, at much lower doses as used here for
inhibition, (±)-linalool excited strongly and 1-heptanol weakly the ORN
specialized to 2,6-dimethyl-5-heptene-2-ol; the responses to
(±)-linalool seem to consist of an excitatory and an inhibitory
component (Van der Goes van Naters,
2001). This could indicate simultaneous receptor activation and
ion channel inhibition by (±)-linalool in female ORNs. The off-effects
observed after the end of (±)-linalool application in male ORNs could
be explained by a combined excitatory and inhibitory effect, where the
inhibition might have a shorter time-course
(Stange and Kaissling,
1995).
In the silkmoth Antheraea pernyi, inhibitory effects of geraniol
on pheromone-sensitive ORNs were described
(Schneider et al.,
1964). Other workers
(Kaissling et al.,
1989) found in B. mori that 70% of the
bombykol-sensitive ORNs were inhibited, 10% excited and 20% unaffected by
(±)-linalool. This corresponds well with our experiments, where 87% of
the ORNs responding to bombykol were inhibited and 13% excited by
(±)-linalool. These observations show an unexpected inhomogeneity of
pheromone receptors. There are even time-dependent variations, since some ORNs
were first excited and later inhibited by (±)-linalool
(Figure 5D). Furthermore, after
excitation of nerve impulse responses by the G-protein activator NaF, male
ORNs were usually inhibited but in a few cases excited by 1-heptanol
(Table 1;
Figure 8f). Such variable
effects of (±)-linalool and 1-heptanol were observed only after
excitation by pheromone or the G-protein activator NaF. If the transduction
process was activated at a later step by DOG
(Figure 9), both
(±)-linalool and 1-heptanol always had an inhibitory effect
(Table 2). It might be that
(±)-linalool and 1-heptanol inhibit the diacylglycerol-dependent part
of the transduction process, but do not affect the IP3-dependent
part, or even activate it in some cases.
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Acknowledgments |
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We thank K.-E. Kaissling for helpful discussion and critical reading of the manuscript, A. Guerrero for providing the DTFP and A. Thorson for grammatical corrections. The work was supported by the Deutsche Forschungsgemeinschaft (Ka 339/10-2, PO 739/1-1). The experiments comply with the principles of laboratory animal care and the German law on the protection of animals (Deutsches Tierschutzgesetz).
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Accepted February 14, 2002
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