Chemical Senses Vol. 29 No. 8 © Oxford University Press
2004; all rights reserved
A Specific Receptor Site for Glycerol, a New Sweet Tastant for Drosophila: Structure–Taste Relationship of Glycerol in the Labellar Sugar Receptor Cell
1 Department of Developmental Biology and Neuroscience, Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan and 2 Laboratory of Information Biology, Graduate School of Information Science, Tohoku University, Sendai 980-8578, Japan
Correspondence to be sent to: Ichiro Shimada, Department of Developmental Biology and Neuroscience, Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan. e-mail: ishimada{at}mail.tains.tohoku.ac.jp
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Abstract |
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Glycerol, a linear triol, is a sweet tastant for mammals but it has not previously been recognized to stimulate the sense of taste in insects. Here we show by electrophysiological experimentation that it effectively stimulates the labellar sugar receptor cell of Drosophila. We also show that in accord with the electrophysiological observations, the behavioral feeding response to glycerol is dose dependent. 3-Amino-1,2-propanediol inhibited the response of the sugar receptor cell to glycerol, specifically and competitively, while it had almost no effect on responses to sucrose, D-glucose, D-fructose and trehalose. In the null Drosophila mutant for the trehalose receptor (
EP19), the
response to glycerol showed no change, in sharp contrast with a characteristic drastic
decrease in the response to trehalose. The glycerol concentration–response curves
for I-type and L-type labellar hairs were statistically indistinguishable, while those
for sucrose, D-glucose, D-fructose and trehalose were clearly
different. These all indicate the presence of a specific receptor site for glycerol. The
glycerol site was characterized by comparing the effectiveness of various derivatives of
glycerol. Based on this structure–taste relationship of glycerol, a model is
proposed for the glycerol site including three subsites and two steric barriers, which
cannot accommodate carbon-ring containing sugars such as D-glucose.
Key words: chemoreception, electrophysiology, fly, inhibitor, mutant, receptor model
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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Animals select and ingest nutrients among various substances in the environment according to their own requirements and food habits. They must detect various chemicals and discriminate them strictly, which may explain the evolution of multiple stereospecific receptor sites in insect taste cells. For example, the labellar sugar receptor cell of the fleshfly, Boettcherisca peregrina, responds to certain sugars, amino acids and nucleotides. Combining both pharmacological methods and analysis of the structure–taste relationships of stimulants, at least five different sites (pyranose, furanose, aryl, alkyl and nucleotide sites) have been revealed in a single sugar receptor cell (Shimada et al., 1974
;
Shimada, 1987;
Furuyama et al., 1999). Their
stereospecificity for each ligand is rigid. For example, sucrose and D-glucose
react with the pyranose site and D-fructose, L-phenylalanine,
L-valine and adenosine 5'-diphosphate (ADP) bind to the furanose, aryl,
alkyl and nucleotide sites, respectively. Most of these receptor sites have been
suggested to be G-protein-coupled receptors (GPCRs;
Koganezawa and Shimada, 1997). In the
fly genus Phormia, 4-nitrophenyl-
-glucoside and D-galactose
were proven to bind to sites different from the pyranose and furanose sites (Wieczorek and Köppl, 1982;
Wieczorek et al., 1988). The
housefly, Musca domestica, was reported to respond to lactose, which is
instimulative to other flies and the specific site for lactose was suggested to be
present in the sugar receptor cell (Schnuch and
Seebauer, 1998). Lactose, abundant in milk, is of high nutritional value only
for M. domestica (Galun and Fraenkel,
1957). The differences in receptor sites among different species of flies may
therefore be related to their specific food requirements.
In Drosophila, the use of taste mutants and the pharmacological approach
have revealed the existence of a pyranose, a ‘fructose’, a trehalose and
other sites in a single sugar receptor cell (Isono and Kikuchi, 1974;
Rodrigues and Siddiqi, 1981;
Tanimura and Shimada, 1981;
Tanimura et al., 1982;
Wieczorek and Wolff, 1989;
Ueno et al., 2001). Recent
genetic studies have suggested that a family of GPCR genes, the Gr genes,
comprising at least 56 members, encode Drosophila taste receptors. One of these
genes, Gr5a, was the first to be proven functionally to be a specific trehalose
receptor (Clyne et al., 2000;
Dahanuker et al., 2001;
Dunipace et al., 2001;
Scott et al., 2001;
Ueno et al., 2001;
Chyb et al., 2003). Thus,
various sweet taste receptors with rigid stereospecificity for their ligands may have
evolved in the flies.
In mammals, however, receptors for sweet and umami taste are apparently far fewer in
number. T1Rs are a small family of only three GPCRs and candidate receptors, among which
T1R2 and T1R3 associate to function as a broadly tuned sweet receptor for various sugars,
artificial sweeteners and D-amino acids (
Nelson et al., 2001;
Li et al., 2002).
Glycerol tastes sweet to humans (Moskowitz,
1971) and the ability of glycerol to stimulate taste receptors has been
studied electrophysiologically in the gerbil (Jakinovich and Oakley, 1976). In behavioral tests on
Phormia, however, glycerol showed no attractiveness when applied to the tarsi or
single labellar hairs (Dethier, 1955).
In Boettcherisca, preliminary electrophysiological studies (unpublished data)
revealed that glycerol did not stimulate the labellar sugar receptor cell at all.
In the present study, we report electrophysiological evidence that glycerol stimulates the labellar sugar receptor cell of Drosophila, together with corresponding behavioral data. The effects of glycerol are compared to those of sucrose (and D-glucose), D-fructose and trehalose, which are presumed to be typical ligands specific for each of the three receptor sites, that is, the pyranose, ‘fructose’ and trehalose sites, respectively. Several approaches are used to present substantial evidence for the presence of a specific receptor site for glycerol in Drosophila.
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Materials and methods |
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Flies
Strains of Drosophila melanogaster were maintained on a
standard cornmeal agar medium at 25°C. Canton-S, w cx and
EP(X)496 were used as wild types. EP19 was isolated by imprecise
excision of a P-element inserted near the taste receptor gene Tre
(Gr5a) that controls gustatory sensitivity to a disaccharide trehalose. The
mutant has a small genomic deletion that uncovers the whole promotor,
5'-untranslated region and the N-terminal domain of the coding sequence of the gene
and shows noticeably reduced feeding preference to trehalose (Ueno et al., 2001).
Female adult flies (4–6 days old) were fed on cornmeal agar medium for 3 days and then on 100 mM sucrose before the electrophysiological experiments. All the experiments were performed at an ambient temperature of 22 ± 1°C and at a relative humidity of 80–100%.
For behavioral tests, flies were used 1–2 days after eclosion. Prior to the tests, flies were allowed to feed on 100 mM sucrose solution for 2 h and then starved for 24 h, but supplied with distilled water.
Tip-recording method
A glass capillary (tip diameter 50–60 µm) filled with Drosophila
Ringer solution (Ephrussi and Beadle,
1936) was inserted from the abdomen through the head and into the proboscis
and served as an indifferent electrode. Tip-recordings (Hodgson et al., 1955) from the labellar I and L
hairs (Falk et al., 1976;
Nayak and Singh, 1983;
Shanbhag et al., 2001;
Hiroi et al., 2002) were
performed using a recording capillary with a tip diameter of 30–40 µm.
Usually, the electrolyte in which the stimulants were dissolved was 5 mM choline chloride
(Wako Pure Chemical Industries Ltd, Tokyo, Japan). The recording electrode was connected
to a preamplifier (MEZ-7101; Nihon Koden Ltd, Tokyo, Japan) and electric signals were
further amplified, digitized (sampling rate = 20 kHz), stored on computer and
analyzed using MacLab/4s (ADInstrument Ltd). Duration of stimulation was 
1 s with
3–5 min intervals to exclude adaptation effects. The solution at the tip of the
recording capillary was renewed before stimulation by pressing a drop of fluid out of the
capillary before touching a taste hair. The magnitude of the response was defined as the
number of spikes obtained in the period from 0.15 to 0.35 s after the onset of the
stimulus. Most electrophysiological data were obtained from I-type labellar hairs except
those in Figure
7.
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Behavioral tests
Determination of amount of intake
Tests were carried out by using micro test plates with 60 small wells (10 µl
each; Nunc, Denmark) (Tanimura et al.,
1982) filled with glycerol solutions (3–1000 mM) prepared with
1% agar (Difco, noble) and 0.125 mg/ml brilliant blue FCF (a blue food dye). About
20 female flies were introduced into the plate. After being left to feed for 30 min at
25°C in the dark, flies were killed by freezing at –20°C. The amount of
intake was determined colorimetrically after homogenization of the flies which had
ingested the test solutions with the dye. Twenty female flies were homogenized in a
centrifugation tube with a Teflon pestle in 200 µl of modified concentration of
phosphate buffer, pH 7.4, including 75% ethanol. After centrifugation at
15 000 g for 60 min, the absorbance of the supernatant was
measured at 630 nm.
Proboscis extension reflex (PER) for tarsal and labellar stimulation
Flies were fixed by attaching the dorsal thorax to the tip of a glass capillary
(Narishige G-1) with nail vamish after 24 h starvation. For labellar stimulation, their
legs were also immobilized. They were then placed in a humidified chamber for 6 h. Before
the tests they were satiated with water. Flies were selected for tests only if they
showed a clear PER upon touching the whole labellum or legs with a drop of 1 M sucrose
solution. The results were expressed as the number of flies exhibiting a PER to test
solutions.
Chemicals
Meso– erythritol, L-threitol, 1,2,3-butanetriol, 1,2-butanediol, (R)-1,2-propanediol, (S)-1,2-propanediol, 1,3-propanediol, 2-methyl-1,3-propanediol, 1-propanol, 2-propanol, ethylene glycol, 2-amino-1,3-propanediol and 3-amino-1,2-propanediol were purchased from Tokyo Kasei Kogyo Co. Ltd (Tokyo, Japan). Xylitol, D-threitol, D-(+)-glyceraldehyde, DL-glyceraldehyde, (±)-3-methoxy-1,2-propanediol and D-(+)-trehalose were from Sigma-Aldrich Corp. (St Louis, MO). Sucrose and D-(+)-glucose were from Wako Pure Chemical Industries (Tokyo, Japan). D-(+)-fructose, L-serine and ethanol were from Nacalai Tesque Inc. (Kyoto, Japan). In the inhibitor experiments, all the stimulants and inhibitors were dissolved in 1.8 M L-serine buffer (pH 8.4–8.6).
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Results |
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Glycerol stimulates the sugar receptor cell (S cell)
Figure
1 shows the records from an I-type
sensillum, which is known to have only two taste cells (Falk et al., 1976;
Nayak and Singh, 1983;
Shanbhag et al., 2001;
Hiroi et al., 2002). An
L-type sensillum has typically four taste cells, each of which responds to sugar (S
cell), water (W cell) or salts (L1 and L2 cells) (Hiroi et al., 2002). Since the I-type sensilla
lack W cells, W (water) spikes were never observed in Figure
1a when 5 mM choline chloride was used
as the stimulus (which usually elicits only W spikes). In Figure
1b, the I-type sensillum responded to
250 mM sucrose and elicited only one type of regular spikes (S spikes) with equal
intervals. Stimulation of the sensillum with 1M glycerol also elicited only one type of
regular spikes with equal intervals (Figure
1c). Figure
1d shows the response to a mixture of
250 mM sucrose and 1 M glycerol, which resulted in one type of regular spikes with a
higher frequency than each tastant alone. Since stimulation with 250 mM sucrose elicits S
spikes, one of the spike types elicited in the response to the mixture including 250 mM
sucrose must be an S-type spike. It is, therefore, concluded that glycerol stimulates S
cells.
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Figure 2 shows the concentration–response (C–R) curve for glycerol from the S cell. The maximum response (Rm), the stimulus concentration at one-half of Rm (K) and the Hill coefficient were determined using the least-squares method based on the Hill equation. They were 24.0 ± 1.7 impulses/0.2 s, 324 ± 84 mM and 0.94 ± 0.06, respectively (mean ± SEM). The Hill coefficient is close to one, indicating no cooperativity in the response to glycerol and suggesting a 1:1 ligand–receptor interaction.
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Feeding response to glycerol
Behavioral tests are one criterion to know whether glycerol stimulates S cells, since most sugars that stimulate S cells should elicit a PER, where the flies were obsereved to spread their labellar lobes and begin sucking. Figure 3a shows the dependence of the amount of intake (µl/fly) on the concentration of glycerol. The intake volume of glycerol at 15 mM is significantly larger than water alone, while the ingested volume at 1 M was 0.31 µl, which is comparable with that of glucose (data not shown). In Figure 3b, PER was also clearly dependent on the concentration of glycerol. On stimulating the labellum with glycerol, PER approaches 100%, but only rises to 63% at maximum upon stimulating tarsi. This suggests a difference in the information processing between labellar and tarsal stimulation. On the other hand, PERs approaced 100% for both labellar and tarsal stimulation with sucrose, owing to its strong stimulus strength. These behavioral results may support the electrophysiological conclusion that glycerol stimulates S cells.
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3-Amino-1,2-propanediol and 2-amino-1,3-propanediol, specific inhibitors of the response to glycerol
3-Amino-1,2-propanediol and 2-amino-1,3-propanediol themselves were instimulative for the sugar receptor cell in 1.8 M L-serine buffer (pH 8.4–8.6, itself also instimulative for the sugar receptor cell). However, they clearly inhibited the response to glycerol. Figure 4 compares the control responses to glycerol and four sugar tastants alone with those mixed with 100 mM 3-amino-1,2-propanediol or 200 mM 2-amino-1,3-propanediol. The four sugar tastants are presumed to be typical ligands specific for each of the three known receptor sites, namely pyranose (for sucrose and glucose), ‘fructose’ and trehalose sites, respectively. Both 100 mM 3-amino-1,2-propanediol and 200 mM 2-amino-1,3-propanediol specifically inhibited the response to glycerol, while their effects on the responses to other sugars were negligible (Figure 4).
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Effects of 3-amino-1,2-propanediol on the C–R relationships of glycerol
Figure 5 shows the C–R curves of glycerol alone and when mixed with 100 mM 3-amino-1, 2-propanediol in 1.8 M serine buffer. Both curves are sigmoid. From the curves fitted by the Hill equation, Rm, K and the Hill coefficient were determined using the least-squares method (Table 1). The difference in the values for glycerol alone between Table 1 and Figure 2 may be due to the different solvents; 1.8 M L-serine buffer versus 5 mM choline chloride. The two curves in Figure 5 clearly differ in K-value, but not in the maximum response, Rm. The K-value for the mixture of glycerol with 100 mM 3-amino-1,2-propanediol was three times that for glycerol alone, while the Rm values were indistinguishable. The inhibition therefore seems to be competitive and the inhibitor may bind with the specific site for glycerol. Both Hill coefficients are close to unity, but the slope of the C–R curve for glycerol mixed with 3-amino-1,2-propanediol was slightly steeper than that with glycerol alone, reflecting a slightly larger Hill coefficient.
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Response to glycerol in null mutant for trehalose receptor
As shown in Figure
6a, the C–R curves for glycerol
were indistinguishable between the null mutant (EP19) deficient in
trehalose receptor and the wild type (EP(X)496), whereas the response to
trehalose was typically much less sensitive, but still remained distinguishable in the
mutant (Figure
6b). Therefore, the glycerol site
appears to be different from the trehalose site (receptor).
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Comparison of C–R curves for glycerol and various sugars between I- and L-type sensilla
The C–R curves for glycerol were found to be indistinguishable between the I-type and L-type sensilla (Figure 7). The curves for the four sugars were, however, significantly different: the magnitude of each response from the L-type sensilla being statistically larger than that from the I-type. This difference in the C–R curves between glycerol and the four sugars is compatible with there being a specific receptor site for glycerol.
Comparison of the stimulating activities of glycerol derivatives and related compounds
The stimulatory effectiveness of various derivatives of glycerol and related compounds were examined systematically. The concentration for each compound was 1 M. The structure of each is shown in Figure 8 and the results obtained for their stimulating effectiveness are summarized in Table 2.
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Comparison among linear polyols
The order of stimulating effectiveness of polyols is as follows, using the letter codes in Table 2 and Figure 8: triols (a, f) > diols (g, h, i, j, q) > tetrols (c, e, with the exception of d) > pentols (b) > monools (o, p). The triols are the most stimulative; none is as effective as glycerol.
Comparison of diol derivatives with glycerol
Since the diols (h, i, j) are stimulative, but less effective than glycerol, one of
the three hydroxyl groups of glycerol, regardless of the position, is not essential for
stimulation, but necessary to enhance the efficacy of stimulation. When the third
hydroxyl group of glycerol was replaced by a methoxyl group (–OCH3; n)
or a double-bonded oxygen (=O; l, m), the derivatives became much less
stimulative. This may indicate the role of the hydroxyl group as a hydrogen donor in
hydrogen bond formation. When derivatives (h, i) had one extra (g) or one less (q) methyl
group at the third carbon atom, the response was much reduced. Derivatives with three
carbon atoms, therefore, appear to have the optimal stimulating effectiveness.
Substituents larger than hydrogen, such as a methyl (f) or a hydroxyl methyl group (c, d,
e), at the third carbon atom of glycerol decreased stimulating effectiveness. This may
indicate the presence of a steric barrier of the glycerol site near the third carbon atom
of the stimulant, glycerol. Inferences about the third carbon atom of the derivatives can
be applied equally to the first carbon atom owing to the symmetry of glycerol.
Replacement of a hydrogen at the second carbon atom by a methyl group (k) did not affect
the stimulating effectiveness of 1,3-propanediol (j).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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Glycerol is a sweet tastant for mammals, but was previously thought to be instimulative for the taste of insects (Dethier, 1955
;
Moskowitz, 1971;
Jakinovich and Oakley, 1976). The
present study, however, has provided the evidence that glycerol effectively stimulates
the labellar sugar receptor cell of Drosophila (Figure
1). A new receptor site specific for glycerol
3-Amino-1,2-propanediol inhibited the response to glycerol, specifically and
competitively, compared with almost no effects on those to sucrose, D-glucose,
D-fructose and trehalose (Figures
4 and
5). In the null Drosophila
mutant for the trehalose receptor (EP19), the response to glycerol did
not show any change, in sharp contrast with a characteristic drastic decrease in the
response to trehalose (Figure
6). Note that the results of the
present study indicate that in the Drosophila trehalose mutant the response to
trehalose is greatly reduced but not abolished, in contrast to the report of
Dahanuker et al. (2001). The
C–R curves for glycerol from both I- and L-type labellar hairs were statistically
indistinguishable, while those for sucrose, D-glucose, D-fructose
and trehalose were clearly different (Figure
7). These all indicate the presence of
the specific receptor site for glycerol (glycerol site) different from the pyranose,
‘fructose’ and trehalose sites in Drosophila.
Glycerol site model
By comparing the effectiveness of various derivatives of glycerol, we propose a model
of the specific glycerol site composed of three subsites (X, Y and Z) and two steric
barriers A and B (Figure
9). The three subsites form hydrogen
bonds with the three hydroxyl groups of glycerol, which are necessary to evoke an
effective response in the sugar receptor cell. X, Y and Z are proton acceptors. The two
steric barriers take part in the structural specificity of glycerol for stimulation. They
fit the chain of three carbon atoms of glycerol but cannot accommodate a sugar with a
carbon ring, such as glucose. The absolute configuration of glycerol in the glycerol site
in Figure
9 is shown only tentatively since it
has not yet been determined (Uzawa et
al., 1990).
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The relative response of 0.78 of 1,2,3-butanetriol (which has four carbon atoms) can be explained by the steric hindrance to CH3 added to glycerol at the third carbon atom. Threitols (c, d, e) and xylitol (b), with more than three carbon atoms, are expected to undergo similar steric hindrance. Propanediols (h, i, j, k) are moderately stimulative but less so than glycerol since they have only two hydroxyl groups. Due to strong steric hindrance to the methoxy group, 3-methoxy-1, 2-propanediol (n) is almost instimulative. Ethylene glycol, with two carbon atoms and two hydroxyl groups shows low stimulation. With their aldehyde group, glyceraldehydes (l, m) cannot bind to X or Z due to the property of the proton acceptor and so they, too, show a low level of stimulation. Propanols (o, p) are instimulative because they have only a single hydroxyl group.
The specific inhibition of the glycerol response by 3-amino-1,2-propanediol and 2-amino-1,3-propanediol may be caused by the presence of a protonated amino group (–NH3+), which forms an ionic bond with X, Y, or Z. The interaction may be stronger than a hydrogen bond and may freeze any conformation changes at the glycerol site required to evoke the response.
This glycerol site model contrasts with that for pyranose (cf.
Shimada et al., 1974;
Shimada, 1987). Specificity is much
more rigid in the former than the latter, although for both sites three hydrogen bond
formations are necessary to elicit the full response of the sugar receptor cell. Among
the chemicals examined so far, glycerol is the most stimulative and the only natural
substance that reacts with the glycerol site. On the other hand, D-glucose,
sucrose, maltose and various other oligosaccharides with a pyranose ring residue react
effectively with the pyranose site. The difference in specificity may reflect the
difference in function. The glycerol site is specialized to detect glycerol, which is a
marker indicating the presence of yeast (see below). In contrast, the pyranose site is
relatively generalized for detecting substances that are a source of energy (rather than
other kinds of nutrient).
Biological implications of the glycerol site
The presence of various receptor sites of taste cells revealed so far in different fly
species appears to be related to their particular food habits. Yeast is a main component
of the food of the fruitfly Drosophila. It releases ethanol as the product of
fermentation, which attracts the fruitfly. It also synthesizes glycerol (Gancedo et al., 1968), the
intracellular concentration of which approaches 0.9 M (André et al., 1991). This glycerol is
rapidly released from yeast cells upon hypo-osmotic shock (Kayingo et al., 2001). Glycerol is therefore
abundant around yeast. The fruitfly Drosophila can sense concentrations of 15 m
M glycerol (Figure
2) and ingest it (Figure
3a). It is therefore deduced that the
fruitfly is first attracted by the scent of ethanol vapor released from yeast and
subsequently locates and feeds on the yeast by detecting the presence of the less labile
released glycerol, for which the fly may have evolved specific receptor sites in the
labellar sugar receptor cells.
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Acknowledgements |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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We thank Drs H. Ohrui. and K. Kabuto for useful discussions. We also thank Ms N. Yoshimura for her help with the experiments.
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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Accepted August 6, 2004
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