1 Institute of Developmental Biology, Russian Academy of Science, Moscow 117808,
Russia
2 Tula State Pedagogical University, Tula 300026, Russia
Author for correspondence (e-mail:
lnezlin{at}gwdg.de)
Accepted 28 April 2004
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SUMMARY |
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Key words: Mollusc, Conditioned water, Apical sensory neurones, Larval development, Serotonin, Dopamine, Ergometrine-sensitive receptor
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Introduction |
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Freshwater pond snails can be a convenient tool with which to address this
question. In contrast to marine invertebrates that mainly have free-swimming
larvae, they develop inside transparent egg capsules and, hence, are
well-suited for in vivo experimental studies of embryonic and larval
development (Koss et al.,
2003). Thus, in Helisoma trivolvis and Lymnaea
stagnalis, various aspects of neuronal development and larval physiology
have been studied (Goldberg and Kater,
1989
; Goldberg et al.,
1994
; Diefenbach et al.,
1991
; Diefenbach et al.,
1995
; Croll and Voronezhskaya,
1996
; Croll, 2000
;
Voronezhskaya and Elekes,
2003
).
The development of both species is very similar, and provides several
advantages. Adult snails lay transparent egg masses, and each egg contains a
single embryo. Development of all embryos in each egg mass is highly
synchronous. Embryos of both species pass the same larval stages as
free-swimming larvae of marine molluscs
(blastula-gastrula-trochophore-veliger), undergo metamorphosis inside egg
capsules and hatch as miniature juvenile snails. Throughout the intracapsular
development, they have a limited number of easily identifiable neurones
(reviewed by Croll, 2000). At
the trochophore and veliger stages, only one pair of sensory neurones has been
described (Diefenbach et al.,
1998
; Voronezhskaya et al.,
1999
). These neurones differ in their transmitter content: they
express serotonin (5-HT) in Helisoma
(Goldberg and Kater, 1989
;
Diefenbach et al., 1991
;
Diefenbach et al., 1995
;
Diefenbach et al., 1998
;
Voronezhskaya and Elekes,
1993
; Koss et al.,
2003
), and dopamine (DA) and FMRFamide-related peptides in
Lymnaea (Croll and Voronezhskaya,
1996
; Voronezhskaya et al.,
1999
; Voronezhskaya and
Elekes, 2003
). Until the stage of late veliger these cells are the
only monoaminergic neurones in both species.
Important role of monoamines (catecholamines and 5-HT) in development is
well known. In larval molluscs, they appear at the pre-nervous stages
(Buznikov et al., 2003), and
are expressed in the earliest larval neurones including the first nerve
centre, the apical sensory organ (see Page
and Parries, 2000
; Croll at
al., 2003
). Monoamines are known to mediate larval ciliary beat
frequency (Kuang and Goldberg,
2001
), settlement and metamorphosis
(Leise at al., 2001
;
Pechenik et al., 2002b
). Thus,
it is reasonable to suggest that the first monoaminergic sensory neurones may
be also involved in developmental regulation.
The goal of the present study was to test the hypothesis that conspecific
signalling regulating development exists at the early larval stages of
freshwater pulmonate snails, and the first monoaminergic anterior sensory
neurones are involved in mediating this signals. We report below that
juveniles of Helisoma and Lymnaea reared under conditions of
starvation and crowding, release water-born cues, which conspecifically retard
larval development starting from the trochophore stage. To test whether the
anterior monoaminergic neurones mediate transduction of the cues released by
juveniles, we pharmacologically emulated changes in their activity. First,
endogenous monoamine level was augmented by incubation in its immediate
biochemical precursor (Sakharov,
1991; Diefenbach et al.,
1995
). Conversely, the action of 5-HT and DA was reduced by
treating the embryos with commonly used aromatic amino acid decarboxylase
inhibitor 3-hydroxybenzylhydrazine
(Treseder et al., 2003
),
specific inhibitor of tryptophan 5-hydroxylase activity
L-p-chlorophenylalanine (Baker et
al., 1993
; Diefenbach et al.,
1995
; Pani and Croll,
1998
), methylated analogues of respective monoamines
(Sloley and Orikasa, 1988
) and
receptor antagonists (Goldberg et al.,
1994
; Pavlova,
2001
). Developmental changes were correlated with changes in
anti-5-HT immunofluorescence in Helisoma, and glyoxylate-induced
fluorescence of dopamine in Lymnaea within the first anterior
neurones. Our data indicate that anterior monoaminergic sensory neurones
detect the cues released by juveniles in conditions of food limitation and
overcrowding, and increase synthesis of the respective monoamine, which
retards larval development. This inhibitory effect is carried out via
ergometrine-sensitive receptors. This work has appeared previously in abstract
form (Voronezhskaya and Khabarova,
2003
).
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Materials and methods |
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Conditioned water
For conditioning, 200 juvenile snails (length 1.5-2 mm) deprived of food
for 24 hours were rinsed in several changes of FPW, put in a glass jar in 10
ml of FPW, and kept without food for 12 hours. The snails that climbed above
the water surface were returned to the bath with a soft brush. Then,
conditioned water (CW) was pipetted out, filtered through a 0.2 µm
Millipore filter and used immediately. Juveniles were transferred for the next
12 hours to 1 l glass tanks and fed with lettuce. Then, the cycle repeated
(not more then five times for each group of juveniles). Water was also
conditioned by juveniles continuously fed on lettuce or fish chew (i.e.
without preliminary food deprivation). During conditioning, mortality did not
differ from controls (2-3%). To test the stability of CW, it was heated to
80°C for 10 minutes, boiled for 10 minutes, and frozen for up to one month
at -20°C. Developing eggs were also reared in FPW boiled for 20 minutes to
reduce oxygen content. Whenever water was heated or frozen, it was adjusted to
23°C before larvae were added.
Drug incubations
The following drugs were used (all from Sigma-RBI, USA, unless other
specified): serotonin (5-hydroxytryptamine creatine sulphate, 5-HT); dopamine
(DA); 5-hydroxy-L-tryptophan (5-HTP, metabolic precursor of 5-HT);
L-3,4-dihydroxyphenylalanine (L-DOPA, metabolic precursor of dopamine);
-methyl-tryptophan and
-methyl-DOPA (
-m-T and
-m-DOPA, methylated analogues of the precursors);
3-hydroxybenzilhydrazine (NSD-1015); L-p-chlorophenylalanine (PCPA);
ergometrine maleate (EM, antagonist of dopamine receptors, Serva, USA);
sulpiride; spiperone hydrochloride (antagonists of DA and 5-HT receptors);
mianserin hydrochloride; cyproheptadine hydrochloride; ritanserin; and
ketanserin tartrate (antagonists of 5-HT receptors). NSD-1015 and PCPA were
applied 4 hours prior to the first application of CW or monoamine precursors.
Receptor antagonists were applied simultaneously. All drug solutions were
prepared immediately before use. Sulpiride was first prepared as 1 mM solution
in 40% ethanol. Ascorbic acid (50 µM) was added to all solutions to avoid
oxidative breakdown. Equal amounts of ascorbic acid and ethanol (in case of
experiments with sulpiride) were added to controls, and were shown to have no
effect on the development. Embryos were kept in darkness and solutions were
changed daily.
Cell visualization
Immunochemical procedures have been described in detail elsewhere
(Voronezhskaya et al., 1999).
In brief, embryos were fixed in freshly prepared 4% paraformaldehyde in 0.1 M
phosphate buffer (PB, pH 7.4) for 4 hours at 10°C, and washed in 0.1 M PB.
For double immunolabelling, the specimens were incubated in a mixture of
anti-5-HT (DiaSorin, USA, #20080, polyclonal, rabbit, diluted 1:3000) and
anti-acetylated
-tubulin antibody (Sigma, T-6793, monoclonal, mouse,
diluted 1:1500) in PB with 10% normal goat serum, 0.25% bovine serum albumin,
1% Triton X-100 (TX) and 0.03% sodium azide for 72 hours at 10°C. The
specimens were washed in PB three times for 20 minutes, incubated in a mixture
of goat-anti-rabbit Alexa 488-conjugated IgG and goat-anti-mouse Alexa
546-conjugated IgG (Molecular Probes, USA), both diluted 1:800 in PB-TX, for
12 hours at 10°C. Alternatively, the specimens were sequentially incubated
in anti-TH antibodies (DiaSorin, #22941, monoclonal, mouse, diluted 1:3000)
for 72 hours at 10°C, goat-anti-mouse Alexa 488-conjugated IgG (Molecular
Probes) for 12 hours at 10°C, anti-acetylated
-tubulin antibody
diluted 1:3000 in PB-TX, for 4 hours at 10°C, and goat-anti-mouse Alexa
546-conjugated IgG for 2 hours at 10°C. The specimens were washed in PB,
immersed in 50% glycerol in PB and mounted on glass slides in 80% glycerol in
PB.
The specimens were examined as wholemounts with an LSM-510 confocal laser-scanning microscope (Carl Zeiss, Germany) with appropriate wavelength-filter configuration settings. For illustrations, series of optical sections were projected into one image with greater focal depth using LSM-510 software, and imported into Photoshop 7 (Adobe, USA) where only brightness and contrast were adjusted if necessary. The number and step size of optical sections are given for each image in the legends.
The specificity of the ABs used in our experiments has been shown for
various molluscan larvae (see Croll,
2000). Controls included replacement of the primary ABs with
non-immune serum. No specific staining was observed in control preparations.
Reverse of the colours of the secondary ABs (anti-rabbit Alexa 546 IgG and
anti-mouse Alexa 488 IgG) gave identical results.
For glyoxylic acid reaction (De la
Torre, 1980; Voronezhskaya et
al., 1999
), embryos were removed from egg capsules and immersed in
a freshly prepared, buffered glyoxylic acid-sucrose solution (500 mM sodium
glyoxylate, 150 mM sucrose, 50 mM Tris buffer, pH 7.4) on glass slides at
4°C. After 60 minutes of incubation, the solution was removed, and the
embryos were air-dried at room temperature for 30 minutes. Preparations were
then heated to 60°C for 30 minutes, embedded in paraffin oil, and examined
and imaged by using Jenaval (Zeiss) microscope equipped for ultraviolet
epifluorescence (D filter block) and a CCD camera.
Measurements and statistics
The embryos were imaged daily at approximately the same time (from 9 to 12
AM) with a CCD camera attached to a stereomicroscope MBS-10 (L-ZOS, Russia),
and their maximal length was measured with Photoshop 7. To measure brightness
of fluorescence after glyoxylic acid reaction, the cells were imaged with
constant exposure time, and averaged brightness of cell bodies was measured
with Photoshop 7 using the Histogram Tool. Measurements of confocal images
were carried out using LSM-510 software. Statistical analysis and graph
plotting were carried out using Statistica 6 (StatSoft, USA) and Grapher 3
(Golden Software, USA). Results were expressed as means±standard
deviation (s.d.). The significance of differences among groups was evaluated
using Student's t-test. Differences were considered significant at
P<0.05.
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Results |
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Effect of conditioned water
Incubation of embryos of Helisoma (n=122) and
Lymnaea (n=180) in water conditioned by conspecific
juveniles (CW) induced developmental retardation, which was expressed as
elongation of each developmental stage
(Fig. 2A,B). This retardation
manifested itself starting from the trochophore stage 19 (20% of embryonic
development), and followed the appearance of the first anterior sensory
neurones. As a consequence of this retardation, at the time when control
animals completed metamorphosis and became miniature adult-like snails (stage
28, Fig. 2C,E), the treated
animals were at the veliger stage (stage 23) well before metamorphosis
(Fig. 2D,F). The overall effect
of CW resulted in up to twofold prolongation of the larval lifespan (see
Fig. 7). No differences in the
action of CW were detected after incubation of intact or cut egg masses
(n=201 and 215 embryos, respectively) of Helisoma, and
intact egg cocoons or isolated egg capsules (n=284 and 189 embryos,
respectively) of Lymnaea (data not shown).
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The role of monoamines in developmental retardation
To test the hypothesis that the retarding effect of CW is mediated by the
pair of monoaminergic anterior sensory neurones, we pharmacologically emulated
changes in their activity. As the developmental effect of CW manifested itself
starting from the stage 19 (20% of embryonic development) only, all subsequent
drug applications started from this stage. Incubation in solutions of
monoamine precursors inhibited larval development in a species-specific
manner. Thus, in Helisoma, the precursor of 5-HT, 5-HTP (1 mM)
retarded the development similar to CW (n=96), while the precursor of
DA, L-DOPA, was ineffective (n=205; tested up to 10 mM)
(Fig. 3A). By contrast, in
Lymnaea, the retardation was induced by 1 mM L-DOPA (n=128),
while 5-HTP (n=217; tested up to 10 mM) insignificantly slowed the
development only at the time when embryos reached metamorphic stages 25-27
(65-85%) (Fig. 3B). The effects
of monoamine precursors were reversible and ceased after washout
(n=102) (Fig. 3C,D).
The overall effect of respective monoamine precursors was similar to that of
CW (Fig. 7).
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Cellular correlates of developmental retardation
In both Helisoma and Lymnaea, at the stages 19-24 (20-55%
of development), the only cells containing biogenic monoamines and thus being
candidates for mediating the described developmental effects were the anterior
pairs of neurones (Fig. 8) (see
also Voronezhskaya et al.,
1999; Koss et al.,
2003
). In Helisoma, these cells were 5-HT immunopositive
(Fig. 8A). In Lymnaea,
the cells were mainly producing dopamine and thus best visualized by glyoxylic
acid histochemical reaction (Fig.
8B) or using anti-tyrosine hydroxylase antibodies
(Fig. 8C), although they also
demonstrated weak anti-5-HT immunoreactivity
(Fig. 8D). In both species, at
the trochophore stage 19 (20% of embryonic development), the cells looked
similar. They were symmetrically located dorsolateral to the mouth opening
(Fig. 8A,B). Each neurone had a
short thick apical fibre that penetrated the epithelium and bore a tuft of
short non-motile cilia, a long basal fibre and two to five short thin fibres
emanating from the soma and terminating without ramifications in surrounding
tissues (Fig. 8D,E). The basal
fibre ramified extensively and formed varicose fibre network underneath the
apical ciliary plate in Lymnaea
(Fig. 8C) and underneath the
ciliated areas on the foot in Helisoma
(Fig. 8A,F).
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Discussion |
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The involvement of the anterior monoaminergic cells is clear by several
reasons. First, at the tested embryonic stages (trochophore and early veliger)
these neurones were the only monoaminergic cells present and the only sensory
cells described (Goldberg and Kater,
1989; Voronezhskaya et al.,
1999
; Koss et al.,
2003
). Second, the inhibitory effect of CW expressed only after
the appearance of these cells in development. Third, the effect was emulated
by biochemical precursors of monoamines (5-HTP and L-DOPA) corresponding to
the transmitter content of the anterior cells (5-HT in Helisoma and
DA in Lymnaea). Fourth, the effects of both CW and the respective
precursor were equally attenuated by the monoamine synthesis inhibitors
NSD-1015 and PCPA, and the receptor antagonist ergometrine.
In pre-metamorphic veligers (stage 24; 60%), more monoaminergic cells are
added in both species, e.g. two pairs in pedal ganglia and sensory cells in
the foot (Marois and Croll,
1992; Voronezhskaya et al.,
1999
). Nonetheless, we are confident that the developmental
retardation described above was mediated by ASNs only. First, it already
became profound at the trochophore stage 20 (25%), long before the cells in
the foot appeared. Second, the transmitter contents of the cells in the foot
and pedal ganglia are the same in Helisoma and Lymnaea,
whereas the inhibitory effect of CW was mimicked by different chemicals that
corresponded to the transmitter content of ASNs in each species.
Apical cells are activated rather than inhibited in response to the environmental stimuli
Applications of biochemical precursors are widely used to increase
synthesis and release of monoamines in respective neurones (e.g.
McCaman et al., 1984;
Sakharov, 1991
;
Diefenbach et al., 1995
;
Fickbohm and Katz, 2000
;
Pires et al., 2000a
), which is
generally thought to be a result of neuronal activation. Methylated analogues
and synthesis inhibitors are known to significantly reduce concentrations of
respective monoamines as demonstrated by HPLC (e.g.
Hunter et al., 1993
;
Diefenbach et al., 1995
;
Linard et al., 1996
;
Pani and Croll, 1998
;
Pires et al., 2000b
). In
addition, visible changes in immunofluorescence of 5-HT in identified neurones
have been shown to correspond to more than twofold changes in its content
measured by HPLC (Diefenbach et al.,
1995
; Croll et al.,
1997
), and to change the potency of its synaptic and modulatory
actions (Fickbohm and Katz,
2000
). In our experiments, incubation in the respective precursor
resulted in both increase of histo- or immunofluorescence within the ASNs and
developmental retardation similar to that induced by CW. By contrast,
methylated analogues or synthesis inhibitors did not affect and, sometimes,
even facilitated larval development. Together these facts indicate that ASNs
are more probably activated rather then inhibited by the factor present in
CW.
Attenuation of the retarding effect of monoamine precursors by the
synthesis inhibitor, NSD-1015, shows that conversion of the precursors into
the respective monoamines is required. Thus, the active substance in this
process is the respective monoamine but not the precursor itself. Nonetheless,
applications of 5-HT and DA did not affect the development, though exogenous
5-HT is known to induce metamorphosis acting via internal receptors in the
marine gastropod Ilyanassa obsoleta
(Couper and Leise, 1996). One
of the possible explanations is that penetration of monoamines is much easier
in marine larvae than in fresh-water ones. Indeed, in the marine polychaete
Phyllodoce maculata, developmental effects of 5-HT and 5-HTP are
similar (E.E.V. and L.P.N., unpublished). In fresh-water animals however, at
the tested larval stages, exogenous monoamines can act only on the surface
receptors inducing the increase in embryo rotation speed, but do not penetrate
into the embryo and reach the internal targets responsible for developmental
retardation. However, the precursors can be taken up and can induce both the
increase of monoamine synthesis in selective sets of neurones and the
directional release of monoamines. This issue is unclear and needs further
examination.
Monoamines act through the ergometrine-sensitive receptor
None of the tested specific DA and 5-HT receptor antagonists rescued
retardation effect induced by CW and monoamine precursors. Only ergometrine,
the derivate of ergot alkaloids, averted the developmental retardation in both
Helisoma and Lymnaea. This and relative substances have been
used earlier as dopamine receptor antagonists in molluscs
(Juel, 1983;
Sawada and Maeno, 1987
;
Sakharov and Salanki, 1982
;
Pavlova, 2001
). Besides that,
some of the 5-HT1 and 5-HT5 receptors in vertebrates
exhibit high affinity to ergot derivates
(Gerhardt and Heerikhuizen,
1997
). Thus, the receptor mediating the process of developmental
retardation seems to be an internal monoamine ergometrine-sensitive receptor
similar to that described earlier in the CNS of Aplysia
(Shozushima, 1984
;
Shozushima et al., 1987
), and
its pharmacological profile is different from the receptors, which are known
to be involved in embryonic behaviour of developing gastropods
(Goldberg et al., 1994
).
Normal development is under slight tonic inhibition by the activity of ASNs
Acceleration of larval development in Helisoma by PCPA, and
Lymnaea by ergometrine was slight but statistically significant
(Fig. 7). This may indicate
that in normal conditions monoamines are constantly released from the ASNs and
tonically inhibit the development. The degree of inhibition depends on the
activity of this neurones subjected by environmental stimuli. Spontaneous
release of transmitter from growth cones has been shown for embryonic neurones
in culture (Young and Poo,
1983). Diefenbach and co-authors
(1995
) have demonstrated
intensive neurite outgrowth of the anterior serotonergic neurones in
Helisoma trochophores, which was promoted by PCPA and inhibited by
5-HTP, and suggested that the neurones use their own transmitter in an
autoregulatory fashion to regulate neurite formation during embryonic
development. Perhaps neurite growth autoregulation is one of the mechanisms
involved in the developmental effects of monoamines described above. Further
experiments are required to verify this supposition.
Anterior sensory cells in trochophore animals
Two anterior monoaminergic sensory cells, which develop before the onset of
the CNS formation, express 5-HT, innervate locomotory cilia, and degenerate
after metamorphosis, have been described in various pulmonate embryos
(Goldberg and Kater, 1989;
Voronezhskaya and Elekes,
1993
; Diefenbach et al.,
1998
; Voronezhskaya et al.,
1999
; Kuang and Goldberg,
2001
; Koss et al.,
2003
; Voronezhskaya and
Elekes, 2003
), and are generally believed to be the remnants of
the apical sensory organ (ASO), the structure characteristic for trochophore
animals (Nielsen, 2001
). The
basic plan of the ASO is highly conserved regardless of the planctotrophic or
intracapsular developmental mode (Kempf et
al., 1997
; Marois and Carew,
1997
; Dickinson et al.,
1999
; Page and Parries,
2000
; Nielsen,
2001
; Schaefer and
Ruthensteiner, 2001
). It is known to take part in the induction of
larval settlement and metamorphosis (Chia
and Rice, 1978
; Baxter and
Morse, 1992
; Hadfield et al.,
2000
; Leise at al.,
2001
). However, the ASO fully develops much earlier (from several
days to several weeks) than the larva becomes competent for metamorphosis
(Page, 2002a
), and in some
species partly degenerates before metamorphic competence
(Page, 2002b
;
Wanninger and Haszprunar,
2003
). The essential neurotransmitter of the apical neurones,
5-HT, was able to induce metamorphosis in one species only
(Couper and Leise, 1996
). These
observations contradict speculations about a general role of the ASO for the
metamorphic event.
Our data suggest that the function of the apical sensory neurones in early development of pulmonates is to control premetamorphic larval development and inhibit it in response to negative environmental stimuli. Based on structural uniformity of the ASO in diverse larvae, one may speculate that the developmental mechanism we describe is uniform throughout molluscs. Perhaps, after larvae reach metamorphic competence, the functions of the ASO change. The supposition that the ASO plays different roles in pre-metamorphic and competent larvae resolves the contradictions mentioned above.
Comparison with Caenorhabditis elegans
Inhibition of larval development by chemosensory neurones was first
described in the nematode C. elegans (Bargman and Horvitz, 1991;
Thomas, 1993). Under
conditions of crowding and starvation, a specific pheromone was released by
young animals, and detected by chemosensory neurones of larvae. In the
presence of the pheromone, after the second larval molt they differentiated
into a so called dauer larva, an alternative larval form, which did not feed,
did not develop further and was resistant to harsh environmental conditions.
The response to the pheromone was mediated by identified neurones, some of
them being serotonergic (Schackwitz et
al., 1996
; Sze et al.,
2000
).
The authors suggested that similar mechanisms may be used by other
organisms to evaluate environmental signals and regulate their development
(Bargman and Horvitz, 1991). The development of Helisoma and
Lymnaea is the second example of such regulation, when conspecific
chemical signals informing about food shortage and overpopulation, are
detected by sensory cells and retard the development. However, several basic
differences in the mechanisms of the inhibition must be mentioned. Sensory
neurones were inhibited by the pheromone in C. elegans, and excited
in Helisoma and Lymnaea. In C. elegans, inhibition
or absence of these neurones, as well as lack of 5-HT, resulted in the dauer
larva formation, whereas their activation and 5-HT stimulated normal larval
development or dauer recovery (Daniels et
al., 2000; Sze et al.,
2000
). By contrast, in Helisoma and Lymnaea,
both activation of chemosensory neurones and increased synthesis of the
respective monoamine inhibited the development, while their inactivation
facilitated it. In C. elegans, the action of chemosensory neurones
was indirect. They targeted the nervous system and the nervous system in turn
regulated dauer formation by a different mechanism
(Inoue and Thomas, 2000
). In
Helisoma and Lymnaea, however, no central nervous system is
yet developed until the stage 25 (late veliger), thus the action of monoamines
released by the anterior sensory neurones is either direct or mediated by
early transient peripheral peptidergic neurones.
![]() |
Conclusions |
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In addition to demonstrating a novel role for the apical sensory neurones in the development, our study suggests new avenues for future investigations of a link between environmental signals and developmental regulation. Larval pulmonates provide a unique model in which the environmental stimulus, the sensory cells, the acting chemicals and the resulting developmental effects are all known and can be experimentally manipulated. Thus, this model allows the study of downstream mechanisms underlying developmental regulation.
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ACKNOWLEDGMENTS |
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![]() |
Footnotes |
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