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First published online November 2, 2007
Journal of Experimental Biology 210, 3962-3969 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.006577
Histamine operates Cl–-gated channels in crayfish neurosecretory cells
Department of Physiology, Biophysics and Neuroscience, Centro de Investigación y de Estudios Avanzados del IPN (CINVESTAV-IPN), Av. Instituto Politécnico Nacional 2508, San Pedro Zacatenco, 07360 México City, México
* Author for correspondence (e-mail: ugarcia{at}fisio.cinvestav.mx)
Accepted 3 September 2007
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Summary |
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Key words: Cl–-gated channel, ionotropic histamine receptors, X-organ sinus gland system, peptidergic neuron
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Immunohistochemical studies demonstrated the presence of HA-like reactivity in
lobster stomatogastric ganglion neurons
(Dando and Selverston, 1972;
Sigvart and Mulloney, 1982; Mulloney and
Hall, 1991), thoracic and subesophageal ganglia
(Mulloney and Hall, 1991),
olfactory lobe (Orona et al.,
1990), median protocerebrum, and deutocerebrum and tritocerebrum
(Langworthy et al., 1997). By
contrast, in the spiny lobster, 14 neurons in the stomatogastric ganglion
responded to HA, increasing the Cl– conductance
(Claiborne and Selverston,
1984). Both Panulirus argus and Homarus
americanus olfactory receptor neurons are inhibited by micromolar
concentrations of HA acting directly on gating of a Cl–
channel (McClintock and Ache,
1989). In addition it has been demonstrated that HA mediates
presynaptic inhibition in the escape reaction of the Procambarus
clarkii crayfish (el Manira and
Clarac, 1994), as well as presynaptic inhibition of primary
olfactory afferents in lobster (Wachowiak
and Cohen, 1999). It is known that HA injected into the
circulation inhibits the black pigment dispersion that normally occurs in
crabs transferred from a white to a black background in a dose-dependent
manner (Hanumante and Fingerman,
1982). Recently we found that plasma levels of HA in the crayfish
fluctuate during the day, reaching a maximum value at daybreak
(Cebada et al., 2006). This
evidence suggests that HA might be acting as a neuromodulator on the main
neurosecretory structure of the crustacean, the X-organ sinus gland system
(XO-SG). In agreement with our present findings, HA activates a
Cl– current in crayfish X-organ that has comparable
properties to the homomultimeric HA-gated ion channels expressed in
Xenopus oocytes injected with cRNAs that encode for HisCl-1 or
HisCl-
2 (Zheng et al.,
2002; Gisselmann et al.,
2002).
The XO-SG system is formed by 120 monopolar neurons, whose axons converge
within the medulla terminalis, forming a tract that runs distally to end in an
neurohemal organ (SG), located between the medulla interna (MI) and the
medulla externa (ME) of the eyestalk. This system participates in the control
of different functions, such as molting, regulation of blood glucose levels,
tegumentary and retinal pigment position, locomotion and neuronal activity
(Fingerman, 1997;
García and Aréchiga,
1998). Both spontaneous electrical activity and hormone release in
X-organ neurons are regulated by environmental and endogenous influences, such
as light and darkness, stress and circadian rhythms. These influences appear
to be mediated by a host of neurotransmitters or modulators, most noticeably,
GABA, glutamate (Glu) and serotonin
(García and Aréchiga,
1998). GABA and Glu activate independent
Cl–-gated channels in crab X-organ neurons
(Duan and Cooke, 2000). In the
crayfish X-organ neurons GABA induces a biphasic response, where the
excitatory phase is due to the activation of a Na+-dependent inward
current associated with the GABA uptake, that is followed by an inhibitory
phase due to the activation of a Cl– dependent outward
current which is associated with the activation of GABAA-like
receptors (Garduño et al.,
2002).
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Materials and methods |
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Dissection and culture
The method for isolating the eyestalk and intracellular recording was as
described previously (Onetti et al.,
1990). To obtain neuronal cultures, the animals were deeply
anesthetized by burying them in triturate ice for 20 min, then the eyestalks
were excised and placed in chilled crayfish saline solution, consisting of (in
mmol l–1): 205 NaCl, 5.4 KCl, 2.6 MgCl2, 13.5
CaCl2 and 10 Hepes adjusted to pH 7.4 with NaOH. The exoskeleton,
muscles and connective tissue surrounding the neural structures were carefully
removed under a dissecting microscope. Isolated X-organs were incubated with
200 µg ml–1 collagenase dispase (Roche, Mannheim, Germany)
dissolved in modified Leibovitz L-15 (Gibco, Rockville, MD, USA) culture
medium for 60 min. The enzyme was washed out, and the X-organ neurons were
dissociated by gentle suction through fire-polished micropipettes, as
described previously for the leech Retzius cells
(García et al., 1990),
and plated onto a 200 µl recording chamber, precoated with Concanavaline A
(Type III, Sigma, St Louis, MO, USA). The ionic composition of the culture
medium was adjusted to that of the crayfish saline solution. An additional 5.5
mmol l–1 glucose, 2 mmol l–1
L-glutamine, 16 µg ml–1 gentamycin
(Schering-Plough, Mexico City, Mexico), 5 µg ml–1
streptomycin (Sigma) and 5 units ml–1 penicillin (Sigma) were
added. Culture cells were kept in darkness for 24 h before the experiments
were conducted.
Electrophysiology
Current- and voltage-clamp experiments in the standard whole-cell
configuration were performed in X-organ neurons plated in the recording
chambers, and mounted on the stage of an inverted microscope Diaphot (Nikon,
Melville, NY, USA). The cells were continuously superfused with crayfish
saline solution, but in some experiments, the bath solution was modified by
reducing the NaCl concentration to 80 mmol l–1 and replaced
equimolarly by sodium-methanesulfonate. Recordings were carried out using an
Axopatch 200A amplifier (Axon Instruments, Sunnyvale, CA, USA) and then the
low-pass filtered at 10 kHz with a four-pole Bessel filter and stored on a
computer disk using commercially available hardware and software (Axon
Instruments). To eliminate error signals caused by the pipette and holder
capacitance, in cell-attached configuration, a –5 mV pulse was applied
to cancel the fast transient. The same pulse was used in the whole-cell
configuration to compensate both the cell membrane capacitive current and the
series resistance, using the compensation circuits of the amplifier. The
series resistance was estimated in the range 2.5–4.5 M
and
reduced by 50–70%. Recording electrodes (2–3 M) from
borosilicate glass (Sutter Instruments, San Rafael, CA, USA) were filled with
a solution consisting of (in mmol l–1): 195
KCH3SO4, 12 KCl, 2 CaCl2, 2 MgCl2,
5 EGTA-Na and 10 Hepes.
HA pulses were applied through a `Y' tube placed 100 µm from the neurons, with continuous superfusion of crayfish saline solution. HA, mepyramine, tiotidine, cimetidine and ranitidine were purchased from RBI (Natick, MA, USA) and picrotoxin, bicuculline, strychnine and d-tubocurarine from Sigma. All solutions were prepared on the day of use.
Immunocytochemical staining
The eyestalks were fixed overnight in Bouin's solution at 4°C (10%
formaldehyde, 5% glacial acetic acid and 75% picric acid, saturated aqueous
solution), and then washed several times in sodium phosphate buffer (PBS) 0.1
mol l–1, adjusted to pH 7.4. Then the eyestalks were
permeabilized by incubation overnight with PBS solution containing 5% Triton
X-100 (PBS-Triton). To prevent non-specific binding, the eyestalks were
incubated for 4 h in a blocking solution consisting of 10% normal goat serum
(Vector Lab., Burlingame, CA, USA) in PBS-Triton. After washing, the neural
tissues were incubated in the primary antibody for 3 days at 4°C (rabbit
anti-HA polyclonal antibody, Chemicon Int. Inc., Temecula, CA, USA), this
antibody was diluted 1:500 in PBS-Triton. Then the eyestalks were rinsed three
times and incubated in the secondary antiserum for 5 h at room temperature
under darkness. Secondary antibody solution was goat anti-rabbit conjugated
with fluorescein (FITC; 5 µg ml–1; Vector Lab.) in the
same buffer as the primary antibody. After washing, the eyestalks were
dehydrated in a graded alcohol series from 50% to absolute ethanol (5 min
each) and cleared with methylsalicylate (Merck, Darmstadt, Germany). The
stained eyestalks were visualized using a confocal microscope TCS P2 (Leica,
Heildelberg, Germany) equipped with an Argon-Crypton ion laser. Optical
sections (1 µm) were collected in sequential mode and examined in
stacks.
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Results |
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To test whether HA activated a Cl– current, X-organ neurons were dissociated and cultured for 24 h and the HA-evoked response was recorded in current-clamp conditions at membrane potentials from –100 to –20 mV using pipettes filled with the described internal solution. The voltage changes accompanying the HA response were dependent on the membrane potential; in all cases, voltage changes evoked by HA caused the membrane potential to decrease to –60 mV (Fig. 2A). Hyperpolarizing responses were observed at less polarized potentials and depolarizing responses at more polarized potentials. The reversal potential value suggested that the response is mediated by a Cl– current. In addition, in voltage-clamp conditions HA-evoked currents reversed at the Cl– equilibrium potentials (ECl) recorded. As illustrated in the Fig. 2B, HA-evoked currents reversed between –65 and –55 mV when the ECl corresponded to –62.5 mV and reversed between –40 and –30 mV when the extracellular solution was modifed to obtain a new ECl (–32 mV). The results of these experiments are summarized in Fig. 2D. The current–voltage curves obtained for both experimental conditions indicated that the zero current potential corresponded to –60±3 mV and –32±2 mV.
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In agreement with previous results for some other HA-activated
Cl– channels (Hardie,
1989), the time course of the response to HA developed with
latency <0.5 s, making it unlikely that a second messenger is involved.
This conclusion is supported by the long-term stability (at least 1 h) of
whole cell currents in the presence of only simple buffered saline.
HA activates receptors other than GABA or Glu in X-organ neurons
Previous work (Duan and Cooke,
2000) has shown that GABA and Glu activate different receptors and
Cl– conductances in crab X-organ neurons. To explore the time
course of the currents elicited by HA, GABA or Glu, the cells were maintained
at –40 mV holding potential using the standard pipette solution
(calculated Nernst potential, ECl is approximately
–62.5 mV), in order to evoke Cl– outward currents in
each case. For Glu responses, in 50% of the neurons tested (N=12),
the Glu-evoked current reached its maximum value within the first 300 ms and
then declined to 20% of the peak amplitude, generating a sustained current
during the continued application of Glu
(Fig. 3A). In the other 50% of
the cells, Glu elicited a fully desensitizing current; similar results have
been described previously (Duan and Cooke,
2000). By contrast, as previously reported in crayfish X-organ
neurons (Garduño et al.,
2002), GABA-evoked currents exhibited two components: an early
transient inward current due to the electrogenic GABA uptake, followed by a
sustained outward current generated through ligand-gated Cl–
channels (Fig. 3A, middle
trace). Finally, the HA-evoked current declined slowly during the continued
application (Fig. 3A, right
trace). The time courses of the currents activated by Glu, GABA or HA suggest
that different receptor types mediate each one of these responses. However,
possible heterologous desensitization by GABA or Glu of the HA-evoked current
was explored. Both Glu- and GABA-evoked Cl– currents in
X-organ neurons show significant desensitization when low concentrations of
such substances are present in the bathing solution during the application of
test pulses at concentrations close to the respective EC50 values
(10 µmol l–1 for GABA and 32 µmol l–1
for Glu). Fig. 3B (upper
traces) shows superimposed recordings obtained in response to Glu pulses
applied before, during and after the superfusion of a low Glu concentration (3
µmol l–1). The trace marked by the arrow was obtained
under these conditions; note that the transient current was reduced notably
but the amplitude of the sustained current remained the same. The other two
traces correspond to the control condition and after the Glu washout. The
recordings shown in Fig. 3B
(bottom) were obtained from the same neuron but in response to HA, before,
during and after the superfusion of Glu. Note that neither the amplitude nor
the time course of the HA response was modified. Similar results were obtained
when 1 µmol l–1 GABA was superfused during the HA pulse
application (Fig. 3C).
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HA dose–response relationship
The dose–response was explored by applying histamine pulses at
concentrations between 0.01 to 100 µmol l–1; at least five
concentrations were tested in the same cell with washout intervals of 3 min.
Low HA concentrations (0.01 to 0.1 µmol l–1) failed to
induce detectable currents, whereas concentrations between 1 and 2.5 µmol
l–1 elicited sustained currents. Higher concentrations
(5–100 µmol l–1) induced a fast desensitizing
component followed by a slower desensitizing component
(Fig. 4A). The HA-induced
current was measured at the peak and these values were plotted against the log
of the HA concentration, giving a concentration inducing a half-maximal
response (EC50) of 3.28±1 µmol l–1 and
Hill number of 2.6±0.4 (Fig.
4B). The EC50 value for HA differs considerably from
those reported for Glu and GABA (Duan and
Cooke, 2000; Garduño et
al., 2002). Previous work has shown that the homomeric expression
of the mRNAs encoding HA-gated Cl– channel subunits from the
fruit fly Drosophila melanogaster produced HA receptors with
EC50 values of 166±12 µmol l–1 for
DM-HisCl-1 and 10.8±0.46 DM-HisCl-2
(Gisselmann et al., 2002),
whereas those for HisCl-1 and HisCl-2 were 4.2±1.3 and 14±2.5,
respectively (Zheng et al.,
2002). The HA receptor sensitivity in X-organ neurons was close to
the homomultimeric HA-gated Cl– channels HisCl-1 and
DM-HisCl-2. The pharmacological profile of the HA response in X-organ
neurones cannot easily be classified within the pharmacological categories
developed in mammals. The histamine receptors are a class of endogenous
ligand. Activation of HA metabotropic receptors involves cytoplasmic second
messengers, cofactors, coupling proteins and enzymes, and often could not
occur in cells perfused internally by salts alone
(Hille, 2001). Our results
suggest that the HA response is mediated by ligand-gated anion channels.
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Pharmacology
Cl– channel blockers
Picrotoxin at concentrations between 1 and 100 µmol l–1
blocks most of the inhibitory Glu receptor, as well as GABAA-like
receptors from invertebrates (Lunt,
1991; Cleland,
1996). In contrast, the Cl– currents evoked by HA
in crustacean preparations are insensitive to picrotoxin
(Claiborne and Selverston,
1984; McClintock and Ache,
1989; Hashemzadeh-Gargari and
Freschi, 1992; el Manira and
Clarac, 1994). We found that the HA response in X-organ neurons
was also insensitive to picrotoxin even at high concentrations (100 µmol
l–1). Fig. 5A
illustrates representative current traces obtained before, during and after
picrotoxin superfusion.
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To date, glycine-gated Cl– channels have not been
identified in invertebrates (Roeder,
2003), but the HA-gated Cl– channel subunits from
Drosophila melanogaster show the highest degree of homology to human
glycine receptors (Witte et al.,
2002). By contrast, strychnine is a specific antagonist of these
receptors that reversibly inhibited the glycine-induced currents. We did not
detect glycine-evoked currents in X-organ neurons (N=12) nor blockage
of the HA-evoked currents with strychnine concentrations of 10–100
µmol l–1 (Fig.
5B).
The inhibitory effect of the competitive antagonist from the curare family,
d-tubocurarine (dTC), on HA-activated Cl– channels
in crustacean preparations such as stomatogastric ganglion cells
(Claiborne and Selverston,
1984), olfactory receptor neurons
(Bayer et al., 1989) and
cardiac ganglion motor neurons
(Hashemzadeh-Gargari and Freschi,
1992), is well documented, as well as in oocytes that express
HA-gated Cl– channels
(Gisselmann et al., 2002). In
agreement with the above-mentioned reports, we found that dTC reversibly
blocked the HA response in X-organ cells with an IC50 of
21±2 µmol l–1
(Fig. 5E).
Fig. 5C shows current traces
elicited by 20 µmol l–1 HA obtained after and during the
superfusion of dTC at the indicated potentials. Note that the blockage exerted
by the antagonist was dependent on the holding potential, resulting in more
effective hyperpolarizing potentials (Fig.
5D). This result supports the notion that the HA
Cl–-gated current in crayfish X-organ neurons is generated by
native receptors, with similar characteristics to those described for DM-HisCl
receptors.
HA antagonists
Fig. 6 illustrates the
effect on the HA-evoked currents obtained at –40 mV from four different
cells, before, during and after the superfusion of competitive antagonists
type H1 and H2. In the presence of mepyramine (500 µmol
l–1), the residual current desensitized rapidly and almost
completely (Fig. 6A), whereas
in the presence of the H2 antagonists (ranitinine, tiotidine and cimetidine),
the residual current did not showed desensitization during the continuous
application of HA (Fig.
6B,C,D). The blockage exerted by all the antagonists was fully
reversible. Mepyramine was the least potent, at concentrations of 1–10
µmol l–1, and the amplitude of the HA-evoked current
remained unchanged, reaching complete inhibition at concentrations close to 2
mmol l–1, and with an IC50 of 483±11
µmol l–1 (Fig.
6E, triangles). The IC50 values for the H2 antagonists
were 40±1.3 µmol l–1 for tiotidine, 98 ±2.6
µmol l–1 for cimetidine and 256±11 µmol
l–1 for ranitidine (Fig.
6E, squares, diamonds and circles, respectively). These results
are in agreement with previous reports where Cl–
conductance-gated by HA in Musca domestica and crustacean neurons was
blocked predominantly by H2 antagonists
(Hardie, 1989;
McClintock and Ache, 1989;
Hashemzadeh-Gargari and Freschi,
1992). In addition, the pharmacological profile that we found is
quite similar to those reported for the HA-gated Cl– channel
type DM-HisCl-2 functional expressed in oocytes (Gisselman et al.,
2002).
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), so
it is reasonable to suppose that the HAergic neurons contact with the
neurosecretory system, however to date there are no reports to suggest that
these presynaptic effects are evoked by the XO-SG system.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Long-term intracellular recordings from X-organ neurons
showed that the cells are silent or display a low-level of tonic activity
during the morning and early afternoon hours, but change dramatically toward
the late evening to a fully-fledged pattern of burst activity
(García and Aréchiga,
1998). Overall these studies proved that HA is involved in the
modulation of the X-organ excitability. In the present study, we have
demonstrated that HA operates Cl–-gated channels in the
X-organ neurons. These findings indicate that control of neural activity by HA
could be a mechanism underlying the hormonal secretion from the XO-SG system
to synchronize a variety of circadian physiological functions.
HA activates a Cl– conductance
Four pharmacologically distinct metabotropic G-protein-coupled HA receptor
subtypes have been described and cloned from mammals
(Gantz el al., 1991;
Yamashita et al., 1991;
Lovenberg et al., 1999), and
two ionotropic receptors predicted from Drosophila melanogaster
genome coding for HA-gated Cl– channels by functional
expression in Xenopus oocytes have been described
(Gisselmann et al., 2002;
Zheng et al., 2002). HA
directly activates a Cl– conductance in a number of
invertebrates, including mollusks (McCaman
and Weinreich, 1985), insects
(Hardie, 1989;
Stuart, 1999) and crustaceans
(Clairbone and Selverston, 1984; Prell and
Green, 1986; McClintock and
Ache, 1989;
Hashemzadeh-Gargari and Freschi,
1992). The receptor types mediating these effects are unknown, but
could be related to the novel ligand-gated anion channel from the fruit fly.
Our results indicate that exogenous HA elicits an inhibitory response in both
in situ and cultured X-organ neurons; this response is mediated by an
increase in membrane conductance that reversed at the expected
Cl– equilibrium potential. In addition the time course of the
response to HA developed with short latency, and the long-term stability of
whole cell currents in the presence of only simple saline support the notion
that the Cl– current in X-organ neurons is generated by
ionotropic receptors.
Pharmacology of the HA receptor
In agreement with previous reports
(Claiborne and Selverston,
1984; McClintock and Ache,
1989; Hashemzadeh-Gargari and
Freschi, 1992; el Manira and
Clarac, 1994), we found that picrotoxin at concentrations between
10 and 100 µmol l–1 was incapable of blocking the
Cl– current evoked by HA. This is an advantage, making it
easy to distinguish between the GABA- or the Glu-gated Cl–
currents that are present in X-organ neurons. In addition, the DM-HisCl
receptors expressed in oocytes show a weak sensitivity to picrotoxin
(Gisselmann et al., 2002;
Zheng et al., 2002).
The HAergic antagonists H1 and H2 have been used to characterize native
HA-invertebrate receptors and the HA evoked current is consistently more
sensitive to H2 blockers (Haride, 1988;
McClintock and Ache, 1989;
Hashemzadeh-Gargari and Freschi,
1992; Gisselmann et al.,
2002). In the X-organ neurons the HA response was more efficiently
inhibited by H2 antagonists (tiotidine, cimetidine and ranitidine) than by the
H1 antagonist (mepyramine). The pharmacological profile that we found is close
to that reported for the homomeric DM-HisCl-2 receptor
(Gisselmann et al., 2002);
however it could correspond to the expression of the homomeric channels
HisCl-1 (Zheng et al., 2002).
Further studies of molecular biology should help to confim the homology
between fruit fly HA receptors and crustacean HA receptors.
List of abbreviations
1
2
-aminobutiric acid receptor type A
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Acknowledgments |
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