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The Journal of Neuroscience, March 15, 1998, 18(6):2276-2282
Selective Enhancement of P-Type Calcium Currents by Isoproterenol
in the Rat Amygdala
Chiung-Chun
Huang,
Su-Jane
Wang, and
Po-Wu
Gean
Department of Pharmacology, College of Medicine, National
Cheng-Kung University, Tainan City, Taiwan 70101
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ABSTRACT |
We investigated activation of  -adrenergic receptor-adenylyl
cyclase-cAMP cascade on the whole-cell voltage-dependent
Ca2+ currents
(ICa) in acutely isolated rat
basolateral amygdala neurons. Application of -receptor agonist
isoproterenol (Iso) caused a long-term enhancement of
ICa. The effect of Iso was blocked by concurrent application of -receptor antagonist propranolol. However, delayed application of propranolol after the
ICa enhancement did not affect Iso-induced
potentiation, suggesting that the sustained effect was not caused by a
slow washout of Iso. Nimodipine and  -conotoxin-GVIA reduced the
ICa by ~35 and ~29%, respectively, without reducing enhancement of ICa by Iso
significantly. The modulation appeared to involve P-type current,
because the enhancement was abolished after pretreatment with
-agatoxin-IVA. Forskolin, an adenylyl cyclase activator, mimicked
the action of Iso in enhancing ICa,
and this effect was blocked by an inhibitor of cAMP cascade, indicating
a cAMP-dependent mechanism. Iso also induced a long-term potentiation
(LTP) of synaptic transmission, which could be prevented by P-type
Ca2+ channel blockers. These results suggest that
P-type Ca2+ channels were selectively upregulated in
the basolateral amygdala neurons, and enhancement of P-type currents
could contribute to presynaptic form of LTP.
Key words:
isoproterenol; calcium channel; synaptic transmission; long-term potentiation; amygdala; cAMP
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INTRODUCTION |
Protein phosphorylation is a
widespread mechanism for signal transduction in the CNS (Nestler and
Greengard, 1984 ; Levitan, 1985). The actions of presynaptic protein
kinases in the modulation of transmitter release are particularly
important and are probably involved in short- and long-term synaptic
plasticity (Byrne and Kandel, 1996). In mammalian hippocampus, a role
for cAMP and cAMP-dependent protein kinase (PKA) in the induction of
long-term potentiation (LTP), which is a likely mechanism for learning
and memory (Bliss and Lomo, 1973; Bliss and Collingridge, 1993) at the
mossy fiber CA3 synapses has been demonstrated (Huang et al., 1994;
Weisskopf et al., 1994). Mossy fiber LTP required a rise in presynaptic Ca2+ that activated calmodulin-sensitive adenylyl
cyclase and the consequent rise in cAMP, resulting in a long-lasting
enhancement of glutamate release. In contrast, in the Schaffer
collateralCA1 synapses, activation of -adrenergic receptor and
adenylyl cyclase increased transmitter release in a reversible manner
(Chavez-Noriega and Stevens, 1992; Gereau and Conn, 1994). In addition,
cAMP does not act presynaptically to evoke LTP but instead functions as a gate by regulating the activity of phosphoprotein phosphatases postsynaptically (Blitzer et al., 1995; Thomas et al., 1996).
In the amygdala, we have previously shown that activation of
-adrenergic receptor by isoproterenol (Iso) caused a long-term enhancement of EPSP that was accompanied by a decrease in paired pulse
facilitation (Huang et al., 1996). The sensitivity of postsynaptic neurons to the glutamate receptor agonist was unchanged, consistent with a presynaptic site of action. Furthermore, the effect of Iso was
prevented by low concentrations of -agatoxin-IVA (-AgTX), suggesting that enhancement of presynaptic P-type
Ca2+ currents may underlie the action of Iso.
Because the presynaptic terminals are small and difficult to record
from, in the present study we used whole-cell patch-clamp recording
techniques in acutely dissociated amygdalar neurons to directly examine
the effects of Iso and forskolin on the Ca2+
currents.
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MATERIALS AND METHODS |
Slice preparation and intracellular recordings.Male
Sprague Dawley rats (125-150 gm) were decapitated, and transverse
slices (500 µm) were cut from tissue block of the brain using a
Vibroslice (Campden Instruments, Silbey, UK). The slices were placed in
a beaker of artificial CSF (ACSF) oxygenated with 95%
O2-5% CO2 and kept at room temperature for at
least 1 hr before recording. ACSF solution had the following
composition (in mM): NaCl 117, KCl 4.7, CaCl2
2.5, MgCl2 1.2, NaHCO3 25, NaH2PO4 1.2, and glucose 11.
A single slice then was transferred to the recording chamber, in which
it was held submerged between two nylon nets and maintained at 32 ± 1°C. The chamber consisted of a circular well of low volume (1-2
ml) and was perfused constantly at a rate of 2-3 ml/min. A bipolar
stimulating electrode (SNE-200X; Kopf Instruments, Bern, Germany) was
placed in the ventral endopyriform nucleus, near the recording
electrode (1-2.5 mm apart). Orthodromic stimuli were delivered with
monophasic constant-voltage pulses at 0.033 Hz from a Grass stimulator
with an isolation unit.
Intracellular recording microelectrodes were pulled from 1.0 mm
microfiber capillary tubing on a Brown-Flaming electrode puller (Sutter Instruments, San Rafael, CA). The electrodes were filled with 4 M potassium acetate with resistance ranging from 60 to 120 M . The microelectrode tips were positioned into the basolateral subdivision of the amygdala. Electrical signals were amplified by using
an Axoclamp-2A amplifier (Axon Instruments, Foster City, CA) and
recorded on a Gould 3200 chart recorder. For data acquisition and
analysis, pClamp 6.0 running on a 486 personal computer was used. All
data are expressed as mean ± SE. Statistical analysis was
performed using Student's t test, and p < 0.05 was considered statistically significant.
Preparation of isolated amygdalar neurons and whole-cell
recordings.Amygdalar neurons were isolated using a technique
adapted from Kay and Wong (1986). Male Sprague Dawley rats aged 2-3
weeks were decapitated, and serial transverse slices were cut.
Amygdalar regions were dissected under a dissection microscope and then transferred to 10 ml of 1,4-piperazinethanesulfonic acid (PIPES) saline
solution in a spinner flask. The temperature was maintained at 32 ± 1°C, and 2-3 mg of protease XIV (Sigma, St. Louis, MO) was added.
The amygdalar minislices were stirred gently at a rate sufficient to
prevent them from settling, and the solution was bubbled continuously
with 95% O2-5% CO2. The PIPES saline solution contained (in mM): NaCl 120, KCl 5, CaCl2 1, MgCl2 1, glucose 25, and PIPES 20, pH 7.0.
One hour later, slices were washed with 10 ml of PIPES saline solution
(three times) and transferred for storage to a holding chamber filled
with continuously bubbled PIPES saline solution at room temperature.
When needed, a slice was transferred to 1 ml of external solution, and
the neurons were dissociated by trituration using a fire-polished
Pasteur pipette with an ~1 mm tip diameter. The suspension of
dissociated amygdalar neurons then was transferred to a 0.5-1 ml
recording chamber mounted on an Olympus IMT-2 inverted microscope.
Neurons were allowed to settle on poly-L-lysine-coated coverslips.
Whole-cell Ca2+ currents were recorded using a
patch-clamp amplifier (EPC-7, List Electronic) and filtered at 10 KHz.
Patch pipettes were pulled from borosilicate glass and fire-polished with a resistance of 2-5 M. The external solution contained (in mM): CaCl2 3, glucose 10, tetraethylammonium
hydrochloride (TEA) 120, 4-aminopyridine (4-AP) 5, and PIPES 10; 2 µM tetrodotoxin was always added. Pipette solution
contained (in mM): MgCl2 2, PIPES 10, glucose
10, TEA 20, cesium methanesulfonate 100, EGTA 10, Mg-ATP 4, Na-GTP 0.3, phosphocreatine 20, and leupeptin 0.2.
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RESULTS |
To confirm the involvement of P-type Ca2+
channel in the action of Iso, we investigated the effect of -AgTX on
Iso-induced potentiation. Slices were incubated in 10 nM
-AgTX for at least 30 min before being transferred to the recording
chamber where the drug was present at the same concentration. Figure
1 shows that Iso no longer induced LTP in
slices pretreated with -AgTX (103 ± 10%, n = 8). In contrast, the EPSP amplitude was increased to 183 ± 8%
(n = 6) by Iso in slices pretreated with 1 µM nimodipine (Fig. 1). These results suggest the
involvement of P-type currents in the action of Iso.
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Figure 1.
Inhibition of Iso-induced synaptic potentiation by
P-type Ca2+ channel blockers. The EPSP amplitude was
plotted against time. Bars denote periods of application
of Iso (15 µM), -AgTX (10 nM), or
nimodipine (1 µM). The slices were incubated in 10 nM -AgTX or 1 µM nimodipine for at least
30 min before being transferred to the recording chamber where the drug
was present at the same concentration.
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To determine whether the increase in EPSP was in fact caused by a
decrease in IPSP, we examined the effect of Iso on the monosynaptic IPSP. Monosynaptic IPSPs were evoked by focal stimulation in the presence of glutamate receptor antagonists: 10 µM
6-cyano-7-nitroquinoxaline-2,3-dione and 50 µM
D-2-amino-5-phosphonovalerate. Depolarization of the membrane potential increased the amplitude of IPSP, whereas
hyperpolarization of the membrane potential decreased the amplitude of
IPSP. In six neurons, IPSP reversed polarity at  69 ± 2 mV (data
not shown) (Rainnie et al., 1991). Figure
2 shows that Iso had no effect on the
IPSP, in agreement with previous results described by Washburn and
Moises (1992).
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Figure 2.
Iso does not affect the IPSP. Monosynaptic IPSP
was evoked in the presence of 10 µM
6-cyano-7-nitroquinoxaline-2,3-dione and 50 µM
D-2-amino-5-phosphonovalerate. At the end of experiments, 20 µM bicuculline (Bic) was added to
confirm that the IPSP was indeed mediated by GABAA
receptors.
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We tested the effect of Iso on the whole-cell Ca2+
currents (ICa) directly in dissociated
amygdalar neurons. A sustained inward ICa was
normally activated at approximately 40 mV, peaked at 10 mV, and
reversed between +30 and +40 mV (Foehring and Scroggs, 1994; Viana and
Hille, 1996; Wang et al., 1996) when elicited by 200 msec step commands
from a holding potential of 70 mV. We used pharmacological agents to
dissect the ICa. L-type current was defined as
the current blocked by a saturating concentration of 1 µM
nimodipine. On average, nimodipine blocked 35.0 ± 4.2% (n = 9) of the whole-cell current. N-type current was
defined as the current blocked by 1 µM -conotoxin-GVIA
(-CgTX). On average, 29.5 ± 1.1% (n = 5) of
the ICa was blocked by -CgTX. P-type current was defined as the current blocked by a low concentration of -AgTX (10 nM) (Mintz et al., 1992; Randall and Tsien, 1995). On
average, 10 nM -AgTX blocked 20.0 ± 1.3% of the
ICa, which was consistent with previous
results showing a similar degree of ICa blockage by this concentration of neurotoxin (Foehring and Scroggs, 1994).
Figure 3 illustrates the effects of
nimodipine, nimodipine plus -CgTX, and nimodipine plus -CgTX plus
-AgTX in an amgydalar neuron. Nimodipine (1 µM) alone
blocked 27.6% of the current, and nimodipine plus -CgTX blocked
58%. Simultaneous application of nimodipine plus -CgTX plus
-AgTX blocked 71.3% of the current, leaving 28.7% unblocked. The
current that remained in the presence of all three antagonists may
contain Q- and R-type Ca2+ currents that were
subsequently blocked by 100 µM Cd++. A
similar degree of inhibition was observed in five additional cells.
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Figure 3.
Pharmacological separation of
ICa in amygdalar neurons. Plot of peak
ICa versus time is shown for an experiment
in which 1 µM nimodipine, 1 µM nimodipine
plus -CgTX, 10 nM nimodipine plus -CgTX plus
-AgTX, and 100 µM Cd++ were
sequentially applied to an amygdala neuron.
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Figure 4A shows that
bath application of 15 µM Iso persistently enhanced
ICa. On average, Iso increased the current by
54 ± 7% (n = 11; p < 0.001).
Iso apparently did not change the kinetics of
ICa; the current at the beginning of a
voltage command (the peak current) was enhanced by the same degree as
the current at the end of the command. In addition, as can be seen in
Figure 4A, concurrent application of 1 µM propranolol with Iso prevented the effect of Iso
(102 ± 4%, n = 6), indicating the involvement of
-adrenergic receptors. Furthermore, to exclude the possibility that
the sustained effect was caused by a slow washout of Iso from the
slices, we applied propranolol during the washout period. In six
neurons, delayed application of 1 µM propranolol did not affect the Iso-induced sustained enhancement of
ICa (Fig. 4B), suggesting that
the long-term effect was not the result of a continued activation of
-adrenergic receptors by Iso.
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Figure 4.
Persistent enhancement of
ICa by Iso. A, The percent
change of peak ICa was plotted as a function of time.
Bar denotes the periods of delivery of Iso (15 µM) or Iso plus propranolol (1 µM). The
Iso-induced potentiation was prevented by concurrent application of
propranolol. B, Delayed application of propranolol after
ICa enhancement did not affect Iso-induced
potentiation significantly.
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We next examined whether Iso affects a particular type of channel. If
the Iso modulation was of N-type channel exclusively, then no
modulation should be evident in the presence of 1 µM
-CgTX. However, this is not the case. In six cells pretreated with
-CgTX, Iso increased the current by 68 ± 4% (Fig.
5A). The same experimental design was performed by using 1 µM L-type blocker
nimodipine. As illustrated in Figure 5B, Iso increased the
current by 58 ± 10% (n = 6) in the presence of
nimodipine. These data suggest that N- and L-type channels are not
involved in the modulation by Iso. We next tested the hypothesis that
P-type channels were modulated by Iso. Figure 5A clearly
shows that the effect of Iso was completely eliminated by 10 nM -AgTX. The current remained 102 ± 6%
(n = 8) of its baseline.
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Figure 5.
Selective blockade of Iso-induced enhancement of
ICa by -AgTX. A, The
percent change of ICa was plotted as a
function of time. The isolated amygdalar neurons were incubated in 1 µM -CgTX or 10 nM -AgTX for at least 10 min before recordings were made. B, The
bars represent the enhancement of
ICa (mean ± SEM) by Iso in control and
after application of various types of Ca2+ channel
blockers.
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If activation of -adrenergic receptors enhanced
ICa via PKA activation, then a direct activator
of adenylyl cyclase should mimic the effect of Iso. Figure
6A shows that bath
application of 25 µM forskolin produced an effect similar
to that of Iso. On average, ICa was increased by
38 ± 6% (n = 5). Rp-adenosine 3',5'-cyclic
monophosphothioate (Rp-cAMPS), a membrane-permeable PKA inhibitor,
effectively blocked forskolin-induced enhancement of
ICa. In the presence of 25 µM
Rp-cAMPS, the ICa remained 101 ± 1% of baseline
(n = 6; Fig. 6B). Pretreatment of
cells with -AgTX similarly abolished the effect of forskolin
(100 ± 6% of control; n = 6; Fig.
6A).
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Figure 6.
Sustained enhancement of
ICa by forskolin and its inhibition by
-AgTX and Rp-cAMPS. A, The percent change of peak
ICa was plotted as a function of time.
Bar denotes the period of application of 25 µM forskolin. In 10 nM -AgTX-treated
neurons, the neurotoxin was present for at least 10 min before and
during the period of recording. B, The effect of
forskolin was abolished by Rp-cAMPS. The isolated neurons were
incubated with 25 µM Rp-cAMPS for at least 20 min before
and during the period of recording.
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TEA at a concentration that blocks the delayed rectifier
K+ channels has been shown to produce a long-lasting
enhancement of synaptic transmission (Aniksztejn and Ben-Ari, 1991;
Huang and Malenka, 1993; Hanse and Gustafsson, 1994). Therefore, the
delayed rectifier K+ channels could be a possible
target for modulation. The delayed rectifier K+
currents were elicited by depolarization from a holding potential of
70 to +60 mV in the presence of 100 µM
Cd++ and 5 mM 4-AP. This
K+ current was activated on depolarization positive
to 50 mV, and its magnitude increased on further depolarization. In
all six cells tested, Iso had no affect on the delayed rectifier
K+ currents (Fig.
7).
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Figure 7.
Iso does not affect the delayed rectifier
K+ currents. Delayed rectifier K+
currents were elicited by depolarizing pulses over the potential ranges
of 60 to +60 mV from a holding potential of 70 mV in the presence
of 100 µM Cd++ and 5 mM
4-aminopyridine.
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DISCUSSION |
In many excitatory synapses, activation of the PKA pathway has
been shown to increase transmitter release, persistently or reversibly,
depending on the preparations studied. In hippocampal mossy fiberCA3
synapses (Huang et al., 1994; Weisskopf et al., 1994), cerebellar
parallel fiber synapses (Salin et al., 1996), and basolateral amygdala
neurons (Huang et al., 1996), an increase in cAMP and activation of PKA
resulted in a persistent facilitation of transmitter release, a
phenomenon that may have contributed to a presynaptic form of LTP. In
contrast, in Schaffer collateralCA1 synapses, transmitter release
was enhanced in a reversible manner (Chavez-Noriega and Stevens, 1992;
Gereau and Conn, 1994). Thus, it is likely that the
excitation-secretion coupling processes are differentially regulated
by PKA in different brain areas.
Voltage-dependent Ca2+ channels are unique in
neuronal communication in terms of transduction of an electrical signal
(membrane depolarization) via Ca2+ entry into a
chemical signal (neurotransmitter release) (Llinas et al., 1981).
Theoretically, modification of Ca2+ channels could
be an effective means of regulating neurotransmission. However, it is
suggested that reversible enhancement of glutamate release by forskolin
in cultured hippocampal neurons was not attributable to an alteration
in depolarization-evoked increase in intracellular Ca2+ but was accompanied by a direct modulation of
secretory machinery downstream from Ca2+ influx
(Trudeau et al., 1996). It is not known whether the same mechanism
underlies PKA-induced long-term enhancement of glutamate release in
other synapses.
In the present study, we have demonstrated that activation of
-adrenergic receptor and the enzyme adenylyl cyclase persistently increased the whole-cell Ca2+ currents that
paralleled a long-term enhancement of transmitter release. Both effects
were blocked by the P-type Ca2+ channel blocker
-AgTX but not by L- or N-type blockers. These results indicate that
both presynaptic and postsynaptic P-type Ca2+
channels are subject to neuromodulation by PKA, and that long-term enhancement of Ca2+ currents may underlie the
Iso-induced presynaptic form of LTP in the amygdala. However, unless
presynaptic Ca2+ currents and PSPs could be recorded
simultaneously in the basolateral amygdala, it is difficult to prove
directly any causal relationship between P-type channel modulation and
synaptic potentiation. Therefore, we cannot exclude the possibility
that the enhancement of transmission may involve additional mechanisms
such as a direct modulation of secretory machinery downstream from
Ca2+ influx (Trudeau et al., 1996).
The mechanisms involved in Iso potentiation of P-type
Ca2+ channels in amygdalar neurons remain to be
determined. Phosphorylation by PKA modulates voltage-dependent
Ca2+ channels in several excitable cells (Dolphin,
1996). The modulation of L-type Ca2+ channels has
been repeatedly demonstrated in the central neurons (Gray and Johnston,
1987; Kavalali et al., 1997). Only in two studies, one in hippocampal
CA3 neurons and the other in Xenopus oocytes expressed with
human subunits, was selective enhancement of P-type currents via
stimulation of adenylyl cyclase reported (Mogul et al., 1993; Fukuda et
al., 1996), although the reversibility of the drug effect was not
addressed. In the present study, we found that the increase in
ICa outlasted the duration of application of Iso
and administration of propranolol before but not after ICa enhancement prevented the effect of Iso.
These results suggest that the long-term effect was not attributable to
a slow washout of Iso. In the future, it would be of interest to
determine whether long-term effect was caused by a continued kinase
activity by delayed application of Rp-cAMPS or inhibitors of the PKA
catalytic site.
In light of the significant contribution of P-type channels to
presynaptic Ca2+ entry and transmitter release
(Luebke et al., 1993; Takahashi and Momiyama, 1993; Wheeler et al.,
1994), persistent enhancement of these channels will have a profound
influence on neuronal activity in the amygdala. Indeed, behavioral
studies have shown that post-training intra-amygdala administration of
-adrenergic agonists enhances the retention of an inhibitory
avoidance task (Liang et al., 1986). More importantly, in normal
humans, propranolol, a -adrenergic blocker, selectively impaired
long-term memory for an emotionally arousing short story (Cahill et
al., 1994). In addition, the patient with bilateral brain damage
confined to the amygdala failed to show normal memory associated with
emotional arousal (Cahill et al., 1995).
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FOOTNOTES |
Received Sept. 22, 1997; revised Dec. 5, 1997; accepted Jan. 6, 1998.
This study was supported by the National Science Council of Taiwan
Grant NSC86-2314-B006-002 M10. We thank Drs. M. D. Lai and T. H. Leu for their insightful comments on this manuscript.
Correspondence should be addressed to Dr. Po-Wu Gean at the above
address.
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Top
Abstract
Introduction
