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1 Department of Pharmacology, We examined the role of
K+ channels in the secretion of
adrenal catecholamine (CA) in response to splanchnic nerve stimulation (SNS), acetylcholine (ACh), 1,1-dimethyl-4-phenyl-piperazinium (DMPP),
and muscarine in anesthetized dogs.
K+ channel blockers and the
cholinergic agonists were infused and injected, respectively, into the
adrenal gland. The voltage-dependent K+ channel
(KA type) blocker mast cell
degranulating (MCD) peptide infusion (10-100 ng/min) enhanced
increases in CA output induced by SNS (1-3 Hz), but it did not
affect increases in CA output induced by ACh (0.75-3 µg), DMPP
(0.1-0.4 µg), or muscarine (0.5-2 µg). The
small-conductance Ca2+-activated
K+
(SKCa) channel blocker
scyllatoxin infusion (10-100 ng/min) enhanced the ACh-, DMPP-, and
muscarine-induced increases in CA output, but it did not affect the
SNS-induced increases in CA output. These results suggest that
KA channels may play an inhibitory role in the regulation of adrenal CA secretion in response to SNS and
that SKCa channels may play the
same role in the secretion in response to exogenously applied
cholinergic agonists.
adrenal gland; mast cell degranulating peptide; scyllatoxin; voltage-dependent potassium channels; small-conductance
calcium-activated potassium channels
THE CATECHOLAMINE (CA) secretion from the adrenal
medulla is controlled by splanchnic nerve-innervating chromaffin cells. Activation of the splanchnic nerve causes the release of acetylcholine (ACh) from its terminal into the intrasynaptic cleft, which
subsequently activates nicotinic receptors of the adrenal medullary
chromaffin cells. Stimulation of nicotinic receptors depolarizes the
chromaffin cell membrane, and the resulting depolarization causes
Ca2+ influx through the opening of
voltage-dependent Ca2+ channels
(5, 6). The elevation of intracellular
Ca2+ triggers the exocytotic
secretion of adrenal CA (8). The membrane depolarization may activate
voltage-dependent K+ channels,
leading to the facilitation of repolarization, and the elevation of
intracellular Ca2+ may activate
Ca2+-activated
K+ channels, leading to
hyperpolarization. The facilitation of repolarization or hyperpolarization may cause the inhibition of further influx of
Ca2+. Therefore, blockade of
K+ channels is thought to
facilitate the depolarizing phase and results in the enhancement of
adrenal CA secretion through the increase in
Ca2+ influx.
Subtypes of K+ channels have been
identified in various tissues (25), including adrenal medullary
chromaffin cells (20). It has been reported that
KA channels, one type of
voltage-dependent K+ channel, are
located in sympathetic neurons in the bullfrog (1) and the rat (4, 7).
These experiments suggest that KA
channels play an important role in the regulation of neuronal
excitability. However, the physiological role of
KA channels in the regulation of
adrenal CA secretion has not been understood. On the other hand,
small-conductance Ca2+-activated
K+
(SKCa) channels, one type of
Ca2+-activated
K+ channel, have been
characterized by indirect regulation of
Ca2+ movement and CA secretion in
chromaffin cells in the bovine (18, 30) and the cat (22, 28, 29).
Recently, we suggested that apamin-sensitive
SKCa channels may play an
inhibitory role in the regulation of adrenal CA secretion in the dog
(23).
In the present study, we investigated the effects of mast cell
degranulating (MCD) peptide, a selective
KA channel blocker (27), in
comparison with scyllatoxin, a selective
SKCa channel blocker (10), on the
secretion of CA induced by splanchnic nerve stimulation (SNS), ACh,
1,1-dimethyl-4-phenyl-piperazinium (DMPP), and muscarine in
anesthetized dogs to elucidate a functional role of
KA and
SKCa channels in controlling the
secretion of adrenal CA. MCD peptide, scyllatoxin, and cholinergic
agonists were administered intra-arterially into the adrenal gland to
eliminate their hemodynamic influences on adrenal CA secretion.
Animal preparation.
Mongrel dogs of either sex, weighing 8-12 kg, were anesthetized
intravenously with 30 mg/kg of pentobarbital sodium, and a constant
level of anesthesia was then maintained by an intravenous infusion of
pentobarbital sodium at a rate of 6 mg · kg Administration of drugs into the adrenal gland.
The procedure for intra-arterial administration of drugs into the
adrenal gland was reported previously (15). The left phrenicoabdominal artery was dissected to expose its origin from the abdominal aorta. A
needle connected to a Y-shaped polyethylene catheter was inserted into
the phrenicoabdominal artery at its origin for intra-arterial infusion
of 0.9% saline solution (as a vehicle), MCD peptide, and scyllatoxin.
These drugs were infused into the adrenal gland by using an infusion
pump (975E, Harvard Apparatus). ACh, DMPP, and muscarine were injected
for 3 s during saline, MCD peptide, and scyllatoxin infusion.
SNS.
The left splanchnic nerves were dissected free from surrounding tissue
and cut. A bipolar platinum electrode was placed in contact with the
distal end of the splanchnic nerves. The splanchnic nerves were
stimulated with rectangular pulses of 1 ms and 10 V (supramaximal
voltage) delivered by an electronic stimulator (SEN-1101, Nihon Kohden)
and an isolation unit (SS-101J, Nihon Kohden). Stimuli were applied at
1 Hz for 2 min and subsequently at 2 Hz for 2 min and 3 Hz for 2 min
during a 6-min stimulus period.
Experimental protocol.
The dogs were divided into eight groups (groups
1-4
and groups
5-8,
MCD peptide and scyllatoxin experiments, respectively). In
group
1 (n = 6), the effect of MCD peptide on the SNS-induced increase in CA
output was examined. SNS was repeated four times at 30-min intervals.
The first SNS trial during the infusion of 0.9% saline solution into
the adrenal gland was regarded as a control. MCD peptide infusions (10, 30, and 100 ng/min) were started 5 min before the start of the second,
third, and fourth SNS, respectively. In
group
2 (n = 6), the effect of MCD peptide on the ACh-induced increase in CA
output was examined. A set of ACh injections (0.75, 1.5, and 3 µg)
into the adrenal gland was repeated four times at 40-min intervals. The
interval between each dose of ACh was 10 min. The first set of ACh
injections during the infusion of 0.9% saline solution was regarded as
a control. MCD peptide infusion was started 5 min before the second,
third, and fourth set of ACh injections, respectively. In
groups
3 (n = 6) and 4 (n = 6), the effects of MCD peptide on
increases in CA output induced by DMPP (0.1, 0.2, and 0.4 µg) and
muscarine (0.5, 1, and 2 µg) were examined, respectively, with the
same protocol as used in group 2. The effects of scyllatoxin (10, 30, and 100 ng/min) on increases in CA output induced by SNS
(group 5,
n = 9), ACh
(group 6,
n = 7), DMPP
(group 7,
n = 7), and muscarine
(group 8,
n = 7) were examined with the same
protocol used in the MCD peptide experiments.
ABSTRACT
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
1 · h1
with an infusion pump (201B; Atom, Tokyo, Japan). Artificial respiration was performed by means of a respiration pump (model 607;
Harvard Apparatus, Millis, MA), with room air being administered at 18 strokes/min (20 ml/kg tidal volume). The surgical procedure used in the
present study was described previously (14). The left adrenal gland was
exposed by a retroperitoneal flank incision, and a polyethylene cannula
was inserted into the left adrenolumbar vein for collection of the
venous effluent blood from the adrenal gland. A thread was placed
around the juncture of the adrenolumbar vein and the abdominal vena
cava. Adrenal blood samples were obtained by pulling the thread, thus
occluding the adrenolumbar vein and causing a retrograde flow of blood
to ensue. The 1- or 2-ml blood samples were collected in chilled test
tubes containing disodium EDTA. When it was not being sampled, adrenal
venous blood was returned directly to the vena cava. Coagulation of
blood was prevented by an initial intravenous injection of sodium
heparin (500 U/kg) and hourly intravenous injections of 100 U/kg.
Systemic blood pressure and heart rate were measured by a pressure
transducer (MPU-0.5; Nihon Kohden, Tokyo, Japan) and a
cardiotachometer (RT-5, Nihon Kohden), respectively, and were recorded
on a heat-writing oscillograph (RJG-4128, Nihon Kohden).
Blood sampling and determination of adrenal CA output. Adrenal venous blood was sampled before and during SNS and injections of ACh, DMPP, and muscarine to determine basal CA output and stimuli-induced increases in CA output, respectively. The sampling during basal state (during saline, MCD peptide, or scyllatoxin infusion) was performed 2 min before SNS or sets of cholinergic agonist injections. The time required to collect 1 ml (during basal state or SNS) or 2 ml (during cholinergic agonist injections) of blood served to estimate adrenal venous flow rate.
Adrenal blood samples were centrifuged to obtain plasma samples. CA was extracted from plasma by alumina adsorption method, and plasma epinephrine and norepinephrine concentrations were determined by high-performance liquid chromatography with electrochemical detection (LC-304; Bioanalytical Systems, West Lafayette, IN), as described previously (14). Epinephrine and norepinephrine output (ng/min) were calculated by multiplying plasma concentration (ng/ml) by adrenal plasma flow rate (ml/min), and total output of epinephrine and norepinephrine were expressed as CA output. Adrenal plasma flow rate was calculated by multiplying adrenal venous blood flow by 1
hematocrit. The basal CA output was determined from samples collected
before SNS or injections of the cholinergic agonists. The SNS-, ACh-,
DMPP-, or muscarine-induced changes in CA output were calculated by
subtracting the basal CA output from that obtained during the stimulus
state.
Analysis of data. The results were expressed as means ± SE throughout the study. Analysis of variance and Dunnett's test were used for statistical analysis of multiple comparisons of data. P values <0.05 were considered to be statistically significant.
Drugs. The drugs used were MCD peptide, scyllatoxin (Peptide Institute, Osaka, Japan), ACh chloride (Daiichi Seiyaku, Tokyo, Japan), DMPP iodide (Aldrich, Milwaukee, WI), and muscarine chloride (Sigma, St. Louis, MO). All drugs were dissolved in 0.9% saline solution.
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RESULTS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Increases in CA output in response to SNS, ACh, DMPP, and muscarine. SNS (1, 2, and 3 Hz) or intra-arterial injections of ACh (0.75, 1.5, and 3 µg), DMPP (0.1, 0.2, and 0.4 µg), and muscarine (0.5, 1, and 2 µg) into the adrenal gland produced frequency- or dose-dependent increases in adrenal venous plasma CA concentration (data not shown). The ACh- and muscarine-induced increases in CA concentration were accompanied by increases in adrenal plasma flow rate (Tables 1 and 2). The SNS- and DMPP-induced increases in CA concentration were accompanied by no or slight increases in adrenal plasma flow rate. CA output, calculated by CA concentration and adrenal plasma flow rate, was increased by SNS, ACh, DMPP, and muscarine. The increases in CA output induced by SNS (3 Hz), ACh (3 µg), DMPP (0.4 µg), and muscarine (2 µg) during the control stimulation periods were 448 ± 71 (n = 15), 653 ± 141 (n = 13), 928 ± 151 (n = 13), and 474 ± 114 ng/min (n = 13), respectively, in groups 1-8, in which basal CA output during the resting state was 1.3 ± 0.2 ng/min (n = 54).
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Effects of MCD peptide on the SNS-, ACh-, DMPP-, and muscarine-induced increases in CA output. Infusion of MCD peptide (10, 30, and 100 ng/min) into the adrenal gland enhanced the SNS-induced increase in CA output (Fig. 1A). The enhancements were small, but they were dose dependent and statistically significant. Percentage of enhancement by the highest dose (100 ng/min) of MCD peptide of increases in CA output induced by 1, 2, and 3 Hz of SNS were 38 ± 6, 37 ± 11, and 50 ± 21%, respectively. The ACh-, DMPP-, and muscarine-induced increases in CA output were not affected even by the highest dose (100 ng/min) of MCD peptide (Fig. 1, B-D).
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Effects of scyllatoxin. Infusion of scyllatoxin (10, 30, and 100 ng/min) into the adrenal gland enhanced the ACh-, DMPP-, and muscarine-induced increases in CA output (Fig. 2, B-D). The enhancements were dose dependent with or without significance. Percentages of enhancement by the highest dose (100 ng/min) of scyllatoxin were 150 ± 72, 108 ± 54, and 77 ± 51% at 0.75, 1.5, and 3 µg of ACh, respectively; 171 ± 87, 160 ± 58, and 100 ± 37% at 0.1, 0.2, and 0.4 µg of DMPP, respectively; and 103 ± 27, 73 ± 19, and 52 ± 19% at 0.5, 1, and 2 µg of muscarine, respectively. The SNS-induced increase in CA output was not affected even by the highest dose (100 ng/min) of scyllatoxin (Fig. 2A).
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DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Intra-arterial injections of ACh, DMPP, and muscarine into the adrenal gland produced marked increases in CA output. The highest dose of ACh (3 µg) or muscarine (2 µg) caused a transient depressor response. However, it is unlikely that the baroreflex-mediated CA secretion is involved in the CA response to both agonists, because the adrenal gland was decentralized by cutting the splanchnic nerves and because adrenal venous blood sampling was completed before the pressure change. The intra-arterial administration method made it possible to examine the direct action of MCD peptide and scyllatoxin on adrenal CA secretion in response to SNS and cholinergic agonists under in vivo conditions.
MCD peptide, a 22-amino acid peptide isolated from the venom of the bee Apis mellifera (11), has been reported to suppress KA channels in sensory ganglion cells (27) and brain membranes (17). MCD peptide infused into the adrenal gland enhanced the SNS-induced increase in CA output in a dose-dependent manner without affecting the basal CA output. This indicates that MCD peptide influences the secretion process induced by SNS but does not stimulate the secretion process by itself. Previously, we demonstrated under the same experimental conditions as in this study that the SNS-induced CA secretion is mainly mediated by nicotinic receptors (15, 26). Therefore, the enhancing effect of MCD peptide on the SNS-induced secretion of CA is explained by its facilitatory action on the nicotinic receptor-mediated pathway. However, MCD peptide did not affect increases in CA output in response to ACh, DMPP, or muscarine. We demonstrated also that exogenous ACh causes the secretion of CA by activating both nicotinic and muscarinic receptors (15). Here, the question arises as to why MCD peptide influences the nicotinic receptor-mediated secretion of CA differently, causing a facilitation in the case of SNS and no effect in the case of injections of ACh and DMPP. Two explanations might be possible to understand this discrepant effect of MCD peptide.
One possibility is that KA channels located presynaptically in the splanchnic nerve terminals may play an inhibitory role in the release of ACh and other neurotransmitters. It has been suggested that the secretion of CA is stimulated by neuropeptides, such as opioid peptides and vasoactive intestinal peptide, coreleased with ACh from splanchnic nerves in rat (19) and dog adrenal glands (9, 31). If the membrane depolarization of the terminals evoked by SNS activates KA channels that are capable of facilitating repolarization, it would be expected that activated KA channels attenuate the release of neurotransmitters by diminishing the depolarizing phase. MCD peptide might produce the facilitation of the neurotransmitter release by blocking the KA channel-mediated negative control. Consequently, the secretion of CA in response to SNS may be facilitated. It was suggested that tetraethylammonium, a nonspecific K+ channel blocker, potentiates the SNS-evoked secretion of CA by facilitating the release of noncholinergic substances from splanchnic nerve terminals in the perfused rat adrenal gland (19). This finding might support the possible involvement of presynaptic KA channels capable of inhibiting neurotransmitter release.
Another explanation is that intrasynaptic KA channels in the adrenal medullary cells may play an inhibitory role in the secretion of CA. Activation of nicotinic receptors promotes Na+ and Ca2+ influx through receptor-linked ion channels, and the resulting depolarization produces Ca2+ influx through voltage-dependent Ca2+ channels (5, 8). Simultaneously, the depolarization may activate KA channels, and activated KA channels increase K+ efflux, and the resulting facilitation of repolarization may lead to inhibition of further Ca2+ influx. As a result, the secretion of CA may be inhibited. Therefore, it is probable that MCD peptide enhances the CA secretion mediated by nicotinic receptors by blocking the KA channel-mediated inhibition of Ca2+ influx. Endogenous ACh released from the splanchnic nerves would predominantly activate nicotinic receptors located intrasynaptically. Exogenous ACh and DMPP delivered through the arterial supply could diffuse into extrasynaptic regions and would predominantly activate nicotinic receptors located extrasynaptically. If KA channels are primarily concentrated in intrasynaptic zones but not in extrasynaptic regions, they could affect the depolarization due to the activation of intrasynaptic nicotinic receptors but could not affect the depolarization due to the activation of extrasynaptic nicotinic receptors. Recently, it was reported that KA channels are particularly concentrated at the site of synaptic contacts on postsynaptic membranes in rat supraoptic nucleus neurons (3). This finding might support our hypothesis, although no report is available suggesting synaptic localization of KA channels in chromaffin cells.
Scyllatoxin infused into the adrenal gland enhanced the adrenal CA secretion in response to ACh, DMPP, and muscarine in a dose-dependent manner without affecting the basal CA output. These results are consistent with the observation with apamin, a SKCa channel blocker in the dog (23), indicating that scyllatoxin facilitates the secretion of CA by affecting pathways mediated by both nicotinic and muscarinic receptors but that it does not stimulate the secretion process by itself. From these results, it is suggested that SKCa channels play an inhibitory role in the adrenal CA secretion mediated by both nicotinic and muscarinic receptors, as suggested in the perfused cat adrenal gland (22, 28, 29) and in bovine adrenal chromaffin cells (18).
The elevation of intracellular Ca2+ resulting from the activation of nicotinic receptors triggers the secretion of CA and simultaneously may activate SKCa channels. Increases of K+ efflux caused by the activation of SKCa channels results in hyperpolarization, which leads to inhibition of further Ca2+ influx, and the secretion of CA may be inhibited. Therefore, it seems probable that scyllatoxin enhances the secretion of CA mediated by nicotinic receptors by blocking the SKCa channel-mediated inhibition of Ca2+ influx. On the other hand, the elevation of intracellular Ca2+ mobilized from intracellular storage sites is thought to contribute to the muscarinic receptor-mediated secretion of adrenal CA (12, 21, 24). Furthermore, it has been shown that muscarinic receptor activation depolarizes the adrenal chromaffin cells of chickens (16), rats (2), and guinea pigs (13) and that the secretion of CA induced by methacholine, a pure muscarinic agonist, is potentiated by apamin, but, in the presence of furnidipine, an L-type Ca2+ channel blocker, its potentiation disappears (28). Therefore, the facilitatory effect of scyllatoxin on the muscarinic receptor-mediated secretion of CA can be explained in the same manner as for the nicotinic receptor-mediated secretion.
Scyllatoxin did not affect the SNS-induced increase in CA output. This result indicates that SKCa channels have no role in the nicotinic receptor-mediated secretion in response to endogenous ACh and that they contribute differently to the secretion between endogenous and exogenous ACh. The differential effects of scyllatoxin on the secretion between endogenous and exogenous ACh may be explained by differential distribution of SKCa channels on the medullary cell membrane in intrasynaptic and extrasynaptic regions, although regional localization of SKCa channels in chromaffin cells has not yet been proven. If SKCa channels are primarily concentrated in extrasynaptic regions but not in synaptic zones, they could affect the elevation of Ca2+ due to the activation of extrasynaptic nicotinic and muscarinic receptors but could not affect the elevation of Ca2+ due to the activation of intrasynaptic nicotinic receptors. However, the secretion of CA under physiological conditions is caused by activation of the splanchnic nerves. Therefore, the physiological role of extrasynaptic SKCa channels remains to be resolved.
In conclusion, this study demonstrates that MCD peptide facilitates adrenal CA secretion in response to SNS but not to ACh, DMPP, or muscarine and that scyllatoxin facilitates the secretion in response to ACh, DMPP, and muscarine but not to SNS. These results suggest that KA channels may play an inhibitory role in the regulation of adrenal CA secretion in response to SNS and that SKCa channels may play the same role in the secretion in response to exogenously applied cholinergic agonists.
Perspectives
From the results of this study, it is suggested that KA channels may play an inhibitory role in the regulation of adrenal CA secretion through an intrasynaptic mechanism, a presynaptic inhibition of neurotransmitter release, or a postsynaptic inhibition of the nicotinic receptor-mediated CA secretion and that SKCa channels may play the same role in the control of secretion mediated by extrasynaptic nicotinic and muscarinic receptors. To understand this hypothesis, localization of KA and SKCa channels in splanchnic nerve teminals and adrenal chromaffin cells will need to be clarified.| |
ACKNOWLEDGEMENTS |
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This work was supported in part by Grant 09470510 for Scientific Research from The Ministry of Education, Science and Culture, Japan.
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FOOTNOTES |
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Address for reprint requests: S. Satoh, Dept. of Pharmacology, Pharmaceutical Institute, Tohoku Univ., Aobayama, Sendai, 980-77, Japan.
Received 29 July 1997; accepted in final form 7 January 1998.
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REFERENCES |
|---|
|
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
|
|---|
1.
Adams, P. R.,
D. A. Brown,
and
A. Constanti.
M-currents and other potassium currents in bullfrog sympathetic neurones.
J. Physiol. (Lond.)
330:
537-572,
1982
2.
Akaike, A.,
Y. Mine,
M. Sasa,
and
S. Takaori.
Voltage and current clamp studies of muscarinic and nicotinic excitation of the rat adrenal chromaffin cells.
J. Pharmacol. Exp. Ther.
255:
333-339,
1990
3.
Alonso, G.,
and
H. Widmer.
Clustering of KV4.2 potassium channels in postsynaptic membrane of rat supraoptic neurons: an ultrastructural study.
Neuroscience
77:
617-621,
1997[Medline].
4.
Belluzzi, O.,
O. Sacchi,
and
E. Wanke.
A fast transient outward current in the rat sympathetic neuron studied under voltage-clamp conditions.
J. Physiol. (Lond.)
358:
91-108,
1985
5.
Cena, V.,
G. P. Nicolas,
G. P. Sanchez,
S. M. Kirpekar,
and
A. G. Garcia.
Pharmacological dissection of receptor-associated and voltage-sensitive ionic channels involved in catecholamine release.
Neuroscience
10:
1455-1462,
1983[Medline].
6.
Corcoran, J. J.,
and
N. Kirshner.
Inhibition of calcium uptake, sodium uptake, and catecholamine secretion by methoxyverapamil (D600) in primary cultures of adrenal medulla cells.
J. Neurochem.
40:
1106-1109,
1983[Medline].
7.
Galvan, M.,
and
C. Sedlmeir.
Outward currents in voltage-clamped rat sympathetic neurones.
J. Physiol. (Lond.)
356:
115-133,
1984
8.
Garcia, A. G.,
F. Sala,
J. A. Reig,
S. Viniegra,
J. Frias,
R. Fonteriz,
and
L. Gandia.
Dihydropyridine BAY-K-8644 activates chromaffin cell calcium channels.
Nature
309:
69-71,
1984[Medline].
9.
Gaspo, R.,
N. Yamaguchi,
and
J. de Champlain.
Correlation between neural release of VIP and adrenomedullary catecholamine secretion in vivo.
Am. J. Physiol.
268 (Regulatory Integrative Comp. Physiol. 37):
R1449-R1455,
1995
10.
Goh, J. W.,
M. E. M. Kelly,
P. S. Pennefather,
G. G. Chicchi,
M. A. Cascieri,
M. L. Garcia,
and
G. J. Kaczorowski.
Effect of charybdotoxin and leiurotoxin I on potassium currents in bullfrog sympathetic ganglion and hippocampal neurons.
Brain Res.
591:
165-170,
1992[Medline].
11.
Habermann, E.
Bee and wasp venoms.
Science
177:
314-322,
1972
12.
Harish, O. E.,
L. S. Kao,
R. Raffaniello,
A. R. Wakade,
and
A. S. Schneider.
Calcium dependence of muscarinic receptor-mediated catecholamine secretion from the perfused rat adrenal medulla.
J. Neurochem.
48:
1730-1735,
1987[Medline].
13.
Inoue, M.,
and
H. Kuriyama.
Muscarinic receptor is coupled with a cation channel through a GTP-binding protein in guinea-pig chromaffin cells.
J. Physiol. (Lond.)
436:
511-529,
1991
14.
Kimura, T.,
M. Katoh,
and
S. Satoh.
Inhibition by opioid agonists and enhancement by antagonists of the release of catecholamines from the dog adrenal gland in response to splanchnic nerve stimulation: evidence for the functional role of opioid receptors.
J. Pharmacol. Exp. Ther.
244:
1098-1102,
1988
15.
Kimura, T.,
T. Shimamura,
and
S. Satoh.
Effects of pirenzepine and hexamethonium on adrenal catecholamine release in responses to endogenous and exogenous acetylcholine in anesthetized dogs.
J. Cardiovasc. Pharmacol.
20:
870-874,
1992[Medline].
16.
Knight, D. E.,
and
P. F. Baker.
Observations on the muscarinic activation of catecholamine secretion in the chicken adrenal.
Neuroscience
19:
357-366,
1986[Medline].
17.
Kondo, T.,
K. Ikenaka,
I. Fujimoto,
S. Aimoto,
H. Kato,
K. Ito,
T. Taguchi,
T. Morita,
M. Kasai,
and
K. Mikoshiba.
K+ channel involvement in induction of synaptic enhancement by mast cell degranulating (MCD) peptide.
Neurosci. Res.
13:
207-216,
1992[Medline].
18.
Lara, B.,
P. Zapater,
C. Montiel,
M. T. de la Fuente,
R. Martinez-Sierra,
J. J. Ballesta,
L. Gandia,
and
A. G. Garcia.
Density of apamin-sensitive Ca2+-dependent K+ channels in bovine chromaffin cells: relevance to secretion.
Biochem. Pharmacol.
49:
1459-1468,
1995[Medline].
19.
Malhotra, R. K.,
and
A. R. Wakade.
Non-cholinergic component of rat splanchnic nerves predominates at low neuronal activity and is eliminated by naloxone.
J. Physiol. (Lond.)
383:
639-652,
1987
20.
Marty, A.,
and
E. Neher.
Potassium channels in cultured bovine adrenal chromaffin cells.
J. Physiol. (Lond.)
367:
117-141,
1985
21.
Misbahuddin, M.,
M. Isosaki,
H. Houchi,
and
M. Oka.
Muscarinic receptor-mediated increase in cytoplasmic free Ca2+ in isolated bovine adrenal medullary cells. Effects of TMB-8 and phorbol ester TPA.
FEBS Lett.
190:
25-28,
1985[Medline].
22.
Montiel, C.,
M. G. Lopez,
P. Sanchez-Garcia,
R. Maroto,
P. Zapater,
and
A. G. Garcia.
Contribution of SK and BK channels in the control of catecholamine release by electrical stimulation of the cat adrenal gland.
J. Physiol. (Lond.)
486:
427-437,
1995.
23.
Nagayama, T.,
T. Koshika,
H. Hisa,
T. Kimura,
and
S. Satoh.
Apamin-sensitive SKCa channels modulate adrenal catecholamine release in anesthetized dogs.
Eur. J. Pharmacol.
327:
135-141,
1997[Medline].
24.
Nakazato, Y.,
A. Ohga,
M. Oleshansky,
U. Tomita,
and
Y. Yamada.
Voltage-independent catecholamine release mediated by the activation of muscarinic receptors in guinea-pig adrenal glands.
Br. J. Pharmacol.
93:
101-109,
1988[Medline].
25.
Rudy, B.
Diversity and ubiquity of K channels.
Neuroscience
25:
729-749,
1988[Medline].
26.
Shimamura, T.,
T. Kimura,
and
S. Satoh.
Effects of pirenzepine, AF-DX 116 and gallamine on the release of catecholamines from the dog adrenal gland in response to splanchnic nerve stimulation: interaction of M1 and M2 receptors with nicotinic receptors.
J. Pharmacol. Exp. Ther.
257:
369-373,
1991
27.
Stansfeld, C. E.,
S. J. Marsh,
D. N. Parcej,
J. O. Dolly,
and
D. A. Brown.
Mast cell degranulating peptide and dendrotoxin selectively inhibit a fast-activating potassium current and bind to common neuronal proteins.
Neuroscience
23:
893-902,
1987[Medline].
28.
Uceda, G.,
A. R. Artalejo,
M. T. de la Fuente,
M. G. Lopez,
A. Albillos,
P. Michelena,
A. G. Garcia,
and
C. Montiel.
Modulation by L-type Ca2+ channels and apamin-sensitive K+ channels of muscarinic responses in cat chromaffin cells.
Am. J. Physiol.
266 (Cell Physiol. 35):
C1432-C1439,
1994
29.
Uceda, G.,
A. R. Artalejo,
M. G. Lopez,
F. Abad,
E. Neher,
and
A. G. Garcia.
Ca2+-activated K+ channels modulate muscarinic secretion in cat chromaffin cells.
J. Physiol. (Lond.)
454:
213-230,
1992
30.
Wada, A.,
M. Urabe,
T. Yuhi,
R. Yamamoto,
T. Yanagita,
H. Niina,
and
H. Kobayashi.
Large- and small-conductance Ca2+-activated K+ channels: their role in the nicotinic receptor-mediated catecholamine secretion in bovine adrenal medulla.
Naunyn Schmiedebergs Arch. Pharmacol.
352:
545-549,
1995[Medline].
31.
Yamaguchi, N.
In vivo evidence for adrenal catecholamine release mediated by nonnicotinic mechanism: local medullary effect of VIP.
Am. J. Physiol.
265 (Regulatory Integrative Comp. Physiol. 34):
R766-R771,
1993
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