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Introduction
Mechanical stretch is an important physiological
stimulus in gut smooth muscles. It is well known that mechanical
stretch induces myogenous contraction of gut smooth
muscle, but the mechanism underlying this ionic channel
process remains unknown. Mechanical stretch regulates the
activities of ionic channels, which exist widely in the
membranes of various cells and activate many signal
transduction pathways. A hypothesis was proposed that membrane
stretch induces alterations in the lipid bilayer, which
transmits membrane tension to channel proteins or generates
lipid-soluble second messengers, such as arachidonic acid (AA)
and other endogenous fatty acids, by membrane-bound
phospholipases[1,2]. Unsaturated fatty acids are major
components of membrane lipids and they are mainly released by
phospholipase A2 (PLA2) activation. AA in the cell
membrane is esterified in phospholipids and can be released by
PLA2 in response to various extracellular
stimuli[3,4]. AA and other unsaturated fatty acids modulate the activities of
various ion channels and enzymes through
direct or indirect pathways. For example: AA potentiates hKir2.3 in part by
decreasing inward rectification of the
channel[5]; AA induces membrane depolarization by inhibiting
KATP currents in murine colonic smooth muscle
cells[6]; and AA increases choline acetyltransferase activity in spinal cord
neurons, and this effect is mediated by protein kinase C
(PKC)[7]. In addition, it was shown that AA induces
endothelium-dependent hyperpolarization and relaxation of rabbit aorta through
activation of apamin-sensitive K+
currents[8]. Abundant evidence has revealed that AA is an important mediator in
hyposmotic stress. It was observed that swelling induces
AA release via the 85 kDa cell phospholipase
A2 (cPLA2) in human neuroblastoma
cells[9], and that cell swelling activates
PLA2 in ehrlich ascites tumor
cells[10]. Tinel
et al[11] also reported that AA acts as a second messenger for
hypotonic-induced calcium transients in rat inner medullary collecting
duct (IMCD) cells.
The calcium-activated potassium current
(IK(Ca)) has been considered to play an important role in excitability and
functional regulation in excitable cells. In our previous study,
AA and other unsaturated fatty acids directly inhibited
calcium currents[12] and muscarinic
currents[13]. For both AA and hyposmotic membrane stretch-activated
IK(Ca)[14,15], activation by hyposmotic membrane stretch is associated with
calcium-induced calcium release
(CICR)[16], which is triggered by extracellular calcium influx through the stretch-activated
channels (SAC) in gastric antral circular myocytes of the
guinea pig. However, the roles of AA and other unsaturated
fatty acids in the process of
IK(Ca) activation by membrane stretch in gastric myocytes remains unclear. In the present
study, we therefore investigated the effects of AA and its
metabolites on hyposmotic membrane stretch-induced increases
in IK(Ca) in gastric antral circular myocytes of guinea pig.
Materials and methods
Preparation of cells EWG/B guinea pigs (obtained from
the Experimental Animal Department of Norman Bethune
University, Changchun, China; Certificate
No 10-6004) of either sex, weighing 250-350 g, were killed by lethal dose of
pentobarbital sodium (50 mg/kg, iv). The antral part of the
stomach was cut rapidly, and the muscosal layer was
separated from the muscle layer. Circular muscle was dissected
from the longitudinal layer using fine scissors, and cut into
small segments (1 mm×4 mm). These segments were kept in
a modified Kraft-Bruhe (K-B) medium at 4 ºC for 15 min. The
muscle segments were incubated at 36 ºC in 4 mL of
digestion medium [calcium-free physiological salt solution
(Ca2+-free PSS)] containing 0.1% collagenase (II), 0.1%
dithioery-threitol, 0.15% trypsin inhibitor and 0.2% bovine serum
albumin for 25-35 min. The softened muscle segments were
then transferred into the modified K-B medium, and cells
were dispersed individually by gentle agitation with a
wide-pore fire-polished glass pipette. Isolated gastric myocytes
were kept in modified K-B medium at 4 ºC until use.
Electrophysiological
recording Isolated cells were transferred to a small chamber (0.1 mL) on the stage of an inverted
microscope (IX-70 Olympus, Tokyo, Japan) for 10-15 min to
settle down. The cells were superfused continuously with
isosmotic PSS by gravity (0.9-1.0 mL/min). An 8-channel
perfusion system (L/M-sps-8, List Electronics, Darmstadt,
Germany) was used to change solution. Experiments were
carried out at 20-25 ºC and the whole-cell configuration of
the patch-clamp technique was used. Patch-clamp pipettes
were manufactured from borosilicate glass capillaries (GC
150T-7.5, Clark Electromedical Instruments,
Kent, UK) using a 2-stage puller (PP-83, Narishige, Japan). The resistance of
the patch pipette was 3-5 MW when filled with pipette
solution. Liquid junction potentials were canceled before
seal formation. Whole-cell currents were recorded with an
EPC-10 patch-clamp amplifier (HEKA Instrument,
Darmstadt, Germany) and command pulses were applied by using the
Pentium IV-grade computer and pCLAMP software (Version
6.02; Axon Instruments, USA).
Drugs and solutions All drugs were purchased from
Sigma (Sigma-Aldrich Corp St Louis, MO, USA). Tyrode¡¯s
solution contained 147 mmol/L NaCl, 4 mmol/L KCl,
1.05 mmol/L
MgCl2·6H2O, 2 mmol/L
CaCl2·2H2O,
0.42 mmol/L NaH2PO4, 1.81 mmol/L
Na2HPO4·2H2O and 5.5 mmol/L
glucose, and the pH was adjusted to 7.35 with NaOH.
Ca2+-free solution contained 134.8 mmol/L NaCl, 4.5 mmol/L KCl,
10 mmol/L HEPES, 1 mmol/L
MgCl2 and 5 mmol/L glucose, and the pH was adjusted to 7.4 with TRIZMA BASE (Tris).
The isosmotic solution (290 Osmmol/kg) contained
80 mmol/L NaCl, 4.5 mmol/L KCl, 1 mmol/L
MgCl2·6H2O, 2 mmol/L
CaCl2·2H2O, 5 mmol/L glucose, 10 mmol/L HEPES and
110 mmol/L sucrose, and the pH was adjusted to 7.4 with
Tris. Hypoosmotic solution (200 Osmmol/kg) contained
30 mmol/L sucrose, with the other ingredients at the same
concentrations as in the isosmotic solution. Modified K-B
solution contained 50 mmol/L L-glutamate, 50 mmol/L KCl,
20 mmol/L taurine, 20 mmol/L
KH2PO4, 3 mmol/L
MgCl2·6H2O, 10 mmol/L glucose, 10 mmol/L HEPES ,and 0.5 mmol/L egtazic
acid, and the pH was adjusted to 7.4 with KOH. The pipette
solution contained 110 mmol/L K-aspartic acid, 5 mmol/L
Mg-ATP, 1 mmol/L
MgCl2·6H2O, 20 mmol/L KCl, 0.1 mmol/L or
10 mmol/L egtazic acid, 2.5 mmol/L di-tris-creatine phosphate
and 2.5 mmol/L disodium-creatine phosphate, and the pH
was adjusted to 7.3 with KOH. AA, nordihydroguaiaretic
acid (NDGA) and dimethyleicosadienoic acid (DEDA) were
all prepared as aqueous stock solutions (1 mmol/L).
Data analysis Data were expressed as mean±SD.
Statistical significance was evaluated using the Student¡¯s
t-test. Differences were considered to be statistically significant
when P<0.05.
Results
Effects of hyposmotic membrane stretch and AA on
IK(Ca) and STOC Under whole-cell configuration, membrane
potential was clamped at -60 mV, and
IK(Ca) was elicited by a single-step command pulse from -60 mV to +60 mV for 400 ms
at 15 s intervals. IK(Ca) started increasing at 139.3 s±11.3 s
after cells were exposed to hyposmotic solution (200 mOsm),
and at 165.0 s±25.1 s after cells were exposed to 10 µmol/L
AA (Figure 1A,1B). There was no significant difference
between the 2 latent periods. Hyposmotic membrane stretch
and 10 µmol/L AA increased markedly in peak current ofIK(Ca) to 168.3%±16.1% and 158.5%±20.5%, respectively
(n=6, Figure 1B.).
The calcium-activated potassium current is activated by
intracellular Ca2+ and can be monitored by spontaneous
transient outward currents (STOC)[17]. We therefore observed
STOC to investigate effects of hyposmotic membrane stretch
and AA on IK(Ca). In whole cell configurations, the holding
potential was clamped at -20 mV, and STOC were elicited
and enhanced by hyposmotic membrane stretch and
10 µmol/L AA, respectively (Figure 1C).
Effects of exogenous AA on hyposmotic membrane
stretch-induced increase in
IK(Ca) Under whole-cell
configuration, membrane potential was clamped at -60 mV,
and IK(Ca) was elicited by a step voltage command pulse from
-40 mV to +100 mV for 400 ms with a 20-mV increment at 10-s
intervals. Exogenous AA significantly increased
IK(Ca)
elicited by the command step pulse when membrane
potential was depolarized from -40 mV to+100 mV, and hyposmotic
membrane stretch potentiated the AA-induced increase inIK(Ca) when the membrane potential was depolarized from
-40 mV to+100 mV (Figure 2A, 2B). Hyposmotic membrane
stretch also increased IK(Ca) elicited by the command step
pulse when the membrane potential was depolarized from
-40 mV to +100 mV, and AA potentiated hyposmotic
membrane stretch-induced increase in
IK(Ca) when membrane potential was depolarized from -40 mV to +100 mV (Figure 2A,
2B). The peak current of IK(Ca) was increased to
184.2%±17.7% by hyposmotic membrane stretch and then the
hyposmotic membrane stretch-induced increase in
IK(Ca) was potentiated by
10 µmol/L AA, and the peak current increased
to 281.3%±28.3% at +60 mV (n=8, Figure 2C). In another
way, the peak current of IK(Ca) was increased to 171.8%±20.3
% by 10 µmol/L AA, and the AA-induced increase in
IK(Ca) was potentiated by
hyposmotic membrane stretch, with the peak current
increasing to 311.5%±44.4% at +60 mV
(n=8; Figure 2C). However, there was no significant difference between
the potentiated effects of AA on the hyposmotic membrane
stretch-induced increase in
IK(Ca) and hyposmotic membrane stretch on the AA-induced increase in
IK(Ca) (P>0.05, Figure
2C). As with the protocol above, the effects of hyposmotic
membrane stretch and AA on STOC were investigated.
Hyposmotic membrane stretch markedly increased STOC,
and 10 µmol/L AA potentiated this effect
(n=2, Figure 2D).
Effects of endogenous AA and its metabolites on
hypos-motic membrane stretch-induced increase in
IK(Ca) Intracellular free AA are metabolized by 3
enzymes: cycooxygenase, lipoxygenase and epoxygenase. To determine the effects of
endogenous AA and its metabolites on the hyposmotic
membrane stretch-induced increase in
IK(Ca), DEDA, a non-selective inhibitor of
PLA2, and NDGA, a lipoxygenase inhibitor,
were used to inhibit the hydrolyzation of AA from membranes
and to decrease the production of AA metabolites. DEDA
(100 µmol/L in pipette) significantly suppressed
the hyposmotic membrane stretch-induced increase in
IK(Ca) (Figure 3A,3B), and the increased percentage was reduced from 164.3%±9.8
% of the control to 113.4%±3.6% at +60 mV
(n=15, Figure 3C). When cells were pretreated for 15 min with 10 µmol/L NDGA,
AA (Figure 4A,4B) and hyposmotic stretch-induced
increases in IK(Ca) could be significantly suppressed
(Figure 5A,5B). The AA-induced increase in
IK(Ca) was decreased from 145%±10% to 110%±4% by NDGA
(n=8, Figure 4C). NDGA also suppressed the hyposmotic membrane stretch-induced
increase in IK(Ca) (Figure 5A,5B) and the increased
percentage was reduced from 170%±10% to 142%±3% at +60 mV
(Figure 5C). These results showed that endogenous AA and
its metabolites were involved in the hyposmotic membrane
stretch-induced increase in
IK(Ca).
Effect of calcium mobilization on AA-induced increase
in IK(Ca) It is well known that
IK(Ca) is activated by
intracellular free calcium, while extracellular calcium is necessary for
efficiently controlling calcium homeostasis. To determine
whether the AA-induced increase in
IK(Ca) was mediated by calcium influx, the effect of AA on
IK(Ca) was observed following the removal of extracellular calcium and the addition
of 10 µmol/L EGTA in bath solution. The AA-induced
increase in IK(Ca) was completely blocked by the removal of
extracellular calcium, and the changes in the percentage of
IK(Ca) were 146.30%±10.4% and 95.64%±11.7% in the
presence or absence of extracellular calcium, respectively
(n=6, Figure 6A). Our previous study indicated that hyposmotic
membrane stretch activated L-type calcium
currents[12] and calcium-activated potassium currents
via extracellular calcium influx through SAC in gastric myocytes of guinea
pig[15,16]. We therefore examined the relationship between
the AA-induced increase in
IK(Ca) and L-type calcium channels or SAC. However, 5 mmol/L nicardipine, an L-type
calcium channel blocker, did not block the AA-induced increase
in IK(Ca), but gadolinium
(Gd3+), a blocker of SAC, completely suppressed the AA-induced increase in
IK(Ca). The changes in the percentage of
IK(Ca) were 146.3%±10.4%,
151.1%±14.4% and 102.5%±2.2% in the control, nicardipine and
Gd3+ groups, respectively (n=6, Figure 6A).
Intracellular free calcium has 2 sources: extracellular
calcium influx and intracellular calcium release from calcium
stores. Intracellular calcium is released through 2 pathways,
one is CICR and the other is inositol-triphosphate-induced
calcium release (IICR). We therefore investigated the role of
intracellular calcium release in the AA-induced increase in
IK(Ca). Heparin (3 mg/mL), a potent inhibitor of IICR, could
inhibit STOC significantly, but did not block the AA-induced
increase in STOC (Figure 6B). Ryanodine (10 µmol/L), a
specific CICR inhibitor, binds to CICR channels and locks them
in a subconductance state, thereby functionally depleting
calcium stores[18]. In the present study, ryanodine increased
STOC, and STOC were then almost abolished by ryanodine
after approximately 8 min with caffeine, a CICR activator; AA
could not then enhance them again (Figure 6B). These
results indicated that CICR, but not IICR, was involved in the
AA-induced increase in IK(Ca).
Discussion
Our previous study demonstrated that
IK(Ca) was activated by hyposmotic membrane stretch and
Ca2+ signaling played an important role in the process in gastric antral
circular myocytes of guinea pig[15,16]. Under hyposmotic
conditions, extracellular calcium influx through SAC triggered
CICR, and intracellular free calcium then activated
IK(Ca). However, it remains obscure how the membrane stretch is
turned into the signal for Ca2+ entry from the extracellular
space. We therefore investigated whether AA is involved in
the hyposmotic membrane stretch-induced increase in
IK(Ca).
In the present study, both hyposmotic membrane stretch
and AA significantly increased
IK(Ca) with a similar latent period. Moreover, exogenous AA potentiated the
hypos-motic membrane stretch-induced increase in
IK(Ca) (Figure 1). The results indicated that there may be a similar mechanism
for the IK(Ca) activated by hyposmotic membrane stretch and
AA. Activation of various signaling pathways may induce
an increase in the production of AA, for example,
phospholipase C, phospholipase D and
PLA2. In mammalian tissues AA is mainly liberated directly from phospholipids by
PLA2, which is a ubiquitous
enzyme[4]. We have observed that when cells are exposed to DEDA, a non-selective inhibitor
of PLA2, the hyposmotic membrane stretch-induced increase
in IK(Ca) is significantly blocked by DEDA (Figure 3). The
results suggest that hyposmotic membrane stretch activates
PLA2, which hydrolyzes membrane phospholipids to
produce AA, and AA as a second messenger mediates the
hyposmotic membrane stretch-induced increase in
IK(Ca) in gastric myocytes of guinea pig. Many experiments also
support our results. It was observed that hyposmotic cell
swelling induced AA release from cell membranes in human
neuroblastoma cells[9] and Ehrilich ascites tumor
cells[10]. In rat inner medullary collecting duct cells, AA acted as a
second messenger in hypotonicity-induced calcium
transients[11]. AA was also a second messenger in cultured rabbit principal
cells[19] and ciliary epithelial cells under hyposmotic
conditions[20]. Meanwhile, many reports have described that AA
is able to affect cell functions, via its metabolites, under
hyposmotic conditions in several cell systems. Leucotrienes,
for example, appeared to mediate the inositol efflux in glial
cells[21], and to activate chloride and potassium conductances
as well as taurine transport in Ehrlich ascites
cells[22]. In the present study, we also examined the possibility that AA
metabolites could be involved in activating potassium
currents under hyposmotic conditions by using NDGA, a
lipoxygenase inhibitor. NDGA significantly inhibited AA
and the hyposmotic membrane stretch-induced increase in
IK(Ca) (Figure 4). These results suggest that AA metabolites
generated by lipoxygenase mediate the hyposmotic
membrane stretch-induced increase in
IK(Ca) in gastric myocytes.
In various cell types, AA was found to induce
Ca2+ flux and to mobilize intracellular calcium to trigger different
Ca2+-dependent physiological functions in cells. For example,
AA or its metabolites mobilized Ca2+ from intracellular stores,
and intracellular Ca2+ then activated ion
transport[19]. In several cell types, for example, in rat IMCD
cells[11], human embryonic kidney (HEK293) cells
[23] and Dictyostelium
discoideum[24], AA released Ca2+
from the stores to trigger extracellular
Ca2+ entry, and Ca2+ released from calcium stores
was a prerequisite for extracellular
Ca2+ entry. However, Murthy
et al[20] found that AA induces
Ca2+ influx, which triggers CICR in longitudinal smooth muscle of the intestine.
Our previous study also demonstrated that hyposmotic
membrane stretch activates
IK(Ca) via CICR in gastric
myocytes[15]. In the present study, the roles of AA and its metabolites in
the relationships among hyposmotic membrane
stretch-induced increase in
IK(Ca), extracellular
Ca2+ and intracellular calcium mobilization
were investigated. Under
extracellular calcium-free conditions,
IK(Ca) was not increased by AA or
hyposmotic membrane stretch (Figure 6). It was elucidated
that extracellular calcium is necessary for AA and the
hyposmotic membrane stretch-induced increase in
IK(Ca), and some ionic channels participate in extracellular calcium influx.
McCarty and O¡¯Neil indicated that there are 2 alternative
kinds of channel activated by hyposmotic swelling:
voltage-activated Ca2+ channels and stretch-activated
channels[25]. We observed previously that hyposmotic membrane stretch
increases L-type current in gastric myocytes of guinea
pig[12], and Yamamoto and
Suzuki[26] also observed that there are 2
kinds of SAC in gastric myocytes of guinea pig. In the
present study we examined whether these 2 channels are
associated with extracellular calcium influx. Nicardipine, an
L-type calcium channel blocker, could not block the
AA-induced increase in IK(Ca). However, it was completely blocked
by Gd3+, which blocks not only SAC but also store-operated
Ca2+ channels (Figure 6). A similar effect of
Gd3+ in blocking AA-induced
Ca2+ entry has also been observed in other cell
types, such as IMCD[11] and HEK293
cells[23].
Intracellular Ca2+ release from
Ca2+ stores is the primary source of the increase in intracellular calcium. It was found
that the entry of extracellular calcium via activating
stretch-sensitive channels is amplified by calcium release from inter
nal stores in toad gastric myocytes[26]. Sutko and
Airey[27] suggested that ryanodine-sensitive calcium stores were
positioned near the surface membrane in some smooth muscle
cells, Ca2+ release from which was found to influence the
activity of IK(Ca). Our previous study also indicated that
hyposmotic membrane stretch activates
IK(Ca)[15,16] and carbachol
currents[13], and the activations are associated with
CICR, which is triggered by extracellular calcium
influx[15,28]. In the present study, heparin, a potent inhibitor of inositol
triphosphate receptor, did not block the AA-induced increase
in IK(Ca); however, ryanodine, a CICR agonist, completely
blocked the AA-induced increase in
IK(Ca) (Figure 6B). The results suggest that AA mobilizes intracellular calcium via
triggering CICR and activates
IK(Ca) in gastric antral circular
myocytes of guinea pig. The potassium efflux through
IK(Ca) hyperpolarized the membrane potential of smooth muscle
cells, thereby limiting depolarization-dependent calcium and
promoting relaxation. CICR can thus participate in both the
contraction and relaxation of smooth muscle cells. Therefore,
AA may be involved in both the contraction via activating
extracellular Ca2+ influx and relaxation via activating
IK(Ca) in gastric antral circular myocytes of the guinea pig.
In summary, hyposmotic membrane stretch may act on
cell membranes to activate PLA2 and then generate AA. AA
may then act as a second messenger to mediate
extracellular calcium entry and trigger CICR to activate
IK(Ca) in gastric myocytes of the guinea pig. AA and its metabolites may
play an important role in regulating many cell functions
under the hyposmotic conditions in gastric antral circular
myocytes of the guinea pig.
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