© 1996 American Heart Association, Inc.
Articles |
Effect of Membrane Potential on the Initiation of Acetylcholine-Induced Ca2+ Transients in Isolated Guinea Pig Coronary Myocytes
From the Department of Physiology (V.Y.G.), University of Cologne (Germany) and the Department of Physiology (G.I.), University of Halle (Germany).
Correspondence to Dr V.Y. Ganitkevich, Department of Physiology, University of Cologne, Robert-Koch-Str. 39, 50931 Köln, Germany.
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Abstract |
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Abstract The muscarinic stimulation of single voltage-clamped coronary arterial smooth muscle cells of the guinea pig was used to evaluate the effect of membrane potential on the inositol 1,4,5-tris-phosphate (IP3)–mediated changes of ionized [Ca2+] in the cytoplasm (Ca2+ transient) measured with indo 1. When applied at the membrane potential of -50 mV, 10 µmol/L acetylcholine (ACh) induced a [Ca2+]i increase after the mean latency of 2.6±0.9 s. The latency was reduced to 1.1±0.3 s when the same dose was applied at a holding potential of +50 mV. In paired experiments in the same cells, the latency of response at +50 mV was reduced by a factor of 2.2±0.3 compared with the response at -50 mV. Supramaximal [ACh] (100 µmol/L) induced Ca2+ transients with a 0.4±0.1-s latency, which was independent of membrane potential. When applied repetitively at -50 mV, ACh induced Ca2+ transients with a progressively reduced amplitude and slower rate of rise. Depolarization to +50 mV accelerated the rate of rise of the Ca2+ transient by a factor of 3.4±0.4 without affecting the amplitude. The modulation of the initiation of Ca2+ transient by a 100-mV depolarization can be explained by an approximately threefold increase in the rate of IP3 accumulation.
Key Words: acetylcholine • membrane potential • Ca2+ transients
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Introduction |
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In many types of smooth muscle cells, agonists (like ACh) induce the increase in [Ca2+]i via the release of IP3 from the lipids of the plasma membrane and following IP3-induced Ca2+ release (IICR).1 2 Mostly, the [Ca2+]i signaling is studied without control of membrane potential, ie, in cells that are not voltage-clamped. Recently, it became clear that the membrane potential is, at least in some cells, of importance for IP3-mediated Ca2+ transients. It was shown that depolarization accelerates the PIP2 breakdown,3 that hyperpolarization inhibits the IP3 production,4 5 and that the membrane potential modulates the [Ca2+]i in the presence of agonist.6 However, the consequences of the putative voltage dependence of IP3 accumulation for the initiation of the Ca2+ transient in intact cells are unknown. In the present study, we examined the effect of membrane potential on the initiation of the ACh-induced Ca2+ transient in single isolated voltage-clamped coronary smooth muscle cells.
Assuming that IP3-induced Ca2+ release starts when some "critical" IP3 concentration is reached,7 8 we used the latency of IICR as an indirect measure of the IP3 accumulation rate. Once IICR has started, it is subjected to a feedback by the intracellular mechanisms involved in Ca2+ signaling.9 10 11 We attempt to reduce the influence of positive feedback through released Ca2+ by depleting the IP3-sensitive Ca2+ store with repetitive ACh applications. Under these conditions, the rate of [Ca2+]i rise was used as the approximate measure of the IP3 accumulation. Both approaches give similar results: the initiation of the Ca2+ transient is modified by a 100-mV depolarization in a way that can be explained by an approximately threefold increase of the IP3 accumulation rate.
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Materials and Methods |
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Guinea pigs (200 to 400 g) were killed by cervical dislocation. Single myocytes were enzymatically isolated from the left coronary artery as described before.12 Briefly, the artery was cut out from the heart and placed for 40 to 60 minutes in a nominally Ca2+-free PSS (see below). Thereafter, the artery was placed for 20 to 30 minutes in 1 mL of this solution complemented with 1 mg/mL collagenase (0.5 to 0.7 U/mg, Serva) and 1 mg/mL elastase (130 to 200 U/mg, Serva). The suspension of isolated cells was obtained by pipetting the tissue with a wide-bore Pasteur pipette. Cells were placed in Ca2+-free PSS and stored at 4°C before use on the same day. During the experiment, the myocytes were continuously superfused with a 36°C warm PSS composed of (mmol/L) NaCl 150, CaCl2 2.5, MgCl2 1.2, KCl 5.4, glucose 20, and HEPES 5, adjusted with NaOH to pH 7.4. ACh (Sigma, dissolved in nominally Ca2+-free PSS or Ca2+-free PSS supplemented with 0.1 mmol/L EGTA) was applied to a cell through a four-barrel pipette as described previously,6 and the solution exchange rate was adjusted to be completed within <
0.2 s (as
measured by application of high-K+ solution and the change
of the K+ current). The voltage-clamp method for
measuring membrane currents and the microfluorospectroscopy for
measuring [Ca2+]i have been described
previously.6 Briefly, the isolated cells were loaded with
100 µmol/L K5–indo 1 through patch electrodes of 3- to
5-M
resistance. Whole-cell membrane currents were recorded
with an RK-300 amplifier (Biologic), filtered at 1 kHz, and stored on
an IBM-compatible host computer. For microfluorospectroscopy, the cells
loaded with indo 1 through the patch pipette were excited at 340 nm.
Emitted light in bands from 395 to 425 nm and from 450 to 490 nm was
collected by a pair of photomultipliers (Hamamatsu Photonics). After
filtering at 20 Hz, the fluorescence ratio
F410/F470 was obtained on-line by an
analog divider (Burr Brown DIV100). The background fluorescence
was electronically subtracted in the cell-attached mode.
[Ca2+]i was evaluated off-line, using an
intracellular calibration procedure. The pipettes were filled with a K+ electrode solution containing (mmol/L) KCl 140, Na2ATP 2, MgCl2 3, HEPES 10, and K5–indo 1 0.1, adjusted with NaOH to pH 7.2. Where indicated, 60 µmol/L of PKC inhibitor H-7 (Sigma) was added to the intrapipette solution. Another PKC blocker, GF 109 203X (Boehringer), was dissolved as 2 mmol/L stock solution in dimethyl sulfoxide and was added to the extracellular solution (final concentration, 0.1 µmol/L). All experiments were performed at 36°C. When adequate, the results were expressed as mean±SD.
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Results |
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Effects of Varying the Holding Membrane Potential Between -50 mV and +50 mV on ACh-Induced Ca2+ Transients
Fig 1A
shows the typical response of a
coronary myocyte held at -50 mV to a 50-s application of
10 µmol/L ACh in a Ca2+-free solution supplemented with
0.1 mmol/L EGTA. After application of 10 µmol/L ACh,
[Ca2+]i increased not immediately but
after a
delay of several seconds, and it peaked within 5 s to 1.8 µmol/L. The
ACh-induced [Ca2+]i response often
started with a slow "foot," which is difficult to quantify;
therefore, the latency was measured as the time between the start of
the ACh application and the time when the
[Ca2+]i response reached 20% of its peak.
This latency varied between 0.6 and 4 s in individual cells held at
-50 mV, with a mean value of 2.6±0.9 s (n=35). In 60% of
cells
(n=21), a foot (Fig 1A and 1B) at the
beginning of the Ca2+
transient was observed.11 The
[Ca2+]i increase was slow (<0.1
µmol/L per
second) at the beginning of the Ca2+ transient (Fig
1A and 1B). Subsequently, the rate of
[Ca2+]i
increase was accelerated (maximal rate of rise, up to 10 µmol/L per
second; reached 3.6 s after the start of ACh application). This
acceleration indicates the involvement of the positive feedback. In the
other 40% of the cells, the rise of
[Ca2+]i
was fast from the very beginning (Fig 1C), and no clear foot
could be
distinguished in these cells. Correspondingly, these cells showed
shorter latencies. Within 2 to 4 s after ACh application,
[Ca2+]i peaked to values between 1 and 2
µmol/L. From its peak, [Ca2+]i fell
down
fast initially and then more slowly (Fig 1A). During this slow
decay in
the presence of ACh, [Ca2+]i is thought
to be
extruded from the cell, since subsequent ACh applications induced
greatly attenuated Ca2+ transients (not shown). Therefore,
short (up to 10-s) ACh applications were routinely used in the
following experiments, which induced much more reproducible
Ca2+ transients.
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After receptor occupation by the agonist, the latency of the Ca2+ transient is mainly due to the time required by PLC to cleave PIP2 and to liberate IP3.13 That is, other steps are thought to be considerably faster.14 15 16 17 18 19 20 The Ca2+ release starts when [IP3] reaches some critical level.7 8 The hypothesis that the membrane potential influences the rate of IP3 accumulation predicts that under conditions of constant SR Ca2+ load, the latency of the response depends on membrane potential. Depolarization reduced the latency by accelerating IP3 accumulation so that critical [IP3] could be reached earlier; hyperpolarization of the cell membrane increased the latency. Thus, the effect of the membrane potential on the latency of the IICR was analyzed in the first series of experiments.
When the cell was held at +50 mV, the resting [Ca2+]i was not modified. ACh application induced Ca2+ transients with an amplitude very similar to the one at -50 mV; however, the latency of the response was markedly reduced. In 11 cells, a latency of 1.1±0.3 s was measured at +50 mV, on average. The variability of latencies between cells (see above) complicated the analysis; therefore, the effect of membrane potential on latency was tested in the same cell.
Fig
2A shows two superimposed ACh-induced
Ca2+ transients recorded at holding membrane potentials
of -50 mV and +50 mV in the same cell. The first application of
ACh at -50 mV triggered the Ca2+ transient after a
latency of 3.4 s. There was a clear foot during the rising phase of the
[Ca2+]i response (Fig 2A).
Subsequently,
membrane potential was stepped to +50 mV, and 1 minute later, the ACh
application was repeated. The Ca2+ transient then had a
slightly lower amplitude, suggesting some deprivation of SR
with releasable Ca2+ after the first transient. However,
the latency of the ACh response was then reduced to 1.6 s, and the foot
became less distinguishable. In this cell, the latency was reduced by a
factor of 2.1 by stepping the membrane potential 100 mV in a more
positive direction. In seven cells studied with the same protocol, the
latency of the Ca2+ transient was reduced by a factor of
2.2±0.3.
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IP3 is not the only second messenger produced during the ACh action. Cleavage of PIP2 by PLC results in activation of PKC through the membrane-bound second messenger DAG. PKC activation was shown to inhibit the agonist-induced IP3 accumulation in various types of cells, including smooth muscle cells.21 Therefore, the effect of PKC inhibitors (GF 109 203X and H-7) on the initiation of the ACh-induced Ca2+ transient was studied. Cells were treated for at least 30 minutes with the membrane-permeable PKC blocker GF 109 203X (0.1 µmol/L). Then the whole-cell measurements were performed with an intrapipette solution containing 60 µmol/L of H-7. ACh-induced Ca2+ transients were measured at least 3 minutes after establishment of the whole-cell mode. In five cells, the latency of 2.2±0.4 s was measured at -50 mV. At +50 mV, it was reduced to 1.0±0.3 s. Both values were not significantly different from the control experiments without PKC inhibitors. Thus, the inhibition of PKC does not have an immediate effect on the latency of the ACh-induced Ca2+ transients and on its modulation by the membrane potential.
ACh-Induced Ca2+ Transients and Their Voltage
Dependence at a Varied [ACh]
Since the latency is known to
be a function of receptor
occupancy,8 22 23 the effect of membrane
potential was
compared with the effect of a varied agonist concentration. When
[ACh] was reduced from 10 to 1 µmol/L, the latency of the
Ca2+ transients at +50 mV was increased from
1.1±0.3 to
4.8±1.7 s (n=5). Along with the increase of latency, a clear
foot
appeared with 1 µmol/L ACh (Fig 2B
).
At -50
mV, 1 µmol/L ACh usually did not induce Ca2+
transients (Fig 3), whereas 10 µmol/L triggered
full-sized responses. After stepping to +50 mV, 1 µmol/L ACh
induced Ca2+ transients, although with a lower peak
amplitude and with a slower maximal rate of rise compared with those
found with 10 µmol/L ACh (800 nmol/L and 1 µmol/L per second versus
1600 nmol/L and 8 µmol/L per second). This result suggests that at
low fractional receptor occupancy (ie, a low rate of IP3
accumulation), the membrane potential can determine whether IICR will
happen or not.
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At supramaximal stimulation (high rates of
IP3
accumulation), the latency of IP3-induced Ca2+
release is known to approach its minimal value (<1 s) in
different preparations.8 15 23 This
minimal latency
presumably reflects the saturation of PLC. When supramaximal
concentrations of ACh (100 µmol/L) were applied at -50 mV, the
Ca2+ transients were triggered after a latency of
0.4±0.1
s (n=8). In these experiments, ACh was dissolved in
high-K+
solution to precisely determine the time of solution change (from the
changes in K+ current). When 100 µmol/L ACh was applied
at +50 mV, a similar latency was measured, and in paired applications
to the same cell, latency of response was not influenced by stepping
the holding potential from -50 mV to +50 mV (Fig 4).
These results suggest that conditions that bring PLC
close to saturation, ie, that reduce the latency of the
Ca2+ transient to its minimal value, prevent the effect of
membrane potential on the latency. The lack of the effect of membrane
potential on the latency of [Ca2+]i
responses
to 100 µmol/L ACh suggests that the voltage dependence of the latency
measured between -50 and +50 mV (Fig 2A) is
underestimated. When
corrected for 0.4-s minimal latency, the above change of the holding
potential reduced latency by a factor of 2.8±0.7.
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Effect of Varying of Membrane Potential on the Maximal Rate of Rise
of Ca2+ Transients
The other method, besides assessing
latency, of estimating the
effect of membrane potential on IICR is to analyze the rate of
rise of the Ca2+ transient, which is proportional to the
number of simultaneously opened release channels. In these
cells, ryanodine was without effect on ACh-induced Ca2+
transients11 (authors' unpublished data, 1995); thus,
Ca2+-induced Ca2+ release is not involved in
the Ca2+ transients under study.
Once initiated,
IP3-induced Ca2+ release is
subjected to positive feedback by cytoplasmic
Ca2+.9 10 Under this condition, the
rate of
rise of the Ca2+ transient is not the measure of
[IP3] but is likely to be limited by other
processes (eg, Ca2+-induced transition into a
high-affinity state of IP3
receptor24 25 ). In agreement with this idea, the
maximal
rate of rise was not significantly influenced by changing the membrane
potential to +50 mV, providing that the interval between application
was sufficiently long to allow the recovery of the peak amplitude (Fig
2A).
The influence of Ca2+ feedback can be reduced during desensitization of the transduction pathway, resulting, presumably, in both lower rates of IP3 accumulation and deprivation of the SR of releasable Ca2+. When the SR becomes Ca2+-depleted, the rate of rise of the Ca2+ transient is expected to be less dependent on the positive feedback; hence, it may measure the IP3 accumulation more appropriately.
When 10 µmol/L ACh was applied
repetitively to the cell held at
-50 mV, Ca2+ transients of progressively smaller
amplitude were evoked (Fig 5A). Simultaneous
with the reduction of the peak amplitude, the maximal rate of rise of
[Ca2+]i was reduced from 4.8 µmol/L
per
second (first transient) to 1.24 µmol/L per second (second transient)
and to 0.07 µmol/L per second (fourth transient). At the same time,
the latency become longer (4.5 s for fourth transient compared with 1.8
s for first transient). This result is thought to suggest that the
reduction of the SR Ca2+ load can slow down the rise of the
Ca2+ transient. Because the latency is prolonged in
parallel, the IP3 accumulation rate also seems to be slowed
down. Then the membrane potential was stepped to +50 mV, and 10 s
later, ACh was applied again (Fig 5A). The response was a
Ca2+ transient with a very similar amplitude but with a
markedly shorter latency and faster rate of rise (Fig 5A).
Since the
step to +50 mV did not change the resting
[Ca2+]i and because the peak of
ACh-induced transient at +50 mV was about the same as at -50
mV, we suggest that the holding potential change does not significantly
change the SR Ca2+ load during the time between
applications. Since the SR Ca2+ load was not increased,
then, most likely, an altered gain in feedback through cytoplasmic
Ca2+ ions was not the reason for the acceleration of the
Ca2+ transient at +50 mV (Fig 5). Instead,
the reduction of
the latency in parallel with the increase of maximal rate of rise can
be explained by the assumption that the depolarization accelerates the
IP3 accumulation.
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Evaluation of computer playbacks (Fig
5B) suggests that stepping from
-50 mV to +50 mV increased the maximal rate of rise of the
Ca2+ transient from 160 to 520 nmol/L per second.
Approximately the same peak of [Ca2+]i
(500
nmol/L) was reached at -50 mV within 7 s and at +50 mV within 2 s
after the addition of ACh. However, the maximal rate of
[Ca2+]i rise did not occur at some
definite
level of [Ca2+]i. For example, in the
cell
shown in Fig 5B, the maximal rate of rise of the
Ca2+
transient was reached 4.4 s after the addition of ACh at -50 mV
and 0.7 s at +50 mV (at 240 and 170 nmol/L
[Ca2+]i, respectively). Thus, we did
not observe in this experiment some critical
[Ca2+]11 associated with the maximal
rate of
[Ca2+]i rise. However, the global indo 1
signal does not report [Ca2+]i in the
vicinity of IP3-activated release channels.
This protocol was applied totally to five cells. In summary, changing the holding potential from -50 mV to +50 mV accelerated the maximal rate of rise of the Ca2+ transient by a factor of 3.4±0.4 after it was slowed down by repetitive ACh applications.
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Discussion |
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TopAbstractIntroductionMaterials and Methods Results Discussion References |
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The results of the present study confirm and put forward the idea that the membrane depolarization facilitates the IP3-mediated Ca2+ release. In the present study, we evaluate this idea in terms of the latency of the IICR, and we show that this parameter becomes shorter with increasing [ACh] and with more positive membrane potentials.
As a second messenger, IP3 diffuses much faster than Ca2+ does.26 27 Despite its fast diffusion at 283 (µmol/L)2 per second, it is not possible to exclude that spatial inhomogeneities in [IP3] occur initially (in the subsecond range) at a high degree of PLC activation. [IP3] inhomogeneities would be reported by the IICR, however, not by the chemical determination of IP3. [IP3] was not measured in the present study; hence, the interpretation of the membrane potential effect on IICR depends on the assumption used.
Presumably, the IP3-mediated Ca2+ release starts when [IP3] reaches some threshold level.7 8 14 With this assumption, the IP3 accumulation to the threshold level is related to the time between receptor occupation and the beginning of the IICR, ie, latency of the [Ca2+]i response. Whether IICR will be initiated or not depends on the rate of IP3 production and the rate of IP3 degradation (ie, the lifetime of IP3). If the rate of IP3 production overrides the rate of degradation to such an extent that accumulation to the critical concentration occurs, then the IICR begins. Once initiated, IICR is modified by the feedback of the released Ca2+,9 10 11 which is supposed to transfer the IP3 receptor into a state of higher affinity to IP3.24 25 Another possible feedback presumably involved in IICR is the PKC-mediated inhibition of IP3 accumulation.21 However, to be activated by DAG, PKC needs to be translocated to the membrane. This process seems to be considerably slower than the time scale of the latency measurements.26 Feedbacks involving Ca2+-activated PKC isoforms are unlikely to be of importance for the latency measurements, since the latency was defined as the time until moderate (20%) increase of [Ca2+]i. In agreement with this, our experiments showed no significant effect of PKC inhibitors on the latency of the [Ca2+]i response. This supports the idea that the latency can be related to the accumulation of IP3 to threshold concentration.
According to the above assumptions, the shortening of the latency by membrane depolarization is attributed to the faster rate of IP3 accumulation. For quantification, the minimal latency, which is voltage independent and presumably corresponds to saturated PLC, should be subtracted. In reference to those corrected latency measurements, the 100-mV depolarization shortens the time to reach the threshold concentration by 2.8-fold. This estimate, however, is valid only if the IP3 degradation rate is considerably slower. The estimate also depends critically on the precision of the estimation of minimal latency.
The results of the effect of membrane potential on the response to 1
µmol/L ACh (Fig 3) suggest that with low fractional
receptor
occupancy, the membrane potential can define whether IICR will start or
not. With low fractional receptor occupancy, IP3 is
released at a low rate, presumably comparable to the IP3
degradation rate. The accumulation to the threshold does not happen or
requires a time so long such that a Ca2+ transient at
-50 mV is not evoked (Fig 3). This could mean that the
lifetime
of IP3 is short in coronary myocytes (in other
cells, 1 to 9 s8 27 28 ).
The other approach used in the present analysis is the
measurement of the rate of rise of "desensitized" IICR. Repeated
ACh applications partially depleted the IP3-sensitive
Ca2+ store and, hence, should reduce the influence of the
positive feedback through the released Ca2+. Under these
conditions, the rise in [Ca2+]i was
markedly
slowed, and it could be accelerated again by the subsequent
depolarization. Because the results suggest that the SR
Ca2+ load was not changed, this acceleration of the rate of
rise of IICR by stepping to +50 mV cannot be explained by a
Ca2+ feedback. Most likely, the rise of
[Ca2+]i during desensitized IICR is
rate-limited by a slow accumulation of IP3. The effect
of depolarization on the maximal rate of rise of the Ca2+
transient (factor of 3.4) is likely to be overestimated, since the
IP3 degradation process is likely to be less important
during the fast [Ca2+]i (and
IP3)
rise at +50 mV than during the slow process at -50 mV (Fig
5). In
addition, it is possible that during the slow rise of the desensitized
Ca2+ transient, other feedbacks (mediated through
DAG-activated PKC isoforms and/or
Ca2+-activated PKC isoforms) are of importance.
In conclusion, we have shown for coronary myocytes that the membrane voltage influences the initiation of the Ca2+ transient. The effect was concentration dependent: high [ACh] induced responses that were independent of the membrane potential, whereas the effect of low doses of agonist was voltage dependent. If we accept the assumptions about the rate-limiting processes involved in the initiation of the IICR, then the present results could be explained by an approximately threefold acceleration of IP3 accumulation rate for a 100-mV change of the membrane voltage.
In vivo, even in the absence of agonists, the PLC in vascular smooth muscle has been shown to become activated by stretch.29 Elevation of transmural pressure also directly activates PLC and leads to the production of IP3.30 These findings, together with our findings that the membrane potential exerts more of an effect during low rates of IP3 accumulation, suggest a new role for PLC in coupling the changes of membrane potential to vascular tone.
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Selected Abbreviations and Acronyms |
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Received September 19, 1995; accepted December 7, 1995.
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