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University of Joensuu, Department of Biology, 80101 Joensuu, Finland
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Temperature has a strong influence on the excitability and the contractility of the ectothermic heart that can be alleviated in some species by temperature acclimation. The molecular mechanisms involved in the temperature-induced improvement of cardiac contractility and excitability are, however, still poorly known. The present study examines the role of sarcolemmal K+ currents from rainbow trout (Oncorhynchus mykiss) cardiac myocytes after thermal acclimation. The two major K+ conductances of the rainbow trout cardiac myocytes were identified as the Ba2+-sensitive background inward rectifier current (IK1) and the E-4031-sensitive delayed rectifier current (IKr). In atrial cells, the density of IK1 is very low and the density of IKr is remarkably high. The opposite is true for ventricular cells. Acclimation to cold (4°C) modified the two K+ currents in opposite ways. Acclimation to cold increases the density of IKr and depresses the density of IK1. These changes in repolarizing K+ currents alter the shape of the action potential, which is much shorter in cold-acclimated than warm-acclimated (17°C) trout. These results provide the first concrete evidence that K+ channels of trout cardiac myocytes are adaptable units that provide means to regulate cardiac excitability and contractility as a function of temperature.
inward rectifier; delayed rectifier; thermal acclimation; cardiac myocytes; action potential duration
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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IN NORTH TEMPERATE LATITUDES, ectothermic animals can gain partial independence of seasonal temperature changes by adaptive processes that alter the function of cells in a temperature-dependent manner (20). The expression of different isoforms of metabolic enzymes and contractile proteins in muscle cells with altered catalytic properties and temperature tolerance are examples of such adaptation process (15, 32). Fish hearts are no exception in this regard. For example, in rainbow trout, acclimation to low temperatures increases the rate of cardiac contraction and decreases the refractoriness of the heart, which enable higher heart rates than were otherwise possible in the cold (1). However, the subcellular and molecular mechanisms through which this partial temperature independence in excitability and excitation-contraction coupling is achieved are largely unknown.
The shape and duration of cardiac action potential (AP) differ markedly among different vertebrate species and different types of cardiac myocytes, largely owing to a variety of K+ conductances in the sarcolemma (SL) (27). The great diversity of K+ channels allows fine tuning of the cardiac AP configuration and thus provides the means for regulating myocyte excitability and maintaining electrical stability in the heart. Due to the multiplicity of K+ channel types and their functional differences, K+ currents also have a central role in cardiac adjustment to altered demand (17, 18, 22, 27, 30). K+ channels seem to be plastic entities of the cardiac myocyte, whose expression is changed when environment of the cell is altered, e.g., in cell culture. Accordingly, we reasoned that one potential mechanism of temperature acclimation in fish heart might be modulation of K+ conductance and the resulting effects on the shape of the cardiac AP. Therefore, the objective of the current research was to identify the major K+ conductances of the rainbow trout cardiac myocytes and to explore whether K+ currents are affected by thermal acclimation. It is shown that the two main K+ currents of the rainbow trout cardiac myocytes, IK1 and IKr, are changed in opposite manner by cold adaptation: the background inward rectifier current, IK1, is reduced and the rapid component of the delayed rectifier, IKr, is markedly increased. Temperature-induced changes in K+ conductance reduce AP duration and thereby decrease cardiac refractoriness at low ambient temperatures.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Isolation of atrial and ventricular myocytes. Rainbow trout (mean body mass ± SE of 147 ± 17 g; n = 44) were obtained from a local fish farm (Kontiolahti, Finland) where they had been raised at 9°C. In the laboratory, the fish were randomly divided into two groups and placed in 500-liter stainless steel tanks filled with aerated and circulating (~0.5 l/min) tap water. Water temperature was gradually (1°C/day) changed from 9°C to 17°C [warm-acclimated fish (WA)] or 4°C [cold-acclimated fish (CA)], and the fish were acclimated for >4 wk. The trout were fed commercial food pellets daily (Ewos; Turku, Finland). Photoperiod was a 15:9-h light-dark cycle. The fish were stunned by a sharp blow to the head and the spine was cut. Atrial and ventricular myocytes were isolated by retrograde perfusion of the heart with a nominally Ca2+-free isolation solution (in mM: 100 NaCl, 10 KCl, 1.2 KH2PO4, 4 MgSO4, 50 taurine, 20 glucose, and 10 HEPES at pH 6.9) for 8 min, followed by enzymatic digestion with collagenase (Sigma IA, 1.5 mg/ml) and trypsin (Sigma VIII, 0.5 mg/ml) with added fatty acid-free serum albumin (1 mg/ml; BSA, Sigma) for 20 min at room temperature (~20°C). Atrium and ventricle were separated and cut in small pieces. Myocytes were freed by triturating the muscle pieces through the opening of a Pasteur pipette. Cells were stored in isolation solution at 6°C and were used within 8 h from the isolation.
Patch-clamp recording.
Standard patch-clamp methods in whole cell configuration
(12) were used to record ionic currents and APs in
enzymatically isolated cells (28, 29). A small aliquot of
dissociated cells were placed in a 150-µl chamber (RC-26, Warner
Instrument) mounted on the stage of an inverted microscope (Nikon
Eclipse 200). Cells were allowed to adhere to the bottom of the chamber
and then were superfused continuously with the external solution
prewarmed to either 10 ± 1°C or 20 ± 1°C
(25). Complete replacement of external solution was
achieved in <1 min with the perfusion rate of ~2 ml/min. Glass
pipettes were pulled from borosilicate capillaries (Modulohm) with a
two stage vertical puller (L/M-3P-A, List Electronics) and had a
resistance of 1.5-3 M
when filled with pipette solutions. Voltage and current clamp recordings were made using an Axopatch 1D
amplifier (Axon Instruments) equipped with a CV-4 1/100 headstage. Junction potentials were zeroed before formation of the seal. The
pipette capacitance (4-8 pF) was compensated for after formation of the giga seal. The patch was ruptured by delivering a short voltage
pulse (zap) to the cell, and capacitive transients were eliminated by
iteratively adjusting the series resistance and cell capacitance
circuits. The cell capacitance was read directly from the dial of the
amplifier. Membrane potentials and currents were low-pass filtered at
10 and 2 kHz, respectively, and were sampled at 5 and 1 kHz with
analog-to-digital converter (TL-1 DMA, Axon Instruments). The external
solution contained (in mM) 150 NaCl, 5.4 KCl, 1.5 MgSO4,
0.4 NaH2PO4, 2.0 CaCl2, 10 glucose, and 10 HEPES at pH 7.6. Na+ and Ca2+ currents
were blocked with 1 µM TTX and 10 µM nifedipine, respectively. The
Na+ channels of the rainbow trout cardiac myocytes are
sensitive to TTX with half-maximal and maximal inhibition at the
concentration of ~1 and 30 nM, respectively (results not shown).
Pipette solution for K+ current recordings contained (in
mM) 140 KCl, 4 MgATP, 1 MgCl2, 5 EGTA, and 10 HEPES at pH
7.2. For AP recordings, the pipette solution contained (in mM) 140 KCl,
5 Na2ATP, 1 EGTA, and 10 HEPES at pH 7.4. TTX and
nifedipine were omitted from the external solution when recording APs.
Results are given as means ± SE. Currents were normalized to the
capacitive membrane area and are expressed as current density (pA/pF)
or slope conductance (nS/pF). Differences between acclimation groups
were assessed with Student's t-test with a P
value <0.05 as the limit of statistical significance.
Specific blockers. The delayed rectifier K+ channels were selectively blocked with sotalol (Tocris Cookson) or E-4031 (Wako). Sotalol was dissolved in external saline and E-4031 in ethanol. TTX was obtained either from Alomone Labs or Tocris Cookson. Other chemicals were purchased from Sigma.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Steady-state current-voltage relations.
After blocking other membrane currents, K+ conductances of
the SL were measured by clamping the membrane from a holding potential of 
80 mV to various voltages between 120 and +20 mV at 10° or 20°C. The steady-state current-voltage relationship measured at the
end of 500 ms square-wave pulses varied greatly between atrial and
ventricular cells as well as between WA and CA fish (Fig. 1).
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74 mV) of K+ ions, whereas the
outward current at the positive side of the equilibrium potential was
relatively large. In the ventricular cells, the situation was opposite:
the inward current was much larger than the outward current (Fig. 1).
Thermal acclimation strongly modified sarcolemmal K+
conductances, and the effects were qualitatively similar in atrial and ventricular myocytes. The inward current was strongly reduced by cold
acclimation (Fig. 1). The inhibitory effect of cold acclimation on the
inward current was particularly clear in ventricular cells where this
current component is well developed. In ventricular cells, the slope
conductance between 120 and 80 mV (at 20°C) was 0.737 ± 0.094 nS/pF for WA trout but only 0.269 ± 0.035 nS/pF for CA
trout (P < 0.001), indicating ~64% loss of the
current after acclimation to cold. Due to the very small amplitude of the inward current, the effect of thermal acclimation on
IK1 could not be resolved in atrial cells. The
slope conductance of the atrial inward current of WA fish (0.022 ± 0.005 nS/pF) was not significantly different from the value of CA
fish (0.034 ± 0.005 nS/pF) (20°C) (P = 0.09).
Any temperature-induced changes in the inward current might, however,
be obscured by leakage current in atrial cells.
In contrast to the inward current, the density of the outward current
increased after acclimation to cold (Fig. 1). The densities of the
outward current at +20 mV (20°C) were 2.85 ± 0.35 and 0.96 ± 0.30 pA/pF (P < 0.001) in ventricular cells of CA
and WA fish, respectively. The corresponding values of the atrial cells
were 8.93 ± 0.61 and 1.88 ± 0.32 pA/pF (P < 0.001) for CA and WA fish, respectively. Thus the steady-state
current-voltage relations indicate that acclimation to cold suppresses
inward K+ current(s) but enhances late outward
K+ current(s) in the cardiac myocytes of the rainbow trout
heart (Table 1).
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Blockade of inward and outward currents.
In vertebrate cardiac myocytes, there are several inwardly rectifying
K+ currents, including background inward rectifier
current (IK1), ATP-sensitive K+
current (IK,ATP), and acetylcholine-activated
K+ current (IK,ACh). The
inward current, measured in the absence of external ACh and in the
presence of intracellular ATP, was completely blocked by 200 µM
BaCl2 (Fig. 2) but unaffected
by 10 µM glibenclamide (data not shown), a blocker of
IK,ATP. These findings suggest that the inward
current was flowing through the inwardly rectifying background
K+ channels.
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Characterization of the delayed rectifier current.
The current density of the inward rectifier is very small in trout
atrial cells and, therefore, the properties of the delayed rectifier
currents could be examined in these cells without much interference
from the inward K+ currents. Current-voltage relation of
the delayed rectifier in atrial cells were examined by clamping the
membrane for 2,000 ms to potentials between 80 and +80 mV from a
holding potential of 40 mV. In myocytes of the CA fish, the amplitude
of the activating current (10°C) during the pulse increased with
voltage to a maximum (5.03 ± 0.50 pA/pF) at 0 mV and then
declined at more positive potentials (Fig.
4). In atrial cells of the WA fish, the
current density was much lower (1.53 ± 0.15 pA/pF)
(P < 0.001) and the maximum amplitude was attained at
+20 mV with some inward rectification at more positive voltages (Fig.
4). The density of the tail current, activated by repolarization to
40 mV, was also much less in WA (1.91 ± 0.19 pA/pF) than CA
fish (5.09 ± 0.55 pA/pF) (P < 0.001). These
findings indicate that acclimation to cold increases the peak density
of IKr by 266% in atrial cells of the rainbow
trout.
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40 to +20 mV for 500 ms to activate and inactivate IKr and then
clamped to various test potentials between 120 and +10 mV to measure
the tail current. The initial increase or decrease of the tail current
resulted from the recovery of channels from inactivation, and was
followed by slower deactivation (Fig.
5A). In these experiments, the
inward currents were substantially larger than the outward currents
(Fig. 5C), thus indicating an inward rectification at
positive voltages. The inward current was linear within a limited
voltage range between 100 and 80 mV with slope conductances of
0.230 ± 0.047 and 0.061 ± 0.005 nS/pF (P < 0.001) for CA and WA fish, respectively.
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120 mV
after the conditioning depolarization to +20 mV (Fig. 5B).
After removing the inactivation by the short hyperpolarization, the
channels were conducting also in outward direction and the resulting
instantaneous current-voltage relation was linear up to +20 mV (Fig. 5,
B and C). Slope conductance of this linear
current was 2.5 times higher in CA than WA trout (0.25 ± 0.05 vs.
0.10 ± 0.04 nS/pF).
APs
. Atrial and ventricular APs were recorded in the absence and presence
of 2 µM E-4031, a specific blocker of the fast component of the
delayed rectifier, at 10°C (Fig. 6).
There were marked differences in AP waveforms between atrial and
ventricular myocytes. In atrial myocytes, resting membrane potential
(RP) was less negative and AP duration much shorter than in
ventricular cells (Fig. 6). The RP of unstimulated atrial cells was
44 ± 5 and 47 ± 4 mV (P > 0.05) for CA
and WA fish, respectively. When stimulated to produce APs,
repolarization of AP was followed by an undershoot to a maximum
diastolic potential (MDP) of about 65 mV and subsequent diastolic
depolarization toward RP. In contrast to atrial cells, ventricular
myocytes had stable RPs measuring 77 ± 1.7 (n = 17) and 79 ± 3.3 mV (n = 11) for CA and WA
trout, respectively. There was also considerable differences in AP
duration between acclimation groups. In both atrial and ventricular
myocytes, the duration of AP was much shorter in CA than WA
trout (Fig. 6). Furthermore, AP
duration was prolonged by blocking of the IKr
with 2 µM E-4031. The response to E-4031 could not be quantified in
atrial myocytes, because E-4031 depolarized the RP and made the
myocytes unexcitable. In ventricular cells, E-4031 had no effect on the
RP but markedly increased the duration of AP (Fig. 7).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Potassium conductances of trout atrial and ventricular myocytes. The present results indicate that the two major components of sarcolemmal K+ conductance of the rainbow trout cardiac myocytes are the E-4031-sensitive delayed rectifier current, IKr, and the Ba2+-sensitive background inward rectifier current, IK1. Furthermore, thermal acclimation modifies these K+ conductances in opposite manners: IKr is increased and IK1 decreased in the cold.
IK1 belongs to the Kir2-family of the inwardly rectifying currents (for review, see Ref 27). Due to its large conductance around the Nernst potential of K+ ions and its negative slope conductance between20 and 60 mV, IK1 maintains a stable RP and contributes to the
final repolarization of the AP without having much effect on plateau
duration (27). In mammalian cardiac myocytes, the channels
responsible for IK1 are mainly located in
t-tubular membrane (5). Because rainbow trout cardiac
myocytes do not have any t tubules (23), the spatial distribution of IK1 channels in the fish SL must
differ from that of mammals. The location of the channels in the
peripheral SL might reduce or eliminate the depolarizing effect of fast
spacing, which is considered to occur in mammalian hearts due to the
accumulation of K+ in the narrow t tubules. The exact
spatial distribution of the IK1 channels and its
physiological consequences in fish cardiac myocytes remains to be shown.
In agreement with the earlier findings from mammalian (9,
14) and fish hearts (29), the density of
IK1 was much higher in ventricular than atrial
cells. The density of IK1 in ventricular cells
of the rainbow trout heart is similar to what was recently measured in
crucian carp (Carassius carassius) ventricular myocytes (29). In contrast, the density of
IK1 in trout atrial cells is exceptionally low,
even if compared with the atrial cells of the crucian carp heart
(29). The small magnitude of IK1
explains the relatively depolarized RP of the isolated trout atrial cells.
The delayed rectifier currents (IK) gradually
develop during the plateau phase of AP and conduct outward current at
more positive voltages than the background inward rectifier channels.
In mammalian hearts, IK is comprised of two
pharmacologically and biophysically distinct current components, rapid
(IKr) and slow (IKs)
delayed rectifiers (17). Two characteristics, complete
block by low concentrations of E-4031 and inward rectification due to
rapid inactivation, indicate that the delayed rectifier current of the trout atrial and ventricular myocytes is almost exclusively carried by
the rapid component of the delayed rectifier,
IKr. In contrast to the mammalian cardiac
myocytes, where IKr is usually a minor component
among the diverse K+ conductances (4, 7, 10,
31), the trout cardiac myocytes (especially the atrial cells)
have a very prominent IKr.
In atrial and ventricular myocytes of the mammalian heart, the delayed
rectifier regulates the plateau phase of AP but has little effect on
the rate of final repolarization or on RP (6, 17, 22).
E-4031-induced prolongation of AP and depolarization of RP suggest that
in atrial cells of the rainbow trout heart, IKr not only regulates the duration of AP but
may also contribute to the maintenance of RP. Similarly,
IKr is involved in maintenance of RP in
the esophageal smooth muscle cells (3, 19) and determines MDP of the cardiac pacemaker cells (19). In isolated
atrial cells of the trout heart, the AP undershoot (hyperpolarization) and diastolic depolarization were regular findings and they were abolished by E-4031. Thus, in isolated atrial myocytes,
IKr seems to determine MDP and the decay of
IKr probably causes the diastolic depolarization. In ventricular myocytes of the trout heart, the large
IK1 sets RP and accordingly the inhibition of
IKr had no effect on RP.
Effect of temperature acclimation on K+ conductances. Acclimation to cold depressed IK1 of the ventricular myocytes and strongly increased IKr in both atrial and ventricular myocytes of the rainbow trout heart. The cold-induced increase in IKr can be regarded as compensatory adaptation, which limits AP duration (present study) and decreases refractoriness of the heart (1). This will allow compensatory increases in heart rate (2) and high cardiac output in cold-adapted trout.
The adaptive significance of the cold-induced depression of IK1 is less evident, but might produce energy savings by reducing the demand for ATP-dependent ion pumping across the SL. Moreover, reduction of IK1 might increase the excitability of the ventricular myocytes, because there would be less outward current opposing the initial depolarization in the beginning of AP. The reduction of IK1 did not cause, however, any significant depolarization of RP in ventricular cells of the trout heart. In atrial cells, IK1 was so small that RP must be, at least partially, maintained by the much larger IKr. Furthermore, it is unlikely that the atrial RP in vivo would be as depolarized as it was in enzymatically isolated myocytes. Above all, the tonic parasympathetic tone of the intact fish heart (8, 24) would be assumed to have an effect on atrial K+ currents. The densities of the inwardly rectifying K+ currents might in vivo be much larger than recorded in single atrial myocytes due to Gi/o protein-mediated stimulation of IK,ACh channels (16). Indeed, in intact atria, the RP is more negative (about65 mV; unpublished observations) than in isolated atrial myocytes.
Perspectives
The present findings indicate that sarcolemmal K+ currents are sensitive to chronic temperature stress in a eurythermic fish species and that temperature-dependent expression of K+ currents modifies AP duration and consequently cardiac excitability. In addition to regulation of excitability and refractoriness of the heart, K+ currents are closely involved in the regulation of cardiac contractility. AP duration and plateau height have strong effects on sarcolemmal Ca2+ influx through L-type Ca2+ channels and Na+/Ca2+ exchange (25) and hence temperature-induced changes in repolarizing currents (IKr and IKr) might have a significant indirect affect on Ca2+ management of the fish cardiac myocyte. The shorter AP of the CA fish heart will probably allow less sarcolemmal Ca2+ influx during single excitation, but on the other hand the compensatory increase in heart rate, owing to the reduced refractoriness, will allow a larger frequency-dependent Ca2+-loading of the SR (13). Therefore, it seems that the plasticity of excitation and excitation-contraction coupling of cardiac myocytes in fish is significantly based on temperature-induced changes in K+ conductances of the SL. The task of future research is to examine the presence of this acclimatory response in other ectotherms and to clarify its significance to cardiac contractility in species inhabiting different thermal environments.| |
ACKNOWLEDGEMENTS |
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This study was supported by a grant from the Academy of Finland (project No. 63090) to M. V. Kontiolahti fish farm is gratefully acknowledged for supplying the trout.
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. Vornanen, Dept. of Biology, Univ. of Joensuu, PO Box 111, 80101 Joensuu, Finland (E-mail: matti.vornanen{at}joensuu.fi).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
10.1152/ajpregu.00349.2001
Received 18 June 2001; accepted in final form 3 January 2002.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Aoki T.
Temperature acclimation induces light meromyosin isoforms with different primary structures in carp fast skeletal muscle.
Biochem Biophys Res Commun
208:
118-125,
1995[ISI][Medline].
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