JXB Advance Access originally published online on November 1, 2005
Journal of Experimental Botany 2005 56(422):3103-3110; doi:10.1093/jxb/eri307
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RESEARCH PAPER |
KAT1 inactivates at sub-millimolar concentrations of external potassium
1Institute of Botany, Department of Biology, Darmstadt University of Technology, Schnittspahnstraße 3, D-64287 Darmstadt, Germany
2Department Plant Physiology, University of Szeged, Szeged, Hungary
3Dipartimento di Biologia and IBF-CNR, Università degli Studi di Milano, Italy
To whom correspondence should be addressed. E-mail: thiel{at}bio.tu-darmstadt.de
Received 29 June 2005; Accepted 2 September 2005
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Abstract |
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 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
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Structural analysis of K+ channel pores suggests that the selectivity filter of the pore is an inherent sensor for extracellular K+
channels seem to be inactivated at low 
because of a destabilization of the conducting state and a collapse of the pore. In the present study, the effect of depleting on the activity of a plant K+ channel, KAT1, from Arabidopsis thaliana was investigated. This channel is thought to be insensitive to 
The channel was therefore expressed in mammalian HEK293 cells and measured with patch clamp technology in the whole cell configuration. The effect of depletion on channel activity was monitored from the tail currents before, during, and after washing from the medium. The data show that a depletion of results in a decrease in channel conductance, irrespective of whether K+ is simply removed or replaced by either Na+ or Li+. Quantitative analysis suggests that the channel has two binding sites for K+ with the dissociation constant in the order of 20 µM. This high sensitivity of the channel to could serve as a safety mechanism, which inactivates the channel at low and, in this way, prevents leakage of K+ from the cells via this type of channel. Key words: Cation sensitive gating, HEK293 cells, KAT1, potassium affinity
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The activity of voltage-gated K+ (Kv) channels in animal cells is modulated by external
and internal K+ ions (Almers and Armstrong, 1980
; Pardo et al., 1992; Baukrowitz and Yellen, 1995; Eghbali et al., 2002). When is lowered in the external medium to millimolar concentrations, the channels reversibly inactivate. In other classes of K+ channels, such as the MaxiK channel, the proteins interact with external with such a high affinity that its concentration has to be decreased well below 10 µM to achieve channel inactivation (Vergara et al., 1999).
There are good reasons to believe that the sensitivity of K+ channels to the removal of potassium is related to a collapse of the channel pore. A crystallographic X-ray structure of the KcsA channel determined at low K+ concentration shows a distortion of the selectivity filter with respect to the reference structure obtained in high K+ (Zhou et al., 2001). A similar distorted selectivity filter is also seen in molecular dynamic (MD) simulations of the KcsA K+ carried out in the absence of ions (Bernèche and Roux, 2005). These findings led to the conclusion that a depletion of K+ results in a non-conducting state of the channel because of a partial collapse of the channel pore (Bernèche and Roux, 2005; Zhou et al., 2001).
The general architecture, and particularly the pore of plant inward rectifiers, is very similar to that of animal Kv channels (Latorre et al., 2003). This similarity implies that animal and plant K+ channels share fundamental properties which are inherent in their common structure. The plant inward rectifiers, ZmK1 and ZmK2.1 from Zea mays were found to close down, very much like the animal K+ channels, at low (Philippar et al., 2003; Su et al., 2005). By contrast, different studies report that KAT1, another Shaker-like K+ channel from Arabidopsis thaliana, is insensitive to a depletion of (Véry et al., 1995; Brüggemann et al., 1999; Su et al., 2005). This unusual behaviour of KAT1 implies either that the architecture of the KAT1 channel is completely different from that of all the other K+ channels or that the hypothesis of a pore collapse at low K+ is not correct.
In the present work, the sensitivity of KAT1 to a depletion of extracellular is therefore readdressed. KAT1 was expressed in mammalian HEK293 cells and monitored before and during depletion of A combination of an extensive washing with -free solution and measuring the remaining K+ contamination in the bath solution revealed that the conductance decreased steeply in a voltage-independent manner when was decreased below millimolar concentrations. Quantitative analysis of channel conductance as a function of reveals that the channel has probably two binding sites with a binding constant K0.5 in the order of 20 µM.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Transfection of mammalian cell lines
For functional expression, KAT1 was transfected with 23 µg ml–1 DNA (pCB6-KAT1) into modified human HEK293 cells. HEK293 cells were transiently transfected using a standard calcium phosphate protocol.
Electrophysiology
Experiments were performed on cells incubated after transfection at 37 °C in 5% CO2 for 2–3 d. On the day before the experiment, cells were dispersed by trypsin, plated at a low density on 35 mm culture dishes and allowed to settle overnight. Dishes were then placed on the stage of an inverted microscope and single cells patch-clamped in the whole-cell configuration according to standard methods (Hamill et al., 1981) using an EPC-9 patch clamp amplifier (HEKA, Lambrecht, Germany). Data acquisition and analysis were performed using PULSE software (HEKA).
Cells were perfused (c. 1 chamber volume min–1) at room temperature with a control solution containing 1.8 mM CaCl2, 1 mM MgCl2, 5 mM HEPES (pH 7.4), and either 20 mM KCl, LiCl, or NaCl. Choline-Cl was used to adjust the osmolarity to 300 mOsM. To remove K+ from the bath medium the incubation chamber was exchanged with nominally -free medium. Measurements of this solution revealed that different batches of -free medium contained K+ contaminations ranging from 7–200 µM. Only after taking specific care (new plastic containers for storing, not using pH electrodes which had been stored in KCl) it was possible routinely to obtain solutions with a remaining contamination of c. 7 µM. This remaining contamination could not be eliminated.
Patch pipettes contained 130 mM D-potassium-gluconic acid, 10 mM NaCl, 5 mM HEPES, 5 mM EGTA, 0.1 mM GTP (Na salt), 0.1 mM CaCl2 (free Ca2+ c. 100 nM), 2 mM MgCl2, 5 mM phosphocreatin, and 2 mM ATP (Na salt) (pH 7.4).
K+ measurements
K+ concentrations in the bath solution samples were determined as described previously (Bérczi et al., 1982) using a Hitachi Z-8200 atomic absorption spectrophotometer.
Fitting
Data were fitted using a non-linear Marquardt–Levenburg algorithm. The goodness of fits was judged from the 
2 value.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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To examine the dependency of KAT1 activity on extracellular potassium, the channel protein was expressed in mammalian HEK293 cells. These cells are suitable for heterologous expression of an inward rectifier, because they exhibit, at voltages more negative than about 0 mV, only a very low endogenous conductance (Fig. 1A, C). The mean current at –140 mV of non- or mock-transfected cells (n=22) was only –98±35 pA. With this low background conductance the expression of recombinant KAT1 is easily detectable. Figure 1B shows the current response of a HEK293 cell transfected with kat1 DNA. When clamped from the holding voltage of –10 mV to a series of test voltages between +60 mV and –140 mV, the cell exhibits a large inward current. The mean current at –140 mV of kat1 transfected cells was 3.4±0.2 nA (n=32). This inward current exhibits the typical steady-state I/V relationship and kinetic features of KAT1 (Fig. 1B, C). The KAT1 conductance activates slowly at voltages more negative than about –60 mV and deactivates fast at a post-voltage of –10 mV.
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To examine the effect of
on KAT1 conductance, the bath medium with 20 mM K+ was exchanged for a nominally K+-free solution. Before, during, and after removal of (Fig. 2A) KAT1 activity was determined by analysis of the respective activation curves. Therefore, cells were clamped as in Fig. 1 from the holding voltage of –10 mV to a series of test voltages in order to activate KAT1 fully. From these voltages the membrane was stepped back to the common test voltage of –10 mV and the amplitude of the tail currents plotted against the conditioning voltage (Fig. 2B). For a quantitative comparison of the activation curves in different the plot was expressed as cord conductance (GK) according to the equation
 | (1) |
was well fitted by a Boltzmann function of the form
 | (2) |
was set to unity. From 12 similar experiments in 20 mM mean values for V0.5 and z of –107±6 mV and 1.4±0.3, respectively, were obtained (Table 1). These values for the voltage-dependent coefficient are similar to those reported for KAT1 expressed in Xenopus oocytes (Becker et al., 1996; Moroni et al., 1998). However, the voltage dependency of KAT1 in HEK293 cells is shifted positive compared with that in oocytes; the estimated value for V0.5 in HEK293 cells is 40–60 mV more positive than that reported for KAT1 in oocytes (Véry et al., 1995; Moroni et al., 1998).
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Perfusing the bath medium with the nominally K+-free solution resulted in a progressive dilution of the external K+ concentration. Initially this caused an increase in the tail current amplitude (Fig. 2C). This increase was expected simply because of an increased thermodynamic driving force for K+. Further perfusion of the bath chamber with
however, resulted in a progressive decrease in tail currents (Fig. 2C). This decrease, which was observed in all experiments during removal of K+ from the bath medium, clearly demonstrates a change in channel activity. Continuous lowering of and a constant intracellular concentration should, because of the increase in the driving force for K+ efflux, have resulted in a further increase in tail current amplitude and not in a decrease.
To quantify the effect of on KAT1 conductance, collections were taken immediately after the last I/V scan samples from the bath medium. The actual K+ concentration of this solution was determined with an atomic absorption spectrometer. In the case of the experiment shown in Fig. 2A and B, a concentration, corresponding to the time of the last I/V scan, of 20 µM was measured. With this value and the known intracellular K+ activity, the K+ equilibrium voltage and the corresponding GK/V relationship were calculated and fitted by equation 2. To compare the two GK/V relations in low and high Gmax obtained in 20 µM was expressed as a fraction of that measured in 20 mM (Fig. 2B). Fitting the GK/V relation in low with equation 2 shows that the maximal chord conductance in 20 µM K+ is about 2.5 times lower than in 20 mM The values for V0.5 (–109 mV) and z (1.5) in low are not appreciably different from those obtained in 20 mM Also in nine other experiments in which the extracellular K+ was reduced below 100 µM, the values for V0.5 and z were not significantly different from the reference values in 20 mM K+ (Table 1).
Figure 3 shows the results of similar experiments with a plot of the relative GK-max values as a function of the corresponding concentration. The data show that lowering of below about 100 µM results in a drastic decrease in GK-max. To determine the K+ concentration for half-maximal inhibition the data were fitted by a Hill equation of the form:
 | (3) |
To examine the effect of depleting K+ from the external medium on the kinetics of KAT1, the time-course of the tail currents was estimated in high and low The exemplary data from tail currents in Fig. 4 (conditioning pulse at –140 mV, test voltage for tail current –10 mV) measured in one cell at high (20 mM) and low (20 µM) (same as in Fig. 2) show that depletion of has a minute accelerating effect on the kinetics of channel deactivation. This small effect, however, was not significant (Table 1).
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Channel inhibition is K+ selective
In further experiments, the cation specificity of this decrease in GK-max was determined following
depletion The entire K+ in the bath medium (20 mM) was therefore replaced by an equimolar concentration of either Na+ or Li+. Experiments were performed as in Fig. 2 by monitoring the tail currents before and at different times after replacing K+ by either Na+ or Li+ (Fig. 5A, B). The results of these experiments show that the amplitude of tail currents also decreased in this type of experiment with time of washout (Fig. 2); the constant background of millimolar Na+ or Li+ in the bath did not, apparently, prevent this decrease in KAT1 conductance.
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For a quantitative assessment of the impact of Na+ on KAT1 gating, bath solution was again collected during and at the end of the wash-out process in order to estimate the actual K+ concentration. With this parameter the respective cord conductance of KAT1 could be estimated at high and low
The relevant reversal voltages were calculated from the Goldmann equation assuming a selectivity of KAT1 for K+ over Na+ of 50 (Uozumi et al., 1995). An example of a GK/V relation from one cell at high (20 mM /nominally 0 mM Na+) and low (6 µM /20 mM Na+) is illustrated in Fig. 5C. Both data sets are well fitted by equation 2 with a common V0.5 of –110 mV and a z of 1.5. A similar independency of the voltage-dependent parameters, including the kinetics of tail current deactivation on the replacement of by Na+, was found in all other cells tested (Table. 1).
The main difference between the GK/V plots in Fig. 5 is again a drop of GK-max following the replacement of K+ by Na+. In the present case the relative GK-max (GK-max 20 mM K+/6 µM) is reduced by 4.7-fold upon lowering Figure 3 shows the relative GK-max of KAT1 from 15 measurements as a function of in a solution with a background of 20 mM Na+. The plot reveals that GK-max also decreases drastically in these experiments at concentrations below about 100 µM K+. A fit of the data with equation 3 yields a dependency of GK-max on which is not much different from the value obtained in the absence of Na+; the fit yields a Hill coefficient of 2 and a K0.5 value of 14 µM (Table 1). This means that Na+ has no appreciable effect on the dependent conductance of KAT1.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Experimental studies on a number of animal K+ channels have revealed that a removal of extracellular K+ results in a cation-selective inactivation of channel activity; (Pardo et al., 1992
; Eghbali et al., 2002; Philippar et al., 2003, Su et al., 2005). On an atomic scale this can now be explained in the context of the finding that K+ ions, but not Na+ ions, are able to stabilize the conformation of the selectivity filter in the model K+ channel pore KcsA (Zhou et al., 2001; Bernèche and Roux, 2005). The main finding in the present study is that the plant K+ inward rectifier KAT1 makes, other than suggested previously (Véry et al., 1995; Brüggemann et al., 1999; Su et al., 2005), no exception from this rule. Upon depletion of to µM concentrations, the channel inactivates in a voltage-independent manner. The KAT1 channel has the same overall pore architecture as other K+ channels (Latorre et al., 2003). Hence the present results imply that the stability of the pore of this plant channel is also, in solutions of very low K+, due to a binding of K+ ions to the channel; the analysis further predicts two binding sites for this action. The only remarkable feature of KAT1 compared with many other animal and plant K+ channels is the apparent high affinity of this binding site. While other channels already inactivate when is decreased to concentrations in the millimolar range (Pardo et al., 1992; Eghbali et al., 2002; Su et al., 2005), KAT1 reaches half-maximal inhibition only at 20 µM In this respect KAT1 behaves like the Ca2+-activated K+ (BKCa) channel (MaxiK-channel) in which a -sensitive inactivation occurred at µM concentration of (Vergara et al., 1999).
Previous investigations have detected a cation-sensitive gating mechanism in KAT1 (Moroni et al., 2000). According to this gating scheme the channel is released in a voltage and cation-dependent manner from an inhibited state into the open state. The same scheme implies that the deactivation of the channel follows different kinetics depending on whether the channel is active in high and low The analysis of the present data, however, shows that the kinetics of deactivation of the channel is not affected by high and low concentrations of Hence the mechanism underlying the decrease in open probability at micromolar K+ concentration must depend on a different molecular mechanism. The reduction in tail current amplitude without any kinetic changes rather suggests that it is due to a diminished number of functional channels with unchanged gating properties. These results are in accordance with the criteria of a typical C-type inactivation (Eghbali et al., 2002). Hence a removal of external K+ also seems to destabilize the conducting state in KAT1. Overall, these results suggest that in KAT1, as well as in other voltage-gated K+ channels (Yellen, 2002), the selectivity filter can act as a gate and close with low
The present results are in qualitative agreement with previous reports, which suggested a down-regulation in the activity of native plant K+ inward rectifiers at low K+ concentrations. However, the present straightforward estimate of the binding constant for external to KAT1 is more than one order of magnitude lower than that obtained indirectly from previous studies. In native K+ inward rectifiers from Vicia faba guard cells, a binding constant in the order of 400 µM was estimated from competition between 
-dendrotoxin (DTX) and in intact guard cells (Obermeyer et al., 1994). A similar value was obtained from recordings in V. faba guard cell protoplasts. Depletion of the extracelluar K+ concentration to submillimolar concentrations resulted in a negative shift of the activation voltage; this resulted in a decline in channel activity at moderate membrane voltages (Schroeder and Fang, 1991).
The sensitive inhibition mechanism of KAT1 could be physiologically relevant. KAT1 seems to be predominantly expressed in guard cells where it conducts K+ uptake for stomatal opening (Thiel and Wolf, 1997). The concentration of K+ in the apoplast around guard cells occurs generally in the range of some mM (Mühling and Läuchli, 1999; Felle et al., 2000). However, this is also true for the apoplast of stomatal guard cells activities below 50 µM as reported by Blatt (1985). Hence under conditions of severe K+ starvation and low apoplastic a low poses a substantial problem to plant cells, because the driving force for K+ can, in this case, be directed in favour of K+ efflux (Maathuis and Sanders, 1993). If the K+ inward rectifier were active under these conditions K+ would leak from the cell through this channel.
To judge the effect of a controlled conductance of a K+ inward rectifier, the K+ fluxes at different conditions were simulated in the context of the relevant transporters in a plant plasma membrane. Therefore, a modified skeleton model was used for plasma membrane transport (Gradmann et al., 1993; Thiel and Gradmann, 1994), which comprises for the present purpose a H+-ATPase, a KAT1-like K+ inward rectifier, a Cl– channel, and a 2H+/Cl– symporter with the rate constants for activation and inactivation listed in Table 2. Figure 6 illustrates the results of a simulation for the free-running membrane voltage, the ionic currents, and the changes in K+ concentration inside a cell under conditions of a low of 5 µM. Independent of whether the K+ inward rectifier is inhibited by low or not, the free-running membrane voltage settles at a value positive to the K+ reversal voltage (Fig. 6A). This essentially resembles the experimentally recorded values in A. thaliana root cells with micromolar (Maathuis and Sanders, 1993). The simulations illustrate that, in this case, K+ leaks from the cell. However, when the experimentally determined sensitivity of the K+ inward rectifier to (Fig. 3) is considered, the rate of K+ leakage is drastically reduced. Based on the same simulation the rate of K+ loss from a cell was estimated over a period of 10 s of simulation (as in Fig. 6A) over a wide range of (Fig. 6B). It seems that under the model conditions used for the simulation, K+ starts to leak from the cells at below c. 50 µM. In the absence of any regulation of the inward rectifier by external K+, the leakage increases steadily with lower On the other hand, if the experimentally determined sensitivity of the inward rectifier to is considered in the simulation, potassium leakage is greatly reduced. Hence, a high affinity inhibition mechanism in KAT1, which selectively measures in the apoplast and inactivates the channel if drops to micromolar concentration, can prevent or at least reduce this unwanted leakage.
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For simulation a cell was virtually clamped to –140 mV; at time 0 the clamp was released giving rise to the free-running dynamics of the electrical parameters. (A) Simulations of dynamic behaviour of voltage, transporters (1, ATPase; 2, K+ inward rectifier; 3, Cl– channel; 4, 2H+/Cl– symporter) and 
were calculated for |
Acknowledgements |
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We thank Professor U Lüttge (Darmstadt) for helpful comments on the manuscript. We thank Ágnes Vashegyi for carrying out the AAS measurements. The project was supported by a traveling grant to FH form BMBF at DLR (Project Nr. UNG-030-99).
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Footnotes |
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* These authors contributed equally to this work.
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