K+ transport in Malpighian tubules of Tenebrio molitor L.: is a KATP channel involved?
1 Department of Zoology and Entomology, University of Pretoria, Pretoria
0002, South Africa
2 Laboratory of Physiology, Biomed CMK, Limburgs Universitair Centrum, B3590
Diepenbeek, Belgium
* Author for correspondence (e-mail: emmy.vankerkhove{at}luc.ac.be)
Accepted 10 December 2002
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Summary |
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Key words: K+ transport, KATP channel, Malpighian tubules, Tenebrio molitor, glibenclamide, basolateral membrane potential, fluid secretion rate
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Introduction |
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In transporting epithelia of vertebrates, the activity of the basolateral
Na+/K+-ATPase is directly linked to the basolateral
K+ conductance (Grasset et al.,
1983; Matsumura et al.,
1984
). Inhibition of the Na+/K+-ATPase by
ouabain increases the intracellular ATP concentration, which in turn reduces
the open probability of ATP-regulated K+ (KATP) channels
(Balaban et al., 1980
;
Hurst et al., 1993
;
Urbach et al., 1996
).
In Na+-reabsorbing epithelia, transport of Na+ is
facilitated by passive entry mechanisms in the apical membrane and an active
Na+-translocation step, the basolateral
Na+/K+-ATPase. KATP channels recycle the
obligatory influx of K+ via the
Na+/K+-ATPase
(Mauerer et al., 1998;
Wang et al., 1990
). This
recycling process prevents intracellular K+ accumulation and
maintains a favourable electrical gradient for Na+ transport across
the apical membrane (Hurst et al.,
1993
). Far less is known about the presence of KATP
channels in K+-secreting epithelia. Wang et al.
(1990
), however, have
documented the presence of a low-conductance KATP channel in the
K+-secreting principal cells of the rat cortical collecting
tubule.
A role for KATP channels in insects is expected to be different.
Secretion of K+ from cell to lumen in insect Malpighian tubules is
generally thought (see Nicolson,
1993) to occur via an apical cation/nH+
antiporter. A vacuolar-type H+-ATPase actively extrudes
H+ across the apical membrane, and this (1) energizes the
antiporter, enabling exchange of protons for K+ (or
Na+), and (2) keeps the cell at a negative potential, beyond the
Nernst potential for K+, thereby creating an inward electrochemical
gradient for K+ across the basolateral membrane
(Leyssens et al., 1993
;
Wiehart et al., 2003
). The
possible function of KATP channels, if present, in Malpighian
tubule cells may be to contribute to K+ uptake in certain
conditions, in parallel with the Na+/K+-ATPase and other
K+ uptake mechanisms.
KATP channels were first discovered in cardiac myocytes
(Noma, 1983) and were later
found in many other tissues (Ashcroft and
Ashcroft, 1990
). The properties of KATP channels have
been described (for reviews, see Ashcroft
and Ashcroft, 1990
; Seino,
1999
; Wang et al.,
1992
). Depending on location, these channels exhibit differences
in function and therefore differ somewhat in their properties; however, all
KATP channels are highly selective for K+ ions,
displaying inward rectification with inward conductances in the range of
20-300 pS. They are regulated by the intracellular ATP concentration and
blocked by the highly specific sulfonylureas, of which glibenclamide and
tolbutamide are best described (Ashcroft
and Ashcroft, 1990
).
The present study investigates the possible presence of KATP channels in the tubule epithelium of Tenebrio by testing the effect of glibenclamide on Malpighian tubule secretion rates and basolateral membrane potentials. We investigate the possibility of a functional link between the activity of the basolateral Na+/K+-ATPase and K+ conductance via the proposed KATP channels by first stimulating this pump with an increase in Na+ concentration and then inhibiting it by means of ouabain. Finally, we examine the basolateral membrane sensitivity to the bath K+ in the presence and absence of glibenclamide. To our knowledge, this is the first study that investigates the presence of KATP channels in the Malpighian tubules of an insect.
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Materials and methods |
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Artificial salines
The composition of the control bathing solution was as follows
(Nicolson, 1992): 90 mmol
l-1 NaCl, 50 mmol l-1 KCl, 5 mmol l-1
MgCl2, 2 mmol l-1 CaCl2, 6 mmol
l-1 NaHCO3, 4 mmol l-1
NaH2PO4, 10 mmol l-1 glycine, 10 mmol
l-1 proline, 10 mmol l-1 serine, 10 mmol l-1
histidine, 10 mmol l-1 glutamine and 50 mmol l-1
glucose. The pH was adjusted to 7.0 with HCl and the osmolality was kept at
390 mosmol kg-1. Low [K+] solutions were obtained by
replacing KCl with NaCl, and low [Na+] solutions by replacing NaCl
with KCl (low-Na+ solutions contained 6 mmol l-1
Na+). Solutions were freshly prepared each week, filtered through
0.22 µm Millipore filters and kept at 2°C until used. The pH was
measured daily before use. In low [Na+] experiments and experiments
containing Ba2+, NaH2PO4 was omitted from all
salines to maintain constant osmolality and prevent precipitation. Control
experiments in which NaH2PO4 was omitted showed no
change in secretion rate or electrical profile.
The following pharmacological substances were tested on Malpighian tubule preparations: barium chloride (Sigma, Bornen, Belgium), ouabain (Fluka, Buchs, Switzerland), glibenclamide (Sigma) and cyclic AMP (cAMP; Sigma).
Fluid secretion experiments
The technique of measuring fluid secretion rates was described previously
(Wiehart et al., 2002).
Secretion was measured in control Ringer containing 1 mmol l-1 cAMP
(control) and subsequently in control Ringer containing cAMP and
glibenclamide. Rates of secretion were expressed as a percentage of the third
control rate reading. 6-10 replicates were done for each experiment.
Electrical potential difference measurements
This method was described in detail previously
(Wiehart et al., 2003). In
short, a portion of a Malpighian tubule (3-5 mm) was suspended in a Ringer
bath. Intracellular [basolateral membrane potential (Vbl)]
measurements were performed with 3 mol l-1 KCl-filled
microelectrodes. Cell impalement was accepted if a sudden drop in potential
occurred, if the potential was stable for at least a few minutes and if the
electrode potential differed by not more than 3 mV from the baseline after
withdrawal.
Statistics
Results are presented as means ± S.E.M., with the number of tubules
(N) or number of measurements (n) in parentheses. The
statistical significance of differences in fluid secretion or electrode
potentials was evaluated by paired or unpaired Student's t-tests
(two-tailed). A value of P<0.05 was accepted as statistically
significant.
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Results |
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The effect of glibencamide on Vbl
In a low bath [K+] (5 mmol l-1), the addition of 0.5
mmol l-1 glibenclamide elicited a similar change in
Vbl to that previously seen in the presence of
Ba2+ (Wiehart et al.,
2003), although to a lesser degree. Vbl
responded to glibenclamide by either a small but significant hyperpolarization
from -56.6±3.3 mV to -59.7±3.3 mV
(Fig. 2A; P=0.01,
n=8; in one experiment, there was a marked hyperpolarization of 12
mV) or a significant depolarization from -68.3±3.8 mV to
-52.3±1.5 mV (Fig. 2B;
P=0.008, n=4).
|
Subsequent addition of Ba2+ reinforced either the hyperpolarization or the depolarization initiated by glibenclamide (both responses are shown in Fig. 2).
The experimental protocol was reversed to determine whether glibenclamide had an effect on Vbl in the presence of Ba2+. Again, glibenclamide caused a further hyperpolarization of Vbl from -51.8±5.6 mV to -54.7±5.8 mV (n=5, P<0.006) or depolarization from -45 mV to -41 mV (n=1) (results not shown), following the response initiated by Ba2+. The addition of glibenclamide to control Ringer (50 mmol l-1 K+) had no visible effect on Vbl (n=10).
Vbl in the presence of ouabain
Previously, we found that ouabain (1 mmol l-1) added to control
Ringer (50 mmol l-1 K+) significantly reduced fluid
secretion but had no visible effect on Vbl
(Wiehart et al., 2003).
Blocking of the outward electrogenic current of the
Na+/K+ pump by ouabain is expected to cause, if
anything, a depolarization of the membrane. The absence of a visible effect
could be due to the high conductance (mainly due to K+) of the
basolateral membrane. Ouabain had a variable effect on Vbl
in low bath [K+] (5 mmol l-1), the tubule cells
responding either by a small hyperpolarization of 3 mV (n=1) or a
depolarization of 3-6 mV (n=3; results not shown). This variable
result was further investigated in the presence of 6 mmol l-1
Ba2+ to reduce the impact of highly conductive K+
channels. Two of 16 experiments showed a slight depolarization of
Vbl in the presence of ouabain. Surprisingly, in all other
experiments, Vbl responded by a small but significant
hyperpolarization. Fig. 3A
shows the result of an experiment in which Vbl
hyperpolarized from -64 mV to -73 mV. The observed hyperpolarization occurred
gradually over a period of 3-5 min and dropped back to pre-ouabain-treated
potentials within 1 min of washout. Fig.
3B summarises the results of all 16 experiments. Ouabain had no
detectable effect on Vbl in control Ringer (50 mmol
l-1 K+) in the presence of Ba2+
(n=4).
|
The effect of ouabain on Vbl in the presence
of glibenclamide
The effect of ouabain was tested again but this time in the presence of
glibenclamide (and Ba2+). The experiments in
Fig. 4 illustrate the result.
After the addition of glibenclamide and Ba2+, which either caused a
hyperpolarization (Fig. 4A) or
depolarization (Fig. 4B) of
Vbl, the addition of 1 mmol l-1 ouabain always
resulted in a depolarization of Vbl, averaging
8.5±1.4 mV (n=8, P=0.001).
|
Further indications of KATP channels in the basolateral
membrane
In the presence of Ba2+, although a loss of K+
sensitivity is expected, a change in the bath [K+] from 5 mmol
l-1 K+ to 140 mmol l-1 K+ caused a
depolarization of Vbl from -88.8±2.7 mV to
-13.7±1.9 mV, followed by a repolarization to -51.8±7.0 mV
beginning after 3-8 min (n=6). A typical experiment is shown in
Fig. 5A, and
Fig. 5B summarises the results
of six experiments. Such a repolarization was never seen after a 20 min period
in a high [K+] in the absence of Ba2+ (result not
shown).
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Fig. 6 shows the result of a similar experiment but in the presence of 0.5 mmol l-1 glibenclamide. Although Vbl still depolarized by 43.1±5.7 mV (n=6) when the bath [K+] was changed from 5 mmol l-1 K+ to 140 mmol l-1 K+, this was significantly less than the depolarization of 75 mV previously seen in the absence of glibenclamide. Furthermore, no subsequent repolarization of Vbl was seen in any of the experiments even after 30 min of high [K+]. The rate of response of the basolateral membrane to either the high or low [K+] was noticeably affected in the presence of glibenclamide. With both Ba2+ and glibenclamide present, Vbl hyperpolarized over a mean time of 15 min (n=6) in response to low bath [K+] compared with 8 min (n=7) in the presence of Ba2+ alone. Likewise, Vbl depolarized over a mean period of 12 min (n=6) in response to a high [K+] compared with 3 min when only Ba2+ was present. During these experiments, the basolateral membrane became increasingly less sensitive to the bath [K+] with time. Reintroduction of a low bath [K+] hyperpolarized Vbl to -57±3.8 mV compared with the previous -66±6.2 mV (n=6, P=0.002).
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Discussion |
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The effect of glibenclamide on the basolateral membrane
potential
The involvement of KATP channels in control Ringer (50 mmol
l-1 K+) seems to be indicated by the inhibition of fluid
secretion by glibenclamide, although the substance had no visible effect on
Vbl in control Ringer. The lack of response might be due
to the masking of KATP channel activity by other highly conductive
K+ channels present in the basolateral membrane of insect
tubules.
In low bath [K+] (5 mmol l-1), glibenclamide had a
detectable effect on Vbl similar to that previously
observed with the K+ channel blocker Ba2+
(Wiehart et al., 2003).
Depending on the putative electrochemical gradient for K+,
glibenclamide either caused a small but significant hyperpolarization of
3.6±1.2 mV (Fig. 2A) or
a significant depolarization of 9±1.5 mV
(Fig. 2B) of
Vbl, indicating the inhibition of either inward
(hyperpolarization) or outward (depolarization) K+ movement through
glibenclamide-sensitive K+ channels. The open probability of the
KATP channels at bath concentrations of 135 mmol l-1
NaCl and 5 mmol l-1 KCl must therefore be relatively high. This is
supported by a patch-clamp study on rat cortical collecting tubules in which
the authors found a bath concentration of 5 mmol l-1 KCl and 135
mmol l-1 NaCl to be optimal for KATP channels to be in
an open state (Wang et al.,
1990
).
The addition of 6 mmol l-1 Ba2+ complements the
initial response observed with glibenclamide by a further hyperpolarization or
depolarization of Vbl, demonstrating the inward and
outward electrochemical gradient for K+, respectively
(Fig. 2). The sensitivity of
this large family of KATP channels to Ba2+ is not clear.
Tsuchiya et al. (1992)
determined that KATP channels are almost exclusively responsible
for the K+ conductance in the renal proximal tubule. Blocking the
conductive K+ channels with glibenclamide caused a 95% inhibition
in the basolateral membrane K+ conductance compared with 84% when
blocking with Ba2+. This difference indicated that the
KATP channels were less sensitive to Ba2+. In line with
this study, the KATP channels present in Tenebrio
Malpighian tubule cells appear less sensitive to Ba2+. The
additional hyperpolarization from -51.8±5.6 mV to -54.7±5.8 mV
(n=5) or depolarization from -45 mV to -41 mV (n=1) caused
by glibenclamide in the presence of Ba2+ substantiates this.
However, caution must be exercised when interpreting results with
glibenclamide, as this sulphonylurea compound has been shown to inhibit the
cystic fibrosis transmembrane conductance regulator (CFTR) Cl-
channel (Sheppard and Welsh,
1992; Schultz et al.,
1996
), which is present in most secreting epithelia of
vertebrates. Although this CFTR channel has not been characterized in insects,
we cannot rule out its existence.
The effect of ouabain and glibenclamide on
Vbl
Fluid secretion is inhibited by 1 mmol l-1 ouabain
(Wiehart et al., 2003).
However, ouabain has no detectable effect on Vbl in
control conditions (50 mmol l-1). Possibly, the presence of high
conductance K+ channels masked an effect on any other electrogenic
process in the basolateral membrane. The effect expected when the outward
electrogenic pump current is blocked is a depolarization of the membrane
(Messner et al., 1985
;
Horisberger and Giebisch,
1988
). This has been observed in unstimulated salivary glands of
Calliphora (Berridge and Schlue,
1978
) as well as in Malpighian tubule cells of Drosophila
(Linton and O'Donnell, 1999
).
In low K+, in the presence of Ba2+,
Vbl was affected: in 14 out of 16 cells, the membrane
hyperpolarized in the presence of ouabain. Involvement of KATP
channels was confirmed by applying ouabain after pretreatment with
glibenclamide (in the presence of Ba2+): the effect was reversed
and in all experiments (n=8) ouabain depolarized
Vbl (Fig.
4).
Glibenclamide changes the sensitivity of
Vbl to the external [K+]
In contrast to findings for the forest ant Formica polyctena
(Weltens et al., 1992), the
basolateral membrane of Tenebrio tubule cells does not appear to lose
its sensitivity to the bath [K+] in the presence of 6 mmol
l-1 Ba2+. Increasing the bath [K+] from 5
mmol l-1 to 140 mmol l-1 K+ resulted in an
immediate depolarization of Vbl, with a mean value of
75.3±2.4 mV (n=6). However, this sudden depolarization was
followed by a repolarization of 30-40 mV after 3-8 min
(Fig. 5A). Again, the
involvement of the Na+/K+-ATPase and the KATP
channels seems to be the explanation.
A rise in Na+ transport and intracellular [Na+] is
the primary physiological stimulus for the Na+/K+-ATPase
in vertebrate tissue (Mauerer et al.,
1998; Tsuchiya et al.,
1992
). In our study, a low bath [K+] (5 mmol
l-1), and therefore a high [Na+] (141 mmol
l-1), could be responsible for activating the
Na+/K+-ATPase, thereby increasing the open probability
of the KATP channels. The initial large depolarization seen when
changing the bath [K+] from a low to a high value is most probably
due to the following: (1) Ba2+, being a competitive inhibitor of
K+ channels, is `knocked-off' by the inward flux of K+
ions at high bath [K+] (Eaton
and Brodwick, 1980
; Armstrong
and Taylor, 1980
) and (2) the initial intracellular [ATP] is
relatively low, which means the open probability of the KATP
channels is high, allowing an initial influx of K+ ions. However,
at a bath concentration containing no NaCl (140 mmol l-1 KCl), the
Na+/K+ pump stops functioning, resulting in a
time-dependent increase of intracellular [ATP] and therefore the closing of
KATP channels. This might explain the observed repolarization of
Vbl after a few minutes: the apical V-ATPase increases the
cell negative potential, and compensation by K+ entrance across the
basolateral membrane is slowed down. Again, this response was not seen in
experiments without Ba2+, indicating that other highly conductive
K+ channels mask the presence of KATP channels.
To substantiate the above hypothesis, experiments were repeated in the presence of Ba2+ and 0.5 mmol l-1 glibenclamide. The hyperpolarization of Vbl to a mean of -66±6.2 mV, when [K+] was decreased, was far less than the -88.5±3.4 mV when only Ba2+ was present. Moreover, although a substantial depolarization of Vbl was still seen when the bath [K+] was changed from 5 mmol l-1 to 140 mmol l-1 (43 mV), this was considerably less than in experiments that involved Ba2+ alone. Most remarkable, however, was the sluggish response of Vbl in the presence of both substances. Both the hyperpolarization and depolarization of Vbl in response to a different bath [K+] were much slower, with the depolarization in some experiments taking more than six times longer than in earlier experiments with only Ba2+. Moreover, the depolarization of Vbl was no longer followed by a repolarization, indicating that the putative KATP channels were blocked and therefore insensitive to the increase in intracellular [ATP] expected when the Na+/K+-ATPase is inhibited by a decrease in Na+. The final depolarization (after repolarization), when only Ba2+ was present, was 37±4.9 mV (n=6) and is comparable with the depolarization of 43±5.7 mV (n=6) when both substances were present, possibly indicating that the KATP channels are blocked in both instances. Another marked effect of glibenclamide was that the basolateral membrane became increasingly less responsive to the surrounding [K+] with time. Reintroduction of a low bath [K+] (5 mmol l-1) still elicited a hyperpolarization of Vbl, but to a lesser extent. In experiments where only Ba2+ was present, Vbl stayed responsive to the bath [K+] (Fig. 5A).
In summary, the effects of glibenclamide, a KATP channel blocker, on both the fluid secretion rate and basolateral membrane potentials of Tenebrio Malpighian tubules are strong indications of the presence of KATP channels and the involvement of these channels in ion transport.
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Acknowledgments |
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References |
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