Regulation of Na+/K+-ATPase activity by nitric oxide in the kidney and gill of the brown trout (Salmo trutta)
Institute of Biology, University of Southern Denmark, Odense University, Campusvej 55, DK-5230 Odense M, Denmark
* Author for correspondence (e-mail: steffen{at}biology.sdu.dk)
Accepted 10 February 2003
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Summary |
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Key words: brown trout, Salmo trutta, kidney, gill, Na+/K+-ATPase, nitric oxide, SNP, sodium nitroprusside, cyclic GMP.
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Introduction |
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Compensatory ion transport is accomplished by the gill epithelium in both
FW and SW, countering NaCl loss and influx, respectively. In FW, the combined
action of basolateral Na+/K+-ATPase and apical
H+-ATPase constitutes the driving force for uptake of NaCl
via apical Na+ channels and
Cl/HCO3 exchange
(Avella and Bornancin, 1989;
Marshall, 2002
). Both chloride
cells and pavement cells may be involved in the uptake of NaCl
(Wilson et al., 2000
). In SW,
Cl excretion involves apical Cl channels
and basolateral Na+/K+-ATPase and
Na+/K+/2Cl cotransporter,
Na+ excretion being paracellular (see
Marshall, 2002
). The cellular
site for this salt secretion is known to be chloride cells
(Foskett and Scheffey,
1982
).
Hence, the Na+/K+-ATPase is of major importance in
the salmonid kidney and gill. When the external salinity changes, expression
of this and several other ion transporters in the gill is changed, a process
that is mediated by several slow-acting hormones
(McCormick, 2001;
Evans, 2002
). Hormonal
long-term regulation of Na+/K+-ATPase seems less
prominent in the kidney (Madsen et al.,
1995
), where regulatory adjustments may rely more on rapid
alterations of ion transport protein activity. Whereas expressional regulation
of the Na+/K+-ATPase is well documented in teleosts,
short-term regulatory events are less well investigated. This is despite the
fact that such regulation of pump activity has a great potential, as seen in
various mammalian tissues (Therein and
Blostein, 2000
). A few studies have, however, documented
short-term hormonal regulation in teleost tissue. For instance, in eel kidney
and gill, angiotensin II modulates Na+/K+-ATPase
activity within minutes (Marsigliante et al.,
1997
,
2000
). The second messenger
systems involving protein kinase C (PKC;
Crombie et al., 1996
) and
protein kinase A (PKA; Tipsmark and
Madsen, 2001
) have been shown to modulate
Na+/K+-ATPase activity in the cod and trout gill,
respectively. From the mammalian field, it is known that the nitric
oxidecyclic GMP (NOcGMP) messenger system is involved in
regulation of the Na+/K+-ATPase in the kidney and many
other tissues (Therein and Blostein,
2000
; Ortiz and Garvin,
2002
). Nitric oxide synthase (NOS) catalyzes the production of NO,
working as an autocrine and paracrine messenger. NO itself can activate the
soluble guanylate cyclase (sGC) and can therefore work through the action of
cGMP and the cGMP-activated kinase (PKG;
Lincoln and Komalavilas,
2000
).
It is not known whether NO plays a part in the regulation of Na+/K+-ATPase in lower vertebrates. The aim of the present study was to investigate the possible effect of NO and cGMP on Na+/K+-ATPase activity of the kidney and gill of the brown trout Salmo trutta. We used an in vitro system to analyse the effect of NO and cGMP on in situ Na+/K+-ATPase activity, measured as ouabain-sensitive Rb+ uptake. To further investigate potential mechanisms, the Na+, K+ and cGMP concentrations in the tissues were analysed.
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Materials and methods |
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Preparations of tissue blocks
After stunning the fish with a blow to the head, blood was drawn from the
caudal blood vessels. The fish was then killed by cutting the spinal chord and
pithing of the brain. Blocks of kidney tissue (approximately 48 mg)
were excised from the posterior part of the trunk kidney and rinsed in chilled
salmon Ringer's solution equilibrated with 99% O2/1% CO2
(140 mmol l1 NaCl, 15 mmol l1
NaHCO3, 3.5 mmol l1 KCl, 1.5 mmol
l1 CaCl2, 1.0 mmol l 1
NaH2PO4, 0.8 mmol l1 MgSO4,
5.0 mmol l1 D-glucose and 5.0 mmol l1
N-2-hydroxyethyl-piperazine propanesulfonic acid; osmolality, 310
mosmol kg1; pH 7.8). The gill filaments were excised free of
the cartilage and rinsed in Ringer's. Each gill arch was then cut
transversally into blocks of 35 pairs of filaments (510 mg),
held together by the interfilament septum. Samples were equilibrated for
3060 min in Ringer's at 15°C prior to all incubations and
treatments.
Preparations of cell suspensions
After cutting the spinal chord and pithing of the brain, 2000 U of heparin
(in Ringer's solution) was injected into the heart. The bulbus arteriosus was
cannulated and perfused over 10 min with 1015 ml of heparinized (20 U
ml1) Ca2+- and Mg2+-free Ringer's
solution followed by 5 min of perfusion with heparin-free Ringer's. All gill
arches were excised and rinsed in ice-cold Ca2+- and
Mg2+-free Ringer's solution. The arches were scraped with a micro
slide and the soft tissue suspended in 10 ml lysis buffer (9 parts 0.17 mol
l1 NH4Cl, 1 part 0.17 mol l1
Tris-HCl, pH 7.4: Yust et al.,
1976) according to Verbost et al.
(1994
). Lysis of remaining
blood cells and tissue fractionation was obtained by incubation in lysis
buffer for 1020 min at room temperature. The cells were suspended at
the beginning and re-suspended at the end of this incubation by drawing them
through a 10 ml pipette (3 mm bore diameter). The suspension was filtered
through nylon gauze (80 µm) to remove cartilage and major cell debris. The
cells were washed three times in Ca2+- and Mg2+-free
Ringer's solution and spun down at 150 g for 5 min between
each wash. They were finally re-suspended in 15 ml Ca2+- and
Mg2+-free Ringer's and kept on ice until use. Viability was checked
with the tryphan blue exclusion method
(Sharpe, 1988
) and was
typically around 90%.
Incubations and experiments
In situ Na+/K+-ATPase activity
The method employed followed Tipsmark and Madsen
(2001) with minor
modifications. In order to measure Rb+ uptake in tissue blocks, the
Ringer's was replaced with Rb+-Ringer's solution containing 3.5
mmol l1 RbCl instead of KCl. In all routine measurements,
kidney and gill blocks were incubated in Rb+-Ringer's for 10 min at
15°C. Ouabain-sensitive Rb+ uptake (representing in
situ Na+/K+-ATPase activity) was calculated as the
difference between total uptake and uptake in samples both pre-incubated (10
min in Ringer's) and incubated (10 min in Rb+-Ringer's) with 1 mmol
l1 ouabain. Following incubation, the extracellular space
was washed free of Rb+ for 4x15 min at 0°C in
Tris-sucrose buffer (10 mmol l1 Tris, 260 mmol
l1 sucrose, pH 7.8). The tissue blocks were then blotted on
filter paper and extraction of ions was performed overnight at 4°C in 5%
trichloroacetic acid (TCA).
Rubidium uptake in cell suspensions was measured as described previously
(Tipsmark and Madsen, 2001).
The cell suspension was pelleted (150 g, 5 min) and
re-suspended in a minimal volume of Ca2+- and Mg2+-free
Ringer's. The incubation was started by transferring aliquots (20 µl) to
Rb+-Ringer's in 24-wells with or without 1.0 mmol
l1 ouabain at 15°C. The standard incubation time was 10
min. Incubation was terminated by pelleting the cells (15 000
g, 30 s) and washing three times with 0.1 mol
l1 MgCl2. Rubidium was determined after
extraction in 5% TCA at 4°C for 1 h. The pellet was solubilized overnight
in 0.2 mol l1 NaOH and protein content was determined
according to Lowry et al.
(1951
).
For Rb+ measurements, KCl was added to the extracts to a final concentration of 20 mmol l1, and Rb+ was determined by atomic absorption spectrophotometry at 780.8 nm with a slit of 2.0 nm and a red filter (Perkin Elmer 2380; Mountain View, CA, USA). Rubidium uptake in tissue blocks was expressed as nmol mg1 wet mass h1. Rubidium uptake in cell suspensions was expressed as nmol mg1 protein h1.
Experiments
In all experiments where Na+/K+-ATPase activity was
measured, test agents were present both during incubation in
Rb+-Ringer's and during a 10 min pre-incubation, unless otherwise
indicated. Donors of NO were always dissolved in Ringer's immediately before
the experiment.
The doseresponse relationship of the NO donor sodium nitroprusside (SNP; Sigma, St Louis, MO, USA; 0.001 mmol l1, 0.01 mmol l1, 0.1 mmol l1, 1 mmol l1; 10 min pre-incubation) on Na+/K+-ATPase activity in kidney and gill tissue blocks was investigated in one experiment.
A time-course experiment of the effect of 1 mmol l1 SNP on Na+/K+-ATPase activity in kidney and gill tissue was done by pre-incubation for 0 min, 10 min and 60 min with SNP.
In three separate experiments the effect of (1) the NO donor papa-nonoate
(NOC-15; Sigma; 0.2 mmol l1; concentration selected in
accordance with Maragos et al.,
1993), (2) lipid-soluble dibutyryl cyclic GMP (db-cGMP; Sigma; 1
mmol l1) and (3) the NO scavenger
2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl 3-oxide (PTIO; Sigma; 1 mmol
l1) in combination with SNP (0.5 mmol l1)
on Na+/K+-ATPase activity in kidney and gill tissue
blocks was examined. In each experiment, a parallel incubation with SNP (1.0
mmol l1, 1.0 mmol l1 and 0.5 mmol
l1, respectively) was used for direct comparison. The effect
of SNP (1 mmol l1) on Na+/K+-ATPase
activity of gill cells in suspension was examined without pre-incubation with
SNP.
The effect of SNP (1 mmol l1) on tissue Na+ and K+ levels was examined by incubating kidney and gill tissue in triplicate in Ringer's solution with or without SNP for 2x30 min followed by blotting of the tissue, weighing and extraction overnight at 4°C in 5% TCA. The Na+ and K+ content of the supernatant was determined using a flame photometer (Instrumentation Laboratory 243; Lexington, MA, USA) with lithium as an internal standard. The values were expressed in nmol mg1 wet mass.
The [14C]inulin space was determined after 2x30 min and 3x30 min incubation in Ringer's solution containing [14C]inulin (3700 Bq ml1). The tissues were incubated with or without SNP (1 mmol l1).
The effect of SNP on the cGMP concentration in kidney and gill tissue was
examined. Kidney and gill blocks were incubated in Ringer's with or without
SNP (1 mmol l1) for 10 min. Following homogenization in 0.1
mol l1 HCl (1 ml) with a polytron homogenizer (3040
mg tissue wet mass), the crude homogenate was centrifuged (13 000
g, 15 min) and an aliquot of the supernatant was used for
protein determination (Lowry et al.,
1951). Another aliquot (0.5 ml) was dried overnight in a Speedyvac
centrifuge, re-suspended in 1 ml of assay buffer and centrifuged (13 000
g, 15 min). Cyclic GMP was analyzed in the supernatant after
acetylation of the samples using a commercial enzyme immunoassay (Amersham
Pharmacia Biotech, Uppsala, Sweden) following the manufacturer's protocol, and
cGMP concentration was calculated relative to tissue protein content (fmol
cGMP mg1 protein).
Statistical analyses
Dataset with more than two groups were analysed by a randomized one-way
block analysis of variance (ANOVA) and subsequently compared by the Tukey
honest significant difference (HSD) procedure. Dataset with two groups were
analysed by a paired Student's t-test. All statistical analyses were
done using Systat (Evanston, IL, USA) and significant differences were
accepted when P<0.05. Indicated N values signify the
number of fish represented in each group.
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Results |
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The time-course dependence of the SNP effect on Na+/K+-ATPase activity was investigated using 1 mmol l1 SNP. As shown in Fig. 2, Na+/K+-ATPase activity was inhibited after 10 min and 60 min pre-incubation in kidney tissue and after 0 min and 10 min in the gill. In a separate experiment, the effect of SNP on isolated gill cells was examined, and Na+/K+-ATPase activity was also inhibited by approximately 50% (control, 85.5±4.7 nmol Rb+ mg1 protein h1; 1 mmol l1 SNP, 43.6±9.2 nmol Rb+ mg1 protein h1).
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To confirm that the effect of SNP was indeed associated with NO release, we examined the effect of another NO donor (NOC-15) and the effect of SNP in combination with the NO scavenger PTIO on Na+/K+-ATPase in intact tissue. As shown in Fig. 3, NOC-15 (0.2 mmol l1), like SNP, significantly inhibited Na+/K+-ATPase activity in both the kidney and gill. When employing the NO scavenger PTIO (1 mmol l1) in combination with SNP (0.5 mmol l1), the effect of SNP on the Na+/K+-ATPase was abolished in both tissues (Fig. 4).
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Because intracellular Na+ concentration is a primary substrate regulator of Na+/K+-ATPase activity, we examined whether NO-associated effects on intracellular ion levels could possibly explain the inhibitory effect. Accordingly, Na+ and K+ content and inulin space in the tissue following incubation with SNP (1 mmol l1; 2x30 min) were analysed (Table 1). In the kidney, Na+ content increased and K+ content decreased in a 3:2 ratio. In the gill, there was no effect of SNP on the level of either ion. To ensure that the effect of SNP on Na+ and K+ content were indeed due to changes in intracellular concentrations and not caused by changes in the extracellular compartment, tissue inulin space was determined under similar conditions. The inulin space was unaffected by SNP (1 mmol l1) during 2x30 min incubation with SNP (Table 1). To validate that 2x30 min incubation was sufficient to estimate the inulin space, a parallel incubation for 3x30 min with or without SNP (1 mmol l1) was performed. Since this led to no significant change in inulin space, 2x30 min incubation was sufficient to ensure a correct estimation.
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To further address the possible mechanism of NO, cGMP concentration in the tissues was analysed following 10 min incubation with SNP (1 mmol l1). NO significantly increased the cGMP level in both kidney and gill tissue (Table 1; P<0.05, N=6). To further evaluate the significance of these results, the effect of the lipid-soluble cGMP analogue db-cGMP on in situ Na+/K+-ATPase activity was examined. This was done on intact kidney and gill tissue in parallel with SNP. As shown in Fig. 5, Na+/K+-ATPase activity in both kidney and gill was significantly inhibited by db-cGMP (1 mmol l1) as well as by the NO donor (1 mmol l1 SNP).
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Discussion |
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The present study is the first to demonstrate effects of NO on
Na+/K+-ATPase in fish tissues. In both kidney and gill,
the NO donor SNP inhibited in situ
Na+/K+-ATPase activity in a dose-dependent manner. Since
another NO donor (NOC-15) had a similar effect, and an NO scavenger (PTIO)
abolished the inhibition of the pump, the effect is indeed related to NO
itself. The present study was performed on FW-acclimated fish. Acclimation
salinity is of potential importance for the observed effect, as
Na+/K+-ATPase subunit isoform expression may be salinity
dependent (Lee et al., 1998)
and isoforms may be differentially regulated by NO
(Blanco et al., 1998
;
Pontiggia et al., 1998
).
However, since a similar inhibitory effect of NO on gill
Na+/K+-ATPase has been observed recently in
SW-acclimated Atlantic salmon (L. O. E. Ebbesson and C. K. Tipsmark,
unpublished), the results also apply to SW-acclimated salmonids.
Nitric oxide has been shown to modulate ion transport in several mammalian
tissues, the effect apparently being tissue dependent. Inhibitory effects on
the Na+/K+-ATPase have been found in the kidney
(opossum, Liang and Knox,
1999; rat, McKee et al.,
1994
), the choroid plexus (bovine,
Ellis et al., 2000
), alveolar
cells (rat, Guo et al., 1998
),
aortic endothelial cells (porcine, Gruwel
and Williams, 1998
), liver (rat,
Muriel and Sandoval, 2000
) and
brain (porcine, Sato et al.,
1997
). Stimulatory effects have been found in rat trachea
(de Oliveira Elias et al.,
1999
) and rabbit aorta (Gupta
et al., 1994
). The effect of NO has also been shown to differ
among different kidney segments (Ortiz and
Garvin, 2002
). Isoform-specific effects on
Na+/K+-ATPase of PKG, which is often found to mediate NO
effects, have also been observed. Thus, PKG inhibits the
1-
and
3-but not the
2-isoform in infected
SF-9 cells (Blanco et al.,
1998
) and
1-but not the
2- and
3-isoform in brain endothelial cells
(Pontiggia et al., 1998
).
In addition to effects on the Na+/K+-ATPase, NO has
been shown to inhibit the Na+/K+/2Cl
cotransporter (kidney, Ortiz et al.,
2001), the Na+/H+-exchanger (kidney,
Garvin and Hong, 1999
) and
apical Na+ channels (kidney,
Stoos et al., 1994
). Since
these ion transport proteins are also present in fish osmoregulatory tissues,
the observed action of NO on Na+/K+-ATPase activity
could be indirect and possibly mediated by reduced access to Na+,
the rate-limiting substrate. Assuming that changes in intracellular
Na+ content are reflected in measurements of whole-tissue
Na+ content, the present data indicate that the inhibition by NO
was not caused by reduced Na+ access in either tissue. Hence, the
effect seems to be directly on the Na+/K+-ATPase. The
above assumption requires that the extracellular space is unaffected by
treatment and that there is a diffusion equilibrium between the extracellular
space and incubation medium. Inulin-space estimates validated the former
assumption. The latter assumption was validated through optimisation of the
assay procedure (Tipsmark and Madsen,
2001
), where it was shown that Rb+ uptake was linear
over time and lacked an initial lag phase. Thus, the present changes in
whole-tissue ion levels most likely reflect changes at the intracellular
level. A minor problem with interpretation of the gill ion data, however, is
that the Na+/K+-ATPase is specifically concentrated in a
minor fraction of the epithelial cells, the chloride cells. These cells
constitute 10% or less of the total cell numbers
(Wilson and Laurent, 2002
),
and any change in the ion content of these cells may be masked by a different
or lack of change in the majority of other cells. So, the gill ion data should
be interpreted cautiously, and future studies should focus on changes in
intracellular ion concentrations within specific cell types of the gill.
Activation of the sGC leads to increased intracellular cGMP concentrations
and is believed to mediate many of the physiological effects of NO, even
though cGMP-independent effects have also been described
(Gupta et al., 1994;
Sato et al., 1997
). The
present study demonstrated increased whole-tissue cGMP concentration in
response to SNP, apparently by activating sGC in both tissues. The
lipid-soluble cGMP analogue (db-cGMP) had a similar inhibitory effect as NO on
Na+/K+-ATPase activity. Since NO elevates the cGMP
concentration in both tissues, the NO effect on the
Na+/K+-ATPase may be a cGMP-dependent effect, possibly
related to activation of PKG. Phosphorylation of a PKG substrate could
underlie the regulatory event, and, in fact, the
-subunit of the
Na+/K+-ATPase from the mammalian kidney has itself been
shown to be a substrate for PKG (Fotis et
al., 1999
). The present effect may thus be related to
cGMP-dependent phophorylation of either the
-subunit or, alternatively,
a regulatory protein component, as seen for PKC modulation of the shark rectal
gland enzyme (Mahmmoud et al.,
2000
). The
-subunit has been shown to be a substrate for
PKA and PKC in several species, sometimes associated with modulation of
Na+/K+-ATPase activity
(Therein and Blostein, 2000
).
PKA and PKC can also phosphorylate the brown trout
-subunit in
vitro (C. K. Tipsmark and Y. A. Mahmmoud, unpublished results), and cAMP
modulates activity of the trout enzyme
(Tipsmark and Madsen, 2001
).
Alternatively, more-complex pathways involving secondary modulators could be
involved in the present effect. For example, Liang and Knox
(1999
) found inhibition of
Na+/K+-ATPase in opossum kidney cells by NO to be
associated with activation of the PKC
-isoform.
Several hormones and cytokines are known to influence tissue NO and cGMP
concentrations. Atrial natriuretic peptide (ANP) inhibits
Na+/K+-ATPase via activation of PKG in the rat
kidney (Scavone et al., 1995).
Angiotensin II activates NOS and sGC in the rat kidney
(Zhang and Mayeux, 2001
). In
the mammalian kidney, bradykinin, acetylcholine and oxytocin also activate NOS
and sGC and inhibit Na+/K+-ATPase
(McKee et al., 1994
). Hence, a
number of chemical modulators of ion transport may work via NO/cGMP.
Recent findings by Evans et al.
(2002
) indicate that the
endothelin agonist sarafotoxin and NO itself inhibit short-circuit current
(Isc) across the killifish operculum membrane. The
mechanism behind these observations may be an effect on the
Na+/K+-ATPase, as found in the present study.
Salinity changes have been found to evoke rapid (in the order of a few
hours) modulation of the Na+/K+-ATPase in the gill of
the killifish (Towle et al.,
1977; Mancera and McCormick,
2000
) but not in salmonids, where only long-term expressional
changes (in the order of several days) have been reported so far
(Madsen et al., 1995
;
Mancera and McCormick, 2000
).
Even so, short-term adjustment of ion transport in the gill and kidney should
be anticipated during feeding and stress. Short-term modulation of the
Na+/K+-ATPase as seen in mammalian tissues
(Therein and Blostein, 2000
),
involving hormones and second messengers, has been found in several teleosts
in response to angiotensin II (eel gill,
Marsigliante et al., 1997
; eel
kidney, Marsigliante et al.,
2000
), PKC activation (cod gill,
Crombie et al., 1996
), PKA
activation (trout gill and kidney,
Tipsmark and Madsen, 2001
) and
NO (present study).
Juxta-localization of the neuronal isoform of NOS (nNOS) and
Na+/K+-ATPase has recently been reported using
immunocytochemistry in the killifish opercular membrane
(Evans, 2002). As mentioned
before, the physiological significance of this observation was supported by
data showing the inhibition by NO of the Isc across the
opercular skin (Evans et al.,
2002
). In this study, the NOS inhibitor L-NAME stimulated the
Isc. Thus, NaCl transport over the opercular skin appears
to be under tonic control by endogenously produced NO. In the Atlantic salmon
gill, nNOS co-localizes with Na+/K+-ATPase in chloride
cells and/or adjacent accessory cells, and gill
Na+/K+-ATPase is also inhibited by NO in this species
(L. O. E. Ebbesson and C. K. Tipsmark, unpublished). In the rainbow trout,
nNOS has recently been localized in the kidney
(Jimenez et al., 2001
). These
observations support the present study well and indicate that NO is an
important autocrine/paracrine modulator of ion transport in the salmonid gill
and kidney, adjusting it to the current need. Future studies employing NOS
inhibitors and stimulators should focus on the role of endogenously produced
NO in the regulation of Na+/K+-ATPase.
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Acknowledgments |
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References |
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