Electrogenic proton-regulated oxalate/chloride exchange by lobster hepatopancreatic brush-border membrane vesicles
1 Department of Physiology and Functional Genomics, College of Medicine,
University of Florida, Gainesville, FL 32610, USA
2 Department of Medicine, College of Medicine, University of Florida,
Gainesville, FL 32610, USA
3 Department of Biology, College of Arts & Sciences, University of North
Florida, Jacksonville, FL 32224, USA
* Author for correspondence (e-mail: gag{at}phys.med.ufl.edu)
Accepted 6 October 2003
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Summary |
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Key words: brush-border membrane vesicle, BBMV, oxalate, ion transport, hepatopancreas, electrogenic carrier mechanism, lobster, Homarus americanus
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Introduction |
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In invertebrates, specifically crustaceans, the hepatopancreas is involved
in both digestion and absorption of nutrients
(Gibson and Barker, 1979); in
addition, some investigators have implicated this organ as a site of excretion
(Dall, 1970
). The use of
isolated membrane vesicles has led to the definition of absorptive transport
mechanisms for a number of solutes in the hepatopancreatic brush border
(Ahearn and Clay,
1987a
,b
;
Ahearn et al., 1985
;
Gerencser et al., 1996
) and
also for a number of transport processes, including those for
Ox2, in the basolateral membrane (Gerencser et al.,
1995
,
2000
).
The present study uses hepatopancreatic brush-border membrane vesicles (BBMV) to characterize an electrogenic Ox2/Cl exchange mechanism that is relatively specific with respect to organic anions, is inhibited by stilbenes and is regulated by pH. The mechanism is reversible and, therefore, it can be utilized for either absorption or secretion of Ox2 (for excretory purposes) from the lobster hepatopancreatic epithelium.
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Materials and methods |
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Hepatopancreatic brush-border membrane vesicles (BBMV) were prepared from
fresh tissue removed from individual lobsters. Each membrane batch was
produced from a single organ (1525 g fresh mass) using a method of
combined osmotic disruption, differential centrifugation and magnesium
precipitation described previously by Ahearn and co-workers
(Ahearn and Clay, 1987a;
Ahearn et al., 1985
). Purity of
BBMV prepared by these methods was assessed by comparing the activities of
membrane-bound enzymes in vesicles with the activities of the same enzymes in
the original homogenate. These comparisons showed final pellet enrichments of
alkaline phosphatase (marker enzyme for apical membranes),
Na+/K+-ATPase (marker enzyme for basolateral membranes)
and cytochrome c oxidase (marker enzyme for mitochondrial membranes)
of 19.3-, 0.7- and 0.2-fold, respectively, suggesting that the isolated
vesicles were highly enriched with apical membranes and contained minimal
contamination from basolateral or organelle membranes.
Transport studies were conducted at 15°C using the rapid filtration
technique developed by Hopfer et al.
(1973). For time-course
experiments, a volume of vesicles (e.g. 20 µl) was added to a volume of
incubation media (e.g. 180 µl) containing 0.1 mmol l1
radiolabeled [14C]oxalate (specific activity 12.2 µCi
mmol1). At various incubation times, a known volume (20
µl) of reaction mixture was removed and plunged into 2 ml of ice-cold stop
solution (stop solution composition varied with experiment and generally
consisted of incubation media without any oxalate to stop the uptake process).
The vesicle suspension was then rapidly filtered through 0.65 µm Millipore
filters (presoaked in distilled water) and washed with another 5 ml of
ice-cold stop solution. Filters were transferred to vials containing Ready
Solv HP scintillation cocktail (Beckman, Chicago, IL, USA) and counted for
radioactivity in a Beckman LS-8100 scintillation counter. Transport
experiments involving incubations of less than 10 s wereconducted using a
rapid-exposure uptake apparatus (Inovativ Labor AG, Adliswil, Switzerland).
Uptake was initiated by mixing 5 µl of vesicles with a volume (e.g. 45
µl) of radiolabeled incubation media, and filters were washed and counted
for radioactivity as above. For short-term incubations, a blank was also run
for each condition by mixing stop solution, vesicles and radiolabeled
incubation media simultaneously; the resulting value was subtracted from
corresponding experimental results before determining uptake. Incubation and
intravesicular media varied between experiments and are indicated in the
figure legends. Oxalate uptake values were usually expressed as pmol
mg1 protein (Bio-Rad protein assay) per filter using the
specific activity of oxalate in the incubation media.
Unless otherwise indicated in the text or in the figure legends, valinomycin (50 µmol l1) and bilaterally equal potassium concentrations (10100 mmol l1) across the vesicular wall were present to short-circuit the membranes. Each experiment was repeated at least four times using membranes prepared from different animals. Within a given experiment each point was determined from three to five replicate samples and the experimental scatter between these replicates never exceeded 5%. Differences between experimental and control means were analyzed using a Student's t-test. Results of experiments are presented as means ± S.E.M.
[14C]oxalate as the K+ salt and 36Cl as the Na+ salt were obtained from New England Nuclear (Boston, MA, USA). Valinomycin, 4-acetamido-4'-isothiocyanostilbene-2,2'-disulfonic acid (SITS), 4,4'-diisothiocyano-2,2'-disulfonic stilbene (DIDS), carbonyl cyanide m-chlorophenylhydrazone (CCCP), 9-carboxyanthracene (9-AC), bumetanide, furosemide and other reagent grade chemicals were purchased from Sigma Chemicals (St Louis, MO, USA).
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Results |
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There is some evidence that Ox2 transport across plasma
membranes might occur via a Cl channel
(Freel et al. 1998;
Hatch et al. 1994
); therefore,
the following experiment investigated this premise
(Fig. 2). Vesicular and
incubation media contained 100 mmol l1 TMA-gluconate, 100
mmol l1 K-gluconate and 50 µmol l1
valinomycin. [14C]Ox2 vesicular uptake was
monitored in the presence (test) or absence (control) of 50 µmol
l1 9-AC, which is a Cl channel blocker
(Freel et al., 1998
;
Fig. 2). 9-AC was placed in
both the incubation and vesicular media. As can be seen, 9-AC had no effect on
the uptake of [14C]Ox2 into the vesicle
preparation.
|
Oxalate uptake into BBMV was not stimulated by incubation in media containing 100 mmol l1 K-gluconate (no valinomycin or internal K+) nor in the presence of 50 µmol l1 CCCP (a protonophase used to short-circuit the membrane potential in the absence of K+ and valinomycin, which are the normal reagents used to short-circuit the membrane potential; Fig. 3). However, when vesicles were preloaded with 25 mmol l1 KCl and incubated in TMA-gluconate media containing equimolar K+ and valinomycin, there was an overshoot Ox2 accumulation approximately twice that of the equilibrium value. Such results, and those from Figs 1, 2, indicate an anion exchange mechanism that can utilize a Cl gradient, but not a gradient of HCO3, as a driving force to move Ox2 across the apical membrane.
|
Effect of membrane potential on oxalate uptake
The possible membrane potential sensitivity of
Ox2/Cl exchange was examined by imposing a
valinomycin-induced K+ diffusion potential across the vesicular
wall and measuring the time course of 0.1 mmol l1
[14C]oxalate uptake. Transport was determined under both
inside-negative and inside-positive conditions and was compared with uptake in
short-circuited conditions (equal K+ across the membrane).
Fig. 4 shows that when vesicles
were incubated in media containing 100 mmol l1 K+
(no internal K+) and 50 µmol l1 valinomycin,
Ox2 uptake was stimulated above that with bilateral
K+. By contrast, when vesicles were preloaded with 100 mmol
l1 K+ and 50 µmol l1
valinomycin (no external K+), Ox2 uptake was
significantly inhibited. These data suggest that
Ox2/Cl exchange is enhanced by an
inside-positive membrane potential and inhibited by an inside-negative
vesicular interior, supporting the electrogenic nature of the exchange
process.
|
Specificity of the oxalate-exchange process
The questions of whether Ox2 would exchange with a wide
range of organic ions as transferable substrates was investigated by
trans-stimulation with either 5 mmol l1 oxalate, sulfate,
oxaloacetate, succinate, formate, -ketoglutarate or citrate
(Fig. 5). Only oxalate and
sulfate were able to stimulate 0.1 mmol l1
[14C]Ox2 uptake greater than the response
obtained in the presence of the nonexchangable anion gluconate. This
experiment indicates that in the lobster hepatopancreatic BBMV the antiporter
is relatively specific and will not accept similar dicarboxylic acids or the
tricarboxylic acid citrate as a substrate.
|
Effects of pH on oxalatechloride exchange
Oxalate uptake has been shown to be stimulated by proton (or hydroxyl)
gradients in the basolateral membrane (BLM) of the teleost fish renal
epithelium (Renfro and Pritchard,
1982). The possible proton (hydroxyl) gradient stimulation of
Ox2/Cl exchange in hepatopancreatic BBMV
was investigated in a series of experiments in which the pH of internal and
external media was varied and 0.1 mmol l1
[14C]Ox2 uptake was determined.
Fig. 6 shows that when the pH of the incubation media was maintained at 7.0 and the internal pH was varied from pH 5.0 to 8.0 there was an inequality of Ox2 transport into the BBMV preloaded with 100 mmol l1 Cl. The lowest internal pH of 5.0 corresponded to the slowest uptake of Ox2, whereas when the internal pH was greater (pHin=8.0) than the external pH, Ox2 uptake was enhanced over that of all other conditions. Alternatively, the observed phenomena may have been attributed to competition of internal hydroxyl concentration with Cl.
|
In a reciprocal experiment where the internal pH was kept constant at pH 7.0 and the pH of the incubation media was raised from 5.0 to 8.0, there was again a gradation of Ox2 uptake into vesicles preloaded with 100 mmol l1 Cl (Fig. 7). With a decrease in external pH there was a corresponding increase in Ox2 accumulation. These results indicate that an increase in external proton (or decrease in external hydroxyl) concentration can stimulate Ox2/Cl exchange.
|
In contrast to the previous two experiments, Fig. 8 shows the result of Ox2/Cl exchange at various bilateral pH conditions ranging from 5.0 to 8.0. The maximal uptake of Ox2 into BBMV occurred at pH 5.0 and decreased as pH was raised to 8.0. Results of this experiment indicate that it was not the proton (or hydroxyl) gradient that stimulated Ox2 uptake but rather the external absolute proton (hydroxyl) concentration.
|
36Cl/Ox2 exchange in BBMV
An experiment was designed to determine if
36Cl would exchange for internal
Ox2 and respond to a membrane potential in hepatopancreatic
BBMV. A portion of the vesicle preparation was preloaded with 10 mmol
l1 Ox2 (50 µmol l1
valinomycin) and incubated in media containing 10 mmol l1
Na36Cl, with or without 100 mmol l1 K-gluconate.
Another portion was preloaded with 100 mmol l1 KCl
(valinomycin) and incubated in media containing
[14C]Ox2, with or without 100 mmol
l1 K-gluconate. These conditions provided vesicles that were
either short-circuited or inside-negative.
Fig. 9A indicates that
[14C]Ox2 influx was inhibited by an
inside-negative vesicular membrane potential compared with short-circuited
vesicles. Fig. 9B also
indicates that 36Cl influx was enhanced by an
inside-negative vesicular membrane potential compared with the short-circuited
vesicular membrane potential condition. These data suggest that the
Ox2/Cl exchange occurred in a 1:1 ratio
and that excess negative charge of the internal Ox2 was
repelled by a negative intravesicular space.
|
Effect of inhibitors and competitors on oxalate influx
Potential anion exchange transport inhibitors were tested in the BBMV
preparation in order to further delineate the type of mechanism by which
Ox2 is being transported. The vesicles were preloaded with
100 mmol l1 TMA-gluconate, 100 mmol l1 KCl
and 50 µmol l1 valinomycin
(Fig. 10). The incubation
media consisted of 100 mmol l1 TMA-gluconate, 100 mmol
l1 K-gluconate and either 1 mmol l1 DIDS
(an anion exchange inhibitor), SITS (an anion exchange inhibitor), furosemide
(an Na+-symport inhibitor) or bumetanide (an Na+-symport
inhibitor). The 15-s uptake of [14C]Ox2 was
strongly inhibited by DIDS and SITS, while bumetanide and furosemide had
little, if any, inhibitory effect.
|
Kinetic characteristics of oxalate influx
Oxalate influx (7 s uptake) from incubation media to vesicular interior was
measured in BBMV preloaded with 100 mmol l1 TMA-Cl, 50 mmol
l1 K-gluconate and 50 µmol l1
valinomycin at pH 7.0 and external media of 100 mmol l1
TMA-gluconate, 50 mmol l1 K-gluconate and variable
Ox2 concentrations (0.120 mmol l1)
at pH 7.0. Fig. 11 shows that
Ox2 influx was a curvilinear function of external
Ox2 concentration. An influx relationship such as this can
be described as the sum of at least two independent processes acting
simultaneously: (1) a MichaelisMenten carrier mechanism illustrating
saturation kinetics and (2) a linear entry system with a rate proportional to
the external Ox2 concentration. These two processes
operating together can be described by the equation:
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A nonlinear, iterative, best-fit computer program was utilized to analyze the data in Fig. 11 by equation 1. Apparent transport parameters calculated in this manner are as follows: apparent Kt=0.20 mmol l1; apparent Jmax=1.03 nmol mg1 protein 7 s1 and P=0.31 nmol mg1 protein 7 s1 mmol l1.
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Discussion |
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In the present study, extravesicular Na+ or K+
gradients caused no intravesicular accumulation of Ox2
(Fig. 1), which rules out
cotransport of Ox2 with either of these two cations. An
outward vesicular gradient of HCO3 had no
accumulative effect on Ox2 into the BBMV, which negates an
Ox2/HCO3 antiporter as a
possible mechanism for Ox2 transport
(Fig. 1). Ruling out the
possibility that Ox2 transport across the brush-border
membrane occurs via a Cl channel, as has been shown
and speculated in other species (Freel et
al., 1998; Hatch et al.,
1984
,
1994
), we demonstrated that
9-AC, a known Cl channel blocker
(Freel et al., 1998
), had no
effect on the downhill energetic movement of Ox2 into the
BBMV of lobster hepatopancreatic epithelium
(Fig. 2).
The effect of valinomycin-induced K+ diffusion potentials on
Ox2/Cl exchange was investigated to
determine the effect of membrane potential on Ox2 transport
in the BBMV of lobster hepatopancreatic epithelium. Oxalate uptake was
measured under both inside-negative and inside-positive vesicular membrane
potential conditions and compared with short-circuited conditions.
Fig. 4 indicates that
Ox2/Cl exchange is stimulated by a
positive vesicular interior while inhibited by a negative vesicular interior.
These data suggest that there is an excess of negative charge transferred into
the vesicle during the exchange process. These data also support the idea that
the carrier can accommodate one oxalate ion and one chloride ion, which would
result in an electrogenic Ox2/Cl exchange,
as has been demonstrated for
SO42/Cl exchange in the same
epithelium (Gerencser et al.,
1995).
In the lobster hepatopancreas in vivo there is a pH gradient
maintained across the epithelium, with a lower pH in the lumen than in the
blood (Gibson and Barker,
1979). We therefore tested the effect of pH gradients on the
uptake of Ox2 into the BBMV.
Ox2/Cl exchange was diminished when the
internal pH was less than the external pH
(Fig. 6), and
Ox2 uptake was enhanced as the external pH was decreased
(constant internal pH), as shown in Fig.
7. This suggested that an extravesicular pH lower than internal pH
could stimulate Ox2/Cl (or
Ox2/OH) exchange. When the pH was held
constant on both sides of the BBMV (Fig.
8), there was increased uptake at lower pH, an effect similar to
that obtained in Fig. 6. This
result suggested that it was not the pH gradient but the lower external pH
(increased external protons) that stimulated
Ox2/Cl exchange.
This series of experiments suggests that a proton (or hydroxyl) gradient
does not act as a driving force during
Ox2/Cl exchange, nor could it stimulate
uptake alone, yet there were significant effects of varying pH on the
magnitude of Ox2/Cl exchange. All of the
experiments were short-circuited by the presence of valinomycin and equimolar
K+ across the BBMV so that H+-generated transmembrane
diffusion potentials would be unlikely to cause the results observed in Figs
6 and
7. Protons have been shown to
act as allosteric activators of the Na+/H+ exchanger in
rabbit renal BBMV (Aronson et al.,
1982) and Na+/SO42
cotransport in rabbit ileum BBMV (Ahearn
and Murer, 1984
). Similarly, the results observed in Figs
6,
7,
8 would support the idea of
external protons having a modifier role for stimulating the
Ox2/Cl exchanger.
The existence of internal pH-sensitive regulatory sites for the
Cl/HCO3 exchanger has been
demonstrated on the rabbit ileal brush-border membrane using membrane vesicles
(Mugharbil et al., 1990), in
isolated cell preparations of lymphocytes
(Mason et al., 1989
) and in
Vero cells (Olsnes et al.,
1986
). An external pH-sensitive regulatory site on the
Ox2/Cl exchanger in the hepatopancreatic
brush-border membrane would be physiologically important due to the
2Na+/H+ exchanger also present in the membrane
(Ahearn et al., 1990
). The
2Na+/H+ exchanger operates during luminal acidification
following ingestion of a meal and would provide a stimulus for enhanced
Ox2/Cl exchange. When the
2Na+/H+ exchanger is operating there would be an
increase in the proton concentration in the hepatopancreatic lumen and a
corresponding decrease of protons in the cytoplasm. This would tend to enhance
the Ox2/Cl exchanger due to modification
at an external site, as demonstrated in
Fig. 8.
The influx of [14C]oxalate in hepatopancreatic BBMV occurred by
at least one carrier-mediated mechanism exhibiting MichaelisMenten
kinetics and a second process that may be simple diffusion
(Fig. 11). The apparent
affinity constant (Kt) for oxalate binding to the vesicle
exterior was 0.20 mmol l1, and the maximal transport
velocity (Jmax) was 1.03 nmol mg1
protein 7 s1. The apparent diffusional component had a rate
of 0.31 nmol mg1 protein 7 s1 mmol
l1. These kinetic constants are similar to those obtained
for oxalate transport across the BLMV of lobster hepatopancreas (Gerencser et
al., 1995,
2000
).
The Ox2/Cl exchanger was significantly
(P<0.05) inhibited by the disulfonic stilbenes DIDS and SITS, as
shown in Fig. 10. Oxalate
transport has been shown to be inhibited by SITS and DIDS in other epithelial
preparations (Pritchard, 1987;
Renfro et al., 1987
;
Renfro and Pritchard, 1983
).
Furosemide and bumetanide were not effective as inhibitors in the present
study (Fig. 10). The strong
inhibition by DIDS and SITS provides further evidence for the presence of an
anion exchanger in hepatopancreatic BBMV since both SITS and DIDS are
relatively specific inhibitors for anion exchange processes
(Renfro and Pritchard, 1983
;
Shiu-Ming and Aronson, 1988
;
Talor et al., 1987
).
Under the assumption that exchange mechanisms such as this can operate in
both directions, it should be possible to measure the uptake of
36Cl into vesicles in exchange for internal
Ox2. If the exchange operated at a 1:1 ratio it would be
expected to react to a membrane potential. It was observed that
36Cl influx did respond to an inside-negative
potential (Fig. 9) by an
increased uptake during its incubation. With this arrangement there would be a
secretion of Ox2 from the vesicular interior in exchange for
luminal Cl that is further driven by the inside negative
potential that is characteristic of epithelial cells
(Gerencser, 1985). This
secretion of Ox2 would lead to its excretion unless it were
recycled by the same antiporter. This phenomenon would support the work of
some investigators who have postulated that the crustacean gut can provide an
excretory function in the elimination of certain solutes
(Dall, 1970
;
Gifford, 1962
).
The brush-border membrane Ox2/Cl
exchanger described in the present investigation cannot provide definitive
evidence for absorption or secretion for either Ox2 or
Cl. However, speculatively, this mechanism could provide a
cellular means for ridding the cell of Ox2 and/or taking up
Cl for metabolic functions. This transport would allow for
the elimination of Ox2 from the lobster hepatopancreatic
cells as a means of anion regulation. Oxalate binds divalent cations, such as
Ca2+, and precipitates as calcium oxalate, which could be
deleterious for cellular survival (Binder,
1974; Dobbins and Binder,
1977
; Earnest,
1974
). However, a more realistic function of Ox2
may be that of storing Ca2+ as calcium oxalate in hepatopancreatic
lysosomes and mitochondria for the use of Ca2+ during the molt
cycle, as has been previously reported (Gerencser et al.,
1996
,
2000
). The anion antiporter
could then be used for ridding the cell of excessive Ox2 as
a cytoprotective mechanism after completion of the molting cycle.
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Acknowledgments |
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