Departments of 1 Pediatrics and 2 Internal Medicine, The University of Texas Southwestern Medical Center, Dallas, Texas 75235-9063
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ABSTRACT |
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We have recently
demonstrated that the rates of both active and passive proximal
straight tubule (PST) NaCl transport in neonatal rabbits were less than
in adults. In this segment NaCl entry across the apical membrane is via
parallel Na+/H+ and
Cl/OH
exchangers, which increases
in activity with maturation. The present in vitro microperfusion study
examined whether thyroid hormone plays a role in the maturational
increase in PST NaCl transport. Neonatal and adult PST were perfused
with a high-chloride-low bicarbonate solution without organic solutes,
simulating late proximal tubule fluid. Thyroid hormone-treated neonates
had a higher rate of PST total and passive NaCl transport. In 8-wk-old animals that were hypothyroid since birth, the maturational increase in
total and passive NaCl transport was prevented. Thyroid treatment for 4 days in hypothyroid 8-wk-old rabbits increased the rate of both total
and passive NaCl transport. The maturational increases in both
Na+/H+ and
Cl
/OH
exchange activities were
blunted in 8-wk-old hypothyroid animals and increased to control levels
with thyroid treatment. This study demonstrates that thyroid hormone is
a factor responsible for the maturational increase in both active and
passive PST NaCl transport.
sodium/hydrogen antiporter; chloride/base exchanger; kidney development; passive transport
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INTRODUCTION |
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THE PROXIMAL TUBULE REABSORBS ~60% of the filtered
NaCl. The preferential reabsorption of organic solutes and bicarbonate by the early proximal tubule leaves the luminal fluid with a higher chloride and lower bicarbonate concentration than the peritubular plasma (19, 24). In the proximal tubule approximately one-half of NaCl
transport is passive and paracellular (4, 25). The parallel operation
of the apical membrane Na+/H+ antiporter and
Cl/base exchangers mediate NaCl entry into the
proximal tubule cell (1, 18, 25).
We have recently examined the postnatal developmental changes in proximal straight tubule (PST) NaCl transport (25). In rabbit PST perfused with a high chloride-low bicarbonate solution simulating late proximal tubular fluid and bathed in a serum-like albumin solution, the rate of volume absorption, a reflection of both active and passive NaCl transport, was over twofold higher in the adult than neonatal segment (25). NaCl transport was inhibited by 50% by bath ouabain in adult tubules and totally inhibited in the neonatal segment. Thus the rates of active and passive NaCl transport were higher in the adult tubule than were those in the neonate (25).
In the rabbit PST there was a fivefold increase in the
Na+/H+ antiporter activity during postnatal
development (25). Cl/base exchange in neonatal and
adult PST was not affected by cyanide and acetazolamide,
CO2 and bicarbonate, or the addition of formate, consistent
with Cl
/OH
exchange (18, 25).
There was a sixfold maturational increase in apical membrane PST
Cl
/OH
exchange activity (25).
The factors that produce the profound postnatal changes in active and passive proximal tubular transport remain to be elucidated. Both serum glucocorticoid and thyroid hormone levels are lower in neonates than in adults and increase at about the time of weaning (5, 14, 16, 26, 28). The purpose of the present study was to examine whether thyroid hormone affects neonatal PST active and passive NaCl transport. Our findings in this segment are consistent with an important role for thyroid hormone in the postnatal maturation of both active and passive NaCl transport. Most importantly, this study demonstrates that the postnatal increase in thyroid hormone can affect the permeability properties of the paracellular pathway.
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METHODS |
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Animal preparation. Superficial PST from neonatal (18 ± 1 days) and adult New Zealand White rabbits (55 ± 1 days) were studied. Both male and female rabbits were used in these studies. Hyperthyroidism was induced by daily subcutaneous injection of 10 µg/100 g 3,5,3'-L-triiodothyronine (T3; Sigma Chemical, St. Louis, MO) for 3 days and in the morning 2 h before death. Control neonates were injected with vehicle.
Hypothyroidism was induced by adding 0.1% propylthiouracil (PTU; Sigma Chemical, St. Louis, MO) to the drinking water of pregnant rabbits from the 26th day of gestation (term gestation ~31 days) until the time of experiment at ~8 wk of age (6). Untreated age-matched rabbits served as control adults. Thyroid treatment was administered to some hypothyroid animals by daily subcutaneous injection of T3 (10 µg/100 g body wt) for 3 days and in the morning 2 h before death.In vitro microperfusion. Isolated segments of neonatal and adult superficial PST (S2 segments) were perfused by using concentric glass pipettes as previously described (25). Briefly, tubules were dissected in Hanks' balanced salt solution containing (in mM) 137 NaCl, 5 KCl, 0.8 MgSO4, 0.33 Na2HPO4, 0.44 KH2PO4, 1 MgCl2, 10 Tris, 0.25 CaCl2, 2 glutamine, and 2 lactate at 4°C. Tubules were transferred to a 1.2-ml temperature-controlled bath for flux studies and a 0.2-ml chamber, in which the bathing solution was preheated to 38°C for intracellular pH (pHi) studies.
In vitro microperfusion flux studies. Tubules were perfused at ~10 nl/min with a high-chloride solution simulating late proximal tubular fluid containing (in mM) 146 NaCl, 5 NaHCO3, 5 KCl, 2.3 Na2HPO4, 1 CaCl2, 1 MgCl2, and 0.1 formate. Formate was added because it has been shown to stimulate NaCl transport in this segment (18). The bathing solution was a serum-like albumin solution containing (in mM) 115 NaCl, 25 NaHCO3, 2.3 Na2HPO4, 10 Na acetate, 1.8 mM CaCl2, 1 MgSO4, 5 KCl, 8.3 glucose, 5 alanine, 1 butyrate, 1 glutamine, and 6 g/dl bovine serum albumin. The osmolality of these solutions was adjusted to 295 mosmol/kgH2O. The pH and osmolality of the bathing solution were maintained constant by continuously changing the bath at a rate of 0.5 ml/min in flux studies.
Net volume absorption (JV, in nl · mmMeasurement of pHi.
The solutions used in these experiments are shown in Table
1. The fluorescent dye
2',7'-bis(carboxyethyl)-5(6)-carboxyfluorescein (BCECF) was
used to measure pHi as described previously (3, 18, 25).
pHi was measured by using a Nikon inverted epifluorescent microscope attached to a PTI Ratiomaster at a rate of 30 measurements/s. A variable diaphragm was placed over the area to be
measured. To calculate pH from the ratio of fluorescence
(F500/F450), a nigericin calibration curve was
performed as previously described (3, 25). There was no difference in
the calibration curves of adult and neonatal PST.
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Statistics. Data are expressed as means ± SE. Analysis of variance and the Student's t-test for paired and unpaired data were used to determine statistical significance.
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RESULTS |
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Effect of thyroid hormone status in neonatal and adult animals.
The mean weights of PTU water-treated adult animals and adult control
animals were 1.3 ± 0.1 and 1.8 ± 0.1 kg, respectively (P < 0.05). Similarly, the mean weight of the kidney in the PTU water-treated adults (6.4 ± 0.3 g) was significantly lower than that
in adult control animals (7.8 ± 0.4 g, P < 0.05). As shown in Table 2, serum T3 levels in
the PTU water-treated animals were comparable to neonates and both were
~50% that of adult control animals. However, the serum
corticosterone level in the PTU water-treated group was similar to that
in the adult control group, demonstrating that these animals were not
glucocorticoid deficient. Thyroid administration given to neonates and
PTU-treated adults resulted in levels >800 ng/dl when assayed at the
time of death, 2 h after thyroid hormone administration.
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Effect of thyroid hormone status on PST volume.
The mean tubular volume of PST in the control and thyroid-treated
neonates were 440.0 ± 14.4 × 1012 and 476.9 ± 14.3 × 10
12 l/mm.The mean tubular
volume of PST from hypothyroid and control adult animals and tubules
from hypothyroid animals that received thyroid treatment were 845.1 ± 37.3 × 10
12, 1,075 ± 47.9 × 10
12, and 1,042 ± 31.6 × 10
12 l/mm, respectively. The
tubular volume of the PST from the hypothyroid group was less than the
control and thyroid replacement group (P < 0.01).
Effect of thyroid hormone on neonatal PST NaCl transport.
In the first series of experiments PST were perfused with a
high-chloride low-bicarbonate solution without organic solutes, simulating late proximal tubular fluid. Tubules from control and thyroid-treated neonates (10 µg/100 g body wt for 3 days and in the
morning 2 h before death) were compared as shown in Fig.
1. As can be seen, PST from thyroid-treated
neonates had a higher rate of volume absorption than that of
vehicle-treated control neonates. Ouabain
(105 M) was then added to the bathing
solution to inhibit active transport. The rate of passive transport was
greater in PST from the thyroid-treated than that from vehicle-treated
control neonates. These data are consistent with thyroid hormone
causing acceleration of maturation of PST active and passive NaCl
transport.
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Effect of thyroid hormone on neonatal apical
Na+/H+
and Cl/OH
exchange activity.
We first examined the apical Na+/H+ antiporter
activity in PST perfused with solution D and bathed with
solution C. Both were HEPES-buffered solutions without sodium
and chloride. We excluded chloride from all the solutions to prevent
Cl
/base exchange from attenuating any
pHi changes. In the experimental period, luminal sodium was
added (solution E) and dpHi/dt and JH were measured. As shown in Fig.
2, Na+/H+
antiporter activity in thyroid hormone-treated neonates was
significantly greater than that in the vehicle-treated control
neonates.
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Effect of hypothyroidism and thyroid treatment on NaCl transport in
adult PST.
If the postnatal rise in thyroid hormone was responsible for the
maturational increase in NaCl transport, then the developmental increase in NaCl transport should be prevented in animals made hypothyroid from birth. The rates of PST volume absorption from a
high-chloride perfusate were the same in these 8-wk-old rabbits as we
have measured in adult rabbits of this age and older (25). As is shown
in Fig. 4, hypothyroid animals had a lower
rate of total and passive transport than age-matched controls. The
rates of volume absorption in PST of hypothyroid 8-wk-old rabbits were comparable to the rates in neonatal rabbit PST. In hypothyroid rabbits
that received thyroid replacement, the rates of total and passive
volume absorption were comparable to controls and greater than the
hypothyroid group.
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Effect of hypothyroidism and thyroid treatment on adult PST apical
Na+/H+
and Cl/OH
exchange activities.
To further substantiate the role of thyroid hormone in maturation of
apical Na+/H+ antiporter activity, we examined
PST from hypothyroid animals. As shown in Fig.
5, JH in PST from
hypothyroid adult animals was significantly lower than that from the
adult control group. When these hypothyroid adult animals were treated
with thyroid hormone, JH increased to that in the
adult control group, confirming an important role of thyroid hormone in
the maturation of apical Na+/H+
antiporter activity in the neonatal PST.
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DISCUSSION |
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The present in vitro microperfusion study examined the effect of
thyroid hormone on the maturation of PST NaCl transport. Administration
of thyroid hormone to neonatal rabbits resulted in an increase in
volume absorption in tubules perfused with a high chloride solution
simulating late proximal tubular fluid and when active transport was
inhibited with bath ouabain. Thyroid hormone also increased PST
Na+/H+ antiporter and
Cl/OH
exchange activity.
Hypothyroidism blunted the maturational increase in total and passive
NaCl transport as well as the developmental increase in
Na+/H+ antiporter and
Cl
/OH
exchanger activity in
rabbit PST. These were all reversed with thyroid treatment.
Several studies have examined the effect of hypothyroidism on renal function in adult animals. Hypothyroid rats had a lower glomerular filtration rate and renal blood flow (22), and a higher fractional excretion of sodium than euthyroid control rats (15, 22). Lower rates of proximal tubule sodium transport have been implicated to explain the difference in renal sodium handling compared with euthyroid controls (11, 12, 22). In vivo rat micropuncture and shrinking droplet studies demonstrated a lower rate of proximal tubule transport compared with control animals (11, 12, 22). Administration of thyroid hormone to hypothyroid rats restored proximal tubule transport to control levels (11, 12). Hypothyroid rats and rabbits had a reduction in proximal tubule Na+-K+-ATPase activity that was restored by administration of thyroid hormone (2, 10, 13). However, administration of thyroid hormone to hypothyroid rats resulted in an increase in the rate of proximal tubule volume absorption before the time when a change in Na+-K+-ATPase activity was measured (10-12). These data suggest that the effect of thyroid hormone was not entirely due to its effect on the Na+-K+-ATPase, a result in concordance with this and our previous studies (5, 9).
In this study thyroid hormone resulted in an increase in Na+/H+ antiporter activity. This is in agreement with previous studies in neonates and adults showing an effect of thyroid hormone on brush-border membrane vesicle Na+/H+ antiporter activity (5, 17). The effect of thyroid hormone on Na+/H+ antiporter could be indirect and solely mediated by alterations in renal hemodynamics or other neural or hormonal changes. Although a hemodynamic effect of thyroid hormone on proximal tubular transport may be a contributing factor, a direct effect of thyroid hormone on proximal tubular cells to increase Na+/H+ antiporter activity has been described (9, 29). Thyroid hormone has been shown to increase the maximum velocity of the Na+/H+ antiporter in opossum kidney (OK) cells (28). We have recently found that thyroid hormone increases Na+/H+ antiporter by increasing NHE3 mRNA and protein abundance in OK cells in vitro (9). Thyroid hormone had no effect on NHE3 mRNA or protein stability but activated the promotor to increase NHE3 gene transcription (9).
Serum thyroid hormone levels increase during postnatal maturation (5, 26, 28), which may be of importance in renal development. We have recently examined the effect of thyroid hormone on neonatal rat Na+/H+ antiporter (5). Neonatal rats made hypothyroid by the addition of PTU to their drinking water had a lower rate of renal cortical brush-border membrane Na+/H+ antiporter activity. Renal cortical NHE3 protein abundance was less than one-half of that of euthyroid neonates, however, NHE3 mRNA abundance was comparable. Hyperthyroid neonates had higher rates of brush-border membrane Na+/H+ antiporter activity, NHE3 mRNA, and protein abundance than euthyroid control animals. Although these data suggest a possible role for thyroid hormone in the postnatal maturational increase in Na+/H+ antiporter in the rat, the effect of thyroid hormone on cortical Na+/H+ antiporter activity was small. There was only a 10% decrease in brush-border membrane Na+/H+ antiporter activity in hypothyroid rats and a 10% increase in antiporter activity in rats given thyroid hormone. Thus there may be a difference in the importance of thyroid hormone in promoting the maturation of proximal tubule Na+/H+ antiporter in the rabbit and rat.
Perhaps the most important finding in this study is the effect of
thyroid hormone on the passive NaCl transport. We had previously found
that neonates have lower rates of both active and passive transport
when perfused with a high-chloride solution simulating late proximal
tubular fluid compared with adult tubules (25). Thyroid-treated
neonates had a higher rate of volume absorption from a high-chloride
perfusate compared with control tubules in the presence and absence of
bath ouabain. In addition, the maturational changes in transport from a
high-chloride perfusate in the presence and absence of bath ouabain
were prevented in hypothyroid rabbits, which were studied at ~8 wk of
age. The maturational increase in the rates of PST
Na+/H+ antiporter and
Cl/OH
exchange activities were
also blunted when animals were made hypothyroid.
In addition to the effect on passive and active volume absorption, thyroid hormone affected the transepithelial potential difference. In adult proximal tubules perfused with a late proximal tubular fluid and bathed in a serum-like solution, the transepithelial potential difference is lumen positive due to the anion gradients across the paracellular pathway and the greater permeability of the proximal tubule to chloride ions (4). Inhibition of active transport does not affect the potential difference (4). We found that the potential difference was significantly lower in neonates than adults, consistent with a maturational change in paracellular permeability. Thyroid hormone-treated neonatal PST have a significant increase in the transepithelial potential difference, whereas the maturational increase in potential difference was not seen in hypothyroid adult proximal tubules. Thyroid replacement resulted in an increase in the transepithelial potential difference in 8-wk-old adult rabbits.
Thyroid hormone was shown 35 years ago to affect passive paracellular anion permeability in isolated toad bladders (20, 21). After thyroxine treatment, there was an increase in short-circuit current but no change in electrical potential, consistent with a concomitant increase in paracellular permeability. Addition of thyroxine to toad bladders increased chloride and phosphate permeability. These data are consistent with the present findings, which find a potential role for thyroid hormone in the maturational change in paracellular pathway. Thyroid hormone does not cause a generalized increase in paracellular permeability in epithelia as this group subsequently demonstrated that thyroxine treatment in the rat small intestine decreased passive phosphate and calcium transport (23).
Thyroid hormone has been implicated as a factor in other aspects of renal development. There is evidence that thyroid hormone is a factor in the maturational increase in several proximal tubule mitochondrial oxidative enzymes (27). The growth of the kidney is impaired in hypothyroid rats (8). Importantly, the proximal tubule is shorter in hypothyroid rats (7). Thyroid-treated neonatal PST were of comparable volume per millimeter as that of control. Eight-week-old hypothyroid rabbits had a significant reduction in tubular volume compared with control 8-wk PST, which increased to the control tubular volume with thyroid treatment.
In summary, this study confirms that there is a postnatal rise in both
active and passive NaCl transport in the PST. Administration of thyroid
hormone to neonates resulted in an increase in volume reabsorption from
a high-chloride perfusate. The increase in active NaCl transport was
mediated in part by an increase in apical membrane Cl/OH
and
Na+/H+ exchange activity as well as by changes
in passive NaCl transport. The postnatal maturational increases in both
active and passive NaCl transport were prevented and the maturational
increases in Cl
/OH
and
Na+/H+ exchange activity were blunted in
hypothyroid rabbits. This study is consistent with an important role
for thyroid hormone in postnatal maturation of PST NaCl transport.
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ACKNOWLEDGEMENTS |
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We are grateful for the secretarial assistance of Janell McQuinn.
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FOOTNOTES |
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This work was supported by National Institute of Diabetes and Digestive and Kidney Disease Grant DK-41612 (to M. Baum).
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. §1734 solely to indicate this fact.
1 All proton fluxes are presented as absolute values and are expressed as JH in picomoles per millimeter per minute.
Address for reprint requests and other correspondence: M. Baum, Dept. of Pediatrics, Univ. of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75235-9063 (E-mail: Mbaum{at}mednet.swmed.edu).
Received 15 July 1999; accepted in final form 3 November 1999.
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