Water transport in neonatal and adult rabbit proximal
tubules
Raymond
Quigley1 and
Michel
Baum1,2
Departments of 1 Pediatrics and
2 Internal Medicine, University of Texas
Southwestern Medical Center at Dallas, Dallas, Texas 75390-9063
 |
ABSTRACT |
We have recently demonstrated that
although the osmotic water permeability (Pf) of
neonatal proximal tubules is higher than that of adult tubules, the
Pf of brush-border and basolateral membrane
vesicles from neonatal rabbits is lower than that of adults. The
present study examined developmental changes in the water transport
characteristics of proximal convoluted tubules (PCTs) in neonatal
(9-16 days old) and adult rabbits to determine whether the
intracellular compartment or paracellular pathway is responsible for
the maturational difference in transepithelial water transport. The
permeability of n-butanol was higher in the neonatal PCT
than the adult PCT at all temperatures examined, whereas the
diffusional water permeability was identical. Increasing the osmotic
gradient increased volume absorption in both the neonatal and the adult
PCT to the same degree. The Pf was not different between the neonatal and the adult PCT at any osmotic gradient studied.
To assess solvent drag as a measure of the paracellular transport of
water, the effect of the osmotic gradient on mannitol and chloride
transport were measured. There was no change in chloride or mannitol
transport with the increased osmotic gradient in either group,
indicating that there was no detectable paracellular water movement. In
addition, the mannitol permeability of the neonatal PCT was found to be
lower than that of the adult PCT with the isotonic bath (8.97 ± 4.01 vs. 40.49 ± 13.89 µm/s, P < 0.05). Thus
the intracellular compartment of the neonatal PCT has a lower resistance for water transport than the adult PCT and is responsible for the higher than expected Pf in the neonatal PCT.
proximal convoluted tubules; development; butanol permeability; diffusional water permeability; in vitro microperfusion
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INTRODUCTION |
WATER TRANSPORT ACROSS
CELLULAR membranes is a fundamental biological process that
occurs either by diffusion through the lipid bilayer or by movement
through specific water channels (aquaporins) (3, 11, 28).
There is also evidence that water can traverse across other membrane
transport proteins (12). Transport of water through the
lipid bilayer is characterized by a high activation energy (>9
kcal · mol
1 · degree
1) and
resistance to inhibition by mercury, whereas water movement through
aquaporins is characterized by a low activation energy (~4-5
kcal · mol
1 · degree
1) and
is inhibited by mercury for most aquaporin isoforms (28).
The proximal tubule of the mammalian kidney is responsible for
reabsorbing the bulk of the glomerular ultrafiltrate (24). This process is nearly isosmotic because the proximal tubule has a very
high water permeability, which is thought to be due to the constitutive
presence of the water channel aquaporin-1 (AQP1). The
importance of AQP1 to water transport by this nephron segment is
evidenced by the fact that mice lacking AQP1 have a much lower rate of
fluid transport than wild-type mice (25). Previous studies in the adult kidney have also indicated that most of the water transport through the proximal tubule is transcellular, not
paracellular, and that the intracellular compartment may be responsible
for more than one-half of the resistance to water flow (4,
16).
During renal development, there is a maturational increase in
proximal tubule AQP1 expression (6, 21, 22). However, we
found that the osmotic water permeability (Pf)
in the neonatal rabbit proximal tubule was actually equal to or greater
than that of the adult proximal tubule (20). Further
examination of water transport in this epithelium demonstrated that the
apical and basolateral membranes of the neonatal tubules had a lower
Pf and lower expression of AQP1 than the adult
membranes (21, 22). Thus the reason for the higher
Pf in the neonatal tubules was unclear. This
must be due to either a higher fraction of water traversing the
paracellular pathway in the neonatal tubules than the adult tubules or
the intracellular compartment of the neonatal tubules offering less
resistance to the movement of water than the adult tubules. Because the
apical and basolateral membrane water permeabilities and surface areas
of the adult and neonatal proximal tubules are known (10),
examining and modeling the developmental changes in water transport
could facilitate our understanding of neonatal epithelial water transport.
The purpose of the present study was to determine whether there are
differences between the neonatal and adult proximal tubule intracellular compartments or paracellular pathways that explain the
high neonatal transepithelial water permeability despite the low
Pf of the apical and basolateral membranes.
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METHODS |
Juxtamedullary proximal convoluted tubules (PCTs) from
adult and neonatal (9-16 days old) New Zealand White rabbits were
perfused in vitro as previously described (7, 18).
Briefly, PCTs were dissected in cooled (4°C) modified Hanks'
solution containing (in mM) 137 NaCl, 5 KCl, 0.8 MgSO4,
0.33 Na2HPO4, 0.44 KH2PO4, 1 MgCl2, 10 Tris · HCl, 0.25 CaCl2, 2 glutamine, and 2 L-lactate. This solution was bubbled with 100%
O2 and had a pH of 7.4. Tubules were then transferred to a
1.2-ml thermostatically controlled bathing chamber and perfused with
concentric glass pipettes. The perfusion solution simulated late
proximal tubule fluid and contained in (mM) 140 NaCl, 5 KCl, 4 Na2HPO4, 1 CaCl2, 1 MgCl2, and 1 Na butyrate (20). The bathing
solution was identical, except it also contained 6 g/dl of albumin. All
solutions were bubbled with 100% O2 and had a pH of 7.4. Osmolalities of the perfusion and bathing solutions were adjusted to
295 mosmol/kgH2O by the addition of water or NaCl. The
bathing solution was exchanged at a rate of 0.5 ml/min to keep the
osmolality and pH constant. For determining the effect of increased
osmolality in the bath, raffinose was added to the bathing solution
to increase the osmolality.
Volume absorption (Jv; in
nl · min
1 · mm
1) was
measured as the difference between the perfusion and collection rates
and normalized per millimeter of tubule length. These experiments were
performed at 37°C. The collection rate was determined by timed
collections by using a constant-volume pipette. Exhaustively dialyzed
methoxy-[3H]inulin (New England Nuclear) was added to the
perfusate at a concentration of 50 µCi/ml so that the perfusion rate
could be calculated. The perfusion rate was between 25 and 30 nl/min
for these experiments.
The Pf was calculated from the following
equation (1)
where
0 is the perfusion rate;
C0, CL, and Cb are the
osmolalities of the perfusate, collected fluid, and bathing solution,
respectively, and L is the tubule length; A is
the tubule inner surface area; and
w is the molar volume of water.
CL is determined from the relationship
0C0 =
LCL, where
L is the collection rate measured by
using a constant-volume pipette.
[14C]mannitol was added to the perfusate to
measure the effect of bath osmolality on the flux of mannitol. The flux
of mannitol was calculated as
and the permeability to mannitol was calculated from the
following equation (16, 19)
where
0 and
L
represent the perfusion and collection rates, respectively,
C
and C
represent the
14C counts in the perfusate and collected fluid,
respectively, and C0 represents the mannitol concentration
in the perfusate. Mannitol permeability was normalized to the inner
surface area of the tubule by using the inner diameter. The tubule
length and inner diameter were measured with an eyepiece micrometer.
The transport of chloride was measured by determining the
chloride concentration in the perfusate and collected fluid by using the Ramsey technique as previously described by our laboratory (23, 26). The absorption of chloride was calculated as
where C0 and CL represent the
chloride concentration in the perfusate and collected fluid, respectively.
In a separate set of experiments, n-butanol
permeability was measured at 40, 32, 25, and 20°C by adding
14C-labeled n-butanol to the perfusate at a
concentration of 15-20 µCi/ml. The diffusional water
permeability (PDW) of the tubule was measured by
adding 3H2O to the perfusate at a concentration
of 50 µCi/ml. These permeabilities were calculated by the following
equation
where PX represents the diffusional
permeability of butanol or water, and X0 and
XL represent the counts for butanol or water in
the perfusate and collected fluid, respectively.
All data are expressed as means ± SE. Comparisons were
made by using unpaired analysis (Student's t-test and
linear regression where appropriate), and significance was taken to be
P < 0.05. Calculations were made with SigmaStat
software (Jandell Scientific).
 |
RESULTS |
Pf.
Figure 1 shows the effect of increasing
bath osmolality on the rate of adult and neonatal PCT volume
absorption. As can be seen, the volume absorption rate increased with
an increase in bath osmolality for both the adult (n = 33) and the neonatal tubules (n = 31). There was no
difference between the rates of volume absorption in the adult and
neonatal tubules.

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Fig. 1.
Osmotic gradient dependence of neonatal and adult
proximal convoluted tubule (PCT) volume absorption. Tubules were
perfused with a solution adjusted to 300 mosmol/kgH2O.
Bathing solution was identical except for 6 g/dl of albumin and
raffinose to increase the osmolality. As can be seen, there was no
difference in volume absorption between the adult and neonatal
tubules.
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The Pf of adult and neonatal tubules is shown in
Fig. 2. At each osmotic concentration
gradient examined, there was no difference between the adult
(n = 18) and neonatal (n = 20) PCT
Pf.

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Fig. 2.
Osmotic gradient dependence of osmotic water permeability
(Pf) in adult and neonatal PCT. Data from Fig. 1
were used to calculate the Pf. There was no
significant difference between the Pf of the
adult and neonatal tubules at any bath osmolality.
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n-Butanol permeability and PDW.
To assess the contribution of the intracellular compartment to the
movement of water, the diffusive permeability to n-butanol and water were measured simultaneously. n-Butanol is a
lipophilic substance that has been previously used to examine the
contribution of the intracellular compartment to the resistance to
water flow (4). As seen in Fig.
3, the permeability of the neonatal
tubules (n = 7) to n-butanol was higher than
that of the adult tubules (n = 6) at all temperatures
examined except for 20°C. Thus the resistance of the intracellular
compartment to the movement of water is lower in the neonatal tubules
than the adult tubules at physiological temperatures.

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Fig. 3.
Neonatal and adult PCT butanol permeability
(PDNB). Tubules were perfused with a solution
containing 14C-labeled n-butanol and
3H2O. PDNB of the
neonatal tubules was higher than that of the adult tubules at each
temperature except for 20°C.
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The PDW of adult and neonatal tubules were the
same at each temperature studied (Fig.
4). This is identical to our previous study in the development of proximal tubule water transport
(20). We then applied the analysis of Berry
(4) to examine the PDW of the
membrane component. The PDW of the membrane
[PDW(membrane)] was calculated from the
following equation
where DNB and DW are the free diffusion
constants of n-butanol and water, respectively (15,
29).

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Fig. 4.
Temperature dependence of neonatal and adult PCT
diffusional water permeability (PDW). There was
no difference between the adult and neonatal tubule
PDW at any temperature.
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The PDW(membrane) of neonatal tubules
(n = 7) was lower than that of the adult PCTs
(n = 6), as shown in the Arrhenius plot in Fig.
5. In addition, the slope of the
Arrhenius plot was higher for the neonatal tubules than for the adult
tubules. Thus the activation energy for
PDW(membrane) was higher in the neonatal tubules
than in the adult membranes (5.92 ± 0.77 vs. 3.02 ± 1.08 kcal · degree
1 · mol
1,
P < 0.05). These findings are in agreement with our
previous findings of a lower Pf in neonatal than
adult brush-border and basolateral membranes (21, 22).

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Fig. 5.
PDW of the membrane
[PDW(membrane)]. PDW of
the tubule membrane was calculated from the simultaneous measurement of
PDW and PDNB.
PDW(membrane) of the neonatal tubule was lower
than that of the adult at all temperatures studied. Slope of the
Arrhenius plot is also greater for the neonatal tubules, indicating
that the neonatal membranes have a higher activation energy for water
transport than the adult.
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Paracellular pathway.
We next examined the paracellular pathway to determine whether it is a
contributing factor in explaining the high transcellular Pf in the neonatal tubules despite the low
PDW(membrane). Paracellular transport of
water is difficult to measure directly (27). One approach
is to induce osmotic water flow with an impermeable solute and measure
the solvent drag of small particles. The assumption is that if water
moves between the cells, it will carry small particles with it
(27). We measured the flux of mannitol as a nonionic
solute and chloride as a small ion and determined their flux in
response to an increasing osmotic gradient. As shown in Fig.
6, the transport of mannitol was the same
in both adult (n = 33) and neonatal (n = 31) tubules except for the isotonic bath (300 mosmol/kgH2O). In both the adult and the neonatal tubules, the transport of mannitol did not increase as the bath osmolality was
increased. This would argue against solvent drag. The fact that the
adult transport rate of mannitol was higher than the neonatal transport
rate with the isotonic bath indicated that the mannitol permeability in
the neonatal tubule was lower than that of the adult (Fig.
7).

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Fig. 6.
Osmotic gradient dependence of mannitol transport
(Jmannitol). Tubules were perfused with a
perfusion solution as in Fig. 1 containing [14C]mannitol.
There was no change in Jmannitol as the bath
osmolality was increased.
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Fig. 7.
Developmental changes in mannitol permeability
(Pmannitol). Tubules were perfused with
[14C]mannitol to measure the permeability of mannitol
with an isosmotic bath. Pmannitol was
significantly lower in the neonatal PCT compared with the adult PCT.
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We also examined the osmotic dependence of chloride transport to
further determine characteristics of the paracellular pathway. As seen
in Fig. 8, there was no difference in the
rate of chloride transport between the adult (n = 26)
and neonatal (n = 25) tubules. There was also very
little change in the chloride transport rate as the bath osmolality
increased, suggesting that there is almost no solvent drag. This is
similar to previous studies in adult proximal tubules
(13).

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Fig. 8.
Osmotic gradient dependence of chloride transport.
Tubules were perfused as in Fig. 1, and chloride transport was
measured. There was a small decrease in chloride transport in the
neonatal tubules at the highest osmotic gradient examined.
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Cell height.
The height of the proximal tubule cells was determined by measuring the
inner and outer diameters of the tubules with an eyepiece reticle. The
neonatal proximal tubule cell height (8.6 ± 0.5 µm) was
significantly smaller than the adult cell height (11.0 ± 0.3 µm, P < 0.005). These values are very similar to
previously reported values (2, 10). The ratio of the adult
to neonatal cell heights (1.27) is identical to the ratio of the
neonatal to adult n-butanol permeabilities at 25°C (1.26).
This suggests that the primary determinant for the diffusion of butanol
is the cell interior and is directly proportional to the path length
through the cell.
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DISCUSSION |
The proximal tubule reabsorbs the bulk of the glomerular
ultrafiltrate by a process that is nearly isosmotic because of its high
transepithelial Pf (24).
Hypotonicity of the luminal fluid due to active transport of solute
from the lumen is thought to be the driving force for this water
movement (24). Water can move through the epithelium via
the transcellular pathway, which is made up of the apical membrane, the
cellular compartment, and the basolateral membrane, or the paracellular
pathway. In adult proximal tubules, transepithelial water transport is
predominantly, if not solely, transcellular (16); however,
this remains somewhat controversial (8, 24). Recently,
additional evidence for the transcellular route for water transport
comes from mice that lack the water channel AQP1 (9, 25).
The water permeability in proximal tubules from these mice was
significantly lower than in wild-type mice, indicating that most water
transport must be transcellular and mediated by AQP1.
In the present study, we found that the Pf of
the neonatal PCT was the same as that of the adult. These results are
qualitatively similar to our previous measurements of the
Pf in adult and neonatal tubules at these
perfusion rates (20). However, in our previous study, the
maximum Pf for each tubule was determined by
increasing the perfusion rate and extrapolating to an infinite
perfusion rate. This approach was not feasible in the present study
because of the use of multiple bath osmolalities for each tubule. Thus the methodology for calculating the Pf was
different and may have a direct effect on the calculated values
(3). In the present study, the Pf
of the neonatal tubules was not statistically different from the adult
tubules, as was found in our previous study (20) at an
infinite perfusion rate.
Because the transcellular route for water movement consists of the
apical and basolateral membranes and the intracellular compartment, any
differences in transepithelial water permeability must be due to
differences in one or more of these components. We have previously
demonstrated that the apical and basolateral membranes of the neonatal
tubule have a lower Pf than the adult tubule
(21, 22). The expression of AQP1 in the neonatal membranes was also found to be significantly lower than that of the adult membranes. In the present study, the PDW of the
tubule membranes was shown to be lower in the neonatal tubules than the
adult tubules. In addition, the PDW(membrane) in
the neonatal tubules had a higher activation energy than the adult
tubules that our laboratory has previously found in the apical membrane
(22). Thus the water permeabilities of the cellular
membranes of the proximal tubule would contribute to a lower
Pf for the neonatal tubule than the adult tubule.
The remaining component of transcellular water movement is the
intracellular compartment. The cytoplasmic compartment is a complex
unstirred layer (5) and may account for >50% of the transcellular resistance to water movement (4). Thus small changes in the cellular compartment may significantly affect
transepithelial water permeability. We found that the cell height of
the neonatal proximal tubule was significantly lower than that of the
adult proximal tubule, as previously described by our laboratory and others (2, 10). This suggests that the path length for
water movement through the cell is much shorter in the neonatal
proximal tubule than the adult. To assess this more directly, we
measured the permeability of n-butanol, a lipophilic small
molecule that would have a very high permeability through the membranes
(4). The n-butanol permeability was higher in
the neonatal tubules, thus offering evidence that the intracellular
pathway of water transport in the neonatal tubule has less resistance
to the movement of water than the adult tubule. Interestingly, the
ratio of the adult to neonatal cell heights was equal to the ratio of
the neonatal to adult n-butanol permeability. Thus
the higher than expected transepithelial Pf in
neonatal proximal tubules may be due to developmental changes in the
intracellular compartment.
The remaining component of the transepithelial pathway for water
movement to be examined is the paracellular pathway. This component is
difficult to measure directly (27); thus we made several
indirect measurements to characterize the paracellular pathway in the
adult and neonatal tubules. First, we found that the neonatal tubules
had a lower mannitol permeability than the adult tubules. This is
contrary to previous studies that indirectly determined the mannitol
permeability of the neonatal proximal tubule to be higher than that of
the adult tubule in the guinea pig (14). However, this is
in agreement with developmental changes in permeabilities of other
solutes. We have previously shown that the permeabilities of
bicarbonate and chloride are also lower in the neonatal tubule than the
adult tubule (17, 26). Second, there was no change in the
flux of mannitol when an osmotic gradient was imposed on the tubules.
Thus there is no evidence for the solvent drag of mannitol, a small
nonionic solute, in either the neonatal or the adult tubules. Third,
there was also no influence of the osmotic gradient on the flux of
chloride in either the adult or the neonatal tubules. This is similar
to the results obtained by Jacobson et al. (13) in adult
tubules. Thus there was no solvent drag for chloride, a small ion.
Taken together, these data argue against any appreciable water movement
through the paracellular pathway in the neonatal or the adult tubules.
The differences between the adult and neonatal proximal tubules are
illustrated in Fig. 9. We have previously
shown that the apical and basolateral membranes of the neonatal
proximal tubule have less AQP1 and a lower Pf
than the adult membranes (21, 22). The present study shows
that the intracellular compartment of the neonatal tubules provides
less resistance to the movement of water than that of the adult tubule.
The low water permeability of the neonatal tubule cell membranes is
offset by the high permeability of the cell compartment, making the
overall epithelial water permeability the same as that of the adult
tubule. Thus the intracellular compartment of the proximal tubule plays
a significant role in the overall water permeability of the tubule.

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Fig. 9.
Model of proximal tubule water transport. Transcellular
transport of water is depicted as the apical and basolateral membranes
in series with the intracellular compartment. AQP1, aquaporin-1.
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ACKNOWLEDGEMENTS |
We thank Janell McQuinn for secretarial assistance and Amber Lisec
for technical assistance.
 |
FOOTNOTES |
This work was supported by National Institute of Diabetes and Digestive
and Kidney Diseases Grant DK-41612 (M. Baum).
Address for reprint requests and other correspondence: R. Quigley, Dept. of Pediatrics, Univ. of Texas Southwestern Medical Ctr.,
5323 Harry Hines Blvd., Dallas, TX 75235-9063 (E-mail:
Raymond.Quigley{at}UTSouthwestern.edu).
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. Section 1734 solely to indicate this fact.
10.1152/ajprenal.00341.2001
Received 14 November 2001; accepted in final form 16 January 2002.
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