Role of transcellular pathway in ileal
Ca2+ absorption: stimulation
by low-Ca2+ diet
D.
Auchère1,
S.
Tardivel2,
J.-C.
Gounelle1,
T.
Drüeke3, and
B.
Lacour1,2
1 Laboratoire de Physiologie,
and 2 Laboratoire
du Métabolisme Minéral des Mammifères de l'Ecole
Pratique de Hautes Etudes, Faculté des Sciences Pharmaceutiques
et Biologiques, Université Paris XI, 92290 Châtenay-Malabry; and
3 Institut National de la
Santé et de la Recherche Médicale U90, Hôpital
Necker, 75015 Paris, France
 |
ABSTRACT |
The present study was performed to determine the
respective involvement of the cellular and paracellular routes in ileal
Ca2+ transport. Two groups of rats
were either fed a normal Ca2+ diet
(1.0%) or a Ca2+-deficient diet
(0.02%) for 14 days. Ileal Ca2+
absorption was determined using both an in situ method of continuous luminal perfusion and an in vitro method (Ussing chamber model). The
low-Ca2+ diet stimulated net
Ca2+ flux in the ileum twofold,
associated with a twofold increase of the mucosal-to-serosal
Ca2+ flux in both models. This
effect was observed in the absence of concomitant changes in
Na+ or water flux in the in situ
model or mannitol flux in the in vitro model, excluding the
participation of the paracellular pathway in
Ca2+ transport. Thus only cellular
Ca2+ flux was stimulated. These
data suggest that the ileum plays a major role in the adaptation to low
dietary Ca2+. Whereas under
physiological conditions with usual
Ca2+ intakes the transcellular
pathway of Ca2+ transport is
negligible, it becomes of major importance in the case of
Ca2+ deficiency, at least under
the present conditions of severe
Ca2+ deprivation.
calcium transport; in situ perfusion; Ussing method; unidirectional
flux; cellular flux
 |
INTRODUCTION |
CALCIUM IS ABSORBED across the intestinal wall via two
pathways: the first is transcellular and corresponds to a saturable process, whereas the second is paracellular and represents a
nonsaturable transport. It is generally admitted that the major part of
the transcellular component of
Ca2+ transport takes place in the
duodenum, with a minor part occurring also in the ascending colon,
whereas the paracellular pathway takes place throughout the gut.
Numerous studies have been performed to examine the various steps
involved in the active, transcellular pathway of
Ca2+ transport in the duodenum
(13, 28). Several of them have shown that all these steps may be
stimulated by vitamin D (28, 29). By contrast, our knowledge concerning
the modulation of the paracellular route remains relatively limited to
date.
At present, Ca2+ absorption in the
ileum is widely considered to be devoid of a saturable process. It
appears to be entirely dependent on the luminal
Ca2+ concentration. In the adult
rat, ileal Ca2+ absorption has
been shown to be mainly paracellular, at least in the presence of a
luminal Ca2+ concentration >1
mM. However, some investigators (10, 13) have found evidence in favor
of the cellular pathway in the ileum as well, mainly with a luminal
Ca2+ concentration of 1.25 mM.
The effects of vitamin D and of
Ca2+-restricted diets on ileal
Ca2+ transport have led to
contradictory conclusions. Some authors (5, 11, 14, 20, 26) have
reported an increase of the ileal mucosal-to-serosal flux of
Ca2+, whereas others (2, 9, 10,
18, 25) were unable to confirm this finding. There is only one study
(16) that has addressed this issue in humans, using in situ perfusion
of intestinal segments. This study (16) showed ileal
Ca2+ absorption to be stimulated
after the administration of a diet very low in
Ca2+.
The aim of the present study was to compare the ileal absorption of
Ca2+ in adult rats, after feeding
them either a normal Ca2+ diet
(1.0%) or a Ca2+-deficient diet
(0.02%) for 14 days, using both an in situ method of continuous
luminal perfusion and the in vitro method of the Ussing chamber model.
Water and Na+ fluxes were
simultaneously measured in vivo, as was mannitol flux in vitro, to
estimate the paracellular pathway and thus to determine the respective
involvement of the cellular and paracellular routes.
 |
MATERIALS AND METHODS |
Animal handling and experimentation were done in accordance with the
guidelines issued by the European Economic Community, as published in
the Journal
Officiel
des
Communautés
Européennes (December 18, 1986;
authorization L3600).
Adult male Wistar rats, weighing 250-350 g, were purchased from
Iffa Credo (L'Arbresles, France). They were acclimated for 5 days on
standard diet and exposed to a 12:12-h light-dark cycle. Then they were
fed, over a period of 14 days, either a normal Ca2+ diet or a
low-Ca2+ diet
(210Ca and
212Ca, respectively; UAR
laboratory, Villemoisson, France). The diets contained 0.77%
phosphorus, 0.1% magnesium, 19% protein, 2,500 IU/kg vitamin
D3, and either 1%
Ca2+ (normal
Ca2+ diet) or 0.02%
Ca2+
(low-Ca2+ diet). The rats of the
low-Ca2+ group had free access to
food, and each rat of the control group was pair-fed with a rat of the
low-Ca2+ group to allow for an
identical amount of food ingested by both groups. All rats had free
access to distilled water.
For each experiment, food was withheld at 17 h the day before.
Continuous intestinal perfusion in situ.
The procedure described here was simultaneously carried out each time
in one rat from each group. Rats were anesthetized by an
intraperitoneal injection of pentobarbital (60 mg/kg). An ileal segment, 20 cm in length, was isolated just before the ileocoecal junction, cannulated at its two extremities, rinsed with 20 ml of an
isotonic NaCl solution, which had been prewarmed to 37°C, flushed
with 40 ml of air, and inserted back into the abdominal cavity, which
was then closed again.
Thereafter, the segment was perfused in situ by a single-pass
technique, at a flow rate of 200 µl/min, with an isotonic solution prewarmed to 37°C, using an automatic pump (Braun, Melsungen, Germany). During the equilibration period (the first 60 min), the
effluent was discarded. Subsequently, it was collected during three
consecutive 20-min periods for analytical measures.
The rat was then killed by a lethal pentobarbital injection. The
perfused segment was carefully excised and cut longitudinally. The
intestinal mucosa was dried with absorbant paper before being scraped
and weighed.
The perfusion solution contained 145 mM NaCl, 1.25 mM
CaCl2, 3.4 mM KCl, 12 mM
NaHCO3, 20 mg/l of
phenolsulfonphthalein (PSP), and 600 kBq/ml of
45CaCl2.
The concentrations of Ca2+ and
Na+ in the perfusion solutions and
the collected effluents were determined using a Perkin-Elmer 2380 atomic absorption and emission spectrometer (Norwalk, CT). PSP
concentrations were determined by spectrophotometry at 555 nm, after
dilution of the samples (1 ml/8 ml of 0.015 M NaOH). 45Ca radioactivity was determined
in a Packard Tri-Carb 2000 liquid scintillation spectrometer (Meriden,
CT). Net water
(Jnet H2O), Na+
(Jnet Na),
and Ca2+
(Jnet Ca)
fluxes were expressed in microliters, micromoles, and nanomoles per
hour per gram of mucosa, respectively. Fluxes were calculated according
to the following expression (30)
where
Vi is the perfusion rate of 200 µl/min, PSPi and
PSPo are the PSP concentrations in
perfusion solution before and after perfusion of the intestinal
segment, respectively, and W is mucosa weight.
where
Si and
So are
Na+ or
Ca2+ concentrations in perfusion
solution before and after perfusion of the intestinal segment,
respectively.
The unidirectional luminal-to-mucosal flux of
Ca2+
(Jl
m Ca)
was determined from the disappearance rate of
45Ca from the perfusion solution.
It was calculated using the following formula
where
CPMi and
CPMo are
45Ca radioactivity in counts per
minute in the perfusion solution before and after perfusion of the intestinal segment, respectively.
The unidirectional mucosal-to-luminal
Ca2+ flux
(Jm
l Ca)
was not measured. It was calculated from the difference between Jnet Ca and
Jl
m Ca
as
Jm
l Ca = Jl
m Ca
Jnet Ca.
Ussing chamber experiments in vitro.
After the rats had been anesthetized with ethyl ether, we removed a
portion of the distal ileum, 10 cm before the ileocoecal junction, from
the abdominal cavity. It was rinsed immediately with an isotonic
solution of NaCl (154 mM) and put into a cool oxygenated Ringer
solution. Blood was collected from the abdominal aorta for the
determination of plasma Ca2+ and
phosphorus. The ileal segment was divided into four segments of
2-3 cm2, each of which was
mounted in typical Ussing chambers, having an exchange surface of 0.5 cm2. The serosal and mucosal sides
of the segments were bathed in a Ringer solution composed of (in mM)
120 NaCl, 4.7 KCl, 1.25 CaCl2, 25 NaHCO3, 25 glucose, and 2 mannitol. Each compartment (10 ml) was maintained at 37°C, gassed,
and pulsed with 5% CO2 in
O2 to maintain a constant pH of
7.4.
After a 20-min period required for ion and water flux stabilization,
45CaCl2
and [3H]mannitol (NEN)
were introduced as tracers into a hemichamber (at either the mucosal or
serosal side). After 1 min of equilibration, a sample solution of 100 µl was removed from this compartment to determine the specific
activity. Next, 20, 40, and 60 min later, a 500-µl sample was taken
from the opposite compartment and replaced by 500 µl of prewarmed
Ringer. 45Ca and
[3H]mannitol
radioactivities were then determined in all the samples.
Analytical determinations and calculation of fluxes.
Plasma Ca2+ and phosphorus
concentrations were measured using a colorimetric method. Plasma
calcitriol was determined using a radioreceptor assay (Nichols
Institute, San Juan Capistrano, CA).
45Ca radioactivity was determined
using the materials described above.
45Ca and
3H were counted simultaneously
with correction for 3H channel to
eliminate 45Ca channel
interference. 45Ca efficiency was
85% and that of 3H was 90% to
minimize cross-channel contamination. This correction was verified for
each experiment, and it was taken into account for flux calculations.
The chambers were paired to determine unidirectional fluxes of opposite
direction, when the conductance of the two tissues was >70%.
Unidirectional mucosal-to-serosal
(Jm
s) and serosal-to-mucosal
(Js
m)
fluxes were calculated according to the formula of Schultz and Zalusky
(22). Net fluxes corresponded to the difference between the two
unidirectional fluxes of opposite direction:
Jnet = Jm
s
Js
m.
The tissue was continuously short-circuited with short interruptions at
20-min intervals to determine open-circuit potential difference (PD)
and short-circuit current
(Isc), which
was necessary to calculate tissue conductance
(Gt) as
Gt = Isc/PD.
Statistical analysis of results.
Each individual value corresponded to the mean of three measures done
respectively on the perfusion solution during the three 20-min
collection periods in the in situ perfusion experiments and on the
samples collected at 20, 40, and 60 min in the Ussing chamber
experiments.
Results are expressed as means ± SE for each series of
n animals. Comparison between series
was done using the Fisher exact test
(F test). Differences were considered
significant for P
0.05. Linear
regression was calculated by the least-squares method, and significance
was tested by ANOVA (Statview, Apple).
 |
RESULTS |
No difference was observed in the body weight of rats fed a normal and
a low-Ca2+ diet (318 ± 5.7 vs.
315 ± 5.7 g, respectively) after 2 wk of treatment.
After 14 days of a low-Ca2+ diet,
mean plasma Ca2+ was markedly
decreased (1.6 ± 0.1 mmol/l) compared with that of the control group fed a normal Ca2+ diet (2.2 ± 0.1 mmol/l), and plasma calcitriol was increased from 236 ± 24 to 1,010 ± 40 pg/ml (n = 4 for
each group). Mean plasma phosphorus was identical in both groups of
rats (2.7 ± 0.2 vs. 2.7 ± 0.15 mmol/l).
Continuous intestinal perfusion in situ.
Data for net water, Na+, and
Ca2+ fluxes as well as
unidirectional Ca2+ fluxes are
indicated in Table 1. In both groups of
animals, net water and Na+ fluxes
were similar. The two fluxes were closely correlated, as
shown in Fig.
1A.

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Fig. 1.
A: correlation between net fluxes of
Na+
(Jnet Na)
and H2O
(Jnet H2O)
in rats fed a normal Ca2+ diet
(control) and in rats fed a diet low in
Ca2+.
Jnet H2O
and Jnet Na
are expressed in
µl · h 1 · g 1
and
µmol · h 1 · g 1,
respectively. The linear regression equation was
y = 5.96x 185;
r = 0.984. B: correlation between net flux of
Ca2+
(Jnet Ca)
and luminal-to-mucosal Ca2+ flux
(Jl m Ca)
(expressed in
nmol · h 1 · g 1).
The linear regression equation was y = 1.12x 1,683;
r = 0.938.
|
|
Net Ca2+ flux and luminal-to
mucosal Ca2+ flux were
considerably increased in rats fed the
low-Ca2+ diet. These two fluxes
were tightly correlated in both groups of rats (Fig.
1B). Mucosal-to-luminal
Ca2+ flux was decreased in the
low-Ca2+ diet group. However, this
decrease was not statistically significant.
Ussing chamber experiments in vitro.
Table 2 shows electrical parameters and
fluxes measured in the Ussing chamber under short-circuit conditions.
As in the in situ perfusion model, a large increase of net
Ca2+ flux was observed in response
to the low-Ca2+ diet that was
associated with a marked increase of the mucosal-to-serosal Ca2+ flux, while
mucosal-to-serosal mannitol flux, used as an indicator of paracellular
pathway, was significantly diminished. In both groups of rats,
serosal-to-mucosal Ca2+ flux and
serosal-to-mucosal mannitol flux were similar.
The low-Ca2+ diet modified
electrical parameters, i.e., it induced a decrease in short-circuit
current, transepithelial potential difference, and tissue conductance.
From the results presented in Table 2, we have calculated
Ca2+
(PCa) and
mannitol
(Pmannitol)
permeabilities from serosal to mucosal and from mucosal to serosal,
according to the formulas PCa = JCa/[Ca2+]
and Pmannitol = Jmannitol/[mannitol],
where [Ca2+] and
[mannitol] are the Ca2+
and mannitol concentrations, respectively.
The results of these calculations are shown in Table
3. Obviously, the ratio of
Ca2+ permeability to mannitol
permeability was very close to 1 in both groups for the
serosal-to-mucosal direction and in the control group for the
mucosal-to-serosal direction. In contrast, the latter ratio was
strongly increased in the rats fed a
low-Ca2+ diet.
Figure 2 shows a close correlation between
serosal-to-mucosal Ca2+
permeability and serosal-to-mucosal mannitol
permeability. Because Nellans and Kimberg (15) demonstrated that this
relation, when established in the serosal-to-mucosal direction, could
also be applied to the mucosal-to-serosal direction for the
paracellular route, we have calculated the paracellular component
of mucusal-to-serosal Ca2+
flux
(Jm
s Caparacell)
from the equation that links these parameters in the
serosal-to-mucosal direction
After subtraction of the paracellular component from
mucosal-to-serosal
Ca2+ flux calculated as above, we
calculated the transcellular component of mucosal-to-serosal
Ca2+ flux (Table
4). It was found that in control rats the
major part of Ca2+ absorbed in the
ileum was via the paracellular pathway. By contrast, in the rats fed a
low-Ca2+ diet, the transcellular
component became as important as the paracellular component. This
explained the large increase of mucosal-to-serosal Ca2+ flux and net
Ca2+ flux, in the absence of
changes in mucosal-to-serosal mannitol flux.

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Fig. 2.
Ileal serosal-to-mucosal Ca2+
permeability
(Ps m Ca)
and mannitol permeability
(Ps m mann)
are expressed in
cm · h 1 · 10 3.
The linear regression equation was y = 0.6x + 10.2;
r = 0.824.
|
|
 |
DISCUSSION |
The main finding of the present study was that the ingestion of a diet
very low in Ca2+ strongly
stimulated the net flux of Ca2+ in
the ileum of normal rats. This increase was associated with an increase
of the unidirectional Ca2+ flux
from the mucosal to the serosal side of the gut wall, in the absence of
concomitant changes in Na+ and
water flux. This observation is compatible with a stimulation of the
transcellular Ca2+ transport (as
calculated in Table 4).
The in situ perfusion experiments and in vitro transport studies were
carried out with a Ca2+
concentration of 1.25 mM, to avoid the induction of a chemical gradient
facilitating paracellular absorption of
Ca2+ and thus to favor
transcellular transport.
In the ileum of normal rats, Ca2+
transport occurs mainly via the paracellular pathway and is mainly a
function of luminal Ca2+
concentration. Thus, in rats fed a
Ca2+-rich diet, it has been shown
that the major part of luminal
Ca2+ was transported across the
intestinal wall through the paracellular pathway, following the
chemical concentration gradient (19). In accord with this finding, our
results obtained in the Ussing chamber indicated that in the normal rat
the cellular component of Ca2+
absorption was nearly absent. However, Karbach and Rummel (10) observed
that 31% of the Ca2+ flux
directed from the mucosa to the serosa was due to a transcellular active transport. They (10) used an Ussing chamber model similar to
that in the present experiments, except that solely the mucosal layer
was mounted as surface exchange structure, in contrast to the whole
epithelial layer used in our study. This technique is excellent for the
analysis of transport through the mucosa but is extremely far from
physiological conditions. This might explain the discrepancies between
our results.
It has previously been suggested that, since net
Ca2+ absorption in the ileum is
correlated with net Na+ and water
transport, Ca2+ transport in this
intestinal segment might essentially be considered to be the result of
a solvent drag effect (2). In the rat ileum, actually >85% of total
ion conductance goes through the paracellular pathway (17).
However, ileal Ca2+ absorption has
not always been found to be strictly correlated with
Na+ absorption. Thus, under some
experimental conditions, the replacement of sodium chloride by choline
chloride led to an increase of the mucosal-to-serosal flux of
Ca2+ (5). Furthermore, the
replacement of Na+ by organic
cations in the luminal solution led to an arrest of Na+ absorption, which in return
stopped Ca2+ absorption via
solvent drag (8). In this case, the observed stimulation of
Ca2+ transport obviously occurred
through the transcellular pathway alone. Similarly, in our study a
dissociation was found between changes in
Ca2+ flux and those of
Na+ and water flux.
An increase of ileal Ca2+
absorption in response to a
low-Ca+ diet has been reported in
previous studies in the rat (20, 27) and also in humans (16). The
stimulation of the net Ca2+ flux
in the absence of a change in Na+
absorption is in agreement with a study reported by Norman et al. (16)
in which the paracellular route of
Ca2+ flux was excluded. Similarly,
in experiments carried out in the Ussing chamber model the increase in
Ca2+ absorption was due to the
transcellular transport component alone, in the absence of a change in
the paracellular pathway, as shown by the concomitant determination of
mannitol flux (14).
The effects of a low-Ca2+ diet on
ileal Ca2+ transport might be
explained best by a stimulation of calcitriol production, as suggested by the marked increase of plasma calcitriol observed in
Ca2+-deficient rats of the present
study. Previous studies have shown that
Ca2+-ATPase activity was increased
by calcitriol and that this enzyme, which is located in the basolateral
membrane of enterocytes throughout the gut, from duodenum to ileum (1,
29), is indispensable for Ca2+ to
be extruded from the cell (7, 28). The administration of vitamin D to
vitamin D-deficient rats increased the amount of plasma membrane
Ca2+-ATPase pump protein to the
same extent in three different segments of the small intestine,
including the ileum (29). The increase in intestinal plasma membrane
Ca2+-ATPase protein is preceded by
an increase in its mRNA (31). A
low-Ca2+ diet might increase the
number of pumps inserted into the basolateral membrane and thereby
enhance Ca2+ transport (29). Thus
vitamin D would stimulate Ca2+
absorption across the enterocyte by a mechanism located beyond the
level of the brush-border membrane (21).
Because the ileum of normal rats fed a normal
Ca2+ diet contains calbindin 9k
(4) and since calbindin 9k is a vitamin D-regulated protein (24), it is
possible to incriminate its involvement in the stimulation of
transcellular Ca2+ transport
induced by the low-Ca2+ diet. A
fivefold increase of calbindin 9k has been observed in ileum of pigs in
response to a Ca2+-poor diet
(0.06%) for 5 wk (23).
In conclusion, under physiological conditions the transcellular pathway
is probably of limited importance for
Ca2+ absorption in the ileum, that
is when abundant amounts of dietary Ca2+ are ingested. The long
transit time of Ca2+ in the small
intestine and its greater luminal concentration in ileum than in
duodenum (12) favor the paracellular pathway of
Ca2+ transport. However, the
cellular pathway gains importance and may even become preponderant in
case dietary Ca2+ intake is low
and/or serum calcitriol concentrations are elevated. In
contrast to general belief, under these circumstances, the ileum is as
much involved in active Ca2+
transport as the duodenum. Moreover, when the respective length of each
segment of the small intestine is taken into account, the ileum
probably exerts a more important role in the adaptation to a
low-Ca2+ diet than does the
duodenum. Hence one should consider the ileum, not the duodenum, as the
main body guard to maintain Ca2+
homeostasis. It may be added that the
Ca2+-sensing receptor cloned by
Brown et al. (3) is also expressed in the ileum, as has been found
recently (6). However, its possible implication in the regulation of
ileal Ca2+ transport remains to be
defined.
 |
FOOTNOTES |
Address for reprint requests: D. Auchère, Laboratoire de
Physiologie, Faculté des Sciences Pharmaceutiques et Biologiques,
Université Paris XI, 92290 Châtenay-Malabry, France.
Received 1 December 1997; accepted in final form 15 June 1998.
 |
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