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
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Abstract
Introduction
Materials & Methods
Results
Discussion
References

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
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Abstract
Introduction
Materials & Methods
Results
Discussion
References

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
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Abstract
Introduction
Materials & Methods
Results
Discussion
References

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)
<IT>J</IT><SUB>net H<SUB>2</SUB>O</SUB> = V<SUB>i</SUB> × [1 − (PSP<SUB>i</SUB>/PSP<SUB>o</SUB>)] × 60/W
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.
<IT>J</IT><SUB>net Na or Ca</SUB> = V<SUB>i</SUB> × [S<SUB>i</SUB> − (PSP<SUB>i</SUB>/PSP<SUB>o</SUB>) × S<SUB>o</SUB>] × 60/W
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+ (Jlright-arrow m Ca) was determined from the disappearance rate of 45Ca from the perfusion solution. It was calculated using the following formula
<IT>J</IT><SUB>1→m Ca</SUB> = V<SUB>i</SUB> × [CPM<SUB>i</SUB> − (PSP<SUB>i</SUB>/PSP<SUB>o</SUB>) × CPM<SUB>o</SUB>] 
× [(S<SUB>i</SUB> + S<SUB>o</SUB>)/(CPM<SUB>i</SUB> + CPM<SUB>o</SUB>)] × 60/W
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 (Jmright-arrow l Ca) was not measured. It was calculated from the difference between Jnet Ca and Jlright-arrow m Ca as Jmright-arrow l Ca = Jlright-arrow 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 (Jmright-arrow s) and serosal-to-mucosal (Jsright-arrow 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 = Jmright-arrow s - Jsright-arrow 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
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Abstract
Introduction
Materials & Methods
Results
Discussion
References

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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Table 1.   H2O, Na+, and Ca2+ fluxes measured in ileal segments perfused in situ


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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 (Jlright-arrow 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.

                              
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Table 2.   Ca2+ and mannitol fluxes measured in Ussing chamber

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.

                              
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Table 3.   Ca2+ and mannitol permeabilities

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 (Jmright-arrow s Caparacell) from the equation that links these parameters in the serosal-to-mucosal direction
<IT>J</IT><SUB>m→s Ca<SUB>paracell</SUB></SUB> = (0.6 × <IT>P</IT><SUB>m→s mann</SUB> + 10.2 × 10<SUP>−3</SUP>) × [Ca]
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 (Psright-arrow m Ca) and mannitol permeability (Psright-arrow m mann) are expressed in cm · h-1 · 10-3. The linear regression equation was y = 0.6x + 10.2; r = 0.824.

                              
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Table 4.   Transcellular and paracellular components of unidirectional mucosal-to-serosal Ca2+ flux

    DISCUSSION
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Abstract
Introduction
Materials & Methods
Results
Discussion
References

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.

    REFERENCES
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References

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Am J Physiol Gastroint Liver Physiol 275(5):G951-G956
0002-9513/98 $5.00 Copyright © 1998 the American Physiological Society




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