The colonic epithelium has both absorptive and secretory functions. The transport is characterized by a net absorption of NaCl, short-chain fatty acids (SCFA), and water, allowing extrusion of a fe...

Electrolyte Transport in the Mammalian Colon: Mechanisms and Implications for Disease

Chloride secretion is the major determinant of mucosal hydration throughout the gastrointestinal tract, and chloride transport is also pivotal in the regulation of fluid secretion by organs that drain into the intestine. Moreover, there are pathological consequences if chloride secretion is either reduced or increased such as in cystic fibrosis and secretory diarrhea, respectively. With the molecular cloning of many of the proteins and regulatory factors that make up the chloride secretory mechanism, there have been significant advances in our understanding of this process at the cellular level. Similarly, emerging data have clarified the intercellular relationships that govern the extent of chloride secretion. The goal of our article is to review this area of investigation, with an emphasis on recent developments and their implications for the physiology and pathophysiology of chloride transport.

Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects.

Cl−secretion in the colon can be activated by an increase of either intracellular Ca2+ or cAMP. In this study we examined a possible interdependence of the two second-messenger pathways in human co...

Cholinergic ion secretion in human colon requires coactivation by cAMP

The past 20 years have seen many advances in all aspects of colonic physiology, and the unrelenting appearance of new information is daunting to clinicians and scientists alike. Nevertheless, we should not lose sight of the fact that the main function of the human colon is to absorb about 90% of the 1.5–2 litres of ileal effluent which passes daily through the ileocaecal valve.1 2 In mammalian species, the key determinant of colonic water absorption is the rate of Na+ absorption. We now know that Na+ transport processes are not distributed uniformly throughout the human colon, a concept which has important clinical implications. This review provides an update on the basic mechanisms underlying salt and water transport in the human colon in health and disease, and highlights several interesting areas for future research.

The human colon has a nominal mucosal surface area of about 2000 cm2,3 but in reality the total absorptive area is even greater because colonic crypt cells are capable of absorption as well as secretion.4 Although it is well established that the rates of colonic salt (Na+ plus Cl−) and water absorption are directly related,5 it is only recently that we have begun to appreciate the array of Na+absorptive processes present in human colon. These show considerable intrinsic segmental heterogeneity.6-10 This explains, at least in part, why the colon’s capacity for sodium and water absorption in vivo is greater in the proximal (ascending) segment than in the distal (descending and sigmoid colon/rectum) segment.11-15 Several different active (transcellular) Na+ absorptive processes exist in human colon. It will become clear that segmental differences in the distribution and regulation of these processes play an important role in colonic Na+ salvage during periods of salt …

https://gut.bmj.com/content/gutjnl/43/2/294.full.pdf

Salt and water absorption in the human colon: a modern appraisal

The ubiquitous ClC-2 Cl−channel is thought to contribute to epithelial Cl−secretion, but the distribution of the ClC-2 protein in human epithelia has not been investigated. We have studied the dist...

https://www.physiology.org/doi/pdf/10.1152/ajpcell.00291.2001

Distribution of ClC-2 chloride channel in rat and human epithelial tissues

Although renal potassium transport provides the basis for K+ homeostasis, the distal large intestine contributes to fine tuning of the K+ content of the body. In order to meet this function, the distal colon shows both active K+ absorption and active K+ secretion (Hayslett & Binder, 1982; Binder & Sandle, 1994). The latter can be stimulated by aldosterone as well as by 3′,5′-cyclic monophosphate (cAMP) (Foster, Sandle, Hayslett & Binder, 1983; Foster, Hayslett & Binder, 1984; McCabe, Smith & Sullivan, 1984; Smith & McCabe, 1984). Localization of K+ secretion in rat late distal colon is of interest, because functional differences between the epithelium of the flat surface of the colon mucosa and that of the tubular crypts extending to the muscularis mucosae have been demonstrated.

Sodium absorption induced by physiological (i.e. nanomolar) aldosterone concentration is confined to surface epithelium (Kockerling, Sorgenfrei & Fromm, 1993), but cAMP-induced Cl− secretion occurs not only in the crypts but also in the surface epithelium (Kockerling & Fromm, 1993). There is a controversy, however, about the location of active K+ secretion in the colon. For a long time, it has been attributed to Cl−-secretory crypt cells (Welsh, Smith, Fromm & Frizzell, 1982). This point of view could be maintained for aldosterone-induced K+ secretion, because short-circuit current recordings in mammalian colon show K+ secretion independent of Na+ absorption (Foster et al. 1983, 1984; McCabe et al. 1984; Halm & Frizzell, 1986; Rechkemmer & Halm, 1989), whereas in turtle colon K+ secretion is coupled to Na+ absorption (Halm & Dawson, 1984). An elaborate micropuncture study in rat distal colon challenged this view, finding aldosterone-induced K+ secretion in 82 % of surface cells, but only in 50 % of accessible crypt cells (Lomax & Sandle, 1994; Lomax, McNicholas, Lombes & Sandle, 1994). Micropuncture studies, however, lacking access to deeper crypt cells, do not allow a quantification of the contribution of the whole crypt. The location of cAMP-induced K+ secretion is still obscure. The finding that adrenaline and aldosterone non-additively induce the same amount of K+ secretion in guinea-pig colon suggests that both secretagogues may act on the same transport pathway (Rechkemmer & Halm, 1989), but the site of action has not been determined.

In the present study, aldosterone- and adrenaline-induced K+ secretion in rat late distal colon were assessed in both crypt and surface epithelium by a new method, an improvement of the voltage scanning technique (Fromter, 1972). It is based on the analysis of local differences in current density, which are recorded in the supra-epithelial bath solution with a stepping and scanning glass electrode during application of a transepithelial clamp current (Kockerling & Fromm, 1993; Kockerling et al. 1993). Since the locally differentiated conductivity of an epithelium is evaluated, the method is called conductance scanning. In combination with conventional measurements of short-circuit current and ion fluxes, conductance scanning allowed for localization of transepithelial K+ transport: aldosterone-induced K+ secretion is, like Na+ absorption, confined to surface epithelium, whereas adrenaline-induced K+ secretion can be found in both surface epithelium and crypts.

https://physoc.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-7793.1998.561bt.x

Localization of cAMP‐ and aldosterone‐induced K+ secretion in rat distal colon by conductance scanning

Gogarten W, Kockerling A, Fromm M, Riecken EO, Schulzke JD. Effect of acute Yersinia enterocolitica infection on intestinal barrier function in the mouse. Scand J Gastroenterol 1994;29:814-819.Background: Yersinia enterocolitica is an important cause of diarrhea, but little is known about the underlying mechanisms. We therefore studied the impact of acute Y. enterocolitica infection on intestinal barrier function in a mouse model. Methods: For this purpose CD-I mice were infected with Y. enterocolitica (serotype 08; 6 × 107 viable bacteria), and alternating current impedance analysis was performed on days 1, 2, 3, 5, and 8 after infection. Results: The infection resulted in a decrease in epithelial resistance from 18.0 ± 0.9 ωcm2 (controls) to 12.1 ± 0.5 ωcm2 (day 1, p < 0.001), from which the animals recovered by day 5. To locate this loss in barrier function, the horizontal distribution of local conductances was measured by voltage scanning, yielding two results. First, conductance was homogeneously dis...

Effect of acute Yersinia enterocolitica infection on intestinal barrier function in the mouse

Adenosine 3',5'-cyclic monophosphate (cAMP)-dependent Cl- secretion provides the ionic basis for secretory diarrhea. We quantified the spatial distribution of this process by measuring local ion conductance in crypts and surface epithelium or villi of rat late distal colon and ileum. By use of an improved voltage-scanning technique, the tissue was clamped to a 30-Hz sine-wave current and the electrical field above the respective structures was sensed by a stepping glass microelectrode. Under control conditions, crypts and surface epithelium contributed 61 and 39%, respectively, to the total ion conductance of distal colon. Theophylline (10 mM) increased crypt conductance (Gc) by 64% from 2.5 +/- 0.2 to 4.1 +/- 0.3 mS/cm2 and surface epithelium conductance (Gs) by 69% from 1.6 +/- 0.1 to 2.7 +/- 0.1 mS/cm2. These changes in local conductances were completely Cl- dependent, since theophylline had no effect when Cl- was replaced by gluconate. Similar results were obtained when Cl- secretion was elicited by prostaglandin E1 (1 microM) or by dibutyryl-cAMP (DBcAMP, 1 mM). After stimulation, the Cl- channel blocker 5-nitro-2-(3-phenyl-propylamino)benzoic acid (1 mM) decreased both Gc and Gs. In rat ileum, theophylline plus DBcAMP caused an increase in total conductance of 19% only because of its large paracellular conductance. The ratio of scanning signals above villi and intervillous spaces was unaffected, indicating that Cl- conductance is induced in both crypts and villi. We conclude that in distal large intestine cAMP-dependent Cl- secretion is not confined to crypts but is evenly performed also by surface cells. A similar distribution exists in small intestine.

Origin of cAMP-dependent Cl- secretion from both crypts and surface epithelia of rat intestine

There is no quantitative assignment of large intestinal electrogenic Na+ absorption to surface epithelium and crypts so far. We determined the spatial distribution of electrogenic Na+ absorption to crypts and surface epithelium of rat late distal colon using a modified voltage-scanning technique. Voltage deflections resulting from external 30-Hz current were sensed by an extracellular microelectrode stepping at 0.7 Hz above crypt openings or surface epithelium. Local conductances were calculated applying a planar model of electrical field distribution to surface epithelium and a electrostatic disk source model to the crypts. These models were confirmed by methodological experiments where the electrode position was varied in vertical and horizontal direction. Electrogenic Na+ absorption was detected by blocking apical Na+ channels by mucosal 0.1 mM amiloride. Under control conditions surface epithelium contributed 44% (2.0 +/- 0.2 mS/cm2) and crypts 56% (2.6 +/- 0.2 mS/cm2) to the total conductance of 4.6 +/- 0.4 mS/cm2. Electrogenic Na+ absorption was induced by 6 h in vitro incubation in a medium containing 3 nM aldosterone. This caused a short-circuit current (ISC) of 12.1 +/- 0.8 mumol.h-1.cm-2, which was paralleled by a 2.5-fold increase in surface epithelial conductance to 5.1 +/- 0.4 mS/cm2, whereas crypt conductance was not significantly altered (3.0 +/- 0.2 mS/cm2). Amiloride reversed ISC to -0.8 +/- 0.1 mumol.-1.cm-2 and decreased surface epithelium conductance to 2.3 +/- 0.3 mS/cm2 but again had no significant effect on crypt conductance (2.5 +/- 0.3 mS/cm2). Sham incubation (no hormones added) for 6 h neither induced electrogenic transport nor altered local epithelial conductances.(ABSTRACT TRUNCATED AT 250 WORDS)

Electrogenic Na+ absorption of rat distal colon is confined to surface epithelium: a voltage-scanning study.

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Localization of cAMP‐ and aldosterone‐induced K+ secretion in rat distal colon by conductance scanning

Effect of acute Yersinia enterocolitica infection on intestinal barrier function in the mouse

Origin of cAMP-dependent Cl- secretion from both crypts and surface epithelia of rat intestine

Electrogenic Na+ absorption of rat distal colon is confined to surface epithelium: a voltage-scanning study.