H+ and HCO3- flux across apical surface of rat distal colon

Feldman, George M.; Stephenson, R. L.

doi:10.1152/ajpcell.1990.259.1.c35

Cited by 41 publications

(10 citation statements)

References 17 publications

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“…Our finding that the rodent distal colon, like the cecum, expresses high levels of DRA but negligible NHE3 is compatible with previous reports that this segment, like the cecum, can rapidly secrete HCO 3 Ϫ in a manner that is electroneutral, coupled to Cl Ϫ absorption (7,27,28,46,66,83), and dependent on DRA function (74,79). Our results, however, are inconsistent with previous evidence that NHE3, but not NHE2, participates in electroneutral HCO 3 Ϫ -dependent NaCl absorption by the rat distal colon (5, 51); the experimental use of proximal regions of the distal colon, in which NHE3 is low but clearly present (Fig.…”

Section: Discussionsupporting

confidence: 92%

“…mouse; rat; intestine; electroneutral NaCl absorption TRANSPORT ACROSS THE COLONIC epithelium allows for efficient salvage of water and solutes [Na ϩ , Cl Ϫ , short-chain fatty acid (SCFA)], maintenance of the resident microbial ecosystem, and optimal fecal consistency. The absorptive movements of Na ϩ and Cl Ϫ in the mammalian colon are, to a large degree, mutually interdependent, electrically neutral, and associated with secretory movements of H ϩ and HCO 3 Ϫ (28,29,35,57,71). It is generally accepted that electroneutral NaCl absorption by the intestine largely reflects the tandem operation of apical Na/H exchange and Cl/HCO 3 exchange processes, and studies of rodent colon have established that these processes primarily involve the Na/H exchanger NHE3 (SLC9A3) and the Cl/ HCO 3 exchanger SLC26A3 (alias downregulated in adenoma, or DRA) (5,7,57,71,86).…”

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Segregation of Na/H exchanger-3 and Cl/HCO₃exchanger SLC26A3 (DRA) in rodent cecum and colon

Talbot

Lytle

2010

American Journal of Physiology-Gastrointestinal and Liver Physi

108

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The colon is believed to absorb NaCl via the coupled operation of apical Na/H exchanger-3 (NHE3) and Cl/HCO3 exchanger SLC26A3 (DRA). Efficient coupling requires that NHE3 and DRA operate in close proximity within common luminal and cytosolic microenvironments. Thus we examined whether these proteins coexist along the apical margin of surface enterocytes by quantitative immunofluorescence microscopy in consecutive colon segments from nonfasted mice and rats. The cecocolonic profiles of NHE3 and DRA expression were roughly inverse; NHE3 was highest in proximal colon (PC) and negligible in distal colon, whereas DRA was absent in early PC and highest in the late midcolon, and DRA was prominent in the cecum whereas NHE3 was not. NHE3 and DRA coexisted only in the middle third of the colon. The consequences of unpaired NHE3/DRA expression on mucosal surface (subscript MS) pH and Na ϩ concentration ([Na ϩ ]) were assessed in nonfasted rats in situ using miniature electrodes. In the cecum, where only DRA is expressed, pH MS was ϳ7.5, markedly higher than underlaying stool (6.3), consistent with net HCO 3 Ϫ secretion. In the early PC, where NHE3 is not expressed with DRA, pHMS was acidic (6.2), consistent with unopposed H ϩ secretion. [Na ϩ ]MS was ϳ60 mM in the cecum, decreased along the PC to ϳ20 mM, and declined further to ϳ10 mM distally. Cl Ϫ was secreted into the PC, then reabsorbed distally. Our results suggest a model in which 1) unpaired DRA activity in the cecum maintains an alkaline mucosal surface that could neutralize fermentative H ϩ ; 2) unpaired NHE3 activity in the early PC preserves an acidic mucosal surface that could energize short-chain fatty acid absorption; and 3) coupled NHE3/ DRA activities in the midcolon allow for vigorous NaCl absorption at a neutral pHMS. mouse; rat; intestine; electroneutral NaCl absorption TRANSPORT ACROSS THE COLONIC epithelium allows for efficient salvage of water and solutes [Na

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Section: Discussionsupporting

confidence: 92%

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confidence: 99%

Segregation of Na/H exchanger-3 and Cl/HCO₃exchanger SLC26A3 (DRA) in rodent cecum and colon

Talbot

Lytle

2010

American Journal of Physiology-Gastrointestinal and Liver Physi

108

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“…Using the similar experimental system, Cl − -dependent HCO − 3 secretion was demonstrated in guinea pig and rat cecum (6,27) and in rat distal colon (12,13,24). Interestingly, Cl − -dependent HCO − 3 secretion was reported to be hardly observed in the proximal colon of rabbit as is the case for the mouse (23).…”

Section: Discussionmentioning

confidence: 99%

Chloride-dependent bicarbonate secretion in the mouse large intestine

2006

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The gastrointestinal HCO − 3 secretion functions to limit the mucosal acid damage due to HCl secreted in the stomach or organic acids produced in the large intestine. We studied HCO − 3 secretion in the mouse large intestine with isolated tissues mounted in chambers by using pH stat method. Addition of Cl − to the mucosal side caused an increase in HCO − 3 secretion in the cecum and distal colon but had little, if any, effect in the proximal colon. In agreement with this, mucosal surface pH was higher in the cecum and distal colon than in the proximal colon. The Cl

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“…During the past several years duodenal HCO 3 secretion has been explored by several investigators primarily in relationship with the mechanism of neutralization of gastric acid secretion (8,16). These studies, as well as those previously performed in the ileum and colon (12,24,35,36,38,40), suggested that the mechanism of HCO 3 secretion is primarily Cl-dependent and closely linked to an apical membrane Cl/HCO 3 exchange (12,24,36). Because cAMP also induces HCO 3 secretion, there has been evidence that cAMP-induced HCO 3 secretion may occur via an anion channel (possibly CFTR) or via Cl/HCO 3 exchange coupled to an anion channel (8,16,17,35).…”

Section: Discussionmentioning

confidence: 99%

Role of short-chain fatty acids in colonic HCO₃secretion

Vidyasagar

Barmeyer

Geibel

et al. 2005

American Journal of Physiology-Gastrointestinal and Liver Physi

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tyrate, a relatively poor metabolized short-chain fatty acid (SCFA), induces HCO 3 secretion via a Cl-independent, DIDS-insensitive, carrier-mediated process as well as inhibiting both Cl-dependent and cAMP-induced HCO 3 secretion. The mechanism(s) responsible for these processes have not been well characterized. HCO3 secretion was measured in isolated colonic mucosa mounted in Lucite chambers using pH stat technique and during microperfusion of isolated colonic crypts.14 C-labeled butyrate, 14 C-labeled isobutyrate, and 36 Cl uptake were also determined by apical membrane vesicles (AMV) isolated from surface and/or crypt cells. Butyrate stimulation of Cl-independent, DIDS-insensitive 5-nitro-3-(3-phenylpropyl-amino)benzoic acid-insensitive HCO 3 secretion is greater than that by isobutyrate, suggesting that both SCFA transport and metabolism are critical for HCO 3 secretion. Both lumen and serosal 25 mM butyrate inhibit cAMP-induced HCO3 secretion to a comparable degree (98 vs. 90%). In contrast, Cl-dependent HCO3 secretion is downregulated by lumen 25 mM butyrate considerably more than by serosal butyrate (98 vs. 37%). Butyrate did not induce HCO 3 secretion in isolated microperfused crypts, whereas an outward-directed HCO3 gradient-driven induced 14 C-butyrate uptake by surface but not crypt cell AMV. Both 36 Cl/HCO3 exchange and potential-dependent 36 Cl movement in AMV were inhibited by 96 -98% by 20 mM butyrate. We conclude that 1) SCFA-dependent HCO 3 secretion is the result of SCFA transport across the apical membrane via a SCFA/HCO3 exchange more than intracellular SCFA metabolism; 2) SCFA-dependent HCO3 secretion is most likely a result of an apical membrane SCFA/HCO3 exchange in surface epithelial cells; 3) SCFA downregulates Cldependent and cAMP-induced HCO 3 secretion secondary to SCFA inhibition of apical membrane Cl/HCO3 exchange and anion channel activity, respectively. Cl/HCO3 exchange; short-chain fatty acid/HCO3 exchange; anion channel; pH stat; colonic mucosa SHORT-CHAIN FATTY ACIDS (SCFA) are the primary anion in stool, are not normal dietary constituents, but are synthesized from nonabsorbed carbohydrates by colonic bacteria (5). Of the numerous SCFA, acetate, propionate, and butyrate have the highest fecal concentrations. Butyrate is often considered the most important because it is the principal colonocyte nutrient (33). Critical roles for SCFA have been identified in both health and disease, and SCFA have multiple effects on ion transport in colonocytes (6,10,18,20).In vivo perfusion of the colon with SCFA has been associated with HCO 3 secretion (1, 2, 34, 41). Although relatively little is known about the SCFA-dependent HCO 3 secretion, recent studies indicate that SCFA induce HCO 3 secretion via a Cl-independent, DIDS-insensitive process that probably involves an apical membrane SCFA/HCO 3 exchange (42). Because SCFA could stimulate HCO 3 secretion as a result of their membrane transport and/or metabolism, these initial studies were performed with a poorly metabolized SCFA, isobutyrat...

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H+ and HCO3- flux across apical surface of rat distal colon

Cited by 41 publications

References 17 publications

Segregation of Na/H exchanger-3 and Cl/HCO₃exchanger SLC26A3 (DRA) in rodent cecum and colon

Segregation of Na/H exchanger-3 and Cl/HCO₃exchanger SLC26A3 (DRA) in rodent cecum and colon

Chloride-dependent bicarbonate secretion in the mouse large intestine

Role of short-chain fatty acids in colonic HCO₃secretion

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H+ and HCO3- flux across apical surface of rat distal colon

Cited by 41 publications

References 17 publications

Segregation of Na/H exchanger-3 and Cl/HCO3exchanger SLC26A3 (DRA) in rodent cecum and colon

Segregation of Na/H exchanger-3 and Cl/HCO3exchanger SLC26A3 (DRA) in rodent cecum and colon

Chloride-dependent bicarbonate secretion in the mouse large intestine

Role of short-chain fatty acids in colonic HCO3secretion

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Segregation of Na/H exchanger-3 and Cl/HCO₃exchanger SLC26A3 (DRA) in rodent cecum and colon

Segregation of Na/H exchanger-3 and Cl/HCO₃exchanger SLC26A3 (DRA) in rodent cecum and colon

Role of short-chain fatty acids in colonic HCO₃secretion