Abstract
Fluid and electrolyte absorption by colonic crypts depends on the transport properties of crypt cellular and paracellular routes and of the pericryptal sheath. As a low-Na+ diet increases aldosterone and angiotensin II secretion, either hormone could affect absorption. Control and adrenalectomized (ADX) Sprague-Dawley rats were kept at a high-NaCl (HS) diet and then switched to low-NaCl (LS) diet for 3 days. Aldosterone or angiotensin II plasma concentrations were maintained using implanted osmotic mini-pumps. The extracellular Na+ concentration in isolated rat distal colonic mucosa was determined by confocal microscopy using a low-affinity Na+-sensitive fluorescent dye (Sodium red, and Na+-insensitive BODIPY) bound to polystyrene beads. Crypt permeability to FITC-labelled dextran (10 kDa) was monitored by its rate of escape from the crypt lumen into the pericryptal space. Mucosal ion permeability was estimated by transepithelial electrical resistance (TER) and amiloride-sensitive short-circuit current (SCC). The epithelial Na+ channel, ENaC, was determined by immunolocalization. LS diet decreased crypt wall permeability to dextran by 10-fold and doubled TER. Following ADX, aldosterone decreased crypt wall dextran permeability, increased TER, increased Na+ accumulation in the pericryptal sheath and ENaC expression even in HS. Infusion of angiotensin II to ADX rats did not reverse the effects of aldosterone deprivation. These findings indicate that aldosterone alone is responsible for both the increase in Na+ absorption and the decreased paracellular and pericryptal sheath permeability.
Similar content being viewed by others
References
Abramoff M.D., Magelhaes P.J., Ram S.J. 2004. Image Processing with ImageJ. Biophotonics International 11:36–42
Asher C., Wald H., Rossier B.C., Garty H. 1996. Aldosterone-induced increase in the abundance of Na+ channel subunits. Am. J Physiol. 271:C605–C611
Barlet-Bas C., Khadouri C., Marsy S. Doucet A. 1988. Sodium-independent in vitro induction of Na+ K+-ATPase by aldosterone in renal target cells: permissive effect of triiodothyronine. Proc. Natl. Acad. Sci. USA 85:1707–1711
Campbell D.J., Habener J.F. 1986. Angiotensinogen gene is expressed and differentially regulated in multiple tissues of the rat. J. Clin. Invest. 78:31–39
Campbell S.E., Janicki J.S., Weber K.T. 1995. Temporal differences in fibroblast proliferation and phenotype expression in response to chronic administration of angiotensin II or aldosterone. J. Moll. Cell. Cardiol. 27:1545–1560
Colegio O.R., Van Itallie C., Rahner C., Anderson J.M. 2003. Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture. Am. J. Physiol. 284:C1346–C1354
Cristià E., Afzal I., Pérez-Bosque A., Amat C., Moretó M., Naftalin R.J. 2005. Pericryptal colon fibrosis induced by low sodium diets is mediated by aldosterone. J. Membrane Biol. 206:53–59
De los Rios A.D., Labajos M., Manteca A., Morell M., Souviron A. 1980. Stimulatory action of angiotensin II on water and electrolyte transport by the proximal colon of the rat. J. Endocrinol. 86:35–43
Dolman D., Edmonds C.J., Salas-Coll C. 1978. Effect of aldosterone on lithium permeability of rat colon mucosa. Experientia 34:1174–1175
Due C., Farman N., Canessa C., Bonvalet J., Rossier B.C. 1994. Cell-specific expression of epithelial sodium channel α,β, and γ subunits in aldosterone-responsive epithelia from the rat: localization y in situ hybridization and immunocytochemistry. J. Cell Biol. 127:1907–1921
Fardella C.E., Mosso L. 2002. Primary aldosteronism. Clin. Lab. 48:181–190
Fromm M., Hegel U. 1978. Segmental heterogeneity of epithelial transport in rat large intestine. Pfluegers Arch. 378:71–78
Fukushima K., Naito H., Funayama Y., Yonezawa H., Haneda S., Shibata C., Sasaki I. 2004. In vivo induction of prostasin mRNA in colonic epithelial cells by dietary sodium depletion and aldosterone infusion in rats. J. Gastroenterol. 39:940–947
Funder J.W., Pearce P.T., Smith R., Smith A.I. 1988. Mineralcorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science 242:583–585
Garty H., Benos D.J. 1988. Characteristics and regulatory mechanisms of the amiloride-blockable Na+ channel. Physiol. Rev. 68:309–373
Hirasawa K., Sato Y., Hosoda Y., Yamamoto T., Hanai H. 2002. Immunohistochemical localization of angiotensin II receptor and local renin-angiotensin system in human colonic mucosa. J. Histochem. Cytochem. 50:275–282
Horster M., Fabritius J., Buttner M., Maul R., Weekwerth P. 1994. Colonic-crypt-derived epithelia express induced ion transport differentiation in monolayer cultures on permeable matrix substrata. Pfluegers Arch 426:110–120
Jayaraman S., Song Y., Vetrivel L., Shankar L., Verkman A.S. 2001. Non-invasive fluorescence measurement of salt concentration in the airway surface liquid. J. Clin. Invest. 107:317–324
Klahr S., Morrissey J.J. 1997. Comparative study of ACE inhibitors and angiotensin II receptor antagonists in interstitial scarring. Kidney Int. Suppl. 63:S111–S114
Molteni A., Moulder J.E., Cohen E.F. 2000. Control of radiation-induced pneumopathy and lung fibrosis by angiotensin-converting enzyme inhibitors and an angiotensin II type 1 receptor blocker. Int. J. Radial Biol. 76:523–532
Naftalin R.J. 2004. Alterations in colonic barrier function caused by a low sodium diet or ionizing radiation. J. Environ. Pathol. Toxicol. Oncol. 23:79–97
Naftalin R.J., Pedley 1999. Regional crypt function in rat large intestine in relation to fluid absorption and growth of the pericryptal sheath. J. Physiol. 514:211–227
Naftalin R.J., Zammit P.S., Pedley K.C. 1999. Regional differences in rat large intestinal crypt function in relation to dehydrating capacity in vivo. J. Physiol. 514:201–210
Narikiyo T., Kitamura K., Adachi M., Miyoshi T., Iwashita K., Shiraishi N., Nonoguchi H., Chen L., Chai K.X., Chao J., Tomita K. 2002. Regulation of prostasin by aldosterone in the kidney. J. Clin. Invest. 109:401–408
Paul M., Wagner J., Dzau V.J. 1993. Gene expression of the renin-angiotensin system in human tissue. Quantitative analysis by the polymerase chain reaction. J. Clin. Invest. 91:2058–2064
Peart W.S. 1969. The renin-angiotensin system: a history and review of the renin-angiotensin system. Proc. R. Soc. Lond. B 173:317–325
Rasband, W.S. 1997–2005. Image J. U. S. National Institutes of Health, Bethesda, Maryland, USA, http://rsb.info.nih.gov/ij/
Schulzke J.D., Fromm M., Hegel U. 1986. Epithelial and subepithelial resistance of rat large intestine: segmental differences, effect of stripping, time course, and action of aldosterone. Pfluegers Arch. 407:632–637
Shlyonsky V., Goolaerts A., Van Beneden R., Sariban-Sohraby S. 2005. Differentiation of epithelial Na+ channel function. J. Biol. Chem. 280:24181–24187
Stanton B., Giebisch G., Klein-Robbenhaar G., DeFronzo R., Giebisch G. Wade J. 1985. Effects of adrenalectomy and chronic adrenal corticosteroid replacement on potassium transport in rat kidney. J. Clin Invest. 75:1317–1326
Swaney J.S., Roth D.M., Olson E.R., Naugle J.E., Meszaros J.G., Insel P.A. 2005. Inhibition of cardiac myofibroblast formation and collagen synthesis by activation and overexpression of adenylyl cyclase. Proc. Natl. Acad. Sci., USA 102:437–442
Thiagarajah J.R., Griffiths N.M., Pedley K.C., Naftalin R.J. 2002. Evidence for modulation of pericryptal sheath myofibroblasts in rat descending colon by transforming growth factor β and angiotensin II. Gastroenterology 2:4–15
Thiagarajah J.R., Jayaraman S., Naftalin R.J., Verkman A.S. 2001a. In vivo fluorescence measurement of Na+ concentration in the pericryptal space of mouse descending colon. Am. J. Physiol. 281:C1898–C1903
Thiagarajah J.R., Pedley K.C., Naftalin R.J. 2001b. Evidence of amiloride-sensitive fluid absorption in rat descending colonic crypts from fluorescence recovery of FITC-labeled dextran after photobleaching. J. Physiol. 536:541–553
Tsuruda T., Kato J., Cao Y.N., Hatakeyama K., Masuyama H., Imamura T., Kitamura K., Asada Y., Eto T. 2004. Adrenomedullin induces matrix metalloproteinase-2 activity in rat aortic adventitial fibroblasts. Biochem. Biophys. Res. Commun. 325:80–84
Tsuruda T., Kato J., Hatakeyama K., Masuyama H., Cao Y.N., Imamura T., Kitamura K., Asada Y., Eto T. 2005. Antifibrotic effect of adrenomedullin on coronary adventitia in angiotensin II-induced hypertensive rats. Cardiovasc. Res. 65:921–929
Weber K.T. 1997. Fibrosis, a common pathway to organ failure: angiotensin II and tissue repair. Semin. Nephrol. 17:467–491
Acknowledgement
This work was supported by projects BFI2003-05124 (Ministerio de Ciencia y Tecnología, Spain) and 2001SGR0142 (Generalitat de Catalunya, Spain) and the Wellcome Trust, UK. We are grateful to Dr. Carme Villà for plasma ion determinations and the support of the Confocal Service and the ICP-OES Service, Serveis Científicotècnics, Universitat de Barcelona. E.C. was recipient of a grant from MEC (Spain).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Moretó, M., Cristià, E., Pérez-Bosque, A. et al. Aldosterone Reduces Crypt Colon Permeability during Low-Sodium Adaptation. J Membrane Biol 206, 43–51 (2005). https://doi.org/10.1007/s00232-005-0772-5
Received:
Issue Date:
DOI: https://doi.org/10.1007/s00232-005-0772-5