Abstract
Inhibition of electroneutral NaCl absorption by cyclic adenosine monophosphate (cAMP) results in fluid malabsorption in cholera. Short-chain fatty acids (SCFA) stimulate electroneutral NaCl absorption from the colon. The present study investigated effects of elevated cAMP on SCFA-stimulated NaCl absorption in rat distal colon. The effect of SCFA on fluxes of 22Na and 36Cl was studied under voltage-clamp conditions, in the presence and absence of secretagogues inducing mucosal cAMP elevation [ie, theophylline, cholera toxin (CT) and forskolin]. The effect of butyrate concentration on Na absorption in CT- and theophylline-treated mucosa was compared with control normal mucosa. cAMP was measured in isolated colonocytes in the presence of secretagogues with and without SCFA using a radioassay method. All secretagogues were noted to inhibit net Na absorption and to induce net Cl secretion. In the presence of SCFA, net Na absorption was normal, and net Cl secretion was partly reversed. The flux data indicated that NaCl absorption from secreting colon was stimulated by SCFA and that Cl secretion was partially inhibited. The effects of SCFA on NaCl absorption were similar regardless of the secretagogue used. The kinetics of butyrate-stimulated Na absorption were altered by theophylline and CT, which decreased Km (6.87 and 7.17, respectively, compared to 10.75 mM for control) and increased Vmax (4.55 and 8.33 compared to 3.45 mM/eq/cm2/hr for control). cAMP production by colonocytes in response to secretory stimuli was significantly reduced (34.4%) by butyrate but not by acetate or propionate. In conclusion, SCFA-stimulated Na absorption is up-regulated by cAMP and may be an absorptive pathway that can be utilized in the therapy of cholera. Effects of butyrate on cAMP generation are also likely to be useful in secretory diarrhea.
MeSH Terms
Animals
Biological Transport/drug effects
Cholera Toxin/pharmacology
Colforsin/pharmacology
Colon/metabolism
Cyclic AMP/biosynthesis
Fatty Acids, Volatile/pharmacology
Intestinal Absorption/drug effects
Kinetics
Rats
Rats, Wistar
Sodium Chloride/pharmacokinetics
Theophylline/pharmacology
Chemicals
Fatty Acids, Volatile
Colforsin
Sodium Chloride
Cholera Toxin
Theophylline
Cyclic AMP
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Krishnan S
Department of Gastrointestinal Sciences, Christian Medical College Hospital, Vellore, India.
Ramakrishna B S
Binder H J
References (27)
27 references, click to expand
-
Glucose-stimulated sodium transport by the human intestine during experimental cholera.
Gastroenterology. 1997 May;112(5):1529-35
PMID: 9136831
-
Characterization of butyrate-dependent electroneutral Na-Cl absorption in the rat distal colon.
Pflugers Arch. 1990 Dec;417(4):365-9
PMID: 2080102
-
Apical membrane Cl-butyrate exchange: mechanism of short chain fatty acid stimulation of active chloride absorption in rat distal colon.
J Membr Biol. 1994 Jul;141(1):51-8
PMID: 7966245
-
Characterization of Na-H exchange in apical membrane vesicles of rat colon.
J Biol Chem. 1990 May 25;265(15):8408-14
PMID: 2160456
-
WATER AND ELECTROLYTE LOSSES IN CHOLERA.
Fed Proc. 1964 May-Jun;23:705-12
PMID: 14191978
-
Ion transport across the jejunum in normal and cystic fibrosis mice.
Am J Physiol. 1995 Mar;268(3 Pt 1):G505-13
PMID: 7534995
-
Short-chain fatty acids stimulate active sodium and chloride absorption in vitro in the rat distal colon.
Gastroenterology. 1989 Apr;96(4):989-96
PMID: 2925072
-
Diarrhoea: the failure of colonic salvage.
Lancet. 1982 Aug 28;2(8296):481-3
PMID: 6125648
-
Regulation by butyrate of the cAMP response to cholera toxin and forskolin in pituitary GH1 cells.
Eur J Biochem. 1990 Feb 14;187(3):683-9
PMID: 2154380
-
Organic substrate and electrolyte solutions for oral rehydration in diarrhea.
Annu Rev Nutr. 1994;14:321-42
PMID: 7946523
-
The effects of enterotoxins and short-chain fatty acids on water and electrolyte fluxes in ileal and colonic loops in vivo in the rat.
Digestion. 1990;45(2):93-101
PMID: 2190852
-
The treatment of cholera: clinical science at the bedside.
J Infect Dis. 1992 Jul;166(1):2-14
PMID: 1607698
-
Effect of short-chaim fatty acid on sodium absorption in isolated human colon perfused through the vascular bed.
Dig Dis Sci. 1981 Feb;26(2):100-6
PMID: 7460712
-
Mechanism of intestinal secretion: effect of cyclic AMP on rabbit ileal crypt and villus cells.
Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6249-53
PMID: 1648734
-
Colonic fluid handling in health & acute diarrhoeal diseases.
Indian J Med Res. 1996 Jul;104:52-9
PMID: 8783507
-
Colonic dysfunction in acute diarrhoea: the role of luminal short chain fatty acids.
Gut. 1993 Sep;34(9):1215-8
PMID: 8406157
-
Two major signal pathways linked.
Science. 1993 Nov 12;262(5136):988, 990
PMID: 8257559
-
Theophylline, cyclic AMP, choleragen, and electrolyte transport by rabbit ileum.
Am J Physiol. 1974 Dec;227(6):1428-35
PMID: 4374095
-
Short chain fatty acids in the human colon.
Gut. 1981 Sep;22(9):763-79
PMID: 7028579
-
Preparation of rat enterocyte mitochondria.
Biochem J. 1984 Mar 1;218(2):441-7
PMID: 6424661
-
Method of preparing isolated colonic epithelial cells (colonocytes) for metabolic studies.
Gut. 1979 Jun;20(6):484-8
PMID: 468074
-
Short-chain fatty acids inhibit cAMP-mediated chloride secretion in rat colon.
Am J Physiol. 1996 Dec;271(6 Pt 1):C1853-60
PMID: 8997185
-
Regulation by cAMP-dependent protein kinease of a G-protein-mediated phospholipase C.
Nature. 1996 Jul 4;382(6586):83-7
PMID: 8657310
-
Colonic dysfunction during cholera infection.
Gastroenterology. 1986 Nov;91(5):1164-70
PMID: 3758608
-
Mechanism of short-chain fatty acid uptake by apical membrane vesicles of rat distal colon.
Gastroenterology. 1991 Aug;101(2):331-8
PMID: 2065907
-
Emergence of Na+-glucose cotransport in an epithelial secretory cell line sensitive to cholera toxin.
Am J Physiol. 1989 Feb;256(2 Pt 1):G335-41
PMID: 2537580
-
Electrolyte transport across isolated large intestinal mucosa.
Am J Physiol. 1973 Nov;225(5):1232-9
PMID: 4745226