Abstract
The initial phase of in vitro experiments in Ussing-type chambers on large intestine is characterized by short-circuit currents (ISC) declining from high starting values to a lower plateau within 0.5 h. The origin of this “initial ISC-transient” was investigated by ISC measurements on partially stripped segments of rat rectal colon. Transport was pre-stimulated in vivo by keeping animals in barbiturateanesthesia for 5 h prior to tissue preparation. This procedure caused by endogenous aldosterone-liberation amiloride-sensitive Na-absorption to become the predominant electrogenic transport. The initial ISC-transient was abolished by tetrodotoxin (TTX, 1 μM), indicating a neuronal mediation of this phenomenon. In order to identify the transport which was subject to neuronal control, the amiloride-sensitive Na-absorption was measured during electrical field stimulation (bipolar rectangular pulses: 5 Hz, 1 ms, ±6 mA). There was no difference to unstimulated controls. In contrast, the initial ISC-transient was dependent on Cl in the bath following Michaelis-Menten-kinetics (K M=20 mM) and could be prevented by 10 μM serosal bumetanide. Then, initial filling of the Ussing-chamber was imitated during the course of the experiment by removal and immediate readdition of the bathing fluid. This procedure caused ISC-changes of similar appearance as the initial ISC-transient. To verify that indeed mechanical stretch is the sensory stimulus triggering the initial ISC-transient, the effect of small pressure oscillations was studied. This also produced an ISC-transient which was TTX-sensitive and was abolished after removal of the submucosal plexus Meissner by total stripping. It is concluded that amiloride-sensitive Na-absorption does not contribute to the initial transient and is not affected by the enteric nervous system. Initial ISC-transients asobserved during the first half hour of Ussing experiments are due to electrogenic Cl-secretion which is stimulated by mechanical stretch during tissue preparation and filling of the chamber via a submucosal neuronal reflex pathway. The possible biological meaning of this stretch-induced secretory process could be facilitation of transit during imminent stasis of the gut contents.
Similar content being viewed by others
Abbreviations
- EFS:
-
electrical field stimulation
- ENS:
-
enteric nervous sytem
- ISC:
-
short-circuit current
- R:
-
resistance
- TTX:
-
tetrodotoxin
References
Andres H, Bock R, Bridges RJ, Rummel W, Schreiner J (1985) Submucosal plexus and electrolyte transport across rat colonic mucosa. J Physiol 364:301–312
Beubler E, Juan H (1978) PGE-release, blood flow and transmucosal water movement after mechanical stimulation of the rat jejunal mucosa. Naunyn-Schmiedeberg's Arch Pharmacol 305:91–95
Binder HJ, Sandle GI (1987) Electrolyte absorption and secretion in the mammalian colon. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 2nd ed. Raven Press, New York, pp 1389–1418
Caren JF, Meyer JH, Grossman MI (1974) Canine intestinal secretion during and after rapid distention of the small bowel. Am J Physiol 227:183–188
Carey HV, Cooke HJ, Zafivora M (1985) Mucosal responses evoked by stimulation of ganglion cell somas in the submucosal plexus of the guinea-pig ileum. J Physiol 364:69–79
Cooke HJ, Shonnard K, Wood JD (1983) Effect of neuronal stimulation on mucosal transport in guinea pig ileum. Am J Physiol 245:G290-G296
Fromm M, Hegel U (1984) Aldosterone action in different segments of large intestine. In: Skadhauge E, Heintze K (eds) Intestinal absorption and secretion. MTP Press, Lancaster, pp 233–249
Fromm M, Oelkers W, Hegel U (1983) Time course of aldosterone and corticosterone plasma levels in rats during general anesthesia and abdominal surgery. Pflügers Arch 399:249–254
Greger R (1985) Ion transport mechanisms in thick ascending limb of Henle's loop of mammalian nephron. Physiol Rev 65:760–797
Haas M, McManus TJ (1983) Bumetanide inhibits (Na-K-2 Cl) co-transport at a chloride site. Am J Physiol 245:C235-C240
Harris MS, Kennedy JG (1988) Induction of neuronally-mediated NaHCO3-secretion by luminal distention in the rat ileum. Gastroenterology 94:A173
Heintze K, Stewart CP, Frizzell RA (1983) Sodium-dependent chloride secretion across rabbit descending colon. Am J Physiol 244:G357-G365
Hubel KA (1978) The effects of electrical field stimulation and tetrodotoxin on ion transport by the isolated rabbit ileum. J Clin Invest 62:1039–1047
Hubel KA, Renquist K, Shirazi S (1987) Ion transport in human caecum, transverse colon, and sigmoid colon in vitro. Gastroenterology 92:501–507
Kuwahara A, Bowen S, Wang J, Condon C, Cooke HJ (1987) Epithelial responses evoked by stimulation of submucosal neurons in guinea pig distal colon. Am J Physiol 252:G667-G674
Schulzke JD, Fromm M, Hegel U (1986) Epithelial and subepithelial resistance of rat large intestine: segmental differences, effects of stripping, time course, and action of aldosterone. Pflügers Arch 407:632–637
Schulzke JD, Fromm M, Menge H, Riecken E-O (1987) Impaired intestinal Na- and Cl-transport in the blind loop syndrome of the rat. Gastroenterology 92:693–698
Smith PL, McCabe RD (1984) A23187-induced changes in colonic K and Cl transport are mediated by separate mechanisms. Am J Physiol 247:G695-G702
Tai YH, Tai CY (1981) The conventional short-circuiting technique under-short-circuits most epithelia. J Membr Biol 59:173–177
Thompson SM, Suzuki Y, Schultz SG (1982) The electrophysiology of rabbit descending colon. J Membr Biol 66:41–54
White JF (1977) Alterations in electrophysiology of isolated amphibian small intestine produced by removing the muscle layers. Biochim Biophys Acta 467:91–102
Windmueller HG, Spaeth AE (1978) Identification of ketone bodies and glutamine as the major respiratory fuels in vivo for postabsorptive rat small intestine. J Biol Chem 253:69–76
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Schulzke, JD., Fromm, M., Hegel, U. et al. Ion transport and enteric nervous system (ENS) in rat rectal colon: Mechanical stretch causes electrogenic Cl-secretion via Plexus Meissner and amiloride-sensitive electrogenic Na-absorption is not affected by intramural neurons. Pflugers Arch. 414, 216–221 (1989). https://doi.org/10.1007/BF00580966
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00580966