Inhibition of Acetylcholine Induced Intestinal Motility by Interleukin 1 Beta in the Rat

Overview

Journal Gut

Specialty Gastroenterology

Date 1996 Sep 1

PMID 8949656

Citations 21

Authors

A C Aube

H M Blottiere

C Scarpignato

C Cherbut

C Roze

J P Galmiche

Affiliations

Soon will be listed here.

Abstract

Background/aims: The fact that raised interleukin 1 beta (IL 1 beta) concentrations have been found in the colonic mucosa of rats with experimentally induced colitis and of patients with inflammatory bowel disease indicates that this cytokine may participate in the disturbed intestinal motility seen during inflammatory bowel disease. This study investigated whether IL 1 beta could change the contractility of (a) a longitudinal muscle-myenteric plexus preparation from rat jejunum, ileum, and colon and (b) isolated jejunal smooth muscle cells.

Methods: Isometric mechanical activity of intestinal segments was recorded using a force transducer. Moreover, smooth muscle cell length was measured by image analysis.

Results: Although IL 1 beta did not affect jejunal, ileal, and colonic basal contractility, it significantly reduced contractile response to acetylcholine (ACh). This significant inhibition was seen only after 90 or 150 minutes of incubation with IL 1 beta. Pretreatment with cycloheximide blocked IL 1 beta induced inhibition of ACh stimulated jejunal contraction, suggesting that a newly synthesised protein was involved in the effect. NW-nitro-L-arginine (a nitric oxide synthase inhibitor) did not prevent the inhibition induced by IL 1 beta. Blocking neural transmission with tetrodotoxin abolished the IL 1 beta effect on jejunal contractile activity, whereas IL 1 beta had no effect on isolated and dispersed smooth muscle cells.

Conclusions: IL 1 beta inhibits ACh induced intestinal contraction and this inhibitory effect involves protein synthesis but is independent of nitric oxide synthesis. This effect does not involve a myogenic mechanism but is mediated through the myenteric plexus.

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References

Theodorou V, Eutamene H, Fioramonti J, Junien J, Bueno L . Interleukin 1 induces a neurally mediated colonic secretion in rats: involvement of mast cells and prostaglandins. Gastroenterology. 1994; 106(6):1493-500. DOI: 10.1016/0016-5085(94)90402-2. View

Montuschi P, Tringali G, Curro D, Ciabattoni G, Parente L, Preziosi P . Evidence that interleukin-1 beta and tumor necrosis factor inhibit gastric fundus motility via the 5-lipoxygenase pathway. Eur J Pharmacol. 1994; 252(3):253-60. DOI: 10.1016/0014-2999(94)90170-8. View

Woywodt A, Neustock P, Kruse A, Schwarting K, Ludwig D, Stange E . Cytokine expression in intestinal mucosal biopsies. In situ hybridisation of the mRNA for interleukin-1 beta, interleukin-6 and tumour necrosis factor-alpha in inflammatory bowel disease. Eur Cytokine Netw. 1994; 5(4):387-95. View

Khan I, Blennerhassett M, Kataeva G, Collins S . Interleukin 1 beta induces the expression of interleukin 6 in rat intestinal smooth muscle cells. Gastroenterology. 1995; 108(6):1720-8. DOI: 10.1016/0016-5085(95)90133-7. View

Palmer J, Koch T . Altered neuropeptide content and cholinergic enzymatic activity in the inflamed guinea pig jejunum during parasitism. Neuropeptides. 1995; 28(5):287-97. DOI: 10.1016/0143-4179(95)90045-4. View

Cherbut C, Aube A, Blottiere H, Pacaud P, Scarpignato C, Galmiche J . In vitro contractile effects of short chain fatty acids in the rat terminal ileum. Gut. 1996; 38(1):53-8. PMC: 1382979. DOI: 10.1136/gut.38.1.53. View

Bitar K, Zfass A, Makhlouf G . Interaction of acetylcholine and cholecystokinin with dispersed smooth muscle cells. Am J Physiol. 1979; 237(2):E172-6. DOI: 10.1152/ajpendo.1979.237.2.E172. View

Dinarello C . Interleukin-1. Dig Dis Sci. 1988; 33(3 Suppl):25S-35S. DOI: 10.1007/BF01538128. View

Beasley D, Cohen R, LEVINSKY N . Interleukin 1 inhibits contraction of vascular smooth muscle. J Clin Invest. 1989; 83(1):331-5. PMC: 303680. DOI: 10.1172/JCI113879. View

10.

Mahida Y, Wu K, Jewell D . Enhanced production of interleukin 1-beta by mononuclear cells isolated from mucosa with active ulcerative colitis of Crohn's disease. Gut. 1989; 30(6):835-8. PMC: 1434123. DOI: 10.1136/gut.30.6.835. View

11.

Scarpignato C, Cartella A, Zappia L . Effect of cimetropium bromide and other antispasmodic compounds on in vitro guinea-pig gallbladder. Methods Find Exp Clin Pharmacol. 1989; 11(5):323-9. View

12.

Loppnow H, Libby P . Proliferating or interleukin 1-activated human vascular smooth muscle cells secrete copious interleukin 6. J Clin Invest. 1990; 85(3):731-8. PMC: 296489. DOI: 10.1172/JCI114498. View

13.

Ikejima T, Okusawa S, Ghezzi P, van der Meer J, Dinarello C . Interleukin-1 induces tumor necrosis factor (TNF) in human peripheral blood mononuclear cells in vitro and a circulating TNF-like activity in rabbits. J Infect Dis. 1990; 162(1):215-23. DOI: 10.1093/infdis/162.1.215. View

14.

Ligumsky M, Simon P, Karmeli F, Rachmilewitz D . Role of interleukin 1 in inflammatory bowel disease--enhanced production during active disease. Gut. 1990; 31(6):686-9. PMC: 1378497. DOI: 10.1136/gut.31.6.686. View

15.

Fleming I, Gray G, Parratt J, STOCLET J . Incubation with endotoxin activates the L-arginine pathway in vascular tissue. Biochem Biophys Res Commun. 1990; 171(2):562-8. DOI: 10.1016/0006-291x(90)91183-s. View

16.

Bredt D, Hwang P, Snyder S . Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature. 1990; 347(6295):768-70. DOI: 10.1038/347768a0. View

17.

Vermillion D, Ernst P, Collins S . T-lymphocyte modulation of intestinal muscle function in the Trichinella-infected rat. Gastroenterology. 1991; 101(1):31-8. DOI: 10.1016/0016-5085(91)90456-u. View

18.

Sawada M, Hara N, Maeno T . Ionic mechanism of the outward current induced by extracellular ejection of interleukin-1 onto identified neurons of Aplysia. Brain Res. 1991; 545(1-2):248-56. DOI: 10.1016/0006-8993(91)91293-a. View

19.

Shibata M, Blatteis C . Differential effects of cytokines on thermosensitive neurons in guinea pig preoptic area slices. Am J Physiol. 1991; 261(5 Pt 2):R1096-103. DOI: 10.1152/ajpregu.1991.261.5.R1096. View

20.

Xin L, Blatteis C . Blockade by interleukin-1 receptor antagonist of IL-1 beta-induced neuronal activity in guinea pig preoptic area slices. Brain Res. 1992; 569(2):348-52. DOI: 10.1016/0006-8993(92)90650-x. View