Summary
Eicosanoids are involved in the mediation of inflammatory and allergic processes in the gut. In order to evaluate a potential beneficial effect of the diet, the effect of mediators of inflammation and of a sensitization against egg albumin on anion secretion across the colon was tested using rats fed on a diet containing 15 % fish oil as compared to 15 % olive oil as donor animals.
Feeding on a fish oil diet significantly reduced the response to bradykinin or phospholipase C, known agonists of prostaglandin-induced secretion, by about 50 %. The increase in short-circuit current (Isc) induced by the phospholipase A2 stimulator, melittin, or by distension of the gut wall were only insignificantly inhibited by 15–30 %. Administration of egg albumin to the mucosas from animals sensitized against egg albumin induced an indomethacin- and tetrodotoxin-sensitive increase in Isc. This response was, however, only insignificantly (30 %) reduced by the fish oil diet.
In conclusion, the effect of fish oil diet depends on the stimulus used for activation of prostaglandin release. This suggested that different pools of arachidonic acid are differentially affected by the diet or that certain stimuli for phospholipases are strong enough to overcome the effect of a reduced substrate availability. Consequently, a diet rich in polyunsaturated n-3 fatty acids may only play an adjuvant role for the therapy of inflammatory or allergic intestinal diseases.
Zusammenfassung
Eicosanoide sind an der Entstehung entzündlicher und allergischer Darmerkrankungen beteiligt. Um die Möglichkeit einer diätetischen Beeinflussung dieser Erkrankungen zu untersuchen, wurde die sekretorische Wirkung verschiedener Entzündungsmediatoren und einer Sensibilisierung gegen Hühnereialbumin am Kolon von Ratten in vitro getestet, die eine Diät mit 15 % Fischöl erhielten. Als Kontrolle dienten Ratten, die eine Diät mit 15 % Olivenöl erhielten.
Die Fütterung mit der Fischöldiät hemmte signifikant die prostaglandinvermittelte Sekretion, die durch Bradykinin oder Phospholipase C hervorgerufen wurde, um circa 50 %. Der Anstieg des Kurzschlußstroms (Isc), der durch Melittin, einem Stimulator der Phospholipase A2, oder Dehnung der Darmwand induziert wurde, war dagegen nur geringfügig (um 15–30 %; nicht signifikant) vermindert. Zugabe von Hühnereialbumin zu den Schleimhautpräparaten von Tieren, die gegen dieses Protein sensibilisiert worden waren, rief einen Indomethacin-und Tetrodotoxin-sensitiven Anstieg des Isc hervor. Auch diese Antwort wurde nur in nicht signifikantem Ausmaß (30 %) durch die Fischöldiät vermindert.
Diese Ergebnisse legen den Schluß nahe, daß die Wirkung einer Fischöldiät von der Art des Stimulus abhängig ist, der die Prostaglandinsynthese anregt. Dies weist möglicherweise auf die Existenz verschiedener Arachidonsäurepools hin, die von verschiedenen Stimuli aktiviert und unterschiedlich durch die Diät beeinflußt werden. Dementsprechend kommt einer Diät mit n-3-mehrfach ungesättigten Fettsäuren höchstens eine Rolle als Adjuvans bei der Therapie entzündlicher oder allergischer Darmerkrankungen zu.
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Abbreviations
- Isc :
-
Short circuit current
- Gt :
-
tissue conductance
- PLC :
-
phospholipase C
- SEM :
-
standard error of the mean
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
Baird AW, Cuthbert AW, Pearce FL (1985) Immediate hypersensitivity reactions in epithelia from rats infected with Nippostrongylus brasiliensis. Br J Pharmacol 85:787–795
Bartram HP, Gostner A, Scheppach W, Reddy BS, Rao CV, Dusel G, Richter F, Richter A, Kasper H (1989) Effects of fish oil on rectal proliferation, mucosal fatty acids, and prostaglandin E2 release in healthy subjects. Gastroenterology 105:1317–1322
Bloom FE (1990) Neurohumoral transmission and the central nervous system. In: Gilman GA, Rall TW, Nies AS, Taylor P (eds) The pharmacological basis of therapeutics. 8. ed., Pergamon Press, New York, pp 244–268
Campbell WB (1990) Eicosanoids and platelet-activating factor. In: Gilman GA, Rall TW, Nies AS, Taylor P (eds) The pharmacological basis of therapeutics. 8. ed., Pergamon Press, New York, pp 600–617
Cartwright-Shamoon JM, Dodge JA, McMaster C (1995) A complex biochemical modulation of intestinal ion transport in rats fed on high-fat diets. J Ped Gastroenterol Nutr 20:36–43
Castro GA, Harari Y, Russell D (1987) Mediators of anaphylaxis-induced ion transport changes in small intestine. Am J Physiol 253:G540-G548
Castro GA, Powell DW (1994) Immune system and immune-mediated responses in the gastrointestinal tract. In: Johnson LR (ed) Physiology of the gastrointestinal tract. 2. ed., Raven Press, New York, pp 709–750
Catterall WA (1980) Neurotoxins that act on voltage-sensitive sodium channels in excitable membranes. Ann Rev Pharmacol Toxicol 20:15–43
Craven PA, DeRubertis FR (1983) Patterns of prostaglandin synthesis and degradation in isolated superficial and proliferative colonic epithelial cells compared to residual colon. Prostaglandins 26:583–604
Crowe SE, Sestini P, Perdue MH (1990) Allergic reactions of rat jejunal mucosa. Ion transport responses to luminal antigen and inflammatory mediators. Gastroenterology 99:74–82
Cuthbert AW, Margolius HS (1982) Kinins stimulate net chloride secretion by the rat colon. Br J Pharmacol 75:587–589
Diener M, Bridges RJ, Knobloch SF, Rummel W (1988) Indirect effects of bradykinin on ion transport in rat colon descendens: Mediated by prostaglandins and enteric neurons. Naunyn-Schmiedeberg's Arch Pharmacol 337:69–73
Diener M, Bridges RJ, Knobloch SF, Rummel W (1988) Neuronally mediated and direct effects of prostaglandins on ion transport in rat colon descendens. Naunyn-Schmiedeberg's Arch Pharmacol 337:74–78
Diener M, Eglème C, Rummel W (1991) Phospholipase C-induced anion secretion and its interaction with carbachol in the rat colonic mucosa. Eur J Pharmacol 200:267–276
Diener M, Rummel W (1990) Distension-induced secretion in the rat colon: mediation by prostaglandins and submucosal neurons. Eur J Pharmacol 178:47–57
Diener M, Rummel W (1991) Phospholipase A2 and mediation of the activation of short-circuit current in the rat colonic mucosa. Naunyn-Schmiedeberg's Arch Pharmacol 343:652–658
Endres S, Ghorbani R, Kelley VE, Georgilis K, Lonnemann G, Van der Meer JWM, Cannon JG, Rogers TS, Klempner MS, Weber PC, Schaefer EJ, Wolff SM, Dinarello CA (1989) The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N Engl J Med 320:265–271
Frieling T, Cooke HJ, Wood JD (1994) Neuroimmune communication in the submucous plexus of guinea pig colon after sensitization to milk antigen. Am J Physiol 267:G1087-G1093
Gaginella TS, Kachur JF (1989) Kinins as mediators of intestinal secretion. Am J Physiol 256:G1-G15
Habermann E (1957) Manometrische Bestimmung von Phospholipase A. Biochem Z 328:474–484
Javed NH, Wang YZ, Cooke HJ (1992) Neuroimmune interactions: Role for cholinergic neurons in intestinal anaphylaxis. Am J Physiol 263:G847-G852
Kenakin TP (1987) Pharmacologic analysis of drug-receptor interaction. Raven Press, New York, pp 129–162
Lauritsen K, Laursen LS, Bukhave K, Rask-Madesn J (1988) In vivo profiles of eicosanoids in ulcerative colitis, Crohn's disease, and clostridium difficile colitis. Gastroenterology 95:11–17
Lee TH, Hoover RL, Williams JD, Sperling RI, Ravalese J, Spur BW, Robinson DR, Corey EJ, Lewis RA, Austen KF (1985) Effect of dietary enrichment with eicosapentaenoic acid and docosahexaenoic acid on in vitro neutrophil and monocyte leukotriene generation and neutrophil function. N Engl J Med 312:1217–1224
Lehtonen JYA, Kinnunen PKJ (1995) Phospholipase A2 as a mechanosensor. Biophys J 68:1888–1894
Lindström CC, Rosengreen JE, Fork FT (1979) Colon of the rat. An anatomic, histologic and radiographic investigation. Acta Radiol Diagn 20:523–536
MacGregor IL, Lavigné ME (1979) Inhibition by indomethacin of intestinal distension induced secretion in the rat. J Surg Res 26:167–170
Mæehle L, Eilertsen E, Mollerup S, Schønberg S, Krokan HE, Haugen A (1995) Effects of n-3 fatty acids during neoplastic progression and comparison of in vitro and in vivo sensitivity of two human tumour cell lines. Br J Cancer 71:691–696
Mollay C, Kreil G (1973) Fluorometric measurements on the interaction of melittin with lecithin. Biochim Biophys Acta 316:196–203
Perdue MH, Gall DG (1986) Intestinal anaphylaxis in the rat: jeujunal response to in vitro antigen exposure. Am J Physiol 250:G427-G431
Shahar E, Folsom AR, Wu KK, Dennis BH, Shimakawa T, Conlan MG, Davis CE, Williams OD (1989) Associations of fish intake and dietary n-3 polyunsaturated fatty acids with a hypocoagulable profile. The atherosclerosis risk in communities (ARIC) study. Arterioscler Thromb 13:1205–1212
Sharon P, Stenson WF (1985) Metabolism of arachidonic acid in acetic acid colitis in rats. Similarity to human inflammatory bowel disease. Gastroenterology 88:55–63
Van den Bosch (1982) Phospholipases. In: Hawthorne JN, Ansell GB (eds) Phospholipids. Elsevier, Amsterdam, pp 313–357
Wang YZ, Palmer JM, Cooke HJ (1991) Neuroimmune regulation of colonic secretion in guinea pig. Am J Physiol 260:G307-G314
Weaver BJ, Holob BJ (1988) Health effects and metabolism of dietary eicosapentaenoic acid. Progr Food Nutr Sci 12:111–150
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Hug, F., Diener, M. & Scharrer, E. Modulation by fish oil diet of eicosanoid-induced anion secretion in the rat distal colon. Z Ernährungswiss 35, 323–331 (1996). https://doi.org/10.1007/BF01610550
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DOI: https://doi.org/10.1007/BF01610550