Protective effects of an interaction between vagus nerve and melatonin on gastric ischemia/reperfusion: the role of oxidative stress

Document Type : Original Article

Authors

1 Physiology Research Center, Institute of Neuropharmacology, Kerman University of Medical Sciences, Kerman, Iran

2 Endocrinology and Metabolism Research Center, Institute of Basic and Clinical Physiology Sciences, Kerman University of Medical Sciences, Kerman, Iran

3 Urmia University of Medical Sciences, Urmia, Iran

4 School of Medicine, Kerman University of Medical Sciences, Kerman, Iran

5 Gastroenterology and Hepatology Research Center, Institute of Basic and Clinical Physiology Sciences, Dept. of Physiology, Faculty of Medicine, Kerman University of Medical Sciences, Kerman, Iran

6 Department of Biochemistry, Medical School of Afzalipour, Kerman University of Medical Sciences, Kerman, Iran

Abstract

Objectives:Vagal pathways in gastrointestinal tract are the most important pathways that regulate ischemia/reperfusion (I/R).  Gastrointestinal tract is one of the important sources of melatonin production. The aim of this study was to investigate probable protective effect of the interaction between vagus nerve and melatonin after I/R.
Materials and methods:This study was performed in male rats that were divided into six groups. Cervical vagus nerve was cut bilaterally after induction of I/R and the right one was stimulated by stimulator. Melatonin or vehicle was injected intraperitoneally. The stomach was removed for histopathological and biochemical investigations.
Results: A significant decrease in infiltration of gastric neutrophils and malondialdehyde (MDA) level after I/R was induced by melatonin and was disappeared after vagotomy. The stimulation of vagus nerve significantly enhanced these effects of melatonin. However, a stimulation of vagus nerve alone increased neutrophils infiltration and MDA level. Melatonin significantly increased the activities of catalase, glutathione peroxidase (GPx), superoxide dismutases (SOD). Unlike stimulation of vagus nerve, vagotomy decreased these effects of melatonin.
Conclusion:According to these results, it is probable that protective effects of melatonin after I/R may be mediated by vagus nerve. Therefore, there is an interaction between melatonin and vagus nerve in their protective effects.

Keywords

References

1. Brzozowski T, Konturek PC, Pajdo R, Kwiecień S, Sliwowski Z, Drozdowicz D, et al. Importance of brain-gut axis in the gastroprotection induced by gastric and remote preconditioning. J Physiol Pharmacol 2004; 55:165-177.
2. Tache Y. Brainstem neuropeptides and vagus protection of the gastric mucosal against injury: role of prostaglandins, nitric oxide and calcitonin-gene related peptide in capsaicin afferents. Curr Med Chem 2012; 19:35-42.
3. Rosas-Ballina M, Tracey KJ. Cholinergic control of inflammation. J Intern Med 2009; 265:663-679.
4. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000; 405:458-462.
5. Hamano R, Takahashi HK, Iwagaki H, Yoshino T, Nishibori M, Tanaka N. Stimulation of alpha7 nicotinic acetylcholine receptor inhibits CD14 and the toll-like receptor 4 expression in human monocytes. Shock 2006; 26:358-364.
6. Cho CH, Ogle CW, Dai S. Acute gastric ulcer formation in response to electrical vagus stimulation in rats. Eur J Pharmacol 1976; 35:215-219.
7. Donnelly JE, Hill JO, Jacobsen DJ, Hill JO, Sullivan DK, Johnson SL. Effects of a 16-month randomized controlled exercise trial on body weight and composition in young, overweight men and women: the Midwest Exercise Trial. Arch Intern Med 2003; 163:1343-1350.
8. Macchi MM, Bruce JN. Human pineal physiology and functional significance of melatonin. Front Neuroendocrinol 2004; 25:177-195.
9. Bubenik GA. Gastrointestinal melatonin: locali-zation, function, and clinical relevance. Dig Dis Sci 2002; 47:2336-2348.
10. Chen CQ, Fichna J, Bashashati M, Li YY, Storr M. Distribution, function and physiological role of melatonin in the lower gut. World J Gastroenterol 2011; 17:3888.
11. Reiter RJ, Tan DX, Osuna C, Gitto E. Actions of melatonin in the reduction of oxidative stress. A review. J Biomed Sci 2000; 7:444-458.
12. Kondoh T, Uneyama H, Nishino H, Torii K. Melatonin reduces cerebral edema formation caused by transient forebrain ischemia in rats. Life Sci 2002; 72:583-590.
13. Acuna-Castroviejo D, Martin M, Macias M,Escames G, León J, Khaldy H, M et al. Melatonin, mitochondria, and cellular bioenergetics. J Pineal Res 2001; 30:65-74.
14. Markus RP, Silva CL, Franco DG, Barbosa EM Jr, Ferreira ZS. Is modulation of nicotinic acetylcholine receptors by melatonin relevant for therapy with cholinergic drugs? Pharmacol Ther 2010; 126:251-262.
15. Kato K, Murai I, Asai S, Takahashi Y, Matsuno Y, Komuro S, et al. Central nervous system action of melatonin on gastric acid and pepsin secretion in pylorus-ligated rats. Neuroreport 1998; 9:3989-3992.
16. Jaworek J, Brzozowski T, Konturek SJ. Melatonin as an organoprotector in the stomach and the pancreas. J Pineal Res 2005; 38:73-83.
17. Abdelraheim SR, Okasha AM, Ghany HM, Ibrahim HM. Ghrelin gene expression in rats with ethanol-induced gastric ulcers: a role of melatonin. Endocr Regul 2015; 49:3-10.
18. Ozacmak VH, Sayan H, Arslan SO, Altaner S, Aktas RG. Protective effect of melatonin on contractile activity and oxidative injury induced by ischemia and reperfusion of rat ileum. Life Sci 2005; 76:1575-1588.
19. Fang Q, Chen G, Zhu W, Dong W, Wang Z Influence of melatonin on cerebrovascular proinflammatory mediators expression and oxidative stress following subarachnoid hemorrhage in rabbits. Mediators Inflamm 2009; 2009:426346.
20. Casao A, Cebrian I, Asumpcao ME, Pérez-Pé R, Abecia JA, Forcada F, et al. Seasonal variations of melatonin in ram seminal plasma are correlated to those of testosterone and antioxidant enzymes. Reprod Biol Endocrinol 2010; 8:59.
21. Nawrot-Porabka K, Jaworek J, Leja-Szpak A, Szklarczyk J, Kot M, Mitis-Musioł M, et al. Involvement of vagus nerves in the pancreatostimulatory effects of luminal melatonin, or its precursor L-tryptophan. Study in the rats. J Physiol Pharmacol 2007; 58:81-95.
22. Yamada H, Ogura A, Koizumi S, Yamaguchi A, Moriyama Y. Acetylcholine triggers L-glutamate exocytosis via nicotinic receptors and inhibits melatonin synthesis in rat pinealocytes. J Neurosci 1998; 18:4946-4952.
23. Kang YM, Lamb K, Gebhart GF, Bielefeldt K. Experimentally induced ulcers and gastric sensory-motor function in rats. Am J Physiol Gastrointest Liver Physiol 2005; 288:G284-291.
24. Nabavizadeh Rafsanjani F, Najafi A, Esmaily F. The effects of acute consumption of  heroin on basal and Vagus-Stimulated Gastric Acid and Pepsin Secretion in rat. IJMS؟ 2003; 28:190-194.
25. Kazez A, Demirbag M, Ustundag B, Ozercan IH, Sağlam M. The role of melatonin in prevention of intestinal ischemia-reperfusion injury in rats. J Pediatr Surg 2000; 35:1444-1448.
26. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95:351-358.
27. Konturek SJ, Konturek PC, Brzozowski T. Melatonin in gastroprotection against stress-induced acute gastric lesions and in healing of chronic gastric ulcers. J Physiol Pharmacol 2006; 57:51-66.
28. Beyer CE, Steketee JD, Saphier D. Antioxidant properties of melatonin--an emerging mystery. Biochem Pharmacol 1998; 56:1265-1272.
29. Zhang L, Gong JT, Zhang HQ, Song QH, Xu GH, Cai L, et al. Melatonin Attenuates Noise Stress-induced Gastrointestinal Motility Disorder and Gastric Stress Ulcer: Role of Gastrointestinal Hormones and Oxidative Stress in Rats. J Neurogastroenterol Motil 2015; 21:189-199.
30. Brzezinski A. Melatonin in humans. N Engl J Med 1997; 336:186-195.
31. Sener G, Sehirli AO, Satiroglu H, Keyer-Uysal M, Yeğen BC. Melatonin prevents oxidative kidney damage in a rat model of thermal injury. Life Sci 2002; 70:2977-2985.
32. Zhou XP, Zhang JF, Yan CD, Zhang YM. [Effects of electrical stimulation of lateral hypothalamic area on gastric ischemia-reperfusion injury in rats]. Sheng Li Xue Bao 2002; 54:435-440.
33. Johnson AG. Proximal gastric vagotomy: does it have a place in the future management of peptic ulcer? World J Surg 2000; 24:259-263.
34. Innes DL, Tansy MF. Gastric mucosal ulceration associated with electrochemical stimulation of the limbic brain. Brain Res Bull 1980; 1:33-36.
35. Tsibulevskii A TV, Petrenko Iu M [Change in various properties of catalase in the small intestine of
rats after vagotomy]. Patol Fiziol Eksp Ter 1992; 3:44-46.
36. Kutsuna S, Tsuruta R, Fujita M, Todani M, Yagi T, Ogino Y, et al. Cholinergic agonist physostigmine suppresses excessive superoxide anion radical generation in blood, oxidative stress, early inflammation, and endothelial injury in rats with forebrain ischemia/reperfusion. Brain Res 2010; 1313:242-249.
37. Ruan CJ, Li Z, Zhang L, Chen DH, Du GH, Sun L. et al. Protective effects of trans-2, 4-dimethoxystibene on cognitive, impairments induced by Abeta(25-35) in, hypercholesterolemic rats. Brain Res Bull 2010; 82:251-258.
38. Margaill I, Plotkine M, Lerouet D. Antioxidant strategies in the treatment of stroke. Free Radic Biol Med 2005; 39:429-443.
39. Flemstrom G, Sjoblom M. Epithelial cells and their neighbors. II. New perspectives on efferent signaling between brain, neuroendocrine cells, and gut epithelial cells. Am J Physiol Gastrointest Liver Physiol 2005; 289:G377-380.
40. Li JP, Chang TM, Chey WY. Roles of 5-HT receptors in the release and action of secretin on pancreatic secretion in rats. Am J Physiol Gastrointest Liver Physiol 2001; 280:G595-602.
41. Li Y. Sensory signal transduction in the vagus primary afferent neurons. Curr Med Chem 2007; 14:2554-2563.
42. Sjöblom M. The  duodenal  mucosal  bicarbonate  secretion. Ups J Med ci 2005; 110:115-119.

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