Lipid peroxidation, reactive oxygen species and antioxidative factors in the pathogenesis of gastric mucosal lesions and mechanism of protection against oxidative stress - induced gastric injury

Journal of Physiology and Pharmacology

Volumn 65, Issue 5, 2014, Pages 613-622

  Kwiecien, Slawomir ^a   Jasnos, K ^a   Magierowski, M ^a   Sliwowski, Z ^a   Pajdo, R ^a   Brzozowski, B ^a   Mach, T ^a   Wojcik, D ^a   Brzozowski, T ^a  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

Author keywords

Gastric mucosa; Glutathione; Lipid peroxidation; Malondialdehyde; Peroxynitrite; Reactive oxygen species; Superoxide dismutase

Indexed keywords

4 HYDROXYNONENAL; ARGININE; FREE RADICAL; GLUTATHIONE; HYDROGEN PEROXIDE; MALONALDEHYDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXYNITRITE; POLYUNSATURATED FATTY ACID; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE); REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANTIOXIDANT ASSAY; CELL FUNCTION; ENZYME ACTIVITY; HUMAN; LIPID PEROXIDATION; MICROCIRCULATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PHYSIOLOGY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STOMACH BLOOD FLOW; STOMACH MUCOSA; STOMACH MUCOSA INJURY; ANIMAL; INJURIES; METABOLISM;

ANIMALS; GASTRIC MUCOSA; GLUTATHIONE; HUMANS; LIPID PEROXIDATION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84908402652     PISSN: 08675910     EISSN: 18991505     Source Type: Journal    
DOI: None     Document Type: Review

References (76)

1. Laine L, Takeuchi K, Tarnawski A. Gastric mucosal defense and cytoprotection: bench to bedside. Gastroenterology 2008; 135: 41-60.
2. Tarnawski A, Ahluwalia A, Jones MK. Gastric cytoprotection beyond prostaglandins: cellular and molecular mechanisms of gastroprotective and ulcer healing actions of antacids. Curr Pharm Des 2013; 19: 126-132.
3. deFoneska A, Kaunitz JD. Gastroduodenal mucosal defense. Curr Opin Gastroenterol 2010; 26: 604-610.
4. Brzozowski T, Konturek PC, Konturek SJ, Brzozowska I, Pawlik T. Role of prostaglandins in gastroprotection and gastric adaptation. J Physiol Pharmacol 2005; 56 (Suppl. 5): 33-55.
5. Whittle BJR, Lopez Belmonte J, Moncada S. Regulation of gastric mucosal integrity by endogenous nitric oxide, interactions with prostanoids and sensory neuropeptides in the rat. Br J Pharmacol 1990; 99: 607-611.
6. Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn't the stomach digest itself? Physiol Rev 2008; 88: 1547-1565.
7. Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 1991; 43: 109-142.
8. Brzozowski T, Konturek PC, Pajdo R, et al. Physiological mediators in nonsteroidal anti-inflammatory drugs (NSAIDs)-induced impairment of gastric mucosal defense and adaptation. Focus on nitric oxide and lipoxins. J Physiol Pharmacol 2008; 59 (Suppl. 2): 89-102.
9. Kwiecien S, Pawlik MW, Brzozowski T, et al. Nitric oxide (NO)-releasing aspirin and (NO) donors in protection of gastric mucosa against stress. J Physiol Pharmacol 2008; 59 (Suppl. 2): 103-115.
10. Kwiecien S, Brzozowski T, Konturek PC, et al. The role of reactive oxygen species and capsaicin-sensitive sensory nerves in the pathomechanisms of gastric ulcers induced by stress. J Physiol Pharmacol 2003; 54: 423-437.
11. Ishii K, Chang B, Kerwin JF, Huang ZJ, Murad F. N-nitro-Larginine a potent inhibitor of endothelium-derived relaxing factor formation. Eur J Pharmacol 1990; 176: 219-223.
12. Kwiecien S, Ptak-Belowska A, Krzysiek-Maczka G, et al.: Asymmetric dimethylarginine, an endogenous inhibitor of nitric oxide synthase, interacts with gastric oxidative metabolism and enhances stress-induced gastric lesions. J Physiol Pharmacol 2012; 63: 515-524.
13. Kwiecien S, Konturek PC, Sliwowski Z, et al. Interaction between selective cyclooxygenase inhibitors and capsaicinsensitive afferent sensory nerves in pathogenesis of stressinduced gastric lesions. Role of oxidative stress. J Physiol Pharmacol 2012; 63: 143-151.
14. Szlachcic A, Krzysiek Maczka G, Pajdo R, et al. The impact of asymmetric dimethylarginine (ADAMA), the endogenous nitric oxide (NO) synthase inhibitor, to the pathogenesis of gastric mucosal damage. Curr Pharm Des 2013; 19: 90-97.
15. Szlachcic A, Sliwowski Z, Krzysiek-Maczka G, et al. New satiety hormone nesfatin-1 protects gastric mucosa against stress injury. Mechanistic roles of prostaglandins, nitric oxide, sensory nerves and vanilloid receptors. Peptides 2013; 49: 9-20.
16. Holzer P. Acid sensing by visceral afferent neurones. Acta Physiol (Oxf) 2011; 201: 63-75.
17. Ohno T, Hattori Y, Komine R, et al. Roles of calcitonin generelated peptide in maintenance of gastric mucosal integrity and in enhancement of ulcer healing and angiogenesis. Gastroenterology 2008; 134: 215-225.
18. Brzozowska I, Konturek PC, Brzozowski T, et al. Role of prostaglandins, nitric oxide, sensory nerves and gastrin in acceleration of ulcer healing by melatonin and its precursor, L-tryptophan. J Pineal Res 2002; 32: 149-162.
19. Tache Y. Brainstem neuropeptides and vagal 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.
20. Takeuchi K. Pathogenesis of NSAID-induced gastric damage: importance of cyclooxygenase inhibition and gastric hypermotility. World J Gastroenterol 2012; 18: 2147-2160.
21. Brzozowski T, Konturek PC, Konturek SJ, et al. Ischemic preconditioning of remote organs attenuates gastric ischemiareperfusion injury through involvement of prostaglandins and sensory nerves. Eur J Pharmacol 2004; 499: 201-213.
22. Brzozowski T, Konturek PC, Moran AP, et al. Involvement of capsaicin-sensitive afferent nerves and cholecystokinin 2/gastrin receptors in gastroprotection and adaptation of gastric mucosa to Helicobacter pylori-lipopolysaccharide. J Pharmacol Exp Ther 2004; 310: 116-125.
23. Brzozowski T. Nonsteroidal anti-inflammatory drug-induced experimental gastropathy: is gastric acid the major trigger? Clin Exp Pharm Physiol 2010; 37: 651-653.
24. Lai LH, Chan FK. Nonsteroid anti-inflammatory druginduced gastroduodenal injury. Curr Opin Gastroenterol 2009; 25: 544-548.
25. Park SH, Hong H, Han YM, et al. Non-steroidal antiinflammatory drugs (NSAID) sparing effects of glucosamine hydrochloride through N-glycosylation inhibition; strategy to rescue stomach from NSAID damage. J Physiol Pharmacol 2013; 64: 157-165.
26. Konturek PC, Brzozowski T, Ptak A, et al. Nitric oxide releasing aspirin protects the gastric mucosa against stress and promotes healing of stress-induced gastric mucosal damage: role of heat shock protein 70. Digestion 2002; 66: 160-172.
27. Nemmani KV, Mali SV, Borhade N, et al. NO-NSAIDs: gastric-sparing nitric oxide-releasable prodrugs of nonsteroidal anti-inflammatory drugs. Bioorg Med Chem Lett 2009; 19: 5297-5301.
28. Kwiecien S, Pawlik MW, Brzozowska I, et al. Effect of vasodilators on lipid peroxidation and antioxidative mechanisms in gastric mucosa. Clin Exp Med Lett 2005; 46: 33-38.
29. Yucel AF, Kanter M, Pergel A, Erboga M, Guzel A. The role of curcumin on intestinal oxidative stress, cell proliferation and apoptosis after ischemia/reperfusion injury in rats. J Mol Histol 2011; 42: 579-587.
30. Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE. Oxidative stress: an essential factor in pathogenesis of gastrointestinal mucosal diseases. Physiol Rev 2014; 94: 329-354.
31. Bandyopadhyay D, Chattopadhyay A. Reactive oxygen species-induced gastric ulceration: protection by melatonin. Curr Med Chem 2006; 13: 1187-1202.
32. Kourie JI. Interaction of reactive oxygen species with ion transport mechanisms. Am J Physiol 1998; 275: C1-C24.
33. Kwiecien S, Pawlik MW, Brzozowski T, Pawlik WW, Konturek SJ. Reactive oxygen metabolite action in experimental, stress model of gastric mucosa damage. Gastroenterol Pol 2010; 17: 234-243.
34. Naito Y, Yoshikawa T. Oxidative stress involvement and gene expression in indomethacin-induced gastropathy. Redox Rep 2006; 11: 243-253.
35. Cacanyiova S, Dovinova F, Kristek F. The role of oxidative stress in acetylocholine-induced relaxation of endotheliumdenuded arteries. J Physiol Pharmacol 2013; 64: 241-247.
36. Vucevic D, Mladenovic D, Ninkovic M, et al. Influence of aging on ethanol-induced oxidative stress in digestive tract of rats. Hum Exp Toxicol 2013; 32: 698-705.
37. Targosz A, Brzozowski T, Pierzchalski P, et al. Helicobacter pylori promotes apoptosis, activates cyclooxygenase (COX)-2 and inhibits heat shock protein HSP70 in gastric cancer epithelial cells. Inflamm Res 2012; 61: 955-966.
38. Misra MK, Sarwat M, Bhakuni P, Tuteja R, Tuteja N. Oxidative stress and ischemic myocardial syndromes. Med Sci Monit 2009; 15: RA209-RA219.
39. Nagano Y, Matsui H, Shimokawa O, et al. Biphosphonateinduced gastrointestinal mucosal injury is mediated by mitochondrial superoxide production and lipid peroxidation. J Clin Biochem Nutr 2012; 51: 196-203.
40. Kasazaki K., Yasukawa K, Sano H, Utsumi H. Non-invasive analysis of reactive oxygen species generated in NH4OHinduced gastric lesions of rats using a 300 MHz in vivo ESR technique. Free Radic Res 2003; 37: 757-766.
41. Zhang JY, Wu QF, Wan Y, et al. Protective role of hydrogenrich water on aspirin-induced gastric mucosal damage in rats. World J Gastroenterol 2014; 20: 1614-1622.
42. Yasukawa K, Kasazaki K, Hyodo F, Utsumi H. Non-invasive analysis of reactive oxygen species generated in rats with water immersion restraint-induced gastric lesions using in vivo electron spin resonance spectroscopy. Free Radic Res 2004; 38: 147-155.
43. Konturek PC, Duda A, Brzozowski T, et al. Activation of genes for superoxide dismutase, interleukin-1, tumor necrosis factor-a and intercellular adhesion molecule-1 during healing of ischemia-reperfusion gastric injury. Scand J Gastroenterol 2000; 35, 452-463.
44. Nagano Y, Matsui H, Shimokawa O, et al. Rebamipide attenuates nonsteroidal anti-inflammatory drugs (NSAID) induced lipid peroxidation by manganese superoxide dismutase (MnSOD) overexpression in gastrointestinal epithelial cells. J Physiol Pharmacol 2012; 63: 137-142.
45. Mei X, Xu D, Xu S, Zheng Y, Xu S. Novel role of Zn(II)- curcumin in enhancing cell proliferation and adjusting proinflammatory cytokine-mediated oxidative damage of ethanol-induced acute gastric ulcers. Chem Biol Interact 2012; 197: 31-39.
46. Lorrain B, Dangles O, Loonis M, Armand M, Dufour C. Dietary iron - initiated lipid oxidation and its inhibition by polyphenols in gastric conditions. J Agric Food Chem 2012; 60: 9074-9081.
47. Kwiecien S, Brzozowski T, Konturek SJ. Importance of aldehyde products of lipid peroxidation in the formation of gastric lesions induced by aspirin, ischemia-reperfusion and stress. Gastroenterol Pol 2002; 9: 273-280.
48. Matsuda T, Tao H, Goto M, et al. Lipid peroxidation-induced DNA adducts in human gastric mucosa. Carcinogenesis 2013; 34: 121-127.
49. Getzoff ED, Tainer JA, Weiner PK, Kollman PA, Richardson JS, Richardson DC. Electrostatic recognition between superoxide and copper, zinc superoxide dismutase. Nature 1983; 306: 287-290.
50. Farkas R, Selmeci L, Tulassay Z, Pronai L. Superoxide dismutase activity of the gastric mucosa in patients with Helicobacter pylori infection. Anticancer Res 2003; 23: 4309-4312.
51. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991; 11: 81-128.
52. Dianzani MU. 4-hydroxynonenal from pathology to physiology. Mol Aspects Med 2003; 24: 263-272.
53. Awasthi YC, Sharma R, Cheng JZ, et al. Role of 4- hydroxynonenal in stress-mediated apoptosis signaling. Mol Aspects Med 2003; 24: 219-230.
54. Adamczyk-Sowa M, Sowa P, Pierzchala K, Polaniak R, Labuz-Roszak B. Antioxidative enzymes activity and malondialdehyde concentration during mitoxantrone therapy in multiple sclerosis patients. J Physiol Pharmacol 2012; 63: 683-690.
55. Tamura M, Matsui YN, Nagano T, et al. Salt is an oxidative stressor for gastric epithelial cells. J Physiol Pharmacol 2013; 64: 89-94.
56. Min SY, Kim HS, Jung EJ, Jung EJ, Jee CD, Kim WH. Prognostic significance of glutathione peroxidase 1 (GPX1) down-regulation and correlation with aberrant promoter methylation in human gastric cancer. Anticancer Res 2012; 32: 3169-3175.
57. Korbut E, Ptak-Belowska A, Brzozowski T. Mechanisms promoting physiological cells progression into tumorigenesis. J Physiol Pharmacol 2012; 63: 565-570.
58. Amstad P, Moret R, Ceruti P. Glutathione peroxidase compensates for the hypersensivity of Cu,Zn-superoxide dismutase overproducers to oxidant stress. J Biol Chem 1994; 269: 1606-1609.
59. Ertug PU, Aydinoglu F, Goruroglu Ozturk O, Singirik E, Ogulener N. Comparative study of the quercetin, ascorbic acid, glutathione and superoxide dismutase for nitric oxide protecting effects in mouse gastric fundus. Eur J Pharmacol 2013; 698: 379-387.
60. Liu L, Cui J, Song CJ, et al. H2S-releasing aspirin protects against aspirin-induced gastric injury via reducing oxidative stress. PLoS One 2012; 7: e46301.
61. Winterbourn CC. Superoxide as an intracellular radical sink. Free Radic Biol Med 1993; 14: 85-90.
62. Koppenol WH. A thermodynamic appraisal of the radical sink hypothesis. Free Radic Biol Med 1993; 14: 91-94.
63. Brzozowski T, Konturek PC, Drozdowicz D, et al. Grapefruit-seed extract attenuates ethanol- and stressinduced gastric lesions via activation of prostaglandin, nitric oxide and sensory nerve pathways. World J Gastroenterol 2005; 11: 6450-6458.
64. Brzozowski T, Konturek PC, Sliwowski Z, et al. Prostaglandin/cyclooxygenase pathway in ghrelin-induced gastroprotection against ischemia-reperfusion injury. J Pharmacol Exp Ther 2006; 319: 477-487.
65. Pajdo R, Brzozowski T, Konturek PC, et al. Ischemic preconditioning, the most effective gastroprotective intervention: involvement of prostaglandins, nitric oxide, adenosine and sensory nerves. Eur J Pharmacol 2001; 427: 263-276.
66. Konturek PC, Brzozowski T, Pierzchalski P, et al.Activation of genes for spasmolytic peptide, transforming growth factor alpha and for cyclooxygenase (COX)-1 and COX-2 during gastric adaptation to aspirin damage in rats. Aliment Pharmacol Ther 1998; 12: 767-777.
67. Brzozowski T, Konturek PC, Konturek SJ, et al. Effect of local application of growth factors on gastric ulcer healing and mucosal expression of cyclooxygenase-1 and -2. Digestion 2001; 64: 15-29.
68. Brzozowski T, Konturek PC, Sliwowski Z, et al. Neural aspects of ghrelin-induced gastroprotection against mucosal injury induced by noxious agents. J Physiol Pharmacol 2006; 57 (Suppl. 6): 63-76.
69. Warzecha Z, Ceranowicz P, Dembinski M, et al. Involvement of cyclooxygenase-1 and cyclooxygenase-2 activity in the therapeutic effect of ghrelin in the course of ethanol - induced gastric ulcers in rats. J Physiol Pharmacol 2014; 65: 95-106.
70. Xu L, Li Z, Guo F. Curcumin improves expression of ghrelin through attenuating oxidative stress in gastric tissues of streptozocin - induced diabetic gastroparesis rats. Eur J Pharmacol 2013; 718: 219-225.
71. Handa O, Naito Y, Yoshikawa T. Helicobacter pylori: a ROSinducing bacterial species in the stomach. Inflamm Res 2010; 59: 997-1003.
72. Brzozowski T, Zwolinska-Wcislo M, Konturek PC, et al. Influence of gastric colonization with Candida albicans on ulcer healing in rats: effect of ranitidine, aspirin and probiotic therapy. Scand J Gastroenterol 2005; 40: 286-296.
73. Niv Y, Banic M. Gastric barrier function and toxic damage. Dig Dis 2014; 32: 235-242.
74. Solmaz A, Sener G, Cetinel S, Yuksel M, Yegen C, Yegen BC. Protective and therapeutic effects of resveratrol on acetic acid-induced gastric ulcer. Free Radic Res 2009; 43: 594-603.
75. Kwiecien S, Pawlik MW, Sliwowski Z, et al. Involvement of sensory afferent fibers and lipid peroxidation in the pathogenesis of stress-induced gastric mucosa damage. J Physiol Pharmacol 2007; 58 (Suppl. 3): 149-162.
76. Naito Y, Takagi T, Handa O, Yoshikawa T. Lipid hydroperoxide-derived modification of proteins in gastrointestinal tract. Subcell Biochem 2014; 77: 137-148.