Melatonin ameliorates cerulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats

Journal of Pineal Research

Volumn 48, Issue 3, 2010, Pages 239-250

  Jung, Kyung Hee ^a   Hong, Sang Won ^a   Zheng, Hong Mei ^a   Lee, Hee Seung ^a   Lee, Hyunseung ^a   Lee, Don Haeng ^b   Lee, Sang Yoon ^c   Hong, Soon Sun ^a,d  

^a Inha University   (South Korea)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c Ajou University School of Medicine   (South Korea)

^d Inha University School of Medicine   (South Korea)

Author keywords

Cerulein; Inflammation; Melatonin; Nrf2; Oxidative stress; Pancreatitis

Indexed keywords

AMYLASE; CERULETIDE; GLUTATHIONE PEROXIDASE; HEME OXIDASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MANGANESE SUPEROXIDE DISMUTASE; MELATONIN; OXIDOREDUCTASE; QUINONE OXIDOREDUCTASE 1; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; TRIACYLGLYCEROL LIPASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACINAR CELL; ACUTE PANCREATITIS; AMYLASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEGENERATION; CONTROLLED STUDY; INFLAMMATORY INFILTRATE; NONHUMAN; OXIDATIVE STRESS; RAT; TRIACYLGLYCEROL LIPASE BLOOD LEVEL;

ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; CAERULEIN; CYTOKINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GLUTATHIONE PEROXIDASE; HEME OXYGENASE-1; HISTOCYTOCHEMISTRY; LIPID PEROXIDATION; MALONDIALDEHYDE; MELATONIN; NF-E2-RELATED FACTOR 2; NF-KAPPA B; PANCREATITIS, ACUTE NECROTIZING; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE;

EID: 77749310344     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2010.00748.x     Document Type: Article

References (71)

1. Esrefoglu M, Gul M, Ates B, et al. Ultrastructural clues for the protective effect of ascorbic acid and N-acetylcysteine against oxidative damage on caerulein-induced pancreatitis. Pancreatology 2006 6 : 477 485.
2. Esrefoglu M, Gul M, Ates B, et al. Antioxidative effect of melatonin, ascorbic acid and N-acetylcysteine on caerulein-induced pancreatitis and associated liver injury in rats. World J Gastroenterol 2006 12 : 259 264.
3. Wisner J, Green D, Ferrell L, et al. Evidence for a role of oxygen derived free radicals in the pathogenesis of caerulein induced acute pancreatitis in rats. Gut 1988 29 : 1516 1523.
4. Niederau C, Niederau M, Luthen R, et al. Pancreatic exocrine secretion in acute experimental pancreatitis. Gastroenterology 1990 99 : 1120 1127.
5. Zyromski N, Murr MM. Evolving concepts in the pathophysiology of acute pancreatitis. Surgery 2003 133 : 235 237.
6. Gukovskaya AS, Gukovsky I, Zaninovic V, et al. Pancreatic acinar cells produce, release, and respond to tumor necrosis factor-alpha. Role in regulating cell death and pancreatitis. J Clin Invest 1997 100 : 1853 1862.
7. Sweiry JH, Mann GE. Role of oxidative stress in the pathogenesis of acute pancreatitis. Scand J Gastroenterol Suppl 1996 219 : 10 15.
8. Schoenberg MH, Buchler M, Gaspar M, et al. Oxygen free radicals in acute pancreatitis of the rat. Gut 1990 31 : 1138 1143.
9. Sarr MG, Bulkley GB, Cameron JL. Temporal efficacy of allopurinol during the induction of pancreatitis in the ex vivo perfused canine pancreas. Surgery 1987 101 : 342 346.
10. Dabrowski A, Konturek SJ, Konturek JW, et al. Role of oxidative stress in the pathogenesis of caerulein-induced acute pancreatitis. Eur J Pharmacol 1999 377 : 1 11.
11. Jungermann J, Lerch MM, Weidenbach H, et al. Disassembly of rat pancreatic acinar cell cytoskeleton during supramaximal secretagogue stimulation. Am J Physiol 1995 268 : G328 G338.
12. Talalay P, Dinkova-Kostova AT, Holtzclaw WD. Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Adv Enzyme Regul 2003 43 : 121 134.
13. Zhang Y, Gordon GB. A strategy for cancer prevention: stimulation of the Nrf2-ARE signaling pathway. Mol Cancer Ther 2004 3 : 885 893.
14. Talalay P. Chemoprotection against cancer by induction of phase 2 enzymes. Biofactors 2000 12 : 5 11.
15. Fisher CD, Augustine LM, Maher JM, et al. Induction of drug-metabolizing enzymes by garlic and allyl sulfide compounds via activation of constitutive androstane receptor and nuclear factor E2-related factor 2. Drug Metab Dispos 2007 35 : 995 1000.
16. Yoh K, Hirayama A, Ishizaki K, et al. Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice. Genes Cells 2008 13 : 1159 1170.
17. He X, Kan H, Cai L, et al. Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J Mol Cell Cardiol 2009 46 : 47 58.
18. Bubenik GA, Brown GM. Pinealectomy reduces melatonin levels in the serum but not in the gastrointestinal tract of rats. Biol Signals 1997 6 : 40 44.
19. Hardeland R, Tan DX, Reiter RJ. Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J Pineal Res 2009 47 : 109 126.
20. Peyrot F, Ducrocq C. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J Pineal Res 2008 45 : 235 246.
21. Teixeira A, Morfim MP, De Cordova CA, et al. Melatonin protects against pro-oxidant enzymes and reduces lipid peroxidation in distinct membranes induced by the hydroxyl and ascorbyl radicals and by peroxynitrite. J Pineal Res 2003 35 : 262 268.
22. Ersahin M, Toklu HZ, Cetinel S, et al. Melatonin reduces experimental subarachnoid hemorrhage-induced oxidative brain damage and neurological symptoms. J Pineal Res 2009 46 : 324 332.
23. Kireev RA, Tresguerres AC, Garcia C, et al. Melatonin is able to prevent the liver of old castrated female rats from oxidative and pro-inflammatory damage. J Pineal Res 2008 45 : 394 402.
24. Barlas A, Cevik H, Arbak S, et al. Melatonin protects against pancreaticobiliary inflammation and associated remote organ injury in rats: role of neutrophils. J Pineal Res 2004 37 : 267 275.
25. Qi W, Tan DX, Reiter RJ, et al. Melatonin reduces lipid peroxidation and tissue edema in cerulein-induced acute pancreatitis in rats. Dig Dis Sci 1999 44 : 2257 2262.
26. Munoz-Casares FC, Padillo FJ, Briceno J, et al. Melatonin reduces apoptosis and necrosis induced by ischemia/reperfusion injury of the pancreas. J Pineal Res 2006 40 : 195 203.
27. Jaworek J, Konturek SJ, Tomaszewska R, et al. The circadian rhythm of melatonin modulates the severity of caerulein-induced pancreatitis in the rat. J Pineal Res 2004 37 : 161 170.
28. Jaworek J, Leja-Szpak A, Bonior J, et al. Protective effect of melatonin and its precursor L-tryptophan on acute pancreatitis induced by caerulein overstimulation or ischemia/reperfusion. J Pineal Res 2003 34 : 40 52.
29. Lau HY, Wong FL, Bhatia M. A key role of neurokinin 1 receptors in acute pancreatitis and associated lung injury. Biochem Biophys Res Commun 2005 327 : 509 515. (Pubitemid 40040504)
30. Niehaus WG Jr., Samuelsson B. Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 1968 6 : 126 130.
31. Van Laethem JL, Marchant A, Delvaux A, et al. Interleukin 10 prevents necrosis in murine experimental acute pancreatitis. Gastroenterology 1995 108 : 1917 1922.
32. Alarcon De La Lastra C, Motilva V, Martin MJ, et al. Protective effect of melatonin on indomethacin-induced gastric injury in rats. J Pineal Res 1999 26 : 101 107.
33. Leon J, Acuna-Castroviejo D, Escames G, et al. Melatonin mitigates mitochondrial malfunction. J Pineal Res 2005 38 : 1 9.
34. Tan DX, Reiter RJ, Manchester LC, et al. Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. Curr Top Med Chem 2002 2 : 181 197.
35. Gomez-Cambronero LG, Sabater L, Pereda J, et al. Role of cytokines and oxidative stress in the pathophysiology of acute pancreatitis: therapeutical implications. Curr Drug Targets Inflamm Allergy 2002 1 : 393 403.
36. Folch E, Gelpi E, Rosello-Catafau J, et al. Free radicals generated by xanthine oxidase mediate pancreatitis-associated organ failure. Dig Dis Sci 1998 43 : 2405 2410.
37. Dabrowski A, Gabryelewicz A, Wereszczynska-Siemiatkowska U, et al. Oxygen-derived free radicals in cerulein-induced acute pancreatitis. Scand J Gastroenterol 1988 23 : 1245 1249.
38. Szabolcs A, Reiter RJ, Letoha T, et al. Effect of melatonin on the severity of L-arginine-induced experimental acute pancreatitis in rats. World J Gastroenterol 2006 12 : 251 258.
39. Alhan E, Kalyoncu NI, Kural BV, et al. Effects of melatonin on acute necrotizing pancreatitis in rats. Z Gastroenterol 2004 42 : 967 972. (Pubitemid 39625603)
40. Elbling L, Weiss RM, Teufelhofer O, et al. Green tea extract and (-)-epigallocatechin-3-gallate, the major tea catechin, exert oxidant but lack antioxidant activities. FASEB J 2005 19 : 807 809.
41. Enomoto A, Itoh K, Nagayoshi E, et al. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci 2001 59 : 169 177.
42. Lee JM, Li J, Johnson DA, et al. Nrf2, a multi-organ protector? FASEB J 2005 19 : 1061 1066.
43. Morimitsu Y, Nakagawa Y, Hayashi K, et al. A sulforaphane analogue that potently activates the Nrf2-dependent detoxification pathway. J Biol Chem 2002 277 : 3456 3463.
44. Szymanska J, Tarkkanen M, Wiklund T, et al. A cytogenetic study of malignant fibrous histiocytoma. Cancer Genet Cytogenet 1995 85 : 91 96.
45. Kalayarasan S, Prabhu PN, Sriram N, et al. Diallyl sulfide enhances antioxidants and inhibits inflammation through the activation of Nrf2 against gentamicin-induced nephrotoxicity in Wistar rats. Eur J Pharmacol 2009 606 : 162 171.
46. Sriram N, Kalayarasan S, Sudhandiran G. Epigallocatechin-3-gallate augments antioxidant activities and inhibits inflammation during bleomycin-induced experimental pulmonary fibrosis through Nrf2-Keap1 signaling. Pulm Pharmacol Ther 2009 22 : 221 236.
47. Jung KH, Hong SW, Zheng HM, et al. Melatonin downregulates nuclear erythroid 2-related factor 2 and nuclear factor-kappaB during prevention of oxidative liver injury in a dimethylnitrosamine model. J Pineal Res 2009 47 : 173 183.
48. Copple IM, Goldring CE, Kitteringham NR, et al. The Nrf2-Keap1 defence pathway: role in protection against drug-induced toxicity. Toxicology 2008 246 : 24 33.
49. Kang KA, Kim JS, Zhang R, et al. Induction of heme oxygenase-1 by plant extract KIOM-79 via Akt pathway and NF-E2 related factor 2 in pancreatic beta-cells. J Toxicol Environ Health A 2008 71 : 1392 1399.
50. Song MY, Kim EK, Moon WS, et al. Sulforaphane protects against cytokine- and streptozotocin-induced beta-cell damage by suppressing the NF-kappaB pathway. Toxicol Appl Pharmacol 2009 235 : 57 67.
51. Bhatia M, Brady M, Shokuhi S, et al. Inflammatory mediators in acute pancreatitis. J Pathol 2000 190 : 117 125.
52. Norman J. The role of cytokines in the pathogenesis of acute pancreatitis. Am J Surg 1998 175 : 76 83.
53. Rongione AJ, Kusske AM, Kwan K, et al. Interleukin 10 reduces the severity of acute pancreatitis in rats. Gastroenterology 1997 112 : 960 967.
54. Norman JG, Fink GW, Franz MG. Acute pancreatitis induces intrapancreatic tumor necrosis factor gene expression. Arch Surg 1995 130 : 966 970.
55. Tamizhselvi R, Sun J, Koh YH, et al. Effect of hydrogen sulfide on the phosphatidylinositol 3-kinase-protein kinase B pathway and on caerulein-induced cytokine production in isolated mouse pancreatic acinar cells. J Pharmacol Exp Ther 2009 329 : 1166 1177.
56. Xue D, Zhang W, Zhang Y, et al. Adjusting effects of baicalin for nuclear factor-kappaB and tumor necrosis factor-alpha on rats with caerulein-induced acute pancreatitis. Mediators Inflamm 2006 2006 : 26295.
57. Tanaka T, Yasui Y, Tanaka M, et al. Melatonin suppresses AOM/DSS-induced large bowel oncogenesis in rats. Chem Biol Interact 2009 177 : 128 136.
58. Pedreira PR, Garcia-Prieto E, Parra D, et al. Effects of melatonin in an experimental model of ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol 2008 295 : L820 L827.
59. Wang H, Wei W, Wang NP, et al. Melatonin ameliorates carbon tetrachloride-induced hepatic fibrogenesis in rats via inhibition of oxidative stress. Life Sci 2005 77 : 1902 1915.
60. Koh PO. Melatonin regulates nitric oxide synthase expression in ischemic brain injury. J Vet Med Sci 2008 70 : 747 750.
61. Rogerio F, Teixeira SA, Junior HJ, et al. mRNA and protein expression and activities of nitric oxide synthases in the lumbar spinal cord of neonatal rats after sciatic nerve transection and melatonin administration. Neurosci Lett 2006 407 : 182 187.
62. Leon J, Escames G, Rodriguez MI, et al. Inhibition of neuronal nitric oxide synthase activity by N1-acetyl-5-methoxykynuramine, a brain metabolite of melatonin. J Neurochem 2006 98 : 2023 2033.
63. Chuang JI, Mohan N, Meltz ML, et al. Effect of melatonin on NF-kappa-B DNA-binding activity in the rat spleen. Cell Biol Int 1996 20 : 687 692.
64. Mohan N, Sadeghi K, Reiter RJ, et al. The neurohormone melatonin inhibits cytokine, mitogen and ionizing radiation induced NF-kappa B. Biochem Mol Biol Int 1995 37 : 1063 1070.
65. Li Z, Nickkholgh A, Yi X, et al. Melatonin protects kidney grafts from ischemia/reperfusion injury through inhibition of NF-kB and apoptosis after experimental kidney transplantation. J Pineal Res 2009 46 : 365 372.
66. Alonso M, Collado PS, Gonzalez-Gallego J. Melatonin inhibits the expression of the inducible isoform of nitric oxide synthase and nuclear factor kappa B activation in rat skeletal muscle. J Pineal Res 2006 41 : 8 14.
67. Li JH, Yu JP, Yu HG, et al. Melatonin reduces inflammatory injury through inhibiting NF-kappaB activation in rats with colitis. Mediators Inflamm 2005 2005 : 185 193.
68. Brennan CP, Hendricks GL III., El-Sheikh TM, et al. Melatonin and the enhancement of immune responses in immature male chickens. Poult Sci 2002 81 : 371 375.
69. Garcia-Maurino S, Pozo D, Calvo JR, et al. Correlation between nuclear melatonin receptor expression and enhanced cytokine production in human lymphocytic and monocytic cell lines. J Pineal Res 2000 29 : 129 137.
70. Jin W, Wang H, Yan W, et al. Disruption of Nrf2 enhances upregulation of nuclear factor-kappaB activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury. Mediators Inflamm 2008 2008 : 1 7. Available at: http://www.hindawi.com/journals/mi/2008/725174. html.
71. Thimmulappa RK, Lee H, Rangasamy T, et al. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest 2006 116 : 984 995.