The role of melatonin in pancreatic protection: Could melatonin be used in the treatment of acute pancreatitis?

Current Pharmaceutical Design

Volumn 20, Issue 30, 2014, Pages 4834-4840

  Jaworek, Jolanta ^a   Leja Szpak, Anna ^a   Kot, Michalina ^a   Jaworek, Andrzej ^a   Nawrot Porabka, Katarzyna ^a   Bonior, Joanna ^a   Szklarczyk, Joanna ^a  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

Author keywords

Acute pancreatitis; Antioxidant enzymes; L tryptophan; Melatonin; Pancreatic protection

Indexed keywords

CYTOKINE; GLUTATHIONE PEROXIDASE; HEAT SHOCK PROTEIN; LUZINDOLE; MELATONIN; MELATONIN RECEPTOR; NITROGEN DERIVATIVE; PROSTAGLANDIN; SUPEROXIDE DISMUTASE; TRYPTOPHAN; ANTIOXIDANT; CATALASE; OXYGEN;

ABSENCE OF SIDE EFFECTS; ACUTE PANCREATITIS; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CEREBROVASCULAR ACCIDENT; CLINICAL TRIAL (TOPIC); DEGENERATIVE DISEASE; DISEASE EXACERBATION; DRUG BLOOD LEVEL; GASTROINTESTINAL TRACT; HORMONE METABOLISM; HUMAN; NECROSIS; NONHUMAN; PINEAL BODY; PINEALECTOMY; PRIORITY JOURNAL; PROTECTION; TISSUE REGENERATION; ACUTE DISEASE; METABOLISM; PANCREAS; PANCREATITIS; PHYSIOLOGY; BLOOD LEVEL; DRUG METABOLISM; INTESTINE; PATHOGENESIS; PROGNOSIS; REGENERATION; TISSUE INJURY;

ACUTE DISEASE; HUMANS; MELATONIN; PANCREAS; PANCREATITIS; RECEPTORS, MELATONIN;

EID: 84906278663     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612819666131119105019     Document Type: Article

References (107)

1. Mayerle J, Dummer A, Sendler M, et al. Differential roles of inflammatory cells in pancreatitis. J Gastroenterol Hepatol 2012; Suppl. 2: 47-51.
2. Guszek S, Koziel D. Prevalence and progression of acute pancreatitis in the swietokrzyskie voivodeship population. Pol Przegl Chir 2012; 84: 618-625.
3. Lowenfels AB, Maisonneuve P, Sullivan T. The changing character of acute pancreatitis: epidemiology, etiology, and prognosis. Curr Gastroenterol Rep 2009; 11: 97-103.
4. Peery AF, Dellon ES, Lund J, et al. Burden of gastrointestinal disease in the United States: 2012 update. Gastroenterology 2012; 143: 1179-1187.
5. Cruz-Santamaria DM, Taxonera C, Ginger M. Update on pathogenesis and clinical management of acute pancreatitis. World J Gas-trointest Pathophysiol 2012; 3: 60-70.
6. Kylanpaa ML, Repo H, Puolakkainen PA. Inflammation and immunosupresion in severe acute pancreatitis. World J Gastroenterol 2010; 16(23): 2867-2872.
7. Gukovsky I, Pandol SJ, Mareninova OA, Shalbueva N, Jia VV, Gukavskaya AS. Impaired autophagy and organellar dysfunction in pancreatitis. J Gastroenterol Hepatol 2012; Suppl. 2: 27-32.
8. Chan YC, Leung PS. Acute pancreatitis: animal models and recent advances in basic research. Pancreas 2007; 34(1): 1-14.
9. Bhatia M. Acute pancreatitis as a model of SIRS. Front Biosci 2009; 14: 2042-2050.
10. Mylona V, Koussoulas V, Tzivras D, et al. Changes in adaptative and innate immunity in patients with acute pancreatitis and systemic inflammatory response syndrome. Pancreatology 2011; 11: 475-481.
11. Jaworek, J, Nawrot-Porbka K, Leja-Szpak A, et al. Melatonin as modulator of pancreatic enzyme secretion and pancreatoprotector. J Physiol Pharmacol 2007; 58: Suppl. 6: 65-80.
12. Szabolcs A, Reiter RJ, Letoha T. Effect of melatonin on the severity of L-arginine-induced experimental pancreatitis in rats. World J Gastroenterol 2006; 12: 251-258.
13. Huai JP, Sun XC, Chen MJ, et al. Melatonin attenuates acute pancreatitis-associated lung injury in rats by modulating interleukin 22. World J Gastroenterol 2012; 18: 5122-5128.
14. Gulben K, Ozdemir H, Berberoglu U, et al. Melatonin modulates the severity of taurocholate-induced acute pancreatitis. Dig Dis Sci 2010; 55: 941-946.
15. Belayev O, Herzog T, Munding J, et al. Protective role of endogenous melatonin in the early course of human acute pancreatitis. J Pineal Res. 2011; 50: 71-77.
16. Bubenik, GA. Thirty years since the discovery of gastrointestinal melatonin. J Physiol Pharmacol 2008; 59, Suppl. 2: 33-51.
17. 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: 3888-3898.
18. Tan DX, Hardeland R, Manchester LC, et al. Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. J Expo Bot 2012; 63: 577-597.
19. Lerner AB, Case JD, Lee TH, Mori W. Isolation of melatonin, the pineal factor, that lightens melanocytes. J Am Chem Sci 1958, 80: 2587.
20. Bubenik, GA, Pang, SF, Hacker, RR. Melatonin concentrations in serum and tissues of porcine gastrointestinal tract and their relationship to the intake and passage of food. J Pineal Res 1996; 21: 251-256.
21. Messner M, Huether G, Lorf T. Presence of melatonin in the human hepatobiliary tract. Life Sci 2001; 69: 543-551.
22. Hardeland R, Poeggeler B. Melatonin and synthetic melatonergic agonists: actions and metabolism in the central nervous system. Cent Nerv Syst Agents Med Chem 2012; 12: 189-216.
23. Tan DX, Manchester LC, Liu X, et al. Mitochondria and chloro-plasts as the original sites of melatonin synthesis: a hypothesis related to melatonin's primary function and evolution in eucaryotes. J Pineal Res 2013; 54: 127-138.
24. Stefulj J, Hortner M, Ghosh M, et al. Gene expression of the key enzymes in melatonin synthesis in extrapineal tissues in the rat. J Pineal Res. 2001; 30: 243-247.
25. Shimozuma M, Tokuyama R, Tatehara S, et al. Expression and cellular localization of melatonin-synthesis enzyme in rat and human salivary glands. Histochem Cell Biol 2011; 135: 389-396
26. Harderland 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; 42: 109-126.
27. Carpentieri A, Dioaz de Barboza G, Areco V, Peralta Lopez M, Tolosa de Talamoni N. New perspectives for melatonin uses. Pharmacol Res 2012; 65: 437-444.
28. Zawilska JB, Skene DJ, Arendt J: Physiology and pharmacology of melatonin in relation to biological rhythms. Pharmacol Rep. 2009; 61, 383-410.
29. Stebelova, K, Anttila, K, Manttari, S, Saarela, SI, Zeman M. Immu-nohistochemical definition of MT(2) receptors and melatonin in the gastrointestinal tissues of rat. Acta Histochem 2010; 112: 26-33.
30. Cardinali DP, Esquifino AI, Srinivasan V, Pandi-Perumal SR. Melatonin and the immune system in aging. Neuroimmunomodula-tion 2008; 15: 272-278.
31. Slominski RM, Reiter RJ, Schlabritz-Loutsevitch N, Ostrom RS, Slominski AT. Melatonin membrane receptors in peripheral tissues: distribution and functions. Mol Cel Endocrinol 2012; 35(2): 152-166.
32. Ahmed R, Mahavadi S, Al-Shboul O, Bhattacharya S, Grider JR, Muthry KS. Characterization of signaling pathways coupled to melatonin receptors in gastrointestinal smooth muscle. Regul Pept 2013; 184C: 96-103.
33. Harderland R, Pandi-Perumal SR, Cardinali DP. Melatonin. Int J Biochem Cell Biol 2006; 38: 313-6.
34. Sletten TL, Vincenzi S, Redman JR, Lockley SW, Rajaratnam SM. Timing of sleep and its relationship with the endogenous melatonin rhythm. Front Neurol 2010; 1: 137-147.
35. Harderland R, Madrid JA, Tan DX, Reiter RJ. Melatonin, the cir-cadian multioscillator system and health: the need for detailed analyses of peripheral melatonin signaling. J Pineal Res 2012; 52: 139-166.
36. 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.
37. Chojnacki C, Wisniewska-Jarosihska M, Walecka-Kapica E, Klupihska G, Jaworek, Chojnacki J. Evaluation of melatonin effectiveness in the adjuvant treatment of ulcerative colitis. J Physiol Pharmacol 2011; 62: 327-334.
38. Ochoa JJ, Diaz-Castro J, Kajarabille N, et al. Melatonin supplementation ameliorates oxidative stress and inflammatory signaling induced by strenuous exercise in adult human males. J Pineal Res 2011; 51: 373-380.
39. Kurcer Z, Oguz E, Ozbilge H, Baba F, Aksay N, Celik N. Melatonin protects from ischemia/reperfusion renal injury in rats: this effect is not mediated by proinflammatory cytokines. J Pineal Res 2007; 43: 172-178.
40. Rodriguez MI, Escames G, Lopez LC, et al. Chronic melatonin treatment reduces the age-dependent inflammatory process in se-nescense-accelerated mice. J Pineal Res 2007; 42: 1272-1279.
41. Ganguly K, Sharma AV, Reiter RJ, Swamakar S. Melatonin promotes angiogenesis during protection and healing of indomethacin-induced gastric ulcer: role of matrix metalloproteinase-2. J Pineal Res 2010; 49: 130-140.
42. Miller SC, Pandi-Perumal SR, Esquifino AI, Cardinali DP, Maes-troni GJ. The role of melatonin in immuno-enhancement: potential application in cancer. Int Exp Pathol 2006; 87: 81-87.
43. Carillo-Vico A, Reiter RJ. The modulatory role of melatonin on immune responsiveness. Curr Opin Investig Drugs 2006; 7: 423-431.
44. Paredes SD, Sanchez S, Parvez H, Rodriquez AB, Barriga C. Altered circadian rhythms of corticosterone, melatonin, and phagocytic activity in response to stress in rats. Neuro Endocrinol Lett 2007; 11: 489-495.
45. Yang FL, Soberg MY, Lee CJ, Lee RP, Peng TC, Hsu BG. Melatonin ameliorates hemorrhagic shock-induced organ damage in rats. J Surg Res 2011; 167: 15-21.
46. Terron MP, Delgado J, Paredes SD, Barriga C, Reiter RJ, Ro-droguez AB. Effect of melatonin and L-tryptophan on humoral immunity in young and old ringdoves (Streptopelia risoria). Exp Gerontol 2009; 44: 653-658.
47. Zhou W, Wang P, Tao L. Effect of melatonin on proliferation of neonatal cord blond mononuclear cells. World J Pediatr 2009; 5: 300-303.
48. Mukherjee D, Roy SG, Bandyopadhyay A, et al. Melatonin protects against isoproterenol-induced myocardial injury in the rat: anoxida-tive mechanisms. J Pineal Res 2010, 48: 251-261.
49. Lin GJ, Huang SH, Chen YW, et al. Melatonin prolongs islet graft survival in diabetic NOD mice. J Pineal Res 2009; 47: 284-292.
50. Reiter RJ, Paredes SD, Korkmaz A, Joum J, Tan DX: Melatonin combats molecular terrorism at the mitochondrial level. Interdisc Toxicol 2008; 1: 137-148.
51. Martinez-Cruz F., Osuna C, Guerrero JM. Mitochondrial damage induced by hyperphenylalanemia in then rat brain and liver: prevention by melatonin, Vitamin E and Vitamin C. Neurosci Lett 2006, 392: 1-4,
52. Durante P, Romero F, Perez M, Parra G. Effect of uric acid on nephrotoxicity induced by mercuric chloride in rats. Toxicol Ind Health 2010, 26(3): 163-174.
53. Rosanna DP, Salvadore C. Reactive oxygen species, inflammation, and lung disease. Curr Pharm Des 2012; 18: 3889-3900.
54. Bergaminil CM, Gambetti S, Dondi A, Cervellaci C. Oxygen reactive species and tissue damage. Curr Pharm Des 2004, 10: 1611-1626.
55. Galecka E, Mrowicka M, Malinowska M, Galecki P. Wolne rodniki tlenu i azotu w fizjologii. Pol Merkur Lek 2008; 143: 446-448.
56. Shi C, Andersson R, Zhao X, Wang X. Potential role of oxygen species in pancreatitis-associated multiple organ dysfunction. Pan-creatology 2005; 5; 492-500.
57. Modzelewski B, Janiak A. Lipid peroxidation products as prognostic factors in acute pancreatits. Pol Merkur Lek 2005; 19: 511-513.
58. Reiter RJ, Tan DX, Manchester LC, Pilar-Terron M, Flores LJ, Koppisepi S. Medical implications of melatonin: receptor-mediated and receptor-independent actions. Adv Med Sci 2007; 52: 11-28.
59. Ochoa JJ, Diaz-Castro J, Kajarabille N, et al. Melatonin supplementation ameliorates oxidative stress and inflammatory signaling induced by strenuous exercise in adult human males. J Pineal Res 2011; 51: 373-380.
60. Miller E, Mrowicka M, Malinowska K, Ktjdziora J, Majsterek I. The effect of whole body cryotherapy and melatonin supplementation on total antioxidative status and some antioxidative enzyme in multiple sclerosis patients. Pol Merkur Lek 2011; 31: 150-153.
61. Shagirtha K, Muthumani M, Prabu SM. Melatonin abrogates cadmium induced oxidative stress related neurotoxicity in rats. Eur Rev Med Pharmacol Sci 2011, 15: 1039-1050.
62. Tan DX, Manchester LC, Terran MP, Flores LJ, Reiter RJ. One molecule, many derivatives: a never-ending interaction of melatonin with the reactive oxygen and nitrogen species. J Pineal Res, 2007; 42: 28-42.
63. Sun XF, Zhang H. NFkB and NFkB1 polymorphisms in relation to susceptibility of tumor and other diseases. Histol Histopatol 2007; 22: 1387-1398.
64. Czyz M. Specificity and selectivity of the NFkappaB response. Post Biochem, 2005; 51(1): 60-68.
65. Chen, HM, Chen, JC, Ng, CJ, Chiu, DF, Chen, MF. Melatonin reduces pancreatic prostaglandins production and protects against caerulein-induced pancreatitis. J Pineal Res 2006; 40: 34-39.
66. Gulben K, Ozdemir H, Berberoglu U, et al. Melatonin modulates the severity of taurocholate-induced acute pancreatitis. Dig Dis Sci 2010; 55: 941-946.
67. Jung KH, Hong SW, Zheng HM, et al. Melatonin ameliorates ce-rulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats. J Pineal Res 2010; 48: 239-250.
68. Ganguly K, Sharma AV, Reiter RJ, Swamakar S. Melatonin promotes angiogenesis during protection and healing of indomethacin-induced gastric ulcer: role of matrix metalloproteinase-2. J Pineal Res 2010; 49(2)130-140.
69. Tamura H, Takasaki A, Taketani T, et al. Melatonin as free radical scavenger in the ovarian follicle. Endocrinol J 2013; 60: 1-13.
70. Li X, Zhang M, Tang W. Effect of melatonin on streptozocin-induced retina neuronal apoptosis in high blood glucose rat. Neuro-chem Res 2013; 38: 669-676.
71. Soybir G, Topuzlu C, Odabas O, Dolay K, Bilir A, Koksoy F. The effects of melatonin on angiogenesis and wound healing. Surg Today 2003; 33: 896-901.
72. Raikhlin NT, Kvetnoy IM, Tolkahev VN. Melatonin may be syn-thetized in enterochromaffine cells. Nature 1975; 255: 335-344.
73. Kvetnoy IM, Ingel IE, Kvetnaya TV, et al. Gastrointestinal melatonin: Cellular identification and biological role. Neuro Endocrinol Lett 2002; 23: 121-132.
74. Huether G, Poeggler B, Reimer A, George A. Effects of tryptophan administration on circulating melatonin levels in chicks and rats: evidence for stimulation of melatonin synthesis and release in the gastrointestinal tract. Life Sci 1992; 51: 945-953.
75. Stebelova, K, Herichova, I, Zeman M. Diabetes induces changes in melatonin concentration in peripheral tissues of rat. Neuro Endocrinol Lett, 2007; 28: 159-165.
76. Muhlbauer E, Albrecht E, Bazwinsky-Wutsche I, Peschke E. Melatonin influences insulin secretion primarily via MT(1) receptors in rat insulinoma cells (INS-1) and mouse pancreatic islets. J Pineal Res.2012; 52(4): 446-459.
77. Stebelova, K, Anttila, K, Manttari, S, Saarela, SI, Zeman M. Immu-nohistochemical definition of MT(2) receptors and melatonin in the gastrointestinal tissues of rat. Acta Histochem 2010; 112: 26-33.
78. Bubenik, GA, Brown, GM. Pinealectomy reduces melatonin levels in the serum but not in the gastrointestinal tract of the rat. Biol Sign 1997; 6: 40-44.
79. Jaworek J, Nawrot-Porabka K, Konturek SJ, Leja-Szpak A, Thor P, Pawlik W. Melatonin and its precursor; L-tryptophan: influence on pancreatic amylase secretion in vivo and in vitro. J Pineal Res 2004; 36: 156-64.
80. Leja-Szpak A, Jaworek J, Nawrot K, et al. Modulation of pancreatic enzyme secretion by melatonin and its precursor; L-tryptophan. Role of CCK and afferent nerves. J Physiol Pharmacol 2004; 55: 441-451.
81. Qi W, Tan RX, Reiter RJ. Melatonin reduces lipid peroxidation and tissue edema in caerulein-induced acute pancreatitis in the rats. Dig Dis Sci 1999; 44: 2257-2262.
82. Esrefoglu M, Gul M, Ates B, Selimoglu MA. Ultrastructural clues for the protective effect of melatonin against oxidative damage in cerulein-induced pancreatitis. J Pineal Res 2006; 40: 92-97.
83. Sidhu S, Pandhi P, Malhortra S, Vaiphei K, Khanduya KL. Melatonin treatment is beneficial in pancreatic repair process after experimental acute pancreatitis. Eur J Pharmacol 2010; 628: 282-289.
84. Belayev O, Herzog T, Munding J, et al. Protective role of endogenous melatonin in the early course of human acute pancreatitis. J Pineal Res 2011; 50(1): 71-77.
85. Jin Y, Lin CJ, Dong LM, Chen MJ, Zhou Q, Wu JS. Clinical significance of melatonin concentrations in predicting the severity of acute pancreatitis. Wold J Gastroenterol 2013; 19: 4066-4071
86. Baykal A, Iskit AB, Hamaloglou E, Oguz M, Hascelik G, Sayek Y. Melatonin modulates mesenteric blood flow and TNF alpha concentrations after lipopolysaccharide challenge. Eur J Surg 2000; 166: 722-727.
87. Reiter RJ, Paredes SD, Korkmaz A, Joum J, Tan DX. Melatonin combats molecular terrorism at the mitochondrial level. Interdisc Toxicol, 2008; 1: 137-148.
88. Martinez-Cruz F., Osuna C, Guerrero JM. Mitochondrial damage induced by hyperphenylalanemia in then rat brain and liver: prevention by melatonin, Vitamin E and Vitamin C. Neurosci Lett 2006; 392: 1-4.
89. Shagirtha K, Muthumani M, Prabu SM. Melatonin abrogates cadmium induced oxidative stress related neurotoxicity in rats. Eur Rev Med Pharmacol Sci 2011; 15(9): 1039-1050.
90. Tan DX, Manchester LC, Terran MP, Flores LJ, Reiter RJ. One molecule, many derivatives: a never-ending interaction of melatonin with the reactive oxygen and nitrogen species. J Pineal Res, 2007; 42: 28-42.
91. Reiter RJ, Tan DX, Rosales-Corralv S, Manchester LC. The universal nature, unregular distribution and antioxidant functions of melatonin and its derivatives. Mini Rev Chem 2013; 13: 373-384.
92. 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.
93. Lahiri S, Singh P, Singh S, Rashed N, Palit G, Pant KK. Melatonin protects against experimental reflux esophagitis. J Pineal Res, 2009; 46: 207-213
94. Bonior J, Jaworek J, Konturek SJ, Pawlik WW. Increase of heat shock protein gene expression by melatonin in AR42J cells. J Physiol Pharmacol 2005; 56: 471-481.
95. Joly AL, Wettstein G, Mignot G, Ghiringhelli F, Garrido C. Dual role of heat shock proteins as regulators of apoptosis and innate immunity. J Innate Immun 2010; 2: 238-247.
96. Soga S, Aknaga S, Shiotsu Y. Hsp90 inhibitors as anti-cancer agents from badic discoveries to clinical development. Curr Pharm Des 2013; 19: 366-376.
97. Jaworek J., Konturek SJ, Leja-Szpak A. Role of endogenous mela-tonin and its MT2 receptor in the modulation of caerulein-induced pancreatitis in the rat. J Physiol Pharmacol 2002; 53: 791-804
98. 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.
99. Jaworek J, Zwirska-Korczala K, Szklarczyk J, et al. Pinealectomy aggravates acute pancreatitis in the rat. Pharmacol Rev 2010; 62: 864-873.
100. Zurowski D, Nowak L, Machowska A, Worliczek J, Thor P. Exogenous melatonin abolishes mechanical allodynia but not thermal hyperalgesia in neuropathic pain. The role of opioid system and benzodiazepine-gabaergic mechanism. J Physiol Pharmacol 2012; 6: 641-647.
101. Kostoglou-Athanassiou I. Therapeutic application of melatonin. Ther Adv Endocrinol Metab 2013; 4: 13-24.
102. Cutanado A, Lopez-Valverde A, Arias-Sanrtiago S, De Vincente J, De Diego RG. Role of melatonin in cancer treatment. Anticancer Res 2012; 32: 2747-2753.
103. Di Bella G, Colori B, Mascia F. The di Bella Method (DBM) improved survival, objective response and performance status in a retrospective observational clinical study on 55 cases of lymphomas. Neuro Endocrinol Lett 2012 33: 773-781.
104. Quera Salva MA, Hartley S, Barbot F, Alvarez JC, Lofaso F, Guilleminault C. Circadian rhytms, melatonin and depression. Curr Pharm Des 2011; 17: 1459-1470.
105. Del Fabro E, Dev R, Hui D, Palmer L, Bruera E. Effects of mela-tonin on appetite and other symptoms in patients with advanced cancer and cachexia: a double-blind placebo-controlled trial. J Clin Oncol 2013; 31(10): 1271-1276.
106. Gonciarz M, Gonciarz Z, Bielanski W, et al. The effects of long-lasting melatonin treatment on plasma liver enzymes level and plasma concentrations of lipids and melatonin in patients with non-alcocholic steatohepatitios: a pilot study. J Physiol Pharmacol 2012; 1: 35-40.
107. Pandi-Perumal SR, BaHammam AS, Brown GM, et al. Melatonin antioxidative defense: therapeutic implications for aging and neu-rodegenerative processes. Neurotox Res 2013; 23: 267-300.