The Protective Effect of Melatonin on Plasma Lipid Profile in Rats with Cerulein-induced Acute Pancreatitis

Year 2019, Volume: 21 Issue: 2, 332 - 336, 15.09.2019

Ercan Keskin , Deniz Uluışık

https://doi.org/10.15314/tsed.541829

Cited By: 2

Abstract

ABSTRACT

The objective of this study was to assessment
the effect of melatonin on lipid profile in rats with experimentally induced
acute pancreatitis. In this study, 32 adult, male, healthy Wistar Abino rats were
used. Group I animals was no applied.
Group II animals was intraperitoneally administered 50 mg/kg melatonin
per rat twice for two hours intervals. Animals
of group III received two intraperitoneal injections of cerulein (50 µg/kg and
25 µg/kg bw, respectively) at two hours
intervals. Animals of group IV
received two intraperitoneal injections of cerulein (50 µg/kg and 25 µg/kg bw,
respectively) at two hours intervals and
the rats received an intraperitoneal injection of 50 mg/kg melatonin 30 min
before each cerulein injection. After 12
hours from the last cerulein injection, total cholesterol, triglyceride, LDL, HDL
levels was determined. In this study,
experimentally induced acute pancreatitis resulted in significantly increase in
levels of total cholesterol, triglyceride and LDL (p<0.05), while HDL level
significantly decreased compared with control group level (p<0.05). Pretreatment of melatonin
to the rats with acute pancreatitis importantly reduced triglyceride and LDL
levels compared to pancreatitis group (p<0.05). In conclusion, melatonin pretreatment may alleviate
the abnormalities in plasma lipid profile caused by acute pancreatitis.

Keywords

Cerulein, melatonin, acute pancreatitis, lipid profile

References

• 1. Agil A, Reiter RJ, Jiménez-Aranda A, Ibán-Arias R, Navarro-Alarcón M, Marchal JA, Adem A, Fernández-Vázquez G. Melatonin ameliorates low-grade inflammation and oxidative stress in young Zucker diabetic fatty rats. J Pineal Res, 2013; 54(4): 381-388.
• 2. Akay C, Yaman H, Oztosun M, Cakir E, Yildirim AO, Eyi YE, Agilli M, Akgul EO, Aydin I, Kaldirim U, Tuncer SK, Eken A, Oztas E, Poyrazoglu Y, Yasar M, Ozkan Y. The protective effects of taurine on experimental acute pancreatitis in a rat model. Hum Exp Toxicol, 2013; 32(5): 522-529.
• 3. Aoyama H, Mori N, Mori W. Effects of melatonin on genetic hypercholesterolemia in rats. Atherosclerosis, 1988; 69(2-3): 269-272.
• 4. Bonjoch L, Gea-Sorlí S, Closa D. Lipids generated during acute pancreatitis increase inflammatory status of macrophages by interfering with their M2 polarization. Pancreatology, 2015; 15(4): 352-359.
• 5. Bonnefont-Rousselot D, Collin F, Jore D, Gardès-Albert M. Reaction mechanism of melatonin oxidation by reactive oxygen species in vitro. J Pineal Res, 2011; 50(3): 328-335.
• 6. Bugdaci MS, Sokmen M, Zuhur SS, Altuntas Y. Lipid profile changes and importance of low serum-α-lipoprotein fraction (high-density lipoprotein) in cases with acute pancreatitis. Pancreas, 2011; 40(8): 1241-1244.
• 7. Bukowczan J, Warzecha Z, Ceranowicz P, Kuśnierz-Cabala B, Tomaszewska R. Obestatin accelerates the recovery in the course of ischemia/reperfusion-induced acute pancreatitis in rats. PLoS One, 2015; 10(7): e0134380.
• 8. Carpentier YA, Scruel O. Changes in the concentration and composition of plasma lipoproteins during the acute phase response. Curr Opin Clin Nutr Metab Care, 2002; 5(2): 153-158.
• 9. Carrillo-Vico A, Lardone PJ, Alvarez-Sánchez N, Rodríguez-Rodríguez A, Guerrero JM. Melatonin: buffering the immune system. Int J Mol Sci, 2013; 14(4): 8638-8683.
• 10. Chan TY, Tang PL. Effect of melatonin on the maintenance of cholesterol homeostasis in the rat. Endocr Res, 1995; 21(3): 681-696.
• 11. Chan YC, Leung PS. The Renin-angiotensin system and reactive oxygen species: implications in pancreatitis. Antioxid Redox Signal, 2011; 15(10): 2743-2755.
• 12. Chen X, Wu Y, Liu L, Su Y, Peng Y, Jiang L, Liu X, Huang D. Relationship between high density lipoprotein antioxidant activity and carotid arterial intima-media thickness in patients with essential hypertension. Clin Exp Hypertens, 2010; 32(1): 13-20.
• 13. Cheng L, Luo Z, Xiang K, Ren J, Huang Z, Tang L, Tian F. Clinical significance of serum triglyceride elevation at early stage of acute biliary pancreatitis. BMC Gastroenterol, 2015; 15(1): 19.
• 14. Chikamune T, Katamoto H, Nomura K, Ohashi F. Lipoprotein profile in canine pancreatitis induced with oleic acid. J Vet Med Sci, 1998; 60(4): 413-421.
• 15. Closa D, Bulbena O, Rosello-Catafau J, Fernandez-Cruz L, Gelpi E. Effect of prostaglandins and superoxide dismutase administration on oxygen free radical production in experimental acute pancreatitis. Inflammation, 1993; 17(5): 563-571.
• 16. Damian E. The role of the pineal gland in the lipid metabolism. Endocrinologie, 1978; 16(3): 179-189.
• 17. Dauchy RT, Blask DE, Sauer LA, Davidson LK, Krause JA, Smith LC, Dauchy EM. Physiologic melatonin concentration, omega-3 fatty acids, and conjugated linoleic acid inhibit fatty acid transport in rodent hind limb skeletal muscle in vivo. Comp Med, 2003; 53(2): 186-190.
• 18. Domínguez-Muñoz JE, Jünemann F, Malfertheiner P. Hyperlipidemia in acute pancreatitis. Cause or epiphenomenon?. Int J Pancreatol, 1995; 18(2): 101-106.
• 19. Dong Y, Fan C, Hu W, Jiang S, Ma Z, Yan X, Deng C, Di S, Xin Z, Wu G, Yang Y, Reiter RJ, Liang G. Melatonin attenuated early brain injury induced by subarachnoid hemorrhage via regulating NLRP3 inflammasome and apoptosis signaling. J Pineal Res, 2016; 60(3): 253-262.
• 20. Esquifino A, Agrasal C, Velazquez E, Villanua MA, Cardinali DP. Effect of melatonin on serum cholesterol and phospholipid levels, and on prolactin, thyroid-stimulating hormone and thyroid hormone levels, in hyperprolactinemic rats. Life Sci, 1997; 61(11): 1051-1058.
• 21. Favero G, Franceschetti L, Bonomini F, Rodella LF, Rezzani R. Melatonin as an anti-inflammatory agent modulating inflammasome activation. Int J Endocrinol, 2017; 2017: Article ID 1835195, 1-13.
• 22. Franco-Pons N, Casas J, Fabriàs G, Gea-Sorlí S, de-Madaria E, Gelpí E, Closa D. Fat necrosis generates proinflammatory halogenated lipids during acute pancreatitis. Ann Surg, 2013; 257(5): 943-951.
• 23. Galano A, Tan DX, Reiter RJ. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res, 2011; 51(1): 1-16.
• 24. Galuppo M, Nocentini G, Mazzon E, Ronchetti S, Esposito E, Riccardi L, Sportoletti P, Di Paola R, Bruscoli S, Riccardi C, Cuzzocrea S. The glucocorticoid-induced TNF receptor family-related protein (GITR) is critical to the development of acute pancreatitis in mice. Br J Pharmacol, 2011; 162(5): 1186-1201.
• 25. Gea-Sorlí S, Bonjoch L, Closa D. Differences in the inflammatory response induced by acute pancreatitis in different white adipose tissue sites in the rat. PLoS One, 2012; 7(8): e41933.
• 26. Gillies NA, Pendharkar SA, Singh RG, Asrani VM, Petrov MS. Lipid metabolism in patients with chronic hyperglycemia after an episode of acute pancreatitis. Diabetes Metab Syndr, 2017; 11S: S233-S241.
• 27. Gutierrez PT, Folch-Puy E, Bulbena O, Closa D. Oxidised lipids present in ascitic fluid interfere with the regulation of the macrophages during acute pancreatitis, promoting an exacerbation of the inflammatory response. Gut, 2008; 57(5): 642-648.
• 28. Hammer HF. An update on pancreatic pathophysiology (do we have to rewrite pancreatic pathophysiology?). Wien Med Wochenschr, 2014; 164(3-4): 57-62.
• 29. Hartman H, Abdulla A, Awla D, Lindkvist B, Jeppsson B, Thorlacius H, Regnér S. P-selectin mediates neutrophil rolling and recruitment in acute pancreatitis. Br J Surg, 2012; 99(2): 246-255.
• 30. Hoyos M, Guerrero JM, Perez-Cano R, Olivan J, Fabiani F, Garcia-Perganeda A, Osuna C. Serum cholesterol and lipid peroxidation are decreased by melatonin in diet-induced hypercholesterolemic rats. J Pineal Res, 2000; 28(3): 150-155.
• 31. Hussain SA. Effect of melatonin on cholesterol absorption in rats. J Pineal Res, 2007; 42(3): 267-271.
• 32. Khan J, Nordback I, Sand J. Serum lipid levels are associated with the severity of acute pancreatitis. Digestion, 2013; 87(4): 223-228.
• 33. Koziróg M, Poliwczak AR, Duchnowicz P, Koter-Michalak M, Sikora J, Broncel M. Melatonin treatment improves blood pressure, lipid profile, and parameters of oxidative stress in patients with metabolic syndrome. J Pineal Res, 2011; 50(3): 261-266.
• 34. Lee JH, Park JH, Lee SH, Kim JR, Cho KH. Elevated HDL2-paraoxonase and reduced CETP activity are associated with dramatically lower ratio of LDL-cholesterol/total cholesterol in a hypercholesterolemic and hypertriglyceridemic patient. Int J Mol Med, 2010; 25(6): 945-951.
• 35. Liu M, Shi L, Chen M, Chen S, Zou X. Effects of c-Jun N-terminal kinase signaling pathway on severe acute pancreatitis-associated lung injury. Pancreas, 2012; 41(3): 358-366.
• 36. Mårin P, Andersson B, Ottosson M, Olbe L, Chowdhury B, Kvist H, Holm G, Sjöström L, Björntorp P. The morphology and metabolism of intraabdominal adipose tissue in men. Metabolism, 1992; 41(11): 1242-1248.
• 37. Mauriz JL, Collado PS, Veneroso C, Reiter RJ, González-Gallego J. A review of the molecular aspects of melatonin’s anti-inflammatory actions: recent insights and new perspectives. J Pineal Res, 2013; 54(1): 1-14.
• 38. Mirmalek SA, Boushehrinejad AG, Yavari H, Kardeh B, Parsa Y, Salimi-Tabatabaee SA, Yadollah-Damavandi S, Parsa T, Shahverdi E, Jangholi E. Antioxidant and anti-inflammatory effects of coenzyme Q10 on L-Arginine-induced acute pancreatitis in rat. Oxid Med Cell Longev, Article ID 5818479, 2016; 2016: 1-8.
• 39. Mori N, Aoyama H, Murase T, Mori W. Anti-hypercholesterolemic effect of melatonin in rats. Acta Pathol Jpn, 1989; 39(10): 613-618.
• 40. Müller-Wieland D, Behnke B, Koopmann K, Krone W. Melatonin inhibits LDL receptor activity and cholesterol synthesis in freshly isolated human mononuclear leukocytes. Biochem Biophys Res Commun, 1994; 203(1): 416-421.
• 41. Navina S, Acharya C, DeLany JP, Orlichenko LS, Baty CJ, Shiva SS, Durgampudi C, Karlsson JM, Lee K, Bae KT, Furlan A, Behari J, Liu S, McHale T, Nichols L, Papachristou GI, Yadav D, Singh VP. Lipotoxicity causes multisystem organ failure and exacerbates acute pancreatitis in obesity. Sci Transl Med, 2011; 3(107): 107-110.
• 42. Pan M, Song YL, Xu JM, Gan HZ. Melatonin ameliorates nonalcoholic fatty liver induced by high-fat diet in rats. J Pineal Res, 2006; 41(1): 79-84.
• 43. Pan Z, Feng L, Long H, Wang H, Feng J, Chen F. Effects of local pancreatic renin-angiotensin system on the microcirculation of rat with severe acute pancreatitis. Korean J Physiol Pharmacol, 2015; 19(4): 299-307.
• 44. Pandi-Perumal SR, Srinivasan V, Maestroni GJ, Cardinali DP, Poeggeler B, Hardeland R. Melatonin: nature's most versatile biological signal?. FEBS J, 2006; 273(13): 2813-2838.
• 45. Peng YS, Chen YC, Tian YC, Yang CW, Lien JM, Fang JT, Wu CS, Hung CF, Hwang TL, Tsai YH, Lee MS, Tsai MH. Serum levels of apolipoprotein A-I and high-density lipoprotein can predict organ failure in acute pancreatitis. Crit Care, 2015; 19, 88: 1-9.
• 46. Podrez EA. Antioxidant properties of high density lipoprotein and atherosclerosis. Clin Exp Pharmacol Physiol, 2010; 37(7): 719-725.
• 47. Reiter RJ, Carneiro RC, Oh CS. Melatonin in relation to cellular antioxidative defense mechanisms. Horm Metab Res, 1997; 29(8): 363-372.
• 48. Reiter RJ, Tan DX, Terron MP, Flores LJ, Czarnocki Z. Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim Pol, 2007; 54(1): 1-9.
• 49. Rohan Jeyarajah D, Osman HG, Patel S. Severe acute pancreatitis attacks are associated with significant morbidity and mortality. Curr Probl Surg, 2014; 51(9): 370-372.
• 50. Sanchez-Mateos S, Alonso-Gonzalez C, Gonzalez A, Martinez-Campa CM, Mediavilla MD, Cos S, Sanchez-Barcelo EJ. Melatonin and estradiol effects on food intake, body weight, and leptin in ovariectomized rats. Maturitas, 2007; 58(1): 91-101.
• 51. Sempere L, Martinez J, de Madaria E, Lozano B, Sanchez-Paya J, Jover R, Perez-Mateo M. Obesity and fat distribution imply a greater systemic inflammatory response and a worse prognosis in acute pancreatitis. Pancreatology, 2008; 8(3): 257-264.
• 52. Subramanian P, Mirunalini S, Pandi-Perumal SR, Trakht I, Cardinali DP. Melatonin treatment improves the antioxidant status and decreases lipid content in brain and liver of rats. Eur J Pharmacol, 2007; 571(2-3): 116-119.
• 53. Tan DX, Manchester LC, Terron MP, Flores LJ, Reiter RJ. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species?. J Pineal Res, 2007; 42(1): 28-42.
• 54. Toskes PP. Hyperlipidemic pancreatitis. Gastroenterol Clin North Am, 1990; 19(4): 783-791.
• 55. Tribble DL, Chu BM, Gong EL, van Venrooij F, Nichols AV. HDL antioxidant effects as assessed using a nonexchangeable probe to monitor particle-specific peroxidative stress in LDL-HDL mixtures. J Lipid Res, 1995; 36(12): 2580-2589.
• 56. Túnez L, Muñoz MC, Feijoo-López AL, Valdvira E, Bujalance-Arenas L, Montilla P. Effect of melatonin on hyperlipidemic nephropathy under constant light exposure. J Physiol Biochem, 2002; 58(2): 109-114.
• 57. Unal E, Uzun H, Kusaslan R, Dogan M, Genc H, Gunes P, Titiz I. Serum paraoxonase (a high-density lipoprotein–associated lipophilic antioxidant) activity and lipid profile in experimental acute pancreatitis. Pancreas, 2005; 31(1): 84-87.
• 58. Vaughan MK, Powanda MC, Brainard GC, Johnson LY, Reiter RJ. Effects of blinding or afternoon melatonin injections on plasma cholesterol, triglycerides, glucose, TSH and thyroid hormone levels in male and female Syrian hamsters. Prog Clin Biol Res, 1982; 92: 177-186.
• 59. Yang B, Bai B, Liu CX, Wang SQ, Jiang X, Zhu CL, Zhao QC. Effect of umbilical cord mesenchymal stem cells on treatment of severe acute pancreatitis in rats. Cytotherapy, 2013; 15(2): 154-162.
• 60. Yubero S, Manso MA, Ramudo L, Vicente S, De Dios I. Dexamethasone down-regulates the inflammatory mediators but fails to reduce the tissue injury in the lung of acute pancreatitis rat models. Pulm Pharmacol Ther, 2012; 25(4): 319-324.