Inflammation

, Volume 37, Issue 4, pp 1111–1119 | Cite as

Protective Effect of Melatonin on Infrarenal Aortic Occlusion: This Effect Is Related to Anti-inflammatory Effect and Antioxidant Effect

  • Ahmet Ahsen
  • Yucel Gonul
  • Abdurrahman Genc
  • Memnune Sena Ulu
  • Murat Yagmurca
  • Cevdet Ugur Kocogullari
  • Sefa Celik
  • Seref Yuksel
Article

KEY WORDS

melatonin aortic ischemia–reperfusion renal oxidative stress parameters 

References

  1. 1.
    Parrino, P.E., V.E. Laubach, J.R. Gaughen, et al. 1998. Inhibition of inducible nitric oxide synthase after myocardial ischemia increases coronary flow. Ann Thorac Surg 66: 733–739.PubMedCrossRefGoogle Scholar
  2. 2.
    Koksel, O., A. Ozdulger, B. Aytacoglu, et al. 2005. The influence of iloprost on acute lung injury induced by hind limb ischemia-reperfusion in rats. Pulm Pharmacol Ther 18: 235–241.PubMedCrossRefGoogle Scholar
  3. 3.
    Kozlov, A.V., S. Bahrami, E. Calzia, P. Dungel, L. Gille, A.V. Kuznetsov, et al. 2011. Mitochondrial dysfunction and biogenesis: Do ICU patients die from mitochondrial failure? Ann Intensive Care 1: 41.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Joyce, M., C. Kelly, D. Winter, et al. 2001. Pravastatin, a 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibitor, attenuates renal injury in an experimental model of ischemia-reperfusion. J Surg Res 101: 79.PubMedCrossRefGoogle Scholar
  5. 5.
    Sucu, N., A. Unlu, L. Tamer, et al. 2002. Effects of trimetazidine on tissue damage in kidney after hind limb ischemia-reperfusion. Pharmacol Res 46: 345–349.PubMedCrossRefGoogle Scholar
  6. 6.
    Carden, D.L., and D.N. Granger. 2000. Pathophysiology of ischemia–reperfusion injury. J Pathol 190: 255–266.PubMedCrossRefGoogle Scholar
  7. 7.
    Okutan, H., C. Savas, and N. Delibas. 2004. The antioxidant effect of melatonin in lung injury after aortic occlusion-reperfusion. Interact Cardiovasc Thorac Surg 3: 519.PubMedCrossRefGoogle Scholar
  8. 8.
    Yassin, M.M.I., D.W. Harkin, A.A.B. Barrsos, M.I. Halliday, and B.J. Rowlands. 2002. Lower limb ischemia-reperfusion injury triggers a systemic inflammatory response and multiple organ dysfunction. World J Surg 26: 115–121.PubMedCrossRefGoogle Scholar
  9. 9.
    Ellenberger, C., A. Schweizer, J. Diaper, et al. 2006. Incidence, risk factors, and prognosis of changes in serum creatinine early after aortic abdominal surgery. Intensive Care Med 32: 1808–1816.PubMedCrossRefGoogle Scholar
  10. 10.
    Tallgren, M., T. Niemi, R. Pöyhiä, et al. 2007. Acute renal injury and dysfunction following elective abdominal aortic surgery. Eur J Vasc Endovasc Surg 33: 550–555.PubMedCrossRefGoogle Scholar
  11. 11.
    Gamulin, Z., A. Forster, D. Morel, et al. 1984. Effects of infrarenal aortic cross-clamping on renal hemodynamics in humans. Anesthesiology 61: 394–399.PubMedCrossRefGoogle Scholar
  12. 12.
    Gamulin, Z., A. Forster, F. Simonet, E. Aymon, and H. Favre. 1986. Effects of renal sympathetic blockade on renal hemodynamics in patients undergoing major aortic abdominal surgery. Anesthesiology 65: 688–692.PubMedCrossRefGoogle Scholar
  13. 13.
    Welch, M., D.G. Knight, H.M. Carr, J.V. Smyth, and M.G. Walker. 1994. Influence of renal artery blood flow on renal function during aortic surgery. Surgery 115: 46–51.PubMedGoogle Scholar
  14. 14.
    Summers, S.T., M.J. Zinner, and J.A. Freischlag. 1993. Production of endothelium-derived relaxing factor (EDRF) is compromised after ischemia and reperfusion. Am J Surg 166: 216–220.PubMedCrossRefGoogle Scholar
  15. 15.
    Cuzzocrea, S., and J.R. Reiter. 1994. Pharmacological action of melatonin in shock, inflammation and ischemia/reperfusion injury. Eur J Pharmacol 426: 1–10.CrossRefGoogle Scholar
  16. 16.
    Paller, M.S. 1994. The cell biology of reperfusion injury in the kidney. J Investig Med 42: 632–639.PubMedGoogle Scholar
  17. 17.
    Williams, P., H. Lopez, D. Britt, C. Chan, A. Ezrin, and R. Hottendorf. 1997. Characterization of renal ischemia-reperfusion injury in rats. J Pharmacol Toxicol Methods 37: 1–7.PubMedCrossRefGoogle Scholar
  18. 18.
    Rasoulian, B., M. Jafari, A. Noroozzadeh, et al. 2008. Effects of ischemia-reperfusion on rat renal tissue antioxidant systems and lipid peroxidation. Acta Medica Iranica 46: 353–360.Google Scholar
  19. 19.
    Troyer-Caudle, J. 1993. Reperfusion injury. J Vasc Nurs 11: 76.PubMedGoogle Scholar
  20. 20.
    Adams Jr., J.G., A. Dhar, S.D. Shukla, et al. 1995. Effect of pentoxifylline on tissue injury and platelet-activating factor production during ischemia-reperfusion injury. J Vasc Surg 21: 742.PubMedCrossRefGoogle Scholar
  21. 21.
    Reiter, R.J., D.X. Tan, C. Osuna, and E. Gitto. 2000. Actions of melatonin in the reduction of oxidative stress. J Biomed Sci 7: 444–458.PubMedCrossRefGoogle Scholar
  22. 22.
    Tan, D.X., L.D. Chen, B. Poeggeler, L.C. Manchester, and R.J. Reiter. 1993. Melatonin: A potent, endogenous hydroxyl radical scavenger. Endocr J 1: 57–60.Google Scholar
  23. 23.
    Bonnefont-Rousselot, D., F. Collin, D. Jore, and M. Gardes-Albert. 2011. Reaction mechanism of melatonin oxidation by reactive oxygen species in vitro. J Pineal Res 50(3): 328–335.PubMedCrossRefGoogle Scholar
  24. 24.
    Galano, A., D.X. Tan, and R.J. Reiter. 2011. Melatonin as a natural ally against oxidative stress: A physicochemical examination. J Pineal Res 51(1): 1–16.PubMedCrossRefGoogle Scholar
  25. 25.
    Raghavendra, V., V. Singh, A.V. Shaji, H. Vohra, S.K. Kulkarni, and J.N. Agrewala. 2001. Melatonin provides signal 3 to unprimed CD4(+) T cells but failed to stimulate LPS primed B cells. Clin Exp Immunol 124: 414–422.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Wang, H., W. Wei, N.P. Wang, S.Y. Gui, L. Wu, W.Y. Sun, and S.Y. Xu. 2005. Melatonin ameliorates carbon tetrachloride-induced hepatic fibrogenesis in rats via inhibition of oxidative stress. Life Sci 77: 1902–1915.PubMedCrossRefGoogle Scholar
  27. 27.
    Lahiri, S., P. Singh, S. Singh, N. Rasheed, G. Palit, and K.K. Pant. 2009. Melatonin protects against experimental reflux esophagitis. J Pineal Res 46: 207–213.PubMedCrossRefGoogle Scholar
  28. 28.
    Jung, K.H., S.W. Hong, H.M. Zheng, D.H. Lee, and S.S. Hong. 2009. 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 47: 173–183.PubMedCrossRefGoogle Scholar
  29. 29.
    Rodriguez-Reynoso, S., C. Leal, E. Portilla-de-Buen, and N. Olivares. 2001. Effects of exogenous melatonin on hepatic energetic status during ischemia-reperfusion: Possible role of TNF-a and nitric oxide. J Surg Res 110: 141–149.CrossRefGoogle Scholar
  30. 30.
    Wang, Y., X. Liu, W. Wang, W. Song, L. Chen, Q. Fang, and X. Yan. 2013. The expression of inflammatory cytokines on the aorta endothelia are up-regulated in pinealectomized rats. Inflammation 36(6): 1363–1373.PubMedCrossRefGoogle Scholar
  31. 31.
    Reiter, R.J., D. Melchiorri, E. Sewerynek, B. Poeggeler, L. Barlow-Walden, J. Chuang, et al. 1995. A review of the evidence supporting melatonin’s role as an antioxidant. J Pineal Res 18: 1–11.PubMedCrossRefGoogle Scholar
  32. 32.
    Pieri, C., M. Marra, F. Moroni, R. Recchioni, and F. Marcheselli. 1994. Melatonin: A peroxyl radical scavenger more effective than vitamin E. Life Sci 55: PL271–PL276.PubMedCrossRefGoogle Scholar
  33. 33.
    Erel, O. 2005. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38: 1103–1111.PubMedCrossRefGoogle Scholar
  34. 34.
    Erel, O. 2004. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37: 277–285.PubMedCrossRefGoogle Scholar
  35. 35.
    Esen, C., B.A. Alkan, M. Kırnap, et al. 2012. The effects of chronic periodontitis and rheumatoid arthritis on serum and gingival crevicular fluid total antioxidant/oxidant status and oxidative stress index. J Periodontol 83: 773–779.PubMedCrossRefGoogle Scholar
  36. 36.
    Hauet, T., D. Mothes, J.M. Goujon, et al. 1997. Trimetazidine prevents renal injury in the isolated perfused pig kidney exposed to prolonged cold ischaemia. Transplantation 64: 1082–1086.PubMedCrossRefGoogle Scholar
  37. 37.
    White, P., and P.W. Kaestner. 2009. Gene expression analysis in diabetes research. Methods Mol Biol 560: 239–261.PubMedCrossRefGoogle Scholar
  38. 38.
    Pfaffl, M.W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9): 2002–2007.CrossRefGoogle Scholar
  39. 39.
    Kurcer, Z., E. Oguz, H. Ozbilge, et al. 2007. Melatonin protects from ischemia/reperfusion-induced renal injury in rats: This effect is not mediated by proinflammatory cytokines. J Pineal Res 43: 172–178.PubMedCrossRefGoogle Scholar
  40. 40.
    Yuksel, S., M.T. Sezer, O. Sahin, R. Sutcu, C. Koçogullari, H.R. Yilmaz, E. Uz, Y. Kara, B. Aydin, and A. Altuntas. 2011. The role of carnitine in preventing renal damage developed as a result of infrarenal aortic ischemia–reperfusion. Ren Fail 33(4): 440–449.PubMedCrossRefGoogle Scholar
  41. 41.
    Sener, G., A.O. Sehirli, M. Keyer-Uysal, S. Arbak, Y. Ersoy, and B.C. Yegen. 2002. The protective effect of melatonin on renal ischemia-reperfusion injury in the rat. J Pineal Res 32: 120–126.PubMedCrossRefGoogle Scholar
  42. 42.
    Sezgin, G., G. Öztürk, S. Güney, O. Sinanoglu, and M. Tuncdemir. 2013. Protective effect of melatonin and 1,25-dihydroxyvitamin D3 on renal ischemia–reperfusion injury in rats. Ren Fail 35(3): 374–379.PubMedCrossRefGoogle Scholar
  43. 43.
    Gitto, E., C. Romeo, R.J. Reiter, et al. 2004. Melatonin reduces oxidative stress in surgical neonates. J Pediatr Surg 39: 184–189.PubMedCrossRefGoogle Scholar
  44. 44.
    Veneroso, C., M.J. Tunon, J. Gonzalez-Gallego, and P.S. Collado. 2009. Melatonin reduces cardiac inflammatory injury induced by acute exercise. J Pineal Res 47: 184–191.PubMedCrossRefGoogle Scholar
  45. 45.
    Tak, P.P., and G.S. Firestein. 2001. NF-κB: A key role in inflammatory diseases. J Clin Invest 107: 7–11.PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Sen, C.K., and L. Packer. 1996. Antioxidant and redox regulation of gene transcription. Faseb J 10: 709–720.PubMedGoogle Scholar
  47. 47.
    Li, Z., A. Nickkholgh, X. Yi, H. Bruns, M.L. Gross, K. Hoffmann, E. Mohr, M. Zorn, M.W. Buchler, and P. Schemmer. 2009. Melatonin protects kidney grafts from ischemia/reperfusion injury through inhibition of NF-κB and apoptosis after experimental kidney transplantation. J Pineal Res 46: 365–372.PubMedCrossRefGoogle Scholar
  48. 48.
    Ozbek, E., Y.O. Ilbey, M. Ozbek, A. Simsek, M. Cekmen, and A. Somay. 2009. Melatonin attenuates unilateral ureteral obstruction-induced renal injury by reducing oxidative stress, iNOS, MAPK, and NF-κB expression. J Endourol 23: 1165–1173.PubMedCrossRefGoogle Scholar
  49. 49.
    Pascua, P., C. Camello-Almaraz, P.J. Camello, F.E. Martin-Cano, E. Vara, J.A. Fernandez-Tresguerres, and M.J. Pozo. 2011. Melatonin, and to a lesser extent growth hormone, restores colonic smooth muscle physiology in old rats. J Pineal Res 51: 405–415.PubMedCrossRefGoogle Scholar
  50. 50.
    Yip, H.K., Y.C. Chang, C.G. Wallace, L.T. Chang, T.H. Tsai, Y.L. Chen, H.W. Chang, S. Leu, Y.Y. Zhen, C.Y. Tsai, et al. 2013. Melatonin treatment improves adipose-derived mesenchymal stem cell therapy for acute lung ischemia-reperfusion injury. J Pineal Res 54: 207–221.PubMedCrossRefGoogle Scholar
  51. 51.
    Sahna, E., H. Parlakpinar, F. Ozturk, Y. Cigremis, and A. Acet. 2003. The protective effects of physiological and pharmacological concentrations of melatonin on renal ischemia-reperfusion injury in rats. Urol Res 31: 188–193.PubMedCrossRefGoogle Scholar
  52. 52.
    Isık, A., S.S. Koca, B. Ustundag, and S. Selek. 2007. Decreased total antioxidant response and increased oxidative stress in Behcet’s disease. Tohoku J Exp Med 212: 133–141.PubMedCrossRefGoogle Scholar
  53. 53.
    Reiter, R.J., C.S. Oh, and O. Fujimori. 1996. Melatonin: Its intracellular and genomic actions. Trends Endocrinol Metab 7: 22–27.PubMedCrossRefGoogle Scholar
  54. 54.
    Ozturk, G., S. Coskun, D. Erbas, and E. Hasanoglu. 2000. The effect of melatonin on liver superoxide dismutase activity, serum nitrate and thyroid hormone levels. Jpn J Physiol 50(1): 149–153.PubMedCrossRefGoogle Scholar
  55. 55.
    Rodriguez, C., J.C. Mayo, R.M. Sainz, et al. 2004. Regulation of antioxidant enzymes: A significant role for melatonin. J Pineal Res 36(1): 1–9.PubMedCrossRefGoogle Scholar
  56. 56.
    Wang, J., Q. Long, W. Zhang, and N. Chen. 2012. Protective effects of exogenous interleukin-18 binding protein in rat model of acute renal ischemia-reperfusion injury. Shock 37(3): 333–340.PubMedCrossRefGoogle Scholar
  57. 57.
    Ates, E., A.U. Yalcin, S. Yilmaz, T. Koken, and C. Tokyol. 2005. Protective effect of erythropoietin on renal ischemia and reperfusion injury. ANZ J Surg 75: 1100–1105.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Ahmet Ahsen
    • 1
  • Yucel Gonul
    • 2
  • Abdurrahman Genc
    • 3
  • Memnune Sena Ulu
    • 4
  • Murat Yagmurca
    • 5
  • Cevdet Ugur Kocogullari
    • 6
  • Sefa Celik
    • 7
  • Seref Yuksel
    • 4
  1. 1.Department of Internal MedicineAfyon Kocatepe University School of MedicineAfyonkarahisarTurkey
  2. 2.Department of AnatomyAfyon Kocatepe University School of MedicineAfyonkarahisarTurkey
  3. 3.Department of PhysiologyAfyon Kocatepe University School of MedicineAfyonkarahisarTurkey
  4. 4.Department of NephrologyAfyon Kocatepe University School of MedicineAfyonkarahisarTurkey
  5. 5.Department of HistologyTurgut Ozal University School of MedicineAnkaraTurkey
  6. 6.Department of Cardiovascular SurgeryKocaeli Derince Training and Research HospitalKocaeliTurkey
  7. 7.Department of BiochemistryAfyon Kocatepe University School of MedicineAfyonkarahisarTurkey

Personalised recommendations