Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 4139851, 7 pages
http://dx.doi.org/10.1155/2016/4139851
Research Article

Tempol, a Membrane-Permeable Radical Scavenger, Exhibits Anti-Inflammatory and Cardioprotective Effects in the Cerulein-Induced Pancreatitis Rat Model

1Chair and Department of Pathophysiology, Medical University of Lublin, 20-090 Lublin, Poland
2Chair and Department of Clinical Pathomorphology, Medical University of Lublin, 20-090 Lublin, Poland
3Department of Pharmacology, Medical University of Lublin, 20-093 Lublin, Poland
4Chair and Department of Vascular Surgery and Angiology, Medical University of Lublin, 20-081 Lublin, Poland
5Department of Pharmacology, University of Life Sciences in Lublin, 20-033 Lublin, Poland

Received 4 June 2015; Revised 30 August 2015; Accepted 31 August 2015

Academic Editor: Swaran J. S. Flora

Copyright © 2016 Andrzej Marciniak et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. P. Sah, R. K. Dawra, and A. K. Saluja, “New insights into the pathogenesis of pancreatitis,” Current Opinion in Gastroenterology, vol. 29, no. 5, pp. 523–530, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. J. J. De Waele, “Acute pancreatitis,” Current Opinion in Critical Care, vol. 20, no. 2, pp. 189–195, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Escobar, J. Pereda, A. Arduini et al., “Oxidative and nitrosative stress in acute pancreatitis. Modulation by pentoxifylline and oxypurinol,” Biochemical Pharmacology, vol. 83, no. 1, pp. 122–130, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Milnerowicz, M. Jabłonowska, and A. Bizoń, “Change of zinc, copper, and metallothionein concentrations and the copper-zinc superoxide dismutase activity in patients with pancreatitis,” Pancreas, vol. 38, no. 6, pp. 681–688, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Wang, S. Wang, A. Tang, H. Gong, P. Ma, and L. Chen, “Combined effects of sivelestat and resveratrol on severe acute pancreatitis-associated lung injury in rats,” Experimental Lung Research, vol. 40, no. 6, pp. 288–297, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. A. L. Farré and S. Casado, “Heart failure, redox alterations, and endothelial dysfunction,” Hypertension, vol. 38, no. 6, pp. 1400–1405, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Petit, “Anthracycline-induced cardiotoxicity,” Bulletin du Cancer, vol. 91, supplement 3, pp. 159–165, 2004. View at Google Scholar · View at Scopus
  8. A. Blum, “Heart failure—new insights,” Israel Medical Association Journal, vol. 11, no. 2, pp. 105–111, 2009. View at Google Scholar · View at Scopus
  9. S. E. Aune, S. T. Yeh, P. Kuppusamy, M. L. Kuppusamy, M. Khan, and M. G. Angelos, “Sivelestat attenuates myocardial reperfusion injury during brief low flow postischemic infusion,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 279847, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. B.-Q. Cheng, C.-T. Liu, W.-J. Li et al., “Ethyl pyruvate improves survival and ameliorates distant organ injury in rats with severe acute pancreatitis,” Pancreas, vol. 35, no. 3, pp. 256–261, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. X. Du, Y. Cao, P. Xue, Z. Lin, Z. Zeng, and Q. Xia, “Protective effect of intermedin on myocardial cell in a rat model of severe acute pancreatitis,” Cellular and Molecular Biology Letters, vol. 16, no. 3, pp. 462–476, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. K. K. Kao and M. P. Fink, “The biochemical basis for the anti-inflammatory and cytoprotective actions of ethyl pyruvate and related compounds,” Biochemical Pharmacology, vol. 80, no. 2, pp. 151–159, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. B. P. Soule, F. Hyodo, K.-I. Matsumoto et al., “The chemistry and biology of nitroxide compounds,” Free Radical Biology and Medicine, vol. 42, no. 11, pp. 1632–1650, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. C. S. Wilcox and A. Pearlman, “Chemistry and antihypertensive effects of tempol and other nitroxides,” Pharmacological Reviews, vol. 60, no. 4, pp. 418–469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. C. S. Wilcox, “Effects of tempol and redox-cycling nitroxides in models of oxidative stress,” Pharmacology and Therapeutics, vol. 126, no. 2, pp. 119–145, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Bartha, I. Solti, A. Szabo et al., “Regulation of kinase cascade activation and heat shock protein expression by poly(ADP-ribose) polymerase inhibition in doxorubicin-induced heart failure,” Journal of Cardiovascular Pharmacology, vol. 58, no. 4, pp. 380–391, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. W. Zhou, B. A. Levine, and M. S. Olson, “Lipid mediator production in acute and chronic pancreatitis in the rat,” Journal of Surgical Research, vol. 56, no. 1, pp. 37–44, 1994. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Buyukberber, M. C. Savaş, C. Bagci et al., “Therapeutic effect of caffeic acid phenethyl ester on cerulein-induced acute pancreatitis,” World Journal of Gastroenterology, vol. 15, no. 41, pp. 5181–5185, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Lampel and H. F. Kern, “Acute interstitial pancreatitis in the rat induced by excessive doses of a pancreatic secretagogue,” Virchows Archiv A: Pathological Anatomy and Histology, vol. 373, no. 2, pp. 97–117, 1977. View at Publisher · View at Google Scholar
  20. A. Marciniak, M. Klonowska, M. Chomicki, E. Szpringer, K. Lutnicki, and A. Wojtak, “Effects of a low molecular weight superoxide dismutase mimic, 4-hydroxy-tempo on the lipid peroxidation in burned rats,” Bulletin of the Veterinary Institute in Pulawy, vol. 49, no. 1, pp. 101–106, 2005. View at Google Scholar · View at Scopus
  21. S. M. Hahn, A. M. Deluca, D. Coffin, C. M. Krishna, and J. B. Mitchell, “In vivo radioprotection and effects on blood pressure of the stable free radical nitroxides,” International Journal of Radiation Oncology Biology Physics, vol. 42, no. 4, pp. 839–842, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Leach, S. Frank, A. Olbrich, J. Pfeilschifter, and C. Thiemermann, “Decline in the expression of copper/zinc superoxide dismutase in the kidney of rats with endotoxic shock: effects of the superoxide anion radical scavenger, tempol, on organ injury,” British Journal of Pharmacology, vol. 125, no. 4, pp. 817–825, 1998. View at Publisher · View at Google Scholar · View at Scopus
  23. M. M. Lerch, P. Hoppe-Seyler, and W. Gerok, “Origin and development of exocrine pancreatic insufficiency in experimental renal failure,” Gut, vol. 35, no. 3, pp. 401–407, 1994. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Tani, M. Otsuki, H. Itoh et al., “Histologic and biochemical alterations in experimental acute pancreatitis induced by supramaximal caerulein stimulation,” International Journal of Pancreatology, vol. 2, no. 5-6, pp. 337–348, 1987. View at Publisher · View at Google Scholar · View at Scopus
  25. I. F. F. Benzie and J. J. Strain, “The ferric reducing ability of plasma (FRAP) as a measure of ‘antioxidant power’: the FRAP assay,” Analytical Biochemistry, vol. 239, no. 1, pp. 70–76, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. I. Erdelmeier, D. Gérard-Monnier, K. Régnard, N. Moze-Henry, J.-C. Yadan, and J. Chaudière, “Reactions of 1-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Analytical applications to a colorimetric assay of lipid peroxidation,” Chemical Research in Toxicology, vol. 11, no. 10, pp. 1176–1183, 1998. View at Publisher · View at Google Scholar · View at Scopus
  27. G. L. Ellman, “Tissue sulfhydryl groups,” Archives of Biochemistry and Biophysics, vol. 82, no. 1, pp. 70–77, 1959. View at Publisher · View at Google Scholar · View at Scopus
  28. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Y. Song, J. W. Lim, H. Kim, T. Morio, and K. H. Kim, “Oxidative stress induces nuclear loss of DNA repair proteins Ku70 and Ku80 and apoptosis in pancreatic acinar AR42J cells,” Journal of Biological Chemistry, vol. 278, no. 38, pp. 36676–36687, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Kasai and K. Kawai, “Oxidative DNA damage: mechanisms and significance in health and disease,” Antioxidants & Redox Signaling, vol. 8, no. 5-6, pp. 981–983, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. F. M. Yilmaz, G. Yilmaz, M. F. Erol, S. Köklü, and D. Yücel, “Nitric oxide, lipid peroxidation and total thiol levels in acute appendicitis,” Journal of Clinical Laboratory Analysis, vol. 24, no. 2, pp. 63–66, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Yegneswaran, J. B. Kostis, and C. S. Pitchumoni, “Cardiovascular manifestations of acute pancreatitis,” European Journal of Emergency Medicine, vol. 6, no. 1, pp. 27–29, 1999. View at Google Scholar
  33. R. Pezzilli, B. Barakat, P. Billi, and B. Bertaccini, “Electrocardiographic abnormalities in acute pancreatitis,” European Journal of Emergency Medicine, vol. 6, no. 1, pp. 27–29, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Rubio-Tapia, J. García-Leiva, E. Asensio-Lafuente, G. Robles-Díaz, and F. Vargas-Vorácková, “Electrocardiographic abnormalities in patients with acute pancreatitis,” Journal of Clinical Gastroenterology, vol. 39, no. 9, pp. 815–818, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. C. A. Albrecht and F. A. Laws, “ST segment elevation pattern of acute myocardial infarction induced by acute pancreatitis,” Cardiology in Review, vol. 11, no. 3, pp. 147–151, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. J. H. Yu, J. W. Lim, H. Kim, and K. H. Kim, “NADPH oxidase mediates interleukin-6 expression in cerulein-stimulated pancreatic acinar cells,” The International Journal of Biochemistry & Cell Biology, vol. 37, no. 7, pp. 1458–1469, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. J. H. Yu and H. Kim, “Oxidative stress and inflammatory signaling in cerulein pancreatitis,” World Journal of Gastroenterology, vol. 20, no. 46, pp. 17324–17329, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. D. B. Gough, B. Boyle, W. P. Joyce et al., “Free radical inhibition and serial chemiluminescence in evolving experimental pancreatitis,” British Journal of Surgery, vol. 77, no. 11, pp. 1256–1259, 1990. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Reinheckel, J. Prause, B. Nedelev et al., “Oxidative stress affects pancreatic proteins during the early pathogenesis of rat caerulein pancreatitis,” Digestion, vol. 60, no. 1, pp. 56–62, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Kruse, M. E. Anderson, and S. Loft, “Minor role of oxidative stress during intermediate phase of acute pancreatitis in rats,” Free Radical Biology and Medicine, vol. 30, no. 3, pp. 309–317, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Dąbrowska, D. Jacewicz, A. Łapińska et al., “Pivotal participation of nitrogen dioxide in L-arginine induced acute necrotizing pancreatitis: protective role of superoxide scavenger 4-OH-TEMPO,” Biochemical and Biophysical Research Communications, vol. 326, no. 2, pp. 313–320, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. Z. Śledziński, M. Woźniak, J. Antosiewicz et al., “Protective effect of 4-hydroxy-TEMPO, a low molecular weight superoxide dismutase mimic, on free radical toxicity in experimental pancreatitis,” International Journal of Pancreatology, vol. 18, no. 2, pp. 153–160, 1995. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Cuzzocrea, M. C. McDonald, E. Mazzon et al., “Tempol, a membrane-permeable radical scavenger, reduces dinitrobenzene sulfonic acid-induced colitis,” European Journal of Pharmacology, vol. 406, no. 1, pp. 127–137, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Cuzzocrea, M. C. McDonald, H. M. Filipe et al., “Effects of tempol, a membrane-permeable radical scavenger, in a rodent model of carrageenan-induced pleurisy,” European Journal of Pharmacology, vol. 390, no. 1-2, pp. 209–222, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Murakami, A. Nakao, W. Kishimoto, M. Nakano, and H. Takagi, “Detection of O2- generation and neutrophil accumulation in rat lungs after acute necrotizing pancreatitis,” Surgery, vol. 118, no. 3, pp. 547–554, 1995. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Szuster-Ciesielska, J. Daniluk, and M. Kandefer-Szersze, “Oxidative stress in blood of patients with alcohol-related pancreatitis,” Pancreas, vol. 22, no. 3, pp. 261–266, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Tsuji, N. Watanabe, T. Okamoto, and Y. Niitsu, “Specific interaction of pancreatic elastase and leucocytes to produce oxygen radicals and its implication in pancreatitis,” Gut, vol. 35, no. 11, pp. 1659–1664, 1994. View at Publisher · View at Google Scholar · View at Scopus
  48. G. Chen, F. Xu, J. Li, and S. Lu, “Depletion of neutrophils protects against l-arginine-induced acute pancreatitis in mice,” Cellular Physiology and Biochemistry, vol. 35, no. 6, pp. 2111–2120, 2015. View at Publisher · View at Google Scholar