Renoprotective effect of aliskiren on renal ischemia/reperfusion injury in rats: Electron microscopy and molecular study

Renal Failure

Volumn 37, Issue 2, 2015, Pages 343-354

  Ziypak, Tevfik ^a   Halici, Zekai ^a   Alkan, Erdal ^b   Akpinar, Erol ^a   Polat, Beyzagul ^c   Adanur, Senol ^a   Cadirci, Elif ^c   Ferah, Irmak ^c   Bayir, Yasin ^c   Karakus, Emre ^c   Mercantepe, Tolga ^a  

^a ATATURK UNIVERSITY   (Turkey)

^b MEMORIAL HOSPITAL   (Turkey)

^c ATATÜRK UNIVERSITY   (Turkey)

Author keywords

Aliskiren; Antioxidant; Ischemia reperfusion; Rat; Renin

Indexed keywords

ALISKIREN; ANGIOTENSIN II; BETA ACTIN; CREATININE; GLUTATHIONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MALONALDEHYDE; MESSENGER RNA; RENIN; SUPEROXIDE DISMUTASE; AMIDE; ANTIHYPERTENSIVE AGENT; FUMARIC ACID DERIVATIVE; NITRIC OXIDE; PROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CAPILLARY BASEMENT MEMBRANE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DOWN REGULATION; ELECTRON MICROSCOPY; ENZYME ACTIVITY; GENE EXPRESSION; GLOMERULUS CAPILLARY; HISTOPATHOLOGY; KIDNEY INJURY; KIDNEY ISCHEMIA; KIDNEY TUBULE BASEMENT MEMBRANE; MALE; MESANGIUM CELL; NEPHRECTOMY; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; RAT; RENAL PROTECTION; REPERFUSION INJURY; UREA NITROGEN BLOOD LEVEL; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; DRUG EFFECTS; KIDNEY; KIDNEY DISEASES; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; TREATMENT OUTCOME; WISTAR RAT;

AMIDES; ANGIOTENSIN II; ANIMALS; ANTIHYPERTENSIVE AGENTS; CREATININE; FUMARATES; KIDNEY; KIDNEY DISEASES; MALE; MALONDIALDEHYDE; MICROSCOPY, ELECTRON; NITRIC OXIDE; OXIDATIVE STRESS; PROTECTIVE AGENTS; RATS; RATS, WISTAR; RENIN; REPERFUSION INJURY; SUPEROXIDE DISMUTASE; TREATMENT OUTCOME;

EID: 84923182817     PISSN: 0886022X     EISSN: 15256049     Source Type: Journal    
DOI: 10.3109/0886022X.2014.991327     Document Type: Article

References (66)

1. Zimmerman BJ, Granger DN. Reperfusion injury. Surg Clin North America. 1992;72(1):65-83.
2. Huang WC, Elkin EB, Levey AS, Jang TL, Russo P. Partial nephrectomy versus radical nephrectomy in patients with small renal tumors - is there a difference in mortality and cardiovascular outcomes? J Urol. 2009;181(1):55-61; discussion 61-62.
3. Janetschek G. Laparoscopic partial nephrectomy for RCC: How can we avoid ischemic damage of the renal parenchyma? Eur Urol. 2007;52(5):1303-1305.
4. Gao Y, Chen L, Ning Y, et al. Hydro-Jet-assisted laparoscopic partial nephrectomy with no renal arterial clamping: A preliminary study in a single center. Int Urol Nephrol. 2014;46(7):1289-1293.
5. Versteilen AM, Di Maggio F, Leemreis JR, Groeneveld AB, Musters RJ, Sipkema P. Molecular mechanisms of acute renal failure following ischemia/reperfusion. Int J Artif Organs. 2004;27(12):1019-1029.
6. Molitoris BA, Sutton TA. Endothelial injury and dysfunction: Role in the extension phase of acute renal failure. Kidney Int. 2004;66(2):496-499.
7. Edelstein CL, Ling H, Wangsiripaisan A, Schrier RW. Emerging therapies for acute renal failure. Am J Kidney Dis. 1997;30(5 Suppl 4):S89-S95.
8. Mackie FE, Campbell DJ, Meyer TW. Intrarenal angiotensin and bradykinin peptide levels in the remnant kidney model of renal insufficiency. Kidney Int. 2001;59(4):1458-1465.
9. Siamopoulos KC, Kalaitzidis RG. Inhibition of the renin-angiotensin system and chronic kidney disease. Int Urol Nephrol. 2008;40(4):1015-1025.
10. Koid SS, Ziogas J, Campbell DJ. Aliskiren reduces myocardial ischemia-reperfusion injury by a bradykinin B2 receptor- and angiotensin AT2 receptor-mediated mechanism. Hypertension. 2014;63(4):768-773.
11. Zhang W, Han Y, Meng G, et al. Direct renin inhibition with aliskiren protects against myocardial ischemia/reperfusion injury by activating nitric oxide synthase signaling in spontaneously hypertensive rats. J Am Heart Assoc. 2014;3(1):e000606.
12. Choi DE, Jeong JY, Lim BJ, et al. Aliskiren ameliorates renal inflammation and fibrosis induced by unilateral ureteral obstruction in mice. J Urol. 2011;186(2):694-701.
13. Moriyama T, Tsuruta Y, Kojima C, et al. Beneficial effect of aliskiren combined with olmesartan in reducing urinary protein excretion in patients with chronic kidney disease. Int Urol Nephrol. 2012;44(3):841-845.
14. Lizakowski S, Tylicki L, Renke M, et al. Effect of aliskiren on proteinuria in non-diabetic chronic kidney disease: A double-blind, crossover, randomised, controlled trial. Int Urol Nephrol. 2012;44(6):1763-1770.
15. Sun Y, Oberley LW, Li Y. A simple method for clinical assay of superoxide dismutase. Clin Chem. 1988;34(3):497-500.
16. Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem. 1968;25(1):192-205.
17. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351-358.
18. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402-408.
19. Schrier RW, Wang W. Acute renal failure and sepsis. N Engl J Med. 2004;351(2):159-169.
20. Waikar SS, Bonventre JV. Biomarkers for the diagnosis of acute kidney injury. Curr Opin Nephrol Hypertens. 2007;16(6):557-564.
21. Grace PA. Ischemia-reperfusion injury. Br J Surg. 1994;81(5):637-647.
22. Anaya-Prado R, Toledo-Pereyra LH, Lentsch AB, Ward PA. Ischemia/reperfusion injury. J Surg Res. 2002;105(2):248-258.
23. Masztalerz M, Wlodarczyk Z, Czuczejko J, Slupski M, Kedziora J. Superoxide anion as a marker of ischemia-reperfusion injury of the transplanted kidney. Transplant Proc. 2006;38(1):46-48.
24. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrite-induced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys. 1991;288(2):481-487.
25. Szabo C, Zingarelli B, O'Connor M, Salzman AL. DNA strand breakage, activation of poly (ADP-ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite. Proc Nat Acad Sci USA. 1996;93(5):1753-1758.
26. MacMillan-Crow LA, Crow JP, Kerby JD, Beckman JS, Thompson JA. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc Nat Acad Sci USA. 1996;93(21):11853-11858.
27. Yamakura F, Taka H, Fujimura T, Murayama K. Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosine. J Biol Chem. 1998;273(23):14085-14089.
28. Singh I, Gulati S, Orak JK, Singh AK. Expression of antioxidant enzymes in rat kidney during ischemia-reperfusion injury. Mol Cell Biochem. 1993;125(2):97-104.
29. Davies SJ, Reichardt-Pascal SY, Vaughan D, Russell GI. Differential effect of ischemia-reperfusion injury on anti-oxidant enzyme activity in the rat kidney. Exp Nephrol. 1995;3(6):348-354.
30. Conti M, Eschwege P, Ahmed M, et al. Antioxidant enzymatic activities and renal warm ischemia: Correlation with the duration of ischemia. Transplant Proc. 2000;32(8):2740-2741.
31. Kontogiannis J, Burns KD. Role of AT1 angiotensin II receptors in renal ischemic injury. Am J Physiol. 1998;274(1 Pt 2):F79-F90.
32. Hammad FT, Wheatley AM, Davis G. Long-term renal effects of unilateral ureteral obstruction and the role of endothelin. Kidney Int. 2000;58(1):242-250.
33. Habibey R, Ajami M, Hesami A, Pazoki-Toroudi H. The mechanism of preventive effect of captopril on renal ischemia reperfusion injury is independent of ATP dependent potassium channels. Iran Biomed J. 2008;12(4):241-245.
34. Molinas SM, Cortes-Gonzalez C, Gonzalez-Bobadilla Y, et al. Effects of losartan pretreatment in an experimental model of ischemic acute kidney injury. Nephron Exp Nephrol. 2009;112(1):e10-e19.
35. Hammad FT, Al-Salam S, Lubbad L. Does aliskiren protect the kidney following ischemia reperfusion injury? Physiol Res. 2013;62(6):681-690.
36. Schmerbach K, Pfab T, Zhao Y, et al. Effects of aliskiren on stroke in rats expressing human renin and angiotensinogen genes. PLoS One. 2010;5(11):e15052.
37. Shi X, Yan C, Nadtochiy SM, Abe J, Brookes PS, Berk BC. p90 Ribosomal S6 kinase regulates activity of the renin-angiotensin system: A pathogenic mechanism for ischemia-reperfusion injury. J Mol Cell Cardiol. 2011;51(2):272-275.
38. Oyamada S, Bianchi C, Takai S, et al. Impact of acute myocardial ischemia reperfusion on the tissue and blood-borne renin-angiotensin system. Basic Res Cardiol. 2010;105(4):513-522.
39. Kim SM, Kim YG, Jeong KH, et al. Angiotensin II-induced mitochondrial Nox4 is a major endogenous source of oxidative stress in kidney tubular cells. PLoS One. 2012;7(7):e39739.
40. Thurman JM. Triggers of inflammation after renal ischemia/reperfusion. Clin Immunol. 2007;123(1):7-13.
41. Rashikh A, Ahmad SJ, Pillai KK, Kohli K, Najmi AK. Aliskiren attenuates myocardial apoptosis and oxidative stress in chronic murine model of cardiomyopathy. Biomed Pharmacother. 2012;66(2):138-143.
42. Kacmaz A, Polat A, User Y, Tilki M, Ozkan S, Sener G. Octreotide improves reperfusion-induced oxidative injury in acute abdominal hypertension in rats. J Gastrointest Surg. 2004;8(1):113-119.
43. Li N, Wu X, Li L. Chronic administration of clozapine alleviates reversal-learning impairment in isolation-reared rats. Behav Pharmacol. 2007;18(2):135-145.
44. Ikeda U, Maeda Y, Kawahara Y, Yokoyama M, Shimada K. Angiotensin II augments cytokine-stimulated nitric oxide synthesis in rat cardiac myocytes. Circulation. 1995;92(9):2683-2689.
45. Haidara MA, Yassin HZ, Rateb M, Ammar H, Zorkani MA. Role of oxidative stress in development of cardiovascular complications in diabetes mellitus. Curr Vascul Pharmacol. 2006;4(3):215-227.
46. Adachi Y, Hashimoto K, Ono N, et al. Renal effects of a nitric oxide donor, NOC 7, in anesthetized rabbits. Eur J Pharmacol. 1997;324(2-3):223-226.
47. Kim JI, Jang HS, Park KM. Endotoxin-induced renal tolerance against ischemia and reperfusion injury is removed by iNOS, but not eNOS, gene-deletion. BMB Rep. 2010;43(9):629-634.
48. Modlinger PS, Wilcox CS, Aslam S. Nitric oxide, oxidative stress, and progression of chronic renal failure. Semin Nephrol. 2004;24(4):354-365.
49. Walker LM, Walker PD, Imam SZ, Ali SF, Mayeux PR. Evidence for peroxynitrite formation in renal ischemia-reperfusion injury: Studies with the inducible nitric oxide synthase inhibitor L-N(6)-(1-Iminoethyl)lysine. J Pharmacol Exp Ther. 2000;295(1):417-422.
50. Chatterjee PK, Patel NS, Sivarajah A, et al. GW274150, a potent and highly selective inhibitor of iNOS, reduces experimental renal ischemia/reperfusion injury. Kidney Int. 2003;63(3):853-865.
51. Mark LA, Robinson AV, Schulak JA. Inhibition of nitric oxide synthase reduces renal ischemia/reperfusion injury. J Surg Res. 2005;129(2):236-241.
52. Tan CK, Tan EH, Luo B, et al. SMAD3 deficiency promotes inflammatory aortic aneurysms in angiotensin II-infused mice via activation of iNOS. J Am Heart Assoc. 2013;2(3):e000269.
53. Hayashi T, Takai S, Yamashita C. Impact of the renin-angiotensin-aldosterone-system on cardiovascular and renal complications in diabetes mellitus. Curr Vascul Pharmacol. 2010;8(2):189-197.
54. Camara-Lemarroy CR, Guzman-de la Garza FJ, Alarcon-Galvan G, Cordero-Perez P, Fernandez-Garza NE. Effect of sulfasalazine on renal ischemia/reperfusion injury in rats. Renal Fail. 2009;31(9):822-828.
55. Liu WJ, Tang HT, Jia YT, et al. Notoginsenoside R1 attenuates renal ischemia-reperfusion injury in rats. Shock. 2010;34(3):314-320.
56. Ilieva I, Ohgami K, Jin XH, et al. Captopril suppresses inflammation in endotoxin-induced uveitis in rats. Exp Eye Res. 2006;83(3):651-657.
57. He X, Han B, Mura M, et al. Angiotensin-converting enzyme inhibitor captopril prevents oleic acid-induced severe acute lung injury in rats. Shock. 2007;28(1):106-111.
58. Casas JP, Chua W, Loukogeorgakis S, et al. Effect of inhibitors of the renin-angiotensin system and other antihypertensive drugs on renal outcomes: Systematic review and meta-analysis. Lancet. 2005;366(9502):2026-2033.
59. MacKinnon M, Shurraw S, Akbari A, Knoll GA, Jaffey J, Clark HD. Combination therapy with an angiotensin receptor blocker and an ACE inhibitor in proteinuric renal disease: A systematic review of the efficacy and safety data. Am J Kidney Dis. 2006;48(1):8-20.
60. Berthonneche C, Sulpice T, Tanguy S, et al. AT1 receptor blockade prevents cardiac dysfunction after myocardial infarction in rats. Cardiovas Drugs Ther. 2005;19(4):251-259.
61. Wu B, Lin R, Dai R, Chen C, Wu H, Hong M. Valsartan attenuates oxidative stress and NF-kappaB activation and reduces myocardial apoptosis after ischemia and reperfusion. Eur J Pharmacol. 2013;705(1-3):140-147.
62. Friedewald JJ, Rabb H. Inflammatory cells in ischemic acute renal failure. Kidney Int. 2004;66(2):486-491.
63. Farrar CA, Wang Y, Sacks SH, Zhou W. Independent pathways of P-selectin and complement-mediated renal ischemia/reperfusion injury. Am J Pathol. 2004;164(1):133-141.
64. Singbartl K, Ley K. Leukocyte recruitment and acute renal failure. J Mol Med. 2004;82(2):91-101.
65. Singh V, Jain S, Gowthaman U, et al. Co-administration of IL-1+IL-6+TNF-alpha with Mycobacterium tuberculosis infected macrophages vaccine induces better protective T cell memory than BCG. PLoS One. 2011;6(1):e16097.
66. Schreiber S, Nikolaus S, Hampe J, et al. Tumour necrosis factor alpha and interleukin 1beta in relapse of Crohn's disease. Lancet. 1999;353(9151):459-461.