Hyperbaric oxygen preconditioning and the role of NADPH oxidase inhibition in postischemic acute kidney injury induced in spontaneously hypertensive rats


Autoři: Sanjin Kovacevic aff001;  Milan Ivanov aff002;  Zoran Miloradovic aff002;  Predrag Brkic aff003;  Una Jovana Vajic aff002;  Maja Zivotic aff004;  Nevena Mihailovic-Stanojevic aff002;  Djurdjica Jovovic aff002;  Danijela Karanovic aff002;  Rada Jeremic aff003;  Jelena Nesovic-Ostojic aff001
Působiště autorů: Department of Pathophysiology, Medical Faculty, University of Belgrade, Belgrade, Serbia aff001;  Institute for Medical Research, Department of Cardiovascular Physiology, University of Belgrade, Belgrade, Serbia aff002;  Department of Medical Physiology, Medical Faculty, University of Belgrade, Belgrade, Serbia aff003;  Department of Pathology, Medical Faculty, University of Belgrade, Belgrade, Serbia aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0226974

Souhrn

Renal ischemia/reperfusion injury is a common cause of acute kidney injury (AKI) and hypertension might contribute to the increased incidence of AKI. The purpose of this study was to investigate the effects of single and combined hyperbaric oxygen (HBO) preconditioning and NADPH oxidase inhibition on oxidative stress, kidney function and structure in spontaneously hypertensive rats (SHR) after renal ischemia reperfusion injury. HBO preconditioning was performed by exposing to pure oxygen (2.026 bar) twice a day for two consecutive days for 60 minutes, and 24h before AKI induction. For AKI induction, the right kidney was removed and ischemia was performed by clamping the left renal artery for 45 minutes. NADPH oxidase inhibition was induced by apocynin (40 mg/kg b.m., intravenously) 5 minutes before reperfusion. AKI significantly increased renal vascular resistance and reduced renal blood flow, which were significantly improved after apocynin treatment. Also, HBO preconditioning, with or without apocynin treatment showed improvement on renal hemodynamics. AKI significantly increased plasma creatinine, urea, phosphate levels and lipid peroxidation in plasma. Remarkable improvement, with decrease in creatinine, urea and phosphate levels was observed in all treated groups. HBO preconditioning, solitary or with apocynin treatment decreased lipid peroxidation in plasma caused by AKI induction. Also, combined with apocynin, it increased catalase activity and solitary, glutathione reductase enzyme activity in erythrocytes. While AKI induction significantly increased plasma KIM– 1 levels, HBO preconditioning, solitary or with apocynin decreased its levels. Considering renal morphology, significant morphological alterations present after AKI induction were significantly improved in all treated groups with reduced tubular dilatation, tubular necrosis in the cortico-medullary zone and PAS positive cast formation. Our results reveal that NADPH oxidase inhibition and hyperbaric oxygen preconditioning, with or without NADPH oxidase inhibition may have beneficial effects, but their protective role should be evaluated in further studies.

Klíčová slova:

Blood plasma – Hemodynamics – Hypertension – Kidneys – Lipid peroxidation – Oxidative stress – Oxygen – Renal ischemia


Zdroje

1. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest. 2011;121(11):4210–21. doi: 10.1172/JCI45161 22045571

2. Coca SG, Yusuf B, Shlipak MG, Garg AX, Parikh CR. Long-term risk of mortality and other adverse outcomes after acute kidney injury: a systematic review and meta-analysis. Am J Kidney Dis. 2009;53(6):961–973. doi: 10.1053/j.ajkd.2008.11.034 19346042

3. Choi HM, Kim SC, Kim MG, Jo SK, Cho WY, Kim HK. Etiology and outcomes of anuria in acute kidney injury: a single center study. Kidney research and clinical practice. 2015;34(1):13–19. doi: 10.1016/j.krcp.2014.11.002 26484014

4. Cartin-Ceba R, Kashiouris M, Plataki M, Kor DJ, Gajic O, Casey ET. Risk factors for development of acute kidney injury in critically ill patients: a systematic review and meta-analysis of observational studies. Criti care res pract. 2012;2012:691013.

5. Liano F, Pascual J. Epidemiology of acute renal failure: a prospective, multicenter, community-based study. Madrid Acute Renal Failure Study Group. Kidney Int. 1996;50(3):811–818. 8872955

6. Ivanov M, Mihailovic-Stanojevic N, Grujic Milanovic J, Jovovic D, Markovic-Lipkovski J, Cirovic S, et al. Losartan improved antioxidant defense, renal function and structure of postischemic hypertensive kidney. PloS one. 2014;9(5):e96353. doi: 10.1371/journal.pone.0096353 24796787

7. Miloradovic Z, Ivanov M, Mihailovic-Stanojevic N, Grujic Milanovic J, Jovovic D, Vajic UJ, et al. Acute superoxide radical scavenging reduces blood pressure but does not influence kidney function in hypertensive rats with postischemic kidney injury. Biomed Res Int. 2014;2014:512619.

8. Ratliff BB, Abdulmahdi W, Pawar R, Wolin MS. Oxidant Mechanisms in Renal Injury and Disease. Antioxid Redox Signal. 2016;25(3):119–146. doi: 10.1089/ars.2016.6665 26906267

9. Li Z, Wang Y. Effect of NADPH oxidase inhibitor-apocynin on the expression of Src homology-2 domain-containing phosphatase-1 (SHP-1) exposed renal ischemia/reperfusion injury in rats. Toxicol Rep. 2015;2:1111–1116. doi: 10.1016/j.toxrep.2015.07.019 28962452

10. Stefanska J, Pawliczak R. Apocynin: molecular aptitudes. Mediators Inflamm. 2008;2008:106507.

11. Calvert JW, Cahill J, Zhang JH. Hyperbaric oxygen and cerebral physiology. Neurol Res. 2007;29(2):132–41. doi: 10.1179/016164107X174156 17439697

12. Lavrnja I, Parabucki A, Brkic P, Jovanovic T, Dacic S, Savic D, et al. Repetitive hyperbaric oxygenation attenuates reactive astrogliosis and suppresses expression of inflammatory mediators in the rat model of brain injury. Mediat Inflamm. 2015; 2015:498405.

13. Parabucki A, Bozic I, Bjelobaba I, Lavrnja I, Brkic P, Jovanov T, et al. Hyperbaric oxygenation alters temporal expression pattern of superoxide dismutase 2 after cortical stab injury in rats. Croat Med J. 2012; 53(6):586–597. doi: 10.3325/cmj.2012.53.586 23275324

14. Hentia C, Rizzato A, Camporesi E, Yang Z, Muntean DM, Săndesc D, et al. An overview of protective strategies against ischemia/reperfusion injury: The role of hyperbaric oxygen preconditioning. Brain Behav. 2018;8(5):e00959. doi: 10.1002/brb3.959 29761012

15. Drenjancevic I, Kibel A, Kibel D, Seric V, Cosic A. Blood pressure, acid-base and blood gas status and indicators of oxidative stress in healthy male rats exposed to acute hyperbaric oxygenation. Undersea Hyperb Med. 2013;40(4):319–328. 23957202

16. Mihaljevic Z, Matic A, Stupin A, Rasic L, Jukic I, Drenjancevic I. Acute Hyperbaric Oxygenation, Contrary to Intermittent Hyperbaric Oxygenation, Adversely Affects Vasorelaxation in Healthy Sprague-Dawley Rats due to Increased Oxidative Stress. Oxid Med Cell Longev. 2018;2018:7406027.

17. Mas-Font S, Ros-Martinez J, Perez-Calvo C, Villa-Diaz P, Aldunate-Calvo S, Moreno-Clari E. Prevention of acute kidney injury in Intensive Care Units. Med Intensiva. 2017;41(2):116–126. doi: 10.1016/j.medin.2016.12.004 28190602

18. Brkic P, Mitrovic A, Rakic M, Grajic M, Jovanovic T. Hyperbaric oxygen therapy of angiopathic changes in patients with inherited gene imbalance. Srp Arh Celok Lek. 2007;135(11–12):669–671.

19. Weaver LK. Hyperbaric oxygen therapy indications: the Hyperbaric Oxygen Therapy Committee report. 13th ed. North Palm Beach, Florida: Best Publishing Company; 2014.

20. Vajic UJ, Grujic-Milanovic J, Miloradovic Z, Jovovic D, Ivanov M, Karanovic D, et al. Urtica dioica L. leaf extract modulates blood pressure and oxidative stress in spontaneously hypertensive rats. Phytomedicine. 2018;46:39–45. doi: 10.1016/j.phymed.2018.04.037 30097121

21. Paravicini TM, Touyz RM. NADPH oxidases, reactive oxygen species, and hypertension: clinical implications and therapeutic possibilities. Diabetes Care. 2008;31(2):S170–180.

22. Sureda A, Ferrer MD, Batle JM, Tauler P, Tur JA, Pons A. Scuba diving increases erythrocyte and plasma antioxidant defenses and spares NO without oxidative damage. Med Sci Sports Exerc. 2009;41(6):1271–1276. doi: 10.1249/MSS.0b013e3181951069 19461538

23. Labrouche S, Javorschi S, Leroy D, Gbikpi-Benissan G, Freyburger G. Influence of hyperbaric oxygen on leukocyte functions and haemostasis in normal volunteer divers. Thromb Res. 1999;96(4):309–315. doi: 10.1016/s0049-3848(99)00107-3 10593434

24. Kim CH, Choi H, Chun YS, Kim GT, Park JW, Kim MS. Hyperbaric oxygenation pretreatment induces catalase and reduces infarct size in ischemic rat myocardium. Pflugers Arch. 2001;442(4):519–525. doi: 10.1007/s004240100571 11510883

25. Moreno S, Mugnaini E, Ceru MP. Immunocytochemical localization of catalase in the central nervous system of the rat. J Histochem Cytochemistry. 1995;43(12):1253–1267.

26. Simons JM, Hart BA, Ip Vai Ching TR, Van Dijk H, Labadie RP. Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils. Free Radic Biol Med. 1990;8(3):251–258. doi: 10.1016/0891-5849(90)90070-y 2160411

27. Heumuller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schroder K, et al. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension. 2008;51(2):211–217. doi: 10.1161/HYPERTENSIONAHA.107.100214 18086956

28. Tian N, Moore RS, Phillips WE, Lin L, Braddy S, Pryor JS, et al. NADPH oxidase contributes to renal damage and dysfunction in Dahl salt-sensitive hypertension. Am J Physiol Regul Integr Comp Physiol. 2008;295(6):R1858–1865. doi: 10.1152/ajpregu.90650.2008 18922960

29. Rybka J, Kupczyk D, Kedziora-Kornatowska K, Motyl J, Czuczejko J, Szewczyk-Golec K, et al. Glutathione-related antioxidant defense system in elderly patients treated for hypertension. Cardiovasc Toxicol. 2011;11(1):1–9. doi: 10.1007/s12012-010-9096-5 21140238

30. Tokuda Y, Uozumi T, Kawasaki T. The superoxide dismutase activities of cerebral tissues, assayed by the chemiluminescence method, in the gerbil focal ischemia/reperfusion and global ischemia models. Neurochem Int. 1993;23(2):107–114. doi: 10.1016/0197-0186(93)90087-l 8369736

31. Meng XM, Ren GL, Gao L, Yang Q, Li HD, Wu WF, et al. NADPH oxidase 4 promotes cisplatin-induced acute kidney injury via ROS-mediated programmed cell death and inflammation. Lab Invest. 2018;98(1):63–78. doi: 10.1038/labinvest.2017.120 29106395

32. Park YM, Park MY, Suh YL, Park JB. NAD(P)H oxidase inhibitor prevents blood pressure elevation and cardiovascular hypertrophy in aldosterone-infused rats. Biochem Biophys Res Commun. 2004;313(3):812–817. doi: 10.1016/j.bbrc.2003.11.173 14697264

33. Kinsey GR, Okusa MD. Role of leukocytes in the pathogenesis of acute kidney injury. Crit Care. 2012;16(2):214. doi: 10.1186/cc11228 22429752

34. Kelly KJ, Williams WW, Colvin JRB, Meehan SM, Springer TA, Gutierrez-Ramos JC, et al. Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J Clin Invest. 1996;97(4):1056–1063. doi: 10.1172/JCI118498 8613529

35. Li L, Huang L, Sung SS, Lobo PI, Brown MG, Gregg RK, et al. NKT cell activation mediates neutrophil IFN-gamma production and renal ischemia-reperfusion injury. J Immunol. 2007;178(9):5899–911. doi: 10.4049/jimmunol.178.9.5899 17442974

36. Tadagavadi RK, Reeves BW. Renal dendritic cells ameliorate nephrotoxic acute kidney injury. J Am Soc Nephrol. 2010; 21(1):53–63. doi: 10.1681/ASN.2009040407 19875815

37. Schlüter T, Steinbach AC, Steffen A, Rettig R, Grisk O. Apocynin-induced vasodilation involves Rho kinase inhibition but not NADPH oxidase inhibition. Cardiovasc Res. 2008;80(2):271–279. doi: 10.1093/cvr/cvn185 18596059

38. Rubinstein I, Abassi Z, Milman F, Ovcharenko E, Coleman R, Winaver J, et al. Hyperbaric oxygen treatment improves GFR in rats with ischaemia/reperfusion renal injury: a possible role for the antioxidant/oxidant balance in the ischaemic kidney. Nephrol Dial Transplant. 2009;24(2):428–36. doi: 10.1093/ndt/gfn511 18799609

39. Klemetti E, Rico-Vargas S, Mojon P. Short duration hyperbaric oxygen treatment effects blood flow in rats: pilot observations. Lab Anim. 2005; 39(1):116–121. doi: 10.1258/0023677052886529 15703133

40. Li J, Liu W, Ding S, Xu W, Guan Y, Zhang JH, et al. Hyperbaric oxygen preconditioning induces tolerance against brain ischemia-reperfusion injury by upregulation of antioxidant enzymes in rats. Brain Res. 2008;1210:223–229. doi: 10.1016/j.brainres.2008.03.007 18407255

41. Welch WJ, Baumgartl H, Lubbers D, Wilcox CS. Nephron pO2 and renal oxygen usage in the hypertensive rat kidney. Kidney Int. 2001;59(1):230–237. 11135075

42. Bowmer CJ, Nichols AJ, Warren M, Yates MS. Cardiovascular responses in rats with glycerol-induced acute renal failure. Br J Pharmacol. 1983;79(2):471–476. doi: 10.1111/j.1476-5381.1983.tb11020.x 6652338

43. Baumer AT, Kruger CA, Falkenberg J, Freyhaus HT, Rosen R, Fink K, et al. The NAD(P)H oxidase inhibitor apocynin improves endothelial NO/superoxide balance and lowers effectively blood pressure in spontaneously hypertensive rats: comparison to calcium channel blockade. Clin Exp Hypertens. 2007;29(5):297–299.

44. Virdis A, Gesi M, Taddei S. Impact of apocynin on vascular disease in hypertension. Vascul Pharmacol. 2016;87:1–5. doi: 10.1016/j.vph.2016.08.006 27569106

45. Rubinger D, Wald H, Gimelreich D, Halaihel N, Rogers T, Levi M, et al. Regulation of the renal sodium-dependent phosphawete cotransporter NaPi2 (Npt2) in acute renal failure due to ischemia and reperfusion. Nephron Physiol. 2005;100(1):1–12.

46. Mohamed NS, Mubarak HA. Effects of renal ischemia reperfusion on brain, liver & kidney tissues in adult male rats. Life Sciences. 2011;8:204–212.

47. Kim SY, Moon KA, Jo HY, Jeong S, Seon SH, Jung E, et al. Anti-inflammatory effects of apocynin, an inhibitor of NADPH oxidase, in airway inflammation. Immunol Cell Biol. 2012;90(4):441–448. doi: 10.1038/icb.2011.60 21709687

48. Altintas R, Polat A, Vardi N, Oguz F, Beytur A, Sagir M, et al. The protective effects of apocynin on kidney damage caused by renal ischemia/reperfusion. J Endourol. 2013;27(5):617–624. doi: 10.1089/end.2012.0556 23387559

49. Abdelrahman RS. Protective effect of apocynin against gentamicin-induced nephrotoxicity in rats. Hum Exp Toxicol. 2018;37(1):27–37. doi: 10.1177/0960327116689716 28116922

50. Tajra LC, Martin X, Margonari J, Blanc-Brunat N, Ishibashi M, Vivier G, et al. In vivo effects of monoclonal antibodies against rat beta(2) integrins on kidney ischemia-reperfusion injury. J Surg Res. 1999;87(1):32–8. doi: 10.1006/jsre.1999.5724 10527701

51. Rabb H. Role of leukocytes and leukocyte adhesion molecules in renal ischemic-reperfusion injury. Fronti Biosci. 1996;1:e9–14.

52. He X, Xu X, Fan M, Chen X, Sun X, Luo G, et al. Preconditioning with hyperbaric oxygen induces tolerance against renal ischemia-reperfusion injury via increased expression of heme oxygenase-1. J Surg Res. 2011;170(2):e271–277. doi: 10.1016/j.jss.2011.06.008 21816440

53. Sabbisetti VS, Waikar SS, Antoine DJ, Smiles A, Wang C, Ravisankar A, et al. Blood kidney injury molecule-1 is a biomarker of acute and chronic kidney injury and predicts progression to ESRD in type I diabetes. J Am Soc Nephrol. 2014;25(10):2177–2186. doi: 10.1681/ASN.2013070758 24904085


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