THE ROLE OF PHARMACOLOGICAL PRECONDITIONING IN RENAL ISCHEMIC AND REPERFUSION INJURY


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Abstract

Renal ischemic and reperfusion injury resulting in acute renal failure is a multidisciplinary problem at the junction of pathophysiology, transplantology, urology, nephrology, cardiac surgery and pharmacology. One of renal protection strategies is using the phenomenon of preconditioning. Preconditioning is one of the ways to adopt a tissue to repeated short-term effects of damaging factors to induce an enhanced tolerance to the long period of hypoxia and/or ischemia. There are multiple cellular and molecular mechanisms of the renal protective effects of preconditioning stimuli, but the key effectors and signaling molecules are ATP-dependent potassium channels, nitric oxide synthase, nitric oxide, and mitochondrial pore. Contradictory data on the protective effect of ischemic preconditioning allow searching for approaches to pharmacological correction of ischemic and reperfusion injuries. The article provides data on possible ways of using erythropoietin, darbepoetin and phosphodiesterase 5 inhibitors.

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About the authors

D. A Kostina

Belgorod State National Research University

Email: kostina_da@bsu.edu.ru
Ph.D. Student at the Department of Pharmacology Belgorod, Russia

T. G Pokrovskaya

Belgorod State National Research University

Email: pokrovskaia-tg@mail.ru
Dr.Med.Sci., Professor at the Department of Pharmacology Belgorod, Russia

Yu. V Olefir

Scientific Center on Expertise of Medical Application Products of Minzdrav of Russia

Dr.Med.Sci., Direcor General Moscow, Russia

A. N Yavorskii

Scientific Center on Expertise of Medical Application Products of Minzdrav of Russia

Email: Alexyavorsky@expmed.ru
Dr.Med.Sci., Scientific Secretary Moscow, Russia

V. V Elagin

Kursk State Medical University, of Minzdrav of Russia

Email: vlad.elagin2014@yandex.ru
Ph.D. Student at the Department of Urology Kursk, Russia

References

  1. Chatauret N., Badet L., Barrou B., Hauet T. Ischemia-reperfusion: from cell biology to acute kidney injury. Prog Urol. 2014;24(1):4-12.
  2. Lerman L., Textor S.C. Pathophysiology of ischemic nephropathy. Urol Clin North Am. 2001;28:793-803.
  3. Hammad F.T., Lubbad L. The effect ofthymoquinone on the renal functions following ischemia-reperfusion injury in the rat. International Journal of Physiology, Pathophysiology and Pharmacology. 2016;8(4):152-159.
  4. Touijer K., Jacqmin D., Kavoussi L.R., Montorsi F., Patard J.J., Rogers C.G., Russo P., Uzzo R.G., Van Poppel H. The expanding role of partial nephrectomy: a critical analysis of indications, results, and complications. Eur Urol. 2010;57:214-222, doi: 10.1016/j.eururo.2009.10.019.
  5. Lauver D.A., Carey E.G., Bergin I.L., Lucchesi B.R., Gurm H.S. Sildenafil citrate for prophylaxis of nephropathy in an animal model of contrast-induced acute kidney injury. PLoS ONE. 2014;9(11):e113598. doi: 10.1371/journal.pone.0113598.
  6. Mao H., Katz N., Ariyanon W., Blanca-Martos L., Adýbelli Z., Giuliani A., Danesi T.H., Kim J.C., Nayak A., Neri M., Virzi G.M., Brocca A., Scalzotto E., Salvador L., Ronco C. Cardiac surgery-associated acute kidney injury. Cardiorenal Medicine. 2013;3(3):178-199. doi: 10.1159/000353134.
  7. Арустамова А.А., Покровский М.В., Шабельникова А.С., Кашуба А.С., Якушев В.И. Фармакологическое прекондиционирование ишемических повреждений сетчатки. Научные ведомости Белгородского государственного университета. Серия: Медицина. Фармация. 2012;22(141):13-19
  8. Даниленко Л.М. Роль митохондриальных АТФ-зависимых калиевых каналов в кардиопротекторном эффекте никорандила на модели коронарооклюзионного инфаркта миокарда. Научный результат. Серия «Медицина и фармация». 2015;4(6):40-44
  9. Даниленко Л.М., Покровский М.В., Денисюк Т.А., Колесник И.М., Алехин С.А. NO в сигнальном каскаде фармакологического прекондиционирования при ишемии-реперфузии миокарда. Ведомости Научного центра экспертизы средств медицинского применения 2015;210.
  10. Kolesnik I.M., Pokrovskii M.V., Lazarenko V.A. Pharmacological preconditioning with erythropoietin new possibilities for optimization ofischemic tissues survival potential. Kurskij nauchno-prakticheskij vestnik «Cheloveki ego zdorov’e». 2010;3:32-36
  11. Murry C.E., Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74(5):1124-1136
  12. Лихванцев В.В., Мороз В.В., Гребенчиков О.А., Гороховатский Ю.И., Заржецкий Ю.В., Тимошин С.С., Левиков Д.И., Шайбакова В.Л. Ишемическое и фармакологическое прекондиционирование. Общая реаниматология. 2012;VIII(1):61-66
  13. Anttila V., Haapanen H., Yannopoulos F., Herajärvi J., Anttila T., Juvonen T. Review of remote ischemic preconditioning: from laboratory studies to clinical trials. Scandinavian Cardiovascular Journal 2016;50(5-6) : 355-361
  14. Должикова И.Н., Покровский М.В., Должиков А.А. Морфологическое и иммунногистохимическое исследование почек при ишемии и на фоне дистантного и фармакологического прекондиционирования. Научный аспект. 2015;2(3):282-308
  15. Zhang C., Rosenbaum D.M., Shaikh A.R., Li Q., Rosenbaum P.S., Pelham D.J., Roth S. Ischemic preconditioning attenuates apoptotic cell death in the rat retina. Invest. Ophthalmol. Vis. Sci. 2002;43(9):3059-3066.
  16. Peresypkina A.A., Gubareva V.O., Levkova E.A., Shabelnikova A.S. Correction of retinal angiopathy of hypertensive type by minoxidil, sildenafil in experiment. Research result: pharmacology and clinical pharmacology. 2016;2(4) : 34-44. doi: 10.18413/2500-235X-2016-2-4-34-44.
  17. Kolesnik I.M., Pokrovskii M.V., Lazarenko V.A. Experimental substantiation of an opportunity of the use of vardenafil for pharmacological preconditioning in surgery. Kubanskij nauchnyj meditsinskij vestnik. 2015;2(151):77-81.
  18. Gureev V.V. New approaches of morfofunktional pharmacological correction of violations of cardiovascular system in experimental preeclampsia. Research result: pharmacology and clinical pharmacology. 2016;2(3):11-27.
  19. Joo J.D., Kim M., D’Agati V.D., Lee H.T. Ischemic preconditioning provides both acute and delayed protection against renal ischemia and reperfusion injury in mice. J Am Soc Nephrol. 2006;17:3115-3123.
  20. Park K.M., Byun J.Y., Kramers C., Kim J.I., Huang P.L., Bonventre J.V. Inducible nitric-oxide synthase is an important contributor to prolonged protective effects of ischemic preconditioning in the mouse kidney. J BiolChem 2003;278:2725627266.
  21. Levchenkova O.S., Novikov V.E. Possibilities of pharmacological preconditioning. Vestnik Rossijskoj akademii meditsinskikh nauk. 2016;71( 1): 16-24.
  22. Schulz R., Cohen M.V., Behrends M., Downey J.M, Heusch G. Signal transduction of ischemic preconditioning. Cardiovasc Res. 2001;52(2):181-198.
  23. Gassanov N., Nia A.M., Caglayan E., Er F. Remote ischemic preconditioning and renoprotection: from myth to a novel therapeutic option? J. Am. Soc. Nephrol. 2014;25:216-224.
  24. Goswami S.K., Maulik N., Das D.K. Ischemia-reperfusion and cardioprotection: a delicate balance between reactive oxygen species generation and redox homeostasis. Annals Of Medicine 2007; 39(4):275-289.
  25. Gidday J.M. Cerebral preconditioning and ischaemic tolerance. Nature Reviews Neuroscience. 2006;7:437-448. doi: 10.1038/nrn1927
  26. Kapitsinou P.P., Haase V.H. Molecular mechanisms of ischemic preconditioning in the kidney. American Journal of Physiology - Renal Physiology. 2015;309(10):F821-F834, doi: 10.1152/ajprenal.00224.2015.
  27. Даниленко Л.М. Роль оксида азота в сигнальном каскаде ишемического прекондиционирования при ишемически-реперфузионных повреждениях миокарда. Научные ведомости Белгородского государственного университета. Серия: Медицина. Фармация. 2014;26(11-1):5-18
  28. Ge Y.Z., Wu R., Xin H., Liu H., Lu T.Z., Zhao Y.C., Shen J.W., HuZ.K., Yu P., Zhou L.H., Xu L.W., Xu Z., Wu J.P., Li W.C., Zhu J.G., Jia R.P. Effects of ischemic preconditioning on the systemic and renal hemodynamic changes in renal ischemia reperfusion injury. Int J Clin Exp Pathol. 2015;8(2):1128-1140.
  29. Metzen E., Zhou J., Jelkmann W., Fandrey J., Brüne B. Nitric oxide impairs normoxic degradation of HIF-1a by inhibition ofprolylhydroxylases. Mol Biol Cell. 2003;14:3470-3481.
  30. Palacios-Callender M., Quintero M., Hollis V.S., Springett R.J., Moncada S. Endogenous NO regulates superoxide production at low oxygen concentrations by modifying the redox state of cytochrome c oxidase. Proc Natl Acad Sci USA. 2004;101:7630-7635.
  31. Antonova G.N., Snead C.M., Antonov A.S., Dimitropoulou C., Venema R.C., Catravas J.D. Nitric oxide preconditioning regulates endothelial monolayer integrity via the heat shock protein 90-soluble guanylatecyclase pathway. American Journal of Physiology - Heart and Circulatory Physiology. 2007;292(2):H893-H903.
  32. Murphy E., Steenbergen C. Preconditioning: the mitochondrial connection. Annual Review of Physiology. 2007;69(1):51-67.
  33. Liu Y., O’Rourke B. Opening of mitochondrial KATP channels triggers cardioprotection. Circulation Research. 2001;88:750-752.
  34. Levchenkova O.S., Novikov V.E., Pozhilova E.V. Mitochondrial pore as a pharmacological target. Vestnik Smolenskoi gosudarstvennoi meditsinskoi akademii. 2014;3(4):24-33
  35. Wayel J., Heaton N.D. The role of mitochondria in ischemia/ reperfusion injury in organ transplantation. Kidney International. 2004; 66(2):514-517.
  36. Martinou J.C., Green, D.R. Breaking the mitochondrial barrier. Nature Rev. 2001;2:63-67.
  37. Ravagnan L., Roumier T., and Kromer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol. 2002;192:131-137.
  38. Toosy N., McMorris E.L., Grace P.A., Mathie R. T. Ischaemic preconditioning protects the rat kidney from reperfusion injury. BJU Int. 1999;84(4):489-494.
  39. Wever K.E., Menting T.P., Rovers M., van der Vliet J.A., Rongen G.A., Masereeuw R., Ritskes-Hoitinga M., Hooijmans C.R., Warlé M. Ischemic preconditioning in the animal kidney, a systematic review and meta-analysis. PLoS ONE. 2012;7(2):e32296, doi: 10.1371/journal. pone.0032296.
  40. Conn P.M. Sourcebook of models for biomedical research. Totowa, N.J: Humana Press. 2008;736 p.
  41. Singh D., Chopra K. Effect of trimetazidine on renal ischemia/reperfusion injury in rats. Pharmacological Research. 2004;50(6):623-629.
  42. Chen C.C., Liu Z.M., Wang H.H., He W., Wang Y., Wu W.D. Effects of ulinastatin on renal ischemia-reperfusion injury in rats. Acta Pharmacol Sin. 2004;25(10):1334-1340.
  43. Fan L.H., He L., Cao Z.Q., Xiang B., Liu L. Effect of ischemia preconditioning on renal ischemia/reperfusion injury in rats. International Braz J Urol. 2012;38(6):842-854.
  44. Williams P., Lopez H., Britt D., Chan C., Ezrin A., Hottendorf R. Characterization of renal ischemia-reperfusion injury in rats, Journal of Pharmacological and Toxicological Methods. 1997;37(1):1-7.
  45. Kocoglu H., Ozturk H., Ozturk H., Yilmaz F., Gulcu N. Effect of dexmedetomidine on ischemia-reperfusion injury in rat kidney: a histopathologic study. Renal Failure. 2009;31(1):70-74. doi: 10.1080/08860220802546487.
  46. Okusa M.D., Linden J., Macdonald T., Huang L. Selective A2A adenosine receptor activation reduces ischemia-reperfusion injury in rat kidney. American Journal of Physiology - Renal Physiology. 1999; 277(3):404-412.
  47. Brown P.A.J., Cuzzocrea S., Zacharowski K., Stewart K.N., Mota-Filipe H., Mcdonald M.C., Thiemermann C. Calpain inhibitor-1 reduces renal ischemia/reperfusion injury in the rat. Kidney International. 2001;59(6):2073-2083.
  48. Chen H., Xing B., Liu X., Zhan B., Zhou J., Zhu H., Chen Z. Ischemic postconditioning inhibits apoptosis after renal ischemia/reperfusion injury in rat. Transplant International. 2008;21:364-371. doi: 10.1111/j.1432- 2277.2007.00606.x.
  49. Chok M.K., Conti M., Almolki A., Ferlicot S., Loric S., Dürrbach A., Benoît G., Droupy S., Eschwège P. Renoprotective potency of amifostine in rat renal ischaemia-reperfusion. NephrolDialTransplant. 2010;25(12):3845-3851.
  50. Nitescu N., Ricksten S.E., Marcussen N., Haraldsson B., Nilsson U., Basu S., Guron G. N -acetylcysteine attenuates kidney injury in rats subjected to renal ischaemia-reperfusion.Nephrol Dial Transplant. 2006;21(5): 1240-1247.
  51. Venugopal V., Laing C.M., Ludman A., Yellon D.M., Hausenloy D. Effect of remote ischemic preconditioning on acute kidney injury in nondiabetic patients undergoing coronary artery bypass graft surgery: a secondary analysis of 2 small randomized trials. AmJKidneyDis. 2010; 56:1043-1049.
  52. Zimmerman R.F., Ezeanuna P.U., Kane J.C., Cleland C.D., Kempananjappa T.J., Lucas F.L., Kramer R.S. Ischemic preconditioning at a remote site prevents acute kidney injury in patients following cardiac surgery. Kidney Int. 2011;80:861-867. doi: 10.1038/ki.2011.156.
  53. Pedersen K.R., Ravn H.B., Povlsen J.V., Schmidt M.R., Erlandsen E.J., Hjortdal V.E. Failure of remote ischaemic preconditioning to reduce the risk of postoperative acute kidney injury in children undergoing operation for complex congenital heart disease: a randomized single-center study. The Journal ofthoracic and cardiovascular surgery. 2012;143(3):576-583.
  54. Gallagher S.M., Jones D.A., Kapur A., Harwood S.M., Mathur R., Archbold R.A., Uppal R., Yaqoob M.M. Remote ischaemic preconditioning has a neutral effect on the incidence of kidney injury after coronary artery bypass graft surgery. Kidney international. 2015;87(2):473-481.
  55. Nouraei S.M., Baradari A.G., Jazayeri A. Does remote ischaemic preconditioning protect kidney and cardiomyocytes after coronary revascularization? A double blind controlled clinical trial. Medical Archives. 2016;70(5):373-378. doi: 10.5455/medarh.2016.70.373-378.
  56. Walsh S.R., Tang T.Y., Kullar P., Jenkins D.P., Dutka D.P., Gaunt M.E. Ischaemic preconditioning during cardiac surgery: systematic review and meta-analysis of perioperative outcomes in randomised clinical trials. European Journal of Cardio-Thoracic Surgery.2008;34(5):985-994.
  57. Покровский М.В., Гуреев В.В., Ступакова Е.Г., Анциферова О.Е., Локтева Т.И., Жилинкова Л.А. Биологические механизмы естественной цитопротекции - перспективное направление создания новых лекарственных препаратов для профилактики и лечения преэклампсии. Ведомости Научного центра экспертизы средств медицинского применения. 2016;4:20-27
  58. Skachilova S.Y., Danilenko L.M., Kesarev O.G., Kochkarova I.S. Pharmacological protection of the ischemic myocardium by derivatives of 3-(2,2,2-trimethylhydrazinium) propionate and evaluation of their antioxidant activity. Research result: pharmacology and clinical pharmacology. 2015;1(1):23-27.
  59. Shimizu S., Saito M., Kinoshita Y., Ohmasa F., Dimitriadis F., Shomori K., Hayashi A., Satoh K. Nicorandil ameliorates ischaemia-reperfusion injury in the rat kidney. British Journal of Pharmacology. 2011;163(2):272-282.
  60. Qin Z., Lv E., Zhan L., Xing X., Jiang J., Zhang M. Intravenous pretreatment with emulsified isoflurane preconditioning protects kidneys against ischemia/reperfusion injury in rats. BMC Anesthesiology. 2014;14:28. doi: 10.1186/1471-2253-14-28.
  61. Keel C.E., Wang Z., Colli J., Grossman L., Majid D., Lee B.R. Protective effects of reducing renal ischemia-reperfusion injury during renal hilar clamping: use of allopurinol as a nephroprotective agent. Urology. 2013;81(1):210.e5-10.
  62. Chang M.W., Chen C.H., Chen Y.C., Wu Y.C., Zhen Y.Y., Leu S., Tsai T.H., Ko S.F., Sung P.H., Yang C.C., Chiang H.J., Chang H.W., Chen Y.T., Yip H.K. Sitagliptin protects rat kidneys from acute ischemia-reperfusion injury via upregulation of GLP-1 and GLP-1 receptors. Acta Pharmacologica Sinica. 2015;36(1):119-130. doi: 10.1038/aps.2014.98.
  63. Katagiri D., Hamasaki Y., Doi K., Okamoto K., Negishi K., Nangaku M., Noiri E. Protection of glucagon-like peptide-1 in cisplatin-induced renal injury elucidates gut-kidney connection.Journal of the American Society of Nephrology. JASN. 2013;24(12):2034-2043. Doi:10.1681/ ASN.2013020134.
  64. Yazihan N., Ataoglu H., Kavas G.O., Akyurek N., Yener B., Aydýn C. The effect of K-ATP channel blockage during erythropoietin treatment in renal ischemia-reperfusion injury. J Invest Surg. 2008;21:340-347.
  65. Baker J.E. Erythropoietin mimics ischemic preconditioning. VasculPharmacol. 2005;42:233-241.
  66. Даниленко Л.М., Покровский М.В., Новиков О.О., Корокина Л.В., Гончарова Д.В., Индерова А.В., Светличная Е.Н. Триггерный механизм противоишемического действия эритропоэтина и резвератрола. Научные ведомости Белгородского государственного университета. Серия: Медицина. Фармация. 2012;10(129):138-142
  67. Lipsic E., Schoemaker R.G., van der Meer P., Voors A.A., van Veldhuisen D.J., van Gilst W.H. Protective effects of erythropoietin in cardiac ischemia: from bench to bedside. Journal of the American College of Cardiology. 2006;48(11):2161-2167. doi: 10.1016/j.jacc. 2006.08.031.
  68. Kolesnik I.M., Lazarenko V.A., Pokrovskii M.V. Assessment of the impact of pharmacological preconditioning with recombinant erythropoietin on the state of the resected liver in experiment. Kurskij nauchno-prakticheskij vestnik «Chelovek i ego zdorov’e». 2015;2:74-78.
  69. Ma Y.S., Zhou J., Liu H., Du Y., Lin X.M. Protection effect of recombiant human erythropoietin preconditioning against intrauterine hypoxic-ischemic brain injury and its influence on expression of caspase-3 protein in brain tissue. Sichuan Da Xue Xue Bao Yi Xue Ban. 2013; 44(3):397-401.
  70. Shabelnikova A.S. Correction of ischemic damage to the retina on application of pharmacological preconditioning of recombinant erythropoietin. Research result: pharmacology and clinical pharmacology. 2016;2(2):67-90.
  71. Shabelnikova A.S., Peresypkina A.A., Gubareva V.O., Levkova E.A., Dolzhikov A.A., Nikolaev S.B., Stepchenko A.A. Pharmacological preconditioning by recombinant erythropoietin as the possibility of increasing the stability of tissue of the retina to reperfusion ischemia in experiment. Research result: pharmacology and clinical pharmacology. 2016;1(2):25-29.
  72. Moore E.M., Bellomo R., Nichol A.D. Erythropoietin as a novel brain and kidney protective agent. Anaesth Intensive Care. 2011;39:356-372.
  73. Bahlmann F.H., Fliser D. Erythropoietin and renoprotection. Curr Opin Nephrol Hypertens. 2009; 18:15-20. Doi: 10.1097/ MNH.0b013e32831a9dde.
  74. Liao J.G., Li M.Y., Wang X.H., Xie Q. The protective effect oferythropoietin pretreatment on ischemic acute renal failure in rats. Journal of Acute Disease. 2016;5(5):408-412. doi: 10.1016/j.joad.2016.08.008.
  75. Moore E., Bellomo R. Erythropoietin (EPO) in acute kidney injury. Annals of Intensive Care. 2011;1:3. doi: 10.1186/2110-5820-1-3.
  76. Song Y.R., LeeT., You S.J., Chin H.J., Chae D.W., Lim C., Park K.H., Han S., Kim J.H., Na K.Y. Prevention of acute kidney injury by erythropoietin in patients undergoing coronary artery bypass grafting: a pilot study. Am J Nephrol.2009;30:253-260.
  77. Cassis P., Azzollini N., Solini S., MisterM., Aiello S., Cugini D., Scudeletti P., Gagliardini E., Abbate M., Gallon L., Remuzzi G., Noris M. Both darbepoetinalfa and carbamylated erythropoietin prevent kidney graft dysfunction due to ischemia/reperfusion in rats. Transplantation. 2011;92(3):271-279.
  78. Sohotnik R., Nativ O., Abbasi A., Awad H., Frajewicki V., Bishara B., Sukhotnik I., Armaly Z., Aronson D., Heyman S.N., Nativ O., Abassi Z. Phosphodiesterase-5 inhibition attenuates early renal ischemia-reperfusion-induced acute kidney injury: assessment by quantitative measurement of urinary NGAL and KIM-1. American Journal of Physiology - Renal Physiology. 2013;304(8):1099-1104. Doi: 10.1152/ ajprenal.00649.2012.
  79. Medeiros V.F., Azevedo I.M., Carvalho M.D., Oliveira C.N., Egito E.S., Medeiros A.C. The renoprotective effect of oral Tadalafil pretreatment on ischemia/reperfusion injury in rats. Acta Cir. Bras. 2017;32(2):90-97.
  80. El-Sisi A.E., Sokar S.S., Abu-Risha S.E., Ibrahim H.A. Combination of tadalafil and diltiazem attenuates renal ischemia reperfusion-induced acute renal failure in rats. Biomedicine & Pharmacotherapy. 2016; 84:861-869.
  81. El-Mahdy N.A., El-Sayad Mel-S., El-Kadem A.H. Combination of telmisartan with sildenafil ameliorate progression of diabetic nephropathy in streptozotocin-induced diabetic model. Biomedicine & Pharmacotherapy. 2016;81:136-144. doi: 10.1016/j.biopha.2016.04.001.
  82. Lee K.W., Jeong J.Y., Lim B.J., Chang Y.K., Lee S.J., Na K.R., Shin Y.T., Choi D.E. Sildenafil attenuates renal injury in an experimental model of rat cisplatin-induced nephrotoxicity. Toxicology. 2009;257: 137-143.
  83. ÖzgürB.C., Telli O., Yuceturk C.N., Sarici H., Ozer E., Surer H., Kilinc A.S., Hucumenoglu S., Eroglu M. The effect of sildenafil and udenafil on testicular damage following ischemia-reperfusion injury in rats. J Urol. 2014;192(4):1272-1277. doi: 10.1016/j.juro.2014.04.011

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