Nonsteroidal Mineralocorticoid Receptor Antagonist Finerenone Protects Against Acute Kidney Injury-Mediated Chronic Kidney Disease: Role of Oxidative Stress

Hypertension

Volumn 69, Issue 5, 2017, Pages 870-878

  Lattenist, Lionel ^a   Lechner, Sebastian M ^a   Messaoudi, Smail ^a   Le Mercier, Alan ^a   El Moghrabi, Soumaya ^a   Prince, Sonia ^a   Bobadilla, Norma A ^b   Kolkhof, Peter ^c   Jaisser, Frédéric ^a   Barrera Chimal, Jonatan ^a,b  

^a INSERM   (France)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c BAYER AG   (Germany)

Author keywords

endothelin receptors; fibrosis; ischemia; renal circulation; reperfusion

Indexed keywords

COLLAGEN TYPE 1; ENDOTHELIN B RECEPTOR; FINERENONE; KIDNEY INJURY MOLECULE 1; MALONALDEHYDE; MESSENGER RNA; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; TEMPOL; TRANSFORMING GROWTH FACTOR BETA; CELL ADHESION MOLECULE; HAVCR1PROTEIN, RAT; MINERALOCORTICOID ANTAGONIST; NAPHTHYRIDINE DERIVATIVE;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CHRONIC KIDNEY FAILURE; CONTROLLED STUDY; DRUG EFFICACY; IMMUNOPRECIPITATION; KIDNEY DYSFUNCTION; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY ISCHEMIA; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RENAL PROTECTION; WESTERN BLOTTING; ANIMAL; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; KIDNEY; METABOLISM; RENAL INSUFFICIENCY, CHRONIC; REPERFUSION INJURY; WISTAR RAT;

ACUTE KIDNEY INJURY; ANIMALS; CELL ADHESION MOLECULES; DISEASE MODELS, ANIMAL; KIDNEY; LIPOCALIN-2; MALE; MALONDIALDEHYDE; MINERALOCORTICOID RECEPTOR ANTAGONISTS; NAPHTHYRIDINES; OXIDATIVE STRESS; RATS; RATS, WISTAR; RENAL INSUFFICIENCY, CHRONIC; REPERFUSION INJURY;

EID: 85015807935     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.116.08526     Document Type: Article

References (42)

1. Basile DP, Bonventre JV, Mehta R, Nangaku M, Unwin R, Rosner MH, Kellum JA, Ronco C, ADQI XIII Work Group Progression after AKI: understanding maladaptive repair processes to predict and identify therapeutic treatments. J Am Soc Nephrol 2016 27 687-697. doi: 10.1681/ASN.2015030309.
2. Parr SK, Siew ED, Delayed consequences of acute kidney injury. Adv Chronic Kidney Dis 2016 23 186-194. doi: 10.1053/j.ackd.2016.01.014.
3. Basile DP, Anderson MD, Sutton TA, Pathophysiology of acute kidney injury. Compr Physiol 2012 2 1303-1353. doi: 10.1002/cphy.c110041.
4. Venkatachalam MA, Weinberg JM, Kriz W, Bidani AK, Failed tubule recovery, AKI-CKD transition, and kidney disease progression. J Am Soc Nephrol 2015 26 1765-1776. doi: 10.1681/ASN.2015010006.
5. Basile DP, Friedrich JL, Spahic J, Knipe N, Mang H, Leonard EC, Changizi-Ashtiyani S, Bacallao RL, Molitoris BA, Sutton TA, Impaired endothelial proliferation and mesenchymal transition contribute to vascular rarefaction following acute kidney injury. Am J Physiol Renal Physiol 2011 300 F721-F733. doi: 10.1152/ajprenal.00546.2010.
6. Barrera-Chimal J, Pérez-Villalva R, Rodríguez-Romo R, Reyna J, Uribe N, Gamba G, Bobadilla NA, Spironolactone prevents chronic kidney disease caused by ischemic acute kidney injury. Kidney Int 2013 83 93-103. doi: 10.1038/ki.2012.352.
7. Agarwal A, Dong Z, Harris R, Murray P, Parikh SM, Rosner MH, Kellum JA, Ronco C, Acute Dialysis Quality Initiative XIII Working Group Cellular and molecular mechanisms of AKI. J Am Soc Nephrol 2016 27 1288-1299. doi: 10.1681/ASN.2015070740.
8. Humphreys BD, Cantaluppi V, Portilla D, Singbartl K, Yang L, Rosner MH, Kellum JA, Ronco C, Acute Dialysis Quality Initiative (ADQI) XIII Work Group Targeting endogenous repair pathways after AKI. J Am Soc Nephrol 2016 27 990-998. doi: 10.1681/ASN.2015030286.
9. Mejía-Vilet JM, Ramírez V, Cruz C, Uribe N, Gamba G, Bobadilla NA, Renal ischemia-reperfusion injury is prevented by the mineralocorticoid receptor blocker spironolactone. Am J Physiol Renal Physiol 2007 293 F78-F86. doi: 10.1152/ajprenal.00077.2007.
10. Barba-Navarro R, Tapia-Silva M, Garza-Garcia C, López-Giacoman S, Melgoza-Toral I, Vázquez-Rangel A, Bazúa-Valenti S, Bobadilla N, Wasung de Lay M, Baranda F, Chawla LS, Gamba G, Madero M, The effect of spironolactone on acute kidney injury after cardiac surgery: a randomized, placebo-controlled trial. Am J Kidney Dis 2017 69 192-199. doi: 10.1053/j.ajkd.2016.06.013.
11. Kolkhof P, Nowack C, Eitner F, Nonsteroidal antagonists of the mineralocorticoid receptor. Curr Opin Nephrol Hypertens 2015 24 417-424. doi: 10.1097/MNH.0000000000000147.
12. Barrera-Chimal J, Prince S, Fadel F, El Moghrabi S, Warnock DG, Kolkhof P, Jaisser F, Sulfenic acid modification of endothelin B receptor is responsible for the benefit of a nonsteroidal mineralocorticoid receptor antagonist in renal ischemia. J Am Soc Nephrol 2016 27 398-404. doi: 10.1681/ASN.2014121216.
13. Filippatos G, Anker SD, Böhm M, A randomized controlled study of finerenone vs. eplerenone in patients with worsening chronic heart failure and diabetes mellitus and/or chronic kidney disease. Eur Heart J 2016 37 2105-2114. doi: 10.1093/eurheartj/ehw132.
14. Barrera-Chimal J, Bobadilla NA, Jaisser F, mineralocorticoid receptor antagonism: a promising therapeutic approach to treat ischemic AKI. Nephron 2016 134 10-13. doi: 10.1159/000445080.
15. Barrera-Chimal J, Pérez-Villalva R, Ortega JA, Sánchez A, Rodríguez-Romo R, Durand M, Jaisser F, Bobadilla NA, Mild ischemic injury leads to long-term alterations in the kidney: amelioration by spironolactone administration. Int J Biol Sci 2015 11 892-900. doi: 10.7150/ijbs.11729.
16. Rocha R, Chander PN, Zuckerman A, Stier CT Jr, Role of aldosterone in renal vascular injury in stroke-prone hypertensive rats. Hypertension 1999 33 1 pt 2 232-237. doi: 10.1161/01.HYP.33.1.232.
17. Zitt E, Eller K, Huber JM, Kirsch AH, Tagwerker A, Mayer G, Rosenkranz AR, The selective mineralocorticoid receptor antagonist eplerenone is protective in mild anti-GBM glomeru-lonephritis. Int J Clin Exp Pathol 2011 4 606-615
18. Nakhoul F, Khankin E, Yaccob A, Kawachi H, Karram T, Awaad H, Nakhoul N, Hoffman A, Abassi Z, Eplerenone potentiates the antiproteinuric effects of enalapril in experimental nephrotic syndrome. Am J Physiol Renal Physiol 2008 294 F628-F637. doi: 10.1152/ajprenal.00524.2007.
19. Monrad SU, Killen PD, Anderson MR, Bradke A, Kaplan MJ, The role of aldosterone blockade in murine lupus nephritis. Arthritis Res Ther 2008 10 R5. doi: 10.1186/ar2353.
20. Pérez-Rojas J, Blanco JA, Cruz C, Trujillo J, Vaidya VS, Uribe N, Bonventre JV, Gamba G, Bobadilla NA, Mineralocorticoid receptor blockade confers renoprotection in preexisting chronic cyclosporine nephrotoxicity. Am J Physiol Renal Physiol 2007 292 F131-F139. doi: 10.1152/ajprenal.00147.2006.
21. Pérez-Rojas JM, Derive S, Blanco JA, Cruz C, Martínez de la Maza L, Gamba G, Bobadilla NA, Renocortical mRNA expression of vasoactive factors during spironolactone protective effect in chronic cyclosporine nephrotoxicity. Am J Physiol Renal Physiol 2005 289 F1020-F1030. doi: 10.1152/ajprenal.00166.2005.
22. Greene EL, Kren S, Hostetter TH, Role of aldosterone in the remnant kidney model in the rat. J Clin Invest 1996 98 1063-1068. doi: 10.1172/JCI118867.
23. Trachtman H, Weiser AC, Valderrama E, Morgado M, Palmer LS, Prevention of renal fibrosis by spironolactone in mice with complete unilateral ureteral obstruction. J Urol 2004 172 4 pt 2 1590-1594
24. Guo C, Martinez-Vasquez D, Mendez GP, Toniolo MF, Yao TM, Oestreicher EM, Kikuchi T, Lapointe N, Pojoga L, Williams GH, Ricchiuti V, Adler GK, Mineralocorticoid receptor antagonist reduces renal injury in rodent models of types 1 and 2 diabetes mellitus. Endocrinology 2006 147 5363-5373. doi: 10.1210/en.2006-0944.
25. Tsuboi N, Kawamura T, Okonogi H, Ishii T, Hosoya T, The long-term antiproteinuric effect of eplerenone, a selective aldosterone blocker, in patients with non-diabetic chronic kidney disease. J Renin Angiotensin Aldosterone Syst 2012 13 113-117. doi: 10.1177/1470320311412811.
26. Nielsen SE, Persson F, Frandsen E, Sugaya T, Hess G, Zdunek D, Shjoedt KJ, Parving HH, Rossing P, Spironolactone diminishes urinary albumin excretion in patients with type 1 diabetes and microalbuminuria: a randomized placebo-controlled crossover study. Diabet Med 2012 29 e184-e190. doi: 10.1111/j.1464-5491.2012.03585.x.
27. Saklayen MG, Gyebi LK, Tasosa J, Yap J, Effects of additive therapy with spironolactone on proteinuria in diabetic patients already on ACE inhibitor or ARB therapy: results of a randomized, placebo-controlled, double-blind, crossover trial. J Investig Med 2008 56 714-719. doi: 10.2310/JIM.0b013e31816d78e9.
28. Schupp N, Kolkhof P, Queisser N, Gärtner S, Schmid U, Kretschmer A, Hartmann E, Oli RG, Schäfer S, Stopper H, Mineralocorticoid receptor-mediated DNA damage in kidneys of DOCA-salt hypertensive rats. FASEB J 2011 25 968-978. doi: 10.1096/fj.10-173286.
29. Ma FY, Han Y, Nikolic-Paterson DJ, Kolkhof P, Tesch GH, Suppression of rapidly progressive mouse glomerulonephritis with the non-steroidal mineralocorticoid receptor antagonist BR-4628. PLoS One 2015 10 e0145666. doi: 10.1371/journal.pone.0145666.
30. Kolkhof P, Delbeck M, Kretschmer A, Steinke W, Hartmann E, Bärfacker L, Eitner F, Albrecht-Küpper B, Schäfer S, Finerenone, a novel selective nonsteroidal mineralocorticoid receptor antagonist protects from rat cardiorenal injury. J Cardiovasc Pharmacol 2014 64 69-78. doi: 10.1097/FJC.0000000000000091.
31. Grune J, Benz V, Brix S, Salatzki J, Blumrich A, Höft B, Klopfleisch R, Foryst-Ludwig A, Kolkhof P, Kintscher U, Steroidal and nonsteroidal mineralocorticoid receptor antagonists cause differential cardiac gene expression in pressure overload-induced cardiac hypertrophy. J Cardiovasc Pharmacol 2016 67 402-411. doi: 10.1097/FJC.0000000000000366.
32. Gueret A, Harouki N, Favre J, Galmiche G, Nicol L, Henry JP, Besnier M, Thuillez C, Richard V, Kolkhof P, Mulder P, Jaisser F, Ouvrard-Pascaud A, Vascular smooth muscle mineralocorticoid receptor contributes to coronary and left ventricular dysfunction after myocardial infarction. Hypertension 2016 67 717-723. doi: 10.1161/HYPERTENSIONAHA.115.06709.
33. Pitt B, Kober L, Ponikowski P, Gheorghiade M, Filippatos G, Krum H, Nowack C, Kolkhof P, Kim SY, Zannad F, Safety and tolerability of the novel non-steroidal mineralocorticoid receptor antagonist BAY 94-8862 in patients with chronic heart failure and mild or moderate chronic kidney disease: a randomized, double-blind trial. Eur Heart J 2013 34 2453-2463. doi: 10.1093/eurheartj/eht187.
34. Bakris GL, Agarwal R, Chan JC, Cooper ME, Gansevoort RT, Haller H, Remuzzi G, Rossing P, Schmieder RE, Nowack C, Kolkhof P, Joseph A, Pieper A, Kimmeskamp-Kirschbaum N, Ruilope LM, Mineralocorticoid Receptor Antagonist Tolerability Study-Diabetic Nephropathy (ARTS-DN) Study Group Effect of finerenone on albuminuria in patients with diabetic nephropathy: a randomized clinical trial. JAMA 2015 314 884-894. doi: 10.1001/jama.2015.10081.
35. Chatterjee PK, Cuzzocrea S, Brown PA, Zacharowski K, Stewart KN, Mota-Filipe H, Thiemermann C, Tempol, a membrane-permeable radical scavenger, reduces oxidant stress-mediated renal dysfunction and injury in the rat. Kidney Int 2000 58 658-673. doi: 10.1046/j.1523-1755.2000.00212.x.
36. Noiri E, Nakao A, Uchida K, Tsukahara H, Ohno M, Fujita T, Brodsky S, Goligorsky MS, Oxidative and nitrosative stress in acute renal ischemia. Am J Physiol Renal Physiol 2001 281 F948-F957. doi: 10.1152/ajprenal.0071.2001.
37. de Araujo M, Andrade L, Coimbra TM, Rodrigues AC Jr, Seguro AC, Magnesium supplementation combined with N-acetylcysteine protects against postischemic acute renal failure. J Am Soc Nephrol 2005 16 3339-3349. doi: 10.1681/ASN.2004100832.
38. Maron BA, Zhang YY, White K, Chan SY, Handy DE, Mahoney CE, Loscalzo J, Leopold JA, Aldosterone inactivates the endothelin-B receptor via a cysteinyl thiol redox switch to decrease pulmonary endothelial nitric oxide levels and modulate pulmonary arterial hypertension. Circulation 2012 126 963-974. doi: 10.1161/CIRCULATIONAHA.112.094722.
39. Barrera-Chimal J, André-Grégoire G, Nguyen dinh Cat A, Lechner SM, Cau J, Prince S, Kolkhof P, Loirand G, Sauzeau V, Hauet T, Jaisser F, Benefit of mineralocorticoid receptor antagonism in mouse and pig acute kidney injury: role of vascular smooth muscle Rac1. J Am Soc Nephrol 2017. doi: 10.1681/ASN.2016040477.
40. Rodríguez-Romo R, Benítez K, Barrera-Chimal J, Pérez-Villalva R, Gómez A, Aguilar-León D, Rangel-Santiago JF, Huerta S, Gamba G, Uribe N, Bobadilla NA, AT1 receptor antagonism before ischemia prevents the transition of acute kidney injury to chronic kidney disease. Kidney Int 2016 89 363 373. doi: 10.1038/ki.2015.320.
41. Skrypnyk NI, Voziyan P, Yang H, de Caestecker CR, Theberge MC, Drouin M, Hudson B, Harris RC, de Caestecker MP, Pyridoxamine reduces postinjury fibrosis and improves functional recovery after acute kidney injury. Am J Physiol Renal Physiol 2016 311 F268-F277. doi: 10.1152/ajprenal.00056.2016.
42. Cianciolo Cosentino C, Skrypnyk NI, Brilli LL, Chiba T, Novitskaya T, Woods C, West J, Korotchenko VN, McDermott L, Day BW, Davidson AJ, Harris RC, de Caestecker MP, Hukriede NA, Histone deacetylase inhibitor enhances recovery after AKI. J Am Soc Nephrol 2013 24 943-953. doi: 10.1681/ASN.2012111055.