Tacrolimus-induced hypertension and nephrotoxicity in Fawn-Hooded rats are attenuated by dual inhibition of renin-angiotensin system

Hypertension Research

Volumn 37, Issue 8, 2014, Pages 724-732

  Hošková, Lenka ^a   Málek, Ivan ^a   Kautzner, Josef ^a   Honsová, Eva ^a   Van Dokkum, Richard P E ^b   Husková, Zuzana ^a   Vojtíšková, Alžbeta ^a   Varcabová, Šárka ^a   Červenka, Luděk ^a   Kopkan, Libor ^a  

^a INSTITUTE FOR CLINICAL AND EXPERIMENTAL MEDICINE   (Czech Republic)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

arterial hypertension; calcineurin inhibitor; Fawn Hooded rat; nephrotoxicity; renin angiotensin system

Indexed keywords

AMLODIPINE; ANGIOTENSIN II; CALCINEURIN INHIBITOR; LOSARTAN; METOPROLOL; PERINDOPRIL; TACROLIMUS; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCINEURIN; CALCIUM CHANNEL BLOCKING AGENT; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; IMMUNOSUPPRESSIVE AGENT;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIHYPERTENSIVE THERAPY; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; FAWN HOODED HYPERTENSIVE RAT; FAWN HOODED RAT; HISTOPATHOLOGY; HYPERTENSION; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY INJURY; LONG TERM CARE; MALE; NEPHROTOXICITY; NONHUMAN; PATHOPHYSIOLOGY; RAT; RENAL PROTECTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; TUBULOINTERSTITIAL INJURY; ACUTE KIDNEY INJURY; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; DIET; DRUG EFFECTS;

ACUTE KIDNEY INJURY; ADRENERGIC BETA-ANTAGONISTS; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; CALCINEURIN; CALCIUM CHANNEL BLOCKERS; DIET; IMMUNOSUPPRESSIVE AGENTS; MALE; RATS; RENIN-ANGIOTENSIN SYSTEM; TACROLIMUS;

EID: 84905443775     PISSN: 09169636     EISSN: 13484214     Source Type: Journal    
DOI: 10.1038/hr.2014.79     Document Type: Article

References (56)

1. Burdmann EA, Andoh TF, Nast CC, Evan A, Connors BA, Coffman TM, Lindsley J, Bennett WM. Prevention of experimental cyclosporin-induced interstitial fibrosis by losartan and enalapril. Am J Physiol 1995; 269: F491-F499.
2. Naesens M, Kuypers DR, Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009; 4: 481-508.
3. Chatzikyrkou C, Menne J, Gwinner W, Schmidt BM, Lehner F, Blume C, Schwarz A, Haller H, Schiffer M. Pathogenesis and management of hypertension after kidney transplantation. J Hypertens 2011; 29: 2283-2294.
4. Hoorn EJ, Walsh SB, McCormick JA, Zietse R, Unwin RJ, Ellison DH. Pathogenesis of calcineurin inhibitor-induced hypertension. J Nephrol 2012; 25: 269-275.
5. Lassila M. Interaction of cyclosporine A and the renin-angiotensin system; new perspectives. Curr Drug Metab 2002; 3: 61-71.
6. Nishiyama A, Kobori H, Fukui T, Zhang GX, Yao L, Rahman M, Hitomi H, Kiyomoto H, Shokoji T, Kimura S, Kohno M, Abe Y. Role of angiotensin II and reactive oxygen species in cyclosporine A-dependent hypertension. Hypertension 2003; 42: 754-760.
7. Kidokoro K, Satoh M, Nagasu H, Sakuta T, Kuwabara A, Yorimitsu D, Nishi Y, Tomita N, Sasaki T, Kashihara N. Tacrolimus induces glomerular injury via endothelial dysfunction caused by reactive oxygen species and inflammatory change. Kidney Blood Press Res 2012; 35: 549-557.
8. Damiano S, Scanni R, Ciarcia R, Florio S, Capasso G. Regulation of sodium transporters in the kidney during cyclosporine treatment. J Nephrol 2010; 23 (Suppl 16), S191-S198.
9. Hoorn EJ, Walsh SB, McCormick JA, Fürstenberg A, Yang CL, Roeschel T, Paliege A, Howie AJ, Conley J, Bachmann S, Unwin RJ, Ellison DH. The calcineurin inhibitor tacrolimus activates the renal sodium chloride cotransporter to cause hypertension. Nat Med 2011; 17: 1304-1309.
10. Hosková L, Viklický O, Málek I, Podzimková M, Hegarová M, Pirk J, V́tko S, Kautzner J. Ischaemic heart disease is a risk factor for renal failure after heart transplantation. Int J Cardiol 2008; 123: 358-360.
11. Mancia G, Laurent S, Agabiti-Rosei E, Ambrosioni E, Burnier M, Caulfield MJ, Cifkova R, Clément D, Coca A, Dominiczak A, Erdine S, Fagard R, Farsang C, Grassi G, Haller H, Heagerty A, Kjeldsen SE, Kiowski W, Mallion JM, Manolis A, Narkiewicz K, Nilsson P, Olsen MH, Rahn KH, Redon J, Rodicio J, Ruilope L, Schmieder RE, Struijker-Boudier HA, van Zwieten PA, Viigimaa M, Zanchetti A. European Society of Hypertension. Reappraisal of European guidelines on hypertension management: a European Society of Hypertension Task Force document. J Hypertens 2009; 27: 2121-2158.
12. Volpe M, Danser AH, Menard J, Waeber B, Mueller DN, Maggioni AP, Ruilope LM. Inhibition of the rennin-angiotension-aldosterone system: is there room for dual blockade in the cardiorenal continuum? J Hypertens 2012; 30: 647-654.
13. Wilkinson-Berka JL, Gibbs NJ, Cooper ME, Skinner SL, Kelly DJ. Renoprotective and anti-hypertensive effects of combined valsartan and perindopril in progressive diabetic nephropathy in the transgenic (mRen-2)27 rat. Nephrol Dial Transplant 2001; 16: 1343-1349.
14. Hernández D, Muriel A, Abraira V, Pérez G, Porrini E, Marrero D, Zamora J, González-Posada JM, Delgado P, Rufino M, Torres A. Renin-angiotensin system blockade and kidney transplantation: a longitudinal cohort study. Nephrol Dial Transplant 2012; 27: 417-422.
15. Ruilope LM, Aldigier JC, Ponticelli C, Oddou-Stock P, Botteri F, Mann JF. Safety of the combination of valsartan and benazepril in patients with chronic renal disease. European Group for the Investigation of Valsartan in Chronic Renal Disease. J Hypertens 2000; 18: 89-95.
16. McMurray JJ, Ostergren J, Swedberg K, Granger CB, Held P, Michelson EL, Olofsson B, Yusuf S, Pfeffer MACHARM Investigators and Committees. Effects of candesartan in patients with chronic heart failure and reduced left-ventricular systolic function taking angiotensin-converting-enzyme inhibitors: the CHARM-Added trial. Lancet 2003; 362: 767-771.
17. Simons JL, Provoost AP, Anderson S, Troy JL, Rennke HG, Sandstrom DJ, Brenner BM. Pathogenesis of glomerular injury in the fawn-hooded rat: early glomerular capillary hypertension predicts glomerular sclerosis. J Am Soc Nephrol 1993; 3: 1775-1782.
18. Verseput GH, Provoost AP, Braam BB, Weening JJ, Koomans HA. Angiotensinconverting enzyme inhibition in the prevention and treatment of chronic renal damage in the hypertensive fawn-hooded rat. J Am Soc Nephrol 1997; 8: 249-259.
19. van Dokkum RP, Sun CW, Provoost AP, Jacob HJ, Roman RJ. Altered renal hemodynamics and impaired myogenic responses in the fawn-hooded rat. Am J Physiol 1999; 276: R855-R863.
20. de Keijzer MH, Provoost AP, Molenaar JC. Proteinuria is an early marker in the development of progressive renal failure in hypertensive fawn-hooded rats. J Hypertens 1989; 7: 525-528.
21. Verseput GH, Koomans HA, Braam B, Weening JJ, Provoost AP. ACE inhibition delays development of terminal renal failure in the presence of severe albuminuria. Am J Kidney Dis 2000; 35: 202-210.
22. Ochodnický P, Henning RH, Buikema HJ, de Zeeuw D, Provoost AP, van Dokkum RP. Renal vascular dysfunction precedes the development of renal damage in the hypertensive Fawn-Hooded rat. Am J Physiol Renal Physiol 2010; 298: F625-F633.
23. Schulz A, Kreutz R. Mapping genetic determinants of kidney damage in rat models. Hypertens Res 2012; 35: 675-694.
24. Vanourková Z, Kramer HJ, Husková Z, Vanecková I, Opocenský M, Chábová VC, Tesar V, Skaroupková P, Thumová M, Dohnalová M, Mullins JJ, Cervenka L. AT1 receptor blockade is superior to conventional triple therapy in protecting against end-organ damage in Cyp1a1-Ren-2 transgenic rats with inducible hypertension. J Hypertens 2006; 24: 2465-2472.
25. Kujal P, Chábová VC., Vernerová Z, Walkowska A, Kompanowska-Jezierska E, Sadowski J, Van.ourková Z, Husková Z, Opoc.enský M, Skaroupková P, Schejbalová S, Kramer HJ, Rakus.an D, Malý J, Netuka I, Vane.c.ková I, Kopkan L, Cervenka L. Similar renoprotection after renin-angiotensin-dependent and-independent antihypertensive therapy in 5/6-nephrectomized Ren-2 transgenic rats: are there blood pressureindependent effects? Clin Exp Pharmacol Physiol 2010; 37: 1159-1169.
26. Vanecková I, Kujal P, Husková Z, Vanourková Z, Vernerová Z, Certíková Chábová V, Skaroupková P, Kramer HJ, Tesar. V, Cervenka L. Effects of combined endothelin a receptor and renin-angiotensin system blockade on the course of end-organ damage in 5/6 nephrectomized ren-2 hypertensive rats. Kidney Blood Press Res 2012; 35: 382-392.
27. Kurtz TW, Griffin KA, Bidani AK, Davisson RL, Hall JE. Recommendations for blood pressure measurements in humans and experimental animals. Part 2: blood pressure measurement in experimental animals: a statement for professionals from the subcommittee of professional and public education of the American Heart Association council on high blood pressure research. Hypertension 2005; 45: 299-310.
28. Sochman J, Peregrin JH, Bürgelová M, Kopkan L, Kramer HJ, Cervenka L. N-acetylcysteine attenuates iodine contrast agent-induced nephropathy in 5/6-nephrectomized rats. Kidney Blood Press Res 2010; 33: 149-156.
29. Honetschlägerová Z, Z Husková Z, Vanourková Z, Sporková A, Kramer HJ, Hwang SH, Tsai HJ, Hammock BD, Imig JD, Cervenka L, Kopkan L. Renal mechanisms contributing to the antihypertensive action of soluble epoxide hydrolase inhibition in Ren-2 transgenic rats with inducible hypertension. J Physiol 2011; 589: 207-219.
30. Honetschlägerová Z, Sporková A, Kopkan L, Husková Z, Hwang SH, Hammock BD, Imig JD, Kramer HJ, Kujal P, Vernerová Z, Chábová VC, Tesar. V, Cervenka L. Inhibition of soluble epoxide hydrolase improves the impaired pressure-natriuresis relationship and attenuates the development of hypertension and hypertension-associated endorgan damage in Cyp1a1-Ren-2 transgenic rats. J Hypertens 2011; 29: 1590-1601.
31. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3: 1101-1108.
32. Ashek A, Menzies RI, Mullins LJ, Bellamy CO, Harmar AJ, Kenyon CJ, Flatman PW, Mullins JJ, Bailey MA. Activation of thiazide-sensitive co-transport by angiotensin II in the cyp1a1-Ren2 hypertensive rat. PLoS One 2012; 7: e36311.
33. Maitland K, Bridges L, Davis WP, Loscalzo J, Pointer MA. Different effects of angiotensin receptor blockade on end-organ damage in salt-dependent and saltindependent hypertension. Circulation 2006; 114: 905-911.
34. Stillman IE, Andoh TF, Burdmann EA, Bennett WM, Rosen S. FK506 nephrotoxicity: morphologic and physiologic characterization of a rat model. Lab Invest 1995; 73: 794-803.
35. Briones AM, Nguyen Dinh Cat A, Callera GE, Yogi A, Burger D, He Y, Corrêa JW, Gagnon AM, Gomez-Sanchez CE, Gomez-Sanchez EP, Sorisky A, Ooi TC, Ruzicka M, Burns KD, Touyz RM. Adipocytes produce aldosterone through calcineurin-dependent signaling pathways: implications in diabetes mellitus-associated obesity and vascular dysfunction. Hypertension 2012; 59: 1069-1078.
36. Randhawa PS, Starzl TE, Demetris AJ. Tacrolimus (FK506)-associated renal pathology. Adv Anat Pathol 1997; 4: 265-276.
37. Rüster C, Wolf G. Angiotensin II as a morphogenic cytokine stimulating renal fibrogenesis. J Am Soc Nephrol 2011; 22: 1189-1199.
38. Kobori H, Nangaku M, Navar LG, Nishiyama A. The intrarenal renin-angiotensin system: from physiology to the pathobiology of hypertension and kidney disease. Pharmacol Rev 2007; 59: 251-287.
39. Naesens M, Lerut E, de Jonge H, Van Damme B, Vanrenterghem Y, Kuypers DR. Donor age and renal P-glycoprotein expression associate with chronic histological damage in renal allografts. J Am Soc Nephrol 2009; 20: 2468-2480.
40. Mezzano SA, Ruiz-Ortega M, Egido J. Angiotensin II and renal fibrosis. Hypertension 2001; 38: 635-638.
41. Ozawa Y, Kobori H, Suzaki Y, Navar LG. Sustained renal interstitial macrophage infiltration following chronic angiotensin II infusions. Am J Physiol Renal Physiol 2007; 292: F330-F339.
42. Taal MW, Brenner BM. Renoprotective benefits of RAS inhibition: from ACEI to angiotensin II antagonists. Kidney Int 2000; 57: 1803-1817.
43. Mann JFE, Schmieder RE, McQueen M, Dyal L, Schumacher H, Pogue J, Wang X, Maggioni A, Budaj A, Chaithiraphan S, Dickstein K, Keltai M, Metsärinne K, Oto A, Parkhomenko A, Piegas LS, Svendsen TL, Koon KT, Yusuf S. Renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (the ONTARGET study): a multicentre, randomized, double-blind, controlled trial. Lancet 2008; 372: 547-553.
44. Mann JFE, Anderson C, Gao P, Gerstein HC, Boehm M, Ryden L, Sleight P, Teo KK, Yusuf S, the ONTARGET Investigators. Dual inhibition of the rennin-angiotensin system in high-risk diabetes and risk for stroke and other outcomes: results of the ONTARGET trial. J Hypertens 2013; 31: 414-421.
45. Fried LF, Emanuele N, Zhang JH, Brophy M, Conner TA, Duckworth W, Leehey DJ, McCullough PA, O'Connor T, Palevsky PM, Reilly RF, Seliger SL, Warren SR, Watnick S, Peduzzi P, Guarino PVA NEPHRON-D Investigators. Combined Angiotensin inhibition for the treatment of diabetic nephropathy. New Engl J Med 2013; 369: 1892-1903.
46. ESH/ESC Task Force for the Management of Arterial Hypertension. 2013 Practice guidelines for the management of arterial hypertension of the European Society of Hypertension (ESH) and the European Society of Cardiology (ESC): ESH/ESC task force for the management of arterial hypertension. J Hypertens 2013; 31: 1925-1938.
47. Dieperink H, Hansen HV, Kemp M, Leyssac PP, Starklint H, Kemp E. Antagonist capacity of felodipine on cyclosporin A nephrotoxicity in the rat. Nephrol Dial Transplant 1992; 7: 1124-1129.
48. Dworkin LD, Tolbert E, Recht PA, Hersch JC, Feiner H, Levin RI. Effects of amlodipine on glomerular filtration, growth, and injury in experimental hypertension. Hypertension 1996; 27: 245-250.
49. Mackie FE, Meyer TW, Campbell DJ. Effects of antihypertensive therapy on intrarenal angiotensin and bradykinin levels in experimental renal insufficiency. Kidney Int 2002; 61: 555-563.
50. Park HC, Xu ZG, Choi S, Goo YS, Kang SW, Choi KH, Ha SK, Lee HY, Han DS. Effect of losartan and amlodipine on proteinuria and transforming growth factor-beta1 in patients with IgA nephropathy. Nephrol Dial Transplant 2003; 18: 1115-1121.
51. Ponticelli C, Glassock RJ. Glomerular diseases: membranous nephropathy-a modern view. Clin J Am Soc Nephrol 2014; 9: 609-616.
52. Schweda F, Liebl R, Riegger GA, Krämer BK. Tacrolimus treatment for steroid-and cyclosporin-resistant minimal-change nephrotic syndrome. Nephrol Dial Transplant 1997; 12: 2433-2435.
53. Muller DN, Shagdarsuren E, Park JK, Dechend R, Mervaala E, Hampich F, Fiebeler A, Ju X, Finckenberg P, Theuer J, Viedt C, Kreuzer J, Heidecke H, Haller H, Zenke M, Luft FC. Immunosuppressive treatment protects against angiotensin II-induced renal damage. Am J Pathol 2002; 161: 1679-1693.
54. De Miguel C, Lund H, Mattson DL. High dietary protein exacerbates hypertension and renal damage in Dahl SS rats by increasing infiltrating immune cells in the kidney. Hypertension 2011; 57: 269-274.
55. Prieto MC, Gonzalez AA, Navar LG. Evolving concepts on regulation and function of renin in distal nephron. Pflugers Arch 2013; 465: 121-132.
56. Motawi TK, El-Maraghy SA, Senousy MA. Angiotensin-converting enzyme inhibition and angiotensin AT1 receptor blockade downregulate angiotensin-converting enzyme expression and attenuate renal injury in streptozotocin-induced diabetic rats. J Biochem Mol Toxicol 2013; 27: 378-387.