Blood pressure-independent renoprotection in diabetic rats treated with AT1 receptor-neprilysin inhibition compared with AT1 receptor blockade alone

Clinical Science

Volumn 130, Issue 14, 2016, Pages 1209-1220

  Roksnoer, Lodi C W ^a   van Veghel, Richard ^a   Clahsen van Groningen, Marian C ^a   de Vries, René ^a   Garrelds, Ingrid M ^a   Bhaggoe, Usha M ^a   van Gool, Jeanette M G ^a   Friesema, Edith C H ^a   Leijten, Frank P J ^a   Hoorn, Ewout J ^a   Jan Danser, A H ^a   Batenburg, Wendy W ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

AT1 receptor antagonist; Diabetes; Hypertension; Neprilysin inhibition; Renin angiotensin system

Indexed keywords

ACETYLCHOLINE; ALBUMIN; ALDOSTERONE; ANGIOTENSIN 1 RECEPTOR; CREATININE; CYCLIC GMP; CYSTATIN C; ENDOTHELIN 1; ENDOTHELIN B RECEPTOR; EPITHELIAL SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL ALPHA SUBUNIT; EPITHELIAL SODIUM CHANNEL GAMMA SUBUNIT; INSULIN DETEMIR; IRBESARTAN; MEMBRANE METALLOENDOPEPTIDASE; NATRIURETIC PEPTIDE RECEPTOR A; NATRIURETIC PEPTIDE RECEPTOR B; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; POTASSIUM; PRORENIN; PROTEIN; RENIN; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; SODIUM; SODIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 2; SODIUM PROTON EXCHANGE PROTEIN 3; THIORPHAN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE NEDD4-2; UNCLASSIFIED DRUG; AMINOBUTYRIC ACID DERIVATIVE; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ATRIAL NATRIURETIC FACTOR; SACUBITRIL PLUS VALSARTAN; STREPTOZOCIN; TETRAZOLE DERIVATIVE;

ACETYLCHOLINE RELEASE; ADD ON THERAPY; ALBUMINURIA; ALDOSTERONE URINE LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; BLOOD VESSEL REACTIVITY; CARDIOVASCULAR PARAMETERS; COMBINATION DRUG THERAPY; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CREATININE CLEARANCE; CREATININE URINE LEVEL; DISEASE SEVERITY; DIURESIS; DRUG EFFICACY; DRUG MECHANISM; EXPERIMENTAL DIABETIC NEPHROPATHY; EXPERIMENTAL HYPERTENSION; FOCAL GLOMERULOSCLEROSIS; GENE EXPRESSION; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; HEART WEIGHT TIBIA LENGTH RATIO; INSULIN TREATMENT; KIDNEY CORTEX; KIDNEY FUNCTION; KIDNEY MEDULLA; MONOTHERAPY; MUSCULOSKELETAL SYSTEM PARAMETERS; NATRIURESIS; NONHUMAN; OPTIMAL DRUG DOSE; OSMOTIC MINIPUMP; PLASMA RENIN ACTIVITY; POTASSIUM URINE LEVEL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEINURIA; RAT; RENAL PROTECTION; SECOND MESSENGER; SODIUM URINE LEVEL; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TELEMETRY; UPREGULATION; VASODILATATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; COMPARATIVE STUDY; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; DRUG EFFECTS; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AMINOBUTYRATES; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; ATRIAL NATRIURETIC FACTOR; BLOOD PRESSURE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; NEPRILYSIN; RATS; RATS, SPRAGUE-DAWLEY; STREPTOZOCIN; TETRAZOLES;

EID: 85014114230     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20160197     Document Type: Article

References (40)

1. Shima, M., Seino, Y., Torikai, S. and Imai, M. (1988) Intrarenal localization of degradation of atrial natriuretic peptide in isolated glomeruli and cortical nephron segments. Life Sci. 43, 357-363
2. Ando, S., Rahman, M.A., Butler, G.C., Senn, B.L. and Floras, J.S. (1995) Comparison of candoxatril and atrial natriuretic factor in healthy men: effects on hemodynamics, sympathetic activity, heart rate variability, and endothelin. Hypertension 26, 1160-1166
3. McDowell, G. and Nicholls, D.P. (1999) The endopeptidase inhibitor, candoxatril, and its therapeutic potential in the treatment of chronic cardiac failure in man. Expert Opin. Investig. Drugs 8, 79-84
4. Ruilope, L.M., Dukat, A., Bohm, M., Lacourciere, Y., Gong, J. and Lefkowitz, M.P. (2010) Blood-pressure reduction with LCZ696, a novel dual-acting inhibitor of the angiotensin II receptor and neprilysin: a randomised, double-blind, placebo-controlled, active comparator study. Lancet 375, 1255-1266
5. Solomon, S.D., Zile, M., Pieske, B., Voors, A., Shah, A., Kraigher-Krainer, E., Shi, V., Bransford, T., Takeuchi, M., Gong, J. et al. (2012) The angiotensin receptor neprilysin inhibitor LCZ696 in heart failure with preserved ejection fraction: a phase 2 double-blind randomised controlled trial. Lancet 380, 1387-1395.
6. McMurray, J.J., Packer, M., Desai, A.S., Gong, J., Lefkowitz, M.P., Rizkala, A.R., Rouleau, J.L., Shi, V.C., Solomon, S.D., Swedberg, K. and Zile, M.R. (2014) Angiotensin-neprilysin inhibition versus enalapril in heart failure. N. Engl. J. Med. 371, 993-1004
7. Davidson, E.P., Kleinschmidt, T.L., Oltman, C.L., Lund, D.D. and Yorek, M.A. (2007) Treatment of streptozotocin-induced diabetic rats with AVE7688, a vasopeptidase inhibitor: effect on vascular and neural disease. Diabetes 56, 355-362
8. Voors, A.A., Gori, M., Liu, L.C., Claggett, B., Zile, M.R., Pieske, B., McMurray, J.J., Packer, M., Shi, V., Lefkowitz, M.P. and Solomon, S.D. (2015) Renal effects of the angiotensin receptor neprilysin inhibitor LCZ696 in patients with heart failure and preserved ejection fraction. Eur. J. Heart Fail. 17, 510-517
9. Marin-Grez, M., Fleming, J.T. and Steinhausen, M. (1986) Atrial natriuretic peptide causes pre-glomerular vasodilatation and post-glomerular vasoconstriction in rat kidney. Nature 324, 473-476
10. Pedersen, M.M., Christiansen, J.S., Pedersen, E.B. and Mogensen, C.E. (1992) Determinants of intra-individual variation in kidney function in normoalbuminuric insulin-dependent diabetic patients: importance of atrial natriuretic peptide and glycaemic control. Clin. Sci. (Lond.) 83, 445-451
11. Jacobs, E.M., Vervoort, G., Branten, A.J., Klasen, I., Smits, P. and Wetzels, J.F. (1999) Atrial natriuretic peptide increases albuminuria in type I diabetic patients: evidence for blockade of tubular protein reabsorption. Eur. J. Clin. Invest. 29, 109-115
12. Yano, Y., Katsuki, A., Gabazza, E.C., Ito, K., Fujii, M., Furuta, M., Tuchihashi, K., Goto, H., Nakatani, K., Hori, Y. et al. (1999) Plasma brain natriuretic peptide levels in normotensive noninsulin-dependent diabetic patients with microalbuminuria. J. Clin. Endocrinol. Metab. 84, 2353-2356
13. Wang, T.J., Larson, M.G., Levy, D., Benjamin, E.J., Leip, E.P., Wilson, P.W. and Vasan, R.S. (2004) Impact of obesity on plasma natriuretic peptide levels. Circulation 109, 594-600
14. Magnusson, M., Jujic, A., Hedblad, B., Engstrom, G., Persson, M., Struck, J., Morgenthaler, N.G., Nilsson, P., Newton-Cheh, C., Wang, T.J. and Melander, O. (2012) Low plasma level of atrial natriuretic peptide predicts development of diabetes: the prospective Malmo Diet and Cancer study. J. Clin. Endocrinol. Metab. 97, 638-645
15. Mullins, J.J., Peters, J. and Ganten, D. (1990) Fulminant hypertension in transgenic rats harbouring the mouse Ren-2 gene. Nature 344, 541-544
16. Bachmann, S., Peters, J., Engler, E., Ganten, D. and Mullins, J. (1992) Transgenic rats carrying the mouse renin gene: morphological characterization of a low-renin hypertension model. Kidney Int. 41, 24-36
17. Stasch, J.P., Hirth-Dietrich, C., Ganten, D. and Wegner, M. (1996) Renal and antihypertensive effects of neutral endopeptidase inhibition in transgenic rats with an extra renin gene. Am. J. Hypertens. 9, 795-802
18. Kelly, D.J., Wilkinson-Berka, J.L., Allen, T.J., Cooper, M.E. and Skinner, S.L. (1998) A new model of diabetic nephropathy with progressive renal impairment in the transgenic (mRen-2)27 rat (TGR). Kidney Int. 54, 343-352
19. Roksnoer, L.C.W., van Veghel, R., de Vries, R., Garrelds, I.M., Bhaggoe, U.M., Friesema, E.C.H., Leijten, F.P.J., Poglitsch, M., Domenig, O., Clahsen-van Groningen, M.C. et al. (2015) Optimum AT receptor-neprilysin inhibition has superior cardioprotective effects compared with AT receptor blockade alone in hypertensive rats. Kidney Int. 88, 109-120
20. van Esch, J.H.M., Moltzer, E., van Veghel, R., Garrelds, I.M., Leijten, F.P.J., Bouhuizen, A.M. and Danser, A.H.J. (2010) Beneficial cardiac effects of the renin inhibitor aliskiren in spontaneously hypertensive rats. J. Hypertens. 28, 2145-2155
21. de Lannoy, L.M., Danser, A.H.J., van Kats, J.P., Schoemaker, R.G., Saxena, P.R. and Schalekamp, M.A.D.H. (1997) Renin-angiotensin system components in the interstitial fluid of the isolated perfused rat heart. Local production of angiotensin I. Hypertension 29, 1240-1251
22. Danser, A.H.J., van Kats, J.P., Admiraal, P.J., Derkx, F.H., Lamers, J.M., Verdouw, P.D., Saxena, P.R. and Schalekamp, M.A.D.H. (1994) Cardiac renin and angiotensins. Uptake from plasma versus in situ synthesis. Hypertension 24, 37-48
23. Racusen, L.C., Solez, K., Colvin, R.B., Bonsib, S.M., Castro, M.C., Cavallo, T., Croker, B.P., Demetris, A.J., Drachenberg, C.B., Fogo, A.B. et al. (1999) The Banff 97 working classification of renal allograft pathology. Kidney Int. 55, 713-723
24. van der Lubbe, N., Moes, A.D., Rosenbaek, L.L., Schoep, S., Meima, M.E., Danser, A.H.J., Fenton, R.A., Zietse, R. and Hoorn, E.J. (2013) K+-induced natriuresis is preserved during Na+ depletion and accompanied by inhibition of the Na+-Cl-cotransporter. Am. J. Physiol. Renal Physiol. 305, F1177-F1188
25. Mulvany, M.J. and Halpern, W. (1977) Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ. Res. 41, 19-26
26. MaassenVanDenBrink, A., de Vries, R., Saxena, P.R., Schalekamp, M.A.D.H. and Danser, A.H.J. (1999) Vasoconstriction by in situ formed angiotensin II: role of ACE and chymase. Cardiovasc. Res. 44, 407-415
27. Kamynina, E. and Staub, O. (2002) Concerted action of ENaC, Nedd4-2, and Sgk1 in transepithelial Na+ transport. Am. J. Physiol. Renal Physiol. 283, F377-F387
28. Azizi, M., Bissery, A., Lamarre-Cliche, M. and Menard, J. (2004) Integrating drug pharmacokinetics for phenotyping individual renin response to angiotensin II blockade in humans. Hypertension 43, 785-790
29. Hollenberg, N.K., Fisher, N.D., Nussberger, J., Moukarbel, G.V., Barkoudah, E. and Danser, A.H.J. (2011) Renal responses to three types of renin-angiotensin system blockers in patients with diabetes mellitus on a high-salt diet: a need for higher doses in diabetic patients? J. Hypertens 29, 2454-2461
30. Fagny, C., Michel, A., Leonard, I., Berkenboom, G., Fontaine, J. and Deschodt-Lanckman, M. (1991) In vitro degradation of endothelin-1 by endopeptidase 24.11 (enkephalinase). Peptides 12, 773-778
31. Donowitz, M. and Li, X. (2007) Regulatory binding partners and complexes of NHE3. Physiol. Rev. 87, 825-872
32. Hercule, H.C. and Oyekan, A.O. (2000) Role of NO and cytochrome P-450-derived eicosanoids in ET-1-induced changes in intrarenal hemodynamics in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R2132-R2141
33. Sharma, R., Lovell, H.B., Wiegmann, T.B. and Savin, V.J. (1992) Vasoactive substances induce cytoskeletal changes in cultured rat glomerular epithelial cells. J. Am. Soc. Nephrol. 3, 1131-1138
34. Abi-Gerges, N., Szabo, G., Otero, A.S., Fischmeister, R. and Mery, P.F. (2002) NO donors potentiate the beta-adrenergic stimulation of ICa, L and the muscarinic activation of IK, ACh in rat cardiac myocytes. J. Physiol. 540, 411-424
35. van den Heuvel, M, Sorop, O., Koopmans, S.J., Dekker, R., de Vries, R., van Beusekom, H.M., Eringa, E.C., Duncker, D.J., Danser, A.H.J. and van der Giessen, W.J. (2012) Coronary microvascular dysfunction in a porcine model of early atherosclerosis and diabetes. Am. J. Physiol. Heart Circ. Physiol. 302, H85-H94
36. Cherney, D.Z., Reich, H.N., Jiang, S., Har, R., Nasrallah, R., Hebert, R.L., Lai, V., Scholey, J.W. and Sochett, E.B. (2012) Hyperfiltration and effect of nitric oxide inhibition on renal and endothelial function in humans with uncomplicated type 1 diabetes mellitus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303, R710-R718
37. Moes, A.D., van der Lubbe, N., Zietse, R., Loffing, J. and Hoorn, E.J. (2014) The sodium chloride cotransporter SLC12A3: new roles in sodium, potassium, and blood pressure regulation. Pflugers Arch. 466, 107-118
38. + channels are fully activated by furin-and prostasin-dependent release of an inhibitory peptide from the γ-subunit. J. Biol. Chem. 282, 6153-6160
39. van der Lubbe, N, Lim, C.H., Meima, M.E., van Veghel, R., Rosenbaek, L.L., Mutig, K., Danser, A.H.J., Fenton, R.A., Zietse, R. and Hoorn, E.J. (2012) Aldosterone does not require angiotensin II to activate NCC through a WNK4-SPAK-dependent pathway. Pflugers Arch. 463, 853-863
40. Rijzewijk, L.J., van der Meer, R.W., Smit, J.W., Diamant, M., Bax, J.J., Hammer, S., Romijn, J.A., de Roos, A. and Lamb, H.J. (2008) Myocardial steatosis is an independent predictor of diastolic dysfunction in type 2 diabetes mellitus. J. Am. Coll. Cardiol. 52, 1793-1799