Natriuretic peptides relax human intrarenal arteries through natriuretic peptide receptor type-A recapitulated by soluble guanylyl cyclase agonists.
cGMP
eNOS
endothelium
hypertension
kidney
Journal
Acta physiologica (Oxford, England)
ISSN: 1748-1716
Titre abrégé: Acta Physiol (Oxf)
Pays: England
ID NLM: 101262545
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
08
05
2020
revised:
07
08
2020
accepted:
26
09
2020
pubmed:
4
10
2020
medline:
19
8
2021
entrez:
3
10
2020
Statut:
ppublish
Résumé
Natriuretic peptides, BNP and ANP increase renal blood flow in experimental animals. The signalling pathway in human kidney vasculature is unknown. It was hypothesized that BNP and ANP cause endothelium-independent relaxation of human intrarenal arteries by vascular natriuretic peptide receptor-A, but not -B and -C, which is mimicked by agonists of soluble guanylyl cyclase sGC. Human (n = 54, diameter: 665 ± 29 µm 95% CI) and control murine intrarenal arteries (n = 83, diameter 300 ± 6 µm 95% CI) were dissected and used for force recording by four-channel wire myography. Arterial segments were pre-contracted, then subjected to increasing concentrations of BNP, ANP, phosphodiesterase 5-inhibitor sildenafil, sGC-activator BAY 60-2770 and -stimulator BAY 41-2272. Endothelial nitric oxide synthase (eNOS) dependence was examined by use of L-NAME and eNOS knockout respectively. Molecular targets (NPR A-C, sGC, phosphodiesterase-5 and neprilysin) were mapped by PCR, immunohistochemistry and RNAscope. BNP, ANP, sildenafil, sGC-activation and -stimulation caused concentration-dependent relaxation of human and murine intrarenal arteries. BNP responses were independent of eNOS and were not potentiated by low concentration of phosphodiesterase-5-inhibitor, sGC-stimulator or NPR-C blocker. PCR showed NPR-A and C, phosphodiesterase-5, neprilysin and sGC mRNA in renal arteries. NPR-A mRNA and protein was observed in vascular smooth muscle and endothelial cells in arteries, podocytes, Bowmans capsule and vasa recta. NPR-C was observed in tubules, glomeruli and vasculature. Activation of transmembrane NPR-A and soluble guanylyl cyclase relax human preglomerular arteries similarly to phosphodiestase-5 inhibition. The human renal arterial bed relaxes in response to cGMP pathway.
Substances chimiques
Natriuretic Peptides
0
Guanylate Cyclase
EC 4.6.1.2
Soluble Guanylyl Cyclase
EC 4.6.1.2
Cyclic GMP
H2D2X058MU
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13565Informations de copyright
© 2020 Scandinavian Physiological Society. Published by John Wiley & Sons Ltd.
Références
Lanese DM, Yuan BH, Falk SA, Conger JD. Effects of atriopeptin III on isolated rat afferent and efferent arterioles. Am J Physiol. 1991;261(6 Pt 2):F1102-F1109.
Marin-Grez M, Fleming JT, Steinhausen M. Atrial natriuretic peptide causes pre-glomerular vasodilatation and post-glomerular vasoconstriction in rat kidney. Nature. 1986;324(6096):473-476.
Veldkamp PJ, Carmines PK, Inscho EW, Navar LG. Direct evaluation of the microvascular actions of ANP in juxtamedullary nephrons. Am J Physiol. 1988;254(3 Pt 2):F440-F444.
Loutzenhiser R, Hayashi K, Epstein M. Atrial natriuretic peptide reverses afferent arteriolar vasoconstriction and potentiates efferent arteriolar vasoconstriction in the isolated perfused rat kidney. J Pharmacol Exp Ther. 1988;246(2):522-528.
Endlich K, Steinhausen M. Natriuretic peptide receptors mediate different responses in rat renal microvessels. Kidney Int. 1997;52(1):202-207.
Takezawa K, Cowley AW Jr, Skelton M, Roman RJ. Atriopeptin III alters renal medullary hemodynamics and the pressure-diuresis response in rats. Am J Physiol. 1987;252(6 Pt 2):F992-F1002.
Sward K, Valson F, Ricksten SE. Long-term infusion of atrial natriuretic peptide (ANP) improves renal blood flow and glomerular filtration rate in clinical acute renal failure. Acta Anaesthesiol Scand. 2001;45(5):536-542.
Valsson F, Ricksten SE, Hedner T, Lundin S. Effects of atrial natriuretic peptide on acute renal impairment in patients with heart failure after cardiac surgery. Intensive Care Med. 1996;22(3):230-236.
Thiesson HC, Jensen BL, Jespersen B, et al. Inhibition of cGMP-specific phosphodiesterase type 5 reduces sodium excretion and arterial blood pressure in patients with NaCl retention and ascites. Am J Physiol Renal Physiol. 2005;288(5):F1044-F1052.
Kolsrud O, Damen T, Nygren A, et al. Effects of atrial natriuretic peptide on renal function during cardiopulmonary bypass: a randomized pig model. Eur J Cardiothorac Surg. 2020;57(4):652-659.
Rahman SN, Kim GE, Mathew AS, et al. Effects of atrial natriuretic peptide in clinical acute renal failure. Kidney Int. 1994;45(6):1731-1738.
Sward K, Valsson F, Odencrants P, Samuelsson O, Ricksten SE. Recombinant human atrial natriuretic peptide in ischemic acute renal failure: a randomized placebo-controlled trial. Crit Care Med. 2004;32(6):1310-1315.
Sward K, Valsson F, Sellgren J, Ricksten SE. Differential effects of human atrial natriuretic peptide and furosemide on glomerular filtration rate and renal oxygen consumption in humans. Intensive Care Med. 2005;31(1):79-85.
Haynes R, Judge PK, Staplin N, et al. Effects of sacubitril/valsartan versus irbesartan in patients with chronic kidney disease. Circulation. 2018;138(15):1505-1514.
Holtwick R, Gotthardt M, Skryabin B, et al. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci USA. 2002;99(10):7142-7147.
Holtwick R, van Eickels M, Skryabin BV, et al. Pressure-independent cardiac hypertrophy in mice with cardiomyocyte-restricted inactivation of the atrial natriuretic peptide receptor guanylyl cyclase-A. J Clin Invest. 2003;111(9):1399-1407.
Villar IC, Panayiotou CM, Sheraz A, et al. Definitive role for natriuretic peptide receptor-C in mediating the vasorelaxant activity of C-type natriuretic peptide and endothelium-derived hyperpolarising factor. Cardiovasc Res. 2007;74(3):515-525.
Moyes AJ, Khambata RS, Villar I, et al. Endothelial C-type natriuretic peptide maintains vascular homeostasis. J Clin Invest. 2014;124(9):4039-4051.
Sabrane K, Kruse MN, Fabritz L, et al. Vascular endothelium is critically involved in the hypotensive and hypovolemic actions of atrial natriuretic peptide. J Clin Invest. 2005;115(6):1666-1674.
Edvinsson ML, Uddman E, Edvinsson L, Andersson SE. Brain natriuretic peptide is a potent vasodilator in aged human microcirculation and shows a blunted response in heart failure patients. J Geriatr Cardiol. 2014;11(1):50-56.
Chai SY, Sexton PM, Allen AM, Figdor R, Mendelsohn FA. In vitro autoradiographic localization of ANP receptors in rat kidney and adrenal gland. Am J Physiol. 1986;250(4 Pt 2):F753-F757.
Sexton PM, Zhuo J, Mendelsohn FA. Localization and regulation of renal receptors for angiotensin II and atrial natriuretic peptide. Tohoku J Exp Med. 1992;166(1):41-56.
Bie P. Natriuretic peptides and normal body fluid regulation. Compr Physiol. 2018;8(3):1211-1249.
Hughes AD, Nielsen H, Sever PS. The effect of atrial natriuretic peptide on human isolated resistance arteries. Br J Pharmacol. 1989;97(4):1027-1030.
Schulz S, Singh S, Bellet RA, et al. The primary structure of a plasma membrane guanylate cyclase demonstrates diversity within this new receptor family. Cell. 1989;58(6):1155-1162.
Peng H, Matchkov V, Ivarsen A, Aalkjaer C, Nilsson H. Hypothesis for the initiation of vasomotion. Circ Res. 2001;88(8):810-815.
Otsuka K, Tanaka H, Horinouchi T, Koike K, Shigenobu K, Tanaka Y. Functional contribution of voltage-dependent and Ca2+ activated K+ (BK(Ca)) channels to the relaxation of guinea-pig aorta in response to natriuretic peptides. J Smooth Muscle Res. 2002;38(4-5):117-129.
Staffel J, Valletta D, Federlein A, et al. Natriuretic peptide receptor guanylyl cyclase-A in podocytes is renoprotective but dispensable for physiologic renal function. J Am Soc Nephrol. 2017;28(1):260-277.
Sato F, Kamoi K, Wakiya Y, et al. Relationship between plasma atrial natriuretic peptide levels and atrial pressure in man. J Clin Endocrinol Metab. 1986;63(4):823-827.
Luchner A, Hengstenberg C, Lowel H, Riegger GA, Schunkert H, Holmer S. Effect of compensated renal dysfunction on approved heart failure markers: direct comparison of brain natriuretic peptide (BNP) and N-terminal pro-BNP. Hypertension. 2005;46(1):118-123.
van Kimmenade RR, Januzzi JL Jr, Bakker JA, et al. Renal clearance of B-type natriuretic peptide and amino terminal pro-B-type natriuretic peptide a mechanistic study in hypertensive subjects. J Am Coll Cardiol. 2009;53(10):884-890.
Theilig F, Bostanjoglo M, Pavenstadt H, et al. Cellular distribution and function of soluble guanylyl cyclase in rat kidney and liver. J Am Soc Nephrol. 2001;12(11):2209-2220.
Mundel P, Gambaryan S, Bachmann S, Koesling D, Kriz W. Immunolocalization of soluble guanylyl cyclase subunits in rat kidney. Histochem Cell Biol. 1995;103(1):75-79.
Lledo-Garcia E, Rodriguez-Martinez D, Cabello-Benavente R, et al. Sildenafil improves immediate posttransplant parameters in warm-ischemic kidney transplants: experimental study. Transplant Proc. 2007;39(5):1354-1356.
Lledo-Garcia E, Subira-Rios D, Ogaya-Pinies G, Tejedor-Jorge A, Canizo-Lopez JF, Hernandez-Fernandez C. Intravenous sildenafil as a preconditioning drug against hemodynamic consequences of warm ischemia-reperfusion on the kidney. J Urol. 2011;186(1):331-333.