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Atrial natriuretic peptide receptors along the rat and rabbit nephrons: [125I] α-rat atrial natriuretic peptide binding in microdissected glomeruli and tubules

  • Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands
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Abstract

Binding of [125I] α-rat atrial natriuretic peptide ([125I] α-RANP) was measured in glomeruli and pieces of tubule microdissected from rat and rabbit nephrons. High densities of specific ANP binding sites were found only in the glomeruli (10–30×10−18 mol·glom−1), whereas no specific binding could be detected in the proximal tubule, the thin segments of the Henle's loop, the thick ascending limb, the distal tubule and the cortical and outer medullary collecting tubules. Rising the temperature from 4° C to 35° C resulted in biphasic kinetics of binding, suggesting a temperature-dependent inactivation of labelled hormone by glomeruli. At 4° C, specific binding of [125I] α-RANP was time and dose-dependent and Scatchard analysis of data indicated an apparent equilibrium dissociation constant of 0.63 nM. Competition experiments revealed the following sequence of stereospecificity for binding to rat glomeruli: RANP 3–28>[125I] α-RANP=[125I] α-HANP=α-RANP=atriopeptin III > atriopeptin II, whereas binding was unaffected by pharmacological doses of unrelated peptide hormones, prostaglandins, adrenergic agonists, dopamine, histamine and carbamylcholine. The results indicate that glomerular binding sites might be the physiological ANP receptors.

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Abbreviations

ANP:

atria natriuretic peptide

α0RANP:

alpha rat atrial natriuretic peptide

PCT:

proximal convoluted tubule

PR:

pars recta

TDL:

thin descending limb

TAL:

thin ascending limb

MAL:

medullary thick ascending limb

CAL:

dortical thick ascending limb

DCT:

distal convoluted tubule

DCTb:

distal convoluted tubule bright

DCTg:

distal convoluted tubule granular

CCT:

conrtical collecting tubule

MCT:

outer medullary collecting tubule

References

  • Anderson J, Struthers A, Christofides N, Bloom S (1986) Plasma release of atrial natriuretic peptide and its biological effect in man. Renal Physiol 9:103–104

    Google Scholar 

  • Ausiello DA, Kreisberg JI, Roy C, Karnovsky MJ (1980) Contraction of cultured rat glomerular cells of apparent mesangial origin after stimulation with angiotensin II and arginine vasopressin. J Clin Invest 65:754–760

    Google Scholar 

  • Ballermann BJ, Brenner BM (1985) Biologically active atrial peptides. J Clin Invest 76:2041–2048

    Google Scholar 

  • Ballermann BJ, Hoover RL, Karnovsky MJ, Brenner BM (1985) Physiologic regulation of atrial natriuretic peptide receptors in rat renal glomeruli. J Clin Invest 76:2049–2056

    Google Scholar 

  • Briggs JP, Marin-Grez M, Steipe B, Schubert G, Schnermann J (1984) Inactivation of atrial natriuretic substance by kallikrein. Am J Physiol 247:F480–F484

    Google Scholar 

  • Camargo MJF, Kleinert HD, Atlas SA, Sealey JE, Laragh JH, Maack T (1984) Ca-dependent hemodynamic and natriuretic effects of atrial extract in isolated rat kidney. Am J Physiol 246:F447–F456

    Google Scholar 

  • Cantin M, Thibault G, Gutkowska J, Garcia R, Hamet P, Anand-Srivastava MB, Genest J (1985) The heart as an endocrin gland. Regul Pept Suppl 4:83–88

    Google Scholar 

  • Chabardès D, Montégut M, Mistaoui M, Butlen D, Morel F (1987) Atrial natriuretic peptide effects on cGMP and cAMP contents in microdissected glomeruli and segments of the rat and rabbit nephrons. Pflügers Arch 408:366–372

    Google Scholar 

  • Chai SY, Sexton PM, Allen AM, Figdor R, Mendelsohn FAO (1986) In vitro autoradiographic localization of ANP receptors in rat kidney and adrenal gland. Am J Physiol 250:F753–F757

    Google Scholar 

  • Chaudhari A, Kirschenbaum MA (1985) Specific prostaglandin E2 binding sites in isolated rat glomeruli: evidence for glomerular PGE receptors. Prost Leuk Med 20:55–68

    Google Scholar 

  • Cogan MG (1986) Atrial natriuretic factor can increase renal solute excretion primarily by raising glomerular filtration. Am J Physiol 250:F710–F714

    Google Scholar 

  • De Léan A, Vinay P, Cantin M (1985) Distribution of atrial natriuretic factor receptors in dog kidney fractions. FEBS Lett 193:239–242

    Google Scholar 

  • Dillingham MA, Anderson RJ (1986) Inhibition of vasopressin action by atrial natriuretic factor. Science 231:1572–1573

    Google Scholar 

  • Exton JM (1985) Mechanisms involved in alpha-adrenergic phenomena. Am J Physiol 248:E633–E647

    Google Scholar 

  • Felder RA, Blecher M, Calcagno PL, Jose PA (1984 a) dopamine receptors in the proximal tubule of the rabbit. Am J Physiol 247:F499–F505

    Google Scholar 

  • Felder RA, Blecher M, Eisner GM, Jose PA (1984b) Cortical tubular and glomerular dopamine receptors in the rat kidney. Am J Physiol 246:F557–F568

    Google Scholar 

  • Gex-Fabry M, De Lisi C (1984) Model for kinetic and steady state analysis of receptor mediated endocytosis. Mathematical Biosci 72:245–261

    Google Scholar 

  • Guillon G, Butlen D (1984) Kinetical and physicochemical properties of V1 and V2 vasopressin receptors: relation to cyclic AMP dependent and calcium dependent activation processes. In: Dumont JE, Nunez J (eds) Hormone and cell regulation, vol 8. Elsevier Science Publishers BV, Amsterdam, p 69

    Google Scholar 

  • Hammond TG, Yusufi ANK, Knox FG, Dousa TP (1985) Administration of atrial natriuretic factor inhibits sodium-coupled transport in proximal tubules. J Clin Invest 75:1983–1989

    Google Scholar 

  • Harris RB, Wilson IB (1985) Comparison of hydrolysis of atriopeptin II stand-in substrate by atrial dipeptidyl carboxyhydrolase and angiotensin I-converting enzyme. Int J Peptide Protein Res 26:78–82

    Google Scholar 

  • Healy DP, Fanestil DD (1986) Localization of atrial natriuretic peptide binding sites within the rat kidney. Am J Physiol 250:F573–F578

    Google Scholar 

  • Hori R, Inui KI, Saito H, Matsukawa Y, Okumura K, Nakao K, Morii N, Imura H (1985) Specific receptors for atrial natriuretic polypeptide on basolateral membranes isolated from rat renal cortex. Biochem Biophys Res Commun 129:773–779

    Google Scholar 

  • Imbert M, Chabardès D, Morel F, Montégut M, Clique A (1974) Hormone-sensitive adenylate-cyclase in isolated rabbit glomeruli. Mol Cell Endocrinol 1:295–304

    Google Scholar 

  • Imbert-Teboul M, Chabardès D, Montégut M, Clique A, Morel F (1978) Vasopressin-dependent adenylate cyclase activities in the rat kidney medulla: evidence for two separate sites of action. Endocrinology 102:1254–1261

    Google Scholar 

  • Inui KI, Saito H, Matsukawa Y, Nakao K, Morii N, Imura H, Shimokura M, Kiso Y, Hori R (1985) Specific binding activities and cyclic GMP responses by atrial natriuretic polypeptide in kidney epithelial cell line (LLC-PK1). Biochem Biophys Res Commun 132:253–260

    Google Scholar 

  • Koseki C, Hayashi Y, Torikai S, Furuya M, Ohnuma N, Imai M (1986) Localization of binding sites for alpha-rat atrial natriuretic polypeptide in rat kidney. Am J Physiol 250:F210–F216

    Google Scholar 

  • Kuno T, Andresen JW, Kamisaki Y, Waldman SA, Chang LY, Saheki S, Leitman DC, Nakane M, Murad F (1986) Co-purification of an atrial natriuretic factor receptor and particulate guanylate cyclase from rat lung. J Biol Chem 261:5817–5823

    Google Scholar 

  • Levy M (1975) Further observations on the responses of the glomerular filtration rate to glucagon: comparison with secretin. Can J Physiol Pharmacol 53:81–85

    Google Scholar 

  • Lynch DR, Braas KM, Snyder SH (1986) Atrial natriuretic factor receptors in rat kidney, adrenal gland and brain: autoradiographic localization and fluid balance dependent changes. Proc Natl Acad Sci USA 83:3357–3361

    Google Scholar 

  • Maack T, Camargo MJF, Kleinert HD, Laragh JH, Atlas SA (1985) Atrial natriuretic factor: structure and functional properties. Kidney Int 27:607–615

    Google Scholar 

  • Marchetti J, Imbert-Teboul M, Alhenc-Gelas F, Allegrini J, Menard J, Morel F (1984) Kallikrein along the rabbit microdissected nephron: a micromethod for its measurement. Pflügers Arch 401:27–33

    Google Scholar 

  • McPherson GA, Summers RJ (1983 a) Evidence from binding studies for beta1-adrenoceptors associated with glomeruli isolated from the rat kidney. Life Sci 33:87–94

    Google Scholar 

  • McPherson GA, Summers RJ (1983 b) Evidence from binding studies for alpha2-adrenoceptors directly associated with glomeruli from rat kidney. Eur J Pharmacol 90:333–341

    Google Scholar 

  • Meezan E, Freychet P (1979) Rat renal glomeruli and tubules have specific insulin receptors of differing affinity. Mol Pharmacol 16:1095–1100

    Google Scholar 

  • Morel F, Chabardès D, Imbert-Teboul M (1978) Methodology for enzymatic studies of isolated tubular segments: adenylate cyclase. In: Martinez-Maldonado M (ed) Methods in pharmacology, vol 4B, Renal pharmacology, chapt 11 Plenum Press, New York London, p 297

    Google Scholar 

  • Muntz KH, Garcia C, Hagler HK (1985) Alpha1-receptor localization in rat heart and kidney using autoradiography. Am J Physiol 249:H512-H519

    Google Scholar 

  • Murray RD, Itoh S, Inagami T, Misono K, Seto S, Scicli AG, Carretero OA (1985) Effects of synthetic atrial natriuretic factor in the isolated perfused rat kidney. Am J Physiol 249:F603–F609

    Google Scholar 

  • Nakamura R, Emmanouel DS, Katz AI (1983) Insulin binding sites in various segments of the rabbit nephron. J Clin Invest 72:388–392

    Google Scholar 

  • Nakamura R, Hayashi M, Emmanouel DS, Katz AI (1986) Sites of insulin and glucagon metabolism in the rabbit nephron. Am J Physiol 250:F144–F150

    Google Scholar 

  • Pastan IH, Willingham MC (1981) Journey to the center of the cell: role of the receptosome. Science 214:504–509

    Google Scholar 

  • Sonnenberg H (1986) Mechanisms of release and renal tubular action of atrial natriuretic factor. Fed Proc 45:2106–2110

    Google Scholar 

  • Sosa RE, Volpe M, Marion DN, Atlas SA, Laragh JH, Vaughan ED Jr, Maack T (1986) Relationship between renal hemodynamic and natriuretic effects of atrial natriuretic factor. Am J Physiol 250:F520–F524

    Google Scholar 

  • Sraer JD, Sraer J, Ardaillou R, Mimoune D (1974) Evidence of renal glomerular receptors for angiotensin II. Kidney Int 6:241–246

    Google Scholar 

  • Tomita K, Pisano JJ (1984) Binding of [3H]bradykinin in isolated nephron segments ofthe rabbit. Am J Physiol 246:F732–F737

    Google Scholar 

  • Torres VE, Northrup TE, Edwards RM, Shah SV, Dousa TP (1978) Modulation of cyclic nucleotides in isolated rat glomeruli. Role of histamine, carbamylcholine, parathyroid hormone and angiotensin II. J Clin Invest 62:1334–1343

    Google Scholar 

  • Umemura S, Smyth DD, Pettinger WA (1985) Lack of inhibition by atrial natriuretic factor on cyclic AMP levels in single nephron segments and the glomerulus. Biochem Biophys Res Comm 127:943–949

    Google Scholar 

  • Von Schroeder HP, Nishimura E, McIntosh CHS, Buchan AMJ, Wilson N, Ledsome JR (1985) Autoradiographic localization of binding sites for atrial natriuretic factorl Can J Physiol Pharmacol 63:1373–1377

    Google Scholar 

  • Waldman SA, Rapoport RM, Murad F (1984) Atrial natriuretic factor selectively activates particulate guanylate cyclase and elevates cyclic GMP in rat tissues. J Biol Chem 259:14332–14334

    Google Scholar 

  • Weidmann P, Hasler L, Gnädinger MP, Lang RE, Uehlinger DE, Shaw S, Rascher W, Reubi FC (1986) Blood levels and renal effects of atrial natriuretic peptide in normal man. J Clin Invest 77:734–742

    Google Scholar 

  • Weselcouch EO, Humphrey WR, Aiken JW (1985) Effect of pulmonary and renal circulations on activity of atrial natriuretic factor. Am J Physiol 249:R595-R602

    Google Scholar 

  • Winquist RJ (1985) The relaxant effects of atrial natriuretic factor on vascular smooth muscle. Life Sci 37:1081–1087

    Google Scholar 

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Butlen, D., Mistaoui, M. & Morel, F. Atrial natriuretic peptide receptors along the rat and rabbit nephrons: [125I] α-rat atrial natriuretic peptide binding in microdissected glomeruli and tubules. Pflugers Arch. 408, 356–365 (1987). https://doi.org/10.1007/BF00581129

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