Summary
We studied the effect of brain natriuretic peptide (BNP) on the accumulation of cyclic GMP and the phosphorylation and activity of tyrosine hydroxylase, compared with that of atrial natriuretic peptide (ANP), in cultured bovine adrenal medullary cells. 1. BNP as well as ANP increased cellular cyclic GMP accumulation in a concentration-dependent manner (10–1000 nmol/1). BNP (1 μmol/1) and ANP (1 μmol/1) produced a 60-fold and 30-fold increase in cyclic GMP accumulation, respectively. 2. The stimulatory effects of BNP and ANP on cyclic GMP accumulation were observed even when Ca2+ or Na+ was removed from the incubation medium. 3. 12-O-Tetradecanoylphorbol 13-acetate (TPA), an activator of protein kinase C, inhibited the stimulatory effect of BNP on cyclic GMP accumulation in a concentration-dependent manner (1–100 nmol/1). Furthermore, the BNP-induced accumulation of cyclic GMP was attenuated by forskolin (1 μmol/1), an activator of adenylate cyclase. 4. BNP (1 μmol/1) and ANP (1 μ mol/1) caused a significant increase in phosphorylation and activity of tyrosine hydroxylase in the cells. 5. In digitonin-permeabilized cells, cyclic GMP (1–100 μmol/1) activated tyrosine hydroxylase in the presence of ATP and Mg2+.
These results suggest that BNP stimulates the accumulation of cyclic GMP in a manner similar to that of ANP. The increased accumulation of cyclic GMP by these peptides may be negatively modulated by protein kinase C and cyclic AMP and may cause the phosphorylation and activation of tyrosine hydroxylase-in cultured bovine adrenal medullary cells.
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References
Ballermann BJ, Marala RB, Sharma RK (1988) Characterization and regulation by protein kinase C of renal glomerular atrial natriuretic peptide receptor-coupled guanylate cyclase. Biochem Biophys Res Commun 157:755–761
Blaustein MP, Ratzlaff RW, Kendrick NK (1978) The regulation of intracellular calcium in presynaptic nerve terminals. Ann NY Acad Sci 307:195–212
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Busa WB, Richard N (1984) Metabolic regulation via intracellular pH. Am J Physiol 246:R409-R438
Chang M, Lowe DG, Lewis M, Hellmiss R, Chen E, Goeddel DV (1989) Differential activation by atrial and brain natriuretic peptides of two different receptor guanylate cyclases. Nature 341:68–72
Cooper JR, Bloom FE, Roth RH (1986) The biochemical basis of neuropharmacology. Oxford University Press, New York, pp 215–231
Currie MG, Geller DM, Cole BR, Siegel NR, Fok KF, Adams SP, Eubanks SR, Galluppi GR, Needleman P (1984) Purification and sequence analysis of bioactive atrial peptides (atriopeptins). Science 223:67–69
Douglas WW, Rubin RP (1961) The role of calcium in the secretory response of the adrenal medulla to acetylcholine. J Physiol (Lond) 159:40–57
Drewett J, Marchand G, Ziegler R, Trachte G (1988) Atrial natriuretic factor inhibits norepinephrine release in an adrenergic clonal cell line (PC12). Eur J Pharmacol 150:175–179
Dunn LA, Holz RW, (1983) Catecholamine secretion from digitonin-treated adrenal medullary chromaffin cells. J Biol Chem 258:4989–4993
Flynn TG, de Bold ML, de Bold AJ (1983) The amino acid sequence of an atrial peptide with potent diuretic and natriuretic properties. Biochem Biophys Res Commun 117:859–865
Hamet P, Tremblay J, Pang SC, Garcia R, Thibault G, Gutkowska J, Cantin M, Genest J (1984) Effect of native and synthetic atrial natriuretic factor on cyclic GMP. Biochem Biophys Res Commun 123:515–527
Haycock JW, Meligeni JA, Bennett WF, Waymire JC (1982) Phosphorylation and activation of tyrosine hydroxylase mediate the acetylcholine-induced increase in catecholamine biosynthesis in adrenal chromaffin cells. J Biol Chem 257:12641–12648
Heisler S, Morrier E (1988) Bovine adrenal medullary cells contain functional atrial natriuretic peptide receptors. Biochem Biophys Res Commun 150:781–787
Hirata Y, Shichiri M, Emori T, Marumo F, Kangawa K, Matsuo H (1988) Brain natriuretic peptide interacts with atrial natriuretic peptide receptor in cultured rat vascular smooth muscle cells. FEBS Lett 238:415–418
Houchi H, Nakagawa H, Oka M, Watanabe J, Isosaki M, Ohuchi T (1984) Increase in cyclic AMP level and stimulation of catecholamine synthesis in isolated bovine adrenal medullary cells caused by forskolin. Jpn J Pharmacol 36:97–99
Inagami T (1989) Atrial natriuretic factor. J Biol Chem 264:3043–3046
Jaiswal RK, Sharma RK (1988) Inhibition of α2-adrenergic receptor-mediated cyclic GMP formation by a phorbol ester, a protein kinase C activator. Biochem Biophys Res Commun 156:905–909
Kangawa K, Matsuo H (1984) Purification and complete amino acid sequence of α-human atrial natriuretic polypeptide (α-hANP). Biochem Biophys Res Commun 118:131–139
Minamino N, Aburaya M, Ueda S, Kangawa K, Matsuo H (1988) The presence of brain natriuretic peptide of 12000 daltons in porcine heart. Biochem Biophys Res Commun 155:740–746
Misono KS, Fukumi H, Grammer RT, Inagami T (1984) Rat atrial natriuretic factor: complete amino acid sequence and disulfide linkage essential for biological activity. Biochem Biophys Res Commun 119:524–529
Nakamura M, Inagami T (1986) Atrial natriuretic factor inhibits norepinephrine release evoked by sympathetic nerve stimulation in isolated perfused rat mesenteric arteries. Eur J Pharmacol 123:459–461
Nishizuka Y (1986) Studies and perspectives of protein kinase C. Science 233:305–312
Oehlenschlager WF, Baron DA, Schomer H, Currie MG (1989) Atrial and brain natriuretic peptides share binding sites in the kidney and heart. Eur J Pharmacol 161:159–164
Oka M, Isosaki M, Yanagihara N (1979) Isolated bovine adrenal medullary cells: studies on regulation of catecholamine synthesis and release. In: Usdin E, Kopin IJ, Barchas J (eds) Catecholamines: basic and clinical frontiers. Pergamon Press, Oxford, pp 70–72
Okazaki M, Yanagihara N, Izumi F, Nakashima Y, Kuroiowa A (1989) Carbachol-induced cosecretion of immunoreactive atrial natriuretic peptides with catecholamines from cultured bovine adrenal medullary cells. J Neurochem 52:222–228
Ong H, Lazure C, Nguyen TT, McNicoll N, Seidah N, Chrétien M, De Léan A (1987) Bovine adrenal chromaffin granules are a site of synthesis of atrial natriuretic factor. Biochem Biophys Res Commun 147:957–963
O'Sullivan AJ, Burgoyne RD (1990) Cyclic GMP regulates nicotine-induced secretion from cultured bovine adrenal chromaffin cells: effects of 8-bromo-cyclic GMP, atrial natriuretic peptide, and nitroprusside (nitric oxide). J Neurochem 54:1805–1808
Roskoski R Jr, Roskoski LM (1987) Activation of tyrosine hydroxylase in PC12 cells by the cyclic GMP and cyclic AMP second messenger systems. J Neurochem 48:236–242
Roskoski R Jr, Vulliet PR, Glass DB (1987) Phosphorylation of tyrosine hydroxylase by cyclic GMP-dependent protein kinase. J Neurochem 48:840–845
Song D-L, Kohse KP, Murad F (1988) Brain natriuretic factor: augmentation of cellular cyclic GMP, activation of particulate guanylate cyclase and receptor binding. FEBS Lett 232:125–129
Stahl WL, Swanson PD (1972) Calcium movements in brain slices in low sodium or calcium media. J Neurochem 19:2395–2407
Sudoh T, Kangawa K, Minamino N, Matsuo H (1988) A new natriuretic peptide in porcine brain. Nature 332:78–81
Ueda S, Minamino N, Sudoh T, Kangawa K, Matsuo H (1988) Regional distribution of immunoreactive brain natriuretic peptide in porcine brain and spinal cord. Biochem Biophys Res Commun 155:733–739
Uezono Y, Yanagihara N, Wada A, Koda Y, Yokota K, Kobayashi H, Izumi F (1989) Veratridine-induced phosphorylation and activation of tyrosine hydroxylase, and synthesis of catecholamines in cultured bovine adrenal medullary cells. Naunyn-Schmiedeberg's Arch Pharmacol 339:653–659
Wada A, Takara H, Izumi F, Kobayashi H, Yanagihara N (1985) Influx of 22Na through acetylcholine receptor-associated Na channels: relationship between 22Na influx, 45Ca influx and secretion of catecholamines in cultured bovine adrenal medulla cells. Neuroscience 15:283–292
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
Waldman SA, Rapoport RM, Fiscus RR, Murad F (1985) Effects of atriopeptin on particulate guanylate cyclase from rat adrenal. Biochim Biophys Act 845:298–303
Weiner N (1970) Regulation of norepinephrine biosynthesis. Annu Rev Pharmacol 10:273–290
Weiner N, Lee F-L, Dreyer E, Barnes E (1978) The activation of tyrosine hydroxylase in noradrenergic neurons during acute nerve stimulation. Life Sci 22:1197–1216
Yanagihara N, Isosaki M, Ohuchi T, Oka M (1979) Muscarinic receptor-mediated increase in cyclic GMP level in isolated bovine adrenal medullary cells. FEBS Lett 105:296–298
Yanagihara N, Tank AW, Weiner N (1984) Relationship between activation and phosphorylation of tyrosine hydroxylase by 56 mM K+ in PC12 cells in culture. Mol Pharmacol 26:141–147
Yanagihara N, Uezono Y, Koda Y, Wada A, Izumi F (1987a) Activation of tyrosine hydroxylase by micromolar concentrations of calcium in digitonin-permeabilized adrenal medullary cells. Biochem Biophys Res Commun 146:530–536
Yanagihara N, Yokota K, Wada A, Izumi F (1987b) Intracellular pH and catecholamine synthesis in cultured bovine adrenal medullary cells: effect of extracellular Na+ removal. J Neurochem 49:1740–1746
Yanagihara N, Yokota K, Kobayashi H, Wada A, Uezono Y, Izumi F (1990) Sodium/proton exchange in cultured bovine adrenal medullary cells. J Neurochem 54:1626–1631
Yoshimasa T, Sibley DR, Bouvier M, Lefkowitz RJ, Caron MG (1987) Cross-talk between cellular signalling; pathways suggested by phorbol-ester-induced adenylate cyclase phosphorylation. Nature 327:67–70
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Yanagihara, N., Okazaki, M., Terao, T. et al. Stimulatory effects of brain natriuretic peptide on cyclic GMP accumulation and tyrosine hydroxylase activity in cultured bovine adrenal medullary cells. Naunyn-Schmiedeberg's Arch Pharmacol 343, 289–295 (1991). https://doi.org/10.1007/BF00251128
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DOI: https://doi.org/10.1007/BF00251128