Skip to main content
Log in

Stimulatory effects of brain natriuretic peptide on cyclic GMP accumulation and tyrosine hydroxylase activity in cultured bovine adrenal medullary cells

  • Published:
Naunyn-Schmiedeberg's Archives of Pharmacology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

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

    Google Scholar 

  • Blaustein MP, Ratzlaff RW, Kendrick NK (1978) The regulation of intracellular calcium in presynaptic nerve terminals. Ann NY Acad Sci 307:195–212

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Busa WB, Richard N (1984) Metabolic regulation via intracellular pH. Am J Physiol 246:R409-R438

    Google Scholar 

  • 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

    Google Scholar 

  • Cooper JR, Bloom FE, Roth RH (1986) The biochemical basis of neuropharmacology. Oxford University Press, New York, pp 215–231

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Dunn LA, Holz RW, (1983) Catecholamine secretion from digitonin-treated adrenal medullary chromaffin cells. J Biol Chem 258:4989–4993

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Heisler S, Morrier E (1988) Bovine adrenal medullary cells contain functional atrial natriuretic peptide receptors. Biochem Biophys Res Commun 150:781–787

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Inagami T (1989) Atrial natriuretic factor. J Biol Chem 264:3043–3046

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Nishizuka Y (1986) Studies and perspectives of protein kinase C. Science 233:305–312

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Roskoski R Jr, Vulliet PR, Glass DB (1987) Phosphorylation of tyrosine hydroxylase by cyclic GMP-dependent protein kinase. J Neurochem 48:840–845

    Google Scholar 

  • 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

    Google Scholar 

  • Stahl WL, Swanson PD (1972) Calcium movements in brain slices in low sodium or calcium media. J Neurochem 19:2395–2407

    Google Scholar 

  • Sudoh T, Kangawa K, Minamino N, Matsuo H (1988) A new natriuretic peptide in porcine brain. Nature 332:78–81

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    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 

  • 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

    Google Scholar 

  • Weiner N (1970) Regulation of norepinephrine biosynthesis. Annu Rev Pharmacol 10:273–290

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00251128

Key words

Navigation