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British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1990 Mar;99(3):536–540. doi: 10.1111/j.1476-5381.1990.tb12964.x

Inhibitory action of alpha-human atrial natriuretic peptide on noradrenaline-induced synthesis of myo-inositol 1,4,5-trisphosphate in the smooth muscle cells of rabbit aorta.

J Kajikuri 1, H Kuriyama 1
PMCID: PMC1917350  PMID: 1970498

Abstract

1. Interactions between the synthesis of myo-inositol 1,4,5-trisphosphate (IP3) and guanosine 3':5'-cyclic monophosphate (cyclic GMP) in the smooth muscle cells of the rabbit aorta were investigated. 2. In the presence or absence of vascular endothelium, noradrenaline (NA; 5 microM) consistently reduced the amount of phosphatidylinositol 4,5-bisphosphate (PI-P2) and increased both phosphatidic acid (PA) and IP3. 3. In the presence or absence of endothelium, acetylcholine (ACh; 100 microM but not 5 microM) slightly increased the amount of IP3, but exposure to ACh (100 microM) 4 min after application of NA did not modify NA-induced synthesis of IP3. 4. ACh (100 microM) markedly enhanced the synthesis of cyclic GMP in the presence of endothelium but not in the endothelium-denuded tissues. 5. Prazosin (5 microM) but not dibutyryl cyclic GMP (db-cyclic GMP; 100 microM) blocked the hydrolysis of PI-P2 induced by 5 microM NA. Synthesis of IP3 induced by NA, as estimated with [3H]-inositol was not modified by application of 100 microM db-cyclic AMP or db-cyclic GMP. 6. alpha-Human atrial natriuretic peptide (alpha-hANP; 0.1 microM) increased cyclic GMP in the presence or absence of endothelium. alpha-hANP (0.1 microM) consistently inhibited the hydrolysis of PI-P2 induced by 5 microM NA. 7. The results indicate that synthesis of IP3 is inhibited neither by the synthesis of cyclic GMP in the cytosol nor by cyclic GMP itself. However, synthesis of IP3 through hydrolysis of PI-P2 may be inhibited by an interaction between some steps in the IP3 synthetic process and by the activation of the alpha-hANP-guanylate cyclase process at the sarcolemma.

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Selected References

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  1. Abdel-Latif A. A. Calcium-mobilizing receptors, polyphosphoinositides, and the generation of second messengers. Pharmacol Rev. 1986 Sep;38(3):227–272. [PubMed] [Google Scholar]
  2. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  3. Berridge M. J. Regulation of ion channels by inositol trisphosphate and diacylglycerol. J Exp Biol. 1986 Sep;124:323–335. doi: 10.1242/jeb.124.1.323. [DOI] [PubMed] [Google Scholar]
  4. Billah M. M., Lapetina E. G. Rapid decrease of phosphatidylinositol 4,5-bisphosphate in thrombin-stimulated platelets. J Biol Chem. 1982 Nov 10;257(21):12705–12708. [PubMed] [Google Scholar]
  5. Bokoch G. M., Katada T., Northup J. K., Ui M., Gilman A. G. Purification and properties of the inhibitory guanine nucleotide-binding regulatory component of adenylate cyclase. J Biol Chem. 1984 Mar 25;259(6):3560–3567. [PubMed] [Google Scholar]
  6. Chinkers M., Garbers D. L., Chang M. S., Lowe D. G., Chin H. M., Goeddel D. V., Schulz S. A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature. 1989 Mar 2;338(6210):78–83. doi: 10.1038/338078a0. [DOI] [PubMed] [Google Scholar]
  7. Hashimoto T., Hirata M., Itoh T., Kanmura Y., Kuriyama H. Inositol 1,4,5-trisphosphate activates pharmacomechanical coupling in smooth muscle of the rabbit mesenteric artery. J Physiol. 1986 Jan;370:605–618. doi: 10.1113/jphysiol.1986.sp015953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Holzmann S. Endothelium-induced relaxation by acetylcholine associated with larger rises in cyclic GMP in coronary arterial strips. J Cyclic Nucleotide Res. 1982;8(6):409–419. [PubMed] [Google Scholar]
  9. Ignarro L. J., Harbison R. G., Wood K. S., Wolin M. S., McNamara D. B., Hyman A. L., Kadowitz P. J. Differences in responsiveness of intrapulmonary artery and vein to arachidonic acid: mechanism of arterial relaxation involves cyclic guanosine 3':5'-monophosphate and cyclic adenosine 3':5'-monophosphate. J Pharmacol Exp Ther. 1985 Jun;233(3):560–569. [PubMed] [Google Scholar]
  10. Ignarro L. J., Kadowitz P. J. The pharmacological and physiological role of cyclic GMP in vascular smooth muscle relaxation. Annu Rev Pharmacol Toxicol. 1985;25:171–191. doi: 10.1146/annurev.pa.25.040185.001131. [DOI] [PubMed] [Google Scholar]
  11. Iino M. Calcium dependent inositol trisphosphate-induced calcium release in the guinea-pig taenia caeci. Biochem Biophys Res Commun. 1987 Jan 15;142(1):47–52. doi: 10.1016/0006-291x(87)90449-9. [DOI] [PubMed] [Google Scholar]
  12. Irvine R. F., Moor R. M. Inositol(1,3,4,5)tetrakisphosphate-induced activation of sea urchin eggs requires the presence of inositol trisphosphate. Biochem Biophys Res Commun. 1987 Jul 15;146(1):284–290. doi: 10.1016/0006-291x(87)90723-6. [DOI] [PubMed] [Google Scholar]
  13. Itoh T., Kubota Y., Kuriyama H. Effects of a phorbol ester on acetylcholine-induced Ca2+ mobilization and contraction in the porcine coronary artery. J Physiol. 1988 Mar;397:401–419. doi: 10.1113/jphysiol.1988.sp017008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kikuchi A., Yamashita T., Kawata M., Yamamoto K., Ikeda K., Tanimoto T., Takai Y. Purification and characterization of a novel GTP-binding protein with a molecular weight of 24,000 from bovine brain membranes. J Biol Chem. 1988 Feb 25;263(6):2897–2904. [PubMed] [Google Scholar]
  15. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  16. Ljung B., Kjellstedt A. Functional antagonism of noradrenaline responses by felodipine and other calcium antagonists in vascular smooth muscles. J Cardiovasc Pharmacol. 1987;10 (Suppl 1):S82–S88. doi: 10.1097/00005344-198710001-00016. [DOI] [PubMed] [Google Scholar]
  17. Martin W., Villani G. M., Jothianandan D., Furchgott R. F. Selective blockade of endothelium-dependent and glyceryl trinitrate-induced relaxation by hemoglobin and by methylene blue in the rabbit aorta. J Pharmacol Exp Ther. 1985 Mar;232(3):708–716. [PubMed] [Google Scholar]
  18. Nakashima S., Tohmatsu T., Hattori H., Okano Y., Nozawa Y. Inhibitory action of cyclic GMP on secretion, polyphosphoinositide hydrolysis and calcium mobilization in thrombin-stimulated human platelets. Biochem Biophys Res Commun. 1986 Mar 28;135(3):1099–1104. doi: 10.1016/0006-291x(86)91041-7. [DOI] [PubMed] [Google Scholar]
  19. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  20. Ohya Y., Terada K., Yamaguchi K., Inoue R., Okabe K., Kitamura K., Hirata M., Kuriyama H. Effects of inositol phosphates on the membrane activity of smooth muscle cells of the rabbit portal vein. Pflugers Arch. 1988 Sep;412(4):382–389. doi: 10.1007/BF01907556. [DOI] [PubMed] [Google Scholar]
  21. Okajima F., Katada T., Ui M. Coupling of the guanine nucleotide regulatory protein to chemotactic peptide receptors in neutrophil membranes and its uncoupling by islet-activating protein, pertussis toxin. A possible role of the toxin substrate in Ca2+-mobilizing receptor-mediated signal transduction. J Biol Chem. 1985 Jun 10;260(11):6761–6768. [PubMed] [Google Scholar]
  22. Rapoport R. M. Cyclic guanosine monophosphate inhibition of contraction may be mediated through inhibition of phosphatidylinositol hydrolysis in rat aorta. Circ Res. 1986 Mar;58(3):407–410. doi: 10.1161/01.res.58.3.407. [DOI] [PubMed] [Google Scholar]
  23. Rapoport R. M., Draznin M. B., Murad F. Endothelium-dependent relaxation in rat aorta may be mediated through cyclic GMP-dependent protein phosphorylation. Nature. 1983 Nov 10;306(5939):174–176. doi: 10.1038/306174a0. [DOI] [PubMed] [Google Scholar]
  24. Rapoport R. M., Draznin M. B., Murad F. Mechanisms of adenosine triphosphate-, thrombin-, and trypsin-induced relaxation of rat thoracic aorta. Circ Res. 1984 Oct;55(4):468–479. doi: 10.1161/01.res.55.4.468. [DOI] [PubMed] [Google Scholar]
  25. Rapoport R. M., Murad F. Effect of cyanide on nitrovasodilator-induced relaxation, cyclic GMP accumulation and guanylate cyclase activation in rat aorta. Eur J Pharmacol. 1984 Sep 3;104(1-2):61–70. doi: 10.1016/0014-2999(84)90369-8. [DOI] [PubMed] [Google Scholar]
  26. Rapoport R. M., Murad F. Endothelium-dependent and nitrovasodilator-induced relaxation of vascular smooth muscle: role of cyclic GMP. J Cyclic Nucleotide Protein Phosphor Res. 1983;9(4-5):281–296. [PubMed] [Google Scholar]
  27. Somlyo A. V., Bond M., Somlyo A. P., Scarpa A. Inositol trisphosphate-induced calcium release and contraction in vascular smooth muscle. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5231–5235. doi: 10.1073/pnas.82.15.5231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sternweis P. C., Robishaw J. D. Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain. J Biol Chem. 1984 Nov 25;259(22):13806–13813. [PubMed] [Google Scholar]
  29. Suematsu E., Hirata M., Hashimoto T., Kuriyama H. Inositol 1,4,5-trisphosphate releases Ca2+ from intracellular store sites in skinned single cells of porcine coronary artery. Biochem Biophys Res Commun. 1984 Apr 30;120(2):481–485. doi: 10.1016/0006-291x(84)91279-8. [DOI] [PubMed] [Google Scholar]
  30. Takai Y., Kaibuchi K., Sano K., Nishizuka Y. Counteraction of calcium-activated, phospholipid-dependent protein kinase activation by adenosine 3',5'-monophosphate and guanosine 3',5'-monophosphate in platelets. J Biochem. 1982 Jan;91(1):403–406. doi: 10.1093/oxfordjournals.jbchem.a133700. [DOI] [PubMed] [Google Scholar]
  31. Takai Y., Kikkawa U., Kaibuchi K., Nishizuka Y. Membrane phospholipid metabolism and signal transduction for protein phosphorylation. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;18:119–158. [PubMed] [Google Scholar]
  32. Tremblay J., Gerzer R., Vinay P., Pang S. C., Béliveau R., Hamet P. The increase of cGMP by atrial natriuretic factor correlates with the distribution of particulate guanylate cyclase. FEBS Lett. 1985 Feb 11;181(1):17–22. doi: 10.1016/0014-5793(85)81105-4. [DOI] [PubMed] [Google Scholar]
  33. Waldman S. A., Rapoport R. M., Murad F. Atrial natriuretic factor selectively activates particulate guanylate cyclase and elevates cyclic GMP in rat tissues. J Biol Chem. 1984 Dec 10;259(23):14332–14334. [PubMed] [Google Scholar]
  34. Winquist R. J., Faison E. P., Waldman S. A., Schwartz K., Murad F., Rapoport R. M. Atrial natriuretic factor elicits an endothelium-independent relaxation and activates particulate guanylate cyclase in vascular smooth muscle. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7661–7664. doi: 10.1073/pnas.81.23.7661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yamaguchi K., Hirata M., Kuriyama H. Calmodulin activates inositol 1,4,5-trisphosphate 3-kinase activity in pig aortic smooth muscle. Biochem J. 1987 Jun 15;244(3):787–791. doi: 10.1042/bj2440787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yamamoto K., Kondo J., Hishida T., Teranishi Y., Takai Y. Purification and characterization of a GTP-binding protein with a molecular weight of 20,000 in bovine brain membranes. Identification as the rho gene product. J Biol Chem. 1988 Jul 15;263(20):9926–9932. [PubMed] [Google Scholar]

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