Abstract
In smooth-muscle cells (SMC) isolated from rat aorta, angiotensin II stimulates a phospholipase C with subsequent formation of inositol trisphosphate (InsP3). Short-term (10 min) pretreatment of SMC with 12-O-tetradecanoylphorbol 13-acetate (TPA; 100 nM) decreases the angiotensin II-induced InsP3 formation. However, this inhibition is not observed after incubating the cells for 2 h with TPA. Longer-term pretreatments even lead to an enhanced generation of InsP3. This increased response to angiotensin II occurs without a significant change in the receptor number or Kd value of angiotensin II binding to the cells. The biologically inactive phorbol ester 4 alpha-phorbol 12,13-didecanoate was without effect on angiotensin II-stimulated InsP3 generation, irrespective of the time of preincubation. In parallel with this potentiation of angiotensin II-induced generation of InsP3 by TPA, a down-regulation of protein kinase C activity is observed. A 24 h pretreatment of SMC with TPA decreases protein kinase C activity to less than 10% of that of control cells. Longer-term pretreatment also increases the angiotensin II-induced release of Ca2+ and delays the decay of the transient Ca2+ increase. All these data suggest that protein kinase C exerts a negative feedback control on angiotensin II-stimulated polyphosphoinositide turnover, and that protein kinase C is an important factor in limiting the production of InsP3 in stimulated cells.
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Selected References
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- Aiken J. W., Vane J. R. Intrarenal prostaglandin release attenuates the renal vasoconstrictor activity of angiotensin. J Pharmacol Exp Ther. 1973 Mar;184(3):678–687. [PubMed] [Google Scholar]
- Alexander R. W., Brock T. A., Gimbrone M. A., Jr, Rittenhouse S. E. Angiotensin increases inositol trisphosphate and calcium in vascular smooth muscle. Hypertension. 1985 May-Jun;7(3 Pt 1):447–451. [PubMed] [Google Scholar]
- Ballester R., Rosen O. M. Fate of immunoprecipitable protein kinase C in GH3 cells treated with phorbol 12-myristate 13-acetate. J Biol Chem. 1985 Dec 5;260(28):15194–15199. [PubMed] [Google Scholar]
- Berridge M. J. Inositol trisphosphate and diacylglycerol as second messengers. Biochem J. 1984 Jun 1;220(2):345–360. doi: 10.1042/bj2200345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berridge M. J. Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem. 1987;56:159–193. doi: 10.1146/annurev.bi.56.070187.001111. [DOI] [PubMed] [Google Scholar]
- 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]
- Berridge M. J. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem J. 1983 Jun 15;212(3):849–858. doi: 10.1042/bj2120849. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berthon B., Binet A., Mauger J. P., Claret M. Cytosolic free Ca2+ in isolated rat hepatocytes as measured by quin2. Effects of noradrenaline and vasopressin. FEBS Lett. 1984 Feb 13;167(1):19–24. doi: 10.1016/0014-5793(84)80824-8. [DOI] [PubMed] [Google Scholar]
- Blackshear P. J., Witters L. A., Girard P. R., Kuo J. F., Quamo S. N. Growth factor-stimulated protein phosphorylation in 3T3-L1 cells. Evidence for protein kinase C-dependent and -independent pathways. J Biol Chem. 1985 Oct 25;260(24):13304–13315. [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
- Brock T. A., Rittenhouse S. E., Powers C. W., Ekstein L. S., Gimbrone M. A., Jr, Alexander R. W. Phorbol ester and 1-oleoyl-2-acetylglycerol inhibit angiotensin activation of phospholipase C in cultured vascular smooth muscle cells. J Biol Chem. 1985 Nov 15;260(26):14158–14162. [PubMed] [Google Scholar]
- Brown K. D., Blakeley D. M., Hamon M. H., Laurie M. S., Corps A. N. Protein kinase C-mediated negative-feedback inhibition of unstimulated and bombesin-stimulated polyphosphoinositide hydrolysis in Swiss-mouse 3T3 cells. Biochem J. 1987 Aug 1;245(3):631–639. doi: 10.1042/bj2450631. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Capponi A. M., Lew P. D., Vallotton M. B. Cytosolic free calcium levels in monolayers of cultured rat aortic smooth muscle cells. Effects of angiotensin II and vasopressin. J Biol Chem. 1985 Jul 5;260(13):7836–7842. [PubMed] [Google Scholar]
- Caramelo C., Tsai P., Schrier R. W. Mechanism of cellular effect of phorbol esters on action of arginine vasopressin and angiotensin II on rat vascular smooth muscle cells in culture. Biochem J. 1988 Sep 15;254(3):625–629. doi: 10.1042/bj2540625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins M. K., Rozengurt E. Homologous and heterologous mitogenic desensitization of Swiss 3T3 cells to phorbol esters and vasopressin: role of receptor and postreceptor steps. J Cell Physiol. 1984 Feb;118(2):133–142. doi: 10.1002/jcp.1041180205. [DOI] [PubMed] [Google Scholar]
- Drummond A. H. Bidirectional control of cytosolic free calcium by thyrotropin-releasing hormone in pituitary cells. 1985 Jun 27-Jul 3Nature. 315(6022):752–755. doi: 10.1038/315752a0. [DOI] [PubMed] [Google Scholar]
- Hannun Y. A., Loomis C. R., Merrill A. H., Jr, Bell R. M. Sphingosine inhibition of protein kinase C activity and of phorbol dibutyrate binding in vitro and in human platelets. J Biol Chem. 1986 Sep 25;261(27):12604–12609. [PubMed] [Google Scholar]
- Hepler J. R., Earp H. S., Harden T. K. Long-term phorbol ester treatment down-regulates protein kinase C and sensitizes the phosphoinositide signaling pathway to hormone and growth factor stimulation. Evidence for a role of protein kinase C in agonist-induced desensitization. J Biol Chem. 1988 Jun 5;263(16):7610–7619. [PubMed] [Google Scholar]
- Hidaka H., Inagaki M., Kawamoto S., Sasaki Y. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry. 1984 Oct 9;23(21):5036–5041. doi: 10.1021/bi00316a032. [DOI] [PubMed] [Google Scholar]
- Irvine R. F., Anggård E. E., Letcher A. J., Downes C. P. Metabolism of inositol 1,4,5-trisphosphate and inositol 1,3,4-trisphosphate in rat parotid glands. Biochem J. 1985 Jul 15;229(2):505–511. doi: 10.1042/bj2290505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Irvine R. F., Letcher A. J., Heslop J. P., Berridge M. J. The inositol tris/tetrakisphosphate pathway--demonstration of Ins(1,4,5)P3 3-kinase activity in animal tissues. Nature. 1986 Apr 17;320(6063):631–634. doi: 10.1038/320631a0. [DOI] [PubMed] [Google Scholar]
- Katada T., Gilman A. G., Watanabe Y., Bauer S., Jakobs K. H. Protein kinase C phosphorylates the inhibitory guanine-nucleotide-binding regulatory component and apparently suppresses its function in hormonal inhibition of adenylate cyclase. Eur J Biochem. 1985 Sep 2;151(2):431–437. doi: 10.1111/j.1432-1033.1985.tb09120.x. [DOI] [PubMed] [Google Scholar]
- Kuo J. F., Raynor R. L., Mazzei G. J., Schatzman R. C., Turner R. S., Kem W. R. Cobra polypeptide cytotoxin I and marine worm polypeptide cytotoxin A-IV are potent and selective inhibitors of phospholipid-sensitive Ca2+-dependent protein kinase. FEBS Lett. 1983 Mar 7;153(1):183–186. doi: 10.1016/0014-5793(83)80144-6. [DOI] [PubMed] [Google Scholar]
- Leeb-Lundberg L. M., Cotecchia S., Lomasney J. W., DeBernardis J. F., Lefkowitz R. J., Caron M. G. Phorbol esters promote alpha 1-adrenergic receptor phosphorylation and receptor uncoupling from inositol phospholipid metabolism. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5651–5655. doi: 10.1073/pnas.82.17.5651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lo W. W., Hughes J. Differential regulation of cholecystokinin- and muscarinic-receptor-mediated phosphoinositide turnover in Flow 9000 cells. Biochem J. 1988 May 1;251(3):625–630. doi: 10.1042/bj2510625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch C. J., Charest R., Bocckino S. B., Exton J. H., Blackmore P. F. Inhibition of hepatic alpha 1-adrenergic effects and binding by phorbol myristate acetate. J Biol Chem. 1985 Mar 10;260(5):2844–2851. [PubMed] [Google Scholar]
- MCGIFF J. C., ITSKOVITZ H. D. LOSS OF THE RENAL VASOCONSTRICTOR ACTIVITY OF ANGIOTENSIN II DURING RENAL ISCHEMIA. J Clin Invest. 1964 Dec;43:2359–2367. doi: 10.1172/JCI105110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MacIntyre D. E., McNicol A., Drummond A. H. Tumour-promoting phorbol esters inhibit agonist-induced phosphatidate formation and Ca2+ flux in human platelets. FEBS Lett. 1985 Jan 28;180(2):160–164. doi: 10.1016/0014-5793(85)81063-2. [DOI] [PubMed] [Google Scholar]
- Munson P. J., Rodbard D. Ligand: a versatile computerized approach for characterization of ligand-binding systems. Anal Biochem. 1980 Sep 1;107(1):220–239. doi: 10.1016/0003-2697(80)90515-1. [DOI] [PubMed] [Google Scholar]
- Naccache P. H., Molski T. F., Borgeat P., White J. R., Sha'afi R. I. Phorbol esters inhibit the fMet-Leu-Phe- and leukotriene B4-stimulated calcium mobilization and enzyme secretion in rabbit neutrophils. J Biol Chem. 1985 Feb 25;260(4):2125–2131. [PubMed] [Google Scholar]
- 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]
- Orellana S., Solski P. A., Brown J. H. Guanosine 5'-O-(thiotriphosphate)-dependent inositol trisphosphate formation in membranes is inhibited by phorbol ester and protein kinase C. J Biol Chem. 1987 Feb 5;262(4):1638–1643. [PubMed] [Google Scholar]
- Pandiella A., Vicentini L. M., Meldolesi J. Protein kinase C-mediated feed back inhibition of the Ca2+ response at the EGF receptor. Biochem Biophys Res Commun. 1987 Nov 30;149(1):145–151. doi: 10.1016/0006-291x(87)91616-0. [DOI] [PubMed] [Google Scholar]
- Pfeilschifter J., Bauer C. Different effects of phorbol ester on angiotensin II- and stable GTP analogue-induced activation of polyphosphoinositide phosphodiesterase in membranes isolated from rat renal mesangial cells. Biochem J. 1987 Nov 15;248(1):209–215. doi: 10.1042/bj2480209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfeilschifter J., Bauer C. Pertussis toxin abolishes angiotensin II-induced phosphoinositide hydrolysis and prostaglandin synthesis in rat renal mesangial cells. Biochem J. 1986 May 15;236(1):289–294. doi: 10.1042/bj2360289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfeilschifter J., Kurtz A., Bauer C. Role of phospholipase C and protein kinase C in vasoconstrictor-induced prostaglandin synthesis in cultured rat renal mesangial cells. Biochem J. 1986 Feb 15;234(1):125–130. doi: 10.1042/bj2340125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfeilschifter J. Protein kinase C from rat renal mesangial cells: its role in homologous desensitization of angiotensin II-induced polyphosphoinositide hydrolysis. Biochim Biophys Acta. 1988 May 13;969(3):263–270. doi: 10.1016/0167-4889(88)90061-4. [DOI] [PubMed] [Google Scholar]
- Pfeilschifter J., Rüegg U. T. Cyclosporin A augments angiotensin II-stimulated rise in intracellular free calcium in vascular smooth muscle cells. Biochem J. 1987 Dec 15;248(3):883–887. doi: 10.1042/bj2480883. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfeilschifter J. Tumour promotor 12-O-tetradecanoylphorbol 13-acetate inhibits angiotensin II-induced inositol phosphate production and cytosolic Ca2+ rise in rat renal mesangial cells. FEBS Lett. 1986 Jul 28;203(2):262–266. doi: 10.1016/0014-5793(86)80755-4. [DOI] [PubMed] [Google Scholar]
- Regoli D., Park W. K., Rioux F. Pharmacology of angiotensin. Pharmacol Rev. 1974 Jun;26(2):69–123. [PubMed] [Google Scholar]
- Rodriguez-Pena A., Rozengurt E. Disappearance of Ca2+-sensitive, phospholipid-dependent protein kinase activity in phorbol ester-treated 3T3 cells. Biochem Biophys Res Commun. 1984 May 16;120(3):1053–1059. doi: 10.1016/s0006-291x(84)80213-2. [DOI] [PubMed] [Google Scholar]
- Ross R. The smooth muscle cell. II. Growth of smooth muscle in culture and formation of elastic fibers. J Cell Biol. 1971 Jul;50(1):172–186. doi: 10.1083/jcb.50.1.172. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sagi-Eisenberg R., Lieman H., Pecht I. Protein kinase C regulation of the receptor-coupled calcium signal in histamine-secreting rat basophilic leukaemia cells. Nature. 1985 Jan 3;313(5997):59–60. doi: 10.1038/313059a0. [DOI] [PubMed] [Google Scholar]
- Schwertschlag U. S., Whorton A. R. Platelet-activating factor-induced homologous and heterologous desensitization in cultured vascular smooth muscle cells. J Biol Chem. 1988 Sep 25;263(27):13791–13796. [PubMed] [Google Scholar]
- Sibley D. R., Lefkowitz R. J. Molecular mechanisms of receptor desensitization using the beta-adrenergic receptor-coupled adenylate cyclase system as a model. Nature. 1985 Sep 12;317(6033):124–129. doi: 10.1038/317124a0. [DOI] [PubMed] [Google Scholar]
- Smith C. D., Uhing R. J., Snyderman R. Nucleotide regulatory protein-mediated activation of phospholipase C in human polymorphonuclear leukocytes is disrupted by phorbol esters. J Biol Chem. 1987 May 5;262(13):6121–6127. [PubMed] [Google Scholar]
- Smith J. B., Smith L., Brown E. R., Barnes D., Sabir M. A., Davis J. S., Farese R. V. Angiotensin II rapidly increases phosphatidate-phosphoinositide synthesis and phosphoinositide hydrolysis and mobilizes intracellular calcium in cultured arterial muscle cells. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7812–7816. doi: 10.1073/pnas.81.24.7812. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sommerville L. E., Hartshorne D. J. Intracellular calcium and smooth muscle contraction. Cell Calcium. 1986 Dec;7(5-6):353–364. doi: 10.1016/0143-4160(86)90038-2. [DOI] [PubMed] [Google Scholar]
- Tamaoki T., Nomoto H., Takahashi I., Kato Y., Morimoto M., Tomita F. Staurosporine, a potent inhibitor of phospholipid/Ca++dependent protein kinase. Biochem Biophys Res Commun. 1986 Mar 13;135(2):397–402. doi: 10.1016/0006-291x(86)90008-2. [DOI] [PubMed] [Google Scholar]
- Travo P., Weber K., Osborn M. Co-existence of vimentin and desmin type intermediate filaments in a subpopulation of adult rat vascular smooth muscle cells growing in primary culture. Exp Cell Res. 1982 May;139(1):87–94. doi: 10.1016/0014-4827(82)90321-4. [DOI] [PubMed] [Google Scholar]
- Tsien R. Y., Pozzan T., Rink T. J. Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J Cell Biol. 1982 Aug;94(2):325–334. doi: 10.1083/jcb.94.2.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wahl M., Carpenter G. Regulation of epidermal growth factor-stimulated formation of inositol phosphates in A-431 cells by calcium and protein kinase C. J Biol Chem. 1988 Jun 5;263(16):7581–7590. [PubMed] [Google Scholar]
- Young S., Parker P. J., Ullrich A., Stabel S. Down-regulation of protein kinase C is due to an increased rate of degradation. Biochem J. 1987 Jun 15;244(3):775–779. doi: 10.1042/bj2440775. [DOI] [PMC free article] [PubMed] [Google Scholar]