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. 1996 Nov;119(5):976–984. doi: 10.1111/j.1476-5381.1996.tb15767.x

Multiple prejunctional actions of angiotensin II on noradrenergic transmission in the caudal artery of the rat.

S L Cox 1, D F Story 1, J Ziogas 1
PMCID: PMC1915951  PMID: 8922748

Abstract

1. Angiotensin II produced concentration-dependent enhancement of both stimulation-induced (S-I) efflux of [3H]-noradrenaline and stimulation-evoked vasoconstrictor responses in isolated preparations of rat caudal artery in which the noradrenergic transmitter stores had been labelled with [3H]-noradrenaline. The threshold concentrations of angiotensin II for enhancement of S-I efflux (between 0.03 and 0.1 microM) and of the stimulation-evoked vasoconstrictor responses (about 0.3 microM) were 10-1000 times higher than those that have been found for several other vascular preparations. 2. The AT1 angiotensin II receptor antagonist losartan (0.01 and 0.1 microM), reduced or abolished the enhancement of S-I efflux by 1 and 3 microM angiotensin II and the enhancement of vasoconstrictor responses by 1 microM angiotensin II. Surprisingly, the combination of 0.01 microM losartan and 0.1 microM angiotensin II enhanced S-I efflux to a much greater extent than did 0.1 microM angiotensin II alone. Moreover, the combination of 0.01 microM losartan and 0.1 microM angiotensin II enhanced stimulation-evoked vasoconstrictor responses, in contrast to the lack of effect of 0.1 microM angiotensin II alone. 3. In a concentration of 0.01 microM, the angiotensin II AT2 receptor antagonist PD 123319 did not affect the enhancement of either S-I efflux or vasoconstrictor responses by angiotensin II. However, in a higher concentration (0.1 microM), PD 123319 antagonized the enhancement of both the S-I efflux and vasoconstrictor responses by angiotensin II. 4. In concentrations of 0.01 and 0.1 microM, PD 123319 prevented the marked enhancement of both S-I efflux and stimulation-evoked vasoconstrictor responses produced by the combination of 0.1 microM angiotensin II and 0.01 microM losartan. 5. The potentiation by losartan (0.01 microM) of the facilitatory effect of 0.1 microM angiotensin II on S-I efflux and on stimulation-evoked vasoconstriction was still observed in the presence of either the cyclooxygenase inhibitor indomethacin (3 microM), or the nitric oxide synthase inhibitor N omega-nitro-L-arginine methyl ester (L-NAME, 100 microM). 6. The findings confirm our previous suggestion that, in the rat caudal artery, angiotensin II receptors similar to the AT1B subtype subserve enhancement of transmitter noradrenaline release. 7. The synergistic prejunctional interaction of 0.01 microM losartan and 0.1 microM angiotensin II may be due to either the unmasking by losartan of a latent population of angiotensin II receptors also subserving facilitation of transmitter noradrenaline release, or alternatively, losartan may block an inhibitory action of angiotensin II on transmitter noradrenaline release which normally opposes its facilitatory effect.

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Selected References

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  1. 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]
  2. Boulanger C. M., Caputo L., Lévy B. I. Endothelial AT1-mediated release of nitric oxide decreases angiotensin II contractions in rat carotid artery. Hypertension. 1995 Nov;26(5):752–757. doi: 10.1161/01.hyp.26.5.752. [DOI] [PubMed] [Google Scholar]
  3. Brasch H., Sieroslawski L., Dominiak P. Angiotensin II increases norepinephrine release from atria by acting on angiotensin subtype 1 receptors. Hypertension. 1993 Nov;22(5):699–704. doi: 10.1161/01.hyp.22.5.699. [DOI] [PubMed] [Google Scholar]
  4. Calapai G., Squadrito F., Altavilla D., Zingarelli B., Campo G. M., Cilia M., Caputi A. P. Evidence that nitric oxide modulates drinking behaviour. Neuropharmacology. 1992 Aug;31(8):761–764. doi: 10.1016/0028-3908(92)90038-q. [DOI] [PubMed] [Google Scholar]
  5. Cassis L. A., Dwoskin L. P. Presynaptic modulation of neurotransmitter release by endogenous angiotensin II in brown adipose tissue. J Neural Transm Suppl. 1991;34:129–137. doi: 10.1007/978-3-7091-9175-0_17. [DOI] [PubMed] [Google Scholar]
  6. Catalioto R. M., Renzetti A. R., Criscuoli M., Mizrahi J., Subissi A. Angiotensins induce the release of prostacyclin from rabbit vas deferens: evidence for receptor heterogeneity. Eur J Pharmacol. 1994 Apr 11;256(1):93–97. doi: 10.1016/0014-2999(94)90621-1. [DOI] [PubMed] [Google Scholar]
  7. Chaki S., Inagami T. New signaling mechanism of angiotensin II in neuroblastoma neuro-2A cells: activation of soluble guanylyl cyclase via nitric oxide synthesis. Mol Pharmacol. 1993 Apr;43(4):603–608. [PubMed] [Google Scholar]
  8. Chiu A. T., Herblin W. F., McCall D. E., Ardecky R. J., Carini D. J., Duncia J. V., Pease L. J., Wong P. C., Wexler R. R., Johnson A. L. Identification of angiotensin II receptor subtypes. Biochem Biophys Res Commun. 1989 Nov 30;165(1):196–203. doi: 10.1016/0006-291x(89)91054-1. [DOI] [PubMed] [Google Scholar]
  9. Cox S. L., Ben A., Story D. F., Ziogas J. Evidence for the involvement of different receptor subtypes in the pre- and postjunctional actions of angiotensin II at rat sympathetic neuroeffector sites. Br J Pharmacol. 1995 Mar;114(5):1057–1063. doi: 10.1111/j.1476-5381.1995.tb13313.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ernsberger P., Zhou J., Damon T. H., Douglas J. G. Angiotensin II receptor subtypes in cultured rat renal mesangial cells. Am J Physiol. 1992 Sep;263(3 Pt 2):F411–F416. doi: 10.1152/ajprenal.1992.263.3.F411. [DOI] [PubMed] [Google Scholar]
  11. Ferrer M., Encabo A., Marín J., Balfagón G. Vasoconstrictive effects of angiotensin I and II in cat femoral arteries. Role of endothelium. Gen Pharmacol. 1992 Nov;23(6):1171–1175. doi: 10.1016/0306-3623(92)90307-6. [DOI] [PubMed] [Google Scholar]
  12. Fredholm B., Hedqvist P. Increased release of noradrenaline from stimulated guinea pig vas deferens after indomethacin treatment. Acta Physiol Scand. 1973 Apr;87(4):570–572. doi: 10.1111/j.1748-1716.1973.tb05424.x. [DOI] [PubMed] [Google Scholar]
  13. Gimbrone M. A., Jr, Alexander R. W. Angiotensin II stimulation of prostaglandin production in cultured human vascular endothelium. Science. 1975 Jul 18;189(4198):219–220. doi: 10.1126/science.1138377. [DOI] [PubMed] [Google Scholar]
  14. Gironacci M. M., Adler-Graschinsky E., Peña C., Enero M. A. Effects of angiotensin II and angiotensin-(1-7) on the release of [3H]norepinephrine from rat atria. Hypertension. 1994 Oct;24(4):457–460. doi: 10.1161/01.hyp.24.4.457. [DOI] [PubMed] [Google Scholar]
  15. Graffe K. H., Stefano F. J., Langer S. Z. Preferential metabolism of (-) 3 H-norepinephrine through the deaminated glycol in the rat vas deferens. Biochem Pharmacol. 1973 May 15;22(10):1147–1160. doi: 10.1016/0006-2952(73)90231-1. [DOI] [PubMed] [Google Scholar]
  16. Gruetter C. A., Ryan E. T., Lemke S. M., Bailly D. A., Fox M. K., Schoepp D. D. Endothelium-dependent modulation of angiotensin II-induced contraction in blood vessels. Eur J Pharmacol. 1988 Jan 27;146(1):85–95. doi: 10.1016/0014-2999(88)90489-x. [DOI] [PubMed] [Google Scholar]
  17. Hedqvist P., Stjärne L., Wennmalm A. Facilitation of sympathetic neurotransmission in the cat spleen after inhibition of prostaglandin synthesis. Acta Physiol Scand. 1971 Nov;83(3):430–432. doi: 10.1111/j.1748-1716.1971.tb05099.x. [DOI] [PubMed] [Google Scholar]
  18. Hong K. W., Rhim B. Y., Shin Y. W., Yoo S. E. Characterization of PD 121981- and CGP 42112-induced unmasking of low concentration effects of angiotensin II in rabbit abdominal aorta. J Pharmacol Exp Ther. 1994 Dec;271(3):1591–1596. [PubMed] [Google Scholar]
  19. Jaiswal N., Diz D. I., Tallant E. A., Khosla M. C., Ferrario C. M. The nonpeptide angiotensin II antagonist DuP 753 is a potent stimulus for prostacyclin synthesis. Am J Hypertens. 1991 Mar;4(3 Pt 1):228–233. doi: 10.1093/ajh/4.3.228. [DOI] [PubMed] [Google Scholar]
  20. Jaiswal N., Tallant E. A., Diz D. I., Khosla M. C., Ferrario C. M. Subtype 2 angiotensin receptors mediate prostaglandin synthesis in human astrocytes. Hypertension. 1991 Jun;17(6 Pt 2):1115–1120. doi: 10.1161/01.hyp.17.6.1115. [DOI] [PubMed] [Google Scholar]
  21. Kumagai H., Averill D. B., Khosla M. C., Ferrario C. M. Role of nitric oxide and angiotensin II in the regulation of sympathetic nerve activity in spontaneously hypertensive rats. Hypertension. 1993 Apr;21(4):476–484. doi: 10.1161/01.hyp.21.4.476. [DOI] [PubMed] [Google Scholar]
  22. Lanier S. M., Malik K. U. Attenuation by prostaglandins of the facilitatory effect of angiotensin II at adrenergic prejunctional sites in the isolated Krebs-perfused rat heart. Circ Res. 1982 Nov;51(5):594–601. doi: 10.1161/01.res.51.5.594. [DOI] [PubMed] [Google Scholar]
  23. Lanier S. M., Malik K. U. Facilitation of adrenergic transmission in the canine heart by intracoronary infusion of angiotensin II: effect of prostaglandin synthesis inhibition. J Pharmacol Exp Ther. 1983 Dec;227(3):676–682. [PubMed] [Google Scholar]
  24. Liu E. C., Hedberg A., Goldenberg H. J., Harris D. N., Webb M. L. DuP 753, the selective angiotensin II receptor blocker, is a competitive antagonist to human platelet thromboxane A2/prostaglandin H2 (TP) receptors. Prostaglandins. 1992 Aug;44(2):89–99. doi: 10.1016/0090-6980(92)90070-a. [DOI] [PubMed] [Google Scholar]
  25. Madhun Z. T., Ernsberger P., Ke F. C., Zhou J., Hopfer U., Douglas J. G. Signal transduction mediated by angiotensin II receptor subtypes expressed in rat renal mesangial cells. Regul Pept. 1993 Mar 19;44(2):149–157. doi: 10.1016/0167-0115(93)90238-4. [DOI] [PubMed] [Google Scholar]
  26. Malik K. U. Prostaglandins--modulation of adrenergic nervous system. Fed Proc. 1978 Feb;37(2):203–207. [PubMed] [Google Scholar]
  27. Mizuno K., Tani M., Niimura S., Sanada H., Haga H., Hashimoto S., Watanabe H., Ohtsuki M., Fukuchi S. Losartan, a specific angiotensin II receptor antagonist, increases angiotensin I and angiotensin II release from isolated rat hind legs: evidence for locally regulated renin-angiotensin system in vascular tissue. Life Sci. 1992;50(23):PL209–PL214. doi: 10.1016/0024-3205(92)90070-6. [DOI] [PubMed] [Google Scholar]
  28. Nasjletti A., Malik K. U. Interrelations between prostaglandins and vasoconstrictor hormones: contribution to blood pressure regulation. Fed Proc. 1982 Jun;41(8):2394–2399. [PubMed] [Google Scholar]
  29. Ribeiro M. O., Antunes E., de Nucci G., Lovisolo S. M., Zatz R. Chronic inhibition of nitric oxide synthesis. A new model of arterial hypertension. Hypertension. 1992 Sep;20(3):298–303. doi: 10.1161/01.hyp.20.3.298. [DOI] [PubMed] [Google Scholar]
  30. Sigmon D. H., Beierwaltes W. H. Renal nitric oxide and angiotensin II interaction in renovascular hypertension. Hypertension. 1993 Aug;22(2):237–242. doi: 10.1161/01.hyp.22.2.237. [DOI] [PubMed] [Google Scholar]
  31. Starke K. Regulation of noradrenaline release by presynaptic receptor systems. Rev Physiol Biochem Pharmacol. 1977;77:1–124. doi: 10.1007/BFb0050157. [DOI] [PubMed] [Google Scholar]
  32. Story D. F., Ziogas J. Role of the endothelium on the facilitatory effects of angiotensin I and angiotensin II on noradrenergic transmission in the caudal artery of the rat. Br J Pharmacol. 1986 Jan;87(1):249–255. doi: 10.1111/j.1476-5381.1986.tb10178.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Thorin E., Atkinson J. Modulation by the endothelium of sympathetic vasoconstriction in an in vitro preparation of the rat tail artery. Br J Pharmacol. 1994 Jan;111(1):351–357. doi: 10.1111/j.1476-5381.1994.tb14067.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Whitebread S., Mele M., Kamber B., de Gasparo M. Preliminary biochemical characterization of two angiotensin II receptor subtypes. Biochem Biophys Res Commun. 1989 Aug 30;163(1):284–291. doi: 10.1016/0006-291x(89)92133-5. [DOI] [PubMed] [Google Scholar]
  35. Wong P. C., Bernard R., Timmermans P. B. Effect of blocking angiotensin II receptor subtype on rat sympathetic nerve function. Hypertension. 1992 Jun;19(6 Pt 2):663–667. doi: 10.1161/01.hyp.19.6.663. [DOI] [PubMed] [Google Scholar]
  36. Wong P. C., Hart S. D., Timmermans P. B. Effect of angiotensin II antagonism on canine renal sympathetic nerve function. Hypertension. 1991 Jun;17(6 Pt 2):1127–1134. doi: 10.1161/01.hyp.17.6.1127. [DOI] [PubMed] [Google Scholar]
  37. Zhang J., Van Meel J. C., Pfaffendorf M., Zhang J., Van Zwieten P. A. Endothelium-dependent, nitric oxide-mediated inhibition of angiotensin II-induced contractions in rabbit aorta. Eur J Pharmacol. 1994 Sep 12;262(3):247–253. doi: 10.1016/0014-2999(94)90738-2. [DOI] [PubMed] [Google Scholar]
  38. Zhou J., Ernsberger P., Douglas J. G. A novel angiotensin receptor subtype in rat mesangium. Coupling to adenylyl cyclase. Hypertension. 1993 Jun;21(6 Pt 2):1035–1038. doi: 10.1161/01.hyp.21.6.1035. [DOI] [PubMed] [Google Scholar]
  39. Zimmerman B. G., Gomer S. K., Liao J. C. Action of angiotensin on vascular adrenergic nerve endings: facilitation of norepinephrine release. Fed Proc. 1972 Jul-Aug;31(4):1344–1350. [PubMed] [Google Scholar]
  40. de Gasparo M., Husain A., Alexander W., Catt K. J., Chiu A. T., Drew M., Goodfriend T., Harding J. W., Inagami T., Timmermans P. B. Proposed update of angiotensin receptor nomenclature. Hypertension. 1995 May;25(5):924–927. doi: 10.1161/01.hyp.25.5.924. [DOI] [PubMed] [Google Scholar]

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