DOI QR코드

DOI QR Code

Inhibitory Effects of Olmesartan on Catecholamine Secretion from the Perfused Rat Adrenal Medulla

  • Lim, Hyo-Jeong (Department of Internal Medicine, School of Medicine, Seoul National University) ;
  • Kim, Sang-Yong (Division of Endocrinology, Department of Internal Medicine, College of Medicine, Chosun University) ;
  • Lim, Dong-Yoon (Department of Pharmacology, College of Medicine, Chosun University)
  • Received : 2010.08.02
  • Accepted : 2010.08.19
  • Published : 2010.08.30

Abstract

The present sutdy aimed to determine whether olmesartan, an angiotensin II (Ang II) type 1 ($AT_1$) receptor blocker, can influence the CA release from the isolated perfused model of the rat adrenal medulla. Olmesartan ($5{\sim}50{\mu}M$) perfused into an adrenal vein for 90 min produced dose- and time-dependent inhibition of the CA secretory responses evoked by ACh (5.32 mM), high $K^+$ (56 mM, a direct membrane-depolarizer), DMPP (100 ${\mu}M$) and McN-A-343 (100 ${\mu}M$). Olmesartan did not affect basal CA secretion. Also, in adrenal glands loaded with olmesartan (15 ${\mu}M$), the CA secretory responses evoked by Bay-K-8644 (10 ${\mu}M$, an activator of voltage-dependent L-type $Ca^{2+}$ channels), cyclopiazonic acid (10 ${\mu}M$, an inhibitor of cytoplasmic $Ca^{2+}$-ATPase), veratridine (100 ${\mu}M$, an activator of voltage-dependent $Na^+$ channels), and Ang II (100 nM) were markedly inhibited. However, at high concentrations ($150{\sim}300{\mu}M$), olmesartan rather enhanced the ACh-evoked CA secretion. Taken together, these results show that olmesartan at low concentrations inhibits the CA secretion evoked by cholinergic stimulation (both nicotininc and muscarinic receptors) as well as by direct membrane depolarization from the rat adrenal medulla, but at high concentrations it rather potentiates the ACh-evoked CA secretion. It seems that olmesartan has a dual action, acting as both agonist and antagonist at nicotinic receptors of the isolated perfused rat adrenal medulla, which might be dependent on the concentration. It is also thought that this inhibitory effect of olmesartan may be mediated by blocking the influx of both $Na^+$ and $Ca^{2+}$ into the rat adrenomedullary chromaffin cells as well as by inhibiting the $Ca^{2+}$ release from the cytoplasmic calcium store, which is thought to be relevant to the $AT_1$ receptor blockade, in addition to its enhancement on the CA secreton.

Keywords

References

  1. Mire DE, Silfani TN, Pugsley MK. A review of the structural and functional features of olmesartan medoxomil, an angiotensin receptor blocker. J Cardiovasc Pharmacol. 2005;46:585-593. https://doi.org/10.1097/01.fjc.0000180902.78230.fd
  2. Mizuno M, Sada T, Ikeda M, Fukuda N, Miyamoto M, Yanagisawa H, Koike H. Pharmacology of CS-866, a novel nonpeptide angiotensin II receptor antagonist. Eur J Pharmacol. 1995;285:181-188. https://doi.org/10.1016/0014-2999(95)00401-6
  3. Burnier M. Angiotensin II type 1 receptor blockers. Circulation. 2001;103:904-912. https://doi.org/10.1161/01.CIR.103.6.904
  4. Goodfriend TL, Elliott ME, Catt KJ. Angiotensin receptors and their antagonists. N Engl J Med. 1996;334:1649-1654. https://doi.org/10.1056/NEJM199606203342507
  5. Kakuta H, Sudoh K, Sasamata M, Yamagishi S. Telmisartan has the strongest binding affinity to angiotensin II type 1 receptor: comparison with other angiotensin II type 1 receptor blockers. Int J Clin Pharmacol Res. 2005;25:41-46.
  6. Le MT, Pugsley MK, Vauquelin G, Van Liefde I. Molecular characterisation of the interactions between olmesartan and telmisartan and the human angiotensin II AT1 receptor. Br J Pharmacol. 2007;151:952-962.
  7. Oparil S, Silfani TN, Walker JF. Role of angiotensin receptor blockers as monotherapy in reaching blood pressure goals. Am J Hypertens. 2005;18:287-294. https://doi.org/10.1016/j.amjhyper.2004.07.021
  8. Smith DHG. Strategies to meet lower blood pressure goals with a new standard in angiotensin II receptor blockade. Am J Hypertens. 2002;15:108-114.
  9. Teschemacher AG, Seward EP. Bidirectional modulation of exocytosis by angiotensin II involves multiple G-protein-regulated transduction pathways in chromaffin cells. The J Neurosci. 2000;20:4776-4785.
  10. Uresin Y, Erbas B, Ozek M, Ozkok E, Gürol AO. Losartan may prevent the elevation of plasma glucose, corticosterone and catecholamine levels induced by chronic stress. J Renin Angiotensin Aldosterone Syst. 2004;5:93-96. https://doi.org/10.3317/jraas.2004.017
  11. Seltzer A, Bregonzio C, Armando I, Baiardi G, Saavedra JM. Oral administration of an $AT_{1}$ receptor antagonist prevents the central effects of angiotensin II in spontaneously hypertensive rats. Brain Res. 2004;1028:9-18. https://doi.org/10.1016/j.brainres.2004.06.079
  12. Critchley L, Ding B, Fok B, Wang D, Tomlinson B, James A, Thomas GN, Critchley J. The effects of candesartan and ramipril on adrenal catecholamine release in anaesthetized dogs. Eur J Pharmacol. 2004;489:67-75. https://doi.org/10.1016/j.ejphar.2004.02.036
  13. Takekoshi K, Ishii K, Kawakami Y, Isobe K, Nakai T. Activation of angiotensin II subtype 2 receptor induces catecholamine release in an extracellular $Ca^{2+}$-dependent manner through a decrease of cyclic guanosine 3',5'-monophosphate production in cultured porcine adrenal medullary chromaffin cells. Endocrinol. 2001;142:3075-3086. https://doi.org/10.1210/en.142.7.3075
  14. Martineau D, Lamouche S, Briand R, Yamaguchi N. Functional involvement of angiotensin $AT_{2}$ receptor in adrenal catecholamine secretion in vivo. Can J Physiol Pharmacol. 1999;77: 367-374. https://doi.org/10.1139/y99-037
  15. Worck RH, Frandsen E, Ibsen H, Petersen JS. AT1 and AT2 receptor blockade and epinephrine release during insulin-induced hypoglycemia. Hyperten. 1998;31:384-390. https://doi.org/10.1161/01.HYP.31.1.384
  16. Wakade AR. Studies on secretion of catecholamines evoked by acetylcholine or transmural stimulation of the rat adrenal gland. J Physiol. 1981;313:463-480.
  17. Anton AH, Sayre DF. A study of the factors affecting the aluminum oxidetrihydroxy indole procedure for the analysis of catecholamines. J Pharmacol Exp Ther. 1962;138:360-375.
  18. Tallarida RJ, Murray RB. Manual of pharmacologic calculation with computer programs. 2nd ed. New York: Speringer-Verlag; 1987. 132 p.
  19. Hammer R, Giachetti A. Muscarinic receptor subtypes: $M_{1}$ and $M_{2}$ biochemical and functional characterization. Life Sci. 1982; 31:2992-2998.
  20. Garcia AG, Sala F, Reig JA, Viniegra S, Frias J, Fonteriz R, Gandia L. Dihydropyridine Bay-K-8644 activates chromaffin cell calcium channels. Nature. 1984;309:69-71. https://doi.org/10.1038/309069a0
  21. Lim DY, Kim CD, Ahn KW. Influence of TMB-8 on secretion of catecholamines from the perfused rat adrenal glands. Arch Pharm Res. 1992;15:115-125. https://doi.org/10.1007/BF02974085
  22. Goeger DE, Riley RT. Interaction of cyclopiazonic acid with rat skeletal muscle sarcoplasmic reticulum vesicles. Effect on $Ca^{2+}$ binding and $Ca^{2+}$ permeability. Biochem Pharmacol. 1989;38: 3995-4003. https://doi.org/10.1016/0006-2952(89)90679-5
  23. Seidler NW, Jona I, Vegh N, Martonosi A. Cyclopiazonic acid is a specific inhibitor of the $Ca^{2+}$-ATPase of sarcoplasimc reticulum. J Biol Chem. 1989;264:17816-17823.
  24. Catterall WA. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron. 2000;26:13-25. https://doi.org/10.1016/S0896-6273(00)81133-2
  25. Wada A, Takara H, Izumi F, Kobayashi H, Yanagihara N. Influx of $^{22}Na$ through acetylcholine receptor-associated Na channels: relationship between $^{22}Na$ influx, $^{45}Ca$ influx and secretion of catecholamines in cultured bovine adrenal medulla cells. Neuroscience. 1985;15:283-292. https://doi.org/10.1016/0306-4522(85)90135-6
  26. Hano T, Mizukoshi M, Baba A, Nakamura N, Nishio I. Angiotensin II subtype 1 receptor modulates epinephrine release from isolated rat adrenal gland. Blood Press. 1994;5:S105-108.
  27. Livett BG, Marley PD. Non cholinergic control of adrenal catecholamine secretion. J Anat. 1993;183:277-289.
  28. Plunkett LM, Correa FM, Saavedra JM. Quantitative autoradiographic determination of angiotensin-converting enzyme binding in rat pituitary and adrenal glands with 124I-351A, a specific inhibitor. Regul Pept. 1985;28:263-272.
  29. Phillips MI, Speakman EA, Kimura B. Levels of angiotensin and molecular biology of the tissue rennin angiotensin systems. Regul Pept. 1993;43:1-20. https://doi.org/10.1016/0167-0115(93)90403-U
  30. Israel A, Strömberg C, Tsutsumi K, Garrido MR, Torres M, Saavedra JM. Angiotensin II receptor subtypes and phosphoinositide hydrolysis in rat adrenal medulla. Brain Res Bull. 1995;38:441-446. https://doi.org/10.1016/0361-9230(95)02011-F
  31. Wong PC, Hart SD, Zaspel AM, Chiu AT, Ardecky RJ, Smith RD, Timmermans PB. Functional studies of nonpeptide angiotensin II receptor subtype-specific ligands: DuP 753 (AII-1) and PD123177 (AII-2). J Pharmacol Exp Ther. 1990;255:584-592.
  32. Armando I, Carranza A, Nishimura Y, Hoe KL, Barontini M, Terron JA, Falcon-Neri A, Ito T, Jourio AV, Saavedra JM. Peripheral administration of and angiotensin II $AT_{1}$ receptor antagonist decreases the hypothalamic-pituitary-adrenal response to isolation stress. Endocrinology. 2001;142:3880-3889. https://doi.org/10.1210/en.142.9.3880
  33. Yang G, Xi Z, Wan Y, Wang H, Bi G. Changes in circulating and tissue angiotensin II during acute and chronic stress. Biol Signals. 1993;2:166-172. https://doi.org/10.1159/000109488
  34. McGehee DS, Role LW. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol. 1995;57:521-546. https://doi.org/10.1146/annurev.ph.57.030195.002513
  35. Cheek TR, O'Sullivan AJ, Moreton RB, Berridge MJ, Burgoyne RD. Spatial localization of the stimulus-induced rise in cyrosolic $Ca^{2+}$ in bovine adrenal chromaffin cells: Distinct nicotinic and muscarinic patterns. FEBS Lett. 1989;247:429-434. https://doi.org/10.1016/0014-5793(89)81385-7
  36. Ghosh A, Greenberg ME. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science. 1995;268:239-247. https://doi.org/10.1126/science.7716515
  37. Holz RW, Senter RA, Frye RA. Relationship between $Ca^{2+}$ uptake and catecholamine secretion in primary dissociated cultures of adrenal modulla. J Neurochem. 1982;39:635-640. https://doi.org/10.1111/j.1471-4159.1982.tb07940.x
  38. Suzuki M, Muraki K, Imaizumi Y, Watanabe M. Cyclopiazonic acid, an inhibitor of the sarcoplasmic reticulum $Ca^{2+}$-pump, reduces $Ca^{2+}$-dependent $K^{+}$ currents in guinea-pig smooth muscle cells. Br J Pharmacol. 1992;107:134-140. https://doi.org/10.1111/j.1476-5381.1992.tb14475.x
  39. Challiss RA, Jones JA, Owen PJ, Boarder MR. Changes in inositol 1,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate mass accumulations in cultured adrenal chromaffin cells in response to bradykinin and histamine. J Neurochem. 1991;56: 1083-1086. https://doi.org/10.1111/j.1471-4159.1991.tb02033.x
  40. Dendorfer A, Raasch W, Tempel K, Dominiak P. Interactions between the renin-angiotensin system (RAS) and the sympathetic system. Basic Res Cardiol. 1998;93:S24-29. https://doi.org/10.1007/s003950050202
  41. Stoehr SJ, Smolen JE, Holz RW, Agranoff BW. Inositol trisphosphate mobilizes intracellular calcium in permeabilized adrenal chromaffin cells. J Neurochem. 1986;46:637-640. https://doi.org/10.1111/j.1471-4159.1986.tb13014.x
  42. Dunn LA, Holz RW. Catecholamine secretion from digitonintreated adrenal medullary chromaffin cells. J Biol Chem. 1983;258:4989-4993.
  43. Vijayapandi P, Nagappa AN. Biphasic effects of losartan potassium on immobility in mice. Yakugaku Zasshi. 2005;125: 653-657. https://doi.org/10.1248/yakushi.125.653
  44. Nahmod VE, Finkielman S, Benarroch EE, Pirola CJ. Angiotensin regulates release and synthesis of serotonin in brain. Science. 1978;202:1091-1093. https://doi.org/10.1126/science.152460
  45. Han HJ, Park SH, Koh HJ, Taub M. Mechanism of regulation of $Na^{+}$ transport by angiotensin II in primary renal cells. Kidney Int. 2000;57:2457-2467. https://doi.org/10.1046/j.1523-1755.2000.00104.x

Cited by

  1. Depression-like Effect of Telmisartan in Mice Forced Swim Test: Involvement of Brain Monoaminergic System vol.7, pp.2, 2010, https://doi.org/10.3923/jpt.2012.87.95