The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
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Polyphenols of Rubus coreanum Inhibit Catecholamine Secretion from the Perfused Adrenal Medulla of SHRs

  • Yu, Byung-Sik (Department of Anesthesiology and Pain Medicine, DNA Repair Research Center, Chosun University) ;
  • Na, Duck-Mi (Department of Pharmacology, DNA Repair Research Center, Chosun University) ;
  • Kang, Mi-Young (Department of Bio-materials, DNA Repair Research Center, Chosun University) ;
  • Lim, Dong-Yoon (Department of Pharmacology, DNA Repair Research Center, Chosun University)
  • Published : 2009.12.31
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Abstract

The present study was attempted to investigate whether polyphenolic compounds isolated from wine, which is brewed from Rubus coreanum Miquel (PCRC), may affect the release of catecholamines (CA) from the isolated perfused adrenal medulla of the spontaneously hypertensive rats (SHRs), and to establish its mechanism of action. PCRC $(20\sim180\;{\mu}g/ml)$ perfused into an adrenal vein for 90 min relatively dose-dependently inhibited the CA secretory responses to ACh (5.32 mM), high $K^+$ (56 mM), DMPP $(100\;{\mu}M)$ and McN-A-343 $(100\;{\mu}M)$. PCRC itself did not affect basal CA secretion (data not shown). Also, in the presence of PCRC $(60\;{\mu}g/ml)$, the CA secretory responses to veratridine (a selective $Na^+$ channel activator $(10\;{\mu}M)$, Bay-K-8644 (a L-type dihydropyridine $Ca^{2+}$ channel activator, $10\;{\mu}M$), and cyclopiazonic acid (a cytoplasmic $Ca^{2+}$-ATPase inhibitor, $10\;{\mu}M$) were significantly reduced, respectively. In the simultaneous presence of PCRC $(60\;{\mu}g/ml)$ and L-NAME (an inhibitor of NO synthase, $30\;{\mu}M$), the inhibitory responses of PCRC on the CA secretion evoked by ACh, high $K^+$, DMPP, and Bay-K-8644 were considerably recovered to the extent of the corresponding control secretion compared with that of PCRC-treatment alone. The level of NO released from adrenal medulla after the treatment of PCRC $(60\;{\mu}g/ml)$ was greatly elevated compared with the corresponding basal level. Taken together, these results demonstrate that PCRC inhibits the CA secretion from the isolated perfused adrenal medulla of the SHRs evoked by stimulation of cholinergic receptors as well as by direct membrane-depolarization. It seems that this inhibitory effect of PCRC is mediated by blocking the influx of calcium and sodium into the adrenal medullary chromaffin cells of the SHRs as well as by inhibition of $Ca^{2+}$ release from the cytoplasmic calcium store at least partly through the increased NO production due to the activation of NO synthase.

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References

  1. Andriambeloson E, Kleschyov AL, Muller B, Beretz A, Stoclet JC, Andriantsitohaina R. Nitric oxide production and endothelium- dependent vasorelaxation induced by wine polyphenols in rat aorta. Br J Pharmacol 120: 1053-1058, 1997 https://doi.org/10.1038/sj.bjp.0701011
  2. Andriambeloson E, Magnier C, Haan-Archipoff G, Lobstein A, Anton R, Beretz A, Stoclet JC, Andriantsitohaina R. Lobstein Natural dietary polyphenolic compounds cause endothelium- dependent vasorelaxation in rat thoracic aorta. J Nutr 128: 2324-2333, 1998
  3. Andriambeloson E, Stoclet JC, Andriantsitohaina R. Mechanism of endothelial nitric oxide-dependent vasorelaxation induced by wine polyphenols in rat thoracic aorta. J Cardiovasc Pharmacol 33: 248-254, 1999 https://doi.org/10.1097/00005344-199902000-00011
  4. Anton AH, Sayre DF. A study of the factors affecting the aluminum oxide trihydroxy indole procedure for the analysis of catecholamines. J Pharmacol Exp Ther 138: 360-375, 1962
  5. Breslow MJ, Tobin JR, Bredt DS, Ferris CD, Snyder SH, Traystman RJ. Nitric oxide as a regulator of adrenal blood flow. Am J Physiol 264: H464-469, 1993
  6. Breslow MJ, Tobin JR, Bredt DS, Ferris CD, Snyder SH, Traystman RJ. Role of nitric oxide in adrenal medullary vasodilation during catecholamine secretion. Eur J Pharmacol 210: 105-106, 1992 https://doi.org/10.1016/0014-2999(92)90659-R
  7. Burgoyne RD. Mechanism of secretion from adrenal chromaffin cells. Biochem Biophys Acta 779: 201-216, 1984 https://doi.org/10.1016/0304-4157(84)90009-1
  8. Caderni G, De Filippo C, Luceri C, Salvadori M, Giannini A, Biggeri A, Remy S, Cheynier V, Dolara P. Effects of black tea, green tea and wine extracts on intestinal carcinogenesis induced by azoxymethane in F344 rats. Carcinogenesis 21: 1965-1969, 2000 https://doi.org/10.1093/carcin/21.11.1965
  9. Challiss RAJ, 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 56: 1083-1086, 1991 https://doi.org/10.1111/j.1471-4159.1991.tb02033.x
  10. Cheek TR, O'Sullivan AJ, Moreton RB, Berridge MJ, Burgoyne RD. Spatial localization of the stimulus-induced rise in cytosolic $Ca^{2+}$ in bovine adrenal chromaffin cells: Distinct nicotinic and muscarinic patterns. FEBS Lett 247: 429-434, 1989 https://doi.org/10.1016/0014-5793(89)81385-7
  11. Chen CK, Pace-Asciak CR. Vasorelaxing activity of resveratrol and quercetin in isolated rat aorta. Gen Pharmacol 27: 363-366, 1996 https://doi.org/10.1016/0306-3623(95)02001-2
  12. Diebolt M, Bucher B, Andriantsitohaina R. Wine polyphenols decrease blood pressure, improve NO vasodilatation, and induce gene expression. Hypertension 38: 159-165, 2001 https://doi.org/10.1161/01.HYP.38.2.159
  13. Fisher SK, Holz RW, Agranoff BW. Muscarinic receptors in chromaffin cell culture mediate enhanced phospholipid labeling but not catecholamine secretion. J Neurochem 37: 491-487, 1981 https://doi.org/10.1111/j.1471-4159.1981.tb00482.x
  14. Fitzpatrick DF, Fleming RC, Bing B, Maggi DA, O'Malley R. Isolation and characterization of endothelium-dependent vasorelaxing compounds from grape seeds. J Agric Food Chem 48: 6384-6390, 2000 https://doi.org/10.1021/jf0009347
  15. Flesch M, Schwarz A, Bolun M. Effects of red and white wine on endothelium-dependent vasorelaxation of rat aorta and human coronary arteries. Am J Physiol 275: H1183-1190, 1998
  16. Garcia AG, Sala F, Reig JA, Viniegra S, Frias J, Fonteriz R, Gandia L. Dihydropyridine Bay-K-8644 activates chromaffin cell calcium channels. Nature 309: 69-71, 1984 https://doi.org/10.1038/309069a0
  17. 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 38: 3995-4003, 1989 https://doi.org/10.1016/0006-2952(89)90679-5
  18. Hammer R, Giachetti A. Muscarinic receptor subtypes: M1 and M2 biochemical and functional characterization. Life Sci 31: 2992-2998, 1982
  19. Ilno M. Calcium-induced calcium release mechanism in guinea pig taenia caeci. J Gen Physiol 94: 363-383, 1989 https://doi.org/10.1085/jgp.94.2.363
  20. Kidokoro Y, Ritchie AK. Chromaffin cell action potentials and their possible role in adrenaline secretion from rat adrenal medulla. J Physiol 307: 199-216, 1980
  21. Kilpatrick DL, Slepetis RJ, Corcoran JJ, Kirshner N. Calcium uptake and catecholamine secretion by cultured bovine adrenal medulla cells. J Neurochem 38: 427-435, 1982 https://doi.org/10.1111/j.1471-4159.1982.tb08647.x
  22. Kilpatrick DL, Slepetis RJ, Kirshner N. Ion channels and membrane potential in stimulus-secretion coupling in adrenal medulla cells. J Neurochem 36: 1245-1255, 1981 https://doi.org/10.1111/j.1471-4159.1981.tb01724.x
  23. Knight DE, Kesteven NT. Evoked transient intracellular free $Ca^{2+}$ changes and secretion in isolated bovine adrenal medullary cells. Proc R Soc Lond Biol Sci 218: 177-199, 1983 https://doi.org/10.1098/rspb.1983.0033
  24. Leikert JF, Räthel TR, Wohlfart P, Cheynier V, Vollmar AM, Dirsch VM. Red wine polyphenols enhance endothelial nitric oxide release from endothelial cells. Circulation 106: 1614-1617, 2002 https://doi.org/10.1161/01.CIR.0000034445.31543.43
  25. Lim DY. Comparison of green tea extract and epigallocatechin gallate on secretion of catecholamines from the rabbit adrenal medulla. Arch Pharm Res 28: 914-922, 2005 https://doi.org/10.1007/BF02973877
  26. Lim DY, Hwang DH. Studies on secretion of catecholamines evoked by DMPP and McN-A-343 in the rat adrenal gland. Korean J Pharmacol 27: 53-67, 1991
  27. Lim DY, Kim CD, Ahn KW. Influence of TMB-8 on secretion of catecholamines from the perfused rat adrenal glands. Arch Pharm Res 15: 115-125, 1992 https://doi.org/10.1007/BF02974085
  28. Lim DY, Park HG, Lee BR. Green tea extract, not epigallocatechin gallate inhibits catecholamine release from the rat adrenal medulla. J Applied Pharmacol 11: 33-40, 2003
  29. Marley PD, McLeod J, Anderson C, Thomson KA. Nerves containing nitric oxide synthase and their possible function in the control of catecholamine secretion in the bovine adrenal medulla. J Auton Nerv Syst 54: 184-194, 1995 https://doi.org/10.1016/0165-1838(95)00013-N
  30. McVeigh GE, Hamilton P, Wilson M, Hanratty CG, Leahey WJ, Devine AB, Morgan DG, Dixon LJ, McGrath LT. Platelet nitric oxide and superoxide release during the development of nitrate tolerance: effect of supplemental ascorbate. Circulation 106: 208-213, 2002 https://doi.org/10.1161/01.CIR.0000021600.84149.78
  31. Mizutani K, Ikeda K, Kawai Y, Yamori Y. Extract of wine phenolics improves aortic biomechanical properties in stroke-prone spontaneously hypertensive rats (SHRSP). J Nutr Sci Vitaminol 45: 95-106, 1999 https://doi.org/10.3177/jnsv.45.95
  32. Nakazato Y, Ohga A, Oleshansky M, Tomita U, Yamada Y. Voltage-independent catecholamine release mediated by the activation of muscarinic receptors in guinea-pig adrenal glands. Br J Pharmacol 93: 101-109, 1988 https://doi.org/10.1111/j.1476-5381.1988.tb11410.x
  33. Ndiaye M, Chataigneau T, Andriantsitohaina JCS, Schini-Kerth VB. Red wine polyphenols cause endothelium-dependent EDHF-mediated relaxations in porcine coronary arteries via a redox-sensitive mechanism. Biochem Biophys Res Commun 310: 371-377, 2003 https://doi.org/10.1016/j.bbrc.2003.09.028
  34. Oka M, Isosaki M, Yanagihara N. Isolated bovine adrenal medullary cells: studies on regulation of catecholamine synthesis and release. In: Usdin E, Kopin IJ, Brachas J ed, Catecholamines: Basic and Clinical frontiers. Pergamon Press, Oxford, p 70-72, 1979
  35. Oset-Gasque MJ, Parramon M, Hortelano S, Bosca L, Gonzalez MP. Nitric oxide implication in the control of neurosecretion by chromaffin cells. J Neurochem 63: 1693-1700, 1994 https://doi.org/10.1046/j.1471-4159.1994.63051693.x
  36. O'Sullivan AJ, Burgoyne RD. 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, 1990 https://doi.org/10.1111/j.1471-4159.1990.tb01238.x
  37. Palacios M, Knowles RG, Palmer RM, Moncada S. Nitric oxide from L-arginine stimulates the soluble guanylate cyclase in adrenal glands. Biochem Biophys Res Commun 165: 802-809, 1989 https://doi.org/10.1016/S0006-291X(89)80037-3
  38. Palmer RM, Ashton DS, Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333: 664-666, 1988 https://doi.org/10.1038/333664a0
  39. Rakici O, Kiziltepe U, Coskun B, Aslamaci S, Akar F. Effects of resveratrol on vascular tone and endothelial function of human saphenous vein and internal mammary artery. Int J Cardiol 105: 209-115, 2005 https://doi.org/10.1016/j.ijcard.2005.01.013
  40. Rodriguez-Pascual F, Miras-Portugal MT, Torres M. Effect of cyclic GMP-increasing agents nitric oxide and C-type natriuretic peptide on bovine chromaffin cell function: inhibitory role mediated by cyclic GMP-dependent protein kinase. Mol Pharmacol 49: 1058-1070, 1996
  41. Sakuma I, Stuehr DJ, Gross SS, Nathan C, Levi R. Identification of arginine as a precursor of endothelium-derived relaxing factor. Proc Natl Acad Sci USA 85: 8664-8667, 1988 https://doi.org/10.1073/pnas.85.22.8664
  42. Schramm M, Thomas G, Towart R, Franckowiak G. Novel dihydropyridines with positive inotropic action through activation of $Ca^{2+}$ channels. Nature 303: 535-537, 1983 https://doi.org/10.1038/303535a0
  43. Schwarz PM, Rodriguez-Pascual F, Koesling D, Torres M, Förstermann U. Functional coupling of nitric oxide synthase and soluble guanylyl cyclase in controlling catecholamine secretion from bovine chromaffin cells. Neuroscience 82: 255-265, 1998 https://doi.org/10.1016/S0306-4522(97)00274-1
  44. Seidler NW, Jona I, Vegh N, Martonosi A. Cyclopiazonic acid is a specific inhibitor of the $Ca^{2+}$-ATPase of sarcoplasmic reticulum. J Biol Chem 264: 17816-17823, 1989
  45. Stein JH, Keevil JG, Wiebe DA, Aeschlimann S, Folts JD. Purple grape juice improves endothelial function and reduces the susceptibility of LDL cholesterol to oxidation in patients with coronary artery disease. Circulation 100: 1050-1055, 1999 https://doi.org/10.1161/01.CIR.100.10.1050
  46. 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 107: 134-140, 1992 https://doi.org/10.1111/j.1476-5381.1992.tb14475.x
  47. Tallarida RJ, Murray RB. Manual of pharmacologic calculation with computer programs. 2nd ed. Speringer-Verlag, New York, p 132, 1987
  48. Torres M, Ceballos G, Rubio R. Possible role of nitric oxide in catecholamine secretion by chromaffin cells in the presence and absence of cultured endothelial cells. J Neurochem 63: 988-996, 1994 https://doi.org/10.1046/j.1471-4159.1994.63030988.x
  49. Uchiyama Y, Morita K, Kitayama S, Suemitsu T, Minami N, Miyasako T, Dohi T. Possible involvement of nitric oxide in acetylcholine-induced increase of intracellular $Ca^{2+}$ concentration and catecholamine release in bovine adrenal chromaffin cells. Jpn J Pharmacol 65: 73-77, 1994 https://doi.org/10.1254/jjp.65.73
  50. Uyama Y, Imaizumi Y, Watanabe M. Effects of cyclopiazonic acid, a novel $Ca^{2+}$-ATPase inhibitor on contractile responses in skinned ileal smooth muscle. Br J Pharmacol 106: 208-214, 1992 https://doi.org/10.1111/j.1476-5381.1992.tb14316.x
  51. Viveros OH. Mechanism of secretion of catecholaminies from adrenal medulla. In handbook of physiology, Endocrinology. Vol VI, Sect 7, The adrenal gland. American physiological society, Washington DC, p 389-426, 1975
  52. Wada Y, Satoh K, Taira N. Cardiovascular profile of Bay-K-8644, a presumed calcium channel activator in the dog. Naunyn- Schmiedebergs Arch Pharmacol 328: 382-387, 1985a https://doi.org/10.1007/BF00692905
  53. Wada A, Takara H, Izumi F, Kobayashi H, Yanagihara N. Influx of $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 medullary cells. Neuroscience 15: 283-292, 1985b https://doi.org/10.1016/0306-4522(85)90135-6
  54. Wakade AR. Studies on secretion of catecholamines evoked by acetylcholine or transmural stimulation of the rat adrenal gland. J Physiol 313: 463-480, 1981
  55. Wakade AR, Wakade TD. Contribution of nicotinic and muscarinic receptors in the secretion of catecholamines evoked by endogenous and exogenous acetylcholine. Neuroscience 10: 973-978, 1983 https://doi.org/10.1016/0306-4522(83)90235-X
  56. Wallerath T, Deckert G, Ternes T, Anderson H, Li H, Witte K, Förstermann U. Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase. Circulation 106: 1652-1658, 2002 https://doi.org/10.1161/01.CIR.0000029925.18593.5C
  57. Zenebe W, Pecháòová O, Andriantsitohaina R. Red wine polyphenols induce vasorelaxation by increased nitric oxide bioactivity. Physiol Res 52: 425-432, 2003

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