Resveratrol Inhibits Nicotinic Stimulation-Evoked Catecholamine Release from the Adrenal Medulla

  • Woo, Seong-Chang (Department of Anesthesiology and Pain Medicine, College of Medicine, Eulji University Hospital) ;
  • Na, Gwang-Moon (Department of Pharmacology, College of Medicine, Chosun University) ;
  • Lim, Dong-Yoon (Department of Pharmacology, College of Medicine, Chosun University)
  • Published : 2008.08.31

Abstract

Resveratrol has been known to possess various potent cardiovascular effects in animal, but there is little information on its functional effect on the secretion of catecholamines (CA) from the perfused model of the adrenal medulla. Therefore, the aim of the present study was to determine the effect of resveratrol on the CA secretion from the isolated perfused model of the normotensive rat adrenal gland, and to elucidate its mechanism of action. Resveratrol (10${\sim}100{\mu}$M) during perfusion into an adrenal vein for 90 min inhibited the CA secretory responses evoked by ACh (5.32 mM), high $K^+$ (a direct membrane-depolarizer, 56 mM), DMPP (a selective neuronal nicotinic $N_n$ receptor agonist, 100${\mu}$M) and McN-A-343 (a selective muscarinic $M_1$ receptor agonist, 100${\mu}$M) in both a time- and dose- dependent fashion. Also, in the presence of resveratrol (30${\mu}$M), the secretory responses of CA evoked by veratridine 8644 (an activator of voltage-dependent$Na^+$ channels, 100${\mu}$M), Bay-K-8644 (a L-type dihydropyridine $Ca^{2+}$ channel activator, 10${\mu}$M), and cyc1opiazonic acid (a cytoplasmic $Ca^{2+}$-ATPase inhibitor, 10${\mu}$M) were significantly reduced. In the simultaneous presence of resveratrol (30${\mu}$M) and L-NAME (an inhibitor of NO synthase, 30${\mu}$M), the CA secretory evoked by ACh, high $K^+$, DMPP, McN-A-343, Bay-K-8644 and cyc1opiazonic acid were recovered to a considerable extent of the corresponding control secretion compared with the inhibitory effect of resveratrol alone. Interestingly, the amount of nitric oxide (NO) released from the adrenal medulla was greatly increased in comparison to its basal release. Taken together, these experimental results demonstrate that resveratrol can inhibit the CA secretory responses evoked by stimulation of cholinergic nicotinic receptors, as well as by direct membrane-depolarization in the isolated perfused model of the rat adrenal gland. It seems that this inhibitory effect of resveratrol is exerted by inhibiting an influx of both ions through $Na^+$ and $Ca^{2+}$ channels into the adrenomedullary cells as well as by blocking the release of $Ca^{2+}$ from the cytoplasmic calcium store, which are mediated at least partly by the increased NO production due to the activation of NO synthase.

Keywords

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. Natural dietary polyphenolic compounds cause endothelium-dependent vasorelaxation in rat thoracic aorta. J Nutr 128: 2324-2333, 1998 https://doi.org/10.1093/jn/128.12.2324
  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. Bernatova I, Pechaoova O, Babal P, Kysela S, Stvrtina S, Andriantsitohaina R. Wine polyphenols improve cardiovascular remodelling and vascular function in NO-deficient hypertension. Am J Physiol Heart Circ Physiol 282: H942-H948, 2002 https://doi.org/10.1152/ajpheart.00724.2001
  6. 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-H469, 1993 https://doi.org/10.1152/ajpcell.1993.264.2.C464
  7. 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
  8. 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
  9. Celotti E, Ferrarini R, Zironi R, Conte LS. Resveratrol content of some wines obtained from dried Valpolicella grapes: recioto and Amarone. J Chromatogr A 730: 47-52, 1996 https://doi.org/10.1016/0021-9673(95)00962-0
  10. 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 56: 1083-1086, 1991 https://doi.org/10.1111/j.1471-4159.1991.tb02033.x
  11. 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
  12. 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
  13. Demrow HS, Slane PR. Administration of wine and grape juice inhibits in vivo platelet activity and thrombosis in stenosed canine coronary arteries. Circulation 91: 1182-1188, 1995 https://doi.org/10.1161/01.CIR.91.4.1182
  14. 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
  15. 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
  16. 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
  17. Fitzpatrick DF, Hirschfield SL, Coffey RG. Endothelium-dependent vasorelaxing activity of wine and other grape products. Am J Physiol 265: H77-H78, 1993
  18. Fitzpatrick DF, Hirschfield SL, Ricci T, Jantzen P, Coffey RG. Endothelium-dependent vasorelaxation caused by various plant extracts. J Cardiovasc Pharmacol 26: 90-95, 1995 https://doi.org/10.1097/00005344-199507000-00015
  19. 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-H1190, 1998
  20. Frankel EN, Waterhouse AL, Kinsella JE. Inhibition of human DL oxidation by resveratrol. Lancet 341: 1103-1104, 1993
  21. Freedman JE, Li L, Sauter R, Keaney JF JR. Alpha-Tocopherol and protein kinase C inhibition enhance platelet-derived nitric oxide release. FASEB J 14(15): 2377-2379, 2000. https://doi.org/10.1096/fj.00-0360fje
  22. 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
  23. Gareri P, Falconi U, De Fazio P, De Sarro G. Conventional and new antidepressant drugs in the elderly. Prog Neurobiol 61: 353- 396, 2000 https://doi.org/10.1016/S0301-0082(99)00050-7
  24. German JB, Walzem RL. The health benefits of wine. Annu Rev Nutr 20: 561-593, 2000 https://doi.org/10.1146/annurev.nutr.20.1.561
  25. 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
  26. Hammer R, Giachetti A. Muscarinic receptor subtypes: M1 and M2 biochemical and functional characterization. Life Sci 31: 2992-2998, 1982
  27. 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
  28. Jager U, Nguyen-Duong H. Relaxant effect of trans-resveratrol on isolated porcine coronary arteries. Arzneimitlelforschung 49: 207- 211, 1999
  29. 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 https://doi.org/10.1113/jphysiol.1980.sp013431
  30. 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
  31. Kilpatrick DL, Slepetis RJ, Kirshner N. Ion channels and membrane potential in stimulus-secretion coupling in adrenal med ulla cells. J Neurochem 36: 1245-1255, 1981 https://doi.org/10.1111/j.1471-4159.1981.tb01724.x
  32. 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
  33. Leikert JF, Rathel TR, Wohlfart PV, 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
  34. 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
  35. 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
  36. 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
  37. Martin S, Andriambeloson E, Takeda K, Andriantsitohaina R. Red wine polyphenols increase calcium in bovine aortic endothelial cells: a basis to elucidate signalling pathways leading to nitric oxide production. Br J Pharmacol 135: 1579-1587, 2002 https://doi.org/10.1038/sj.bjp.0704603
  38. 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
  39. Naderali EK, Doyle PJ, Wlliams G. Resveratrol induces vasorelaxation of mesenteric and uterine ateries from female guinea-pigs. Clin Sci 98: 537-543, 2000 https://doi.org/10.1042/CS19990303
  40. Naderali EK, Smith SL, Doyle PJ, Wlliams G. The mechanism of resveratrol-induced vasorelaxation differs in the mesenteric resistance arteries of lean and obese rats. Clin Sci 100: 55-60, 2001 https://doi.org/10.1042/CS20000123
  41. 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, eds, Catecholamines: Basic and Clinical frontiers. Pergamon Press, Oxford, p 70-72, 1979
  42. Orsini F, Pelizzoni F, Verotta L, Aburjai T. Isolation, synthesis, and antiplatelet aggregation activity of resveratrol 3-O-b-D- Glucopyranoside and related compounds. J Nat Prod 60: 1082-1087, 1997 https://doi.org/10.1021/np970069t
  43. 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
  44. 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
  45. Pace-Asciak CR, Hahn SE, Diamandis EP, Soleas G, Goldberg DM. The red wine phenolics trans-resveratrol and quercetin block human platelet aggregation and eicosanoid synthesis: implication for protection against coronary heart disease. Clin Chim Acta 235: 207-219, 1995 https://doi.org/10.1016/0009-8981(95)06045-1
  46. 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
  47. 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
  48. Renaud S, de Lorgeril M. Wine alcohol, platelet and the French paradox for coronary heart disease. Lancet 339: 1523-1526, 1992 https://doi.org/10.1016/0140-6736(92)91277-F
  49. 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
  50. Rotondo S, Rajtar G, Manarinis S. Effect of trans-resveratrol, a natural polyphenolic compound, on human polymorphonuclear leukocyte function. Br J Pharmacol 123: 1691-1699, 1998 https://doi.org/10.1038/sj.bjp.0701784
  51. Sato M, Suzuki Y, Okuda T, Yokotsuka K. Content of resveratrol, piceid and their isomers in commercially available wines made from grapes cultivated in Japan. Biosci Biotechnol Biochem 61: 1800-1805, 1997 https://doi.org/10.1271/bbb.61.1800
  52. 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
  53. Schwarz PM, Rodriguez-Pascual F, Koesling D, Torres M, Forstermann 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
  54. 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
  55. Slotkin TA, Whitmore WL, Dew KL, Kilts CD. Uptake of serotonin into rat platelets and synaptosomes: comparative structure- activity relationships, energetics and evaluation of the effects of acute and chronic nortriptyline administration. Brain Res Bull 17: 67-73, 1986 https://doi.org/10.1016/0361-9230(86)90162-0
  56. 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
  57. Tallarida RJ, Murray RB. Manual of pharmacologic calculation with computer programs. 2nd ed. Speringer-Verlag, New York, p 132, 1987
  58. To SE, Zepf RA, Woods AG. The symptoms, neurobiology, and current pharmacological treatment of depression. J Neurosci Nurs 37: 102-107, 2005
  59. 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
  60. 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
  61. Uenobe F, Nakamura S, Miyazawa M. Antimutagenic effects of resveratrol against Trp-P-1. Mutat Res 373: 197-200, 1997 https://doi.org/10.1016/S0027-5107(96)00191-1
  62. 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
  63. Wada A, Takara H, Izumi F, Kobayashi H, Yanagihara N. Influx of $^22Na$ through acetylcholine receptor-associated Na channels: relationship between $^22Na$ influx, $^45Ca$ influx and secretion of catecholamines in cultured bovine adrenal medullary cells. Neuroscience 15: 283-292, 1985 https://doi.org/10.1016/0306-4522(85)90135-6
  64. Wakade AR. Studies on secretion of catecholamines evoked by acetylcholine or transmural stimulation of the rat adrenal gland. J Physiol 313: 463-480, 1981 https://doi.org/10.1113/jphysiol.1981.sp013676
  65. 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
  66. Wallerath T, Deckert G, Ternes T, Anderson H, Li H, Witte K, Forstermann 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
  67. Yanagihara N, Isosaki M, Ohuchi T, Oka M. Muscarinic receptor- mediated increase in cyclic GMP level in isolated bovine adrenal medullary cells. FEBS Lett 105: 296-298, 1979 https://doi.org/10.1016/0014-5793(79)80633-X
  68. Yanez M, Fraiz N, Cano E, Orallo F. Inhibitory effects of cis- and trans-resveratrol on noradrenaline and 5-hydroxytryptamine uptake and on monoamine oxidase activity. Biochem Biophys Res Commun 344: 688-695, 2006 https://doi.org/10.1016/j.bbrc.2006.03.190
  69. Zenebe W, Pechaoova O, Andriantsitohaina R. Red wine polyphenols induce vasorelaxation by increased nitric oxide bioactivity. Physiol Res 52: 425-432, 2003
  70. Zhou CX, Kong LD, Ye WC, Cheng CH, Tan RX. Inhibition of xanthine and monoamine oxidases by stilbenoids from Veratrum taliense. Planta Med 67: 158-161, 2001 https://doi.org/10.1055/s-2001-11500