Natural Product Sciences

The Korean Society of Pharmacognosy (한국생약학회)
권호 표지

Inhibitory Effects of Self-Fermented Pine Needle Extract on Catecholamine Release in the Rat Adrenal Medulla

  • Choi, Mee-Sung (Department of Physical Education (Sport Physiology), Graduate School, Chosun University) ;
  • Seo, Young-Hwan (Department of Physical Education (Sport Physiology), Graduate School, Chosun University) ;
  • Cheong, Hyeon-Sook (Department of Life Science, College of natural Science, Chosun University) ;
  • Lim, Dong-Yoon (Department of Pharmacology, Chosun University)
  • Received : 2013.01.09
  • Accepted : 2013.03.14
  • Published : 2013.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

The aim of the present study was to investigate the effects of several fractions obtained from methylene chloride ($CH_2Cl_2$) extract of self-fermented pine needle (SFPNE) on the acetylcholine (ACh)-evoked CA release from the isolated perfused model of the rat adrenal medulla and to establish the mechanism of the most active fraction (Fr.)-induced inhibitory action on the CA release. We obtained 6 fractions from $CH_2Cl_2$ extract of self-fermented pine needle. For the ACh (5.32 mM)-evoked CA release, the following rank order of inhibitory potency was obtained: Fr.4-5 > Fr.8-11 ${\gg}$ Fr.3 > Fr.6 = Fr.7 > Fr.1-2. Fr. 4 - 5 (60 ${\mu}g/mL$) perfused into an adrenal vein for 90 min produced relatively time-dependent inhibition of the CA secretory responses to ACh (5.32 mM), DMPP (100 ${\mu}M$), McN-A-343 (100 ${\mu}M$) and high $K^+$ (56 mM). Fr. 4 - 5 itself did not affect basal CA secretion. Also, in the presence of Fr. 4 - 5 (60 ${\mu}g/mL$), the CA secretory responses to angiotensin II (AngII, 0.1 ${\mu}M$), veratridine (50 ${\mu}M$), Bay-K-8644 (10 ${\mu}M$), and cyclopiazonic acid (10 ${\mu}M$) were significantly reduced, respectively. In the simultaneous presence of Fr. 4 - 5 (60 ${\mu}g/mL$) and L-NAME (30 ${\mu}M$), the inhibitory responses of Fr. 4 - 5 on the CA secretion evoked by ACh, DMPP, high $K^+$, AngII, Bay-K-8644 and veratridine were considerably recovered to the extent of the corresponding control secretion compared with that of Fr. 4 - 5-treatment alone. The level of NO released from adrenal medulla after the treatment of Fr. 4 - 5 (60 ${\mu}g/mL$) was greatly elevated compared with the basal level. Taken together, these results demonstrate that Fr. 4 - 5 inhibits the CA secretion from the isolated perfused rat adrenal medulla evoked by stimulation of cholinergic receptors as well as by direct membrane-depolarization. It seems that this inhibitory effect of Fr. 4 - 5 is mediated by blocking the influx of $Ca^{2+}$ and $Na^+$ into the adrenomedullary chromaffin cells as well as by inhibition of $Ca^{2+}$ release from the cytoplasmic calcium store, which is evoked at least partly through the increased NO production due to the activation of NO synthase. Based on these results, it is also thought that Fr. 4 - 5 isolated from $CH_2Cl_2$ extract of pine needle may contain beneficial antihypertensive components to prevent or treat hypertension.

Keywords

References

  1. Andriambeloson, E., Kleschyov, A.L., Muller, B., Beretz, A., Stoclet, J.C., and Andriantsitohaina, R., Nitric oxide production and endotheliumdependent 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, J.C., and 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, J.C., and 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, A.H. and Sayre, D.F., 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, M.J., Tobin, J.R., Bredt, D.S., Ferris, C.D., Snyder, S.H., and Traystman, R.J., Nitric oxide as a regulator of adrenal blood flow. Am. J. Physiol. (Heart Circ Physiol) 264, H464-H469 (1993). https://doi.org/10.1152/ajpheart.1993.264.2.H464
  6. Breslow, M.J., Tobin, J.R., Bredt, D.S., Ferris, C.D., Snyder, S.H., and Traystman, R.J., 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, R.D., Mechanism of secretion from adrenal chromaffin cells. Biochem. Biophys. Acta. 779, 201-216 (1984).
  8. Challis, R.A.J., Jones, J.A., Owen, P.J., and Boarder, M.R., 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
  9. Cheek, T.R., O'Sullivan, A.J., Moreton, R.B., Berridge, M.J., and Burgoyne, R.D., 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
  10. Cheong, H., Paudyal, D.P., Jun, J.Y., Yeum, C.H., Yoon, P.J., Park, C.G., Kim, M.Y., So, I., Kim, K.W., and Choi, S., Effects of pine needle extract on pacemaker currents in interstitial cells of Cajal from the murine small intestine. Mol. Cells 20, 235-240 (2005).
  11. Cheong, H.S. and Lim, D.Y., Pine needle extracts inhibit contractile responses of the isolated rat aortic strips. Natural Product Sciences 16, 123-132 (2010).
  12. Chung, Y.J., Bae, M.W., Choung, M.I., Lee, J.S., and Chung, K.S., Cytotoxic effect of the distilled pine-needle extracts on several cancer cell lines in vitro. J. Korean Soc. Food Sci. Nutr. 31, 691695 (2002).
  13. Diebolt, M., Bucher, B., and 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
  14. Douglas, W.W., Stimulus-secretion coupling: The concept and clues from chromaffin and other cells. Br. J. Pharmacol. 34, 451-474 (1968). https://doi.org/10.1111/j.1476-5381.1968.tb08474.x
  15. Fisher, S.K., Holz, R.W., and Agranoff, B.W., 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, D.F., Bing, B., and Rohdewald, P., Endothelium-dependent vascular effects of $Pycnogenol^{(R)}$. Journal of Cardiovascular Pharmacology 32, 509-515 (1998). https://doi.org/10.1097/00005344-199810000-00001
  17. Fitzpatrick, D.F., Fleming, R.C., Bing, B., Maggi, D.A., and 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
  18. Fitzpatrick, D.F., Hirschfield, S.L., and Coffey, R.G., Endotheliumdependent vasorelaxing activity of wine and other grape products. Am. J. Physiol. 265, H77-78 (1993).
  19. Fitzpatrick, D.F., Hirschfield, S.L., Ricci, T., Jantzen, P., and Coffey, R. G., Endothelium-dependent vasorelaxation caused by various plant extracts. J. Cardiovasc. Pharmacol. 26, 90-95 (1995). https://doi.org/10.1097/00005344-199507000-00015
  20. Freedman, J.E., Li, L., and Sauter, R. et al., alpha-Tocopherol and protein kinase C inhibition enhance platelet-derived nitric oxide release. FASEB J. 14, 2377-23779 (2000). https://doi.org/10.1096/fj.00-0360fje
  21. Freedman, N.J. and Lefkowitz R.J., Anti-beta(1)-adrenergic receptor antibodies and heart failure: causation, not just correlation. J. Clin. Invest. 113, 1379-1382 (2004). https://doi.org/10.1172/JCI21748
  22. Garcia, A.G., Sala, F., Reig, J.A., Viniegra, S., Frias, J., Fonteriz, R., and Gandia, L., Dihydropyridine Bay-K-8644 activates chromaffin cell calcium channels. Nature 309, 69-71 (1984). https://doi.org/10.1038/309069a0
  23. Goeger, D.E. and Riley, R.T., Interaction of cyclopiazonic acid with rat skeletal muscle sarcoplasmic reticulum vesicles. Effect on $ Ca^{2+}$ binding and Ca2+ permeability. Biochem. Pharmacol. 38, 3995-4003 (1989). https://doi.org/10.1016/0006-2952(89)90679-5
  24. Hammer, R. and Giachetti, A., Muscarinic receptor subtypes: M1 and M2 biochemical and functional characterization. Life Sci. 31, 2992-2998 (1982).
  25. Hano, T., Mizukoshi, M., Baba, A., Nakamura, N., and Nishio, I., Angiotensin II subtype 1 receptor modulates epinephrine release from isolated rat adrenal gland. Blood Press. 5, S105-108 (1994).
  26. Huang, Y., Chan, N.W.K., Lau, C.W., Yao, X.Q., Chan, F.L., and Chen, Z.Y., Involvement of endothelium/nilvicoxide in vasorelaxation induced by purified green tea (-) epicatechin. Biochim. Biophys. Acta. 1427, 322-328 (1999). https://doi.org/10.1016/S0304-4165(99)00034-3
  27. Hsu, T.Y., Sheu, S.C., Liaw, E.T., Wang, T.C., and Lin, C.C., Antioxidant activity and effect of Pinus morrisonicola Hay. on the survival of leukemia cell line U937. Phytomedicine 12, 663-669 (2005). https://doi.org/10.1016/j.phymed.2004.03.013
  28. 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
  29. Jung, M.J., Chung, H.Y., Choi, J.H., and Choi, J.S., Antioxidant principles from the needles of red pine, Pinus densiflora. Phytother. Res. 17, 1064-1068 (2003). https://doi.org/10.1002/ptr.1302
  30. Kaye, D.M., Lefkowits, J., Jennings, G.L., Bergin, P., Broughton, A., and Esler, M.D., Adverse consequences of high sympathetic nervous activity in the failing human heart. J. Am. Coll. Cardiol. 26, 1257- 1263 (1995). https://doi.org/10.1016/0735-1097(95)00332-0
  31. Kee, Y.W. and Lim, D.Y., Influence of polyphenolic compounds isolated from Rubus coreanum on catecholamine release in the rat adrenal medulla. Arch. Pharm. Res. 30, 1240-1251 (2007). https://doi.org/10.1007/BF02980265
  32. Kidokoro, Y. and Ritchie, A.K., 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
  33. Kilpatrick, D.L., Slepetis, R.J., Corcoran, J.J., and 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
  34. Kilpatrick, D.L., Slepetis, R.J., and 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
  35. Knight, D.E. and Kesteven, N.T., 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
  36. Lee, E., Effects of powdered pine neele (Pinus densiflora seib et Zucc.) on serum and liver lipid composition and antioxidative capacity in rats fed high oxidized fat. J. Korean Soc. Food Sci. Nutr. 32, 926930 (2003).
  37. Lee, K.H., Kim, A.J., and Choi, E.M., Antioxidant and antiinflammatory activity of pine pollen extract in vitro. Phytother. Res. 23, 41-48 (2009). https://doi.org/10.1002/ptr.2525
  38. Lim, D.Y. and Hwang, D.H., Studies on secretion of catecholamines evoked by DMPP and McN-A-343 in the rat adrenal gland. Korean J. Pharmacol. 27, 53-67 (1991).
  39. Lim, D.Y., Kim, C.D., and Ahn, K.W., 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
  40. Lymperopoulos, A., Rengo, G., Funakoshi, H., Eckhart, A.D., and Koch, W.J., Adrenal GRK2 upregulation mediates sympathetic overdrive in heart failure. Nat. Med. 13, 315-323 (2007). https://doi.org/10.1038/nm1553
  41. Marley, P.D., McLeod, J., Anderson, C., and Thomson, K.A., 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
  42. Mizutani, K., Ikeda, K., Kawai, Y., and Yamori, Y., Extract of wine phenolics improves aortic biomechanical properties in stroke-prone spontaneously hypertensive rats (SHRSP). J. Nutr. Sci. Vitaminol. (Tokyo) 45, 95-106 (1999). https://doi.org/10.3177/jnsv.45.95
  43. Oka, M., Isosaki, M., and Yanagihara, N., Isolated bovine adrenal medullary cells: studies on regulation of catecholamine synthesis and release, in Usdin, E., Kopin, I.J., and Brachas, J. (eds.), Catecholamines: Basic and Clinical frontiers, Pergamon Press, Oxford, pp. 70-72, 1979.
  44. Oset-Gasque, M.J., Parramon, M., Hortelano, S., Bosca, L., and Gonzalez, M.P., Nitric oxide implication in the control of neurosecretion by chromaffin cells. J. Neurochem. 63, 1693-1700 (1994).
  45. O'Sullivan, A.J. and Burgoyne, R.D., Cyclic GMP regulates nicotineinduced 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
  46. Palacios, M., Knowles, R.G., Palmer, R.M., and 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. Park, C.S., Kwon, C.J., Choi, M.A., Park, G.S., and Choi, K.H., Antioxidative and nitrite scavenging activities of mugwort and pine needle extracts. Korean J. Food Pres. 9, 248-252 (2002).
  48. Pecha ova, O., Bernatova, I., Babál, P., Martinez, M.C., Kysela, S., Stvrtina, S., and Andriantsitohaina, R., Red wine polyphenols prevent cardiovascular alterations in L-NAME-induced hypertension. J. Hypertens. 22, 1551-1559 (2004a). https://doi.org/10.1097/01.hjh.0000133734.32125.c7
  49. Rodriguez-Pascual, F., Miras-Portugal, M.T., and 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. Schramm, M., Thomas, G., Towart, R., and 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
  51. Schwarz, P.M., Rodriguez-Pascual, F., Koesling, D., Torres, M., and 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).
  52. Seidler, N.W., Jona, I., Vegh, N., and Martonosi, A., Cyclopiazonic acid is a specific inhibitor of the $ Ca^{2+}$-ATPase of sarcoplasmic reticulum. J. Biol. Chem. 264, 17816-17823 (1989).
  53. Seidler, N.W., Jona, I., Vegh, N., and Martonosi, A., Cyclopiazonic acid is a specific inhibitor of the $ Ca^{2+}$-ATPase of sarcoplasmic reticulum. J. Biol. Chem. 264, 17816-17823 (1989).
  54. Suzuki, M., Muraki, K., Imaizumi, Y., and 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
  55. Tallarida, R.J. and Murray, R.B., Manual of pharmacologic calculation with computer programs. 2nd ed, Speringer-Verlag, New York, 1987
  56. Torres, M., Ceballos, G., and 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).
  57. Uchiyama, Y., Morita, K., Kitayama, S., Suemitsu, T., Minami, N., Miyasako, T., and 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
  58. Uyama, Y., Imaizumi, Y., and 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
  59. Wada, Y., Satoh, K., and Taira, N., Cardiovascular profile of Bay-K-8644, a presumed calcium channel activator in the dog. Naunyn- Schmiedebergs Arch. Pharmacol. 328, 382-387 (1985a).
  60. Wada, A., Takara, H., Izumi, F., Kobayashi, H., and 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 (1985b). https://doi.org/10.1016/0306-4522(85)90135-6
  61. Wakade, A.R., 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
  62. Wakade, A.R. and Wakade, T.D., 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
  63. Wang, D., Chen, J., Xu, Z., Qiao, X., and Huang, L., Disappearance of polycyclic aromatic hydrocarbons sorbed on surfaces of pine [Pinua thunbergii] needles under irradiation of sunlight: Volatilization and photolysis. Atmos. Environ.39, 4583-4591 (2005). https://doi.org/10.1016/j.atmosenv.2005.04.008
  64. Westfall, T.C. and Westfall, D.P., Adrenergic agonists and antagonists, in Brunton, L.L., Lazo, J.S., and Parker, K.L. (eds.), Goodman & Gilman the pharmacological basis of therapeutics, 11th ed, McGraw-Hill, New York, pp. 237-295, 2005.
  65. Yanagihara, N., Isosaki, M., Ohuchi, T., and 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
  66. Yu, B.S., Ko, W.S., and Lim, D.Y., Inhibitory mechanism of polyphenol compounds isolated from red wine on catecholamine release in the perfused rat adrenal medulla. Biomolecules & Therapeutics 16, 147- 160 (2008). https://doi.org/10.4062/biomolther.2008.16.2.147
  67. Zenebe, W., Pecháòova, O., and Andriantsitohaina, R., Red wine polyphenols induce vasorelaxation by increased nitric oxide bioactivity. Physiol. Res. 52, 425-432 (2003).