Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Influence of Glibenclamide on Catecholamine Secretion in the Isolated Rat Adrenal Gland

  • No, Hae-Jeong (Department of Pharmacology, College of Medicine, Chosun University, Department of Family Medicine, Eulji University Hospital) ;
  • Woo, Seong-Chang (Department of Anesthesiology, Eulji University Hospital) ;
  • Lim, Dong-Yoon (Department of Pharmacology, College of Medicine, Chosun University)
  • Published : 2007.06.30
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Abstract

The aim of the present study was to investigate the effect of glibenclamide, a hypoglycemic sulfonylurea, which selectively blocks ATP-sensitive K$^+$ channels, on secretion of catecholamines (CA) evoked by cholinergic stimulation and membrane depolarization from the isolated perfused rat adrenal glands. The perfusion of glibenclamide (1.0 mM) into an adrenal vein for 90 min produced time-dependently enhanced the CA secretory responses evoked by ACh (5.32 mM), high K$^+$ (a direct membrane depolarizer, 56 mM), DMPP (a selective neuronal nicotinic receptor agonist, 100 ${\mu}$M for 2 min), McN-A-343 (a selective muscarinic M1 receptor agonist, 100 ${\mu}$M for 2 min), Bay-K-8644 (an activator of L-type dihydropyridine Ca$^{2+}$ channels, 10 ${\mu}$M for 4 min) and cyclopiazonic acid (an activator of cytoplasmic Ca$^{2+}$-ATPase, 10 ${\mu}$M for 4 min). In adrenal glands simultaneously preloaded with glibenclamide (1.0 mM) and nicorandil (a selective opener of ATP-sensitive K$^+$ channels, 1.0 mM), the CA secretory responses evoked by ACh, high potassium, DMPP, McN-A-343, Bay-K-8644 and cyclopiazonic acid were recovered to the considerable extent of the control release in comparison with that of glibenclamide-treatment only. Taken together, the present study demonstrates that glibenclamide enhances the adrenal CA secretion in response to stimulation of cholinergic (both nicotinic and muscarinic) receptors as well as by membrane depolarization from the isolated perfused rat adrenal glands. It seems that this facilitatory effect of glibenclamide may be mediated by enhancement of both Ca$^{2+}$ influx and the Ca$^{2+}$ release from intracellular store through the blockade of K$_{ATP}$ channels in the rat adrenomedullary chromaffin cells. These results suggest that glibenclamide-sensitive K$_{ATP}$ channels may play a regulatory role in the rat adrenomedullary CA secretion.

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References

  1. Akaike, A., Mine, Y., Sasa, M. and Takaori, S. (1990). Voltage and current clamp studies of muscarinic and nicotinic excitation of the rat adrenal chromaffin cells. J. Pharmacol. Expt. Ther. 255, 333-339
  2. Anton, A. H. and Sayre, D. F. (1962). A study of the factors affecting the aluminum oxidetrihydroxy indole procedure for the analysis of catecholamines. J. Pharmacol. Exp. Ther. 138, 360-375
  3. Aguilar-Bryan, L., Clement, J. P., Gonzalez, G., Kunjilwar, K., Babenko, A. and Bryan, J. (1998). Toward understanding the assembly and structure of KATP channels. Physiol. Rev. 78, 227-245 https://doi.org/10.1152/physrev.1998.78.1.227
  4. Asano, M., Masuzawa-Ito, K. and Matsuda, T. (1994). Vasodilating actions of cromakalim in resting and contracting states of carotid arteries from spontaneously hypertensive rats. European J. Pharmacol. 263, 121-131 https://doi.org/10.1016/0014-2999(94)90532-0
  5. Ashcroft, F. M. (1988). Adenosine 5'-triphosphate-sensitive potassium channels. Annu. Rev. Neurosci. 11, 763-770
  6. Ashford, M. L. J., Sturgess, N. C., Trout, N. J., Gardner, N. J. and Hales, C. N. (1988). Adenosine 5'-triphosphate-sensitive ion channels in neonatal rat cultured central neurones. Pflugers Arch. 412, 297-304 https://doi.org/10.1007/BF00582512
  7. Benndorf, K., Thierfelder, S., Doepner, B., Gebhardt, C. and Hirche, H. (1997). Role of cardiac K-ATP channels during anoxia and ischemia. News Physiol. Sci. 12, 78-83
  8. Burgoyne, R. D. (1984). Mechanism of secretion from adrenal chromaffin cells. Biochem. Biophys. Acta. 779, 201-216 https://doi.org/10.1016/0304-4157(84)90009-1
  9. Cena, V., Nicolas, G. P., Sanchez-Garcia, P., Kirpekar, S. M. and Garcia, A. G. (1983). Pharmacological dissection of receptorassociated and voltage-sensitive ionic channels involved in catecholamine release. Neuroscience 10, 1455-1462 https://doi.org/10.1016/0306-4522(83)90126-4
  10. Challiss, R. A. J., Jones, J. A., Owen, P. J. and Boarder, M. R. (1991). 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 https://doi.org/10.1111/j.1471-4159.1991.tb02033.x
  11. Cheek, T. R., O'Sullivan, A. J., Moreton, R. B., Berridge, M. J. and Burgoyne, R. D. (1989). 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 https://doi.org/10.1016/0014-5793(89)81385-7
  12. Cook, N. S. (1988). The pharmacology of potassium channel and their therapeutic potential. Trends Pharmacol. Sci. 9, 21-28 https://doi.org/10.1016/0165-6147(88)90238-6
  13. Corcoran, J. J. and Kirshner, N. (1983). Inhibition of calcium uptake, sodium uptake, and catecholamine secretion by methoxyverapamil (D600) in primary cultures of adrenal medulla cells. J. Neurochem. 40, 1106-1109 https://doi.org/10.1111/j.1471-4159.1983.tb08099.x
  14. Edwards, G., Duty, S., Trezise, D. J. and Weston, A. H. (1992). Effects of potassium-channel modulators on the cardiovascular system. In Potassium channel modulators: Phamacological, molecular and clinical aspects (A. H. Weston, T. C. Hamilton, Ed.), pp. 369-463. Blackwell Science, Oxford
  15. Endoh, M. and Taira, N. (1983). Relationship between relaxation and cyclic GMP formation caused by nicorandil in canine mesenteric arteries. Naunyn-Schmiedeberg's Arch. Pharmacol. 322, 319 https://doi.org/10.1007/BF00508349
  16. Finta, E. P., Harms, L., Sevick, J., Fischer, H. D. and Illes, P. (1993). Effects of potassium channel openers and their antagonists on rat locus coerulus neurones. Br. J. Pharmacol. 109, 308-315 https://doi.org/10.1111/j.1476-5381.1993.tb13571.x
  17. Furukawa, K., Itoh, I., Kajiwara, M., Kitamura, K., Suzuki, H., Ito, Y. and Kuriyama, H. (1981). Effects of 2-nicotinamidoethyl nitrate on smooth muscle cells and on adrenergic transmission in guinea-pig and porcine mesenteric arteries. J. Pharmacol. Exp. Ther. 218, 260
  18. Garcia, A. G., Sala, F., Reig, J. A., Viniegra, S., Frias, J., Fonteriz, R. and Gandia, L. (1984). Dihydropyridine Bay-K-8644 activates chromaffin cell calcium channels. Nature 309, 69-71 https://doi.org/10.1038/309069a0
  19. Goeger, D. E. and Riley, R. T. (1989). 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 https://doi.org/10.1016/0006-2952(89)90679-5
  20. Hamilton, T. and Weston, A. (1989). Cromakalim, nicorandil and pinacidil: novel drugs which open potassium channels in smooth muscle. Gen. Pharmacol. 20, 1-9 https://doi.org/10.1016/0306-3623(89)90052-9
  21. Hammer, R. and Giachetti, A. (1982). Muscarinic receptor subtypes: $M_1$ and $M_2$ biochemical and functional characterization. Life Sci. 31, 2992-2998
  22. Heldman, E., Levine, M., Rabeh, L. and Pollard, H. B. (1989). Barium ions enter chromaffin cells via voltage-dependent calcium channels and induce secretion by a mechanism independent of calcium. J. Biol. Chem. 264, 7914-7920
  23. Holzmann, S. (1983). cGMP as a possible mediator of coronary arterial relaxation by nicorandil (SG-75). J. Cardiovasc. Pharmacol. 5, 364-370 https://doi.org/10.1097/00005344-198305000-00004
  24. Holzmann, S., Kukovetz, W. R., Braida, C. and Poch, G. (1992). Pharmacological interaction experiments differentiate between glibenclamide-sensitive potassium channels and cyclic GMP as components of vasodilation by nicorandil. Eur. J. Pharmacol. 215, 1-7 https://doi.org/10.1016/0014-2999(92)90600-9
  25. Ilno, M. (1989). Calcium-induced calcium release mechanism in guinea pig taenia caeci. J. Gen. Physiol. 94, 363-383 https://doi.org/10.1085/jgp.94.2.363
  26. Kukovetz, W. R., Holzmann, S., Braida C. and Poch, G. (1991). Dual mechanism of the relaxing effect of nicorandil by stimulation of cGMP formation and by hyperpolarisation. J. Cardiovasc. Pharmacol. 17, 627-633 https://doi.org/10.1097/00005344-199104000-00016
  27. Ladona, M. G., Aunis, D., Gandia, A. G. and Garcia, A. G. (1987). Dihydropyridine modulation of the chromaffin cell secretory response. J. Neurochem. 48, 483-490 https://doi.org/10.1111/j.1471-4159.1987.tb04118.x
  28. Lim, D. Y. and Hwang, D. H. (1991). Studies on secretion of catecholamines evoked by DMPP and McN-A-343 in the rat adrenal gland. Korean J. Pharmacol. 27, 53-67
  29. Lim, D. Y., Kim, C. D. and Ahn, K. W. (1992). Influence of TMB-8 on secretion of catecholamines from the perfused rat adrenal glands. Arch. Pharm. Res. 15, 115-125 https://doi.org/10.1007/BF02974085
  30. Lim, D. Y., Park, G. H. and Park, S. H. (2000). Inhibitory mechanism of pinacidil on catecholamine secretion from the rat perfused adrenal gland evoked by cholinergic stimulation and membrane depoialrization. J. Auton. Pharmacol. 20, 123-132 https://doi.org/10.1046/j.1365-2680.2000.00171.x
  31. Masuda, Y., Yoshizumi, M., Ishimura, Y., Katoh, I. and Oka, M. (1994). Effects of the potassium channel openers cromakalim and pinacidil on catecholamine secretion and calcium mobilization in cultured bovine adrenal chromaffin cells. Biochem. Pharmacol. 47, 1751-1758 https://doi.org/10.1016/0006-2952(94)90302-6
  32. Meisheri, K. D., Cipkus-Dubray, L. A., Hosner J. M. and Khan, S. (1991). Nicorandil-induced vasorelaxation: Functional evidence for $K^+$ channel-dependent and cyclic GMP-dependent components in a single vascular preparation. J. Cardiovasc. Pharmacol. 17, 903 https://doi.org/10.1097/00005344-199106000-00007
  33. Murphy, K. P. and Greenfield, S. A. (1992). Neuronal selectivity of ATP-sensitive potassium channels in guinea-pig substantia nigra revealed by responses to anoxia. J. Physiol. (Lond) 453, 167-183 https://doi.org/10.1113/jphysiol.1992.sp019222
  34. Noma, A. (1983). ATP-regulated single K channels in cardiac muscle. Nature 305, 147-148 https://doi.org/10.1038/305147a0
  35. Oka, M., Isosaki, M. and Yanagihara, N. (1979). Isolated bovine adrenal medullary cells: studies on regulation of catecholamine synthesis and release. In Catecholamines: Basic and Clinical frontiers (E. Usdin, I. J. Kopin, J. Brachas, Ed.), pp. 70-72. Pergamon Press, Oxford
  36. Perez-Vizcaino, F., Casis, O., Rodriguez, R., Comez, L. A., Garcia Rafanell, J. and Tamargo, J. (1993). Effect of the novel potassium channel opener, UR-8225, on contractile responses in rat isolated smooth muscle. Br. J. Pharmacol. 110, 1165-1171 https://doi.org/10.1111/j.1476-5381.1993.tb13936.x
  37. Petersen, O. H. and Maruyama, Y. (1984). Calcium-activated potassium channels and their role in secretion. Nature 307, 693-696 https://doi.org/10.1038/307693a0
  38. Pierrefiche, O., Bischoff, A. M. and Richter, D. W. (1996). ATP-sensitive $K^{+}$ channels are functional in expiratory neurones of normoxic cats. J. Physiol. (Lond) 494, 399-409
  39. Quast, U. and Cook, N. S. (1989). Moving together: K+ channel openers and ATP-sensitive K+ channels. Trends Pharmacol. Sci. 10, 431-435 https://doi.org/10.1016/S0165-6147(89)80003-3
  40. Schmid-Antomarchi, H., Amoroso, S., Fosset, M. and Lazdunski, M. (1990). $K^{+}$ channel openers activate brain sulphonylureasensitive $K^{+}$ channels and block neurosecretion. Proc. Natl. Acad. Sci. U.S.A. 87, 3489-3492 https://doi.org/10.1073/pnas.87.9.3489
  41. Seidler, N. W., Jona, I., Vegh, N. and Martonosi, A. (1989). Cyclopiazonic acid is a specific inhibitor of the $Ca^{2+}$-ATPase of sarcoplasimc reticulum. J. Biol. Chem. 264, 17816-17823
  42. Standen, N. B., Quatly, J. M., Davies, N. W., Brayden, J. E., Huang, Y. and Nelson, M. T. (1989). Hyperpolarizing vasodilators activate ATP-sensitive K+ channels in arterial smooth muscle. Science 245, 177-1780 https://doi.org/10.1126/science.2501869
  43. Suzuki, M., Muraki, K., Imaizumi, Y. and Watanabe, M. (1992). 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 https://doi.org/10.1111/j.1476-5381.1992.tb14475.x
  44. Tallarida, R. J. and Murray, R. B. (1987). Manual of pharmacologic calculation with computer programs. 2nd Ed. Speringer-Verlag, New York, pp. 132
  45. Terbush, D. R. and Holz, R. W. (1992). Barium and calcium stimulate secretion from digitonin-permeabilized bovine adrenal chromaffin cells by similar pathways. J. Neurochem. 58, 680-687 https://doi.org/10.1111/j.1471-4159.1992.tb09771.x
  46. Uceda, G., Artalejo, A. R., Lopez, M. G., Abad, F., Neher, E. and Garcia, A. G. (1992). $Ca^{2+}$-activated $K^{+}$ channels modulate muscarinic secretion in cat chromaffin cells. J. Physiol. 454, 213-230 https://doi.org/10.1113/jphysiol.1992.sp019261
  47. Uyama, Y., Imaizumi, Y. and Watanabe, M. (1992). Effects of cyclopiazonic acid, a novel $Ca^{2+}$-ATPase inhibitor on contractile responses in skinned ileal smooth muscle. Br. J. Pharmacol. 106, 208-214 https://doi.org/10.1111/j.1476-5381.1992.tb14316.x
  48. Wada, A., Kobayashi, H., Arita, M., Yanagihara, N. and Izumi, F. (1987). Potassium channels in cultured bovine adrenal medullary cells: effects of high K, veratridine and carbachol on 86rubidium efflux. Neuroscience 22, 1085-1092 https://doi.org/10.1016/0306-4522(87)92983-6
  49. Wakade, A. R. (1981). Studies on secretion of catecholamines evoked by acetylcholine or transmural stimulation of the rat adrenal gland. J. Physiol. 313, 463-480 https://doi.org/10.1113/jphysiol.1981.sp013676
  50. Watson, S. and Abbott, A. (1991). Receptor Nomenclature Supplement. Trends Pharmacol. Sci. (Suppl), 31-33
  51. Weston, A. H., Longmore, J., Newgreen, D. T., Edwards, G., Bray, K. M. and Duty, S. (1990). The potassium channel openers: a new class of vasorelaxants. Blood Vessels 27, 306-313
  52. Weston, A. H., Southerton, J. S., Bray, K. M., Newgreen, D. T. and Taylor, S. G. (1988). The mode of action of pinacidil and its analogs P1060 and P1368: Results of studies in rat blood vessels. J. Cardiovasc. Pharmacol. 12 (Suppl), S10-S16
  53. Wu, C. W., Leung, C. K. and Yung, W. H. (1996). Sulphonylureas reverse hypoxia induced $K^{+}$ conductance increase in substantia nigra pars reticulata neurones. Neuroreport 7, 2513-2517 https://doi.org/10.1097/00001756-199611040-00022

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