Influence of Naloxone on Catecholamine Release Evoked by Nicotinic Receptor Stimulation in the Isolated Rat Adrenal Gland

  • Kim Ok-Min (Department of Pharmacology, College of Medicine, Chosun University) ;
  • Lim Geon-Han (Department of Neurology, College of Medicine, Chosun University) ;
  • Lim Dong-Yoon (Department of Pharmacology, College of Medicine, Chosun University)
  • Published : 2005.06.01

Abstract

The present study was designed to investigate the effect of naloxone, a well known opioid antagonist, on the secretion of catecholamines (CA) evoked by cholinergic stimulation and membrane-depolarization in the isolated perfused rat adrenal glands, and to establish its mechanism of action. Naloxone ($10^{-6}\~10^{-5}$ M), perfused into an adrenal vein for 60 min, produced dose- and time-dependent inhibition of CA secretory responses evoked by ACh ($5.32\times10^{-3}$ M), high K+ ($5.6\times10^{-2}$ M), DMPP ($10^{-4}$ M) and McN-A-343 ($10^{-4}$ M). Naloxone itself also failed to affect the basal CA output. In adrenal glands loaded with naloxone ($3\times10^{-6}$ M), the CA secretory responses evoked by Bay-K-8644, an activator of L-type $Ca^{2+}$ channels, and cyclopiazonic acid, an inhibitor of cytoplasmic $Ca^{2+}$-ATPase, were also inhibited. In the presence of met-enkephalin ($5\times10^{-6}$ M), a well known opioid agonist, the CA secretory responses evoked by ACh, high $K^+$, DMPP, McN-A-343, Bay-K-8644 and cyclopiazonic acid were also significantly inhibited. Taken together, these results suggest that naloxone greatly inhibits the CA secretion evoked by stimulation of cholinergic (both nicotinic and muscarinic) receptors as well as that by membrane depolarization. It seems that these inhibitory effects of naloxone does not involve opioid receptors, but might be mediated by blocking both the calcium influx into the rat adrenal medullary chromaffin cells and the uptake of $Ca^{2+}$ into the cytoplasmic calcium store, which are at least partly relevant to the direct interaction with the nicotinic receptor itself.

Keywords

References

  1. Albillos, A., Gandía, L., Michelena, P., Gilabert, J. A., del Valle, M., Carbone, E., and García, A.G., The mechanism of calcium channel facilitation in bovine chromaffin cells. J. Physiol., 494, 687-695 (1996) https://doi.org/10.1113/jphysiol.1996.sp021524
  2. Anton, A. H. and Sayre, D. F., A study of the factors affecting the aluminum oxidetrihydroxy indole procedure for the analysis of catecholamines. J. Pharmacol. Exp. Ther., 138, 360-375 (1962)
  3. Artalejo, C. R., Adams, M. E., and Fox, A. P., Three types of $Ca^{2+}$ channel trigger secretion with different efficacies in chromaffin cells. Nature, 367, 72-76 (1994) https://doi.org/10.1038/367072a0
  4. Barron, B. A. and Hexum, T. D., Modulation of bovine adrenal gland secretion by etorphine and diprenorphine. Life Sci., 38, 935-940 (1986) https://doi.org/10.1016/0024-3205(86)90262-6
  5. Boarder, M. R., Marriott, D., and Adams, M., Stimulus secretion coupling in cultured chromaffin cells, dependency on external sodium and on dihydropyridine-sensitive calcium channels. Biochem. Pharmacol., 36, 163-167 (1987) https://doi.org/10.1016/0006-2952(87)90394-7
  6. Bunn, S. J. and Dunkley, P. R., Opioid inhibition of nicotineinduced $45Ca^{2+}$-uptake into cultured bovine adrenal medullary cells. Biochem. Pharmacol., 41, 715-722 (1991) https://doi.org/10.1016/0006-2952(91)90071-C
  7. Cena, V., Nicholas, G., Sanchez-Garcia, P., Kjrpekar, S. M., and Garcia, A. G., Pharmacological dissection of receptorassociated and voltage-sensitive ionic channeIs involved in catecholamine release. Neuroscience, 10, 1455-1462 (1983) https://doi.org/10.1016/0306-4522(83)90126-4
  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 stimulusinduced 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. Conway, E. L., Brown, M. J., and Dollery, C. T., Studies on the pharmacology of central opioid-induced increases in plasma catecholamines in conscious rats. Neuropharmacol., 23(11), 1291-1296 (1984) https://doi.org/10.1016/0028-3908(84)90047-9
  11. Dean, D. M., Lemaire, S., and Livett, B. G., Evidence that inhibition of nicotine-mediated catecholamine secretion from adrenal chromaffin cells by enkephalin, beta-endorphin, dynorphin (1-13), and opiates is not mediated via specific opiate receptors. J. Neurochem., 38, 606-614 (1982) https://doi.org/10.1111/j.1471-4159.1982.tb08674.x
  12. Dendorfer, A. and Dominiak, P., Characterisation of bradykinin receptors mediating catecholamine release in PC12 cells. Naunyn-Schmiedeberg's Arch. Pharmacol., 351, 274-281 (1995)
  13. Dermitzaki, E., Gravanis, A., Venihaki, M., Stournaras, C., and Margioris, A. N., Opioids suppress basal and nicotineinduced catecholamine secretion via a stabilizing effect on actin filaments. Endocrinology, 142(5), 2022-2031 (2001) https://doi.org/10.1210/en.142.5.2022
  14. DougIas, W. W., Kanno, T., and Sampson, S. R., Effects of acetylcholine and other medullary secretagogues and antagonists on the membrane potential of adrenal chromaffin cells : An analysis employing techniques of tissue culture. J. Physiol., 188, 107-120 (1967) https://doi.org/10.1113/jphysiol.1967.sp008127
  15. Douglas, W. W., Kanno, T., and Sampson, S. R., Influence of the ionic environment on the membrane potential of adrenal cells and on the depolarizing effect of acetylcholine. J. Physiol., 191, 107-121 (1967) https://doi.org/10.1113/jphysiol.1967.sp008239
  16. Epple, A., Nibbio, B., Spector, S., and Brinn, J. E., Endogenous codeine: autocrine regulator of catecholamine release from chromaffin cells. Life Sci., 54(11), 695-702 (1994) https://doi.org/10.1016/0024-3205(94)90157-0
  17. 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
  18. Goeger, D. E. and Riley, R. T., 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
  19. Hammer, R. and Giachetti, A., Muscarinic receptor subtypes: $M_1$ and $M_2$ biochemical and functional characterization. Life Sci., 31, 2992-2998 (1982) https://doi.org/10.1016/0024-3205(82)90066-2
  20. 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
  21. Jarry, H., Dietrich, M., Barthel, A., Giesler, A., and Wuttke, W., In vivo demonstration of a paracrine, inhibitory action of Metenkephalin on adrenomedullary catecholamine release in the rat. Endocrinology, 125, 624-629 (1989) https://doi.org/10.1210/endo-125-2-624
  22. Kimura, T., Katoh, M., and Satoh, S., Inhibition by opioid agonists and enhancement by antagonists of the release of catecholamines from the dog adrenal gland in response to splanchnic nerve stimulation: Evidence for the functional role of opioid receptors. J. Pharmacol. Exp. Ther., 244(3), 1098-1102 (1988)
  23. Kitamura, G., Ohta, T., Kai, T., Kon, Y., and Ito, S., Inhibitory effects of opioids on voltage-dependent $Ca^{2+}$ channels and catecholamine secretion in cultured porcine adrenal chromaffin cells. Brain Res., 942(1-2), 11-22 (2002) https://doi.org/10.1016/S0006-8993(02)02648-3
  24. Kleppisch, T., Ahnert-Hilger, G., Gollasch, M., Spicher, K., Hescheler, J., Schultz, G., and Rosenthal, W., Inhibition of voltage-dependent $Ca^{2+}$ channels via $\alpha_2$-adrenergic and opioid receptors in cultured bovine adrenal chromaffin cells. Pflugers Arch., 421, 131–137 (1992) https://doi.org/10.1007/BF00374819
  25. Kumakura, K., Karoum, F., Guidotti, A., and Costa, E., Modulation of nicotinic receptors by opiate receptor agonists in cultured adrenal chromaffin cells. Nature, 283, 489-492 (1980) https://doi.org/10.1038/283489a0
  26. Lemaire, S., Day, R., Dumont, M., Chouinard, L., and Calvert, R., Dynorphin and enkephalins in adrenal paraneurons. Opiates in adrenal medulla. Can. J. Physiol. Pharmacol., 62, 484-492 (1984) https://doi.org/10.1139/y84-078
  27. 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(2), 115-125 (1992) https://doi.org/10.1007/BF02974085
  28. Lim, D. Y., Lee, J. J., and Choi, C. H., Effect of opioid on nicotinic receptor-mediated catecholamine secretion in the rat adrenal gland. Korean J. Pharmacol., 28(2), 181-190 (1992)
  29. Livett, B. G. and Boksa, P., Receptors and receptor modulation in cultured chromaffin cells. Can. J. Physiol. Pharmacol., 62, 467-476 (1984) https://doi.org/10.1139/y84-076
  30. Livett, B. G., Dean, D. M., Whelan, L. G., Udenfriend, S., and Rossier, J., Co-release of enkephalin and catecholamines from cultured adrenal chromaffin cells. Nature, 289, 317-319 (1981) https://doi.org/10.1038/289317a0
  31. Lopez, M. G., Fonteriz, R., Gandia, L., De la Fuente, M., Villarroya, M., Garcia-Sancho, J., and Garcia, A. G., The nicotinic ACh receptor of the bovine chromaffin cell, a new target for dihydropyridines. Eur. J. Pharmacol. Molec. Biol., 247, 199-207 (1993) https://doi.org/10.1016/0922-4106(93)90078-N
  32. Mannelli, M., Maggi, M., DeFeo, M. L., Boscaro, M., Opocher, G., Mantero, F., Baldi, E., and Giusti, G., Opioid modulation of normal and pathological human chromaffin tissue. J. Clin. Endocrinol. Metab., 62, 577-582 (1986) https://doi.org/10.1210/jcem-62-3-577
  33. Marley, P. D. and Livett, B. G., Effects of opioid compounds on desensitization of the nicotinic response of isolated bovine adrenal chromaffin cells. Biochem. Pharmacol., 36(8), 2937-2944 (1987) https://doi.org/10.1016/0006-2952(87)90206-1
  34. Marley, P. D., Mitchelhill, K. I., and Livett, B.G., Effects of opioid peptides containing the sequence of $Met^5$-enkephalin or $Leu^5$-enkephalin on nicotine-induced secretion from bovine adrenal chromaffin cells. J. Neurochem., 46, 1-11 (1986) https://doi.org/10.1111/j.1471-4159.1986.tb12918.x
  35. O'Farrell, N., Zigas, J., and Marley, P. D., Effect of N- and L-type calcium channel antagonists and (${\pm}$)-Bay-K-8644 on nerveinduced catecholamine secretion from bovine perfused adrenal glands. Br. J. Pharmacol., 121, 381-388 (1997) https://doi.org/10.1038/sj.bjp.0701131
  36. Owen, P. J., Marriott, D. B., and Boarder, M. R., Evidence for a dihydropyridine-sensitive and conotoxin-insensitive release of noradrenaline and uptake of calcium in adrenal chromaffin cells. Br. J. Pharmacol., 97, 133-138 (1989) https://doi.org/10.1111/j.1476-5381.1989.tb11933.x
  37. Ritchie, A. K., Catecholamine secretion in a rat pheochromocytoma cell line: Two pathways for calcium entry. J. Physiol., 286, 541-561 (1979) https://doi.org/10.1113/jphysiol.1979.sp012636
  38. Saiani, L. and Guidotti, A., Opiate receptor-mediated inhibition of catecholamine release in primary cultures of bovine adrenal chromaffin cells. J. Neurochem., 39, 1669–1676 (1982) https://doi.org/10.1111/j.1471-4159.1982.tb08001.x
  39. Seidler, N. W., Jona, I., Vegh, N., and Martonosi, A., Cyclopiazonic acid is a specific inhibitor of the $Ca^{2+}$-ATPase of sarcoplasimc reticulum. J. Biol. Chem., 264(30), 17816-17823 (1989)
  40. 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 guineapig smooth muscle cells. Br. J. Pharmacol., 107, 134-140 (1992) https://doi.org/10.1111/j.1476-5381.1992.tb14475.x
  41. Tallarida, R. J. and Murray, R. B., Manual of pharmacologic calculation with computer programs. 2nd Ed. New York, Speringer-Verlag, pp.132, (1987)
  42. Tome, A. R., Izaguirre, V., Rosario, L. M., Cena, V., and Gonzalez- Garcia, C., Naloxone inhibits nicotine-induced receptor current and catecholamine secretion in bovine chromaffin cells. Brain Res., 903(1-2), 62-65 (2001) https://doi.org/10.1016/S0006-8993(01)02388-5
  43. Twitchell, W. A. and Rane, S. G., Opioid peptide modulation of $Ca^{2+}$-dependent $K^+$ and voltage-activated $Ca^{2+}$ currents in bovine adrenal chromaffin cells. Neuron, 10, 701-709 (1993) https://doi.org/10.1016/0896-6273(93)90171-M
  44. 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
  45. Wakade, A. R., Studies on secretion of catecholamines evoked by ACh or transmural stimulation of the rat adrenal gland. J. Physiol., 313, 463-480 (1981) https://doi.org/10.1113/jphysiol.1981.sp013676
  46. Winkler, H. and Westhead, E., The molecular organization of adrenal chromaffin granules. Neuroscience, 5, 1803-1823 (1980) https://doi.org/10.1016/0306-4522(80)90031-7