Influence of Tacrine on Catecholamine Secretion in the Perfused Rat Adrenal Gland

  • Jang, Seok-Jeong (Departments of Neurosurgery, College of Medicine, Chosun University) ;
  • Yang, Won-Ho (Departments of Pharmacology, College of Medicine, Chosun University) ;
  • Lim, Dong-Yoon (Departments of Pharmacology, College of Medicine, Chosun University)
  • Published : 2002.08.21

Abstract

The present study was designed to clarify whether tacrine affects the release of catecholamines (CA) from the isolated perfused model of rat adrenal gland or not and to elucidate the mechanism of its action. Tacrine $(3{\times}10^{-5}{\sim}3{\times}10^{-4}\;M)$ perfused into an adrenal vein for 60 min inhibited CA secretory responses evoked by ACh $(5.32{\times}10^{-3}\;M),$ DMPP (a selective neuronal nicotinic agonist, $10^{-4}$ M for 2 min) and McN-A-343 (a selective muscarinic M1-agonist, $10^{-4}$ M for 2 min) in relatively dose- and time- dependent manners. However, tacrine failed to affect CA secretion by high $K^+\;(5.6{\times}10^{-2}\;M).$ Tacrine itself at concentrations used in the present experiments did not also affect spontaneous CA output. Furthermore, in the presence of tacrine $(10^{-4}\;M),$ CA secretory responses evoked by Bay-K-8644 (an activator of L-type $Ca^{2+}$ channels, $10^{-4}\;M),$ but not by cyclopiazonic acid (an inhibitor of cytoplasmic $Ca^{2+}-ATPase,\;10^{-4}\;M),$ was relatively time-dependently attenuated. Also, physostigmine $10^{-4}\;M),$ given into the adrenal gland for 60 min, depressed CA secretory responses evoked by ACh, McN-A-343 and DMPP while did not affect that evoked by high $K^+.$ Collectively, these results obtained from the present study demonstrate that tacrine greatly inhibits CA secretion from the perfused rat adrenal gland evoked by stimulation of cholinergic (both nicotinic and muscarinic) receptors, but does fail to affect that by direct membrane-depolarization. It is suggested that this inhibitory effect of tacrine may be exerted by blocking both the calcium influx into the rat adrenal medullary chromaffin cells without $Ca^{2+}$ release from the cytoplasmic calcium store, that is relevant to the cholinergic blockade. Also, the mode of action between tacrine and physostigmine in rat adrenomedullary CA secretion seems to be similar.

Keywords

References

  1. Akaike A, Mine Y, Sasa M, Takaori S. Voltage and current clamp studies of muscarinic and nicotinic excitation of the rat adrenal chromaffin cells. J Pharmacol Expt Ther 255: 333-339, 1990
  2. Allal C, Lazartigues E, Tran MA, Brefel-Courbon C, Gharib C, Montastruc JL, Rascol O. Central cardiovascular effects of tacrine in the conscious dog: a role for catecholamines and vasopressine release. Eur J Pharmacol 348: 191-198, 1998 https://doi.org/10.1016/S0014-2999(98)00143-5
  3. Anton AH, Sayre DF. A study of the factors affecting the aluminum oxidetrihydroxy indole procedure for the analysis of catecholamines. J Pharmacol Exp Ther 138: 360-375, 1962
  4. Braga MFM, Harvey AL, Rowan EG. Effects of tacrine, velnacrine (HP029), suronacrine (HP128) and 3,4-diaminopyridine on skeletal neuromuscular transmission in vitro. Br J Pharmacol 102: 909, 1991 https://doi.org/10.1111/j.1476-5381.1991.tb12275.x
  5. 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
  6. Cena V, Nicolas GP, Sanchez-Garcia P, Kirpekar SM, Garcia AG. Pharmacological dissection of receptor associated and voltagesensitive ionic channels involved in catecholamine release. Neuroscience 10: 1455-1462, 1983 https://doi.org/10.1016/0306-4522(83)90126-4
  7. Clarke PBS, Reuben M, El-Bizri H. Blockade of nicotinic responses by physostigmine, tacrine and other cholinesterase inhibitors in rat striatum. Brit J Pharmacol 111: 695-702, 1994 https://doi.org/10.1111/j.1476-5381.1994.tb14793.x
  8. Davis KL, Thal LJ, Gamzu ER, Davis CS, Woolson RF, Gracon SL, Drachman DA, Schneider LS, Whitehouse PJ, Hoover TM, et al. A double-blind, placebo-controlled multicenter study of tacrine fro Alzheimer's disease. The tacrine collaborative group. N Engl J Med 327(18): 1253-1259, 1992
  9. Douglas WW. Secretomotor control of adrenal medullary secretion: synaptin, membrane and ionic events in stimulus-secretion coupling, in Handbook of physiology Sect 7 Vol 6 (Blasko H, Sayers G, Smith AD eds. American Physiology Society, Washington D.C. pp 366-388, 1975
  10. Drukarch B, Kits KS, Van der Meer EG, Lodder JC, Stoof JC. 9-Amino-1,2,3,4-tetrahydroacridine (THA), an alleged drug for the treatment of Alzheimer's disease, inhibits acetylcholinesterase activity and slow outward K$^+$ current. Eur J Pharmacol 141: 153-157, 1987 https://doi.org/10.1016/0014-2999(87)90424-9
  11. Eagger SA, Levy R, Sahakian BJ. Tacrine in Alzheimer's disease. Lancet 337: 989-992, 1991 https://doi.org/10.1016/0140-6736(91)92656-M
  12. Elinder F, Mohammed AK, Winblad B, Århem P. Effects of THA on ionic currents in myelinated axons of Xenopus laevis. Eur J Pharmacol 164: 599-602, 1989 https://doi.org/10.1016/0014-2999(89)90272-0
  13. Fabianni ME, Kabo P, Story OF. Prejunctional actions of tacrine on autonomic neuroeffector transmission in rabbit isolated pulmonary artery and rat isolated atria. Clin Exp Pharmacol Physiol 19: 631-640, 1992 https://doi.org/10.1111/j.1440-1681.1992.tb00516.x
  14. Farlow M, Gracon SI, Hershey LA, Lewis KW, Sadowsky CH, Dolan-Ureno J. A controlled trial of tacrine in Alzheimer's disease. J Am Med Assoc 268: 2523-2529, 1992 https://doi.org/10.1001/jama.268.18.2523
  15. Flynn DD, Mash DC. Multiple in vitro interactions with and differential in vivo regulation of muscarinic receptor subtypes by tetrahydroaminoacridine. J Pharmacol Exp Ther 250: 573, 1989
  16. Freeman SE, Lau WM, Szilagyi M. Blockade of a cardiac K$^+$ channel by tacrine: interactions with muscarinic and adenosine receptors. Eur J Pharmacol 154: 59, 1988 https://doi.org/10.1016/0014-2999(88)90363-9
  17. Gandia L, Borges R, Albillos A, Garcia AG. Multiple calcium channel subtypes in isolates rat chromaffin cells. Pflugers Arch 430: 55-63, 1995 https://doi.org/10.1007/BF00373839
  18. 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
  19. 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
  20. Hammer R, Giachetti A. Muscarinic receptor subtypes: M1 and M2 biochemical and functional characterization. Life Sci 31: 2992- 2998, 1982
  21. Heilbronn E. Inhibition of cholinesterases by tetrahydroaminoacridine. Acta Chem Scand 15: 1386, 1961 https://doi.org/10.3891/acta.chem.scand.15-1386
  22. Kao LS, Schneider AS. Calcium mobilization and catecholamine secretion in adrenal chromaffin cells: a Quin 2 fluorescence study. J Biol Chem 261: 4881-4888, 1986
  23. Kelly KM, Gross RA, Macdonald RL. Tetrahydroaminoacridine (THA) reduces voltage-dependent calcium currents in rat sensory neurons. Neurosci Lett 132: 247-250, 1991 https://doi.org/10.1016/0304-3940(91)90312-H
  24. Kiefer-Day JS, Campbell HE, Towles J, El-Fakahany EE. Muscarinic subtype selectivity of tetrahydroaminoacridine: possible relationship to its capricious efficacy. Eur J Pharmacol 203: 421-423, 1991 https://doi.org/10.1016/0014-2999(91)90901-2
  25. Kiefer-Day JS, Abdallah ESAM, Forray C, Lee NH, Kim ON, El-Fakahany EE. Effects of tacrine on brain muscarinic- receptor- mediated second-messenger signals. Pharmacology 47: 98- 110, 1993
  26. Kitamura N, Ohta T, Ito S, Nakazato Y. Calcium channel subtypes in porcine adrenal chromaffin cells. Pflugers Arch 434: 179-187, 1997 https://doi.org/10.1007/s004240050381
  27. Knapp MJ, Knopman DS, Solomon PR, Pendlebury WW, Davis CS, Gracon SI. A 30-week randomized controlled trial of high-dose tacrine in patients with Alzheimer's disease. J Am Med Assoc 271: 985-991, 1994 https://doi.org/10.1001/jama.271.13.985
  28. Ladona MG, Aunis D, Gandia AG, Garcia AG. Dihydropyridine modulation of the chromaffin cell secretory response. J Neurochemstry 48: 483-490, 1987 https://doi.org/10.1111/j.1471-4159.1987.tb04118.x
  29. Lim DY, Kim CD, Ahn KW. 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
  30. 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(1): 53-67, 1991
  31. Lopez MG, Villarroya M, Lara B, Sierra RM, Albillos A, Garcia AG, Gandia L. Q-and L-type Ca2+ channels dominate the control of secretion in bovine chromaffin cells. FEBS Lett 349: 331-337, 1994 https://doi.org/10.1016/0014-5793(94)00696-2
  32. Mizobe F, Livett BG. Biphasic effect of eserine and other acetylcholinesterase inhibitors on the nicotinic response to acetylcholine in cultured adrenal chromaffin cells. J Neurochem 39: 379-385, 1982 https://doi.org/10.1111/j.1471-4159.1982.tb03959.x
  33. Nielsen JA, Mena EE, Williams IH, Nocerini MR, Liston D. Correlation of brain levels of 9-amino-1,2,3,4-tetrahydoracridine (THA) with neurochemical and behavioral changes. Eur J Pharmacol 173: 53, 1989 https://doi.org/10.1016/0014-2999(89)90008-3
  34. Nilsson L, Adem A, Hardy J, Winblad B, Nordberg A. Do tetrahydroaminoacridine (THA) and physostigmine restore acetylcholine release in Alzheimer brains via nicotinic receptors? J Neural Transm 70: 357-368, 1987 https://doi.org/10.1007/BF01253610
  35. Oka M, Isosaki M, Yanagihara N. Isolated bovine adrenal medullary cells: studies on regulation of catecholamine synthesis and release. In: Catecholamines: Basic and Clinical frontiers (Eds. Usdin E, Kopin IJ and Brachas J), Pergamon Press, Oxford, pp. 70-72, 1979
  36. Osterrieder W. 9-Amino-1,2,3,4-tetrahydoracridine (THA) is a potent blocker of cardiac potassium channels. Br J Pharmacol 92: 521, 1987 https://doi.org/10.1111/j.1476-5381.1987.tb11352.x
  37. Perry EK, Smith CJ, Court JA, Bonham JR, Rodway BM, Atack JR. Interaction of 9-amino-1,2,3,4-tetrahydoramino-acridine (THA) with human cortical nicotinic and muscarinic receptor binding in vitro. Neurosci Lett 91: 211, 1988 https://doi.org/10.1016/0304-3940(88)90770-7
  38. Rogawski MA. Tetrahydroaminoacridine blocks voltage-dependent ion channels in hippocampal neurons. Eur J Pharmacol 142: 169, 1987 https://doi.org/10.1016/0014-2999(87)90670-4
  39. Sahakian BJ, Coull JT. Tetrahydroaminoacridine (THA) in Alzheimer's disease: an assessment of attention and memory function using CANTAB. Acta Neurol Scand 149(Suppl): 29-35, 1993
  40. Sahakian BJ, Owen AM, Mornt NJ, Eagger SA, Boddington S, Crayton L, Crockford HA, Crooks M, Hill K, Levy R. Further analysis of the cognitive effects of tetrahydroaminoacridine (THA) in Alzheimer's disease: assessment of attention and memory function using CANTAB. Psychopharmacology 110: 395-401, 1993 https://doi.org/10.1007/BF02244644
  41. Savci V, Gurun MS, Gavun S, Ulus IS. Cardiovascular effects of centrally injected tetrahydroaminoacridine in conscious normotensive rats. Eur J Pharmacol 346: 35-41, 1998 https://doi.org/10.1016/S0014-2999(98)00019-3
  42. Schauf CL, Sattin A. Tetrahydroaminoacridine blocks potassium channels and inhibits sodium inactivation in Myxicola. J Pharmacol Exp Ther 243: 609, 1987
  43. Schramm M, Thomas G, Towart R, Franckowiak G. Novel dihydropyridines with positive isotropic action through activation of Ca$^2+$ channels. Nature 303: 535-537, 1982 https://doi.org/10.1038/303535a0
  44. Seidler NW, Jona I, Vegh N, Martonosi A. Cyclopiazonic acid is a specific inhibitor of the Ca$^2+$-ATPase of sarcoplasimc reticulum. J Biol Chem 264: 17816-17823, 1989
  45. Stevens DR, Cotman CW. Excitatory actions of tetrahydro-9- aminoacridine (THA) on hippocampal pyramidal neurons. Neurosci Lett 79: 301, 1987 https://doi.org/10.1016/0304-3940(87)90448-4
  46. Sugawara T, Kitamura N, Ohta T, Ito S, Nakazato Y. Inhibitory effects of tacrine and physostigmine on catecholamine secretion and membrane currents in guinea-pig adrenal chromaffin cells. Fundam Clin Pharmacol 12: 279-285, 1998 https://doi.org/10.1111/j.1472-8206.1998.tb00955.x
  47. Sugawara T, Ohta T, Asano T, Ito S, Nakazato Y. Tacrine inhibits nicotinic secretory and current responses in adrenal chromaffin cells. Eur J Pharmacol 319: 123-130, 1997 https://doi.org/10.1016/S0014-2999(96)00835-7
  48. Summers WK, Majovski LV, Marsh GM, Tachiki K, Kling A. Oral tetrahydroaminoacridine in long-term treatment of senile dementia, Alzheimer type. N Engl J Med 315: 1241-1245, 1986 https://doi.org/10.1056/NEJM198611133152001
  49. Sunaga K, Chuang DM, Ishitani R. Autoradiographic demonstration of an increase in muscarinic cholinergic receptors in cerebellar granule cells treated with tetrahydroaminoacridine. Neurosci Lett 151: 45-47, 1993 https://doi.org/10.1016/0304-3940(93)90041-I
  50. 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
  51. Szilagyi M, Lau WM. Interaction of tacrine at M1 and M2 cholinoceptors in guinea pig brain. Pharmacology 47: 223-229, 1993 https://doi.org/10.1159/000139101
  52. Tallarida RJ, Murray RB. Manual of pharmacologic calculation with computer programs. 2nd Ed New York Speringer-Verlag 132, 1987
  53. Thesleff S, Sellin LC, Taggerud S. Tetrahydroamino-acridine (tacrine) stimulates neurosecretion at mammalian motor endplates. Br J Pharmacol 100: 487, 1990 https://doi.org/10.1111/j.1476-5381.1990.tb15834.x
  54. Uceda G, Artalejo AR, Lopez MG, Abad F, Neher E, Garcia AG. Ca$^2+$-activated K$^+$ channels modulated muscarinic secretion in ca chromaffin cells. J Physiol 454: 213-230, 1992 https://doi.org/10.1113/jphysiol.1992.sp019261
  55. 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, 1985 https://doi.org/10.1007/BF00692905
  56. 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
  57. Warpman U, Zhang X, Nordberg A. Effect of tacrine on in vivo release of dopamine and its metaboltes in the striatum of freely moving rats. J Pharmacol Expt Ther 277: 917-922, 1996
  58. Xiao WB, Nordberg A, Zhang X. Effect of in vivo microdialysis of 1,2,3,4-tetrahydroaminoacridine (THA) on the extracellular concentration of acetylcholine in the striatum of anesthetized rats. J Pharmacol Exp Ther 265: 759-764, 1993