The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
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Influence of Ketamine on Catecholamine Secretion in the Perfused Rat Adrenal Medulla

  • Ko, Young-Yeob (Departments of Internal Medicine (Cardiology), College of Medicine, Chosun University) ;
  • Jeong, Yong-Hoon (Departments of Pharmacology, College of Medicine, Chosun University) ;
  • Lim, Dong-Yoon (Departments of Pharmacology, College of Medicine, Chosun University)
  • Published : 2008.06.30
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Abstract

The aim of the present study was to examine the effects of ketamine, a dissociative anesthetics, on secretion of catecholamines (CA) secretion evoked by cholinergic stimulation from the perfused model of the isolated rat adrenal gland, and to establish its mechanism of action, and to compare ketamine effect with that of thiopental sodium, which is one of intravenous barbiturate anesthetics. Ketamine ($30{\sim}300{\mu}M$), perfused into an adrenal vein for 60 min, dose- and time-dependently inhibited the CA secretory responses evoked by ACh (5.32 mM), high $K^+$ (a direct membrane-depolarizer, 56 mM), DMPP (a selective neuronal nicotinic NN receptor agonist, $100{\mu}M$) and McN-A-343 (a selective muscarinic M1 receptor agonist, $100{\mu}M$). Also, in the presence of ketamine ($100{\mu}M$), the CA secretory responses evoked by veratridine (a voltage-dependent $Na^+$ channel activator, $100{\mu}M$), Bay-K-8644 (an L-type dihydropyridine $Ca^{2+}$ channel activator, $10{\mu}M$), and cyclopiazonic acid (a cytoplasmic $Ca^{2+}$-ATPase inhibitor, $10{\mu}M$) were significantly reduced, respectively. Interestingly, thiopental sodium ($100{\mu}M$) also caused the inhibitory effects on the CA secretory responses evoked by ACh, high $K^+$, DMPP, McN-A-343, veratridine, Bay-K-8644, and cyclopiazonic acid. Collectively, these experimental results demonstrate that ketamine inhibits the CA secretion evoked by stimulation of cholinergic (both nicotinic and muscarinic) receptors and the membrane depolarization from the isolated perfused rat adrenal gland. It seems likely that the inhibitory effect of ketamine is mediated by blocking the influx of both $Ca^{2+}$ and $Na^+$ through voltage-dependent $Ca^{2+}$ and $Na^+$ channels into the rat adrenal medullary chromaffin cells as well as by inhibiting $Ca^{2+}$ release from the cytoplasmic calcium store, which are relevant to the blockade of cholinergic receptors. It is also thought that, on the basis of concentrations, ketamine causes similar inhibitory effect with thiopental in the CA secretion from the perfused rat adrenal medulla.

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 Exp Ther 255: 333−339, 1990
  2. 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
  3. Azzaro AJ, Smith DJ. The inhibitory action of ketamine HCl on [$^3H$]5-hydroxytryptamine accumulation by rat brain synaptosomal-rich fractions: comparison with [$^3H$]catecholamine and [$^3H]^V-$aminobutyric acid uptake. Neuropharmacology 16: 349−356, 1977
  4. Burgoyne RD. Mechanisms of secretion from adrenal chromaffin cells. Biochim Biophys Acta 779: 201−216, 1984
  5. Cena V, Nicolas GP, Sanchez-Garcia P, Kirpekar SM, Garcia AG. Pharmacological dissection of receptor-associated and voltage- sensitive ionic channels involved in catecholamine release. Neuroscience 10: 1455−1462, 1983
  6. Challis 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
  7. 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
  8. Clanachan AS, McGrath JC. Effects of ketamine on the peripheral autonomic nervous system of the rat. Br J Pharmacol 58: 247−252, 1976
  9. Cohen ML, Chan SL, Way WL, Trevor AJ. Distribution in the brain and metabolism of ketamine in the rat after intravenous administration. Anesthesiology 39: 370−376, 1973
  10. Corssen G, Domino EF. Dissociative anesthesia: further pharmacologic studies and first clinical experience with the phencyclidine derivative CI-581. Anesth Analg 45: 29−40, 1966
  11. Diaz FA, Bianco JA, Bello A, Beer N, Velarde H, Izquierdo JP, Jaen R. Effects of ketamine on canine cardiovascular function. Br J Anaesth 48: 941−946, 1976
  12. Domino EF, Chodoff P, Corssen G. Pharmacologic effects of CI-581, a new dissociative anesthetic in man. Clin Pharmacol Ther 6: 279−291, 1965
  13. Domino EF, Zsigmond EK, Domino LE, Domino KE, Kothary SP, Domino SE. Plasma levels of ketamine and two of its metabolites in surgical patients using a gas chromatographic mass fragmentographic assay. Anesth Analg 61: 87−92, 1982
  14. Douglas WW, Kanno T, Sampson SR. Influence of the ionic environment on the membrane potential of adrenal chromaffin cells and on the depolarizing effect of acetylcholine. J Physiol 191: 107−121, 1967
  15. Dowdy EG, Kaya K. Studies of the mechanism of cardiovascular responses to CI-581. Anesthesiology 29: 931−943, 1968
  16. Gallagher JP, Dun N, Higashi H, Nisihi S. Actions of ketamine on synaptic transmission in frog sympathetic ganglia. Neuropharmacology 15: 139−143, 1976
  17. 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
  18. Garty M, Deka-Starosta A, Stull R, Kopin IJ, Goldstein DS. Effects of general anesthetics on plasma levels of catechols in intact and in adrenal-demedullated rats. Biogenic Amines 7: 435−443, 1990
  19. Gemperle M, Szappanyos G, Rifat K. Neuroleptanesthesia in gerontosurgery. Int Anesthesiol Clin 11: 125−138, 1973
  20. 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
  21. Goldberg AH, Keane PW, Phear WP. Effects of ketamine on contractile performance and excitability of isolated heart muscle. J Pharmacol Exp Ther 175: 388−394, 1970
  22. Graf BM, Vicenzi MN, Martin E, Bosnjak ZJ, Stowe DF. Ketamine has stereospecific effects in the isolated perfused guinea pig heart. Anesthesiology 82: 1426-1437, 1995 https://doi.org/10.1097/00000542-199506000-00014
  23. Hammer R, Giachetti A. Muscarinic receptor subtypes: M1 and M2 biochemical and functional characterization. Life Sci 31: 2991-2998, 1982 https://doi.org/10.1016/0024-3205(82)90066-2
  24. Hara K, Minami K, Ueno S, Toyohira Y, Tsutsui M, Shigematsu A, Yanagihara N. Up-regulation of noradrenaline transporter in response to prolonged exposure to ketamine. Naunyn Schmiedeberg's Arch Pharmacol 365: 406−412, 2002
  25. Hara K, Yanagihara N, Minami K, Ueno S, Toyohira Y, Sata T, Kawamura M, Bruss M, Bonisch H, Shigematsu A, Izumi F. Ketamine interacts with the noradrenaline transporter at a site partly overlapping the desipramine binding site. Naunyn- Schmiedeberg's Arch Pharmacol 358: 328−333, 1998
  26. Harish OE, Kao LS, Raffaniello R, Wakade AR, Schneider AS. Calcium dependence of muscarinic receptor-mediated catecholamine secretion from the perfused rat adrenal medulla. J Neurochem 48: 1730−1735, 1987
  27. Hensel I, Braun U, Kettler D, Knoll D, Martel J, Paschen K. Studies on circulatory and metabolic changes during ketamine anaesthesia. Anaesthesist 21: 44−49, 1972
  28. Idvall J, Ahlgren I, Aronsen KF, Stenberg P. Ketamine infusions: pharmacokinetics and clinical effects. Br J Anaesth 51: 1167− 1173, 1979 https://doi.org/10.1093/bja/51.12.1167
  29. Ilno M. Calcium-induced calcium release mechanism in guinea pig taenia caeci. J Gen Physiol 94: 363−383, 1989
  30. Inoue M, Kuriyama H. Muscarinic receptor is coupled with a cation channel through a GTP-binding protein in guinea-pig chromaffin cells. J Physiol (Lond) 436: 511−529, 1991
  31. Juang MS, Yonemura K, Morita T, Tanaka T. Ketamine acts on the peripheral sympathetic nervous system of guinea pigs. Anesth Analg 59: 45−49, 1980
  32. Kidokoro Y, Miyazaki S, Ozawa S. Acetylcholine-induced membrane depolarization and potential fluctuations in the rat adrenal chromaffin cell. J Physiol 324: 203−220, 1982
  33. Kitagawa H, Yamazaki T, Akiyama T, Yahagi N, Kawada T, Mori H, Sunagawa K. Modulatory effects of ketamine on catecholamine efflux from in vivo cardiac sympathetic nerve endings in cats. Neurosci Lett 324: 232−236, 2002
  34. Klose R, Peter K. Clinical studies on single-drug anesthesia using ketamine in patients with burns. Anaesthesist 22: 121−126, 1973
  35. Knight DE, Baker PF. Observations on the muscarinic activation of catecholamine secretion in the chicken adrenal. Neuroscience 19: 357−366, 1986
  36. Kolka MA, Elizondo RS, Weinberg RP. Sympathoadrenal responses to cold and ketamine anesthesia in the rhesus monkey. J Appl Physiol 54: 896−900, 1983
  37. Kreuscher H, Gauch H. The effect of phencylidine derivatives ketamine (CI 581) on the cardiovascular system of the man. Anaesthesist 16: 229−233, 1967
  38. Ladona MG, Aunis D, Gandia AG, Garcia AG. Dihydropyridine modulation of the chromaffin cell secretory response. J Neurochem 48: 483−490, 1987
  39. Lanning CF, Harmel MH. Ketamine anesthesia. Annu Rev Med 26: 137−141, 1975
  40. 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
  41. 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
  42. Mahmoodi V, Byrne AJ, HeaIy TE, Hussain SZ. Effect of ketamine on transmission in sympathetic ganglia. Br J Anaesth 52: 371−375, 1980
  43. Maleque MA, Warnick JE, Albuquerque EX. The mechanism and site of action of ketamine on skeletal muscle. J Pharmacol Exp Ther 219: 638−645, 1981
  44. McCarthy DA, Chen G, aup DH, Ensor C. General anesthetic and other pharmacological properties of 2-(O-chlorophenyl)-2- methylamino cyclohexane HCl (CI-581). J New Drugs 5: 21−33, 1965
  45. McGrath JC, MacKenzie JE, Millar RA. Circulatory responses to ketamine: dependence on respiratory pattern and background anaesthesia in the rabbit. Br J Anaesth 47: 1149−1156, 1975
  46. Misbahuddin M, Isosaki M, Houchi H, Oka M. Muscarinic receptor-mediated increase in cytoplasmic free $Ca^{2+}$ in isolated bovine adrenal medullary cells. Effects of TMB-8 and phorbol ester TPA. FEBS Lett 190: 25−28, 1985
  47. Nakazato Y, Ohga A, Oleshansky M, Tomita U, Yamada Y. Voltage-independent catecholamine release mediated by the activation of muscarinic receptors in guinea-pig adrenal glands. Br J Pharmacol 93: 101−109, 1988
  48. 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 ed, Catecholamines: Basic and Clinical frontiers. Pergamon Press, Oxford, p 70−72, 1979
  49. Okamoto T, Okutani R, Tashiro C. The dual effect of ketamine on dopamine release from rat pheochromocytoma (PC-12) cells. Masui 45: 1083−1087, 1996
  50. Purifoy JA, Holz RW. The effects of ketamine, phencyclidine and lidocaine on catecholamine secretion from cultured bovine adrenal chromaffin cells. Life Sci 35: 1851−1857, 1984
  51. Rust M, Landauer B, Kolb E. Ketamine--a suitable agent for emergency situations. Anaesthesist 27: 205−212, 1978
  52. Schwartz DA, Horwitz LD. Effects of ketamine on left ventricular performance. J Pharmacol Exp Ther 194: 410−414, 1975
  53. 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
  54. Sumikawa K, Matsumoto T, Amenomori Y, Hkano H, Amakata Y. Selective actions of intravenous anesthetics on nicotinic- and muscarinic-receptor-mediated response of the dog adrenal medulla. Anesthesiology 59: 412−416, 1983
  55. 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
  56. Takara H, Wada A, Arita M, Sumikawa K, Izumi F. Ketamine inhibits $^{45}Ca$ influx and catecholamine secretion by inhibiting $^{22}Na$ influx in cultured bovine adrenal medullary cells. Eur J Pharmacol 125: 217−224, 1986
  57. Tallarida RJ, Murray RB. Manual of pharmacologic calculation with computer programs. 2nd ed. Speringer-Verlag, New York, p 132, 1987
  58. Taube HD, Montel H, Hau G, Starke K. Phencyclidine and ketamine: comparison with the effect of cocaine on the noradrenergic neurones of the rat brain cortex. Naunyn- Schmiedeberg's Arch Pharmacol 291: 47−54, 1975
  59. Traber DL, Wilson RD, Priano LL. Differentiation of the cardiovascular effects of CI-581. Anesth Analg 47: 769−778, 1968
  60. Uceda G, Artalejo AR, Lopez MG, Abad F, Neher E, Garcia AG. $Ca^{2+}$-activated $K^{+}$ channels modulate muscarinic secretion in cat chromaffin cells. J Physiol 454: 213−230, 1992
  61. 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
  62. Virtue RW, Alanis JM, Mori M, Lafargue RT, Vogal JHK, Metcalf DR. An anesthetic agent: 2-(O-chlorophenyl)-2-methylamino cyclohexane HCl (CI-581). Anesthesiology 28: 823−833, 1967
  63. Volle RL, Alkadhi KA, Branisteanu DD, Reynolds LS, Epstein PM, Amilowitz H, Lambert JJ, Henderson EG. Ketamine and ditran block end-plate ion conductance and [$^{3}H$]phencyclidine binding to electric organ membrane. J Pharmacol Exp Ther 221: 570−576, 1982
  64. Wada A, Izumi F, Yanagihara N, Kobayashi H. Modulation by oubain and diphenylhydantoin of veratridine-induced $^{22}Na$ influx and its relation to $^{45}Ca$ influx and secretion of catecholamines in cultured bovine adrenal medullary cells. Naunyn-Schmiedberg's Arch Pharmacol 328: 273−278, 1985a
  65. Wada A, Takara H, Izumi F, Kobayashi H, Yanagihara N. Influx of 22Na through acetylcholine receptor-associated Na channels: relationship between $^{22}Na$ influx, $^{45}Ca$ influx and secretion of catecholamines in cultured bovine adrenal medulla cells. Neuroscience 15: 283−292, 1985b
  66. Wakade AR. Studies on secretion of catecholamines evoked by acetylcholine or transmural stimulation of the rat adrenal gland. J Physiol 313: 463−480, 1981
  67. Wieber J, Gugler R, Ohuchi T, Oka M. Pharmacokinetics of ketamine in man. Anesthesist 24: 260−283, 1975
  68. Yamanaka I, Dowdy EG. The effects of ketamine on spiral-cut strips of rabbit aorta. Anesthesiology 40: 222−227, 1974