Effect of $Ca^{2+}-channel$ Blockers on Norepinephrine Release in the Rat Hippocampal Slice and Synaptosome

  • Kim, Suk-Won (Department of Pharmacology, Wonkwang University School of Medicine, Wonkwang University) ;
  • Jung, Kyu-Yong (Department of Pharmacology, Wonkwang University School of Medicine, Wonkwang University) ;
  • Choi, Bong-Kyu (Department of Pharmacology, Wonkwang University School of Medicine, Wonkwang University)
  • Published : 2002.04.21

Abstract

The aim of this study was to investigate the role of $Ca^{2+}-channel$ blockers in norepinephrine (NE) release from rat hippocampus. Slices and synaptosomes were incubated with $[^3H]-NE$ and the releases of the labelled products were evoked by 25 mM KCl stimulation. Nifedipine, diltiazem, nicardipine, flunarizine and pimozide did not affect the evoked and basal release of NE in the slice. But, diltiazem, nicardipine and flunarizine decreased the evoked NE release with a dose-related manner without any change of the basal release from synaptosomes. Also, a large dose of pimozide produced modest decrement of NE release. ${\omega}-conotoxin$ (CTx) GVIA decreased the evoked NE release in a dose-dependent manner without changing the basal release. And ${\omega}-CTxMVIIC$ decreased the evoked NE release in the synaoptosomes without any effect in the slice, but the effect of decrement was far less than that of ${\omega}-CTxGVIA.$ In interaction experiments with ${\omega}-CTxGVIA,\;{\omega}-CTxMVIIC$ slightly potentiated the effect of ${\omega}-CTxGVIA$ on NE release in the slice and synaptosomal preparations. These results suggest that the NE release in the rat hippocampus is mediated mainly by N-type $Ca^{2+}-channels,$ and that other types such as L-, T- and/or P/Q-type $Ca^{2+}-channels$ could also be participate in this process.

Keywords

References

  1. Augustine GJ, Charlton MP, Smith SJ. Calcium action in synaptic release. Annu Rev Neurosci 10: 633-693, 1987 https://doi.org/10.1146/annurev.ne.10.030187.003221
  2. Bostwick JR, Abbe R, Appel SH. Modulation of acetylcholine release in rat hippocampus by amino alcohols and Bay K 8644. Brain Res 629: 79-87, 1993 https://doi.org/10.1016/0006-8993(93)90484-5
  3. Clos MV, Sanz AG, Sabrià J, Pastor C, Badia A. Differential contribution of L- and N-type calcium channels on rat hippocampal acetylcholine release. Neurosci Letter 182: 125-128, 1994 https://doi.org/10.1016/0304-3940(94)90779-X
  4. Devoto P, Pani L, Kuzmin A, Montis GD. Inhibition of $[^{3}H]$-dopamine uptake by flunarizine. Eur J Pharmacol 203: 67-69, 1991 https://doi.org/10.1016/0014-2999(91)90791-N
  5. Fredholm BB. Presynaptic regulation of hippocampal acetylcholine release is unaffected by calcium channel blockers and intracellular calcium chelation. Acta Physiol Scand 147: 461-463, 1993 https://doi.org/10.1111/j.1748-1716.1993.tb09523.x
  6. Gandhi VC, Jones DJ. Protein kinase C modulates the release of $[^{3}H]$-5-Hydroxytryptamine in the spinal cord of the rat: the role of L-type voltage dependent calcium channel. Neuropharmacology 31: 1101-1108, 1992 https://doi.org/10.1016/0028-3908(92)90005-A
  7. Grassi C, Martire M, Altobelli D, Azzena GB, Preziosi P. Characterization of $Ca^{2+}$-channels responsible for $K^+$-evoked $[^3H]$-noradrenaline release from rat brain cortex synaptosomes and their response to amyotrophic lateral sclerosis lgGs. Experimental Neurology 159: 520-527, 1999 https://doi.org/10.1006/exnr.1999.7164
  8. Hertting G, Zumstein A, Jackisch R, Hoffman I, Stake K. Modulation by endogenous dopamine of the release of acetylcholine in the caudate nucleus of the rabbit. Naunyn-Schmied Arch pharmacol 315: 111-117, 1980 https://doi.org/10.1007/BF00499253
  9. Hirning LD, Fox AP, McClesky, EW, Olivera BM, Thayer SA, Miller RJ, Tsien RW. Dominant role of N-type calcium channels in evoked release of norepinephrine from sympathetic neurons. Science 239: 57-61, 1988 https://doi.org/10.1126/science.2447647
  10. Jessell TM, Kandel ER: Synaptic transmission. a bidirectional and self-modifiable form of cell-cell communication. Cell 72 Suppl: 1-30, 1993
  11. Kasai H, Aosaki T, Fukuda J. Presynaptic calcium antagonist $\omega$- conotoxin irreversibly blocks N-type calcium channels in chick sensory neurons. Neurosci Res 4: 228-235, 1987 https://doi.org/10.1016/0168-0102(87)90014-9
  12. Kimura M, Yamanishi Y, Hanada T, Kagaya T, Kuwada M, Watanabe T, Katayama K, Nishizawa Y. Involvement of P-type calcium channels in high potassium-elicited release of neurotransmitters from rat brain slices. Neuroscience 66: 609-615, 1995 https://doi.org/10.1016/0306-4522(95)00023-C
  13. Linàs R, Sugimori M, Silver RB. Microdomains of high calcium concentration in a presynaptic terminal. Science 256: 677-679, 1992 https://doi.org/10.1126/science.1350109
  14. Lowry OH, Rosebrough NJ, Farr AL, Randal RJ. Protein measurement with Folin phenol reagent. J Biol Chem 193: 265-275, 1951
  15. Lundy PM, Stauderman K, Goulet JC, Frew R. Effect of omegaconotoxin GVⅠA on calcium influx and endogenous acetylcholine release from chicken brain preparations. Neurochem Int 14: 49-54, 1989 https://doi.org/10.1016/0197-0186(89)90008-9
  16. Middlemiss DN. The calcium channel activator, Bay K 8644 enhances K$^+$-evoked efflux of acetylcholine and noradrenaline from rat brain slices. Naunyn-Schmiedeber's Arch Pharmacol 331: 114 -116, 1985 https://doi.org/10.1007/BF00498860
  17. Miller RJ. Multiple calcium channels and neuronal function. Science 235: 46-52, 1987 https://doi.org/10.1126/science.2432656
  18. Nowycky MC, Fox AP, Tsien RW. Three types of neuronal calcium channels with different calcium agonist sensitivity. Nature (London) 316: 440-445, 1985 https://doi.org/10.1038/316440a0
  19. Olivera BM, McIntosh JM, Cruz LJ, Luque FA, Gray WR. Purification and sequence of presynaptic peptide toxin from Conus geographus venom. Biochemistry 23: 5087-5090, 1984 https://doi.org/10.1021/bi00317a001
  20. Pani L, Kuzmin A, Diana M, De Montis G, Gessa L, Rossetti ZL. Calcium blockers differ in modifying cocaine effects in the CNS. Eur J Pharmacol 190: 217-220, 1990 https://doi.org/10.1016/0014-2999(90)94128-K
  21. Pullar IA, Findlay JD. Effect of voltage-sensitive calcium channel antagonists on the release of 5-hydroxytryptamine from rat hippocampus in vivo. J Neurochem 59: 553-559, 1992 https://doi.org/10.1111/j.1471-4159.1992.tb09405.x
  22. Quirion R. Autoradiographic localization of a calcium channel antagonist, $[^3H]$-nitrendipine binding site in brain. Neurosci Lett 36: 267-272, 1983 https://doi.org/10.1016/0304-3940(83)90011-3
  23. Raiteri M, Bonnanno G, Marchi M, Maura G. Is there a functional linkage between neurotransmitter uptake mechanisms and presynaptic receptors. J Pharmacol Exp Ther 231: 671-677, 1984
  24. Randall A, Tsien RW. Pharmacological dissection of multiple types of Ca$^2+$ channel currents in rat cerebellar granule neurons. J Neurosci 15: 2995-3012
  25. Sabria J, Pastor C, Clos MV, Garcia A, Badia A. Involvement of voltage-sensitive calcium channels in the presynaptic regulation of noradrenaline release in rat brain cortex and hippocampus. J Neurochem 64: 2567-2571, 1995 https://doi.org/10.1046/j.1471-4159.1995.64062567.x
  26. Saydoff JA, Zaczek R. Blockade of N- and Q-type $Ca^{2+}$channels inhibit $K^+$-evoked $[^3H]$acetylcholine release in rat hippocampal slices. Brain Res Bull 40: 283-286, 1996 https://doi.org/10.1016/0361-9230(96)00071-8
  27. Schoffelmeer ANM, Wemer J, Mulder AH. Comparison between electrically evoked and potassium-induced $^3$H-noradrenaline release from rat neocortex slices: role of calcium ions and transmitter pools. Neurochem Int 3: 129-136, 1981 https://doi.org/10.1016/0197-0186(81)90031-0
  28. Skattebol A, Trigle DJ. Regional distribution of calcium channel ligand (1,4-dihydropyridine) binding sites and Ca$^2+$ uptake processes in rat brain. Biochem Pharmacol 36: 4163-4166, 1987 https://doi.org/10.1016/0006-2952(87)90575-2
  29. Spedding M, Kilpatrick AT, Alps BJ. Activators of calcium channels: effects in the central nervous system. Fund Clin Pharmac 3: 3s-29s, 1989 https://doi.org/10.1111/j.1472-8206.1989.tb00674.x
  30. Starke K, Spath L, Wichmann T. Effects of verapamil, diltiazem and ryosidine on the release od dopamine and acetylcholine in rabbit caudate nucleus slices. Naunyn-Schmiedeber's Arch Pharmacol 325: 124-130, 1984. https://doi.org/10.1007/BF00506191
  31. Suszkiw JB, Murawsky MM, Fortner RC. Heterogeneity of presynaptic calcium channels revealed by species differences in the sensitivity of synaptosomal calcium entry to omega-conotoxin. Biochem Biophys Res Commun 145: 1283-1286, 1987 https://doi.org/10.1016/0006-291X(87)91576-2
  32. Thomas J, Feuerstein TJ, Dooley DJ, Seeger W. Inhibition of norepinephrine and acetylcholine release from human neocortex by $\omega$-conotoxin GVIA. J Pharmac Exp Ther 252: 778-785, 1989
  33. Tsien RW, Lipscombe D, Madison DV, Bley KR, Fox AP. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11: 431-438, 1988 https://doi.org/10.1016/0166-2236(88)90194-4
  34. Turner TJ, Adams ME, Dunlap K. Calcium channels coupled to glutamate release identified by $\omega$-Aga-IVA. Science 258: 310- 313, 1992 https://doi.org/10.1126/science.1357749
  35. Uchitel OD, Protti DA, Sanchez V, Cherksey BD, Sugimori M, Llinas R. P-type voltage-dependent calcium channel mediates presynaptic calcium influx and transmitter release in mammalian synapses. Proc Natl Acad Sci USA 89: 3330-3333, 1992. https://doi.org/10.1073/pnas.89.8.3330
  36. Wheeler DB, Randall AD, Tsien RW. Roles of N-type and Q-type Ca$^2+$ channels in supporting hippocampal synaptic transmission. Science 264: 107-111, 1994 https://doi.org/10.1126/science.7832825