Evidence for the induction of repetitive action potentials in synaptosomes by K+-channel inhibitors: An analysis of plasma membrane ion fluxes

Journal of Neurochemistry

Volumn 67, Issue 1, 1996, Pages 389-397

  Tibbs, Gareth R ^a,c   Dolly, J Oliver ^a   Nicholls, David G ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

4 Aminopyridine; Calcium; Charybdotoxin; Exocytosis; K+ channel inhibitors; Rubidium 86; Synaptosome; Tetraethylammonium; Tetrodotoxin; Dendrotoxin

Indexed keywords

4 AMINOPYRIDINE; CHARYBDOTOXIN; DENDROTOXIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; RUBIDIUM 86; TETRODOTOXIN; TETRYLAMMONIUM;

ACTION POTENTIAL; ANALYTIC METHOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL POLARITY; CONTROLLED STUDY; EXOCYTOSIS; GENE INDUCTION; GUINEA PIG; ION TRANSPORT; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; SYNAPTOSOME;

ANIMALIA; CAVIA PORCELLUS; STROPHANTHUS GRATUS; SUS SCROFA;

EID: 0029886775     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1996.67010389.x     Document Type: Article

References (49)

1. Adam-Vizi V. and Ligetti E. (1986) Calcium uptake of rat brain synaptosomes as a function of membrane potential under different depolarizing conditions. J. Physiol. (Lond.) 372, 363-377.
2. Anderson C. S., MacKinnon R., Smith C., and Miller C. (1988) Charybdotoxin block of single Ca2+-activated K+ channels. Effects of channel gating, voltage, and ionic strength. J. Gen. Physiol. 91, 317-333.
3. Barrie A. P., Nicholls D. G., Sanchez-Prieto J., and Sihra T. S. (1991) An ion channel locus for the protein kinase C potentiation of transmitter glutamate release from guinea pig cerebrocortical synaptosomes. J. Neurochem. 57, 1398-1404.
4. Bartschat D. K. and Blaustein M. P. (1985a) Potassium channels in isolated presynaptic nerve terminals from rat brain. J. Physiol. (Lond.) 361, 419-440.
5. Bartschat D. K. and Blaustein M. P. (1986) Calcium-activated potassium channels in isolated presynaptic nerve terminals from rat brain. J. Physiol. (Lond.) 361, 441-457.
6. Benishin C. G., Sorensen R. G., Brown W. E., Krueger B. K., and Blaustein M. P. (1988) Four polypeptide components of green mamba venom selectively block certain potassium channels in rat brain synaptosomes. Mol. Pharmacol. 34, 152-159.
7. Black A. R., Breeze A. L., Othman I. B., and Dolly J. O. (1986) Involvement of neuronal acceptors for dendrotoxin in its convulsive action in rat brain. Biochem. J. 237, 397-404.
8. Brew H. and Attwell D. (1987) Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327, 707-709. [published erratum appears in Nature (1987) 328, 742].
9. Coffey E. T., Sihra T. S., and Nicholls D. G. (1993) Protein kinase C and the regulation of glutamate exocytosis from cerebrocortical synaptosomes. J. Biol. Chem. 268, 21060-21065.
10. Coffey E. T., Herrero I., Sihra T. S., Sánchez-Prieto J., and Nicholls D. G. (1994) Glutamate exocytosis and MARCKS phosphorylation are enhanced by a metabotropic glutamate receptor coupled to a protein kinase C synergistically activated by diacylglycerol and arachidonic acid J. Neurochem. 63, 1303-1310. [published erratum appears in J. Neurochem. (1995) 64, 471].
11. Colby K. A. and Blaustein M. P. (1988) Inhibition of voltage-gated K channels in synaptosomes by sn-1,2-dioctanoylglycerol, an activator of protein kinase C. J. Neurosci. 8, 4685-4692.
12. Doležal V. and Tuček S. (1983) The effects of 4-aminopyridine and tetrodotoxin on the release of acetylcholine from rat striatal slices. Naunyn Schmiedebergs Arch. Pharmacol. 323, 90-95.
13. Dolly J. O. (1988) Potassium channels - what can the protein chemistry contribute? Trends Neurosci. 11, 186-188.
14. Dolly J. O., Rettig J., Scott V. E., Parcej D. N., Wittkat R., Sewing S., and Pongs O. (1994) Oligomeric and subunit structures of neuronal voltage-sensitive K+ channels. (Review) Biochem. Soc. Trans. 22, 473-478.
15. Gornall A. G., Bardawill C. J., and David M. M. (1949) Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177, 751-766.
16. Grynkiewicz G., Poenie M., and Tsien R. Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
17. Gustafsson B., Galvan M., Grafe P., and Wigstrom H. (1982) A transient outward current in a mammalian central neurone blocked by 4-aminopyridine. Nature 299, 252-254.
18. Harvey A. L., Marshall D. L., De-Allie F. A., and Strong P. N. (1989) Interactions between dendrotoxin, a blocker of voltage-dependent potassium channels, and charybdotoxin, a blocker of calcium-activated potassium channels, at binding sites on neuronal membranes. Biochem. Biophys. Res. Commun. 163, 394-397.
19. Herrero I., Miras-Portugal M. T., and Sánchez-Prieto J. (1992a) Activation of protein kinase C by phorbol esters and arachidonic acid required for the optimal potentiation of glutamate exocytosis. J. Neurochem. 59, 1574-1577.
20. Herrero I., Miras-Portugal M. T., and Sánchez-Prieto J. (1992b) Positive feedback of glutamate exocytosis by metabotropic presynaptic receptor stimulation. Nature 360, 163-166.
21. Hille B. (1992) Ionic Channels of Excitable Membranes. Sinauer Associate Inc., Sunderland, Massachusetts.
22. 2+. J. Neurochem. 56, 86-94.
23. Miller C., Moczydlowski E, Latorre R., and Phillips M. (1985) Charybdotoxin, a protein inhibitor of single Ca2+-activated K+ channels from mammalian skeletal muscle. Nature 313, 316-318.
24. Nicholls D. G. (1992) Neurotransmission. A retrograde step forward [news; comment]. Nature 360, 106-107.
25. Nicholls D. G. and Coffey E. T. (1994) Glutamate exocytosis from isolated nerve terminals. (Review) Adv. Second Messenger Phosphoprotein Res. 29, 189-203.
26. Nicholls D. G. and Sihra T. S. (1986) Synaptosomes possess an exocytotic pool of glutamate. Nature 321, 772-773.
27. Penner R., Petersen M., Pierau F. K., and Dreyer F. (1986) Dendrotoxin: a selective blocker of a non-inactivating potassium current in guinea-pig dorsal root ganglion neurones. Pflugers Arch. 407, 365-369.
28. Reid P. F., Pongs O., and Dolly J. O. (1992) Cloning of a bovine voltage-grated K+ channel gene utilising partial amino acid sequence of a dendrotoxin-binding protein from brain cortex. FEBS Lett. 302, 31-34.
29. Reinhart P. H., Chung S., and Levitan I. B. (1989) A family of calcium-dependent potassium channels from rat brain. Neuron 2, 1031-1041.
30. Rogawski M. A. (1985) The A-current: how ubiquitous a feature of excitable cells is it? Trends Neurosci. 8, 214-219.
31. Rogawski M. A. and Barker J. L. (1983) Effects of 4-aminopyridine on calcium action potentials and calcium current under voltage clamp in spinal neurons. Brain Res. 280, 180-185.
32. Rudy B. (1988) Diversity and ubiquity of K channels. (Review) Neuroscience 25, 729-749.
33. Schneider M. J., Rogowski R. S., Krueger B. K., and Blaustein M. P. (1989) Charybdotoxin blocks both Ca-activated K channels and Ca-independent voltage-gated K channels in rat brain synaptosomes. FEBS Lett. 250, 433-436.
34. Scott I. D. and Nicholls D. G. (1980) Energy transduction in intact synaptosomes. Influence of plasma-membrane depolarization on the respiration and membrane potential of internal mitochondria determined in situ. Biochem. J. 186, 21-33.
35. Scott V. E., Parcej D. N., Keen J. N., Findlay J. B., and Dolly J. O. (1990) Alpha-dendrotoxin acceptor from bovine brain is a K+ channel protein. Evidence from the N-terminal sequence of its larger subunit. J. Biol. Chem. 265, 20094-20097.
36. + channels in dorsal root ganglion cells. Neurosci. Lett. 93, 49-55.
37. Stansfeld C. E., Marsh S. J., Halliwell J. V., and Brown D. A. (1986) 4-Aminopyridine and dendrotoxin induce repetitive firing in rat visceral sensory neurones by blocking a slowly inactivating outward current. Neurosci. Lett. 64, 299-304.
38. Stansfeld C. E., Marsh S. J., Parcej D. N., Dolly J. O., and Brown D. A. (1987) Mast cell degranulating peptide and dendrotoxin selectively inhibit a fast-activating potassium current and bind to common neuronal proteins. Neuroscience 23, 893-902.
39. Storm J. F. (1988) Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature 336, 379-381.
40. Stuhmer W., Ruppersberg J. P., Schroter K. H., Sakmann B., Stocker M., Giese K. P., Perschke A., Baumann A., and Pongs O. (1989) Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J. 8, 3235-3244.
41. Suszkiw J. B., Murawsky M. M., and Shi M. (1989) Further characterization of phasic calcium influx in rat cerebrocortical synaptosomes: inferences regarding calcium channel type(s) in nerve endings. J. Neurochem. 52, 1260-1269.
42. Tapia R., Sitges M., and Morales E. (1985) Mechanism of the calcium-dependent stimulation of transmitter release by 4-aminopyridine in synaptosomes. Brain Res. 361, 373-382.
43. Thomas R. C. (1969) Membrane current and intracellular sodium changes in a snail neurone during extrusion of injected sodium. J. Physiol. (Lond.) 201, 495-514.
44. 2+ and glutamate release. J. Neurochem. 53, 1693-1699.
45. 2+-dependent release of glutamate from guinea-pig cerebrocortical synaptosomes. J. Neurochem. 52, 201-206.
46. Tibbs G. R., Nicholls D. G., and Dolly J. O. (1989c) Dendrotoxin and charybdotoxin increase the cytosolic concentration of free Ca2+ in cerebrocortical synaptosomes: an effect not shared by apamin. FEBS Lett. 255, 159-162.
47. 2+ homeostasis and synaptosomal preparation. J. Neurochem. 51, 1667-1674.
48. Weller U., Bernhardt U., Siemen D., Dreyer F., Vogel W., and Habermann E. (1985) Electrophysiological and neurobiochemical evidence for the blockade of a potassium channel by dendrotoxin. Naunyn Schmiedebergs Arch. Pharmacol. 330, 77-83.
49. Werkman T. R., Kawamura T., Yokoyama S., Higashida H., and Rogawski M. A. (1992) Charybdotoxin, dendrotoxin and mast cell degranulating peptide block the voltage-activated K+ current of fibroblast cells stably transfected with NGK4 (Kv1.2) K+ channel complementary DNA. Neuroscience 50, 935-946.