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Modulation of the gating of the transient outward potassium current of rat isolated cerebellar granule neurons by lanthanum

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Abstract

The effects of the trivalent cation, lanthanum (La3+) on voltage-dependent K+ conductances were studied in rat isolated cerebellar granule neurons under whole-cell voltage-clamp conditions. La3+ at low micromolar concentrations caused a pronounced enhancement in the outward current evoked by depolarising steps from −50 mV, with the apparent recruitment of an inactivating component. The steady-state inactivation curve for the transient outward current, evoked by depolarising steps from −140 mV, was shifted by approximately 40 mV in the depolarising direction by 10 μM La3+, with a slight increase in the slope factor. The kinetics of activation and inactivation were slowed in the presence of La3+. A shift of 10 mV in the depolarising direction was seen for the activation curve of the delayed rectifier current in the presence of 10 μM La3+. These results indicate that La3+ has a potent effect on the gating characteristics of voltage-activated K+ currents. This effect cannot be explained by surface charge considerations.

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References

  1. Agus ZS, Dukes ID, Morad M (1991) Divalent cations modulate the transient outward current in rat ventricular myocytes. Am J Physiol 30:C310-C318

    Google Scholar 

  2. Armstrong CM, Cota G (1990) Modification of sodium channel gating by lanthanum: some effects that cannot be explained by surface charge theory. J Gen Physiol 96:1129–1140

    Google Scholar 

  3. Bardoni R, Belluzzi, O (1993) Kinetic study and numerical reconstruction of A-type current in granule cells of rat cerebellar slices. J Neurophysiol 69:2222–2231

    Google Scholar 

  4. Belluzzi O, Bardoni R, Magherini PC (1993) Zinc modulation of transient outward current in a mammalian neurone. 32nd International Union of Physiological Sciences Congress, Glasgow 204 31/P

  5. Bourne GW, Trifaro JM (1982) The gadolinium ion:a potent blocker of calcium channels and catecholamine release from cultured chromaffin cells. Neuroscience 7:1615–1622

    Google Scholar 

  6. Carignani C, Robello M, Marchetti C, Maga L (1991) A transient outward current dependent on external calcium in rat cerebellar granule cells. J Membr Biol 122:259–265

    Google Scholar 

  7. Cull-Candy SG, Marshall CG, Ogden D (1989) Voltage-activated membrane currents in rat cerebellar granule neurones. J Physiol (Lond) 414:179–199

    Google Scholar 

  8. D'Arrigo JS (1973) Possible screening of surface charges on crayfish axons by polyvalent metal ions. J Physiol (Lond) 231:117–128

    Google Scholar 

  9. Fagni L, Bossu JL, Bockaert J (1991) Activation of a large conductance Ca2+-dependent K+ channel by stimulation of glutamate phosphoinositide-coupled receptors in cultured cerebellar granule cells. Eur J Neurosci 3:778–789

    Google Scholar 

  10. Frankenhauser B, Hodgkin AL (1957) The action of calcium on the electrical properties of squid axons. J Physiol (Lond) 137:218–244

    Google Scholar 

  11. Gallo V, Ciotti MT, Coletti A, Alolsi F, Levi G (1982) Selective release of glutamate from cerebellar granule cells differentiating in culture. Proc Natl Acad Sci USA 79:7919–7923

    Google Scholar 

  12. Gilbert DL, Ehrenstein G (1969) Effect of divalent cations on potassium conductance of squid axons: determination of surface charge. Biophys J 9:447–463

    Google Scholar 

  13. Gilly WF, Armstrong CM (1982) Divalent cations and the activation kinetics of potassium channels in squid giant axons. J Gen Physiol 79:965–996

    Google Scholar 

  14. Halliwell, JV (1990) K+ channels in the central nervous system. In: Cook, NS (ed) Potassium channels, structure, classification, function and therapeutic potential. Ellis Horwood Chichester, pp 348–381

    Google Scholar 

  15. Hamill OP, Marty A, Sakmann B, Neher E, Sigworth FJ (1981) Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100

    Google Scholar 

  16. Harrison NL, Radke HK, Tamkun MM, Lovinger DM (1993) Modulation of gating of cloned rat and human K+ channels by micromolar Zn2+. Mol Pharmacol 43:482–486

    Google Scholar 

  17. Hille B (1992) Ionic channels of excitable membranes, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  18. Hille B, Woodhull AM, Shapiro BI (1975) Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos Trans R Soc Lond Biol 270:301–318

    Google Scholar 

  19. Hockberger PE, Tseng H-Y, Connor JA (1987) Immunocytochemical and electrophysiological differentiation of rat cerebellar granule cells in explant cultures. J Neurosci 7:1370–1383

    Google Scholar 

  20. Huang R-C, Peng Y-W, Yau K-W (1993) Zinc modulation of a transient potassium current and histochemical localisation of the metal in neurons of the suprachiasmatic nucleus. Proc Natl Acad Sci USA 90:11806–11810

    Google Scholar 

  21. Huston E, Cullen G, Sweeney MI, Pearson H, Fazelli MS, Dolphin AC (1993) Pertussis toxin treatment increases glutamate release and dihydropyridine binding sites in cultured rat cerebellar granule neurones. Neuroscience 52:787–798

    Google Scholar 

  22. Lancaster B, Nicoll RA, Perkel DJ (1991) Calcium activates two types of potassium channels in rat hippocampal neurons in culture. J Neurosci 11:23–30

    Google Scholar 

  23. Mayer ML, Sugiyama K (1988) A modulatory action of divalent cations on transient outward current in cultured rat sensory neurones. J Physiol (Lond) 396:417–433

    Google Scholar 

  24. McLaughlin SGA, Szabo G, Eisenman G (1971) Divalent ions and the surface potential of charged phospholipid membrane. J Gen Physiol 58:667–687

    Google Scholar 

  25. Narahashi T, Tsunoo A, Yoshii M (1987) Characterization of two types of calcium channels in mouse neuroblastoma cells. J Physiol (Lond) 383:231–249

    Google Scholar 

  26. Przywara DA, Bhave SV, Bhave A, Chowdhury PS, Wakade TD, Wakade AR (1992) Activation of K+ channels by lanthanum contributes to the block of transmitter release in chick and rat sympathetic neurons. J Membr Biol 125:155–162

    Google Scholar 

  27. Reinhart PH, Chung S, Levitan IB (1989) A family of calcium-dependent potassium channels from rat brain. Neuron 2:1031–1041

    Google Scholar 

  28. Robello M, Carignani C, Marchetti C (1989) A transient voltage-dependent outward current in cultured cerebellar granules. Biosci Rep 9:451–457

    Google Scholar 

  29. Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25:729–749

    Google Scholar 

  30. Sanguinetti MC, Jurkiewicz NK (1990) Lanthanum blocks a specific component of IK and screens membrane surface charge in cardiac cells. Am J Physiol 259:H1881-H1889

    Google Scholar 

  31. Schwindt PC, Spain WJ, Foehring RC, Stafstrom CE, Chubb MC, Crill WE (1988) Multiple conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Neurophysiol 59:424–449

    Google Scholar 

  32. Spires S, Begenisich T (1992) Chemical properties of the divalent cation binding site on potassium channels. J Gen Physiol 100:181–193

    Google Scholar 

  33. Storm, JF (1987) Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol (Lond) 385:733–759

    Google Scholar 

  34. Watkins CS, Mathie A (1993a) The voltage-activated transient K+ current in rat isolated cerebellar granule neurones. 32nd International Union of Physiological Sciences Congress, Glasgow 204 3/P

  35. Watkins CS, Mathie A (1993b) The modulation by lanthanum of the gating of voltage-dependent potassium currents in rat cerebellar granule neurones. J Physiol (Lond) 473:160P

    Google Scholar 

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Watkins, C.S., Mathie, A. Modulation of the gating of the transient outward potassium current of rat isolated cerebellar granule neurons by lanthanum. Pflügers Arch. 428, 209–216 (1994). https://doi.org/10.1007/BF00724499

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  • DOI: https://doi.org/10.1007/BF00724499

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