Abstract
The effect of glucose on kinetics and the voltage-dependent characteristics of glucose-sensitive channels in hippocampal neurons were examined with the cell-attached mode of the patch-clamp technique. Recordings of a 100-pS K+ channel in the presence or absence of glucose demonstrate that the increase in channel open state probability (P o) induced by glucose deprivation (40- to 400-times the control in high-glucose medium) was largely due to a decrease in the global amount of time spent by the channel in a long-lived closed state. TheP o value of the same 100-pS channel was also found to increase (by approx. 80-times) following a depolarization of 40 mV from rest, the main factor responsible for this being a dramatic shortening of the long closed-times on depolarization. Another glucose-sensitive channel of smaller conductance (approx. 10 pS) showed a similar dependence ofP o on glucose, but different dependence on voltage, with long openings at the same hyperpolarized potentials where the 100-pS channel was almost always closed. Our results indicate that the action of glucose on the kinetics of hippocampal channels closely resembles that of ATP-sensitive channels in pancreaticβ-cells. Furthermore, they indicate that the two types of glucose-sensitive channels found in hippocampal neurons, differing not only in their single-channel conductance but also in the dependence on voltage, could play different roles in the responses of these cells to modified energetic supply.
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References
Abele AE, Miller RJ (1990) Potassium channel activators abolish excitotoxicity in cultured hippocampal pyramidal neurons. Neurosci Lett 115:195–200
Amoroso S, Schmid-Antomarchi H, Fosset M, Lazdunski M (1990) Glucose, sulfonylureas and transmitter release: role of ATP-sensitive K+ channels. Science 247:852–854
Ashcroft FM, Harrison DE, Ashcroft SJH (1984) Glucose induces closure of single potassium channels in isolated rat pancreaticβ cells. Nature 312:446–448
Ashcroft FM, Ashcroft SJH, Harrison DE (1988) Properties of single potassium channels modulated by glucose in rat pancreatic β-cells. J Physiol (Lond) 400:501–527
Ashcroft SJH, Ashcroft FM (1990) Properties and functions of ATP-sensitive K-channels. Cell Signal 2:197–214
Ashford MLJ, Sturgess NC, Trout NJ, Gardner NJ, Hales CN (1988) Adenosine-5′-triphosphate-sensitive ion channels in neonatal rat cultured central neurones Pflügers Arch 412:297–304
Ashford MLJ, Boden PR, Treherne JM (1990) Glucose-induced excitation of hypothalamic neurones is mediated by ATP-sensitive K+ channels. Pflügers Arch 415:479–483
Colquhoun D, Hawkes AG (1981) On the stochastic properties of single ion channels. Proc R Soc Lond [Biol] 211:205–235
Colquhoun D, Sigworth FJ (1983) Fitting and statistical analysis of single channel records. In: Sackmann B, Neher E (eds) Single-channel recording. Plenum, New York, pp 191–263
Cook DL, Hales CN (1984) Intracellular ATP directly blocks K+ channels in pancreatic β-cells. Nature 311:269–273
Greif GJ, Lin Y, Freedman JE (1992) Dopamine sensitive and insensitive K+ channels in rat striatal neurons. Soc Neurosci Abstr 18:1500
Horn R, Lange K (1983) Estimating kinetics constants from single channel data. Biophys J 43:207–223
Kakei M, Noma A (1984) Adenosine-5′-triphospahte-sensitive single potassium channels in the atrioventricular node cell of the rabbit heart. J Physiol (Lond) 352:265–284
Kakei M, Noma A, Shibasaki T (1985) Properties of adenosine-triphosphate-regulated potassium channels in guinea-pig ventricular cells. J Physiol (Lond) 363:441–462
Noma A (1983) ATP-regulated K+ channels in cardiac muscle. Nature 305:147–148
Ohno-Shosaku T, Yamamoto C (1992) Identification of an ATP-sensitive K+ channel in rat cultured cortical neurons. Pflügers Arch 422:260–266
Politi DMT, Rogawski MA (1991) Glyburide-sensitive K+ channels in cultured rat hippocampal neurons: activation by cromakalim and energy-depleting conditions. Mol Pharmacol 40:308–315
Qin D, Takano M, Noma A (1989) Kinetics of ATP-sensitive K+ channel revealed with oil-gate concentration jump method. Am J Physiol 257:H1624-H1633
Röper J, Hainsworth AH, Ashcroft FM (1990) ATP-sensitive K+ in guinea-pig isolated substantia nigra neurones are modulated by cellular metabolism. J Physiol (Lond) 430:130P
Salvaggio A, Tromba C, Volterra A (1992) A Bayesian approach to the analysis of single-channel records. In: Morucci JP, Plonsey R, Coatrieux JL, Laxminarayan S (eds) Proceedings of the 14th Annual International Conference of IEEE Engineers in Medicine and Biology Society, Paris, France, Oct. 29–Nov. 1, 1992, vol. 14, IEEE, Psicataway, pp 184–185
Sigworth FJ, Sine SM (1987) Data transformations for an improved display and fitting of single-channel dwell time histograms. Biophys J 52:1047–1054
Spruce AE, Standen NB, Stanfield PR (1985) Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane Nature 316:736–738
Spruce AE, Standen NB, Stanfield PR (1987) Studies of the unitary properties of adenosine-5′-triphosphate-regulated potassium channels of frog skeletal muscle. J Physiol (Lond) 382:213–236
Spuler A, Endres W, Grafe P (1988) Glucose depletion hyperpolarizes guinea pig hippocampal neurons by an increase in potassium conductance. Exp Neurol 100:248–252
Tromba C, Salvaggio A, Racagni G, Volterra A (1992) Hypoglycemia-activated K+ channels in hippocampal neurons. Neurosci Lett 143:185–189
Trube G, Rorsman P, Ohno-Shosaku T (1986) Opposite effects of tolbutamide and diazoxide on the ATP-dependent K+ channel in mouse pancreaticβ-cells. Pflügers Arch 407:493–499
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Tromba, C., Salvaggio, A., Racagni, G. et al. Hippocampal hypoglycaemia-activated K+ channels: single-channel analysis of glucose and voltage dependence. Pflugers Arch. 429, 58–63 (1994). https://doi.org/10.1007/BF02584030
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DOI: https://doi.org/10.1007/BF02584030