ATP-sensitive Potassium Channel and Bursting in the Pancreatic Beta Cell. A Theoretical Study

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 1989 Aug 1

PMID 2673420

Citations 56

Authors

J Keizer

G Magnus

Affiliations

Soon will be listed here.

Abstract

Based on the existence of ATP-sensitive potassium channels in the plasma membrane of pancreatic beta cells, we develop a quantitative explanation of the electrical activity observed in pancreatic islets. The proposed mechanism involves the voltage-dependent inward calcium and outward potassium currents described by Rorsman and Trube (1986), which are voltage-activated when an increase in the cytoplasmic ATP/ADP ratio decreases the conductance of the ATP-sensitive potassium channels. It is proposed that modulation of the ATP/ADP ratio occurs through calcium inhibition of oxidative phosphorylation. In this picture the mitochondria serve as a transducer of metabolic activity whose sensitivity is modulated by cytosolic calcium. Solution of the differential equations that describe this mechanism gives rise to both bursting and continuous spiking electrical activity similar to that observed experimentally. While the mechanism for bursting in this model involves the ATP/ADP ratio, the feedback is still provided by calcium, as originally proposed by Chay and Keizer (1983) using a Ca2+-activated potassium conductance. A mixed-model, which includes both ATP-sensitive and Ca2+-activated potassium conductances, also reproduces the experimentally observed electrical activity and may correspond more closely to the actual situation in vivo.

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References

MEISSNER H, Atwater I . The kinetics of electrical activity of beta cells in response to a "square wave" stimulation with glucose or glibenclamide. Horm Metab Res. 1976; 8(1):11-6. DOI: 10.1055/s-0028-1093685. View

Sherman A, Rinzel J, Keizer J . Emergence of organized bursting in clusters of pancreatic beta-cells by channel sharing. Biophys J. 1988; 54(3):411-25. PMC: 1330341. DOI: 10.1016/S0006-3495(88)82975-8. View

Plant R . The effects of calcium++ on bursting neurons. A modeling study. Biophys J. 1978; 21(3):217-37. PMC: 1473693. DOI: 10.1016/S0006-3495(78)85521-0. View

Atwater I, Dawson C, Ribalet B, Rojas E . Potassium permeability activated by intracellular calcium ion concentration in the pancreatic beta-cell. J Physiol. 1979; 288:575-88. PMC: 1281445. View

Atwater I, Dawson C, Scott A, Eddlestone G, Rojas E . The nature of the oscillatory behaviour in electrical activity from pancreatic beta-cell. Horm Metab Res Suppl. 1980; Suppl 10:100-7. View

Wollheim C, SHARP G . Regulation of insulin release by calcium. Physiol Rev. 1981; 61(4):914-73. DOI: 10.1152/physrev.1981.61.4.914. View

Chay T, Keizer J . Minimal model for membrane oscillations in the pancreatic beta-cell. Biophys J. 1983; 42(2):181-90. PMC: 1329221. DOI: 10.1016/S0006-3495(83)84384-7. View

Malaisse W, Malaisse-Lagae F, Sener A . Anomeric specificity of hexose metabolism in pancreatic islets. Physiol Rev. 1983; 63(3):773-86. DOI: 10.1152/physrev.1983.63.3.773. View

Rorsman P, Abrahamsson H, Gylfe E, Hellman B . Dual effects of glucose on the cytosolic Ca2+ activity of mouse pancreatic beta-cells. FEBS Lett. 1984; 170(1):196-200. DOI: 10.1016/0014-5793(84)81398-8. View

10.

Cook D, Ikeuchi M, Fujimoto W . Lowering of pHi inhibits Ca2+-activated K+ channels in pancreatic B-cells. Nature. 1984; 311(5983):269-71. DOI: 10.1038/311269a0. View

11.

Cook D, Hales C . Intracellular ATP directly blocks K+ channels in pancreatic B-cells. Nature. 1984; 311(5983):271-3. DOI: 10.1038/311271a0. View

12.

Ashcroft F, Harrison D, Ashcroft S . Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature. 1984; 312(5993):446-8. DOI: 10.1038/312446a0. View

13.

Findlay I, Dunne M, Petersen O . High-conductance K+ channel in pancreatic islet cells can be activated and inactivated by internal calcium. J Membr Biol. 1985; 83(1-2):169-75. DOI: 10.1007/BF01868748. View

14.

Rorsman P, Trube G . Calcium and delayed potassium currents in mouse pancreatic beta-cells under voltage-clamp conditions. J Physiol. 1986; 374:531-50. PMC: 1182737. DOI: 10.1113/jphysiol.1986.sp016096. View

15.

Misler S, Falke L, Gillis K, McDaniel M . A metabolite-regulated potassium channel in rat pancreatic B cells. Proc Natl Acad Sci U S A. 1986; 83(18):7119-23. PMC: 386665. DOI: 10.1073/pnas.83.18.7119. View

16.

Kakei M, Kelly R, Ashcroft S, Ashcroft F . The ATP-sensitivity of K+ channels in rat pancreatic B-cells is modulated by ADP. FEBS Lett. 1986; 208(1):63-6. DOI: 10.1016/0014-5793(86)81533-2. View

17.

Trube G, Rorsman P . Opposite effects of tolbutamide and diazoxide on the ATP-dependent K+ channel in mouse pancreatic beta-cells. Pflugers Arch. 1986; 407(5):493-9. DOI: 10.1007/BF00657506. View

18.

Chay T . On the effect of the intracellular calcium-sensitive K+ channel in the bursting pancreatic beta-cell. Biophys J. 1986; 50(5):765-77. PMC: 1329801. DOI: 10.1016/S0006-3495(86)83517-2. View

19.

Himmel D, Chay T . Theoretical studies on the electrical activity of pancreatic beta-cells as a function of glucose. Biophys J. 1987; 51(1):89-107. PMC: 1329866. DOI: 10.1016/S0006-3495(87)83314-3. View

20.

Dunne M, Findlay I, Petersen O, Wollheim C . ATP-sensitive K+ channels in an insulin-secreting cell line are inhibited by D-glyceraldehyde and activated by membrane permeabilization. J Membr Biol. 1986; 93(3):271-9. DOI: 10.1007/BF01871181. View