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. 1978 May;278:117–139. doi: 10.1113/jphysiol.1978.sp012296

Cyclic changes in potential and resistance of the beta-cell membrane induced by glucose in islets of Langerhans from mouse.

I Atwater, B Ribalet, E Rojas
PMCID: PMC1282341  PMID: 353252

Abstract

1. The effects of KCl on the membrane potential were studied in cells from mouse islets of Langerhans identified as beta-cells by the characteristic pattern of electrical activity induced by 11.1 mM glucose. 2. In the absence of glucose, when the beta-cell membrane does not exhibit electrical activity, the dependence of the membrane potential upon external potassium [K+]o, could be described by the constant field equation using a PK/PNa ratio between 30 and 75. 3. In 11.1 mM glucose, when the beta-cell membrane potential fluctuates between a silent phase at about -50 mV and an active phase at about -40 mV giving rise to a train of spikes, the dependence of the membrane potential upon [K+]o could also be described with the constant field equation using a smaller PK/PNa of about 15, during the silent phase, and of about 8, during the active phase (foot of the spikes during the burst). 4. A bridge amplifier for measuring the changes in membrane potential during the application of pulses of current through the same micro-electrode was used to estimate the input resistance of a beta-cell. In 11.1 mM glucose, rough estimates of the membrane resistance during the silent phase averaged 1.2 X 10(8) omega. 5. The time course of the changes in input resistance of the cell when switching from 0 to 11.1 mM glucose showed a transient decrease from 0.9 X 10(8) to 0.7 X 10(8) omega followed by an increase to 1.2 X 10(8) omega. 6. The burst pattern was shown to result from the superposition of two potential changes: (a) 5--10 mV depolarization (lasting about 10 sec in 11.1 mM glucose), and (b) 10--50 mM spikes (lasting about 0.1 sec). Only the latter could be suppressed by hyperpolarizing current injection. 7. Application of pulses of current during the various phases of the electrical activity in 11.1 mM glucose enable us to compare the resistance during the silent and active phases. This was found to be oscillating between a high resistance value at about 1.2 X 10(8) omega before each burst and a low resistance value at 0.9 X 10(8) omega during the active phase at the foot of the spikes. In some cells the resistance during the silent phase remained fairly constant. In other cells it increased gradually from 1.1 X 10(8) to 1.3 X 10(8) omega measured just before each burst of spikes. 8. The observed increase in resistance induced by glucose together with the measured dependency of the membrane potential on [K+]o with and without glucose can be explained by postulating that in the presence of glucose the K+ permeability of the beta-cell membrane is reduced. 9. The oscillations between a high and a low resistance state in the presence of 11.1 mM glucose could be due to a sudden decrease in K+ permeability followed by a much larger increase in permeability to other ions, presumably Na+ and Ca2+.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ashcroft S. J. The control of insulin release by sugars. Ciba Found Symp. 1976;41:117–139. doi: 10.1002/9780470720233.ch7. [DOI] [PubMed] [Google Scholar]
  2. Atwater I., Beigelman P. M. Dynamic characteristics of electrical activity in pancreatic beta-cells. I. - Effects of calcium and magnesium removal. J Physiol (Paris) 1976 Nov;72(6):769–786. [PubMed] [Google Scholar]
  3. Atwater I., Meissner H. P. Electrogenic sodium pump in beta-cells of islets of Langerhans. J Physiol. 1975 May;247(1):56P–58P. [PubMed] [Google Scholar]
  4. Beigelman P. M., Ribalet B., Atwater I. Electric activity of mouse pancreatic beta-cells. II. Effects of glucose and arginine. J Physiol (Paris) 1977 Jul;73(2):201–217. [PubMed] [Google Scholar]
  5. DRAPER M. H., WEIDMANN S. Cardiac resting and action potentials recorded with an intracellular electrode. J Physiol. 1951 Sep;115(1):74–94. doi: 10.1113/jphysiol.1951.sp004653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dean P. M., Matthews E. K. Electrical activity in pancreatic islet cells. Nature. 1968 Jul 27;219(5152):389–390. doi: 10.1038/219389a0. [DOI] [PubMed] [Google Scholar]
  7. Dean P. M., Matthews E. K. Electrical activity in pancreatic islet cells: effect of ions. J Physiol. 1970 Sep;210(2):265–275. doi: 10.1113/jphysiol.1970.sp009208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dean P. M., Matthews E. K. Glucose-induced electrical activity in pancreatic islet cells. J Physiol. 1970 Sep;210(2):255–264. doi: 10.1113/jphysiol.1970.sp009207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dean P. M. Ultrastructural morphometry of the pancreatic -cell. Diabetologia. 1973 Apr;9(2):115–119. doi: 10.1007/BF01230690. [DOI] [PubMed] [Google Scholar]
  10. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. LOEWENSTEIN W. R., KANNO Y. STUDIES ON AN EPITHELIAL (GLAND) CELL JUNCTION. I. MODIFICATIONS OF SURFACE MEMBRANE PERMEABILITY. J Cell Biol. 1964 Sep;22:565–586. doi: 10.1083/jcb.22.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mattews E. K., Sakamoto Y. Pancreatic islet cells: electrogenic and electrodiffusional control of membrane potential. J Physiol. 1975 Mar;246(2):439–457. doi: 10.1113/jphysiol.1975.sp010898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Matthews E. K., Sakamoto Y. Electrical characteristics of pancreatic islet cells. J Physiol. 1975 Mar;246(2):421–437. doi: 10.1113/jphysiol.1975.sp010897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Meissner H. P., Atwater I. J. The kinetics of electrical activity of beta cells in response to a "square wave" stimulation with glucose or glibenclamide. Horm Metab Res. 1976 Jan;8(1):11–16. doi: 10.1055/s-0028-1093685. [DOI] [PubMed] [Google Scholar]
  16. Meissner H. P. Electrophysiological evidence for coupling between beta cells of pancreatic islets. Nature. 1976 Aug 5;262(5568):502–504. doi: 10.1038/262502a0. [DOI] [PubMed] [Google Scholar]
  17. Meissner H. P., Schmelz H. Membrane potential of beta-cells in pancreatic islets. Pflugers Arch. 1974;351(3):195–206. doi: 10.1007/BF00586918. [DOI] [PubMed] [Google Scholar]
  18. NOBLE D. The voltage dependence of the cardiac membrane conductance. Biophys J. 1962 Sep;2:381–393. doi: 10.1016/s0006-3495(62)86862-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Orci L., Unger R. H., Renold A. E. Structural coupling between pancreatic islet cells. Experientia. 1973 Aug 15;29(8):1015–1018. doi: 10.1007/BF01930436. [DOI] [PubMed] [Google Scholar]
  20. Pace C. S., Price S. Bioelectrical effects of hexoses on pancreatic islet cells. Endocrinology. 1974 Jan;94(1):142–147. doi: 10.1210/endo-94-1-142. [DOI] [PubMed] [Google Scholar]
  21. Pace C. S., Price S. Electrical responses of pancreatic islet cells to secretory stimuli. Biochem Biophys Res Commun. 1972 Feb 25;46(4):1557–1563. doi: 10.1016/0006-291x(72)90785-1. [DOI] [PubMed] [Google Scholar]
  22. Sehlin J., Taljedal I. B. Glucose-induced decrease in Rb+ permeability in pancreatic beta cells. Nature. 1975 Feb 20;253(5493):635–636. doi: 10.1038/253635a0. [DOI] [PubMed] [Google Scholar]
  23. Sehlin J., Täljedal I. B. Transport of rubidium and sodium in pancreatic islets. J Physiol. 1974 Oct;242(2):505–515. doi: 10.1113/jphysiol.1974.sp010720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. TRAUTWEIN W., KASSEBAUM D. G. On the mechanism of spontaneous impulse generation in the pacemaker of the heart. J Gen Physiol. 1961 Nov;45:317–330. doi: 10.1085/jgp.45.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. WEIDMANN S. Effect of current flow on the membrane potential of cardiac muscle. J Physiol. 1951 Oct 29;115(2):227–236. doi: 10.1113/jphysiol.1951.sp004667. [DOI] [PMC free article] [PubMed] [Google Scholar]

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