Home LiteratureArticle Details
PMID: 1484353 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The relationship between glucose-induced K+ATP channel closure and the rise in [Ca2+]i in single mouse pancreatic beta-cells.

The Journal of physiology ·Vol. 455 ·1992-09-00 ·Pages 173-86

Valdeolmillos M, Nadal A, Contreras D, Soria B

Abstract

1. Intracellular calcium [Ca2+]i and channel activity were simultaneously recorded in single, dissociated mouse beta-cells kept in culture for 1-3 days. [Ca2+]i was estimated from microfluorometric ratio methods using Indo-1. Channel activity was measured using the cell-attached configuration of the patch-clamp technique. 2. At low glucose concentrations (0.3 mM), resting K+ATP channel activity was prevalent. Increasing glucose up to 16 mM, produced a gradual decrease in K+ATP channel activity over a time course of 90-120 s (temperature = 23 degrees C) and an increase in [Ca2+]i. 3. In the majority of experiments, glucose elicited biphasic action currents (action potentials) which preceded the rise in [Ca2+]i. There was a close correlation between spike frequency and the levels of [Ca2+]i. 4. The sulphonylurea tolbutamide (1 mM) blocked K+ATP channels in 10-20 s. K+ATP channel blockade was associated with a quick rise in [Ca2+]i. 5. When K+ATP channel activity was stimulated in the presence of diazoxide (100 microM), increasing the glucose concentration from 3 to 16 mM produced a decrease in [Ca2+]i. Only when diazoxide was removed did glucose produce an increase in [Ca2+]i. 6. In a small population of cells, glucose (16 mM) produced a small decrease in K+ATP channel activity but not an increase in [Ca2+]i. In such cells, tolbutamide blocked K+ATP channels and produced an increase in [Ca2+]i. 7. These results demonstrate a close correlation between K+ATP channel activity and [Ca2+]i in beta-cells. The findings are consistent with the model in which glucose metabolism produces a rise in [Ca2+]i through the blockade of K+ATP channels, membrane depolarization and calcium current activation.

MeSH Terms
Animals Calcium/metabolism Dose-Response Relationship, Drug Glucose/pharmacology Islets of Langerhans/metabolism Membrane Potentials/drug effects Mice Potassium Channels/metabolism Tolbutamide/pharmacology
Chemicals
Potassium Channels Tolbutamide Glucose Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Valdeolmillos M
Department of Physiology, School of Medicine, University of Alicante, Spain.
Nadal A
Contreras D
Soria B
References (34)
34 references, click to expand
  1. Widespread synchronous [Ca2+]i oscillations due to bursting electrical activity in single pancreatic islets.
    Pflugers Arch. 1991 May;418(4):417-22 PMID: 1876486
  2. Ion channels of glucose-responsive and -unresponsive beta-cells.
    Diabetes. 1991 Aug;40(8):1069-78 PMID: 1713562
  3. Single islet beta-cell stimulation by nutrients: relationship between pyridine nucleotides, cytosolic Ca2+ and secretion.
    EMBO J. 1990 Jan;9(1):53-60 PMID: 2403930
  4. Opposite effects of tolbutamide and diazoxide on the ATP-dependent K+ channel in mouse pancreatic beta-cells.
    Pflugers Arch. 1986 Nov;407(5):493-9 PMID: 2431383
  5. Properties of single potassium channels modulated by glucose in rat pancreatic beta-cells.
    J Physiol. 1988 Jun;400:501-27 PMID: 2458459
  6. Biophysical properties of gap junctions between freshly dispersed pairs of mouse pancreatic beta cells.
    Biophys J. 1991 Jan;59(1):76-92 PMID: 2015391
  7. Glucose induces temperature-dependent oscillations of cytoplasmic Ca2+ in single pancreatic beta-cells related to their electrical activity.
    Cell Calcium. 1990 Jun-Jul;11(6):413-8 PMID: 2203530
  8. Simultaneous recordings of glucose dependent electrical activity and ATP-regulated K(+)-currents in isolated mouse pancreatic beta-cells.
    FEBS Lett. 1990 Feb 12;261(1):187-90 PMID: 2407553
  9. Calcium and delayed potassium currents in mouse pancreatic beta-cells under voltage-clamp conditions.
    J Physiol. 1986 May;374:531-50 PMID: 2427706
  10. Interaction of diazoxide, tolbutamide and ATP4- on nucleotide-dependent K+ channels in an insulin-secreting cell line.
    J Membr Biol. 1987;99(3):215-24 PMID: 2447283
  11. Electrophysiology of the pancreatic beta-cell.
    Prog Biophys Mol Biol. 1989;54(2):87-143 PMID: 2484976
  12. Antidiabetic sulfonylureas: localization of binding sites in the brain and effects on the hyperpolarization induced by anoxia in hippocampal slices.
    Brain Res. 1989 May 1;486(1):159-64 PMID: 2497930
  13. Glucose-induced oscillations of intracellular Ca2+ concentration resembling bursting electrical activity in single mouse islets of Langerhans.
    FEBS Lett. 1989 Dec 18;259(1):19-23 PMID: 2689228
  14. Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion.
    Physiol Rev. 1987 Oct;67(4):1185-248 PMID: 2825225
  15. Effects of sulphonylureas and diazoxide on insulin secretion and nucleotide-sensitive channels in an insulin-secreting cell line.
    Br J Pharmacol. 1988 Sep;95(1):83-94 PMID: 3146398
  16. Dual effect of glucose on cytoplasmic Ca2+ in single pancreatic beta-cells.
    Biochem Biophys Res Commun. 1988 Jan 15;150(1):419-25 PMID: 3276310
  17. Heterogeneity and contact-dependent regulation of hormone secretion by individual B cells.
    Exp Cell Res. 1986 Feb;162(2):507-20 PMID: 3510882
  18. A new generation of Ca2+ indicators with greatly improved fluorescence properties.
    J Biol Chem. 1985 Mar 25;260(6):3440-50 PMID: 3838314
  19. The preparation of, and studies on, free cell suspensions from mouse pancreatic islets.
    Diabetologia. 1974 Oct;10(5):431-8 PMID: 4375640
  20. Intracellular ATP directly blocks K+ channels in pancreatic B-cells.
    Nature. 1984 Sep 20-26;311(5983):271-3 PMID: 6090930
  21. Inositol 1,4,5-trisphosphate mobilizes intracellular Ca2+ from permeabilized insulin-secreting cells.
    Biochem J. 1984 Oct 15;223(2):467-73 PMID: 6093775
  22. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  23. Direct communication of homologous and heterologous endocrine islet cells in culture.
    J Cell Biol. 1982 Jan;92(1):221-6 PMID: 7035468
  24. The mechanism of early contractile failure of isolated rat ventricular myocytes subjected to complete metabolic inhibition.
    J Physiol. 1989 Jun;413:329-49 PMID: 2600854
  25. Localization and heterogeneity of agonist-induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura-2.
    EMBO J. 1989 Feb;8(2):401-11 PMID: 2721487
  26. Properties and calcium-dependent inactivation of calcium currents in cultured mouse pancreatic B-cells.
    J Physiol. 1988 Oct;404:731-47 PMID: 2855352
  27. Glucose-induced early changes in cytoplasmic calcium of pancreatic beta-cells studied with time-sharing dual-wavelength fluorometry.
    J Biol Chem. 1988 Apr 15;263(11):5044-8 PMID: 3281934
  28. Glucose-induced accumulation of inositol trisphosphates in isolated pancreatic islets. Predominance of the 1,3,4-isomer.
    Biochem J. 1986 Jul 1;237(1):259-63 PMID: 3541896
  29. Electrical activity in pancreatic islet cells.
    Nature. 1968 Jul 27;219(5152):389-90 PMID: 4873864
  30. Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells.
    Nature. 1984 Nov 29-Dec 5;312(5993):446-8 PMID: 6095103
  31. A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine.
    J Physiol. 1982 Oct;331:577-97 PMID: 6296371
  32. Cyclic changes in potential and resistance of the beta-cell membrane induced by glucose in islets of Langerhans from mouse.
    J Physiol. 1978 May;278:117-39 PMID: 353252
  33. Electrophysiological evidence for coupling between beta cells of pancreatic islets.
    Nature. 1976 Aug 5;262(5568):502-4 PMID: 785280
  34. Mechanism of potassium efflux and action potential shortening during ischaemia in isolated mammalian cardiac muscle.
    J Physiol. 1990 Dec;431:713-41 PMID: 2129231
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
1992-09-00
Pages
173-86
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1175638
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com