Home LiteratureArticle Details
PMID: 8735691 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

In vivo synchronous membrane potential oscillations in mouse pancreatic beta-cells: lack of co-ordination between islets.

The Journal of physiology ·Vol. 493 ( Pt 1) ·1996-05-15 ·Pages 9-18

Valdeolmillos M, Gomis A, Sánchez-Andrés JV

Abstract

1. The properties of the oscillations in electrical activity of different beta-cells within the same islet of Langerhans, and of different islets within the same pancreas, recorded in vivo, are described. 2. Simultaneous recordings of two cells within the same islet showed that the oscillations were synchronous. A rapid increase in blood glucose led to the simultaneous appearance of a transitory phase of continuous electrical activity in both cells. These results indicate that under physiological conditions, the islets operate as a functional syncytium. 3. Simultaneous recordings of cells from two different islets within the same pancreas showed that the oscillations in the electrical activity were not synchronous, which suggests that each islet is a functionally independent unit. Rapid changes in blood glucose led to the appearance of a transitory phase of increased electrical activity in both islets, although of different duration. These results suggest that the endocrine pancreas lacks a pacemaker driving the electrical activity of all the islets. 4. The comparison of the degree of activation of different islets, simultaneously recorded at different glucose concentrations, indicated that all the islets had a similar sensitivity to glucose. Furthermore, when the glucose concentration was increased, the electrical activity in both islets increased in parallel, suggesting that the amount of insulin released due to the increase in glycaemia was produced by the simultaneous response of all the islets and not by the recruitment of islets with different sensitivities to glucose. 5. Our results predict that the synchronous electrical activity of all the cells within an islet will result in widespread intracellular calcium oscillations and pulsatile insulin secretion. The periodicity of the pulses of insulin secretion in different islets is suggested to be of slightly different length and asynchronous.

MeSH Terms
Animals Blood Glucose/metabolism Electrophysiology Insulin/metabolism Insulin Secretion Islets of Langerhans/cytology,metabolism Membrane Potentials/physiology Mice Mice, Inbred Strains
Chemicals
Blood Glucose Insulin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Valdeolmillos M
Departamento de Fisiología, Facultad de Medicina, Universidad de Alicante, Spain.
Gomis A
Sánchez-Andrés J V
References (24)
24 references, click to expand
  1. Biophysical properties of gap junctions between freshly dispersed pairs of mouse pancreatic beta cells.
    Biophys J. 1991 Jan;59(1):76-92 PMID: 2015391
  2. Three types of cytoplasmic Ca2+ oscillations in stimulated pancreatic beta-cells.
    Arch Biochem Biophys. 1989 Jan;268(1):404-7 PMID: 2536264
  3. Functional subpopulations of individual pancreatic B-cells in culture.
    Endocrinology. 1991 Jun;128(6):3193-8 PMID: 2036985
  4. Widespread synchronous [Ca2+]i oscillations due to bursting electrical activity in single pancreatic islets.
    Pflugers Arch. 1991 May;418(4):417-22 PMID: 1876486
  5. Heterogeneous changes in [Ca2+]i induced by glucose, tolbutamide and K+ in single rat pancreatic B cells.
    Cell Calcium. 1991 Sep;12(8):577-86 PMID: 1954649
  6. Heterogeneity in pancreatic beta-cell population.
    Diabetes. 1992 Jul;41(7):777-81 PMID: 1612191
  7. Influence of membrane potential changes on cytoplasmic Ca2+ concentration in an electrically excitable cell, the insulin-secreting pancreatic B-cell.
    J Biol Chem. 1992 Oct 15;267(29):20713-20 PMID: 1400388
  8. The relationship between glucose-induced K+ATP channel closure and the rise in [Ca2+]i in single mouse pancreatic beta-cells.
    J Physiol. 1992 Sep;455:173-86 PMID: 1484353
  9. Fluorescence digital image analysis of glucose-induced [Ca2+]i oscillations in mouse pancreatic islets of Langerhans.
    Diabetes. 1993 Aug;42(8):1210-4 PMID: 8325454
  10. Heterogeneity in glucose sensitivity among pancreatic beta-cells is correlated to differences in glucose phosphorylation rather than glucose transport.
    EMBO J. 1993 Jul;12(7):2873-9 PMID: 8335003
  11. Oscillations of secretion driven by oscillations of cytoplasmic Ca2+ as evidences in single pancreatic islets.
    J Biol Chem. 1993 Oct 25;268(30):22265-8 PMID: 8226733
  12. Immunocytochemical and ultrastructural heterogeneities of normal and glibenclamide stimulated pancreatic beta cells in the rat.
    Virchows Arch. 1994;425(3):305-13 PMID: 7812517
  13. Slow and fast oscillations of cytoplasmic Ca2+ in pancreatic islets correspond to pulsatile insulin release.
    Am J Physiol. 1995 Feb;268(2 Pt 1):E282-7 PMID: 7864105
  14. The electrical activity of mouse pancreatic beta-cells recorded in vivo shows glucose-dependent oscillations.
    J Physiol. 1995 Jul 1;486 ( Pt 1):223-8 PMID: 7562637
  15. Electrophysiological evidence for coupling between beta cells of pancreatic islets.
    Nature. 1976 Aug 5;262(5568):502-4 PMID: 785280
  16. Cyclic oscillations of basal plasma glucose and insulin concentrations in human beings.
    N Engl J Med. 1979 Nov 8;301(19):1023-7 PMID: 386121
  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. Greater in vivo than in vitro pulsatility of insulin secretion with synchronized insulin and somatostatin secretory pulses.
    Endocrinology. 1987 Jun;120(6):2272-8 PMID: 2883001
  19. Stimulation of insulin secretion reveals heterogeneity of pancreatic B cells in vivo.
    J Clin Invest. 1987 Jul;80(1):175-83 PMID: 3110211
  20. Glucose-evoked changes in [K+] and [Ca2+] in the intercellular spaces of the mouse islet of Langerhans.
    Adv Exp Med Biol. 1986;211:31-51 PMID: 3300189
  21. Pulsatile insulin release and electrical activity from single ob/ob mouse islets of Langerhans.
    Adv Exp Med Biol. 1986;211:413-25 PMID: 3300197
  22. Impaired pulsatile secretion of insulin in relatives of patients with non-insulin-dependent diabetes.
    N Engl J Med. 1988 May 12;318(19):1225-30 PMID: 3283553
  23. Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells.
    Proc Natl Acad Sci U S A. 1988 Jun;85(11):3865-9 PMID: 3287379
  24. Electrophysiology of the pancreatic beta-cell.
    Prog Biophys Mol Biol. 1989;54(2):87-143 PMID: 2484976
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
1996-05-15
Pages
9-18
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1158947
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: [email protected]