Skip to main content
Log in

Modulation of the frequency of glucose-dependent bursts of electrical activity by HCO3/CO2 in rodent pancreatic B-cells: experimental and theoretical results

  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

The burst pattern of electrical activity recorded from pancreatic B-cells in response to 11 mM glucose shows a large islet to islet variability. The relationship between burst frequency and glucose sensing (the threshold for electrical activity and the graded increase in electrical response to glucose, i.e. active phase %) has not been investigated within the same islet. In this work, we show that low HCO3 (5 mM) Hepes buffered solutions reversibly reduce the frequency of bursts compared to control (25 mM) HCO3 buffered solutions in the same islet. There was no change in the threshold or active phase (%). Using the mathematical model of Sherman et al. 1988, we explored mechanisms for a change in frequency independent of a change in active phase (%). Increased exchangeable calcium pool size and increased cell to cell coupling were the two theoretical treatments which could reproduce the experimental data. We conclude that burst frequency can be modulated independent of the active phase and that alteration of a calcium pool size best fits the experimental data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atwater I, Beigelman PM (1976) Dynamic characteristics of electrical activity in pancreatic beta-cells: I. Effects of calcium and magnesium removal. J Physiol (Paris) 72:769–786

    Google Scholar 

  • Atwater I, Rinzel J (1986) The B-cell bursting pattern and intracellular calcium. In: Latorre R (ed) Ionic channels in cells and model systems. Plenum Press, New York, pp 353–362

    Google Scholar 

  • Atwater I, Ribalet B, Rojas E (1978) Cyclic changes in potential and resistance of the B-cell membrane induced by glucose in islets of Langerhans from mouse. J Physiol 278:117–139

    Google Scholar 

  • Atwater I, Dawson CM, Scott AM, Eddlestone G, Rojas E (1980) The nature of the oscillatory behavior in electrical activity from pancreatic B-cell. Horm Metab Res 10:100–107

    Google Scholar 

  • Atwater I, Rosario LM, Rojas E (1983) Properties of the Ca-activated K+ channel in pancreatic beta-cells. Cell Calcium 4:451–461

    Google Scholar 

  • Beigelman PM, Ribalet B, Atwater I (1977) Electrical activity of mouse pancreatic beta-cells. II. Effects of glucose and arginine. J Physiol (Paris) 73:201–217

    Google Scholar 

  • Carroll PB, Li M-X, Rojas E, Atwater I (1988) The ATP-sensitive potassium channel in pancreatic B-cells is inhibited in physiological bicarbonate buffer. FEBS Lett 234:208–212

    Google Scholar 

  • Chay TR (1985) Glucose response to bursting-spiking pancreatic B-cells by a barrier kinetic model. Biol Cybern 52:339–349

    Google Scholar 

  • Chay TR, Kang HS (1988) Role of single-channel stochastic noise on bursting clusters of pancreatic B-cells. Biophys J 54:427–435

    Google Scholar 

  • Chay TR, Keizer J (1983) Minimal model for membrane oscillations in the pancreatic B-cell. Biophys J 42:181–190

    Google Scholar 

  • Cook DL, Perara E (1982) Islet electrical pacemaker response to alpha adrenergic stimulation. Diabetes31:985–990

    Google Scholar 

  • Cook DL, Crill WE, Porte D (1981) Glucose and acetylcholine have different effects on the plateau pacemaker of pancreatic islet cells. Diabetes 30:558–561

    Google Scholar 

  • Dean PM, Matthews EK (1970) Glucose-induced electrical activity in pancreatic islet cells. J Physiol (London) 210:255–264

    Google Scholar 

  • Eddlestone GT, Goncalves A, Bangham JA, Rojas E (1984) Electrical coupling between B-cells in islets of Langerhans from mouse. J Membr Biol 77:1–14

    Google Scholar 

  • Frankel BJ, Imagawa WT O'Connor DL, Lundquist I, Kromhout JA, Fanska RE, Grodsky GM (1978) Glucose-stimulated 45Calcium efflux from isolated rat pancreatic islets. J Clin Invest 62:525–531

    Google Scholar 

  • Gillis K, Tabcharani J, Hammoud A, Misler S (1988) Effects of ammonium chloride (NH4Cl) and sodium proprionate (NaPr) on the activity of a metabolite regulated K+ channel in rat pancreatic islet and RIN insulinoma cells. Biophys J 53:550a

    Google Scholar 

  • Henquin J-C, Lambert AE (1976) Bicarbonate modulation of glucose-induced biphasic insulin release by rat islets. Am J Physiol 231:713–721

    Google Scholar 

  • Himmel DM, Chay TR (1987) Theoretical studies on the electrical activity of pancreatic B-cells as a function of glucose. Biophys J 51:89–107

    Google Scholar 

  • Keizer JE (1988) Electrical activity and insulin release in pancreatic beta-cells. Math Biosci 90:127–138

    Google Scholar 

  • Lea TJ (1986) A comparison of the abilities of CO2/HCO3 protonophores, and changes in solution pH to release Ca2+ from the S.R. of barnacle myofibrillar bundles. Pflügers Arch 406:315–322

    Google Scholar 

  • Lindstrom P, Sehlin J (1986) Effect of intracellular alkalinization on pancreatic islet calcium uptake and insulin secretion. Biochem J 239:199–204

    Google Scholar 

  • Malaisse-Lagae F, Malaisse WJ (1971) The stimulus secretion coupling of glucose induced insulin secretion III. Uptake of 45Ca by isolated islets of Langerhans. Endocrinology 88:72–80

    Google Scholar 

  • Martiel J-L, Goldbeter A (1987) A model based on receptor densensitization for cAMP signalling in Dictyostelium cells. Biophys J 52:807–828

    Google Scholar 

  • Meda P, Atwater I, Goncalves A, Bangham JA, Orci L, Rojas E (1984) The topography of electrical synchrony among B-cells in the mouse islet of Langerhans. Q J Exp Physiol 69:719–735

    Google Scholar 

  • Meda P, Santos RM, Atwater I (1986) Direct identification of electrophysiologically monitored cells within intact mouse islets of Langerhans. Diabetes 35:232–236

    Google Scholar 

  • Meissner HP, Schmeltz H (1974) Membrane potential of Beta cells in pancreatic islets. Pflügers Arch 351:195–206

    Google Scholar 

  • Nassar V, Pollard HB, Rojas E (1988) Electrical activity in adrenal chromaffin cells of intact mouse adrenal gland. Am J Physiol 254:C675-C683

    Google Scholar 

  • Nordman JJ, Stuenkel EL (1986) Electrical properties of axons and neuro-hypophyseal nerve terminals and their relationship to secretion in the rat. J Physiol 380:521–539

    Google Scholar 

  • Perez-Armendariz EM, Spray DC, Bennett MVL (1988) Properties of gap junctions between pairs of pancreatic beta-cells of mice. Biophys J 53:53a

    Google Scholar 

  • Rinzel J, Chay TR, Himmel D, Atwater I (1986) Prediction of the glucose-induced changes in membrane ionic permeability and cytosolic Ca2+ by mathematical modeling. In: Atwater I, Rojas E, Soria B (eds) Biophysics of the pancreatic B-cell. Plenum Press, New York, pp 247–263

    Google Scholar 

  • Rorsman P, Trube G (1986) Calcium and delayed potassium currents in mouse pancreatic B-cells under voltage clamp conditions. J Physiol 374:531–550

    Google Scholar 

  • Rosario LM, Atwater I, Rojas E (1985) Membrane potential measurements in islets of Langerhans from ob/ob obese mice suggest an alteration in [Ca]2+-activated K+ permeability. Q J Exp Physiol 70:137–150

    Google Scholar 

  • Scott AM, Atwater I, Rojas E (1981) A method for the simultaneous measurement of insulin release and B-cell membrane potential in single mouse islets of Langerhans. Diabetologia 21:470–475

    Google Scholar 

  • Sherman A, Rinzel J, Keizer J (1988) Emergence of organized bursting in clusters of pancreatic B-cells by channel sharing. Biophys J 54:411–425

    Google Scholar 

  • Spray D, Bennett MVL (1985) Physiology and pharmacology of gap junctions. Ann Rev Physiol 47:281–303

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Offprint requests to: P. B. Carroll

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carroll, P.B., Sherman, A., Ferrer, R. et al. Modulation of the frequency of glucose-dependent bursts of electrical activity by HCO3/CO2 in rodent pancreatic B-cells: experimental and theoretical results. Eur Biophys J 18, 71–77 (1990). https://doi.org/10.1007/BF00183265

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00183265

Key words

Navigation