Skip to main content

Electrical, Calcium, and Metabolic Oscillations in Pancreatic Islets

  • Reference work entry
  • First Online:
Book cover Islets of Langerhans

Abstract

Oscillations are an integral part of insulin secretion and are due ultimately to oscillations in the electrical activity of pancreatic β-cells, called bursting. We discuss the underlying mechanisms for bursting oscillations in mouse islets and the parallel oscillations in intracellular calcium and metabolism. We present a unified biophysical model, called the dual oscillator model, in which fast electrical oscillations are due to the feedback of Ca2+ onto K+ ion channels and the slow component is due to oscillations in glycolysis. The combination of these mechanisms can produce the wide variety of bursting and Ca2+ oscillations observed in islets , including fast, slow, compound, and accordion bursting. We close with a description of recent experimental studies that have tested unintuitive predictions of the model and have thereby provided the best evidence to date that oscillations in glycolysis underlie the slow (~5 min) component of electrical, calcium, and metabolic oscillations in mouse islets.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 699.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 549.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ainscow EK, Rutter GA (2002) Glucose-stimulated oscillations in free cytosolic ATP concentration imaged in single islet β-cells. Diabetes 51:S162–S170

    Article  PubMed  CAS  Google Scholar 

  • Ämmälä C, Ashcroft FM, Rorsman P (1993) Calcium-independent potentiation of insulin release by cyclic AMP in single β-cells. Nature 363:356–358

    Article  PubMed  Google Scholar 

  • Arden C, Hampson LJ, Huang GC, Shaw JAM, Aldibbiat A, Holliman G, Manas D, Khan S, Lange AJ, Agius L (2008) A role for PFK-2/FBPase-2, as distinct from fructose 2,6-bisphosphate, in regulation of insulin secretion in pancreatic β-cells. Biochem J 411:41–51

    Article  PubMed  CAS  Google Scholar 

  • Arredouani A, Henquin J-C, Gilon P (2002) Contribution of the endoplasmic reticulum to the glucose-induced [Ca2+]c response in mouse pancreatic islets. Am J Physiol 282:E982–E991

    Article  CAS  Google Scholar 

  • Ashcroft FM, Harrison DE, Ashcroft SJH (1984) Glucose induces closure of single potassium channels in isolated rat pancreatic β-cells. Nature 312:446–448

    Article  PubMed  CAS  Google Scholar 

  • Banaszynski LA, Chen L-C, Maynard-Smith LA, Ooi AGL, Wandless TJ (2006) A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules. Cell 126:995–1004

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Beauvois MC, Merezak C, Jonas J-C, Ravier MA, Henquin J-C (2006) Glucose-induced mixed [Ca2+]c oscillations in mouse β-cells are controlled by the membrane potential and the SERCA3 Ca2+-ATPase of the endoplasmic reticulum. Am J Physiol 290:C1503–C1511

    Article  CAS  Google Scholar 

  • Beigelman PM, Ribalet B (1980) β-cell electrical activity in response to high glucose concentration. Diabetes 29:263–265

    Article  PubMed  CAS  Google Scholar 

  • Bergsten P (1995) Slow and fast oscillations of cytoplasmic Ca2+ in pancreatic islets correspond to pulsatile insulin release. Am J Physiol 268:E282–E287

    PubMed  CAS  Google Scholar 

  • Bergsten P (1998) Glucose-induced pulsatile insulin release from single islets at stable and oscillatory cytoplasmic Ca2+. Am J Physiol 274:E796–E800

    PubMed  CAS  Google Scholar 

  • Bergsten P, Hellman B (1993) Glucose-induced amplitude regulation of pulsatile insulin secretion from individual pancreatic islets. Diabetes 42:670–674

    Article  PubMed  CAS  Google Scholar 

  • Bergsten P, Grapengiesser E, Gylfe E, Tengholm A, Hellman B (1994) Synchronous oscillations of cytoplasmic Ca2+ and insulin release in glucose-stimulated pancreatic islets. J Biol Chem 269:8749–8753

    PubMed  CAS  Google Scholar 

  • Bergsten P, Westerlund J, Liss P, Carlsson P-O (2002) Primary in vivo oscillations of metabolism in the pancreas. Diabetes 51:699–703

    Article  PubMed  CAS  Google Scholar 

  • Bertram R, Arceo RC II (2008) A mathematical study of the differential effects of two SERCA isoforms on Ca2+ oscillations in pancreatic islets. Bull Math Biol 70:1251–1271

    Article  PubMed  Google Scholar 

  • Bertram R, Sherman A (2004a) A calcium-based phantom bursting model for pancreatic islets. Bull Math Biol 66:1313–1344

    Article  PubMed  CAS  Google Scholar 

  • Bertram R, Sherman A (2004b) Filtering of calcium transients by the endoplasmic reticulum in pancreatic β-cells. Biophys J 87:3775–3785

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bertram R, Satin L, Zhang M, Smolen P, Sherman A (2004) Calcium and glycolysis mediate multiple bursting modes in pancreatic islets. Biophys J 87:3074–3087

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bertram R, Satin LS, Pedersen MG, Luciani DS, Sherman A (2007a) Interaction of glycolysis and mitochondrial respiration in metabolic oscillations of pancreatic islets. Biophys J 92:1544–1555

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bertram R, Sherman A, Satin LS (2007b) Metabolic and electrical oscillations: partners in controlling pulsatile insulin secretion. Am J Physiol 293:E890–E900

    CAS  Google Scholar 

  • Cha CY, Nakamura Y, Himeno Y, Wang J, Fujimoto S, Inagaki N, Earm YE, Noma A (2011) Ionic mechanisms and Ca2+ dynamics underlying the glucose response of pancreatic β cells: a simulation study. J Gen Physiol 138:21–37

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chou H-F, Berman N, Ipp E (1992) Oscillations of lactate released from islets of Langerhans: evidence for oscillatory glycolysis in β-cells. Am J Physiol 262:E800–E805

    PubMed  CAS  Google Scholar 

  • Civelek VN, Deeney JT, Shalosky NJ, Tornheim K, Hansford RG, Prentki M, Corkey BE (1996) Regulation of pancreatic β-cell mitochondrial metabolism: influence of Ca2+, substrate and ADP. Biochem J 318:615–621

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cook DL (1983) Isolated islets of Langerhans have slow oscillations of electrical activity. Metabolism 32:681–685

    Article  PubMed  CAS  Google Scholar 

  • Dahlgren GM, Kauri LM, Kennedy RT (2005) Substrate effects on oscillations in metabolism, calcium and secretion in single mouse islets of Langerhans. Biochim Biophys Acta 1724:23–36

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Detimary P, Gilon P, Henquin JC (1998) Interplay between cytoplasmic Ca2+ and the ATP/ADP ratio: a feedback control mechanism in mouse pancreatic islets. Biochem J 333:269–274

    PubMed  CAS  PubMed Central  Google Scholar 

  • Diederichs F (2006) Mathematical simulation of membrane processes and metabolic fluxes of the pancreatic β-cell. Bull Math Biol 68:1779–1818

    Article  PubMed  CAS  Google Scholar 

  • Eaton RP, Allen RC, Schade DS (1983) Hepatic removal of insulin in normal man: dose response to endogenous insulin secretion. J Clin Endocrinol Metab 56:1294–1300

    Article  PubMed  CAS  Google Scholar 

  • Foe LG, Latshaw SP, Kemp RG (1983) Binding of hexose bisphosphates to muscle phosphofructokinase. Biochemistry 22:4601–4606

    Article  PubMed  CAS  Google Scholar 

  • Fridlyand LE, Tamarina N, Phillipson LH (2003) Modeling the Ca2+ flux in pancreatic β-cells: role of the plasma membrane and intracellular stores. Am J Physiol 285:E138–E154

    CAS  Google Scholar 

  • Gilon P, Shepherd RM, Henquin JC (1993) Oscillations of secretion driven by oscillations of cytoplasmic Ca2+ as evidenced in single pancreatic islets. J Biol Chem 268:22265–22268

    PubMed  CAS  Google Scholar 

  • Gilon P, Arredouani A, Gailly P, Gromada J, Henquin J-C (1999) Uptake and release of Ca2+ by the endoplasmic reticulum contribute to the oscillations of the cytosolic Ca2+ concentration triggered by Ca2+ influx in the electrically excitable pancreatic β-cell. J Biol Chem 274:20197–20205

    Article  PubMed  CAS  Google Scholar 

  • Goforth PB, Bertram R, Khan FA, Zhang M, Sherman A, Satin LS (2002) Calcium-activated K+ channels of mouse β-cells are controlled by both store and cytoplasmic Ca2+: experimental and theoretical studies. J Gen Physiol 114:759–769

    Google Scholar 

  • Goldbeter A, Lefever R (1972) Dissipative structures for an allosteric model; application to glycolytic oscillations. Biophys J 12:1302–1315

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Göpel SO, Kanno T, Barg S, Eliasson L, Galvanovskis J, Renström E, Rorsman P (1999) Activation of Ca2+-dependent K+ channels contributes to rhythmic firing of action potentials in mouse pancreatic β-cells. J Gen Physiol 114:759–769

    Article  PubMed  PubMed Central  Google Scholar 

  • Henquin JC (1990) Glucose-induced electrical activity in β-cells: feedback control of ATP-sensitive K+ channels by Ca2+? Diabetes 39:1457–1460

    Article  PubMed  CAS  Google Scholar 

  • Henquin JC, Meissner HP, Schmeer W (1982) Cyclic variations of glucose-induced electrical activity in pancreatic β cells. Pflugers Arch 393:322–327

    Article  PubMed  CAS  Google Scholar 

  • Higgins ER, Cannell MB, Sneyd J (2006) A buffering SERCA pump in models of calcium dynamics. Biophys J 91:151–163

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jung S-K, Aspinwall CA, Kennedy RT (1999) Detection of multiple patterns of oscillatory oxygen consumption in single mouse islets of Langerhans. Biochem Biophys Res Commun 259:331–335

    Article  PubMed  CAS  Google Scholar 

  • Jung S-K, Kauri LM, Qian W-J, Kennedy RT (2000) Correlated oscillations in glucose consumption, oxygen consumption, and intracellular free Ca2+ in single islets of Langerhans. J Biol Chem 275:6642–6650

    Article  PubMed  CAS  Google Scholar 

  • Juntti-Berggren L, Webb D-L, Arkhammar POG, Schultz V, Schweda EKH, Tornheim K, Berggren P-O (2003) Dihydroxyacetone-induced oscillations in cytoplasmic free Ca2+ and the ATP/ADP ratio in pancreatic β-cells at substimulatory glucose. J Biol Chem 278:40710–40716

    Article  PubMed  CAS  Google Scholar 

  • Keizer J, De Young G (1993) Effect of voltage-gated plasma membrane Ca2+ fluxes on IP3-linked Ca2+ oscillations. Cell Calcium 14:397–410

    Article  PubMed  CAS  Google Scholar 

  • Keizer J, Magnus G (1989) The ATP-sensitive potassium channel and bursting in the pancreatic β cell. Biophys J 56:229–242

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kennedy RT, Kauri LM, Dahlgren GM, Jung S-K (2002) Metabolic oscillations in β-cells. Diabetes 51:S152–S161

    Article  PubMed  CAS  Google Scholar 

  • Kindmark H, Köhler M, Brown G, Bränström R, Larsson O, Berggren P-O (2001) Glucose-induced oscillations in cytoplasmic free Ca2+ concentration precede oscillations in mitochondrial membrane potential in the pancreatic β-cell. J Biol Chem 276:34530–34536

    Article  PubMed  CAS  Google Scholar 

  • Krippeit-Drews P, Dufer M, Drews G (2000) Parallel oscillations of intracellular calcium activity and mitochondrial membrane potential in mouse pancreatic β-cells. Biochem Biophys Res Commun 267:179–183

    Article  PubMed  CAS  Google Scholar 

  • Kulkarni RN, Roper MG, Dahlgren GM, Shih DQ, Kauri LM, Peters JL, Stoffel M, Kennedy RT (2004) Islet secretory defect in insulin receptor substrate 1 null mice is linked with reduced calcium signaling and expression of sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA)-2b and −3. Diabetes 53:1517–1525

    Article  PubMed  CAS  Google Scholar 

  • Lang DA, Matthews DR, Burnett M, Turner RC (1981) Brief, irregular oscillations of basal plasma insulin and glucose concentrations in diabetic man. Diabetes 30:435–439

    Article  PubMed  CAS  Google Scholar 

  • Langer S, Kaminski MT, Lenzen S, Baltrusch S (2010) Endogenous activation of glucokinase by 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase is glucose dependent. Mol Endocrinol 24:1988–1997

    Article  PubMed  CAS  Google Scholar 

  • Longo EA, Tornheim K, Deeney JT, Varnum BA, Tillotson D, Prentki M, Corkey BE (1991) Oscillations in cytosolic free Ca2+, oxygen consumption, and insulin secretion in glucose-stimulated rat pancreatic islets. J Biol Chem 266:9314–9319

    PubMed  CAS  Google Scholar 

  • Luciani DS, Misler S, Polonsky KS (2006) Ca2+ controls slow NAD(P)H oscillations in glucose-stimulated mouse pancreatic islets. J Physiol 572:379–392

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • MacDonald MJ, Fahien LA, Buss JD, Hasan NM, Fallon MJ, Kendrick MA (2003) Citrate oscillates in liver and pancreatic β cell mitochondria and in INS-1 insulinoma cells. J Biol Chem 278:51894–51900

    Article  PubMed  CAS  Google Scholar 

  • Magnus G, Keizer J (1997) Minimal model of β-cell mitochondrial Ca2+ handling. Am J Physiol 273:C717–C733

    PubMed  CAS  Google Scholar 

  • Magnus G, Keizer J (1998) Model of β-cell mitochondrial calcium handling and electrical activity. I. Cytoplasmic variables. Am J Physiol 274:C1158–C1173

    PubMed  CAS  Google Scholar 

  • Malisse WJ, Malaisse-Lagae F, Sener A (1982) Glucose-induced accumulation of fructose-2,6-bisphosphate in pancreatic islets. Diabetes 31:90–93

    Article  Google Scholar 

  • Matthews DR, Lang DA, Burnett M, Turner RC (1983) Control of pulsatile insulin secretion in man. Diabetologia 24:231–237

    Article  PubMed  CAS  Google Scholar 

  • Matveyenko AV, Veldhuis JD, Butler PC (2008) Measurement of pulsatile insulin secretion in the rat: direct sampling from the hepatic portal vein. Am J Physiol 295:E569–E574

    CAS  Google Scholar 

  • Matveyenko AV, Liuwantara D, Gurlo T, Kirakossian D, Dalla Man C, Cobelli C, White MF, Copps KD, Volpi E, Fujita S, Butler PC (2012) Pulsatile portal vein insulin delivery enhances hepatic insulin action and signaling. Diabetes 61:2269–2279

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Meier JJ, Veldhuis JD, Butler PC (2005) Pulsatile insulin secretion dictates systemic insulin delivery by regulating hepatic insulin extraction in humans. Diabetes 54:1649–1656

    Article  PubMed  CAS  Google Scholar 

  • Meissner HP, Schmelz H (1974) Membrane potential of β-cells in pancreatic islets. Pflugers Arch 351:195–206

    Article  PubMed  CAS  Google Scholar 

  • Merrins MJ, Fendler B, Zhang M, Sherman A, Bertram R, Satin LS (2010) Metabolic oscillations in pancreatic islets depend on the intracellular Ca2+ level but not Ca2+ oscillations. Biophys J 99:76–84

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Merrins MJ, Bertram R, Sherman A, Satin LS (2012) Phosphofructo-2-kinase/fructose-2,6-bisphosphatase modulates oscillations of pancreatic islet metabolism. PLoS One 7(4):e34036

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nilsson T, Schultz V, Berggren P-O, Corkey BE, Tornheim K (1996) Temporal patterns of changes in ATP/ADP ratio, glucose 6-phosphate and cytoplasmic free Ca2+ in glucose-stimulated pancreatic β-cells. Biochem J 314:91–94

    PubMed  CAS  PubMed Central  Google Scholar 

  • Nunemaker CS, Zhang M, Wasserman DH, McGuinness OP, Powers AC, Bertram R, Sherman A, Satin LS (2005) Individual mice can be distinguished by the period of their islet calcium oscillations: is there an intrinsic islet period that is imprinted in vivo? Diabetes 54:3517–3522

    Article  PubMed  CAS  Google Scholar 

  • Nunemaker CS, Bertram R, Sherman A, Tsaneva-Atanasova K, Daniel CR, Satin LS (2006) Glucose modulates [Ca2+]i oscillations in pancreatic islets via ionic and glycolytic mechanisms. Biophys J 91:2082–2096

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • O’Rahilly S, Turner RC, Matthews DR (1988) Impaired pulsatile secretion of insulin in relatives of patients with non-insulin-dependent diabetes. N Engl J Med 318:1225–1230

    Article  PubMed  Google Scholar 

  • Ortsäter H, Liss P, Lund PE, Åkerman KEO, Bergsten P (2000) Oscillations in oxygen tension and insulin release of individual pancreatic ob/ob mouse islets. Diabetologia 43:1313–1318

    Article  PubMed  Google Scholar 

  • Polonsky KS, Jaspan J, Emmanouel D, Holmes K, Moossa AR (1983) Differences in the hepatic and renal extraction of insulin and glucagon in the dog: evidence for saturability of insulin metabolism. Acta Endocrinol (Copenh) 102:420–427

    CAS  Google Scholar 

  • Polonsky KS, Given BD, Hirsch LJ, Tillil H, Shapiro ET, Beebe C, Frank BH, Galloway JA, van Cauter E (1988) Abnormal patterns of insulin secretion in non-insulin-dependent diabetes mellitus. N Engl J Med 318:1231–1239

    Article  PubMed  CAS  Google Scholar 

  • Pørksen N (2002) The in vivo regulation of pulsatile insulin secretion. Diabetologia 45:3–20

    Article  PubMed  Google Scholar 

  • Pørksen N, Munn S, Steers J, Vore S, Veldhuis J, Butler P (1995) Pulsatile insulin secretion accounts for 70 % of total insulin secretion during fasting. Am J Physiol 269:E478–E488

    PubMed  Google Scholar 

  • Pørksen N, Nyholm B, Veldhuis JD, Butler PC, Schmitz O (1997) In humans at least 75 % of insulin secretion arises from punctuated insulin secretory bursts. Am J Physiol 273:E908–E914

    PubMed  Google Scholar 

  • Ravier MA, Daro D, Roma LP, Jonas JC, Cheng-Xue R, Schuit FC, Gilon P (2011) Mechanisms of control of the free Ca2+ concentration in the endoplasmic reticulum of mouse pancreatic β-cells: interplay with cell metabolism and [Ca2+]c and role of SERCA2β and SERCA3. Diabetes 60:2533–2545

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ren J, Sherman A, Bertram R, Goforth PB, Nunemaker CS, Waters CD, Satin LS (2013) Slow oscillations of KATP conductance in mouse pancreatic islets provide support for electrical bursting driven by metabolic oscillations. Am J Physiol 305:E805–E817

    CAS  Google Scholar 

  • Ristow M, Vorgerd M, Möhlig M, Schatz H, Pfeiffer A (1997) Deficiency of phosphofructo-1-kinase/muscle subtype in humans impairs insulin secretion and causes insulin resistance. J Clin Invest 100:2833–2841

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ristow M, Carlqvist H, Hebinck J, Vorgerd M, Krone W, Pfeiffer A, Muller-Wieland D, Ostenson CG (1999) Deficiency of phosphofructo-1-kinase/muscle subtype in humans is associated with impairment of insulin secretory oscillations. Diabetes 48:1557–1561

    Article  PubMed  CAS  Google Scholar 

  • Ritzel RA, Veldhuis JD, Butler PC (2006) The mass, but not the frequency, of insulin secretory bursts in isolated human islets is entrained by oscillatory glucose exposure. Am J Physiol 290:E750–E756

    CAS  Google Scholar 

  • Sakurai T, Johnson JH, Uyeda K (1996) Islet fructose 6-phosphate, 2-kinase: fructose 2,6-bisphosphatase: isozymic form, expression, and characterization. Biochem Biophys Res Commun 218:159–163

    Article  PubMed  CAS  Google Scholar 

  • Santos RM, Rosario LM, Nadal A, Garcia-Sancho J, Soria B, Valdeolmillos M (1991) Widespread synchronous [Ca2+]i oscillations due to bursting electrical activity in single pancreatic islets. Pflugers Arch 418:417–422

    Article  PubMed  CAS  Google Scholar 

  • Sel’kov EE (1968) Self-oscillations in glycolysis: a simple kinetic model. Eur J Biochem 4:79–86

    Article  PubMed  Google Scholar 

  • Sener A, Van Schaftingen E, Van de Winkel M, Pipeleers DG, Malaisse-Lagae F, Malaisse WJ, Hers HG (1984) Effects of glucose and glucagon on the fructose 2,6-bisphosphate content of pancreatic islets and purified pancreatic β-cells. Biochem J 221:759–764

    PubMed  CAS  PubMed Central  Google Scholar 

  • Smolen P (1995) A model for glycolytic oscillations based on skeletal muscle phosphofructokinase kinetics. J Theor Biol 174:137–148

    Article  PubMed  CAS  Google Scholar 

  • Smolen P, Keizer J (1992) Slow voltage inactivation of Ca2+ currents and bursting mechanisms for the mouse pancreatic β-cell. J Membr Biol 127:9–19

    Article  PubMed  CAS  Google Scholar 

  • Song SH, McIntyre SS, Shah H, Veldhuis JD, Hayes PC, Butler PC (2000) Direct measurement of pulsatile insulin secretion from the portal vein in human subjects. J Clin Endocrinol Metab 85:4491–4499

    PubMed  CAS  Google Scholar 

  • Stagner JI, Samols E, Weir GC (1980) Sustained oscillations of insulin, glucagon, and somatostatin from the isolated canine pancreas during exposure to a constant glucose concentration. J Clin Invest 65:939–942

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tornheim K (1979) Oscillations of the glycolytic pathway and the purine nucleotide cycle. J Theor Biol 79:491–541

    Article  PubMed  CAS  Google Scholar 

  • Tornheim K (1997) Are metabolic oscillations responsible for normal oscillatory insulin secretion? Diabetes 46:1375–1380

    Article  PubMed  CAS  Google Scholar 

  • Tornheim K, Lowenstein JM (1974) The purine nucleotide cycle: IV. Interactions with oscillations of the glycolytic pathway in muscle extracts. J Biol Chem 249:3241–3247

    PubMed  CAS  Google Scholar 

  • Tornheim K, Andrés V, Schultz V (1991) Modulation by citrate of glycolytic oscillations in skeletal muscle extracts. J Biol Chem 266:15675–15678

    PubMed  CAS  Google Scholar 

  • Valdeolmillos M, Santos RM, Contreras D, Soria B, Rosario LM (1989) Glucose-induced oscillations of intracellular Ca2+ concentration resembling electrical activity in single mouse islets of Langerhans. FEBS Lett 259:19–23

    Article  PubMed  CAS  Google Scholar 

  • Watts M, Fendler B, Merrins MJ, Satin LS, Bertram R (2014) Calcium and Metabolic Oscillations in Pancreatic Islets: Who's Driving the Bus? SIAM J Appl Dyn Syst 13:683–703

    Article  Google Scholar 

  • Weigle DS (1987) Pulsatile secretion of fuel-regulatory hormones. Diabetes 36:764–775

    Article  PubMed  CAS  Google Scholar 

  • Westermark PO, Lansner A (2003) A model of phosphofructokinase and glycolytic oscillations in the pancreatic β-cell. Biophys J 85:126–139

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wierschem K, Bertram R (2004) Complex bursting in pancreatic islets: a potential glycolytic mechanism. J Theor Biol 228:513–521

    Article  PubMed  CAS  Google Scholar 

  • Yaney GC, Schultz V, Cunningham BA, Dunaway GA, Corkey BE, Tornheim K (1995) Phosphofructokinase isozymes in pancreatic islets and clonal β-cells (INS-1). Diabetes 44:1285–1289

    Article  PubMed  CAS  Google Scholar 

  • Zhan X, Yang L, Ming Y, Jia Y (2008) RyR channels and glucose-regulated pancreatic β-cells. Eur Biophys J 37:773–782

    Article  PubMed  CAS  Google Scholar 

  • Zhang M, Goforth P, Sherman A, Bertram R, Satin L (2003) The Ca2+ dynamics of isolated mouse β-cells and islets: implications for mathematical models. Biophys J 84:2852–2870

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors thank Bernard Fendler, Pranay Goel, Matthew Merrins, Craig Nunemaker, Morten Gram Pedersen, Brad Peercy, and Min Zhang, who each collaborated on some of the work described herein. RB is supported by NIH grant DK80714. AS is supported by the Intramural Research Program of the NIH (NIDDK). LS is supported by NIH grant RO1 DK 46409.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard Bertram .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media Dordrecht

About this entry

Cite this entry

Bertram, R., Sherman, A., Satin, L.S. (2015). Electrical, Calcium, and Metabolic Oscillations in Pancreatic Islets. In: Islam, M. (eds) Islets of Langerhans. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6686-0_10

Download citation

Publish with us

Policies and ethics