Metabolic and electrical oscillations: Partners in controlling pulsatile insulin secretion

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 4, 2007, Pages

  Bertram, Richard ^a   Sherman, Arthur ^b   Satin, Leslie S ^c  

^a FLORIDA STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Diabetes; Mathematical model; Pancreatic cells

Indexed keywords

6 PHOSPHOFRUCTOKINASE;

CALCIUM CURRENT; CALCIUM SIGNALING; CELL FUNCTION; CELL MEMBRANE POTENTIAL; ENZYME ACTIVITY; ENZYME RELEASE; GLUCOSE BLOOD LEVEL; HUMAN; INSULIN BLOOD LEVEL; INSULIN RELEASE; MATHEMATICAL MODEL; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSCILLATION; PANCREAS ISLET CELL; PRIORITY JOURNAL; PULSATILE HORMONE RELEASE; SHORT SURVEY;

ANIMALS; BIOLOGICAL CLOCKS; CALCIUM SIGNALING; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; PULSATILE FLOW; TIME FACTORS;

EID: 35148816130     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00359.2007     Document Type: Short Survey

References (90)

1. Ainscow EK, Rutter GA. Glucose-stimulated oscillations in free cytosolic ATP concentration imaged in single islet beta-cells: evidence for a Ca2+-dependent mechanism. Diabetes 51, Suppl 1: S162-S170, 2002.
2. Ashcroft FM, Harrison DE, Ashcroft SJ. Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature 312: 446-448, 1984.
3. Aspinwall CA, Lakey JR, Kennedy RT. Insulin-stimulated insulin secretion in single pancreatic beta cells. J Biol Chem 274: 6360-6365, 1999.
4. 2+-ATPase of the endoplasmic reticulum. Am J Physiol Cell Physiol 290: C1503-C1511, 2006.
5. Beigelman PM, Ribalet B. Beta-cell electrical activity in response to high glucose concentration. Diabetes 29: 263-265, 1980.
6. 2+ in pancreatic islets correspond to pulsatile insulin release. Am J Physiol Endocrinol Metab 268: E282-E287, 1995.
7. 2+ and insulin release in glucose-stimulated pancreatic islets. J Biol Chem 269: 8749-8753, 1994.
8. Bergsten P, Hellman B. Glucose-induced amplitude regulation of pulsatile insulin secretion from individual pancreatic islets. Diabetes 42: 670-674, 1993.
9. Bergsten P, Westerlund J, Liss P, Carlsson PO. Primary in vivo oscillations of metabolism in the pancreas. Diabetes 51: 699-703, 2002.
10. Bertram R, Previte J, Sherman A, Kinard TA, Satin LS. The phantom burster model for pancreatic β-cells. Biophys J 79: 2880-2892, 2000.
11. Bertram R, Satin L, Zhang M, Smolen P, Sherman A. Calcium and glycolysis mediate multiple bursting modes in pancreatic islets. Biophys J 87: 3074-3087, 2004.
12. Bertram R, Satin LS, Pedersen MG, Luciani DS, Sherman A. Interaction of glycolysis and mitochondrial respiration in metabolic oscillations of pancreatic islets. Biophys J 92: 1544-1555, 2007.
13. Bertram R, Sherman A. A calcium-based phantom bursting model for pancreatic islets. Bull Math Biol 66: 1313-1344, 2004.
14. Bertram R, Sherman A. Filtering of calcium transients by the endoplasmic reticulum in pancreatic β-cells. Biophys J 87: 3775-3785, 2004.
15. Bertram R, Wierschem K, Zhang M, Goforth P, Sherman A, Satin L. Phantom bursting in pancreatic islets: A potential role for insulin feedback. Recent Res Devel Biophys 1: 31-51, 2002.
16. Chou HF, Berman N, Ipp E. Oscillations of lactate released from islets of Langerhans: evidence for oscillatory glycolysis in β-cells. Am J Physiol Endocrinol Metab 262: E800-E805, 1992.
17. Christesen HBT, Herold K, Noordam K, Gloyn AL. Glucokinase linked hypoglycemia. In: Glucokinase and Glycemic Disease: From Basics to Novel Therapeutics, edited by Matchinsky FM and Magnuson MA. Basel, Switzerland: Karger, 2004, p. 75-91.
18. 2+, substrate and ADP. Biochem J 318: 615-621, 1996.
19. Cook DL. Isolated islets of Langerhans have slow oscillations of electrical activity. Metabolism 32: 681-685, 1983.
20. + channels in pancreatic β-cells: spare-channel hypothesis. Diabetes 37: 495-498, 1988.
21. Dahlgren GM, Kauri LM, Kennedy RT. Substrate effects on oscillations in metabolism, calcium and secretion in single mouse islets of Langerhans. Biochim Biophys Acta 1724: 23-36, 2005.
22. Dean PM, Mathews EK. Glucose-induced electrical activity in pancreatic islet cells. J Physiol 210: 255-264, 1970.
23. 2+ and the ATP/ADP ratio: a feedback control mechanism in mouse pancreatic islets. Biochem J 333: 269-274, 1998.
24. Diederichs F. Mathematical simulation of membrane processes and metabolic fluxes of the pancreatic β-cell. Bull Math Biol 68: 1779-1818, 2006.
25. -/-- beta cells. Diabetologia 47: 488-498, 2004.
26. 2+ flux in pancreatic β-cells: role of the plasma membrane and intracellular stores. Am J Physiol Endocrinol Metab 285: E138-E154, 2003.
27. 2+ as evidenced in single pancreatic islets. J Biol Chem 268: 22265-22268, 1993.
28. Gloyn AL, Weedon MN, Owen KR, Turner MJ, Knight BA, Hitman G, Walker M, Levy JC, Sampson M, Halford S, McCarthy MI, Hattersley AT, Frayling TM. Large scale association studies of variants in genes encoding the pancreatic β-cell KATP channel subunits Kir6.2 (KCNJ11) and SUR1 (ABCC8) confirm that the KCNJ11 E23K variant is associated with type 2 diabetes. Diabetes 52: 568-572, 2003.
29. 2+: experimental and theoretical studies. J Gen Physiol 114: 759-769, 2002.
30. + channels contributes to rhythmic firing of action potentials in mouse pancreatic β cells. J Gen Physiol 114: 759-769, 1999.
31. -/-- mice. Diabetologia 48: 913-921, 2005.
32. Heart E, Corkey RF, Wikstrom JD, Shirihai OS, Corkey BE. Glucose-dependent increase in mitochondrial membrane potential, but not cytoplasmic calcium, correlates with insulin secretion in single islet cells. Am J Physiol Endocrinol Metab 290: E143-E148, 2006.
33. Heart E, Smith PJS. Rhythm of the β-cell oscillator is not governed by a single regulator: multiple systems contribute to oscillatory behavior. Am J Physiol Endocrinol Metab 292: E1295-E1300, 2007.
34. 2+ in the release of pancreatic islet hormones. Diabete Metab 20: 123-131, 1994.
35. Henquin JC. Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49: 1751-1760, 2000.
36. Henquin JC, Meissner HP, Schmeer W. Cyclic variations of glucose-induced electrical activity in pancreatic B cells. Pflügers Arch 393: 322-327, 1982.
37. Jung SK, Aspinwall CA, Kennedy RT. Detection of multiple patterns of oscillatory oxygen consumption in single mouse islets of Langerhans. Biochem Biophys Res Commun 259: 331-335, 1999.
38. 2+ in single islets of Langerhans. J Biol Chem 275: 6642-6650, 2000.
39. 2+ and the ATP/ADP ratio in pancreatic β-cells at substimulatory glucose. J Biol Chem 278: 40710-40716, 2003.
40. Kennedy RT, Kauri LM, Dahlgren GM, Jung SK. Metabolic oscillations in β-cells. Diabetes 51: S152-S161, 2002.
41. + channels in pancreatic β-cells through a phosphatidylinositol 3-kinase-dependent pathway. Diabetes 50: 2192-2198, 2001.
42. 2+ concentration precede oscillations in mitochondrial membrane potential in the pancreatic β-cell. J Biol Chem 276: 34530-34536, 2001.
43. ATP channels. Proc Natl Acad Sci USA 99: 16992-16997, 2002.
44. 2+-ATPase (SERCA)-2b and -3. Diabetes 53: 1517-1525, 2004.
45. i oscillations in mouse pancreatic islets by glucose, α-ketoisocaproic acid, glyceraldehyde and glycolytic intermediates. Biochim Biophys Acta 1523: 65-72, 2000.
46. 2+, oxygen consumption, and insulin secretion in glucose-stimulated rat pancreatic islets. J Biol Chem 266: 9314-9319, 1991.
47. 2+ controls slow NAD(P)H oscillations in glucose-stimulated mouse pancreatic islets. J Physiol 572: 379-392, 2006.
48. MacDonald MJ, Fahien LA, Buss JD, Hasan NM, Fallon MJ, Kendrick MA. Citrate oscillates in liver and pancreatic beta cell mitochondria and in INS-1 insulinoma cells. J Biol Chem 278: 51894-51900, 2003.
49. 2+ handling. Am J Physiol Cell Physiol 273: C717-C733, 1997.
50. Magnus G, Keizer J. Model of β-cell mitochondrial calcium handling and electrical activity. I. Cytoplasmic variables. Am J Physiol Cell Physiol 274: C1158-C1173, 1998.
51. i oscillations induced by ketoisocaproate in single mouse pancreatic islets. Diabetes 44: 300-305, 1995.
52. i oscillations in single mouse pancreatic islets of Langerhans. J Physiol 486: 361-371, 1995.
53. Matthews DR, Lang DA, Burnett M, Turner RC. Control of pulsatile insulin secretion in man. Diabetologia 24: 231-237, 1983.
54. Matthews DR, Naylor BA, Jones RG, Ward GM, Turner RC. Pulsatile insulin has greater hypoglycemic effect than continuous delivery. Diabetes: 617-621, 1983.
55. McCormack J, Longo EA, Corkey B. Glucose-induced activation of pyruvate dehydrogenase in isolated rat pancreatic islets. Biochem J 267: 527-530, 1990.
56. Meissner HP, Schmelz H. Membrane potential of beta-cells in pancreatic islets. Pflügers Arch 351: 195-206, 1974.
57. 2+ in glucose-stimulated pancreatic β-cells. Biochem J 314: 91-94, 1996.
58. i oscillations in pancreatic islets via ionic and glycolytic mechanisms. Biophys J 91: 2082-2096, 2006.
59. Nunemaker CS, Zhang M, Wasserman DH, McGuinness OP, Powers AC, Bertram R, Sherman A, Satin LS. 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, 2005.
60. O'Rahilly S, Turner RC, Matthews DR. Impaired pulsatile secretion of insulin in relatives of patients with non-insulin-dependent diabetes. N Engl J Med 318: 1225-1230, 1988.
61. Ortsäter H, Liss P, Lund PE, Åkerman KE, Bergsten P. Oscillations in oxygen tension and insulin release of individual pancreatic ob/ob mouse islets. Diabetologia 43: 1313-1318, 2000.
62. Pedersen MG. Phantom bursting is highly sensitive to noise and unlikely to account for slow bursting in β-cells: considerations in favor of metabolically driven oscillations. J Theor Biol. In press.
63. Pedersen MG, Bertram R, Sherman A. Intra- and inter-islet synchronization of metabolically driven insulin secretion. Biophys J 89: 107-119, 2005.
64. Polonsky KS, Given BD, Hirsch LJ, Tillil H, Shapiro ET, Beebe C, Frank BH, Galloway JA, van Cauter E. Abnormal patterns of insulin secretion in non-insulin-dependent diabetes mellitus. N Engl J Med 318: 1231-1239, 1988.
65. Pørksen N. The in vivo regulation of pulsatile insulin secretion. Diabetologia 45: 3-20, 2002.
66. Pørksen N, Munn S, Steers J, Vore S, Veldhuis J, Butler P. Pulsatile insulin secretion accounts for 70% of total insulin secretion during fasting. Am J Physiol Endocrinol Metab 269: E478-E488, 1995.
67. Ravier MA, Henquin JC. Time and amplitude regulation of pulsatile insulin secretion by triggering and amplifying pathways in mouse islets. FEBS Lett 530: 215-219, 2002.
68. Remedi MS, Rocheleau JV, Tong A, Patton BL, McDaniel ML, Piston DW, Koster JC, Nichols CG. Hyperinsulinism in mice with heterozygous loss of KATP channels. Diabetologia 49: 2368-2378, 2006.
69. Ristow M, Carlqvist H, Hebinck J, Vorgerd M, Krone W, Pfeiffer A, Muller-Wieland D, Ostenson CG. Deficiency of phosphofructo-1-kinase/muscle subtype in humans is associated with impairment of insulin secretory oscillations. Diabetes 48: 1557-1561, 1999.
70. Ritzel RA, Veldhuis JD, Butler PC. The mass, but not the frequency, of insulin secretory bursts in isolated human islets is entrained by oscillatory glucose exposure. Am J Physiol Endocrinol Metab 290: E750-E756, 2006.
71. ATP channel activity for regulated insulin secretion. PLoS Biol 4: e26, 2006.
72. Satin LS, Tavalin SJ, Smolen P. Calcium channel inactivation in HIT cells studied with an imposed burst waveform. Biophys J 66: 141-148, 1994.
73. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU, Prokunia-Olsson L, Ding CJ, Swift AJ, Narisu N, Hu T, Rruim R, Xiao-Yi L, Conneely KN, Riebow NL, Sprau AG, Tong M, White PP, Hetrick KN, Barnhart MW, Bark CW, Goldstein JL, Watkins L, Xiang F, Saramies J, Buchanan TA, Watanabe RM, Valle TT, Kinnunen L, Abscasis GR, Push EW, Doheny KF, Bergman RN, Tuomilehto J, Collins FS, Boehnke M. A genome wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316: 1341-1345, 2007.
74. Smolen P. A model for glycolytic oscillations based on skeletal muscle phosphofructokinase kinetics. J Theor Biol 174: 137-148, 1995.
75. Stagner JI, Samols E. Role of intrapancreatic ganglia in regulation of periodic insular secretions. Am J Physiol Endocrinol Metab 248: E522-E530, 1985.
76. Stagner JI, Samols E, Weir GC. 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, 1980.
77. + channels. J Biol Chem 282: 1747-1756, 2007.
78. Tornheim K. Are metabolic oscillations responsible for normal oscillatory insulin secretion? Diabetes 46: 1375-1380, 1997.
79. Tornheim K. Fructose 2,6-bisphosphate and glycolytic oscillations in skeletal muscle extracts. J Biol Chem 263: 2619-2624, 1988.
80. Tornheim K. Oscillations of the glycolytic pathway and the purine nucleotide cycle. J Theor Biol 79: 491-541, 1979.
81. Tornheim K, Andrés V, Schultz V. Modulation by citrate of glycolytic oscillations in skeletal muscle extracts. J Biol Chem 266: 15675-15678, 1991.
82. Tornheim K, Lowenstein JM. The purine nucleotide cycle. IV. Interactions with oscillations of the glycolytic pathway in muscle extracts. J Biol Chem 249: 3241-3247, 1974.
83. Tsaneva-Atanasova K, Zimliki CL, Bertram R, Sherman A. Diffusion of calcium and metabolites in pancreatic islets: killing oscillations with a pitchfork. Biophys J 90: 3434-3446, 2006.
84. Valdeolmillos M, Gomis A, Sánchez-Andrés JV. In vivo synchronous membrane potential oscillations in mouse pancreatic β-cells: lack of co-ordination between islets. J Physiol 493: 9-18, 1996.
85. 2+ concentration resembling electrical activity in single mouse islets of Langerhans. FEBS Lett 259: 19-23, 1989.
86. Vionnet N, Stoffel M, Takeda J, Yasuda K, Bell GI, Zouali H, Lesage S, Velho G, Iris F, Passa PH, Froguel PH, Cohen D. Nonsense mutation in the glucokinase gene causes early-onset non-insulin-dependent diabetes mellitus. Nature 256: 721-722, 1992.
87. Weigle DS. Pulsatile secretion of fuel-regulatory hormones. Diabetes 36: 764-775, 1987.
88. Westermark PO, Lansner A. A model of phosphofructokinase and glycolytic oscillations in the pancreatic β-cell. Biophys J 85: 126-139, 2003.
89. Yaney GC, Schultz V, Cunningham BA, Dunaway GA, Corkey BE, Tornheim K. Phosphofructokinase isozymes in pancreatic islets and clonal β-cells (INS-1). Diabetes 44: 1285-1289, 1995.
90. 2+ dynamics of isolated mouse β-cells and islets: implications for mathematical models. Biophys J 84: 2852-2870, 2003.