Glucose-stimulated insulin secretion correlates with changes in mitochondrial and cytosolic Ca2+ in aequorin-expressing INS-1 cells

Journal of Clinical Investigation

Volumn 98, Issue 11, 1996, Pages 2524-2538

  Kennedy, Eleanor D ^a   Rizzuto, Rosario ^b   Theler, Jean Marc ^a,d   Pralong, William F ^a   Bastianutto, Carlo ^b   Pozzan, Tullio ^b   Wollheim, Claes B ^a,c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF PADOVA   (Italy)

^c Center Médical Universitaire   (Switzerland)

^d Carl Zeiss AG   (Switzerland)

Author keywords

aequorin; cytosolic calcium; insulin secretion; mitochondrial calcium; signal transduction

Indexed keywords

AEQUORIN;

ADAPTATION; ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL FUNCTION; CELL MEMBRANE DEPOLARIZATION; COUPLING FACTOR; DESENSITIZATION; EXOCYTOSIS; INSULIN RELEASE; MITOCHONDRIAL MEMBRANE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SECRETORY GRANULE;

EID: 0029808483     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119071     Document Type: Article

References (51)

1. Wollheim, C.B., and G.W.G. Sharp. 1981. Regulation of insulin release by calcium. Physiol. Rev. 61:914-973.
2. Wollheim, C.B., and T.J. Biden. 1986. Signal transduction in insulin secretion: Comparison between fuel stimuli and receptor agonists. Ann. NY Acad. Sci. 488:317-333.
3. 2+, cAMP and phospholipid derived messengers in coupling mechanisms of insulin secretion. Physiol. Rev. 67:1185-1248.
4. Rasmussen, H., K.C. Zawalich, S. Ganesan, R. Calle, and W.S. Zawalich. 1990. Physiology and pathophysiology of insulin secretion. Diabetes Care. 13: 655-666.
5. Thorens, B., Y.-J. Wu, J.L. Leahy, and G.C. Weir. 1992. The loss of GLUT2 expression by glucose-unresponsive B-cells of db/db mice is reversible, and is induced by the diabetic environment. J. Clin. Invest. 90:77-85.
6. Matschinsky, F., Y. Liang, P. Kesavan, L. Wang, P. Froguel, G. Velho, D. Cohen, M.A. Permutt, Y. Tanizawa, T.L. Jetton, et al. 1993. Glucokinase as pancreatic B cell glucose sensor and diabetes gene. J. Clin. Invest. 92:2092-2098.
7. Heimberg, H., A. De Vos, A. Vandercammen, E. Van Schaftingen, D. Pipeleers, and F. Schuit. 1993. Heterogeneity in glucose sensitivity among pancreatic B-cells is correlated to differences in glucose phosphorylation rather than glucose transport. EMBO J. 12:2873-2879.
8. Sekine, N., V. Cirulli, R. Regazzi, L.J. Brown, E. Gine, J. Tamarit-Rodriguez, M. Girotti, S. Marie, M.J. MacDonald, C.B. Wollheim. 1994. Low lactate dehydrogenase and high mitochondrial glycerol phosphate dehydrogenase in pancreatic B-cells. J. Biol. Chem. 269:4895-4902.
9. MacDonald, M.J. 1995. Feasibility of a mitochondrial pyruvate malate shuttle in pancreatic islets. J. Biol. Chem. 270:20051-20058.
10. 2+, and secretion EMBO J. 9:53-60.
11. Erecinska, M., J. Bryla, M. Michalik, M.D. Meglasson, and D. Nelson. 1992. Energy metabolism in islets of Langerhans. Biochim. Biophys. Acta. 1101: 273-295.
12. Prentki, M., S. Vischer, M.C. Glennon, R. Regazzi, J.T. Deeney, and B.E. Corkey. 1992. Malonyl-CoA, and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion J. Biol. Chem. 267:5802-5810.
13. Prentki, M. 1996. New insights into pancreatic B-cell metabolic signaling in insulin secretion. Eur. J. Endocrinol. 134:272-286.
14. Ashcroft, F.M., and P. Rorsman. 1989. Electrophysiology of the pancreatic B-cell. Prog. Biophys. Mol. Biol. 54:87-143.
15. Detimary, P., J.-C. Jonas, and J.-C. Henquin. 1995. Possible links between glucose-induced changes in the energy state of pancreatic B cells and insulin release. J Clin. Invest. 96:1738-1745.
16. Rorsman, P., C. Ämmälä, P.-O. Berggren, K. Bokvist, and O. Larsson. 1992. Cytoplasmic calcium transients due to single action potentials and voltage-clamp depolarizations in mouse pancreatic B-cells. EMBO J. 11:2877-2884.
17. 2+ in pancreatic B-cells stimulated by glucose, carbachol, and ATP. J. Biol. Chem. 267: 18110-18117.
18. 2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic B-cells. EMBO J. 14:50-57.
19. i oscillations due to bursting electrical activity in single pancreatic islets. Pflueg. Arch. 418:417-422.
20. 2+ as evidenced in single pancreatic islets. J. Biol. Chem. 268:22265-22268.
21. 2+ in the release of pancreatic islet hormones. Diabete Metab. 20:123-131.
22. 2+ to supramicromolar levels in a pancreatic B-cell line. J. Biol. Chem. 268:22385-22390.
23. Asfari, M., D. Janjic, P. Meda, G. Li, P.A. Halban, and C.B. Wollheim. 1992. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology. 130:167-178.
24. 2+-independent insulin secretion from permeabilized RINm5F cells. J. Biol. Chem. 262:5049-5056.
25. McCormack, J.G., A.P. Halestrap, and R.M. Denton. 1990. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev. 70:391-425.
26. 2+-binding to citrate cycle dehydrogenases. Int. J. Biochem. 22:1081-1088.
27. 2+ in cells and tissues. J. Bioenerg. Biomembr. 23:823-854.
28. 2+ transients. J. Biol. Chem. 269:27310-27314.
29. 2+ by specifically targeted recombinant aequorin. Nature (Lond.). 358:325-327.
30. c). J. Biol. Chem. 270:9896-9903.
31. Blinks, J.R., P.H. Mattingly, B.R. Jewell, M. van Leeuwen, G.C. Harrer, and D.G. Allen. 1978. Practical aspects of the use of aequorin as a calcium indicator: Assay, preparation, microinjection, and interpretation of signals. Methods Enzymol. 57:292-328.
32. Cobbold, P.H., and T.J. Rink. 1987. Fluorescence and bioluminescence measurement of cytoplasmic free calcium. Biochem. J. 248:313-328.
33. Field, J., J.-I. Nikawa, D. Broek, B. MacDonald, L. Rodgers, I.A. Wilson, R.A. Lerner, and M. Wigler. 1988. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol. 8:2159-2165.
34. Smiley, S.T., M. Reers, C. Mottola-Hartshorn, M. Lin, A. Chen, T.W. Smith, G.D. Steele, and L. Bo Chen. 1991. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA. 88:3671-3675.
35. Heytler, P.G., and W.W. Prichard. 1962. A new class of uncoupling agents - carbonyl cyanide phenylhydrazone. Biochem. Biophys. Res Commun. 7:272-275.
36. Rossier, J.R., J.A. Cox, E.J. Niesor, and C.L. Bentzen. 1989. A new class of calcium entry blockers defined by 1,3-diphosphonates. J. Biol. Chem. 264: 16598-16607.
37. 3-sensitive channels that are sensed by neighboring mitochondria. Science (Wash. DC). 262:744-747.
38. 2+ homeostasis in intact cells. J. Cell Biol. 126:1183-1194.
39. 2+ with recombinant targeted aequorin: significance for the regulation of pyruvate dehydrogenase activity. Proc. Natl. Acad. Sci. USA. 93:5489-5494.
40. Hajnoczky, G., L.D. Robb-Gaspers, M.B. Seitz, and A.P. Thomas. 1995. Decoding the cytosolic calcium oscillations in the mitochondria. Cell. 82:415-424.
41. Gunter, T.E., K.K. Gunter, S.S. Sheu, and C.E. Gavin. 1994. Mitochondrial calcium transport: physiological and pathological relevance. Am. J. Physiol. 267:C313-C339.
42. 2+ concentration in living single rat cardiac myocytes. Am. J. Physiol. 261:H1123-H1134.
43. Glennon, M.C., G. St.J. Bird, H. Takemura, O. Thastrup, B.A. Leslie, and J.W. Putney, Jr. 1992. In situ imaging of agonist-sensitive calcium pools in AR4-2J pancreatoma cells. J. Biol. Chem. 267:25568-25575.
44. Satin, L.S., and P.D. Smolen. 1994. Electrical bursting in B-cells of the pancreatic islets of Langerhans. Endocrine. 2:677-687.
45. 2+ influx in rat pancreatic B-cell. Diabetes. 41:438-443.
46. Hermans, M.P., W. Schmeer, and J.-C. Henquin. 1987. Modulation of the effect of acetylcholine on insulin release by the membrane potential of B-cells. Endocrinology, 120:1765-1773.
47. 2+ channels. Mol. Pharmacol. 42:489-498.
48. 2+ in hyperpolarized pancreatic B cells. Pflueg. Arch. 419:639-643.
49. 2+ concentration in the endoplasmic reticulum of intact cells. EMBO J. 14:5467-5475.
50. Ämmälä, C., L. Eliasson, K. Bokvist, O. Larsson, F.M. Ashcroft, and P. Rorsman. 1993. Exocytosis elicited by action potentials and voltage-clamp calcium currents in individual mouse pancreatic B-cells. J. Physiol. 472:665-688.
51. Lawrie, A.M., R. Rizzuto, T. Pozzan, and A.W.M. Simpson. 1996. A role for calcium influx in the regulation of mitochondrial calcium in endothelial cells. J. Biol. Chem. 271:10753-10759.