Glucagon-like peptide-1 mobilizes intracellular Ca2+ and stimulates mitochondrial ATP synthesis in pancreatic MIN6 β-cells

Biochemical Journal

Volumn 369, Issue 2, 2003, Pages 287-299

  Tsuboi, Takashi ^a   Silva Xavier, Gabriela Da ^a   Holz, George G ^c   Jouaville, Laurence S ^b   Thomas, Andrew P ^b   Rutter, Guy A ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c NONE

Author keywords

Aequorin; Insulin; Islet; Luciferase; Mitochondria

Indexed keywords

CELLS; GLUCOSE; PROTEINS;

RYANODINE RECEPTORS (RYR);

BIOCHEMISTRY;

ADENOSINE 3',5' PHOSPHOROTHIOATE; ADENOSINE TRIPHOSPHATE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RYANODINE; RYANODINE RECEPTOR;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CHELATION; CONCENTRATION RESPONSE; GLUCOSE METABOLISM; INSULIN RELEASE; ISOMERISM; MITOCHONDRION; PANCREAS CELL; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CALCIUM SIGNALING; CARBACHOL; CELL LINE; CHELATING AGENTS; CHOLINERGIC AGONISTS; CYCLIC AMP; DIAZOXIDE; EGTAZIC ACID; ENZYME INHIBITORS; FORSKOLIN; GLUCAGON; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; HOMEOSTASIS; INSULIN; ISLETS OF LANGERHANS; MACROCYCLIC COMPOUNDS; MITOCHONDRIA; OXAZOLES; PEPTIDE FRAGMENTS; PROTEIN PRECURSORS; RYANODINE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; THIONUCLEOTIDES;

EID: 0037440025     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021288     Document Type: Article

References (57)

1. Rutter, G. A. (2001) Nutrient-secretion coupling in the pancreatic islet β-cell: recent advances. Mol. Aspects Med. 22, 247-284
2. Maechler, P. and Wollheim, C. B. (2000) Mitochondrial signals in glucose-stimulated insulin secretion in the β-cell. J. Physiol. 529, 49-56
3. Aguilar-Bryan, L. and Bryan, J. (1999) Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocrinol. Rev. 20, 101-135
4. Safayhi, H., Haase, H., Kramer, U., Bihlmayer, A., Roenfeldt, M., Ammon, H. P., Froschmayr, M., Cassidy, T. N., Morano, I., Ahlijanian, M. K. and Striessnig, J. (1997) L-type calcium channels in insulin-secreting cells: biochemical characterization and phosphorylation in RINm5F cells. Mol. Endocrinol. 11, 619-629
5. Aizawa, T., Komatsu, M., Asanuma, N., Sato, Y. and Sharp, G. W. (1998) Glucose action 'beyond ionic events' in the pancreatic β-cell. Trends Pharmacol. Sci. 19, 496-499
6. Henquin, J. C. (2000) Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49, 1751-1760
7. Gromada, J., Holst, J. J. and Rorsman, P. (1998) Cellular regulation of islet hormone secretion by the incretin hormone glucagon-like peptide 1. Pflügers Arch. 435, 583-594
8. Montague, W. and Cook, J. R. (1971) The role of adenosine 32′:5′-cyclic monophosphate in the regulation of insulin release by isolated rat islets of Langerhans. Biochem. J. 122, 115-120
9. Montague, W. and Howell, S. L. (1972) The mode of action of adenosine 3′:5′-cyclic monophosphate in mammalian islets of Langerhans. Preparation and properties of islet-cell protein phosphokinase. Biochem. J. 129, 551-560
10. Schuit, F. C. and Pipeleers, D. G. (1985) Regulation of adenosine 3′,5′-monophosphate levels in the pancreatic β-cell. Endocrinology 117, 834-840
11. Gromada, J., Ding, W. G., Barg, S., Renstrom, E. and Rorsman, P. (1997) Multisite regulation of insulin secretion by cAMP-increasing agonists: evidence that glucagon-like peptide 1 and glucagon act via distinct receptors. Pflügers Arch. 434, 515-524
12. Gromada, J., Dissing, S., Bokvist, K., Renstrom, E., Frokjaer-Jensen, J., Wulff, B. S. and Rorsman, P. (1995) Glucagon-like peptide I increases cytoplasmic calcium in insulin-secreting β TC3-cells by enhancement of intracellular calcium mobilization. Diabetes 44, 767-774
13. 2+ and electrolyte mobilization following agonist application to the pancreatic β-cell line HIT. Pflügers Arch. 440, 828-834
14. 2+ retease in INS-1 pancreatic β-cells. J. Physiol. 536, 375-385
15. Islam, M. S., Leibiger, I., Leibiger, B., Rossi, D., Sorrentino, V., Ekstrom, T. J., Westerblad, H., Andrade, F. H. and Berggren, P. O. (1998) in situ activation of the type 2 ryanodine receptor in pancreatic β-cells requires cAMP-dependent phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 95, 6145-6150
16. 2+-ATPase (SERCA)-2 and ryanodine receptors. Diabetes 51 (Suppl. 1), S190-S201
17. 2+ flux in reconstituted lipid vesicles. J. Biol. Chem. 269, 6735-6742
18. Cullinan, C. A., Brady, E. J., Saperstein, R. and Leibowitz, M. D. (1994) Glucose-dependent alterations of intracellular free calcium by glucagon-like peptide-1 (7-36amide) in individual obl ob mouse β-cells. Cell Calcium 15, 391-400
19. 2+-signaling pathway in pancreatic β-cells by the insulinotropic hormone glucagon-like peptide-1. J. Biol. Chem. 270, 17749-17757
20. Reale, V., Hales, C. N. and Ashford, M. L. (1995) Regulation of calcium-activated nonselective cation channel activity by cyclic nucleotides in the rat insulinoma cell line, CRI-G1. J. Membr. Biol. 145, 267-278
21. Kawasaki, H., Springett, G. M., Mochizuki, N., Toki, S., Nakaya, M., Matsuda, M., Housman, D. E. and Graybiel, A. M. (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282, 2275-2279
22. Ozaki, N., Shibasaki, T., Kashima, Y., Miki, T., Takahashi, K., Ueno, H., Sunaga, Y., Yano, H., Matsuura, Y., Iwanaga, T. et al. (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat. Cell Biol. 2, 805-811
23. Kashima, Y., Miki, T., Shibasaki, T., Ozaki, N., Miyazaki, M., Yano, H. and Seino, S. (2001) Critical role of cAMP-GEFII-Rim2 complex in incretin-potentiated insulin secretion. J. Biol. Chem. 276, 46046-46053
24. 2+ to supramicromolar levels in a pancreatic β-cell line. Possible role in glucose and agonist-induced insulin secretion. J. Biol. Chem. 268, 22385-22390
25. 2+ in aequorin-expressing INS-1 cells. J. Clin. Invest. 98, 2524-2538
26. 2- oscillations in the pancreatic β-cell line, MIN6. Diabetologia 41, 279-286
27. 2+ oscillations and insulin secretion in pancreatic islets. Biochem. J. 353, 175-180
28. Ainscow, E. K., Zhao, C. and Rutter, G. A. (2000) Acute overexpression of lactate dehydrogenase-A perturbs β-cell mitochondrial metabolism and insulin secretion. Diabetes 49, 1149-1155
29. Kennedy, H. J., Pouli, A. E., Ainscow, E. K., Jouaville, L. S., Rizzuto, R. and Rutter, G. A. (1999) Glucose generates sub-plasma membrane ATP microdomains in single islet β-cells. Potential role for strategically located mitochondria. J. Biol. Chem. 274, 13281-13291
30. Jouaville, L. S., Pinton, P., Bastianutto, C., Rutter, G. A. and Rizzuto, R. (1999) Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc. Natl. Acad. Sci. U.S.A. 96, 13807-13812
31. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y. and Yamamura, K. (1990) Establishment of a pancreatic β-cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127, 126-132
32. Fisher, R. J. and Burgoyne, R. D. (1999) The effect of transfection with Botulinum neurotoxin C1 light chain on exocytosis measured in cell populations and by single-cell amperometry in PC12 cells. Pflügers Arch. 437, 754-762
33. Varadi, A., Ainscow, E. K., Allan, V. J. and Rutter, G. A. (2002) Involvement of conventional kinesin in glucose-stimulated secretory granule movements and exocytosis in clonal pancreatic β-cells. J. Cell Sci. 115, 4177-4189
34. Rafiq, I., da Silva Xavier, G., Hooper, S. and Rutter, G. A. (2000) Glucose-stimulated preproinsulin gene expression and nuclear trans-location of pancreatic duodenum homeobox-1 require activation of phosphatidylinositol 3-kinase but not p38 MAPK/SAPK2. J. Biol. Chem. 275, 15977-15984
35. 2+ revealed by specifically targeted recombinant aequorin. Nature (London) 358, 325-327
36. 2+ release: an intimate connection. Trends Biochem. Sci. 25, 215-221
37. Henquin, J. C. (1987) Regulation of insulin release by ionic and electrical events in β-cells. Horm. Res. 27, 168-178
38. 2+-ATPase. Proc. Natl. Acad. Sci. U.S.A. 87, 2466-2470
39. 2+, and insulin release in carbamylcholine-stimulated RINm5F cells. J. Biol. Chem. 251, 8314-8319
40. 2+ pumps. Cell Calcium 26, 9-13
41. Gafni, J., Munsch, J. A., Lam, T. H., Catlin, M. C., Costa, L. G., Molinski, T. F. and Pessah, I. N. (1997) Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron 19, 723-733
42. Kleppisch, T. and Nelson, M. T. (1995) Adenosine activates ATP-sensitive potassium channels in arterial myocytes via A2 receptors and cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 92, 12441-12445
43. Bode, H. P., Moormann, B., Dabew, R. and Goke, B. (1999) Glucagon-like peptide 1 elevates cytosolic calcium in pancreatic β-cells independently of protein kinase A. Endocrinology 140, 3919-3927
44. Thorens, B. (1992) Expression cloning of the pancreatic β-cell receptor for the gluco-incretin hormone glucagon-like peptide 1. Proc. Natl. Acad. Sci. U.S.A. 89, 8641-8645
45. Liu, Y. J., Grapengiesser, E., Gylfe, E. and Hellman, B. (1996) Crosstalk between the cAMP and inositol trisphosphate-signalling pathways in pancreatic β-cells. Arch. Biochem. Biophys. 334, 295-302
46. 2+ signaling system stimulated by the insulinotropic hormone glucagon-like peptide-1-(7-37). J. Biol. Chem. 274, 14147-14156
47. 2+ release in insulin-secreting cells. FEBS Lett. 296, 287-291
48. 2+ mobilization without increasing the cellular levels of inositol polyphosphates. J. Biol. Chem. 266, 4772-4781
49. Marx, S. O., Reiken, S., Hisamatsu, Y., Jayaraman, T., Burkhoff, D., Rosemblit, N. and Marks, A. R. (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101, 365-376
50. 2+ release from microsomal vesicles of rat parotid acinar cells. Biochem. Biophys. Res. Commun. 246, 422-425
51. 2+ store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J. Cell Biol. 155, 41-51
52. 2+ responses. Science 280, 1763-1766
53. Pinton, P., Tsuboi, T., Ainscow, E. K., Pozzan, T., Rizzuto, R. and Rutter, G. A. (2002) Dynamics of glucose-induced membrane recruitment of protein kinase C βII in living pancreatic islet β-cells. J. Biol. Chem. 277, 37702-37710
54. + channels in mouse β-cells. J. Clin. Invest. 89, 1288-1295
55. 2+ in rat pancreatic islets. Proc. Natl. Acad. Sci. U.S.A. 92, 10728-10732
56. Henquin, J. C., Ishiyama, N, Nenquin, M., Ravier, M. A. and Jonas, J. C. (2002) Signals and pools underlying biphasic insulin secretion. Diabetes. 51 (Suppl. 1), S60-S67
57. 2+-free conditions. J. Endocrinol. 155, 545-551