Cholinergic augmentation of insulin release requires ankyrin-B

Science Signaling

Volumn 3, Issue 113, 2010, Pages

  Healy, Jane A ^a   Nilsson, Kent R ^a   Hohmeier, Hans E ^a,b   Berglund, Jelena ^a,c   Davis, Jonathan ^a   Hoffman, Janis ^a   Kohler, Martin ^c   Li, Luo Sheng ^c   Berggren, Per Olof ^c   Newgard, Christopher B ^a,b   Bennett, Vann ^a  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANKYRIN; ANKYRIN B; CALCIUM ION; CARBACHOL; FURA 2; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INOSITOL TRISPHOSPHATE; PANCRELIPASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADRENERGIC STIMULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; FEMALE; GENOTYPE; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; GLYCEMIC CONTROL; HEART MUSCLE CELL; HUMAN; HYPERGLYCEMIA; HYPOINSULINEMIA; INSULIN RELEASE; INSULIN TOLERANCE TEST; MAJOR CLINICAL STUDY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PARASYMPATHETIC FUNCTION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; RAT; REGULATORY MECHANISM; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; ANKYRINS; CALCIUM; CARBACHOL; DIABETES MELLITUS, TYPE 2; GLUCOSE; IMMUNOBLOTTING; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICROSCOPY, FLUORESCENCE; MUTATION, MISSENSE; PARASYMPATHETIC NERVOUS SYSTEM; POLYMORPHISM, SINGLE NUCLEOTIDE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK FACTORS; RNA, SMALL INTERFERING;

MUS;

EID: 77953844541     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000771     Document Type: Article

References (33)

1. B. Ahrén, Autonomic regulation of islet hormone secretion-implications for health and disease. Diabetologia 43, 393-410 (2000).
2. 3 muscarinic acetylcholine receptors in regulating insulin release and blood glucose homeostasis in vivo. Cell Metab. 3, 449-461 (2006).
3. J. Iversen, Effect of acetyl choline on the secretion of glucagon and insulin from the isolated, perfused canine pancreas. Diabetes 22, 381-387 (1973).
4. S. R. Bloom, A. V. Edwards, Effects of certain metabolites on pancreatic endocrine responses to stimulation of the vagus nerves in conscious calves. J. Physiol. 362, 303-310 (1985).
5. L. Benthem, T. O. Mundinger, G. J. Taborsky Jr., Meal-induced insulin secretion in dogs is mediated by both branches of the autonomic nervous system. Am. J. Physiol. Endocrinol. Metab. 278, E603-E610 (2000).
6. 3 receptor in a cardiac T-tubule/SR microdomain. PLoS Biol. 3, e423 (2005).
7. P. J. Mohler, J. Q. Davis, L. H. Davis, J. A. Hoffman, P. Michaely, V. Bennett, Inositol 1, 4, 5-trisphosphate receptor localization and stability in neonatal cardiomyocytes requires interaction with ankyrin-B. J. Biol. Chem. 279, 12980-12987 (2004).
8. P. J. Mohler, J. J. Schott, A. O. Gramolini, K. W. Dilly, S. Guatimosim, W. H. duBell, L. S. Song, K. Haurogné, F. Kyndt, M. E. Ali, T. B. Rogers, W. J. Lederer, D. Escande, H. Le Marec, V. Bennett, Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 421, 634-639 (2003).
9. P. J. Mohler, I. Splawski, C. Napolitano, G. Bottelli, L. Sharpe, K. Timothy, S. G. Priori, M. T. Keating, V. Bennett, A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc. Natl. Acad. Sci. U. S. A. 101, 9137-9142 (2004).
10. C. F. Kline, H. T. Kurata, T. J. Hund, S. R. Cunha, O. M. Koval, P. J. Wright, M. Christensen, M. E. Anderson, C. G. Nichols, P. J. Mohler, Dual role of K ATP channel C-terminal motif in membrane targeting and metabolic regulation. Proc. Natl. Acad. Sci. U. S. A. 106, 16669-16674 (2009).
11. P. J. Mohler, J. A. Healy, H. Xue, A. A. Puca, C. F. Kline, R. R. Allingham, E. G. Kranias, H. A. Rockman, V. Bennett, Ankyrin-B syndrome: Enhanced cardiac function balanced by risk of cardiac death and premature senescence. PLoS One 2, e1051 (2007).
12. 2+ release in pancreatic β-cells. Biochem. J. 248, 329-336 (1987).
13. 2+ release in permeabilized pancreatic β-cells. FEBS Lett. 229, 211-214 (1988).
14. E. Gagerman, L. A. Idahl, H. P. Meissner, I. B. Taljedal, Insulin release, cGMP, cAMP, and membrane potential in acetylcholine-stimulated islets. Am. J. Physiol. 235, E493-E500 (1978).
15. M. C. Garcia, M. P. Hermans, J. C. Henquin, Glucose-, calcium- and concentrationdependence of acetylcholine stimulation of insulin release and ionic fluxes in mouse islets. Biochem. J. 254, 211-218 (1988).
16. P. Gilon, J. C. Henquin, Mechanisms and physiological significance of the cholinergic control of pancreatic β-cell function. Endocr. Rev. 22, 565-604 (2001).
17. 2+ oscillation frequency and insulin exocytosis. Cell 119, 273-284 (2004).
18. ++ uptake by rat pancreatic islets. Endocrinology 107, 924-929 (1980).
19. S. N. Yang, P. O. Berggren, The role of voltage-gated calcium channels in pancreatic β-cell physiology and pathophysiology. Endocr. Rev. 27, 621-676 (2006).
20. D. J. Drucker, The biology of incretin hormones. Cell Metab. 3, 153-165 (2006).
21. E. Cerasi, R. Luft, The plasma insulin response to glucose infusion in healthy subjects and in diabetes mellitus. Acta Endocrinol. (Copenh.) 55, 278-304 (1967).
22. M. J. Davies, G. Rayman, A. Grenfell, I. P. Gray, J. L. Day, C. N. Hales, Loss of the first phase insulin response to intravenous glucose in subjects with persistent impaired glucose tolerance. Diabet. Med. 11, 432-436 (1994).
23. S. Del Prato, A. Tiengo, The importance of first-phase insulin secretion: Implications for the therapy of type 2 diabetes mellitus. Diabet Metab. Res. Rev. 17, 164-174 (2001).
24. L. J. Raffel, D. C. Robbins, J. M. Norris, E. Boerwinkle, R. A. DeFronzo, S. C. Elbein, W. Fujimoto, C. L. Hanis, S. E. Kahn, M. A. Permutt, K. C. Chiu, J. Cruz, D. A. Ehrmann, R. P. Robertson, J. I. Rotter, J. Buse, The GENNID Study. A resource for mapping the genes that cause NIDDM. Diabetes Care 19, 864-872 (1996).
25. P. J. Mohler, S. Le Scouarnec, I. Denjoy, J. S. Lowe, P. Guicheney, L Caron, I. M. Driskell, J. J. Schott, K. Norris, A. Leenhardt, R. B. Kim, D. Escande, D. M. Roden, Defining the cellular phenotype of "ankyrin-B syndrome" variants: Human ANK2 variants associated with clinical phenotypes display a spectrum of activities in cardiomyocytes. Circulation 115, 432-441 (2007).
26. S. R. Cunha, P. J. Mohler, Obscurin targets ankyrin-B and protein phosphatase 2A to the cardiac M-line. J. Biol. Chem. 283, 31968-31980 (2008).
27. 2+-dependent insulin secretion from the islets of Langerhans. Endocrine 13, 251-262 (2000).
28. J. L. Chiasson, R. G. Josse, R. Gomis, M. Hanefeld, A. Karasik, M. Laakso; STOP-NIDDM Trial Research Group, Acarbose for prevention of type 2 diabetes mellitus: The STOP-NIDDM randomised trial. Lancet 359, 2072-2077 (2002).
29. F. A. Van de Laar, P. L. Lucassen, R. P. Akkermans, E. H. Van de Lisdonk, W. J. De Grauw, Alpha-glucosidase inhibitors for people with impaired glucose tolerance or impaired fasting blood glucose. Cochrane Database Syst. Rev. CD005061 (2006).
30. + channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49, 424-430 (2000).
31. J. R. Bain, J. C. Schisler, K. Takeuchi, C. B. Newgard, T. C. Becker, An adenovirus vector for efficient RNA interference-mediated suppression of target genes in insulinoma cells and pancreatic islets of langerhans. Diabetes 53, 2190-2194 (2004).
32. 3 receptor complex. EMBO J. 9, 61-67 (1990).
33. Acknowledgments: We acknowledge the American Diabetes Association for management of the GENNID database and DNA samples. Funding: J. H. was supported in part by a predoctoral fellowship from the American Heart Association. V. B. was supported by the Howard Hughes Medical Institute. P.-O. B. was supported by the Swedish Council and the Family Erling-Persson Foundation. C. B. N. was supported by NIH grant DK42583. J. B. was supported by the Wenner-Gren Foundations. Author contributions: J. H. performed experiments, participated in data analysis and experimental design, and wrote the paper. V. B. participated in experimental design and data analysis and wrote the paper. K. R. N. performed experiments, participated in data analysis, and helped write the paper. H. E. H., J. B., M. K., L.-S. L., and J. H. performed experiments and participated in data analysis. C. B. N. and P.-O. B. participated in experimental design and data analysis and edited the paper. Competing interests: We are preparing to submit a patent related to the finding of a role of ankyrin-B mutation in human diabetes and we are patenting the usage of ankyrin-B SNPs for human disease stratification. The 832/13 insulinoma cell line used in this study is available to all laboratories but requires signing of a material transfer agreement (MTA) provided by Duke University.