Activators of PKA and epac distinctly influence insulin secretion and cytosolic Ca2+in female mouse islets stimulated by glucose and tolbutamide

Endocrinology (United States)

Volumn 155, Issue 9, 2014, Pages 3274-3287

  Henquin, Jean Claude ^a   Nenquin, Myriam ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPORTER; CALCIUM ION; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENZYME ACTIVATOR; EXCHANGE PROTEIN DIRECTLY ACTIVATED BY CAMP; GLICLAZIDE; GLUCOSE; NATEGLINIDE; POTASSIUM CHLORIDE; TOLBUTAMIDE; UNCLASSIFIED DRUG; CALCIUM; EPAC PROTEIN, MOUSE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INSULIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CYTOSOL; ENZYME ACTIVATION; ENZYME MECHANISM; EXOCYTOSIS; FEMALE; INSULIN RELEASE; INSULIN RESPONSE; MEMBRANE DEPOLARIZATION; METABOLIC PARAMETERS; MOUSE; NONHUMAN; PANCREAS ISLET; PROTEIN INTERACTION; SECRETION (PROCESS); STEADY STATE; STIMULATION; ANIMAL; C57BL MOUSE; DRUG EFFECT; DRUG POTENTIATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSOL; ENZYME ACTIVATORS; FEMALE; GLUCOSE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INSULIN; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; TOLBUTAMIDE;

EID: 84907044034     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1247     Document Type: Article

References (59)

1. MacDonald PE, Joseph JW, Rorsman P. Glucose-sensing mechanisms in pancreatic β-cells. Philos Trans R Soc Lond B Biol Sci. 2005;360:2211-2225.
2. Henquin JC. Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia. 2009;52:739-751.
3. Bertram R, Sherman A, Satin LS. Electrical bursting, calcium oscillations, and synchronization of pancreatic islets. Adv Exp Med Biol. 2010;654:261-279.
4. Seino S. Cell signalling in insulin secretion: the molecular targets of ATP, cAMP and sulfonylurea. Diabetologia. 2012;55:2096-2108.
5. Straub SG, Sharp GW. Hypothesis: one rate-limiting step controls the magnitude of both phases of glucose-stimulated insulin secretion. Am J Physiol Cell Physiol. 2004;287:C565-C571.
6. Mourad NI, Nenquin M, Henquin JC. Metabolic amplifying pathway increases both phases of insulin secretion independently of β-cell actin microfilaments. Am J Physiol Cell Physiol. 2010;299: C389-C398.
7. Ahrén B. Islet G protein-coupled receptors as potential targets for treatment of type 2 diabetes. Nat Rev Drug Discov. 2009;8:369-385.
8. Sharp GW. The adenylate cyclase-cyclic AMP system in islets of Langerhans and its role in the control of insulin release. Diabetologia. 1979;16:287-296.
9. 2+, cAMP, and phospholipid-de-rived messengers in coupling mechanisms of insulin secretion. Physiol Rev. 1987;67:1185-1248.
10. Jones PM, Persaud SJ. Protein kinases, protein phosphorylation, and the regulation of insulin secretion from pancreatic β-cells. Endocr Rev. 1998;19:429-461.
11. Renström E, Eliasson L, Rorsman P. Protein kinase A-dependent and-independent stimulation of exocytosis by cAMP in mouse pancreatic β-cells. J Physiol. 1997;502:105-118.
12. Ozaki N, Shibasaki T, Kashima Y, et al. cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol. 2000;2:805-811.
13. 2+release and exocytosis in pancreatic β-cells. J Biol Chem. 2003;278: 8279-8285.
14. Holz GG. Epac: a new cAMP-binding protein in support of gluca-gon-like peptide-1 receptor-mediated signal transduction in the pancreatic β-cell. Diabetes. 2004;53:5-13.
15. Gloerich M, Bos JL. Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol. 2010;50:355-375.
16. ATPchannel sulfonylurea sensitivity by a cAMP analog selective for the cAMP-regulated guanine nucleotide exchange factor Epac. Islets. 2010;2:72-81.
17. Song WJ, Mondal P, Li Y, Lee SE, Hussain MA. Pancreatic β-cell response to increased metabolic demand and to pharmacologic secretagogues requires EPAC2A. Diabetes. 2013;62:2796-2807.
18. Tian G, Sandler S, Gylfe E, Tengholm A. Glucose-and hormone-induced cAMP oscillations in a-and β-cells within intact pancreatic islets. Diabetes. 2011;60:1535-1543.
19. 2+-mediated activation of Ras in pancreatic β-cells. Sci Signal. 2013;6:ra29.1-11.
20. Christensen AE, Selheim F, de Rooij J, et al. cAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J Biol Chem. 2003;278:35394-35402.
21. Vliem MJ, Ponsioen B, Schwede F, et al. 8-pCPT-2'-O-Me-cAMP-AM: an improved Epac-selective cAMP analogue. Chembiochem. 2008;9:2052-2054.
22. Holz GG, Chepurny OG, Schwede F. Epac-selective cAMP analogs: new tools with which to evaluate the signal transduction properties of cAMP-regulated guanine nucleotide exchange factors. Cell Signal. 2008;20:10-20.
23. Chepurny OG, Kelley GG, Dzhura I, et al. PKA-dependent potentiation of glucose-stimulated insulin secretion by Epac activator 8-pCPT-2'-O-Me-cAMP-AM in human islets of Langerhans. Am J Physiol Endocrinol Metab. 2010;298:E622-E633.
24. Nenquin M, Szollosi A, Aguilar-Bryan L, Bryan J, Henquin JC. Both triggering and amplifying pathways contribute to fuel-induced insulin secretion in the absence of sulfonylurea receptor-1 in pancreatic β-cells. J Biol Chem. 2004;279:32316-32324.
25. Detimary P, Jonas JC, Henquin JC. Stable and diffusible pools of nucleotides in pancreatic islet cells. Endocrinology. 1996;137: 4671-4676.
26. Henquin JC. Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes. 2000;49:1751-1760.
27. Tsalkova T, Mei FC, Li S, et al. Isoform-specific antagonists of exchange proteins directly activated by cAMP. Proc Natl Acad Sci USA. 2012;109:18613-18618.
28. Rehmann H. Epac-inhibitors: facts and artefacts. Sci Rep. 2013;3: 3032.
29. Kai AK, Lam AK, Chen Y, et al. Exchange protein activated by cAMP 1 (Epac1)-deficient mice develop β-cell dysfunction and metabolic syndrome. FASEB J. 2013;27:4122-4135.
30. 2+in mouse pancreatic β-cells. Diabetes. 1998;47: 1266-1273.
31. Zhang CL, Katoh M, Shibasaki T, et al. The cAMP sensor Epac2 is a direct target of antidiabetic sulfonylurea drugs. Science. 2009; 325:607-610.
32. Takahashi T, Shibasaki T, Takahashi H, et al. Antidiabetic sulfonylureas and cAMP cooperatively activate Epac2A. Sci Signal. 2013; 6:ra94.
33. Mourad NI, Nenquin M, Henquin JC. cAMP-mediated and metabolic amplification of insulin secretion are distinct pathways sharing independence of β-cell microfilaments. Endocrinology. 2012;153: 4644-4654.
34. Kelley GG, Chepurny OG, Schwede F, et al. Glucose-dependent potentiation of mouse islet insulin secretion by Epac activator 8-pCPT-2'-O-Me-cAMP-AM. Islets. 2009;1:260-265.
35. Song WJ, Seshadri M, Ashraf U, et al. Snapin mediates incretin action and augments glucose-dependent insulin secretion. Cell Metab. 2011;13:308-319.
36. Kaihara KA, Dickson LM, Jacobson DA, et al. β-Cell-specific protein kinase A activation enhances the efficiency of glucose control by increasing acute-phase insulin secretion. Diabetes. 2013;62:1527-1536.
37. 2+influx. Mol Pharmacol. 2013; 83:191-205.
38. Idevall-Hagren O, Barg S, Gylfe E, Tengholm A. cAMP mediators of pulsatile insulin secretion from glucose-stimulated single β-cells. J Biol Chem. 2010;285:23007-23018.
39. Hatakeyama H, Kishimoto T, Nemoto T, Kasai H, Takahashi N. Rapid glucose sensing by protein kinase A for insulin exocytosis in mouse pancreatic islets. J Physiol. 2006;570:271-282.
40. Shibasaki T, Takahashi H, Miki T, et al. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci USA. 2007;104:19333-19338.
41. 2+-dependent electrical activity induced by glucose in mouse pancreatic β-cells. Endocrinology. 1983; 112:2218-2220.
42. 2+oscillations in isolated pancreatic β-cells. J Biol Chem. 1991;266:12207-12210.
43. 2+channel activity. Endocrinology. 1993;133:1685-1692.
44. Leech CA, Dzhura I, Chepurny OG, et al. Molecular physiology of glucagon-like peptide-1 insulin secretagogue action in pancreatic β cells. Prog Biophys Mol Biol. 2011;107:236-247.
45. 2+by forskolin and phorbol ester. FEBS Lett. 1985;183:430-432.
46. Jones PM, Fyles JM, Howell SL. Regulation of insulin secretion by cAMP in rat islets of Langerhans permeabilised by high-voltage discharge. FEBS Lett. 1986;205:205-209.
47. Ammälä C, Ashcroft FM, Rorsman P. Calcium-independent potentiation of insulin release by cyclic AMP in single β-cells. Nature. 1993;363:356-358.
48. 2+entry. Pflügers Arch. 1993;424:195-197.
49. Eliasson L, Ma X, Renström E, et al. SUR1 regulates PKA-indepen-dent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol. 2003;121:181-197.
50. Gaisano HY. Here come the newcomer granules, better late than never. Trends Endocrinol Metab. 2014;25:381-388.
51. Herbst KJ, Coltharp C, Amzel LM, Zhang J. Direct activation of Epac by sulfonylurea is isoform selective. Chem Biol. 2011;18:243-251.
52. Tsalkova T, Gribenko AV, Cheng X. Exchange protein directly activated by cyclic AMP isoform 2 is not a direct target of sulfonylurea drugs. Assay Drug Dev Technol. 2011;9:88-91.
53. Rehmann H. Epac2: a sulfonylurea receptor? Biochem Soc Trans. 2012;40:6-10.
54. 2+in pancreatic β-cells. Eur J Pharmacol. 1996;298: 279-286.
55. +channels in mouse β-cells. J Clin Invest. 1993;91:871-880.
56. +channel-independent pathway of glucose signaling in rat pancreatic islets. Diabetes. 1999;48:1006-1012.
57. Kasai H, Hatakeyama H, Ohno M, Takahashi N. Exocytosis in islet β-cells. Adv Exp Med Biol. 2010;654:305-338.
58. 2+. J Gen Physiol. 2004;124:653-662.
59. 2+-sensitive pool of granules is regulated by glucose andprotein kinases in insulin-secreting INS-1 cells. J Gen Physiol. 2004;124:641-651.