Impaired cAMP generation contributes to defective glucose-stimulated insulin secretion after long-term exposure to palmitate

Diabetes

Volumn 64, Issue 3, 2015, Pages 904-915

  Tian, Geng ^a,b   Maria Sol, E Ri ^b   Xu, Yunjian ^b   Shuai, Hongyan ^b   Tengholm, Anders ^b  

^a BINZHOU MEDICAL UNIVERSITY   (China)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE 9; CALCIUM; CYCLIC AMP; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; PALMITIC ACID; UNCLASSIFIED DRUG; INSULIN;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL STIMULATION; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; FEMALE; HUMAN; HUMAN CELL; INSULIN RELEASE; INSULINOMA CELL LINE; LONG TERM EXPOSURE; MOUSE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; PANCREAS ISLET BETA CELL; REAL TIME POLYMERASE CHAIN REACTION; SECRETION (PROCESS);

ANIMALS; CALCIUM; CELL SURVIVAL; CELLS, CULTURED; CYCLIC AMP; FEMALE; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; MICE; PALMITIC ACID; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84928210510     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-1036     Document Type: Article

References (50)

1. Unger RH. Lipotoxicity in the pathogenesis of obesity-dependent NIDDM. Genetic and clinical implications. Diabetes 1995;44:863-870
2. McGarry JD. Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 2002;51:7-18
3. Malaisse WJ, Malaisse-Lagae F. Stimulation of insulin secretion by noncarbohydrate metabolites. J Lab Clin Med 1968;72:438-448
4. Prentki M, Vischer S, Glennon MC, Regazzi R, Deeney JT, Corkey BE. Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J Biol Chem 1992;267:5802-5810
5. Bollheimer LC, Skelly RH, Chester MW, McGarry JD, Rhodes CJ. Chronic exposure to free fatty acid reduces pancreatic beta cell insulin content by increasing basal insulin secretion that is not compensated for by a corresponding increase in proinsulin biosynthesis translation. J Clin Invest 1998;101:1094-1101
6. Zhou YP, Grill VE. Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J Clin Invest 1994;93:870-876
7. Maedler K, Spinas GA, Dyntar D, Moritz W, Kaiser N, Donath MY. Distinct effects of saturated and monounsaturated fatty acids on b-cell turnover and function. Diabetes 2001;50:69-76
8. Biden TJ, Robinson D, Cordery D, Hughes WE, Busch AK. Chronic effects of fatty acids on pancreatic b-cell function: new insights from functional genomics. Diabetes 2004;53(Suppl. 1):S159-S165
9. Poitout V, Amyot J, Semache M, Zarrouki B, Hagman D, Fontés G. Glucolipotoxicity of the pancreatic beta cell. Biochim Biophys Acta. 2010;1801:289-298
10. Malmgren S, Spégel P, Danielsson AP, et al. Coordinate changes in histone modifications, mRNA levels, and metabolite profiles in clonal INS-1 832/13 b-cells accompany functional adaptations to lipotoxicity. J Biol Chem 2013;288:11973-11987
11. Larsson O, Deeney JT, Bränström R, Berggren PO, Corkey BE. Activation of the ATP-sensitive K+ channel by long chain acyl-CoA. A role in modulation of pancreatic b-cell glucose sensitivity. J Biol Chem 1996;271:10623-10626
12. Maestre I, Jordán J, Calvo S, et al. Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the b-cell line INS-1. Endocrinology 2003;144:335-345
13. Kharroubi I, Ladrière L, Cardozo AK, Dogusan Z, Cnop M, Eizirik DL. Free fatty acids and cytokines induce pancreatic b-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress. Endocrinology 2004;145:5087-5096
14. Lupi R, Dotta F, Marselli L, et al. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that b-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 2002;51:1437-1442
15. Joseph JW, Koshkin V, Saleh MC, et al. Free fatty acid-induced b-cell defects are dependent on uncoupling protein 2 expression. J Biol Chem 2004; 279:51049-51056
16. Olofsson CS, Collins S, Bengtsson M, et al. Long-term exposure to glucose and lipids inhibits glucose-induced insulin secretion downstream of granule fusion with plasma membrane. Diabetes 2007;56:1888-1897
17. Hoppa MB, Collins S, Ramracheya R, et al. Chronic palmitate exposure inhibits insulin secretion by dissociation of Ca2+ channels from secretory granules. Cell Metab 2009;10:455-465
18. Henquin JC. Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia 2009;52:739-751
19. Rorsman P, Braun M. Regulation of insulin secretion in human pancreatic islets. Annu Rev Physiol 2013;75:155-179
20. Campbell JE, Drucker DJ. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab 2013;17:819-837
21. Dyachok O, Idevall-Hagren O, Sågetorp J, et al. Glucose-induced cyclic AMP oscillations regulate pulsatile insulin secretion. Cell Metab 2008;8:26-37
22. Idevall-Hagren O, Barg S, Gylfe E, Tengholm A. cAMP mediators of pulsatile insulin secretion from glucose-stimulated single b-cells. J Biol Chem 2010;285: 23007-23018
23. Tian G, Sandler S, Gylfe E, Tengholm A. Glucose-and hormone-induced cAMP oscillations in a-and b-cells within intact pancreatic islets. Diabetes 2011;60:1535-1543
24. Dyachok O, Isakov Y, Sågetorp J, Tengholm A. Oscillations of cyclic AMP in hormone-stimulated insulin-secreting b-cells. Nature 2006;439:349-352
25. Goto M, Eich TM, Felldin M, et al. Refinement of the automated method for human islet isolation and presentation of a closed system for in vitro islet culture. Transplantation 2004;78:1367-1375
26. Merglen A, Theander S, Rubi B, Chaffard G, Wollheim CB, Maechler P. Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology 2004;145:667-678
27. Miyazaki J, Araki K, Yamato E, et al. Establishment of a pancreatic b cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 1990;127:126-132
28. Idevall-Hagren O, Jakobsson I, Xu Y, Tengholm A. Spatial control of Epac2 activity by cAMP and Ca2+-mediated activation of Ras in pancreatic b cells. Sci Signal 2013;6:1-11, S1-S6
29. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012;9:671-675
30. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985;260:3440-3450
31. Itoh Y, Kawamata Y, Harada M, et al. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 2003;422:173-176
32. Landa LR Jr, Harbeck M, Kaihara K, et al. Interplay of Ca2+ and cAMP signaling in the insulin-secreting MIN6 beta-cell line. J Biol Chem 2005;280: 31294-31302
33. Kim JW, Roberts CD, Berg SA, Caicedo A, Roper SD, Chaudhari N. Imaging cyclic AMP changes in pancreatic islets of transgenic reporter mice. PLoS ONE 2008;3:e2127
34. Eliasson L, Ma X, Renström E, et al. SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol 2003; 121:181-197
35. 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
36. Ammälä C, Ashcroft FM, Rorsman P. Calcium-independent potentiation of insulin release by cyclic AMP in single b-cells. Nature 1993;363:356-358
37. Seino S, Shibasaki T. PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 2005;85:1303-1342
38. Tengholm A. Cyclic AMP dynamics in the pancreatic b-cell. Ups J Med Sci 2012;117:355-369
39. 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 U S A 2007;104:19333-19338
40. Dzhura I, Chepurny OG, Leech CA, et al. Phospholipase C-links Epac2 activation to the potentiation of glucose-stimulated insulin secretion from mouse islets of Langerhans. Islets 2011;3:121-128
41. Iizuka K, Nakajima H, Namba M, et al. Metabolic consequence of long-term exposure of pancreatic b cells to free fatty acid with special reference to glucose insensitivity. Biochim Biophys Acta 2002;1586:23-31
42. Allagnat F, Alonso F, Martin D, Abderrahmani A, Waeber G, Haefliger JA. ICER-1g overexpression drives palmitate-mediated connexin36 down-regulation in insulin-secreting cells. J Biol Chem 2008;283:5226-5234
43. Hodson DJ, Mitchell RK, Bellomo EA, et al. Lipotoxicity disrupts incretinregulated human b cell connectivity. J Clin Invest 2013;123:4182-4194
44. Vikman J, Svensson H, Huang YC, et al. Truncation of SNAP-25 reduces the stimulatory action of cAMP on rapid exocytosis in insulin-secreting cells. Am J Physiol Endocrinol Metab 2009;297:E452-E461
45. Shibasaki T, Sunaga Y, Fujimoto K, Kashima Y, Seino S. Interaction of ATP sensor, cAMP sensor, Ca2+ sensor, and voltage-dependent Ca2+ channel in insulin granule exocytosis. J Biol Chem 2004;279:7956-7961
46. Hodson DJ, Mitchell RK, Marselli L, et al. ADCY5 couples glucose to insulin secretion in human islets. Diabetes 2014;63:3009-3021
47. Cooper DM. Regulation and organization of adenylyl cyclases and cAMP. Biochem J 2003;375:517-529
48. Thangavel M, Liu X, Sun SQ, Kaminsky J, Ostrom RS. The C1 and C2 domains target human type 6 adenylyl cyclase to lipid rafts and caveolae. Cell Signal 2009;21:301-308
49. Delint-Ramirez I, Willoughby D, Hammond GV, Ayling LJ, Cooper DM. Palmitoylation targets AKAP79 protein to lipid rafts and promotes its regulation of calcium-sensitive adenylyl cyclase type 8. J Biol Chem 2011;286:32962-32975
50. Kwon G, Pappan KL, Marshall CA, Schaffer JE, McDaniel ML. cAMP Dosedependently prevents palmitate-induced apoptosis by both protein kinase A-and cAMP-guanine nucleotide exchange factor-dependent pathways in beta-cells. J Biol Chem 2004;279:8938-8945