Disallowance of Acot7 in β-cells is required for normal glucose tolerance and insulin secretion

Diabetes

Volumn 65, Issue 5, 2016, Pages 1268-1282

  Martinez Sanchez, Aida ^a   Pullen, Timothy J ^a   Chabosseau, Pauline ^a   Zhang, Qifeng ^b   Haythorne, Elizabeth ^a   Cane, Matthew C ^a   Nguyen Tu, Marie Sophie ^a   Sayers, Sophie R ^a   Rutter, Guy A ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COA THIOESTERASE 7; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; FATTY ACID; MESSENGER RNA; PALMITOYL COENZYME A HYDROLASE; UNCLASSIFIED DRUG; ACOT7 PROTEIN, MOUSE; GLUCOSE; INSULIN; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; EXOCYTOSIS; FEMALE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; INSULIN RELEASE; LIPIDOMICS; MALE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXYGEN CONSUMPTION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CALCIUM SIGNALING; CELL CLONE; CYTOLOGY; DOWN REGULATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PANCREAS ISLET; PATHOLOGY; RAT; SECRETION (PROCESS); SEXUAL DEVELOPMENT; TISSUE CULTURE TECHNIQUE; TRANSGENIC MOUSE; TUMOR CELL LINE; UPREGULATION;

ANIMALS; CALCIUM SIGNALING; CELL LINE, TUMOR; CLONE CELLS; DOWN-REGULATION; FATTY ACIDS, NONESTERIFIED; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; GLUCOSE INTOLERANCE; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN SPECIFICITY; PALMITOYL-COA HYDROLASE; RATS; RECOMBINANT PROTEINS; SEX CHARACTERISTICS; TISSUE CULTURE TECHNIQUES; UP-REGULATION;

EID: 84964596770     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-1240     Document Type: Article

References (45)

1. Rutter GA, Pullen TJ, Hodson DJ, Martinez-Sanchez A. Pancreatic b-cell identity, glucose sensing and the control of insulin secretion. Biochem J 2015;466:203-218
2. Thorrez L, Laudadio I, Van Deun K, et al. Tissue-specific disallowance of housekeeping genes: the other face of cell differentiation. Genome Res 2011;21:95-105
3. Pullen TJ, Khan AM, Barton G, Butcher SA, Sun G, Rutter GA. Identification of genes selectively disallowed in the pancreatic islet. Islets 2010;2:89-95
4. Pullen TJ, Rutter GA. When less is more: the forbidden fruits of gene repression in the adult b-cell. Diabetes Obes Metab 2013;15:503-512
5. Sekine N, Cirulli V, Regazzi R, et al. Low lactate dehydrogenase and high mitochondrial glycerol phosphate dehydrogenase in pancreatic beta-cells. Potential role in nutrient sensing. J Biol Chem 1994;269:4895-4902
6. Otonkoski T, Kaminen N, Ustinov J, et al. Physical exercise-induced hyperinsulinemic hypoglycemia is an autosomal-dominant trait characterized by abnormal pyruvate-induced insulin release. Diabetes 2003;52:199-204
7. Pullen TJ, Sylow L, Sun G, Halestrap AP, Richter EA, Rutter GA. Overexpression of monocarboxylate transporter-1 (SLC16A1) in mouse pancreatic β-cells leads to relative hyperinsulinism during exercise. Diabetes 2012;61:1719-1725
8. Ainscow EK, Zhao C, Rutter GA. Acute overexpression of lactate dehydrogenase-A perturbs beta-cell mitochondrial metabolism and insulin secretion. Diabetes 2000;49:1149-1155
9. Chen H, Gu X, Liu Y, et al. PDGF signalling controls age-dependent proliferation in pancreatic β-cells. Nature 2011;478:349-355
10. Yamada J, Matsumoto I, Furihata T, Sakuma M, Suga T. Purification and properties of long-chain acyl-CoA hydrolases from the liver cytosol of rats treated with peroxisome proliferator. Arch Biochem Biophys 1994;308:118-125
11. Hunt MC, Yamada J, Maltais LJ, Wright MW, Podesta EJ, Alexson SE. A revised nomenclature for mammalian acyl-CoA thioesterases/hydrolases. J Lipid Res 2005;46:2029-2032
12. Hunt MC, Greene S, Hultenby K, Svensson LT, Engberg S, Alexson SE. Alternative exon usage selectively determines both tissue distribution and subcellular localization of the acyl-CoA thioesterase 7 gene products. Cell Mol Life Sci 2007;64:1558-1570
13. Yamada J. Long-chain acyl-CoA hydrolase in the brain. Amino Acids 2005;28:273-278
14. Sakuma S, Fujimoto Y, Sawada T, Saeki K, Akimoto M, Fujita T. Existence of acyl-CoA hydrolase-mediated pathway supplying arachidonic acid for prostaglandin synthesis in microsomes from rabbit kidney medulla. Prostaglandins Other Lipid Mediat 1999;57:63-72
15. Ellis JM, Wong GW, Wolfgang MJ. Acyl coenzyme A thioesterase 7 regulates neuronal fatty acid metabolism to prevent neurotoxicity. Mol Cell Biol 2013;33:1869-1882
16. Parton LE, McMillen PJ, Shen Y, et al. Limited role for SREBP-1c in defective glucose-induced insulin secretion from Zucker diabetic fatty rat islets: a functional and gene profiling analysis. Am J Physiol Endocrinol Metab 2006;291:E982-E994
17. Marselli L, Thorne J, Dahiya S, et al. Gene expression profiles of beta-cell enriched tissue obtained by laser capture microdissection from subjects with type 2 diabetes. PLoS One 2010;5:e11499
18. Prentki M, Matschinsky FM, Madiraju SR. Metabolic signaling in fuelinduced insulin secretion. Cell Metab 2013;18:162-185
19. Trapnell C, Roberts A, Goff L, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012;7:562-578
20. Martinez-Sanchez A, Nguyen-Tu MS, Rutter GA. DICER inactivation identifies pancreatic β-cell "disallowed" genes targeted by microRNAs. Mol Endocrinol 2015;29:1067-1079
21. Varadi A, Ainscow EK, Allan VJ, Rutter GA. Involvement of conventional kinesin in glucose-stimulated secretory granule movements and exocytosis in clonal pancreatic beta-cells. J Cell Sci 2002;115:4177-4189
22. Cnop M, Hannaert JC, Hoorens A, Eizirik DL, Pipeleers DG. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 2001;50:1771-1777
23. Sun G, Tarasov AI, McGinty JA, et al. LKB1 deletion with the RIP2. Cre transgene modifies pancreatic beta-cell morphology and enhances insulin secretion in vivo. Am J Physiol Endocrinol Metab 2010;298:E1261-E1273
24. Ravier MA, Rutter GA. Isolation and culture of mouse pancreatic islets for ex vivo imaging studies with trappable or recombinant fluorescent probes. Methods Mol Biol 2010;633:171-184
25. Hodson DJ, Tarasov AI, Gimeno Brias S, et al. Incretin-modulated beta cell energetics in intact islets of Langerhans. Mol Endocrinol 2014;28:860-871
26. Tarasov AI, Semplici F, Ravier MA, et al. The mitochondrial Ca2+ uniporter MCU is essential for glucose-induced ATP increases in pancreatic β-cells. PLoS One 2012;7:e39722
27. Wikstrom JD, Sereda SB, Stiles L, et al. A novel high-throughput assay for islet respiration reveals uncoupling of rodent and human islets. PLoS One 2012;7:e33023
28. Tantama M, Martínez-François JR, Mongeon R, Yellen G. Imaging energy status in live cells with a fluorescent biosensor of the intracellular ATP-to-ADP ratio. Nat Commun 2013;4:2550
29. Schug ZT, Peck B, Jones DT, et al. Acetyl-CoA synthetase 2 promotes acetate utilization and maintains cancer cell growth under metabolic stress. Cancer Cell 2015;27:57-71
30. Miyazaki J, Araki K, Yamato E, et al. Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 1990;127:126-132
31. Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, Newgard CB. Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channeldependent and -independent glucose-stimulated insulin secretion. Diabetes 2000;49:424-430
32. Milo-Landesman D, Surana M, Berkovich I, et al. Correction of hyperglycemia in diabetic mice transplanted with reversibly immortalized pancreatic beta cells controlled by the TET-on regulatory system. Cell Transplant 2001;10:645-650
33. Wicksteed B, Brissova M, Yan W, et al. Conditional gene targeting in mouse pancreatic β-cells: analysis of ectopic Cre transgene expression in the brain. Diabetes 2010;59:3090-3098
34. Van Heek M, Compton DS, France CF, et al. Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J Clin Invest 1997;99:385-390
35. Tarasov AI, Griffiths EJ, Rutter GA. Regulation of ATP production by mitochondrial Ca (2+). Cell Calcium 2012;52:28-35
36. Piccand J, Strasser P, Hodson DJ, et al. Rfx6 maintains the functional identity of adult pancreatic β cells. Cell Reports 2014;9:2219-2232
37. Hodson DJ, Schaeffer M, Romanò N, et al. Existence of long-lasting experience-dependent plasticity in endocrine cell networks. Nat Commun 2012;3:605
38. McTaggart LR, Richardson SE, Witkowska M, Zhang SX. Phylogeny and identification of Nocardia species on the basis of multilocus sequence analysis. J Clin Microbiol 2010;48:4525-4533
39. Rutter GA. Visualising insulin secretion. The Minkowski Lecture 2004. Diabetologia 2004;47:1861-1872
40. Tarasov AI, Nicolson TJ, Riveline JP, et al. A rare mutation in ABCC8/SUR1 leading to altered ATP-sensitive K+ channel activity and beta-cell glucose sensing is associated with type 2 diabetes in adults. Diabetes 2008;57:1595-1604
41. Hunt MC, Alexson SE. The role acyl-CoA thioesterases play in mediating intracellular lipid metabolism. Prog Lipid Res 2002;41:99-130
42. Donath MY, Ehses JA, Maedler K, et al. Mechanisms of beta-cell death in type 2 diabetes. Diabetes 2005;54(Suppl. 2):S108-S113
43. Klett EL, Chen S, Edin ML, et al. Diminished acyl-CoA synthetase isoform 4 activity in INS 832/13 cells reduces cellular epoxyeicosatrienoic acid levels and results in impaired glucose-stimulated insulin secretion. J Biol Chem 2013;288:21618-21629
44. Corkey BE, Deeney JT, Yaney GC, Tornheim K, Prentki M. The role of longchain fatty acyl-CoA esters in beta-cell signal transduction. J Nutr 2000;130(Suppl.):299S-304S
45. Rorsman P, Renström E. Insulin granule dynamics in pancreatic beta cells. Diabetologia 2003;46:1029-1045