Downregulation of carnitine acyl-carnitine translocase by miRNAs 132 and 212 amplifies glucose-stimulated insulin secretion

Diabetes

Volumn 63, Issue 11, 2014, Pages 3805-3814

  Soni, Mufaddal S ^a   Rabaglia, Mary E ^a   Bhatnagar, Sushant ^a   Shang, Jin ^b   Ilkayeva, Olga ^c   Mynatt, Randall ^d   Zhou, Yun Ping ^b   Schadt, Eric E ^e   Thornberry, Nancy A ^b   Muoio, Deborah M ^c   Keller, Mark P ^a   Attie, Alan D ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARNITINE ACYL CARNITINE TRANSLOCASE; CARNITINE DERIVATIVE; CARRIER PROTEIN; ETHER DERIVATIVE; GLUCOSE; INSULIN; MICRORNA; MICRORNA 132; MICRORNA 212; PALMITOYLCARNITINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CARNITINE ACYLTRANSFERASE;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DOWN REGULATION; FATTY ACID OXIDATION; GENE; GENE AMPLIFICATION; GENE OVEREXPRESSION; HORMONE RESPONSE; INS 1 CELL LINE; INSULIN RELEASE; MITOCHONDRION; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; RAT; REGULATORY MECHANISM; SLC25A20 GENE; ANIMAL; CELL LINE; DRUG EFFECTS; GENETICS; METABOLISM; SECRETION (PROCESS);

ANIMALS; CARNITINE ACYLTRANSFERASES; CELL LINE; DOWN-REGULATION; GLUCOSE; INSULIN; MICE; MICRORNAS; RATS;

EID: 84908635307     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1677     Document Type: Article

References (58)

1. Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1963;1:785-789
2. Prentki M, Matschinsky FM, Madiraju SR. Metabolic signaling in fuel-induced insulin secretion. Cell Metab 2013;18:162-185
3. Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A. Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J Lipid Res 2009;50:3-21
4. Gremlich S, Bonny C, Waeber G, Thorens B. Fatty acids decrease IDX-1 expression in rat pancreatic islets and reduce GLUT2, glucokinase, insulin, and somatostatin levels. J Biol Chem 1997;272:30261-30269
5. Kelpe CL, Moore PC, Parazzoli SD, Wicksteed B, Rhodes CJ, Poitout V. Palmitate inhibition of insulin gene expression is mediated at the transcriptional level via ceramide synthesis. J Biol Chem 2003;278:30015-30021
6. Littman ED, Pitchumoni S, Garfinkel MR, Opara EC. Role of protein kinase C isoenzymes in fatty acid stimulation of insulin secretion. Pancreas 2000;20: 256-263
7. Yaney GC, Korchak HM, Corkey BE. Long-chain acyl CoA regulation of protein kinase C and fatty acid potentiation of glucose-stimulated insulin secretion in clonal beta-cells. Endocrinology 2000;141:1989-1998
8. Majumdar S, Rossi MW, Fujiki T, et al. Protein kinase C isotypes and signaling in neutrophils. Differential substrate specificities of a translocatable calcium- and phospholipid-dependent beta-protein kinase C and a phospholipiddependent protein kinase which is inhibited by long chain fatty acyl coenzyme A. J Biol Chem 1991;266:9285-9294
9. 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
10. Zhao E, Keller MP, Rabaglia ME, et al. Obesity and genetics regulate microRNAs in islets, liver, and adipose of diabetic mice. Mamm Genome 2009;20:476-485
11. Bhatnagar S, Oler AT, Rabaglia ME, et al. Positional cloning of a type 2 diabetes quantitative trait locus; tomosyn-2, a negative regulator of insulin secretion. PLoS Genet 2011;7:e1002323
12. Colca JR, Wolf BA, Comens PG, McDaniel ML. Protein phosphorylation in permeabilized pancreatic islet cells. Biochem J 1985;228:529-536
13. Su WL, Kleinhanz RR, Schadt EE. Characterizing the role of miRNAs within gene regulatory networks using integrative genomics techniques. Mol Syst Biol 2011;7:490
14. Brockenbrough JS, Korc M. Inhibition of epidermal growth factor binding in rat pancreatic acini by palmitoyl carnitine: evidence for Ca2+ and protein kinase C independent regulation. Cancer Res 1987;47:1805-1810
15. Ramachandran P, Fitzwater SP, Aneja S, et al. Prospective multi-centre sentinel surveillance for Haemophilus influenzae type b & other bacterial meningitis in Indian children. Indian J Med Res 2013;137:712-720
16. Jakupciak JP, Wang W, Markowitz ME, et al. Mitochondrial DNA as a cancer biomarker. J Mol Diagn 2005;7:258-267
17. Muoio DM, Noland RC, Kovalik JP, et al. Muscle-specific deletion of carnitine acetyltransferase compromises glucose tolerance and metabolic flexibility. Cell Metab 2012;15:764-777
18. Tan CP, Feng Y, Zhou YP, et al. Selective small-molecule agonists of G protein-coupled receptor 40 promote glucose-dependent insulin secretion and reduce blood glucose in mice. Diabetes 2008;57:2211-2219
19. Velasco R, Zharkikh A, Affourtit J, et al. The genome of the domesticated apple (Malus 3 domestica Borkh.). Nat Genet 2010;42:833-839
20. Nesca V, Guay C, Jacovetti C, et al. Identification of particular groups of microRNAs that positively or negatively impact on beta cell function in obese models of type 2 diabetes. Diabetologia 2013;56:2203-2212
21. Poy MN, Eliasson L, Krutzfeldt J, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004;432:226-230
22. Wang GL, Wang J, Douglas G, et al. Expanded molecular features of carnitine acyl-carnitine translocase (CACT) deficiency by comprehensive molecular analysis. Mol Genet Metab 2011;103:349-357
23. Garcia-Huidobro T, Valenzuela E, Leisewitz AV, Valderrama J, Bronfman M. Anti-proliferative effect of two novel palmitoyl-carnitine analogs, selective inhibitors of protein kinase C conventional isoenzymes. Eur J Biochem 1999;266: 855-864
24. Herrero L, Rubí B, Sebastián D, et al. Alteration of the malonyl-CoA/carnitine palmitoyltransferase I interaction in the beta-cell impairs glucose-induced insulin secretion. Diabetes 2005;54:462-471
25. Gremlich S, Nolan C, Roduit R, et al. Pancreatic islet adaptation to fasting is dependent on peroxisome proliferator-activated receptor alpha transcriptional upregulation of fatty acid oxidation. Endocrinology 2005;146:375-382
26. Tordjman K, Standley KN, Bernal-Mizrachi C, et al. PPARalpha suppresses insulin secretion and induces UCP2 in insulinoma cells. J Lipid Res 2002;43: 936-943
27. Mulder H, Lu D, Finley J 4th, et al. Overexpression of a modified human malonyl-CoA decarboxylase blocks the glucose-induced increase in malonyl-CoA level but has no impact on insulin secretion in INS-1-derived (832/13) beta-cells. J Biol Chem 2001;276:6479-6484
28. Boucher A, Lu D, Burgess SC, et al. Biochemical mechanism of lipidinduced impairment of glucose-stimulated insulin secretion and reversal with a malate analogue. J Biol Chem 2004;279:27263-27271
29. 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
30. Vo N, Klein ME, Varlamova O, et al. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci U S A 2005;102:16426-16431
31. Betel D, Koppal A, Agius P, Sander C, Leslie C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol 2010;11:R90
32. Prentki M, Matschinsky FM. Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol Rev 1987;67:1185-1248
33. Keller DM, Clark EA, Goodman RH. Regulation of microRNA-375 by cAMP in pancreatic β-cells. Mol Endocrinol 2012;26:989-999
34. Keller MP, Choi Y, Wang P, et al. A gene expression network model of type 2 diabetes links cell cycle regulation in islets with diabetes susceptibility. Genome Res 2008;18:706-716
35. Iacobazzi V, Invernizzi F, Baratta S, et al. Molecular and functional analysis of SLC25A20 mutations causing carnitine-acylcarnitine translocase deficiency. Hum Mutat 2004;24:312-320
36. York B, Reineke EL, Sagen JV, et al. Ablation of steroid receptor coactivator- 3 resembles the human CACT metabolic myopathy. Cell Metab 2012;15:752-763
37. Holland PC, Sherratt HS. Biochemical effects of the hypoglycaemic compound pent-4-enoic acid and related non-hypoglycaemic fatty acids. Effects of the free acids and their carnitine esters on coenzyme A-dependent oxidations in rat liver mitochondria. Biochem J 1973;136:157-171
38. Glasgow AM, Engel AG, Bier DM, et al. Hypoglycemia, hepatic dysfunction, muscle weakness, cardiomyopathy, free carnitine deficiency and long-chain acylcarnitine excess responsive to medium chain triglyceride diet. Pediatr Res 1983;17:319-326
39. Pepin E, Guay C, Delghingaro-Augusto V, Joly E, Madiraju SR, Prentki M. Short-chain 3-hydroxyacyl-CoA dehydrogenase is a negative regulator of insulin secretion in response to fuel and non-fuel stimuli in INS832/13 β-cells. J Diabetes 2010;2:157-167
40. Stein DT, Esser V, Stevenson BE, et al. Essentiality of circulating fatty acids for glucose-stimulated insulin secretion in the fasted rat. J Clin Invest 1996;97: 2728-2735
41. Roduit R, Nolan C, Alarcon C, et al. A role for the malonyl-CoA/long-chain acyl-CoA pathway of lipid signaling in the regulation of insulin secretion in response to both fuel and nonfuel stimuli. Diabetes 2004;53:1007-1019
42. Nałecz KA, Szczepankowska D, Czeredys M, Kulikova N, Grzes̈kiewicz S. Palmitoylcarnitine regulates estrification of lipids and promotes palmitoylation of GAP-43. FEBS Lett 2007;581:3950-3954
43. Sobiesiak-Mirska J, Nałecz MJ, Nałecz KA. Interaction of palmitoylcarnitine with protein kinase C in neuroblastoma NB-2a cells. Neurochem Int 2003;42:45-55
44. Katoh N, Wrenn RW, Wise BC, Shoji M, Kuo JF. Substrate proteins for calmodulin-sensitive and phospholipid-sensitive Ca2+-dependent protein kinases in heart, and inhibition of their phosphorylation by palmitoylcarnitine. Proc Natl Acad Sci U S A 1981;78:4813-4817
45. Johnson JE, Giorgione J, Newton AC. The C1 and C2 domains of protein kinase C are independent membrane targeting modules, with specificity for phosphatidylserine conferred by the C1 domain. Biochemistry 2000;39:11360-11369
46. Harris TE, Persaud SJ, Jones PM. Atypical isoforms of pKc and insulin secretion from pancreatic beta-cells: evidence using Gö 6976 and Ro 31-8220 as Pkc inhibitors. Biochem Biophys Res Commun 1996;227:672-676
47. Uchida T, Iwashita N, Ohara-Imaizumi M, et al. Protein kinase Cdelta plays a non-redundant role in insulin secretion in pancreatic beta cells. J Biol Chem 2007;282:2707-2716
48. Zhang H, Nagasawa M, Yamada S, Mogami H, Suzuki Y, Kojima I. Bimodal role of conventional protein kinase C in insulin secretion from rat pancreatic beta cells. J Physiol 2004;561:133-147
49. Schmitz-Peiffer C, Laybutt DR, Burchfield JG, et al. Inhibition of PKCepsilon improves glucose-stimulated insulin secretion and reduces insulin clearance. Cell Metab 2007;6:320-328
50. Sheu L, Pasyk EA, Ji J, et al. Regulation of insulin exocytosis by Munc13-1. J Biol Chem 2003;278:27556-27563
51. Zhao S, Mugabo Y, Iglesias J, et al. a/b-Hydrolase domain-6-accessible monoacylglycerol controls glucose-stimulated insulin secretion. Cell Metab 2014; 19:993-1007
52. Spedding M, Mir AK. Direct activation of Ca2+ channels by palmitoyl carnitine, a putative endogenous ligand. Br J Pharmacol 1987;92:457-468
53. Wu J, Corr PB. Influence of long-chain acylcarnitines on voltage-dependent calcium current in adult ventricular myocytes. Am J Physiol 1992;263:H410-H417
54. Liu QY, Rosenberg RL. Activation and inhibition of reconstituted cardiac L-type calcium channels by palmitoyl-L-carnitine. Biochem Biophys Res Commun 1996;228:252-258
55. Dumonteil E, Barré H, Meissner G. Effects of palmitoyl carnitine and related metabolites on the avian Ca(2+)-ATPase and Ca2+ release channel. J Physiol 1994;479:29-39
56. Haruna T, Horie M, Takano M, et al. Alteration of the membrane lipid environment by L-palmitoylcarnitine modulates K(ATP) channels in guinea-pig ventricular myocytes. Pflugers Arch 2000;441:200-207
57. Sampey BP, Freemerman AJ, Zhang J, et al. Metabolomic profiling reveals mitochondrial-derived lipid biomarkers that drive obesity-associated inflammation. PLoS ONE 2012;7:e38812
58. Koves TR, Ussher JR, Noland RC, et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 2008;7:45-56