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

Volumn 53, Issue 4, 2004, Pages 1007-1019

  Roduit, Raphaël ^a,g   Nolan, Christopher ^a   Alarcon, Cristina ^b   Moore, Patrick ^b   Barbeau, Annie ^a   Delghingaro Augusto, Viviane ^a   Przybykowski, Ewa ^a   Morin, Johane ^a   Massé, Frédéric ^a   Massie, Bernard ^c   Ruderman, Neil ^d   Rhodes, Christopher ^b,e   Poitout, Vincent ^b   Prentki, Marc ^a,f  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITY OF WASHINGTON   (United States)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d BOSTON MEDICAL CENTER   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^f CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^g LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; GLUCOSE; INSULIN; LIPID; LONG CHAIN FATTY ACID COENZYME A LIGASE; MALONYL COENZYME A; PALMITIC ACID; PSEUDOEPHEDRINE PLUS TRIPROLIDINE; TRIACSIN C; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ESTERIFICATION; EXOCYTOSIS; FATTY ACID METABOLISM; FATTY ACID OXIDATION; GENE OVEREXPRESSION; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; INSULIN RELEASE; LIPID ANALYSIS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 12144291143     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.53.4.1007     Document Type: Article

References (70)

1. Hedeskov CJ: Mechanism of glucose-induced insulin secretion. Physiol Rev 60:442-509, 1980
2. Matschinsky FM: Banting Lecture 1995: a lesson in metabolic regulation inspired by the glucokinase glucose sensor paradigm. Diabetes 45:223-241, 1996
3. Prentki M: New insights into pancreatic beta-cell metabolic signaling in insulin secretion. Eur J Endocrinol 134:272-286, 1996
4. Dobbins RL, Chester MW, Daniels MB, McGarry JD, Stein DT: Circulating fatty acids are essential for efficient glucose-stimulated insulin secretion after prolonged fasting in humans. Diabetes 47:1613-1618, 1998
5. Dobbins RL, Chester MW, Stevenson BE, Daniels MB, Stein DT, McGarry JD: A fatty acid-dependent step is critically important for both glucose- and non-glucose-stimulated insulin secretion. J Clin Invest 101:2370-2376, 1998
6. Stein DT, Esser V, Stevenson BE, Lane KE, Whiteside JH, Daniels MB, Chen S, McGarry JD: Essentiality of circulating fatty acids for glucose-stimulated insulin secretion in the fasted rat. J Clin Invest 97:2728-2735, 1996
7. Koyama K, Chen G, Wang MY, Lee Y, Shimabukuro M, Newgard CB, Unger RH: Beta-cell function in normal rats made chronically hyperleptinemic by adenovirus-leptin gene therapy. Diabetes 46:1276-1280, 1997
8. Chalkley SM, Kraegen EW, Furler SM, Campbell LV, Chisholm DJ: NEFA elevation during a hyperglycaemic clamp enhances insulin secretion. Diabet Med 15:327-333, 1998
9. Stein DT, Stevenson BE, Chester MW, Basit M, Daniels MB, Turley SD, McGarry JD: The insulinotropic potency of fatty acids is influenced profoundly by their chain length and degree of saturation. J Clin Invest 100:398-403, 1997
10. McGarry JD, Dobbins RL: Fatty acids, lipotoxicity and insulin secretion. Diabetologia 42:128-138, 1999
11. Unger RH: Lipotoxicity in the pathogenesis of obesity-dependent NIDDM: genetic and clinical implications. Diabetes 44:863-870, 1995
12. Prentki M, Joly E, El-Assaad W, Roduit R: Malonyl-CoA signaling, lipid partitioning, and glucolipotoxicity: role in β-cell adaptation and failure in the etiology of diabetes. Diabetes 51 (Suppl. 3):S405-S413, 2002
13. Prentki M, Corkey BE: Are the β-cell signaling molecules malonyl-CoA and cystolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 45:273-283, 1996
14. El-Assaad W, Buteau J, Peyot M-L, Nolan C, Roduit R, Hardy S, Joly E, Dbaibo G, Rosenberg L, Prentki M: Saturated fatty acids synergize with elevated glucose to cause pancreatic-cell death. Endocrinology: 144:4154-4163, 2003
15. Shimabukuro M, Zhou YT, Levi M, Unger RH: Fatty acid-induced beta cell apoptosis: a link between obesity and diabetes. Proc Natl Acad Sci U S A 95:2498-2502, 1998
16. Roduit R, Morin J, Masse F, Segall L, Roche E, Newgard CB, Assimacopoulos-Jeannet F, Prentki M: Glucose down-regulates the expression of the peroxisome proliferator-activated receptor-alpha gene in the pancreatic beta-cell. J Biol Chem 275:35799-35806, 2000
17. Prentki M, Matschinsky FM: Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol Rev 67:1185-1248, 1987
18. Yaney GC, Fairbanks JM, Deeney JT, Korchak HM, Tornheim K, Corkey BE: Potentiation of insulin secretion by phorbol esters is mediated by PKC-alpha and nPKC isoforms. Am J Physiol Endocrinol Metab 283:E880-E888, 2002
19. Meglasson MD, Matschinsky FM: Pancreatic islet glucose metabolism and regulation of insulin secretion. Diabetes Metab Rev 2:163-214, 1986
20. Newgard CB, McGarry JD: Metabolic coupling factors in pancreatic beta-cell signal transduction. Annu Rev Biochem 64:689-719, 1995
21. Ashcroft FM, Rorsman P: ATP-sensitive K+ channels: a link between B-cell metabolism and insulin secretion. Biochem Soc Trans 18:109-111, 1990
22. Deeney JT, Prentki M, Corkey BE: Metabolic control of beta-cell function. Semin Cell Dev Biol 11:267-275, 2000
23. ATP channel-independent signaling pathways in human islets. Diabetes 47:758-763, 1998
24. Aizawa T, Sato Y, Komatsu M: Importance of nonionic signals for glucose-induced biphasic insulin secretion. Diabetes 51 (Suppl. 1):S96-S98, 2002
25. Gembal M, Gilon P, Henquin JC: Evidence that glucose can control insulin release independently from its action on ATP-sensitive K+ channels in mouse B cells. J Clin Invest 89:1288-1295, 1992
26. 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 267:5802-5810, 1992
27. Corkey BE, Glennon MC, Chen KS, Deeney JT, Matschinsky FM, Prentki M: A role for malonyl-CoA in glucose-stimulated insulin secretion from clonal pancreatic beta-cells. J Biol Chem 264:21608-21612, 1989
28. Farfari S, Schulz V, Corkey B, Prentki M: Glucose-regulated anaplerosis and cataplerosis in pancreatic β-cells: possible implication of a pyruvate/ citrate shuttle in insulin secretion. Diabetes 49:718-726, 2000
29. Schuit F, De Vos A, Farfari S, Moens K, Pipeleers D, Brun T, Prentki M: Metabolic fate of glucose in purified islet cells: glucose-regulated anaplerosis in beta cells. J Biol Chem 272:18572-18579, 1997
30. Brun T, Roche E, Assimacopoulos-Jeannet F, Corkey BE, Kim KH, Prentki M: Evidence for an anaplerotic/malonyl-CoA pathway in pancreatic β-cell nutrient signaling. Diabetes 45:190-198, 1996
31. MacDonald MJ, Fahien LA, Buss JD, Hasan NM, Fallon MJ, Kendrick MA: Citrate oscillates in liver and pancreatic beta cell mitochondria and in INS-1 insulinoma cells. J Biol Chem 278:51894-51900, 2003
32. Liang Y, Matschinsky FM: Content of CoA-esters in perifused rat islets stimulated by glucose and other fuels. Diabetes 40:327-333, 1991
33. Malaisse WJ, Malaisse-Lagae F, Sener A, Hellerstrom C: Participation of endogenous fatty acids in the secretory activity of the pancreatic B-cell. Biochem J 227:995-1002, 1985
34. Chen S, Ogawa A, Ohneda M, Unger RH, Foster DW, McGarry JD: More direct evidence for a malonyl-CoA-carnitine palmitoyltransferase I interaction as a key event in pancreatic β-cell signaling. Diabetes 43:878-883, 1994
35. Segall L, Lameloise N, Assimacopoulos-Jeannet F, Roche E, Corkey P, Thumelin S, Corkey BE, Prentki M: Lipid rather than glucose metabolism is implicated in altered insulin secretion caused by oleate in INS-1 cells. Am J Physiol 277:E521-E528, 1999
36. Peter-Riesch B, Fathi M, Schlegel W, Wollheim CB: Glucose and carbachol generate 1,2-diacylglycerols by different mechanisms in pancreatic islets. J Clin Invest 81:1154-1161, 1988
37. Wolf BA, Williamson JR, Easom RA, Chang K, Sherman WR, Turk J: Diacylglycerol accumulation and microvascular abnormalities induced by elevated glucose levels. J Clin Invest 87:31-38, 1991
38. Deeney JT, Gromada J, Hoy M, Olsen HL, Rhodes CJ, Prentki M, Berggren PO, Corkey BE: Acute stimulation with long chain acyl-CoA enhances exocytosis in insulin-secreting cells (HIT T-15 and NMRI beta-cells). J Biol Chem 275:9363-9368, 2000
39. Roduit R, Masiello P, Wang SP, Li H, Mitchell GA, Prentki M: A role for hormone-sensitive lipase in glucose-stimulated insulin secretion: a study in hormone-sensitive lipase-deficient mice. Diabetes 50:1970-1975, 2001
40. Zhang S, Kim KH: Acetyl-CoA carboxylase is essential for nutrient-induced insulin secretion. Biochem Biophys Res Commun 229:701-705, 1996
41. Zhang S, Kim KH: Essential role of acetyl-CoA carboxylase in the glucose-induced insulin secretion in a pancreatic beta-cell line. Cell Signal 10:35-42, 1998
42. Flamez D, Berger V, Kruhoffer M, Orntoft T, Pipeleers D, Schuit FC: Critical role for cataplerosis via citrate in glucose-regulated insulin release. Diabetes 51:2018-2024, 2002
43. Rubi B, Antinozzi PA, Herrero L, Ishihara H, Asins G, Serra D, Wollheim CB, Maechler P, Hegardt FG: Adenovirus-mediated overexpression of liver carnitine palmitoyltransferase I in INS1E cells: effects on cell metabolism and insulin secretion. Biochem J 364:219-226, 2002
44. Antinozzi PA, Segall L, Prentki M, McGarry JD, Newgard CB: Molecular or pharmacologic perturbation of the link between glucose and lipid metabolism is without effect on glucose-stimulated insulin secretion: a re-evaluation of the long-chain acyl-CoA hypothesis. J Biol Chem 273:16146-16154, 1998
45. Mulder H, Lu D, Finley JT, An J, Cohen J, Antinozzi PA, McGarry JD, Newgard CB: 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 276:6479-6484, 2001
46. Roche E, Farfari S, Witters LA, Assimacopoulos-Jeannet F, Thumelin S, Brun T, Corkey BE, Saha AK, Prentki M: Long-term exposure of β-INS cells to high glucose concentrations increases anaplerosis, lipogenesis, and lipogenic gene expression. Diabetes 47:1086-1094, 1998
47. Massie B, Mosser DD, Koutroumanis M, Vitte-Mony I, Lamoureux L, Couture F, Paquet L, Guilbault C, Dionne J, Chahla D, Jolicoeur P, Langelier Y: New adenovirus vectors for protein production and gene transfer. Cytotechnology 28:53-64, 1998
48. Wang H, Iynedjian PB: Modulation of glucose responsiveness of insulinoma beta-cells by graded overexpression of glucokinase. Proc Natl Acad Sci U S A 94:4372-4377, 1997
49. Caron AW, Massie B, Mosser DD: Use of a micromanipulator for high-efficiency cloning of cells co-expressing fluorescent proteins. Methods Cell Sci 22:137-145, 2000
50. Massie B, Couture F, Lamoureux L, Mosser DD, Guilbault C, Jolicoeur P, Belanger F, Langelier Y: Inducible overexpression of a toxic protein by an adenovirus vector with a tetracycline-regulatable expression cassette. J Virol 72:2289-2296, 1998
51. Jani A, Lochmuller H, Acsadi G, Simoneau M, Huard J, Garnier A, Karpati G, Massie B: Generation, validation, and large scale production of adenoviral recombinants with large size inserts such as a 6.3 kb human dystrophin cDNA. J Virol Methods 64:111-124, 1997
52. 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+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49:424-430, 2000
53. Gotoh M, Maki T, Satomi S, Porter J, Bonner-Weir S, O'Hara CJ, Monaco AP: Reproducible high yield of rat islets by stationary in vitro digestion following pancreatic ductal or portal venous collagenase injection. Transplantation 43:725-730, 1987
54. Saha AK, Schwarsin AJ, Roduit R, Masse F, Kaushik V, Tornheim K, Prentki M, Ruderman NB: Activation of malonyl-CoA decarboxylase in rat skeletal muscle by contraction and the AMP-activated protein kinase activator 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside. J Biol Chem 275:24279-24283, 2000
55. Kudo N, Barr AJ, Barr RL, Desai S, Lopaschuk GD: High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 5′-AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J Biol Chem 270: 17513-17520, 1995
56. Voilley N, Roduit R, Vicaretti R, Bonny C, Waeber G, Dyck JR, Lopaschuk GD, Prentki M: Cloning and expression of rat pancreatic beta-cell malonyl-CoA decarboxylase. Biochem J 340 (Suppl.):213-217, 1999
57. Fulgencio JP, Kohl C, Girard J, Pegorier JP: Troglitazone inhibits fatty acid oxidation and esterification, and gluconeogenesis in isolated hepatocytes from starved rats. Diabetes 45:1556-1562, 1996
58. Briaud I, Harmon JS, Kelpe CL, Segu VB, Poitout V: Lipotoxicity of the pancreatic β-cell is associated with glucose-dependent esterification of fatty acids into neutral lipids. Diabetes 50:315-321, 2001
59. McGarry JD, Foster DW: An improved and simplified radioisotopic assay for the determination of free and esterified carnitine. J Lipid Res 17:277-281, 1976
60. Alarcon C, Wicksteed B, Prentki M, Corkey BE, Rhodes CJ: Succinate is a preferential metabolic stimulus-coupling signal for glucose-induced proinsulin biosynthesis. Diabetes 52:2496-2504, 2002
61. Bratanova-Tochkova TK, Cheng H, Daniel S, Gunawardana S, Liu YJ, Mulvaney-Musa J, Schermerhorn T, Straub SG, Yajima H, Sharp GW: Triggering and augmentation mechanisms, granule pools, and biphasic insulin secretion. Diabetes 51 (Suppl. 1):S83-S90, 2002
62. Fujita Y, Sasaki T, Fukui K, Kotani H, Kimura T, Hata Y, Sudhof TC, Scheller RH, Takai Y: Phosphorylation of Munc-18/n-Sec1/rbSec1 by protein kinase C: its implication in regulating the interaction of Munc-18/n-Sec1/ rbSec1 with syntaxin. J Biol Chem 271:7265-7268, 1996
63. Gonzalo S, Linder ME: SNAP-25 palmitoylation and plasma membrane targeting require a functional secretory pathway. Mol Biol Cell 9:585-597, 1998
64. Chapman ER, Blasi J, An S, Brose N, Johnston PA, Sudhof TC, Jahn R: Fatty acylation of synaptotagmin in PC12 cells and synaptosomes. Biochem Biophys Res Commun 225:326-332, 1996
65. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Sudhof TC, Takahashi M, Rosenmund C, Brose N: Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108:121-133, 2002
66. Sheu L, Pasyk EA, Ji J, Huang X, Gao X, Varoqueaux F, Brose N, Gaisano HY: Regulation of insulin exocytosis by munc13-1. J Biol Chem 278:27556-27563, 2003
67. Itoh Y, Kawamata Y, Harada M, Kobayashi M, Fujii R, Fukusumi S, Ogi K, Hosoya M, Tanaka Y, Uejima H, Tanaka H, Maruyama M, Satoh R, Okubo S, Kizawa H, Komatsu H, Matsumura F, Noguchi Y, Shinohara T, Hinuma S, Fujisawa Y, Fujino M: Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422:173-176, 2003
68. Kotarsky K, Nilsson NE, Flodgren E, Owman C, Olde B: A human cell surface receptor activated by free fatty acids and thiazolidinedione drugs. Biochem Biophys Res Commun 301:406-410, 2003
69. Briscoe CP, Tadayyon M, Andrews JL, Benson WG, Chambers JK, Eilert MM, Ellis C, Elshourbagy NA, Goetz AS, Minnick DT, Murdock PR, Sauls HR Jr, Shabon U, Spinage LD, Strum JC, Szekeres PG, Tan KB, Way JM, Ignar DM, Wilson S, Muir AI: The orphan G protein-coupled receptor GPR40 is activated by medium and long chain fatty acids. J Biol Chem 278:11303-11311, 2003
70. Cruz WS, Kwon G, Marshall CA, McDaniel ML, Semenkovich CF: Glucose and insulin stimulate heparin-releasable lipoprotein lipase activity in mouse islets and INS-1 cells: a potential link between insulin resistance and beta-cell dysfunction. J Biol Chem 276:12162-12168, 2001