A Role for Cytosolic Isocitrate Dehydrogenase as a Negative Regulator of Glucose Signaling for Insulin Secretion in Pancreatic ß-Cells

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Guay, Claudiane ^a   Joly, Érik ^a   Pepin, Émilie ^a   Barbeau, Annie ^a   Hentsch, Lisa ^a   Pineda, Marco ^a   Madiraju, S R Murthy ^a   Brunengraber, Henri ^c   Prentki, Marc ^a,b  

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

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; ISOCITRATE DEHYDROGENASE; MALATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PYRUVATE CARBOXYLASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; DNA SEQUENCE; DOWN REGULATION; ENZYME ACTIVITY; FATTY ACID METABOLISM; GENE AMPLIFICATION; GENE REPRESSION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; INSULIN RELEASE; LIPOGENESIS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE, TUMOR; CYTOSOL; ENERGY METABOLISM; FATTY ACIDS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE KNOCKDOWN TECHNIQUES; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; ISOCITRATE DEHYDROGENASE; RATS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84885402048     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077097     Document Type: Article

References (80)

1. Prentki M, Matschinsky FM, Madiraju SR, (2013) Metabolic signaling in fuel-induced insulin secretion. Cell Metab 18: 162-185.
2. Aguilar-Bryan L, Nichols CG, Wechsler SW, Clement JPt, Boyd AE 3rd, et al. (1995) Cloning of the beta cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 268: 423-426.
3. Ashcroft FM, Harrison DE, Ashcroft SJ, (1984) Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature 312: 446-448.
4. Straub SG, Sharp GW, (2002) Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab Res Rev 18: 451-463.
5. Ashcroft FM, (1991) Ca2+ channels and excitation-contraction coupling. Curr Opin Cell Biol 3: 671-675.
6. Henquin JC, (1992) Adenosine triphosphate-sensitive K+ channels may not be the sole regulators of glucose-induced electrical activity in pancreatic B-cells. Endocrinology 131: 127-131.
7. Corkey BE, Glennon MC, Chen KS, Deeney JT, Matschinsky FM, et al. (1989) A role for malonyl-CoA in glucose-stimulated insulin secretion from clonal pancreatic beta-cells. J Biol Chem 264: 21608-21612.
8. Prentki M, Vischer S, Glennon MC, Regazzi R, Deeney JT, et al. (1992) Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J Biol Chem 267: 5802-5810.
9. Fahien LA, MacDonald MJ, (2002) The succinate mechanism of insulin release. Diabetes 51: 2669-2676.
10. Maechler P, Wollheim CB, (1999) Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature 402: 685-689.
11. Kibbey RG, Pongratz RL, Romanelli AJ, Wollheim CB, Cline GW, et al. (2007) Mitochondrial GTP regulates glucose-stimulated insulin secretion. Cell Metab 5: 253-264.
12. Pi J, Bai Y, Zhang Q, Wong V, Floering LM, et al. (2007) Reactive oxygen species as a signal in glucose-stimulated insulin secretion. Diabetes 56: 1783-1791.
13. Leloup C, Tourrel-Cuzin C, Magnan C, Karaca M, Castel J, et al. (2009) Mitochondrial reactive oxygen species are obligatory signals for glucose-induced insulin secretion. Diabetes 58: 673-681.
14. MacDonald MJ, (1995) Feasibility of a mitochondrial pyruvate malate shuttle in pancreatic islets. Further implication of cytosolic NADPH in insulin secretion. J Biol Chem 270: 20051-20058.
15. Ivarsson R, Quintens R, Dejonghe S, Tsukamoto K, In 't Veld P, et al. (2005) Redox control of exocytosis: regulatory role of NADPH, thioredoxin, and glutaredoxin. Diabetes 54: 2132-2142.
16. MacDonald MJ, Fahien LA, Brown LJ, Hasan NM, Buss JD, et al. (2005) Perspective: emerging evidence for signaling roles of mitochondrial anaplerotic products in insulin secretion. Am J Physiol Endocrinol Metab 288: E1-15.
17. Maechler P, Kennedy ED, Pozzan T, Wollheim CB, (1997) Mitochondrial activation directly triggers the exocytosis of insulin in permeabilized pancreatic beta-cells. Embo J 16: 3833-3841.
18. Khan A, Ling ZC, Landau BR, (1996) Quantifying the carboxylation of pyruvate in pancreatic islets. J Biol Chem 271: 2539-2542.
19. MacDonald MJ, (1993) Glucose enters mitochondrial metabolism via both carboxylation and decarboxylation of pyruvate in pancreatic islets. Metabolism 42: 1229-1231.
20. Schuit F, De Vos A, Farfari S, Moens K, Pipeleers D, et al. (1997) Metabolic fate of glucose in purified islet cells. Glucose-regulated anaplerosis in beta cells. J Biol Chem 272: 18572-18579.
21. Farfari S, Schulz V, Corkey B, Prentki M, (2000) Glucose-regulated anaplerosis and cataplerosis in pancreatic beta-cells: possible implication of a pyruvate/citrate shuttle in insulin secretion. Diabetes 49: 718-726.
22. Liu YQ, Jetton TL, Leahy JL, (2002) beta-Cell adaptation to insulin resistance. Increased pyruvate carboxylase and malate-pyruvate shuttle activity in islets of nondiabetic Zucker fatty rats. J Biol Chem 277: 39163-39168.
23. Lu D, Mulder H, Zhao P, Burgess SC, Jensen MV, et al. (2002) 13C NMR isotopomer analysis reveals a connection between pyruvate cycling and glucose-stimulated insulin secretion (GSIS). Proc Natl Acad Sci U S A 99: 2708-2713.
24. Pongratz RL, Kibbey RG, Shulman GI, Cline GW, (2007) Cytosolic and mitochondrial malic enzyme isoforms differentially control insulin secretion. J Biol Chem 282: 200-207.
25. Xu J, Han J, Long YS, Lock J, Weir GC, et al. (2008) Malic enzyme is present in mouse islets and modulates insulin secretion. Diabetologia 51: 2281-2289.
26. Guay C, Madiraju SR, Aumais A, Joly E, Prentki M, (2007) A role for ATP-citrate lyase, malic enzyme, and pyruvate/citrate cycling in glucose-induced insulin secretion. J Biol Chem 282: 35657-35665.
27. Ronnebaum SM, Ilkayeva O, Burgess SC, Joseph JW, Lu D, et al. (2006) A pyruvate cycling pathway involving cytosolic NADP-dependent isocitrate dehydrogenase regulates glucose-stimulated insulin secretion. J Biol Chem 281: 30593-30602.
28. Lorenz MA, El-Azzouny MA, Kennedy RT, Burant CF, (2013) Metabolome Response to Glucose in the beta-cell line INS-1 832/13. J Biol Chem.
29. Hedeskov CJ, Capito K, Thams P, (1987) Cytosolic ratios of free [NADPH]/[NADP+] and [NADH]/[NAD+] in mouse pancreatic islets, and nutrient-induced insulin secretion. Biochem J 241: 161-167.
30. Reinbothe TM, Ivarsson R, Li DQ, Niazi O, Jing X, et al. (2009) Glutaredoxin-1 mediates NADPH-dependent stimulation of calcium-dependent insulin secretion. Mol Endocrinol 23: 893-900.
31. Brown LJ, Longacre MJ, Hasan NM, Kendrick MA, Stoker SW, et al. (2009) Chronic reduction of the cytosolic or mitochondrial NAD(P)-malic enzyme does not affect insulin secretion in a rat insulinoma cell line. J Biol Chem 284: 35359-35367.
32. Ronnebaum SM, Jensen MV, Hohmeier HE, Burgess SC, Zhou YP, et al. (2008) Silencing of cytosolic or mitochondrial isoforms of malic enzyme has no effect on glucose-stimulated insulin secretion from rodent islets. J Biol Chem 283: 28909-28917.
33. Comte B, Vincent G, Bouchard B, Benderdour M, Des Rosiers C, (2002) Reverse flux through cardiac NADP(+)-isocitrate dehydrogenase under normoxia and ischemia. Am J Physiol Heart Circ Physiol 283: H1505-1514.
34. Sazanov LA, Jackson JB, (1994) Proton-translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Lett 344: 109-116.
35. Sies H, Akerboom TP, Tager JM, (1977) Mitochondrial and cytosolic NADPH systems and isocitrate dehydrogenase indicator metabolites during ureogensis from ammonia in isolated rat hepatocytes. Eur J Biochem 72: 301-307.
36. Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, et al. (2000) Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and-independent glucose-stimulated insulin secretion. Diabetes 49: 424-430.
37. Gotoh M, Maki T, Satomi S, Porter J, Bonner-Weir S, et al. (1987) Reproducible high yield of rat islets by stationary in vitro digestion following pancreatic ductal or portal venous collagenase injection. Transplantation 43: 725-730.
38. Joseph JW, Jensen MV, Ilkayeva O, Palmieri F, Alarcon C, et al. (2006) The mitochondrial citrate/isocitrate carrier plays a regulatory role in glucose-stimulated insulin secretion. J Biol Chem 281: 35624-35632.
39. Joseph JW, Odegaard ML, Ronnebaum SM, Burgess SC, Muehlbauer J, et al. (2007) Normal flux through ATP-citrate lyase or fatty acid synthase is not required for glucose-stimulated insulin secretion. J Biol Chem 282: 31592-31600.
40. Jensen MV, Joseph JW, Ilkayeva O, Burgess S, Lu D, et al. (2006) Compensatory responses to pyruvate carboxylase suppression in islet beta-cells. Preservation of glucose-stimulated insulin secretion. J Biol Chem 281: 22342-22351.
41. Bonnerot C, Rocancourt D, Briand P, Grimber G, Nicolas JF, (1987) A beta-galactosidase hybrid protein targeted to nuclei as a marker for developmental studies. Proc Natl Acad Sci U S A 84: 6795-6799.
42. Massie B, Couture F, Lamoureux L, Mosser DD, Guilbault C, et al. (1998) Inducible overexpression of a toxic protein by an adenovirus vector with a tetracycline-regulatable expression cassette. J Virol 72: 2289-2296.
43. Roduit R, Morin J, Masse F, Segall L, Roche E, et al. (2000) Glucose down-regulates the expression of the peroxisome proliferator-activated receptor-alpha gene in the pancreatic beta-cell. J Biol Chem 275: 35799-35806.
44. Fulgencio JP, Kohl C, Girard J, Pegorier JP, (1996) Troglitazone inhibits fatty acid oxidation and esterification, and gluconeogenesis in isolated hepatocytes from starved rats. Diabetes 45: 1556-1562.
45. Roduit R, Nolan C, Alarcon C, Moore P, Barbeau A, et al. (2004) 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 53: 1007-1019.
46. Roche E, Farfari S, Witters LA, Assimacopoulos-Jeannet F, Thumelin S, et al. (1998) Long-term exposure of beta-INS cells to high glucose concentrations increases anaplerosis, lipogenesis, and lipogenic gene expression. Diabetes 47: 1086-1094.
47. McGarry JD, Foster DW, (1976) An improved and simplified radioisotopic assay for the determination of free and esterified carnitine. J Lipid Res 17: 277-281.
48. Iezzi M, Regazzi R, Wollheim CB, (2000) The Rab3-interacting molecule RIM is expressed in pancreatic beta-cells and is implicated in insulin exocytosis. FEBS Lett 474: 66-70.
49. Lilja L, Johansson JU, Gromada J, Mandic SA, Fried G, et al. (2004) Cyclin-dependent kinase 5 associated with p39 promotes Munc18-1 phosphorylation and Ca(2+)-dependent exocytosis. J Biol Chem 279: 29534-29541.
50. Lewis GD, Wei R, Liu E, Yang E, Shi X, et al. (2008) Metabolite profiling of blood from individuals undergoing planned myocardial infarction reveals early markers of myocardial injury. J Clin Invest 118: 3503-3512.
51. Luo B, Groenke K, Takors R, Wandrey C, Oldiges M, (2007) Simultaneous determination of multiple intracellular metabolites in glycolysis, pentose phosphate pathway and tricarboxylic acid cycle by liquid chromatography-mass spectrometry. J Chromatogr A 1147: 153-164.
52. Qian T, Cai Z, Yang MS, (2004) Determination of adenosine nucleotides in cultured cells by ion-pairing liquid chromatography-electrospray ionization mass spectrometry. Anal Biochem 325: 77-84.
53. MacDonald MJ, Smith AD 3rd, Hasan NM, Sabat G, Fahien LA, (2007) Feasibility of pathways for transfer of acyl groups from mitochondria to the cytosol to form short chain acyl-CoAs in the pancreatic beta cell. J Biol Chem 282: 30596-30606.
54. Hasan NM, Longacre MJ, Stoker SW, Boonsaen T, Jitrapakdee S, et al. (2008) Impaired anaplerosis and insulin secretion in insulinoma cells caused by small interfering RNA-mediated suppression of pyruvate carboxylase. J Biol Chem 283: 28048-28059.
55. Henquin JC, (2000) Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49: 1751-1760.
56. Nolan CJ, Prentki M, (2008) The islet beta-cell: fuel responsive and vulnerable. Trends Endocrinol Metab 19: 285-291.
57. Li D, Yin X, Zmuda EJ, Wolford CC, Dong X, et al. (2008) The repression of IRS2 gene by ATF3, a stress-inducible gene, contributes to pancreatic beta-cell apoptosis. Diabetes 57: 635-644.
58. Icyuz M, Bryant SM, Fortinberry HK, Molakandov K, Siegal GP, et al. (2009) Adenovirus infection activates akt1 and induces cell proliferation in pancreatic islets1. Transplantation 87: 821-824.
59. Olofsson CS, Salehi A, Holm C, Rorsman P, (2004) Palmitate increases L-type Ca2+ currents and the size of the readily releasable granule pool in mouse pancreatic beta-cells. J Physiol 557: 935-948.
60. Kebede MA, Alquier T, Latour MG, Poitout V, (2009) Lipid receptors and islet function: therapeutic implications? Diabetes Obes Metab 11 Suppl 4: 10-20.
61. Nolan CJ, Madiraju MS, Delghingaro-Augusto V, Peyot ML, Prentki M, (2006) Fatty acid signaling in the beta-cell and insulin secretion. Diabetes 55 Suppl 2: S16-23.
62. Prentki M, Madiraju SR, (2012) Glycerolipid/free fatty acid cycle and islet beta-cell function in health, obesity and diabetes. Mol Cell Endocrinol 353: 88-100.
63. Jensen MV, Joseph JW, Ronnebaum SM, Burgess SC, Sherry AD, et al. (2008) Metabolic cycling in control of glucose-stimulated insulin secretion. Am J Physiol Endocrinol Metab 295: E1287-1297.
64. Takahashi N, Kadowaki T, Yazaki Y, Ellis-Davies GC, Miyashita Y, et al. (1999) Post-priming actions of ATP on Ca2+-dependent exocytosis in pancreatic beta cells. Proc Natl Acad Sci U S A 96: 760-765.
65. Prentki M, Matschinsky FM, (1987) Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol Rev 67: 1185-1248.
66. Rutter GA, Da Silva Xavier G, Leclerc I, (2003) Roles of 5′-AMP-activated protein kinase (AMPK) in mammalian glucose homoeostasis. Biochem J 375: 1-16.
67. Matschinsky FM, (1996) Banting Lecture 1995. A lesson in metabolic regulation inspired by the glucokinase glucose sensor paradigm. Diabetes 45: 223-241.
68. Peyot ML, Gray JP, Lamontagne J, Smith PJ, Holz GG, et al. (2009) Glucagon-like peptide-1 induced signaling and insulin secretion do not drive fuel and energy metabolism in primary rodent pancreatic beta-cells. PLoS One 4: e6221.
69. Hillgartner FB, Salati LM, Goodridge AG, (1995) Physiological and molecular mechanisms involved in nutritional regulation of fatty acid synthesis. Physiol Rev 75: 47-76.
70. Brun T, Roche E, Assimacopoulos-Jeannet F, Corkey BE, Kim KH, et al. (1996) Evidence for an anaplerotic/malonyl-CoA pathway in pancreatic beta-cell nutrient signaling. Diabetes 45: 190-198.
71. Tiano JP, Delghingaro-Augusto V, Le May C, Liu S, Kaw MK, et al. (2011) Estrogen receptor activation reduces lipid synthesis in pancreatic islets and prevents beta cell failure in rodent models of type 2 diabetes. J Clin Invest 121: 3331-3342.
72. Lee SM, Koh HJ, Park DC, Song BJ, Huh TL, et al. (2002) Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radic Biol Med 32: 1185-1196.
73. Jo SH, Son MK, Koh HJ, Lee SM, Song IH, et al. (2001) Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J Biol Chem 276: 16168-16176.
74. Lee SM, Park SY, Shin SW, Kil IS, Yang ES, et al. (2009) Silencing of cytosolic NADP(+)-dependent isocitrate dehydrogenase by small interfering RNA enhances the sensitivity of HeLa cells toward staurosporine. Free Radic Res 43: 165-173.
75. Kim SY, Lee SM, Tak JK, Choi KS, Kwon TK, et al. (2007) Regulation of singlet oxygen-induced apoptosis by cytosolic NADP+-dependent isocitrate dehydrogenase. Mol Cell Biochem 302: 27-34.
76. Kim SY, Park JW, (2003) Cellular defense against singlet oxygen-induced oxidative damage by cytosolic NADP+-dependent isocitrate dehydrogenase. Free Radic Res 37: 309-316.
77. Prentki M, (1996) New insights into pancreatic beta-cell metabolic signaling in insulin secretion. Eur J Endocrinol 134: 272-286.
78. Pepin E, Guay C, Delghingaro-Augusto V, Joly E, Madiraju SR, et al. (2010) Short-chain 3-hydroxyacyl-CoA dehydrogenase is a negative regulator of insulin secretion in response to fuel and non-fuel stimuli in INS832/13 beta-cells. J Diabetes 2: 157-167.
79. Li C, Chen P, Palladino A, Narayan S, Russell LK, et al. (2010) Mechanism of hyperinsulinism in short-chain 3-hydroxyacyl-CoA dehydrogenase deficiency involves activation of glutamate dehydrogenase. J Biol Chem 285: 31806-31818.
80. Khan A, Chandramouli V, Ostenson CG, Low H, Landau BR, et al. (1990) Glucose cycling in islets from healthy and diabetic rats. Diabetes 39: 456-459.