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

Journal of Biological Chemistry

Volumn 288, Issue 30, 2013, Pages 21618-21629

  Klett, Eric L ^a   Chen, Shufen ^a   Edin, Matthew L ^b   Li, Lei O ^c   Ilkayeva, Olga ^d   Zeldin, Darryl C ^b   Newgard, Christopher B ^d   Coleman, Rosalind A ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c The University of North Carolina at Chapel Hill   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL-COA SYNTHETASE; BETA CELL; EPOXYEICOSATRIENOIC ACIDS; GLUCOSE-STIMULATED INSULIN SECRETIONS; INSULIN SECRETION; ISOFORMS; LIPID METABOLISMS; NOVEL STRATEGIES;

GLUCOSE; INSULIN; METABOLISM;

PHYSIOLOGY;

ACYL COA SYNTHETASE ISOFORM 4; ACYL COENZYME A; ARACHIDONIC ACID; EPOXYICOSATRIENOIC ACID; GLUCOSE; GLYCEROPHOSPHOLIPID; INSULIN; LINOLEIC ACID; LONG CHAIN ACYL COENZYME A; LONG CHAIN FATTY ACID COENZYME A LIGASE; MESSENGER RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACSL4 GENE; ACSL5 GENE; ANIMAL CELL; ARTICLE; CELL LEVEL; CELL MEMBRANE; CELL STRAIN; CELL STRAIN INS 13; CELL STRAIN INS 832; CONTROLLED STUDY; ENDOCRINE DISEASE; ENZYME ACTIVITY; ENZYME REGULATION; ESTERIFICATION; FATTY ACID OXIDATION; GENE SILENCING; GLUCOSE STIMULATED INSULIN SECRETION; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; RAT; REGULATORY MECHANISM;

ACYL-COA SYNTHETASE; ARACHIDONIC ACID; BETA-CELL; EICOSANOID; EPOXYEICOSATRIENOIC ACIDS; INSULIN SECRETION; POLYUNSATURATED FATTY ACIDS;

8,11,14-EICOSATRIENOIC ACID; ACYL COENZYME A; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; COENZYME A LIGASES; FATTY ACIDS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; GLYCEROPHOSPHOLIPIDS; INSULIN; INSULIN-SECRETING CELLS; INSULINOMA; MEMBRANE LIPIDS; MITOCHONDRIAL PROTEINS; OXIDATION-REDUCTION; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

EID: 84881248414     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.481077     Document Type: Article

References (47)

1. McGarry, J. D., and Dobbins, R. L. (1999) Fatty acids, lipotoxicity and insulin secretion. Diabetologia 42, 128-138
2. Stein, D. T., Esser, V., Stevenson, B. E., Lane, K. E., Whiteside, J. H., Daniels, M. B., Chen, S., and McGarry, J. D. (1996) Essentiality of circulating fatty acids for glucose-stimulated insulin secretion in the fasted rat. J. Clin. Invest. 97, 2728-2735
3. Corkey, B. E., Deeney, J. T., Yaney, G. C., Tornheim, K., and Prentki, M. (2000) The role of long chain fatty acyl-CoA esters in beta-cell signal transduction. J. Nutr. 130, 299S-304S
4. Corkey, B. E., Glennon, M. C., Chen, K. S., Deeney, J. T., Matschinsky, F. M., and Prentki, M. (1989) A role for malonyl-CoA in glucose-stimulated insulin secretion from clonal pancreatic beta-cells. J. Biol. Chem. 264, 21608-21612
5. Prentki, M., Vischer, S., Glennon, M. C., Regazzi, R., Deeney, J. T., and Corkey, B. E. (1992) Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J. Biol. Chem. 267, 5802-5810
6. Alquier, T., Peyot, M. L., Latour, M. G., Kebede, M., Sorensen, C. M., Gesta, S., Kahn, C. R., Smith, R. D., Jetton, T. L., Metz, T. O., Prentki, M., and Poitout, V. (2009) Deletion of GPR40 impairs glucose-induced insulin secretion in vivo in mice without affecting intracellular fuel metabolism in islets. Diabetes 58, 2607-2615
7. 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., and Fujino, M. (2003) Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422, 173-176
8. Yaney, G. C., and Corkey, B. E. (2003) Fatty acid metabolism and insulin secretion in pancreatic beta cells. Diabetologia 46, 1297-1312
9. Ramanadham, S., Bohrer, A., Mueller, M., Jett, P., Gross, R. W., and Turk, J. (1993) Mass spectrometric identification and quantitation of arachidonate-containing phospholipids in pancreatic islets: prominence of plasmenylethanolamine molecular species. Biochemistry 32, 5339-5351
10. Turk, J., Colca, J. R., Kotagal, N., and McDaniel, M. L. (1984) Arachidonic acid metabolism in isolated pancreatic islets. II. The effects of glucose and of inhibitors of arachidonate metabolism on insulin secretion and metabolite synthesis. Biochim. Biophys. Acta 794, 125-136
11. 2+ mobilization by arachidonic acid. Comparison with myoinositol 1,4,5-trisphosphate in isolated pancreatic islets. J. Biol. Chem. 261, 3501-3511
12. Wolf, B. A., Pasquale, S. M., and Turk, J. (1991) Free fatty acid accumulation in secretagogue-stimulated pancreatic islets and effects of arachidonate on depolarization-induced insulin secretion. Biochemistry 30, 6372-6379
13. Bao, S., Bohrer, A., Ramanadham, S., Jin, W., Zhang, S., and Turk, J. (2006) Effects of stable suppression of Group VIA phospholipase A2 expression on phospholipid content and composition, insulin secretion, and proliferation of INS-1 insulinoma cells. J. Biol. Chem. 281, 187-198
14. Bao, S., Song, H., Wohltmann, M., Ramanadham, S., Jin, W., Bohrer, A., and Turk, J. (2006) Insulin secretory responses and phospholipid composition of pancreatic islets from mice that do not express Group VIA phospholipase A2 and effects of metabolic stress on glucose homeostasis. J. Biol. Chem. 281, 20958-20973
15. Kelly, K. L., and Laychock, S. G. (1981) Prostaglandin synthesis and metabolism in isolated pancreatic islets of the rat. Prostaglandins 21, 759-769
16. Zeldin, D. C., Foley, J., Boyle, J. E., Moomaw, C. R., Tomer, K. B., Parker, C., Steenbergen, C., and Wu, S. (1997) Predominant expression of an arachidonate epoxygenase in islets of Langerhans cells in human and rat pancreas. Endocrinology 138, 1338-1346
17. Falck, J. R., Manna, S., Moltz, J., Chacos, N., and Capdevila, J. (1983) Epoxyeicosatrienoic acids stimulate glucagon and insulin release from isolated rat pancreatic islets. Biochem. Biophys. Res. Commun. 114, 743-749
18. Coleman, R. A., Lewin, T. M., Van Horn, C. G., and Gonzalez-Baro, M. R. (2002) Do long chain acyl-CoA synthetases regulate fatty acid entry into synthetic versus degradative pathways? J. Nutr. 132, 2123-2126
19. Ellis, J. M., Mentock, S. M., Depetrillo, M. A., Koves, T. R., Sen, S., Watkins, S. M., Muoio, D. M., Cline, G. W., Taegtmeyer, H., Shulman, G. I., Willis, M. S., and Coleman, R. A. (2011) Mouse cardiac acyl coenzyme a synthetase 1 deficiency impairs fatty acid oxidation and induces cardiac hypertrophy. Mol. Cell. Biol. 31, 1252-1262
20. Li, L. O., Ellis, J. M., Paich, H. A., Wang, S., Gong, N., Altshuller, G., Thresher, R. J., Koves, T. R., Watkins, S. M., Muoio, D. M., Cline, G. W., Shulman, G. I., and Coleman, R. A. (2009) Liver-specific loss of long chain acyl-CoA synthetase-1 decreases triacylglycerol synthesis and beta-oxidation and alters phospholipid fatty acid composition. J. Biol. Chem. 284, 27816-27826
21. Hohmeier, H. E., Mulder, H., Chen, G., Henkel-Rieger, R., Prentki, M., and Newgard, C. B. (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
22. Cao, Y., Dave, K. B., Doan, T. P., and Prescott, S. M. (2001) Fatty acid CoA ligase 4 is up-regulated in colon adenocarcinoma. Cancer Res. 61, 8429-8434
23. Polokoff, M. A., and Bell, R. M. (1978) Limited palmitoyl-CoA penetration into microsomal vesicles as evidenced by a highly latent ethanol acyltransferase activity. J. Biol. Chem. 253, 7173-7178
24. Kim, J. H., Lewin, T. M., and Coleman, R. A. (2001) Expression and characterization of recombinant rat Acyl-CoA synthetases 1, 4, and 5. Selective inhibition by triacsin C and thiazolidinediones. J. Biol. Chem. 276, 24667-24673
25. Hosaka, K., Mishina, M., Tanaka, T., Kamiryo, T., and Numa, S. (1979) Acyl-coenzyme-A synthetase I from Candida lipolytica. Purification, properties and immunochemical studies. Eur. J. Biochem. 93, 197-203
26. Igal, R. A., Wang, P., and Coleman, R. A. (1997) Triacsin C blocks de novo synthesis of glycerolipids and cholesterol esters but not recycling of fatty acid into phospholipid. Evidence for functionally separate pools of acyl-CoA. Biochem. J. 324, 529-534
27. Weintraub, N. L., Fang, X., Kaduce, T. L., VanRollins, M., Chatterjee, P., and Spector, A. A. (1999) Epoxide hydrolases regulate epoxyeicosatrienoic acid incorporation into coronary endothelial phospholipids. Am. J. Physiol. 277, H2098-H2108
28. Edin, M. L., Wang, Z., Bradbury, J. A., Graves, J. P., Lih, F. B., DeGraff, L. M., Foley, J. F., Torphy, R., Ronnekleiv, O. K., Tomer, K. B., Lee, C. R., and Zeldin, D. C. (2011) Endothelial expression of human cytochrome P450 epoxygenase CYP2C8 increases susceptibility to ischemia-reperfusion injury in isolated mouse heart. FASEB J. 25, 3436-3447
29. Magnes, C., Sinner, F. M., Regittnig, W., and Pieber, T. R. (2005) LC/ MS/MS method for quantitative determination of long chain fatty acyl-CoAs. Anal. Chem. 77, 2889-2894
30. Deutsch, J., Grange, E., Rapoport, S. I., and Purdon, A. D. (1994) Isolation and quantitation of long chain acyl-coenzyme A esters in brain tissue by solid-phase extraction. Anal. Biochem. 220, 321-323
31. Minkler, P. E., Kerner, J., Ingalls, S. T., and Hoppel, C. L. (2008) Novel isolation procedure for short-, medium-, and long chain acyl-coenzyme A esters from tissue. Anal. Biochem. 376, 275-276
32. Kang, M. J., Fujino, T., Sasano, H., Minekura, H., Yabuki, N., Nagura, H., Iijima, H., and Yamamoto, T. T. (1997) A novel arachidonate-preferring acyl-CoA synthetase is present in steroidogenic cells of the rat adrenal, ovary, and testis. Proc. Natl. Acad. Sci. U.S.A. 94, 2880-2884
33. Mashek, D. G., Li, L. O., and Coleman, R. A. (2006) Rat long chain acyl-CoA synthetase mRNA, protein, and activity vary in tissue distribution and in response to diet. J. Lipid Res. 47, 2004-2010
34. 2+, substrate and ADP. Biochem. J. 318, 615-621
35. Karara, A., Dishman, E., Falck, J. R., and Capdevila, J. H. (1991) Endogenous epoxyeicosatrienoyl-phospholipids. A novel class of cellular glycerolipids containing epoxidized arachidonate moieties. J. Biol. Chem. 266, 7561-7569
36. Weintraub, N. L., Fang, X., Kaduce, T. L., VanRollins, M., Chatterjee, P., and Spector, A. A. (1997) Potentiation of endothelium-dependent relaxation by epoxyeicosatrienoic acids. Circ. Res. 81, 258-267
37. Gross, G. J., Gauthier, K. M., Moore, J., Falck, J. R., Hammock, B. D., Campbell, W. B., and Nithipatikom, K. (2008) Effects of the selective EET antagonist, 14,15-EEZE, on cardioprotection produced by exogenous or endogenous EETs in the canine heart. Am. J. Physiol. Heart Circ. Physiol. 294, H2838-H2844
38. Brash, A. R. (2001) Arachidonic acid as a bioactive molecule. J. Clin. Invest. 107, 1339-1345
39. Antinozzi, P. A., Segall, L., Prentki, M., McGarry, J. D., and Newgard, C. B. (1998) 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
40. Roduit, R., Nolan, C., Alarcon, C., Moore, P., Barbeau, A., Delghingaro-Augusto, V., Przybykowski, E., Morin, J., Massé, F., Massie, B., Ruderman, N., Rhodes, C., Poitout, V., and Prentki, M. (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
41. Carroll, M. A., Balazy, M., Margiotta, P., Falck, J. R., and McGiff, J. C. (1993) Renal vasodilator activity of 5,6-epoxyeicosatrienoic acid depends upon conversion by cyclooxygenase and release of prostaglandins. J. Biol. Chem. 268, 12260-12266
42. Johnson, D. G., Fujimoto, W. Y., and Williams, R. H. (1973) Enhanced release of insulin by prostaglandins in isolated pancreatic islets. Diabetes 22, 658-663
43. Pek, S., Tai, T. Y., Elster, A., and Fajans. (1975) Stimulation by prostaglandin E2 of glucagon and insulin release from isolated rat pancreas. Prostaglandins 10, 493-502
44. Pek, S., Tai, T. Y., and Elster, A. (1978) Stimulatory effects of prostaglandins E-1, E-2, and F-2-alpha on glucagon and insulin release in vitro. Diabetes 27, 801-809
45. Luo, P., Chang, H. H., Zhou, Y., Zhang, S., Hwang, S. H., Morisseau, C., Wang, C. Y., Inscho, E. W., Hammock, B. D., and Wang, M. H. (2010) Inhibition or deletion of soluble epoxide hydrolase prevents hyperglycemia, promotes insulin secretion, and reduces islet apoptosis. J. Pharmacol. Exp. Ther. 334, 430-438
46. Borradaile, N. M., Han, X., Harp, J. D., Gale, S. E., Ory, D. S., and Schaffer, J. E. (2006) Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J. Lipid Res. 47, 2726-2737
47. Watt, M. J., Hoy, A. J., Muoio, D. M., and Coleman, R. A. (2012) Distinct roles of specific fatty acids in cellular processes. Implications for interpreting and reporting experiments. Am. J. Physiol. Endocrinol. Metab. 302, E1-E3