Novel insights into pancreatic β-cell glucolipotoxicity from real-time functional analysis of mitochondrial energy metabolism in INS-1E insulinoma cells

Biochemical Journal

Volumn 456, Issue 3, 2013, Pages 417-426

  Barlow, Jonathan ^a   Affourtit, Charles ^a  

^a UNIVERSITY OF PLYMOUTH   (United Kingdom)

Author keywords

Glucose stimulated insulin secretion; Mitochondrial dysfunction; Oxidative phosphorylation; Pancreatic cell glucolipotoxicity; Reactive oxygen species; Type 2 diabetes

Indexed keywords

ADENOSINE TRIPHOSPHATE; FATTY ACID; GLUCOSE; INSULIN; PALMITIC ACID; PALMITOLEIC ACID; PROTON; REACTIVE OXYGEN METABOLITE; ENZYME INHIBITOR;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; GLUCOLIPOTOXICITY; INSULIN RELEASE; INSULINOMA; MITOCHONDRIAL RESPIRATION; OXIDATIVE PHOSPHORYLATION; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; TUMOR CELL; ANIMAL; DRUG EFFECTS; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; PATHOLOGY; PROTON MOTIVE FORCE; RAT; SECRETION (PROCESS); TOXICITY; TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE, TUMOR; ENZYME INHIBITORS; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; INSULINOMA; MITOCHONDRIA; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PALMITIC ACID; PROTON-MOTIVE FORCE; RATS;

EID: 84888411572     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131002     Document Type: Article

References (50)

1. Garber, A. J. (2012) Obesity and type 2 diabetes: which patients are at risk? Diabetes, Obes. Metab. 14, 399-408
2. Muoio, D. M. and Newgard, C. B. (2008) Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and β-cell failure in type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9, 193-205
3. Unger, R. H. (1995) Lipotoxicity in the pathogenesis of obesity-dependent NIDDM. Genetic and clinical implications. Diabetes 44, 863-870
4. Prentki, M. and Nolan, C. J. (2006) Islet β-cell failure in type 2 diabetes. J. Clin. Invest. 116, 1802-1812
5. Poitout, V., Amyot, J., Semache, M., Zarrouki, B., Hagman, D. and Font́es, G. (2010) Glucolipotoxicity of the pancreatic β-cell. Biochim. Biophys. Acta 1801, 289-298
6. Newsholme, P., Keane, D., Welters, H. J. and Morgan, N. G. (2007) Life and death decisions of the pancreatic β-cell: the role of fatty acids. Clin. Sci. 112, 27-42
7. Morgan, N. G. and Dhayal, S. (2010) Unsaturated fatty acids as cytoprotective agents in the pancreatic β-cell. Prostaglandins, Leukotrienes Essent. Fatty Acids 82, 231-236
8. Prentki, M., Joly, E., El-Assaad, W. and Roduit, R. (2002) Malonyl-CoA signaling, lipid partitioning, and glucolipotoxicity: role in β-cell adaptation and failure in the etiology of diabetes. Diabetes 51, S405-S413
9. Lee, M.-S., Kim, K.-A. and Kim, H. S. (2012) Role of pancreatic β-cell death and cell death-associated inflammation in diabetes. Curr. Mol. Med. 12, 1297-1310
10. Elks, M. L. (1993) Chronic perifusion of rat islets with palmitate suppresses glucose-stimulated insulin release. Endocrinology 133, 208-214
11. Lovis, P., Roggli, E., Laybutt, D. R., Gattesco, S., Yang, J.-Y., Widmann, C., Abderrahmani, A. and Regazzi, R. (2008) Alterations in microRNA expression contribute to fatty acid-induced pancreatic β-cell dysfunction. Diabetes 57, 2728-2736
12. Malmgren, S., Spegel, P., Danielsson, A. P., Nagorny, C. L., Andersson, L. E., Nitert, M. D., Ridderstråle, M., Mulder, H. and Ling, C. (2013) Coordinate changes in histone modifications, mRNA levels and metabolite profiles in clonal INS-1 832/13 β-cells accompany functional adaptations to lipotoxicity. J. Biol. Chem. 288, 11973-11987
13. Akash, M. S. H., Rehman, K. and Chen, S. (2013) Role of inflammatory mechanisms in pathogenesis of type 2 diabetes mellitus. J. Cell. Biochem. 114, 525-531
14. Haber, E. P., Hirabara, S. M., Gomes, A. D., Curi, R., Carpinelli, A. R. and Carvalho, C. R. O. (2003) Palmitate modulates the early steps of insulin signalling pathway in pancreatic islets. FEBS Lett. 544, 185-188
15. Pi, J. and Collins, S. (2010) Reactive oxygen species and uncoupling protein 2 in pancreatic β-cell function. Diabetes, Obes. Metab. 12, 141-148
16. Cnop, M., Foufelle, F. and Velloso, L. A. (2012) Endoplasmic reticulum stress, obesity and diabetes. Trends Mol. Med. 18, 59-68
17. Lowell, B. B. and Shulman, G. I. (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307, 384-387
18. Prentki, M. and Madiraju, S. R. M. (2012) Glycerolipid/free fatty acid cycle and islet β-cell function in health, obesity and diabetes. Mol. Cell. Endocrinol. 353, 88-100
19. Nolan, C. J. and Larter, C. Z. (2009) Lipotoxicity: why do saturated fatty acids cause and monounsaturates protect against it? J. Gastroenterol. Hepatol. 24, 703-706
20. Zhang, C.-Y., Baffy, G., Perret, P., Krauss, S., Peroni, O., Grujic, D., Hagen, T., Vidal-Puig, A. J., Boss, O., Kim, Y-B. et al. (2001) Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, β-cell dysfunction, and type 2 diabetes. Cell 105, 745-755
21. Pi, J., Bai, Y., Daniel, K. W., Liu, D., Lyght, O., Edelstein, D., Brownlee, M., Corkey, B. E. and Collins, S. (2009) Persistent oxidative stress due to absence of uncoupling protein 2 associated with impaired pancreatic β-cell function. Endocrinology 150, 3040-3048
22. Affourtit, C. and Brand, M. D. (2008) Uncoupling protein-2 contributes significantly to high mitochondrial proton leak in INS-1E insulinoma cells and attenuates glucose-stimulated insulin secretion. Biochem. J. 409, 199-204
23. Affourtit, C., Jastroch, M. and Brand, M. D. (2011) Uncoupling protein-2 attenuates glucose-stimulated insulin secretion in INS-1E insulinoma cells by lowering mitochondrial reactive oxygen species. Free Radical Biol. Med. 50, 609-616
24. Robson-Doucette, C. A., Sultan, S., Allister, E. M., Wikstr?om, J. D., Koshkin, V., Bhatacharjee, A., Prentice, K. J., Sereda, S. B., Shirihai, O. S. and Wheeler, M. B. (2011) β-Cell uncoupling protein 2 regulates reactive oxygen species production, which influences both insulin and glucagon secretion. Diabetes 60, 2710-2719
25. Mulder, H. and Ling, C. (2009) Mitochondrial dysfunction in pancreatic β-cells in Type 2 diabetes. Mol. Cell. Endocrinol. 297, 34-40
26. Brand, M. D. and Nicholls, D. G. (2011) Assessing mitochondrial dysfunction in cells. Biochem. J. 435, 297-312
27. Malmgren, S., Nicholls, D. G., Taneera, J., Bacos, K., Koeck, T., Tamaddo, A., Wibom, R., Groop, L., Ling, C., Mulder, H. and Sharoyko, V. V. (2009) Tight coupling between glucose and mitochondrial metabolism in clonal β-cells is required for robust insulin secretion. J. Biol. Chem. 284, 32395-32404
28. Pi, J., Bai, Y., Zhang, Q., Wong, V., Floering, L. M., Daniel, K., Reece, J. M., Deeney, J. T., Andersen, M. E., Corkey, B. E. and Collins, S. (2007) Reactive oxygen species as a signal in glucose-stimulated insulin secretion. Diabetes 56, 1783-1791
29. Affourtit, C. and Brand, M. D. (2009) Measuring mitochondrial bioenergetics in INS-1E insulinoma cells. Methods Enzymol. 457, 405-424
30. Merglen, A., Theander, S., Rubi, B., Chaffard, G., Wollheim, C. B. and Maechler, P. (2004) Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology 145, 667-678
31. Huber, A. H., Kampf, J. P., Kwan, T., Zhu, B. and Kleinfeld, A. M. (2006) Fatty acid-specific fluorescent probes and their use in resolving mixtures of unbound free fatty acids in equilibrium with albumin. Biochemistry 45, 14263-14274
32. Barlow, J., Hirschberg, V., Brand, M. D. and Affourtit, C. (2013) Measuring mitochondrial uncoupling protein-2 level and activity in insulinoma cells. Methods Enzymol. 528, 257-267
33. Rutter, G. A. (2001) Nutrient-secretion coupling in the pancreatic islet β-cell: recent advances. Mol. Aspects Med. 22, 247-284
34. Affourtit, C. and Brand, M. D. (2006) Stronger control of ATP/ADP by proton leak in pancreatic β-cells than skeletal muscle mitochondria. Biochem. J. 393, 151-159
35. Barlow, J., Hirschberg, V. and Affourtit, C. (2013) On the role of mitochondria in pancreatic β-cells. In Research on Diabetes, iConcept Press
36. Robinson, K. M., Janes, M. S., Pehar, M., Monette, J. S., Ross, M. F., Hagen, T. M., Murphy, M. P. and Beckman, J. S. (2006) Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U.S.A. 103, 15038-15043
37. Newsholme, P., Morgan, D., Rebelato, E., Oliveira-Emilio, H. C., Procopio, J., Curi, R. and Carpinelli, A. (2009) Insights into the critical role of NADPH oxidase(s) in the normal and dysregulated pancreatic β-cell. Diabetologia 52, 2489-2498
38. Morgan, D., Oliveira-Emilio, H. R., Keane, D., Hirata, A. E., Santos da Rocha, M., Bordin, S., Curi, R., Newsholme, P. and Carpinelli, A. R. (2006) Glucose, palmitate and pro-inflammatory cytokines modulate production and activity of a phagocyte-like NADPH oxidase in rat pancreatic islets and a clonal β-cell line. Diabetologia 50, 359-369
39. Hue, L. and Taegtmeyer, H. (2009) The Randle cycle revisited: a new head for an old hat. Am. J. Physiol. Endocrinol. Metab. 297, E578-E591
40. Luiken, J. J., Niessen, H. E., Coort, S. L., Hoebers, N., Coumans, W. A., Schwenk, R. W., Bonen, A. and Glatz, J. F. (2009) Etomoxir-induced partial carnitine palmitoyltransferase-I (CPT-I) inhibition in vivo does not alter cardiac long-chain fatty acid uptake and oxidation rates. Biochem. J. 419, 447-455
41. Larsson, O., Deeney, J. T., Br?anstr?om, R., Berggren, P. O. and Corkey, B. E. (1996) Activation of the ATP-sensitive K+ channel by long chain acyl-CoA. A role in modulation of pancreatic β-cell glucose sensitivity. J. Biol. Chem. 271, 10623-10626
42. Zhao, Y., Sharp, G. W. G. and Straub, S. G. (2007) The inhibitors of protein acylation, cerulenin and tunicamycin, increase voltage-dependent Ca2+ currents in the insulin-secreting INS 832/13 cell. Biochem. Pharmacol. 74, 273-280
43. Hoppa, M. B., Collins, S., Ramracheya, R., Hodson, L., Amisten, S., Zhang, Q., Johnson, P., Ashcroft, F. M. and Rorsman, P. (2009) Chronic palmitate exposure inhibits insulin secretion by dissociation of Ca2+ channels from secretory granules. Cell Metab. 10, 455-465
44. Wikström, J. D., Sereda, S. B., Stiles, L., Elorza, A., Allister, E. M., Neilson, A., Ferrick, D. A., Wheeler, M. B. and Shirihai, O. S. (2012) A novel high-throughput assay for islet respiration reveals uncoupling of rodent and human islets. PLoS ONE 7, e33023
45. Diakogiannaki, E., Dhayal, S., Childs, C. E., Calder, P. C., Welters, H. J. and Morgan, N. G. (2007) Mechanisms involved in the cytotoxic and cytoprotective actions of saturated versus monounsaturated long-chain fatty acids in pancreatic β-cells. J. Endocrinol. 194, 283-291
46. Maestre, I., Jord́an, J., Calvo, S., Reig, J. A., Ce?na, V., Soria, B., Prentki, M. and Roche, E. (2003) Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the β-cell line INS-1. Endocrinology 144, 335-345
47. Joseph, J., Chan, C. and Wheeler, M. (2005) UCP2 knockout mouse islets have lower consumption and faster oscillations of β-cell oxygen. Can. J. Diabetes 29, 19-26
48. Hovsepyan, M., Sargsyan, E. and Bergsten, P. (2010) Palmitate-induced changes in protein expression of insulin secreting INS-1E cells. J. Proteomics 73, 1148-1155
49. Listenberger, L. L., Han, X., Lewis, S. E., Cases, S., Farese, R. V., Ory, D. S. and Schaffer, J. E. (2003) Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. U.S.A. 100, 3077-3082
50. Gravena, C., Mathias, P. C. and Ashcroft, S. J. H. (2002) Acute effects of fatty acids on insulin secretion from rat and human islets of Langerhans. J. Endocrinol. 173, 73-80