312
Views
2
CrossRef citations to date
0
Altmetric
Reviews

Lipid-Induced β-cell Dysfunction And Oxidative Stress

&
Pages 455-463 | Published online: 18 Jan 2017

Bibliography

  • Paolisso G, Gambardella A, Amato L et al.: Opposite effects of short- and long-term fatty acid infusion on insulin secretion in healthy subjects. Diabetologia 38(11), 1295–1299 (1995).
  • We consider this paper of particular interest as it is the first demonstration of an impairing effect of prolonged free fatty acid elevation in humans.
  • Warnotte C, Gilon P, Nenquin M, Henquin JC: Mechanisms of the stimulation of insulin release by saturated fatty acids. A study of palmitate effects in mouse β-cells. Diabetes 43(5), 703–711 (1994).
  • Crespin SR, Greenough WB, III, Steinberg D: Stimulation of insulin secretion by long-chain free fatty acids. A direct pancreatic effect. J. Clin. Invest. 52(8), 1979–1984 (1973).
  • Hennes MM, Dua A, Kissebah AH: Effects of free fatty acids and glucose on splanchnic insulin dynamics. Diabetes 46(1), 57–62 (1997).
  • 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. 97(12), 2728–2735 (1996).
  • 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(7), 878–883 (1994).
  • Unger RH, Zhou YT: Lipotoxicity of β-cells in obesity and in other causes of fatty acid spillover. Diabetes 50(Suppl. 1), S118–S121 (2001).
  • We consider this paper important as it summarizes the effects of lipotoxicity.
  • Lenzen S, Drinkgern J, Tiedge M: Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic. Biol. Med. 20(3), 463–466 (1996).
  • Maechler P, Jornot L, Wollheim CB: Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic cells. J. Biol. Chem. 274(39), 27905–27913 (1999).
  • Moriscot C, Richard MJ, Favrot MC, Benhamou PY: Protection of insulinsecreting INS-1 cells against oxidative stress through adenoviral-mediated glutathione peroxidase overexpression. Diabetes Metab. 29(2 Pt 1), 145–151 (2003).
  • Kaneto H, Kajimoto Y, Miyagawa J et al.: Beneficial effects of antioxidants in diabetes: possible protection of pancreatic β-cells against glucose toxicity. Diabetes 48(12), 2398–2406 (1999).
  • Tanaka Y, Gleason CE, Tran PO, Harmon JS, Robertson RP: Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. Proc. Natl Acad. Sci. USA 96(19), 10857–10862 (1999).
  • Poitout V, Robertson RP. Minireview: Secondary β-cell failure in Type 2 diabetes--a convergence of glucotoxicity and lipotoxicity. Endocrinology 143(2), 339–342 (2002).
  • 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).
  • Boden G, Chen X, Iqbal N: Acute lowering of plasma fatty acids lowers basal insulin secretion in diabetic and nondiabetic subjects. Diabetes 47(10), 1609–1612 (1998).
  • 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-glucosestimulated insulin secretion. J. Clin. Invest. 101(11), 2370–2376 (1998).
  • Bergman RN, Ader M: Free fatty acids and pathogenesis of Type 2 diabetes mellitus. Trends Endocrinol. Metab. 11(9), 351–356 (2000).
  • McGarry JD, Dobbins RL: Fatty acids, lipotoxicity and insulin secretion. Diabetologia 42(2), 128–138 (1999).
  • Itoh Y, Hinuma S. GPR40, a free fatty acid receptor on pancreatic cells, regulates insulin secretion. Hepatol. Res. 33(2), 171–173 (2005).
  • Elks ML: Chronic perifusion of rat islets with palmitate suppresses glucosestimulated insulin release. Endocrinology 133(1), 208–214 (1993).
  • Moore PC, Ugas MA, Hagman DK, Parazzoli SD, Poitout V: Evidence against the involvement of oxidative stress in fatty acid inhibition of insulin secretion. Diabetes 53(10), 2610–2616 (2004).
  • Patane G, Piro S, Rabuazzo AM, Anello M, Vigneri R, Purrello F: Metformin restores insulin secretion altered by chronic exposure to free fatty acids or high glucose: a direct metformin effect on pancreatic β-cells. Diabetes 49(5), 735–740 (2000).
  • Patane G, Anello M, Piro S, Vigneri R, Purrello F, Rabuazzo AM: Role of ATP production and uncoupling protein-2 in the insulin secretory defect induced by chronic exposure to high glucose or free fatty acids and effects of peroxisome proliferatoractivated receptor- inhibition. Diabetes 51(9), 2749–2756 (2002).
  • Zhou YP, Grill VE: Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J. Clin. Invest. 93(2), 870–876 (1994).
  • Zhou YP, Grill V: Long term exposure to fatty acids and ketones inhibits B-cell functions in human pancreatic islets of Langerhans. J. Clin. Endocrinol. Metab. 80(5), 1584–1590 (1995).
  • Zhou YP, Berggren PO, Grill V: A fatty acid-induced decrease in pyruvate dehydrogenase activity is an important determinant of β-cell dysfunction in the obese diabetic db/db mouse. Diabetes 45(5), 580–586 (1996).
  • Assimacopoulos-Jeannet F, Thumelin S, Roche E, Esser V, McGarry JD, Prentki M: Fatty acids rapidly induce the carnitine palmitoyltransferase I gene in the pancreatic β-cell line INS-1. J. Biol. Chem. 272(3), 1659–1664 (1997).
  • Brun T, Assimacopoulos-Jeannet F, Corkey BE, Prentki M: Long-chain fatty acids inhibit acetyl-CoA carboxylase gene expression in the pancreatic β-cell line INS-1. Diabetes 46(3), 393–400 (1997).
  • Liang Y, Buettger C, Berner DK, Matschinsky FM: Chronic effect of fatty acids on insulin release is not through the alteration of glucose metabolism in a pancreatic -cell line ( HC9). Diabetologia 40(9), 1018–1027 (1997).
  • Wang X, Li H, De Leo D et al.: Gene and protein kinase expression profiling of reactive oxygen species-associated lipotoxicity in the pancreatic β-cell line MIN6. Diabetes 53(1), 129–140 (2004).
  • Sako Y, Grill VE: A 48-hour lipid infusion in the rat time-dependently inhibits glucoseinduced insulin secretion and B cell oxidation through a process likely coupled to fatty acid oxidation. Endocrinology 127(4), 1580–1589 (1990).
  • Of particular interest as it is the first study describing an impairment in β-cell function induced by prolonged exposure to free fatty acid (FFA).
  • Boden G, Chen X, Rosner J, Barton M: Effects of a 48-h fat infusion on insulin secretion and glucose utilization. Diabetes 44(10), 1239–1242 (1995).
  • Most quoted paper describing the effects of prolonged fat infusion in humans.
  • Magnan C, Collins S, Berthault MF et al.: Lipid infusion lowers sympathetic nervous activity and leads to increased β-cell responsiveness to glucose. J. Clin. Invest. 103(3), 413–419 (1999).
  • Stefan N, Wahl HG, Fritsche A, Haring H, Stumvoll M: Effect of the pattern of elevated free fatty acids on insulin sensitivity and insulin secretion in healthy humans. Horm. Metab. Res. 33(7), 432–438 (2001).
  • Mason TM, Goh T, Tchipashvili V et al.: Prolonged elevation of plasma free fatty acids desensitizes the insulin secretory response to glucose in vivo in rats. Diabetes 48(3), 524–530 (1999).
  • Kashyap S, Belfort R, Gastaldelli A et al.: A sustained increase in plasma free fatty acids impairs insulin secretion in nondiabetic subjects genetically predisposed to develop Type 2 diabetes. Diabetes 52(10), 2461–2474 (2003).
  • Cusi K, Kashyap S, Gastaldelli A, Bajaj M, Cersosimo E: Effects on Insulin Secretion and Action of a 48-Hour Reduction of Plasma FFA with Acipimox in Non-Diabetic Subjects Genetically Predisposed to Type 2 Diabetes. Am. J. Physiol Endocrinol. Metab. doi: 10.1152/ajpendo.00624.2006 (2007) (Epub ahead pf print).
  • Robertson RP: Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet cells in diabetes. J. Biol. Chem. 279(41), 42351–42354 (2004).
  • We consider this review important as it summarizes the effects of oxidative stress on glucotoxicity in islets.
  • Tanaka Y, Tran PO, Harmon J, Robertson RP: A role for glutathione peroxidase in protecting pancreatic cells against oxidative stress in a model of glucose toxicity. Proc. Natl Acad. Sci. USA 99(19), 12363–12368 (2002).
  • Carlsson C, Borg LA, Welsh N: Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 140(8), 3422–3428 (1999).
  • Important as it provides evidence for reactive oxygen species (ROS) generation in islets exposed to fat.
  • Kaneto H, Xu G, Fujii N, Kim S, Bonner-Weir S, Weir GC: Involvement of c-Jun N-terminal kinase in oxidative stressmediated suppression of insulin gene expression. J. Biol. Chem. 277(33), 30010–30018 (2002).
  • Garcia-Ruiz C, Colell A, Mari M, Morales A, Fernandez-Checa JC: Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J. Biol. Chem. 272(17), 11369–11377 (1997).
  • Inoguchi T, Li P, Umeda F et al.: High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 49(11), 1939–1945 (2000).
  • Kaneto H, Xu G, Song KH et al.: Activation of the hexosamine pathway leads to deterioration of pancreatic β-cell function through the induction of oxidative stress. J. Biol. Chem. 276(33), 31099–31104 (2001).
  • Du XL, Edelstein D, Rossetti L et al.: Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc. Natl Acad. Sci. USA 97(22), 12222–12226 (2000).
  • Kunisaki M, Bursell SE, Umeda F, Nawata H, King GL: Normalization of diacylglycerol-protein kinase C activation by vitamin E in aorta of diabetic rats and cultured rat smooth muscle cells exposed to elevated glucose levels. Diabetes 43(11), 1372–1377 (1994).
  • Liu B, Hannun YA: Inhibition of the neutral magnesium-dependent sphingomyelinase by glutathione. J. Biol. Chem. 272(26), 16281–16287 (1997).
  • Azevedo-Martins AK, Lortz S, Lenzen S, Curi R, Eizirik DL, Tiedge M: Improvement of the mitochondrial antioxidant defense status prevents cytokineinduced nuclear factor- B activation in insulin-producing cells. Diabetes 52(1), 93–101 (2003).
  • Evans JL, Goldfine ID, Maddux BA, Grodsky GM: Oxidative stress and stressactivated signaling pathways: a unifying hypothesis of Type 2 diabetes. Endocr. Rev. 23(5), 599–622 (2002).
  • Very comprehensive review which summarizes the effects of oxidative stress in Type 2 diabetes.
  • Cooksey RC, Jouihan HA, Ajioka RS et al.: Oxidative stress, β-cell apoptosis, and decreased insulin secretory capacity in mouse models of hemochromatosis. Endocrinology 145(11), 5305–5312 (2004).
  • Paolisso G, Gambardella A, Tagliamonte MR et al.: Does free fatty acid infusion impair insulin action also through an increase in oxidative stress? J. Clin. Endocrinol. Metab. 81(12), 4244–4248 (1996).
  • Robertson RP, Harmon J, Tran PO, Poitout V: β-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in Type 2 diabetes. Diabetes 53(Suppl. 1), S119-S124 (2004).
  • Gopaul NK, Anggard EE, Mallet AI, Betteridge DJ, Wolff SP, Nourooz-Zadeh J: Plasma 8-epi-PGF2 levels are elevated in individuals with non-insulin dependent diabetes mellitus. FEBS Lett. 368(2), 225–229 (1995).
  • Nourooz-Zadeh J, Tajaddini-Sarmadi J, McCarthy S, Betteridge DJ, Wolff SP: Elevated levels of authentic plasma hydroperoxides in NIDDM. Diabetes 44(9), 1054–1058 (1995).
  • Shin CS, Moon BS, Park KS et al: Serum 8- hydroxy-guanine levels are increased in diabetic patients. Diabetes Care 24(4), 733–737 (2001).
  • Murakami K, Kondo T, Ohtsuka Y, Fujiwara Y, Shimada M, Kawakami Y: Impairment of glutathione metabolism in erythrocytes from patients with diabetes mellitus. Metabolism 38(8), 753–758 (1989).
  • Grinberg L, Fibach E, Amer J, Atlas D: N-acetylcysteine amide, a novel cellpermeating thiol, restores cellular glutathione and protects human red blood cells from oxidative stress. Free Radic. Biol. Med. 38(1), 136–145 (2005).
  • Ihara Y, Yamada Y, Toyokuni S et al.: Antioxidant -tocopherol ameliorates glycemic control of GK rats, a model of Type 2 diabetes. FEBS Lett. 473(1), 24–26 (2000).
  • Brons C, Spohr C, Storgaard H, Dyerberg J, Vaag A: Effect of taurine treatment on insulin secretion and action, and on serum lipid levels in overweight men with a genetic predisposition for Type II diabetes mellitus. Eur. J. Clin. Nutr. 58(9), 1239–1247 (2004).
  • De Mattia G, Bravi MC, Laurenti O et al.: Influence of reduced glutathione infusion on glucose metabolism in patients with noninsulin- dependent diabetes mellitus. Metabolism 47(8), 993–997 (1998).
  • Grill V, Qvigstad E. Fatty acids and insulin secretion. Br. J. Nutr. 83(Suppl. 1), S79–S84 (2000).
  • Miwa I, Ichimura N, Sugiura M, Hamada Y, Taniguchi S: Inhibition of glucose-induced insulin secretion by 4-hydroxy-2-nonenal and other lipid peroxidation products. Endocrinology 141(8), 2767–2772 (2000).
  • Sakai K, Matsumoto K, Nishikawa T et al.: Mitochondrial reactive oxygen species reduce insulin secretion by pancreatic β- cells. Biochem. Biophys. Res. Commun. 300(1), 216–222 (2003).
  • Pecqueur C, Alves-Guerra MC, Gelly C et al.: Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J. Biol. Chem. 276(12), 8705–8712 (2001).
  • Chan CB, De Leo D, Joseph JW et al.: Increased uncoupling protein-2 levels in β- cells are associated with impaired glucosestimulated insulin secretion: mechanism of action. Diabetes 50(6), 1302–1310 (2001).
  • Koshkin V, Wang X, Scherer PE, Chan CB, Wheeler MB: Mitochondrial functional state in clonal pancreatic β-cells exposed to free fatty acids. J. Biol. Chem. 278(22), 19709–19715 (2003).
  • Lameloise N, Muzzin P, Prentki M, Assimacopoulos-Jeannet F: Uncoupling protein 2: a possible link between fatty acid excess and impaired glucose-induced insulin secretion? Diabetes 50(4), 803–809 (2001).
  • Li LX, Skorpen F, Egeberg K, Jorgensen IH, Grill V: Induction of uncoupling protein 2 mRNA in β-cells is stimulated by oxidation of fatty acids but not by nutrient oversupply. Endocrinology 143(4), 1371–1377 (2002).
  • 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(2), 315–321 (2001).
  • Jacqueminet S, Briaud I, Rouault C, Reach G, Poitout V: Inhibition of insulin gene expression by long-term exposure of pancreatic cells to palmitate is dependent on the presence of a stimulatory glucose concentration. Metabolism 49(4), 532–536 (2000).
  • Ruderman NB, Saha AK, Vavvas D, Witters LA: Malonyl-CoA, fuel sensing, and insulin resistance. Am. J. Physiol. 276(1 Pt 1), E1- E18 (1999).
  • 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. 278(32), 30015–30021 (2003).
  • Leibiger B, Leibiger IB, Moede T et al.: Selective insulin signaling through A and B insulin receptors regulates transcription of insulin and glucokinase genes in pancreatic cells. Mol. Cell 7(3), 559–570 (2001).
  • Xu GG, Rothenberg PL: Insulin receptor signaling in the β-cell influences insulin gene expression and insulin content: evidence for autocrine β-cell regulation. Diabetes 47(8), 1243–1252 (1998).
  • Rhodes CJ, White MF. Molecular insights into insulin action and secretion. Eur. J. Clin. Invest. 32(Suppl. 3), 3–13 (2002).
  • Hribal ML, Perego L, Lovari S et al.: Chronic hyperglycemia impairs insulin secretion by affecting insulin receptor expression, splicing, and signaling in RIN cell line and human islets of Langerhans. FASEB J. 17(10), 1340–1342 (2003).
  • Wrede CE, Dickson LM, Lingohr MK, Briaud I, Rhodes CJ: Fatty acid and phorbol ester-mediated interference of mitogenic signaling via novel protein kinase C isoforms in pancreatic β-cells (INS-1). J. Mol. Endocrinol. 30(3), 271–286 (2003).
  • Kawamori D, Kaneto H, Nakatani Y et al.: The forkhead transcription factor Foxo1 bridges the JNK pathway and the transcription factor PDX-1 through its intracellular translocation. J. Biol. Chem. 281(2), 1091–1098 (2006).
  • Solinas G, Naugler W, Galimi F, Lee MS, Karin M: Saturated fatty acids inhibit induction of insulin gene transcription by JNK-mediated phosphorylation of insulinreceptor substrates. Proc. Natl Acad. Sci. USA 103(44), 16454–16459 (2006).
  • Rakatzi I, Mueller H, Ritzeler O, Tennagels N, Eckel J: Adiponectin counteracts cytokine- and fatty acid-induced apoptosis in the pancreatic β-cell line INS-1. Diabetologia 47(2), 249–258 (2004).
  • Kharroubi I, Ladriere L, Cardozo AK, Dogusan Z, Cnop M, Eizirik DL: Free fatty acids and cytokines induce pancreatic β-cell apoptosis by different mechanisms: role of nuclear factor- B and endoplasmic reticulum stress. Endocrinology 145(11), 5087–5096 (2004).
  • Shimabukuro M, Ohneda M, Lee Y, Unger RH: Role of nitric oxide in obesityinduced cell disease. J. Clin. Invest. 100(2), 290–295 (1997).
  • Shimabukuro M, Higa M, Zhou YT, Wang MY, Newgard CB, Unger RH: Lipoapoptosis in β-cells of obese prediabetic fa/fa rats. Role of serine palmitoyltransferase overexpression. J. Biol. Chem. 273(49), 32487–32490 (1998).
  • Chen M, Robertson RP. Restoration of the acute insulin response by sodium salicylate. A glucose dose-related phenomenon. Diabetes 27(7), 750–756 (1978).
  • Metz S, Fujimoto W, Robertson RP: Modulation of insulin secretion by cyclic AMP and prostaglandin E: the effects of theophylline, sodium salicylate and tolbutamide. Metabolism 31(10), 1014–1022 (1982).
  • Tran PO, Gleason CE, Robertson RP: Inhibition of interleukin-1 -induced COX- 2 and EP3 gene expression by sodium salicylate enhances pancreatic islet β-cell function. Diabetes 51(6), 1772–1778 (2002).
  • Harding HP, Zeng H, Zhang Y et al.: Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 7(6), 1153–1163 (2001).
  • Kaneto H, Matsuoka TA, Nakatani Y et al.: Oxidative stress, ER stress, and the JNK pathway in Type 2 diabetes. J. Mol. Med. 83(6), 429–439 (2005).
  • Karaskov E, Scott C, Zhang L, Teodoro T, Ravazzola M, Volchuk A: Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic β-cell apoptosis. Endocrinology 147(7), 3398–3407 (2006).
  • Hawkins M, Barzilai N, Liu R, Hu M, ChenW, Rossetti L. Role of the glucosamine pathway in fat-induced insulin resistance. J. Clin. Invest. 99(9), 2173–2182 (1997).
  • Lewis GF, Carpentier A, Adeli K, Giacca A: Disordered fat storage and mobilization in the pathogenesis of insulin resistance and Type 2 diabetes. Endocr. Rev. 23(2), 201–229 (2002).
  • Maestre I, Jordan J, Calvo S et al.: Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the β-cell line INS-1. Endocrinology 144(1), 335–345 (2003).
  • Eizirik DL, Korbutt GS, Hellerstrom C. Prolonged exposure of human pancreatic islets to high glucose concentrations in vitro impairs the β-cell function. J. Clin. Invest. 90(4), 1263–1268 (1992).
  • El Assaad W, Buteau J, Peyot ML et al.: Saturated fatty acids synergize with elevated glucose to cause pancreatic β-cell death. Endocrinology 144(9), 4154–4163 (2003).
  • Mayer-Davis EJ, Costacou T, King I, Zaccaro DJ, Bell RA.: Plasma and dietary vitamin E in relation to incidence of Type 2 diabetes: The Insulin Resistance and Atherosclerosis Study (IRAS). Diabetes Care 25(12), 2172–2177 (2002).
  • Lonn E, Yusuf S, Hoogwerf B et al.: Effects of vitamin E on cardiovascular and microvascular outcomes in high-risk patients with diabetes: results of the HOPE study and MICRO-HOPE substudy. Diabetes Care 25(11), 1919–1927 (2002).
  • Mann JF, Lonn EM, Yi Q et al.: Effects of vitamin E on cardiovascular outcomes in people with mild-to-moderate renal insufficiency: results of the HOPE study. Kidney Int. 65(4), 1375–1380 (2004).
  • Baynes JW, Thorpe SR: Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48(1), 1–9 (1999).
  • Habeck M: Catalytic antioxidants prevent Type 1 diabetes. Drug Discov. Today 7(18), 933–934 (2002).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.