Fatty Acid-Induced Lipotoxicity in Pancreatic Beta-Cells During Development of Type 2 Diabetes

Yoon Sin Oh1, Gong Deuk Bae2, Dong Jae Baek3, Eun‐Young Park3, Hee‐Sook Jun2,4,5
1Department of Food and Nutrition, Eulji University, Seongnam, South Korea
2Department of Molecular Medicine, Lee Gil Ya Cancer and Diabetes Institute, Gachon University, Incheon, South Korea
3College of Pharmacy and Natural Medicine Research Institute, Mokpo National University, Jeonnam, South Korea
4Gachon Institute of Pharmaceutical Science, College of Pharmacy, Gachon University, Incheon, South Korea
5Gachon University Gil Medical Center, Gachon Medical and Convergence Institute, Incheon, South Korea

Tóm tắt

Từ khóa


Tài liệu tham khảo

Paolisso, 1995, A high concentration of fasting plasma non-esterified fatty acids is a risk factor for the development of NIDDM, Diabetologia, 38, 1213, 10.1007/s001250050414

Charles, 1997, The role of non-esterified fatty acids in the deterioration of glucose tolerance in Caucasian subjects: results of the Paris Prospective Study, Diabetologia, 40, 1101, 10.1007/s001250050793

Sharma, 2014, Lipotoxicity in the pancreatic β cell: not just survival and function, but proliferation as well?, Curr Diab Rep, 14, 492, 10.1007/s11892-014-0492-2

Cnop, 2005, Mechanisms of pancreatic β-cell death in type 1 and type 2 diabetes: many differences, few similarities, Diabetes, 54, S97, 10.2337/diabetes.54.suppl_2.S97

Oh, 2015, Mechanistic insights into pancreatic β-cell mass regulation by glucose and free fatty acids, Anat Cell Biol., 48, 16, 10.5115/acb.2015.48.1.16

Johnston, 2018, Association of NEFA composition with insulin sensitivity and β cell function in the Prospective Metabolism and Islet Cell Evaluation (PROMISE) cohort, Diabetologia, 61, 821, 10.1007/s00125-017-4534-6

Palomer, 2018, Palmitic and oleic acid: the yin and yang of fatty acids in type 2 diabetes mellitus, Trends Endocrinol Metab., 29, 178, 10.1016/j.tem.2017.11.009

Poudyal, 2013, Effects of ALA, EPA and DHA in high-carbohydrate, high-fat diet-induced metabolic syndrome in rats, J Nutr Biochem., 24, 1041, 10.1016/j.jnutbio.2012.07.014

Newsholme, 2007, Life and death decisions of the pancreatic β-cell: the role of fatty acids, Clin Sci., 112, 27, 10.1042/CS20060115

Keane, 2011, Arachidonic acid actions on functional integrity and attenuation of the negative effects of palmitic acid in a clonal pancreatic β-cell line, Clin Sci., 120, 195, 10.1042/CS20100282

Baynes, 2018, The role of polyunsaturated fatty acids (n-3 PUFAs) on the pancreatic β-cells and insulin action, Adipocyte, 14, 1, 10.1080/21623945.2018.1443662

Su, 2007, Angiopoietin-1 production in islets improves islet engraftment and protects islets from cytokine-induced apoptosis, Diabetes, 56, 2274, 10.2337/db07-0371

Wei, 2010, Cellular production of n-3 PUFAs and reduction of n-6-to-n-3 ratios in the pancreatic β-cells and islets enhance insulin secretion and confer protection against cytokine-induced cell death, Diabetes, 59, 471, 10.2337/db09-0284

Acosta-Montano, 2018, Effects of dietary fatty acids in pancreatic β cell metabolism, implications in homeostasis, Nutrients, 10, E393, 10.3390/nu10040393

Hagman, 2005, Palmitate inhibits insulin gene expression by altering PDX-1 nuclear localization and reducing MafA expression in isolated rat islets of Langerhans, J Biol Chem., 280, 32413, 10.1074/jbc.M506000200

Shimabukuro, 1998, Fatty acid-induced β cell apoptosis: a link between obesity and diabetes, Proc Natl Acad Sci U S A., 95, 2498, 10.1073/pnas.95.5.2498

Briaud, 2002, Differential effects of hyperlipidemia on insulin secretion in islets of langerhans from hyperglycemic versus normoglycemic rats, Diabetes, 51, 662, 10.2337/diabetes.51.3.662

Carpentier, 2010, Plasma nonesterified Fatty Acid intolerance and hyperglycemia are associated with intravenous lipid-induced impairment of insulin sensitivity and disposition index, J Clin Endocrinol Metab., 95, 1256, 10.1210/jc.2009-1932

Moulle, 2017, Nutrient regulation of pancreatic β-cell proliferation, Biochimie, 143, 10, 10.1016/j.biochi.2017.09.017

Silverstein, 2010, Mechanisms of cell signaling by the scavenger receptor CD36: implications in atherosclerosis and thrombosis, Trans Am Clin Climatol Assoc., 121, 206

Wallin, 2010, Facilitation of fatty acid uptake by CD36 in insulin-producing cells reduces fatty-acid-induced insulin secretion and glucose regulation of fatty acid oxidation, Biochim Biophys Acta, 1801, 191, 10.1016/j.bbalip.2009.11.002

Hua, 2015, CD36 Mediated fatty acid-induced podocyte apoptosis via oxidative stress, PLoS ONE, 10, e0127507, 10.1371/journal.pone.0127507

Vangaveti, 2010, Free fatty acid receptors: emerging targets for treatment of diabetes and its complications, Ther Adv Endocrinol Metab., 1, 165, 10.1177/2042018810381066

Itoh, 2003, Free fatty acids regulate insulin secretion from pancreatic β cells through GPR40, Nature, 422, 173, 10.1038/nature01478

Miyauchi, 2010, New frontiers in gut nutrient sensor research: free fatty acid sensing in the gastrointestinal tract, J Pharmacol Sci., 112, 19, 10.1254/jphs.09R09FM

Steneberg, 2005, The FFA receptor GPR40 links hyperinsulinemia, hepatic steatosis, and impaired glucose homeostasis in mouse, Cell Metab., 1, 245, 10.1016/j.cmet.2005.03.007

Kristinsson, 2013, FFAR1 is involved in both the acute and chronic effects of palmitate on insulin secretion, Endocrinology, 154, 4078, 10.1210/en.2013-1352

Tuo, 2012, Long-term in vitro treatment of INS-1 rat pancreatic β-cells by unsaturated free fatty acids protects cells against gluco- and lipotoxicities via activation of GPR40 receptors, Clin Exp Pharmacol Physiol., 39, 423, 10.1111/j.1440-1681.2012.05691.x

Nagasumi, 2009, Overexpression of GPR40 in pancreatic β-cells augments glucose-stimulated insulin secretion and improves glucose tolerance in normal and diabetic mice, Diabetes, 58, 1067, 10.2337/db08-1233

Wagner, 2013, Reevaluation of fatty acid receptor 1 as a drug target for the stimulation of insulin secretion in humans, Diabetes, 62, 2106, 10.2337/db12-1249

Liou, 2011, The G-protein-coupled receptor GPR40 directly mediates long-chain fatty acid-induced secretion of cholecystokinin, Gastroenterology, 140, 903, 10.1053/j.gastro.2010.10.012

Li, 2018, Free Fatty Acid Receptor 1 (FFAR1) as an emerging therapeutic target for type 2 diabetes mellitus: recent progress and prevailing challenges, Med Res Rev, 38, 381, 10.1002/med.21441

Leifke, 2012, A multiple-ascending-dose study to evaluate safety, pharmacokinetics, and pharmacodynamics of a novel GPR40 agonist, TAK-875, in subjects with type 2 diabetes, Clin Pharmacol Ther., 92, 29, 10.1038/clpt.2012.43

Li, 2015, Fasiglifam (TAK-875) Inhibits hepatobiliary transporters: a possible factor contributing to Fasiglifam-induced liver injury, Drug Metab Dispos., 43, 1751, 10.1124/dmd.115.064121

Hirasawa, 2005, Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120, Nat Med., 11, 90, 10.1038/nm1168

Katsuma, 2005, Free fatty acids inhibit serum deprivation-induced apoptosis through GPR120 in a murine enteroendocrine cell line STC-1, J Biol Chem., 280, 19507, 10.1074/jbc.M412385200

Ichimura, 2012, Dysfunction of lipid sensor GPR120 leads to obesity in both mouse and human, Nature, 483, 350, 10.1038/nature10798

Tang, 2015, Loss of FFA2 and FFA3 increases insulin secretion and improves glucose tolerance in type 2 diabetes, Nat Med., 21, 173, 10.1038/nm.3779

Tolhurst, 2012, Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2, Diabetes, 61, 364, 10.2337/db11-1019

Chu, 2007, A role for β-cell-expressed G protein-coupled receptor 119 in glycemic control by enhancing glucose-dependent insulin release, Endocrinology, 148, 2601, 10.1210/en.2006-1608

Chu, 2010, N-oleoyldopamine enhances glucose homeostasis through the activation of GPR119, Mol Endocrinol., 24, 161, 10.1210/me.2009-0239

Grygiel-Gorniak, 2014, Peroxisome proliferator-activated receptors and their ligands: nutritional and clinical implications–a review, Nutr J., 13, 17, 10.1186/1475-2891-13-17

Frigerio, 2010, Peroxisome proliferator-activated receptor alpha (PPARalpha) protects against oleate-induced INS-1E β cell dysfunction by preserving carbohydrate metabolism, Diabetologia, 53, 331, 10.1007/s00125-009-1590-6

Popescu, 2010, The nuclear receptor FXR is expressed in pancreatic β-cells and protects human islets from lipotoxicity, FEBS Lett., 584, 2845, 10.1016/j.febslet.2010.04.068

Chavez, 2003, Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes, Arch Biochem Biophys, 419, 101, 10.1016/j.abb.2003.08.020

Summers, 2006, Ceramides in insulin resistance and lipotoxicity, Prog Lipid Res., 45, 42, 10.1016/j.plipres.2005.11.002

Veret, 2011, Ceramide synthase 4 and de novo production of ceramides with specific N-acyl chain lengths are involved in glucolipotoxicity-induced apoptosis of INS-1 β-cells, Biochem J., 438, 177, 10.1042/BJ20101386

Maedler, 2003, Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic β-cell turnover and function, Diabetes, 52, 726, 10.2337/diabetes.52.3.726

Boslem, 2013, Alteration of endoplasmic reticulum lipid rafts contributes to lipotoxicity in pancreatic β-cells, J Biol Chem., 288, 26569, 10.1074/jbc.M113.489310

Lei, 2010, A link between endoplasmic reticulum stress-induced β-cell apoptosis and the group VIA Ca2+-independent phospholipase A2 (iPLA2β), Diabetes Obes Metab., 12, 93, 10.1111/j.1463-1326.2010.01270.x

Garcia-Ruiz, 2002, Trafficking of ganglioside GD3 to mitochondria by tumor necrosis factor-alpha, J Biol Chem., 277, 36443, 10.1074/jbc.M206021200

Chavez, 2003, A role for ceramide, but not diacylglycerol, in the antagonism of insulin signal transduction by saturated fatty acids, J Biol Chem., 278, 10297, 10.1074/jbc.M212307200

Bachmann, 2001, Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans, Diabetes, 50, 2579, 10.2337/diabetes.50.11.2579

Shimabukuro, 1998, Lipoapoptosis in β-cells of obese prediabetic fa/fa rats. Role of serine palmitoyltransferase overexpression, J Biol Chem., 273, 32487, 10.1074/jbc.273.49.32487

Tang, 2017, Neutral ceramidase secreted via exosome protects against palmitate-induced apoptosis in INS-1 cells, Exp Clin Endocrinol Diabetes, 125, 130, 10.1055/s-0042-116314

Ducharme, 2008, Lipid droplets in lipogenesis and lipolysis, Endocrinology, 149, 942, 10.1210/en.2007-1713

Brasaemle, 2007, Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis, J Lipid Res., 48, 2547, 10.1194/jlr.R700014-JLR200

Borg, 2009, Perilipin is present in islets of Langerhans and protects against lipotoxicity when overexpressed in the β -cell line INS-1, Endocrinology, 150, 3049, 10.1210/en.2008-0913

Chen, 2017, PLIN2 is a key regulator of the unfolded protein response and endoplasmic reticulum stress resolution in pancreatic β cells, Sci Rep., 7, 40855, 10.1038/srep40855

Faleck, 2010, Adipose differentiation-related protein regulates lipids and insulin in pancreatic islets, Am J Physiol Endocrinol Metab., 299, E249, 10.1152/ajpendo.00646.2009

Laybutt, 2007, Endoplasmic reticulum stress contributes to β cell apoptosis in type 2 diabetes, Diabetologia, 50, 752, 10.1007/s00125-006-0590-z

Biden, 2014, Lipotoxic endoplasmic reticulum stress, β cell failure, and type 2 diabetes mellitus, Trends Endocrinol Metab., 25, 389, 10.1016/j.tem.2014.02.003

Marchetti, 2007, The endoplasmic reticulum in pancreatic β cells of type 2 diabetes patients, Diabetologia, 50, 2486, 10.1007/s00125-007-0816-8

Choi, 2008, A chemical chaperone 4-PBA ameliorates palmitate-induced inhibition of glucose-stimulated insulin secretion (GSIS), Arch Biochem Biophys., 475, 109, 10.1016/j.abb.2008.04.015

Song, 2008, Chop deletion reduces oxidative stress, improves β cell function, and promotes cell survival in multiple mouse models of diabetes, J Clin Invest., 118, 3378, 10.1172/JCI34587

Allagnat, 2011, Mcl-1 downregulation by pro-inflammatory cytokines and palmitate is an early event contributing to β-cell apoptosis, Cell Death Differ, 18, 328, 10.1038/cdd.2010.105

Salvado, 2015, Targeting endoplasmic reticulum stress in insulin resistance, Trends Endocrinol Metab., 26, 438, 10.1016/j.tem.2015.05.007

Hara, 2014, Calcium efflux from the endoplasmic reticulum leads to β -cell death, Endocrinology, 155, 758, 10.1210/en.2013-1519

Marmugi, 2016, Sorcin Links Pancreatic β -Cell Lipotoxicity to ER Ca2+ Stores, Diabetes, 65, 1009, 10.2337/db15-1334

Santulli, 2015, Calcium release channel RyR2 regulates insulin release and glucose homeostasis, J Clin Invest., 125, 1968, 10.1172/JCI79273

Haynes, 2004, Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death, Mol Cell., 15, 767, 10.1016/j.molcel.2004.08.025

Preston, 2009, Reduced endoplasmic reticulum (ER)-to-Golgi protein trafficking contributes to ER stress in lipotoxic mouse β cells by promoting protein overload, Diabetologia, 52, 2369, 10.1007/s00125-009-1506-5

Cadavez, 2014, Chaperones ameliorate β cell dysfunction associated with human islet amyloid polypeptide overexpression, PLoS ONE, 9, e101797, 10.1371/journal.pone.0101797

Konarkowska, 2006, The aggregation potential of human amylin determines its cytotoxicity towards islet β -cells, FEBS J., 273, 3614, 10.1111/j.1742-4658.2006.05367.x

Meier, 2006, Inhibition of human IAPP fibril formation does not prevent β-cell death: evidence for distinct actions of oligomers and fibrils of human IAPP, Am J Physiol Endocrinol Metab., 291, E1317, 10.1152/ajpendo.00082.2006

Szabadkai, 2008, Mitochondria: the hub of cellular Ca2+ signaling, Physiology, 23, 84, 10.1152/physiol.00046.2007

Deniaud, 2008, Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis, Oncogene, 27, 285, 10.1038/sj.onc.1210638

Ly, 2017, Oxidative stress and calcium dysregulation by palmitate in type 2 diabetes, Exp Mol Med., 49, e291, 10.1038/emm.2016.157

Cunha, 2008, Initiation and execution of lipotoxic ER stress in pancreatic β-cells, J Cell Sci., 121, 2308, 10.1242/jcs.026062

Pfaffenbach, 2010, Linking endoplasmic reticulum stress to cell death in hepatocytes: roles of C/EBP homologous protein and chemical chaperones in palmitate-mediated cell death, Am J Physiol Endocrinol Metab., 298, E1027, 10.1152/ajpendo.00642.2009

Wiederkehr, 2006, Minireview: implication of mitochondria in insulin secretion and action, Endocrinology, 147, 2643, 10.1210/en.2006-0057

Wiederkehr, 2012, Mitochondrial signals drive insulin secretion in the pancreatic β-cell, Mol Cell Endocrinol., 353, 128, 10.1016/j.mce.2011.07.016

Tumova, 2016, Excess of free fatty acids as a cause of metabolic dysfunction in skeletal muscle, Physiol Res., 65, 193, 10.33549/physiolres.932993

Maechler, 1999, Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic β cells, J Biol Chem., 274, 27905, 10.1074/jbc.274.39.27905

Tiedge, 1997, Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells, Diabetes, 46, 1733, 10.2337/diab.46.11.1733

MacDonald, 2013, Identification of ATP synthase as a lipid peroxide protein adduct in pancreatic islets from humans with and without type 2 diabetes mellitus, J Clin Endocrinol Metab., 98, E727, 10.1210/jc.2012-4203

Carlsson, 1999, Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro, Endocrinology, 140, 3422, 10.1210/endo.140.8.6908

Supale, 2012, Mitochondrial dysfunction in pancreatic β cells, Trends Endocrinol Metab, 23, 477, 10.1016/j.tem.2012.06.002

Chan, 1999, Overexpression of uncoupling protein 2 inhibits glucose-stimulated insulin secretion from rat islets, Diabetes, 48, 1482, 10.2337/diabetes.48.7.1482

Poitout, 2010, Glucolipotoxicity of the pancreatic β cell, Biochim Biophys Acta, 1801, 289, 10.1016/j.bbalip.2009.08.006

Joseph, 2004, Free fatty acid-induced β-cell defects are dependent on uncoupling protein 2 expression, J Biol Chem., 279, 51049, 10.1074/jbc.M409189200

Pi, 2009, Persistent oxidative stress due to absence of uncoupling protein 2 associated with impaired pancreatic β-cell function, Endocrinology, 150, 3040, 10.1210/en.2008-1642

Hirschberg Jensen, 2015, Mitochondrial uncoupling protein-2 is not involved in palmitate-induced impairment of glucose-stimulated insulin secretion in INS-1E insulinoma cells and is not needed for the amplification of insulin release, Biochem Biophys Rep., 1, 8, 10.1016/j.bbrep.2015.03.008

Higa, 1999, Troglitazone prevents mitochondrial alterations, β cell destruction, and diabetes in obese prediabetic rats, Proc Natl Acad Sci U S A., 96, 11513, 10.1073/pnas.96.20.11513

Twig, 2008, Fission and selective fusion govern mitochondrial segregation and elimination by autophagy, EMBO J., 27, 433, 10.1038/sj.emboj.7601963

Jung, 2008, Loss of autophagy diminishes pancreatic β cell mass and function with resultant hyperglycemia, Cell Metab., 8, 318, 10.1016/j.cmet.2008.08.013

Bindokas, 2003, Visualizing superoxide production in normal and diabetic rat islets of Langerhans, J Biol Chem., 278, 9796, 10.1074/jbc.M206913200

Anello, 2005, Functional and morphological alterations of mitochondria in pancreatic β cells from type 2 diabetic patients, Diabetologia, 48, 282, 10.1007/s00125-004-1627-9

Molina, 2009, Mitochondrial networking protects β -cells from nutrient-induced apoptosis, Diabetes, 58, 2303, 10.2337/db07-1781

Wiederkehr, 2009, Linking fatty acid stress to β -cell mitochondrial dynamics, Diabetes, 58, 2185, 10.2337/db09-0967

Las, 2010, The role of autophagy in β-cell lipotoxicity and type 2 diabetes, Diabetes Obes Metab., 12, 15, 10.1111/j.1463-1326.2010.01268.x

Wong, 2013, The ULK1 complex: sensing nutrient signals for autophagy activation, Autophagy, 9, 124, 10.4161/auto.23323

Parzych, 2014, An overview of autophagy: morphology, mechanism, and regulation, Antioxid Redox Signal., 20, 460, 10.1089/ars.2013.5371

Li, 2006, Islet microvasculature in islet hyperplasia and failure in a model of type 2 diabetes, Diabetes, 55, 2965, 10.2337/db06-0733

Ebato, 2008, Autophagy is important in islet homeostasis and compensatory increase of β cell mass in response to high-fat diet, Cell Metab., 8, 325, 10.1016/j.cmet.2008.08.009

Choi, 2009, Protective role of autophagy in palmitate-induced INS-1 β-cell death, Endocrinology, 150, 126, 10.1210/en.2008-0483

Las, 2011, Fatty acids suppress autophagic turnover in β-cells, J Biol Chem., 286, 42534, 10.1074/jbc.M111.242412

Li, 2013, Cathepsin B contributes to autophagy-related 7 (Atg7)-induced nod-like receptor 3 (NLRP3)-dependent proinflammatory response and aggravates lipotoxicity in rat insulinoma cell line, J Biol Chem., 288, 30094, 10.1074/jbc.M113.494286