Oxidative stress and calcium dysregulation by palmitate in type 2 diabetes

Experimental and Molecular Medicine

Volumn 49, Issue 2, 2017, Pages

  Ly, Luong Dai ^a   Xu, Shanhua ^a   Choi, Seong Kyung ^a   Ha, Chae Myeong ^b   Thoudam, Themis ^b   Cha, Seung Kuy ^a   Wiederkehr, Andreas ^c   Wollheim, Claes B ^d   Lee, In Kyu ^b   Park, Kyu Sang ^a  

^a Yonsei University Wonju   (South Korea)

^b Kyungpook National University   (South Korea)

^c NESTLÉ RESEARCH CENTER   (Switzerland)

^d UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CARNITINE PALMITOYLTRANSFERASE I; CD36 ANTIGEN; DIACYLGLYCEROL ACYLTRANSFERASE; GLUCOSE TRANSPORTER 4; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PALMITIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; RYANODINE RECEPTOR 1; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; STRESS ACTIVATED PROTEIN KINASE; CALCIUM; FATTY ACID; PALMITIC ACID DERIVATIVE;

APOPTOSIS; BIOACCUMULATION; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME SYNTHESIS; HUMAN; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; LIPOTOXICITY; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PATHOGENESIS; PERIODONTITIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; REVIEW; ANIMAL; ENDOPLASMIC RETICULUM; METABOLISM; PATHOLOGY;

ANIMALS; CALCIUM; CD36 ANTIGENS; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS, NONESTERIFIED; HUMANS; INSULIN-SECRETING CELLS; MITOCHONDRIA; OXIDATIVE STRESS; PALMITIC ACIDS; REACTIVE OXYGEN SPECIES;

EID: 85011578616     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2016.143     Document Type: Review

References (157)

1. Choi CS, Savage DB, Kulkarni A, Yu XX, Liu ZX, Morino K et al. Suppression of diacylglycerol acyltransferase-2 (DGAT2), but not DGAT1, with antisense oligonucleotides reverses diet-induced hepatic steatosis, insulin resistance. J Biol Chem 2007; 282: 22678-22688.
2. Hagenfeldt L, Wahren J, Pernow B, Raf L. Uptake of individual free fatty acids by skeletal muscle, liver in man. J Clin Invest 1972; 51: 2324-2330.
3. Fraze E, Donner CC, Swislocki AL, Chiou YA, Chen YD, Reaven GM. Ambient plasma free fatty acid concentrations in noninsulin-dependent diabetes mellitus: evidence for insulin resistance. J Clin Endocrinol Metab 1985; 61: 807-811.
4. Miles JM, Wooldridge D, Grellner WJ, Windsor S, Isley WL, Klein S et al. Nocturnal, postprandial free fatty acid kinetics in normal, type 2 diabetic subjects: effects of insulin sensitization therapy. Diabetes 2003; 52: 675-681.
5. Charles MA, Eschwege E, Thibult N, Claude JR, Warnet JM, Rosselin GE et al. The role of non-esterified fatty acids in the deterioration of glucose tolerance in Caucasian subjects: results of the Paris Prospective Study. Diabetologia 1997; 40: 1101-1106.
6. Abumrad NA, el-Maghrabi MR, Amri EZ, Lopez E, Grimaldi PA. Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J Biol Chem 1993; 268: 17665-17668.
7. Van Nieuwenhoven FA, Verstijnen CP, Abumrad NA, Willemsen PH, Van Eys GJ, Van der Vusse GJ et al. Putative membrane fatty acid translocase, cytoplasmic fatty acid-binding protein are co-expressed in rat heart, skeletal muscles. Biochem Biophys Res Commun 1995; 207: 747-752.
8. Coburn CT, Knapp FF Jr, Febbraio M, Beets AL, Silverstein RL, Abumrad NA. Defective uptake, utilization of long chain fatty acids in muscle, adipose tissues of CD36 knockout mice. J Biol Chem2000; 275: 32523-32529.
9. He J, Lee JH, Febbraio M, Xie W. The emerging roles of fatty acid translocase/CD36, the aryl hydrocarbon receptor in fatty liver disease. Exp Biol Med (Maywood) 2011; 236: 1116-1121.
10. Swerlick RA, Lee KH, Wick TM, Lawley TJ. Human dermal microvascular endothelial but not human umbilical vein endothelial cells express CD36 in vivo, in vitro. J Immunol 1992; 148: 78-83.
11. Endemann G, Stanton LW, Madden KS, Bryant CM, White RT, Protter AA. CD36 is a receptor for oxidized low density lipoprotein. J Biol Chem. 1993; 268: 11811-11816.
12. Huh HY, Pearce SF, Yesner LM, Schindler JL, Silverstein RL. Regulated expression of CD36 during monocyte-to-macrophage differentiation: potential role of CD36 in foam cell formation. Blood 1996; 87: 2020-2028.
13. Noushmehr H, D'Amico E, Farilla L, Hui H, Wawrowsky KA, Mlynarski W et al. Fatty acid translocase (FAT/CD36) is localized on insulin-containing granules in human pancreatic beta-cells, mediates fatty acid effects on insulin secretion. Diabetes 2005; 54: 472-481.
14. Mayrhofer C, Krieger S, Huttary N, Chang MW, Grillari J, Allmaier G et al. Alterations in fatty acid utilization, an impaired antioxidant defense mechanism are early events in podocyte injury: a proteomic analysis. Am J Pathol 2009; 174: 1191-1202.
15. Ibrahimi A, Bonen A, Blinn WD, Hajri T, Li X, Zhong K et al. Muscle-specific overexpression of FAT/CD36 enhances fatty acid oxidation by contracting muscle, reduces plasma triglycerides, fatty acids, , increases plasma glucose, insulin. J Biol Chem 1999; 274: 26761-26766.
16. Febbraio M, Abumrad NA, Hajjar DP, Sharma K, Cheng W, Pearce SF et al. A null mutation in murine CD36 reveals an important role in fatty acid, lipoprotein metabolism. J Biol Chem 1999; 274: 19055-19062.
17. Garbacz WG, Lu P, Miller TM, Poloyac SM, Eyre NS, Mayrhofer G et al. Hepatic overexpression of CD36 improves glycogen homeostasis, attenuates high-fat diet induced hepatic steatosis, insulin resistance. Mol Cell Biol 2016; 36: 2715-2727.
18. Hames KC, Vella A, Kemp BJ, Jensen MD. Free fatty acid uptake in humans with CD36 deficiency. Diabetes 2014; 63: 3606-3614.
19. Wilson CG, Tran JL, Erion DM, Vera NB, Febbraio M, Weiss EJ. Hepatocyte-Specific Disruption of CD36 Attenuates Fatty Liver, Improves Insulin Sensitivity in HFD-Fed Mice. Endocrinology 2016; 157: 570-585.
20. Silverstein RL, Li W, Park YM, Rahaman SO. Mechanisms of cell signaling by the scavenger receptor CD36: implications in atherosclerosis, thrombosis. Trans Am Clin Climatol Assoc 2010; 121: 206-220.
21. Kuda O, Jenkins CM, Skinner JR, Moon SH, Su X, Gross RW et al. CD36 protein is involved in store-operated calcium flux, phospholipase A2 activation, , production of prostaglandin E2. J Biol Chem 2011; 286: 17785-17795.
22. Abdoul-Azize S, Selvakumar S, Sadou H, Besnard P, Khan NA. Ca2+ signaling in taste bud cells, spontaneous preference for fat: unresolved roles of CD36, GPR120. Biochimie 2014; 96: 8-13.
23. Kim YW, Moon JS, Seo YJ, Park SY, Kim JY, Yoon JS et al. Inhibition of fatty acid translocase cluster determinant 36 (CD36), stimulated by hyperglycemia, prevents glucotoxicity in INS-1 cells. Biochem Biophys Res Commun 2012; 420: 462-466.
24. Hua W, Huang HZ, Tan LT, Wan JM, Gui HB, Zhao L et al. CD36 mediated fatty acid-induced podocyte apoptosis via oxidative stress. PLoS ONE 2015; 10: e0127507.
25. Wallin T, Ma Z, Ogata H, Jorgensen IH, Iezzi M, Wang H et al. Facilitation of fatty acid uptake by CD36 in insulin-producing cells reduces fatty-acidinduced insulin secretion, glucose regulation of fatty acid oxidation. Biochim Biophys Acta 2010; 1801: 191-197.
26. Gharib M, Tao H, Fungwe TV, Hajri T. Cluster differentiating 36 (CD36) deficiency attenuates obesity-associated oxidative stress in the heart. PLoS ONE 2016; 11: e0155611.
27. Febbraio M, Podrez EA, Smith JD, Hajjar DP, Hazen SL, Hoff HF et al. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest 2000; 105: 1049-1056.
28. Harmon CM, Luce P, Beth AH, Abumrad NA. Labeling of adipocyte membranes by sulfo-N-succinimidyl derivatives of long-chain fatty acids: inhibition of fatty acid transport. J Membr Biol 1991; 121: 261-268.
29. Coort SL, Willems J, Coumans WA, van der Vusse GJ, Bonen A, Glatz JF et al. Sulfo-N-succinimidyl esters of long chain fatty acids specifically inhibit fatty acid translocase (FAT/CD36)-mediated cellular fatty acid uptake. Mol Cell Biochem 2002; 239: 213-219.
30. Xu S, Nam SM, Kim JH, Das R, Choi SK, Nguyen TT et al. Palmitate induces ER calcium depletion, apoptosis in mouse podocytes subsequent to mitochondrial oxidative stress. Cell Death Dis 2015; 6: e1976.
31. Souza AC, Bocharov AV, Baranova IN, Vishnyakova TG, Huang YG, Wilkins KJ et al. Antagonism of scavenger receptor CD36 by 5A peptide prevents chronic kidney disease progression in mice independent of blood pressure regulation. Kidney Int 2016; 89: 809-822.
32. Trachootham D, Lu W, Ogasawara MA, Nilsa RD, Huang P. Redox regulation of cell survival. Antioxid Redox Signal 2008; 10: 1343-1374.
33. Wehinger S, Ortiz R, Diaz MI, Aguirre A, Valenzuela M, Llanos P et al. Phosphorylation of caveolin-1 on tyrosine-14 induced by ROS enhances palmitate-induced death of beta-pancreatic cells. Biochim Biophys Acta 2015; 1852: 693-708.
34. Liu J, Chang F, Li F, Fu H, Wang J, Zhang S et al. Palmitate promotes autophagy, apoptosis through ROS-dependent JNK, p38 MAPK. Biochem Biophys Res Commun 2015; 463: 262-267.
35. Carlsson C, Borg LA, Welsh N. Sodium palmitate induces partial mitochondrial uncoupling, reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 1999; 140: 3422-3428.
36. Sato Y, Fujimoto S, Mukai E, Sato H, Tahara Y, Ogura K et al. Palmitate induces reactive oxygen species production, beta-cell dysfunction by activating nicotinamide adenine dinucleotide phosphate oxidase through Src signaling. J Diabetes Investig 2014; 5: 19-26.
37. Barlow J, Affourtit C. Novel insights into pancreatic beta-cell glucolipotoxicity from real-time functional analysis of mitochondrial energy metabolism in INS-1E insulinoma cells. Biochem J 2013; 456: 417-426.
38. Joseph LC, Barca E, Subramanyam P, Komrowski M, Pajvani U, Colecraft HM et al. Inhibition of NAPDH oxidase 2 (NOX2) Prevents oxidative stress, mitochondrial abnormalities caused by saturated fat in cardiomyocytes. PLoS ONE 2016; 11: e0145750.
39. Brodeur MR, Bouvet C, Barrette M, Moreau P. Palmitic acid increases medial calcification by inducing oxidative stress. J Vasc Res 2013; 50: 430-441.
40. Yamagishi S, Okamoto T, Amano S, Inagaki Y, Koga K, Koga M et al. Palmitate-induced apoptosis of microvascular endothelial cells, pericytes. Mol Med 2002; 8: 179-184.
41. Taheripak G, Bakhtiyari S, Rajabibazl M, Pasalar P, Meshkani R. Protein tyrosine phosphatase 1B inhibition ameliorates palmitate-induced mitochondrial dysfunction, apoptosis in skeletal muscle cells. Free Radic Biol Med 2013; 65: 1435-1446.
42. Gao D, Nong S, Huang X, Lu Y, Zhao H, Lin Y et al. The effects of palmitate on hepatic insulin resistance are mediated by NADPH Oxidase 3-derived reactive oxygen species through JNK, p38MAPK pathways. J Biol Chem 2010; 285: 29965-29973.
43. Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME. The c-Jun N-terminal kinase mediates the induction of oxidative stress, insulin resistance by palmitate, toll-like receptor 2, 4 ligands in 3T3-L1 adipocytes. Horm Metab Res 2009; 41: 523-530.
44. Lambertucci RH, Hirabara SM, Silveira Ldos R, Levada-Pires AC, Curi R, Pithon-Curi TC. Palmitate increases superoxide production through mitochondrial electron transport chain, NADPH oxidase activity in skeletal muscle cells. J Cell Physiol 2008; 216: 796-804.
45. Nakamura S, Takamura T, Matsuzawa-Nagata N, Takayama H, Misu H, Noda H et al. Palmitate induces insulin resistance in H4IIEC3 hepatocytes through reactive oxygen species produced by mitochondria. J Biol Chem 2009; 284: 14809-14818.
46. Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX et al. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration, activation of uncoupling proteins. Diabetes 2007; 56: 2457-2466.
47. Choi SE, Jung IR, Lee YJ, Lee SJ, Lee JH, Kim Y et al. Stimulation of lipogenesis as well as fatty acid oxidation protects against palmitateinduced INS-1 beta-cell death. Endocrinology 2011; 152: 816-827.
48. Namgaladze D, Lips S, Leiker TJ, Murphy RC, Ekroos K, Ferreiros N et al. Inhibition of macrophage fatty acid beta-oxidation exacerbates palmitateinduced inflammatory, endoplasmic reticulum stress responses. Diabetologia 2014; 57: 1067-1077.
49. Fu D, Lu J, Yang S. Oleic/palmitate induces apoptosis in human articular chondrocytes via upregulation of NOX4 expression, ROS production. Ann Clin Lab Sci 2016; 46: 353-359.
50. Das R, Xu S, Quan X, Nguyen TT, Kong ID, Chung CH et al. Upregulation of mitochondrial Nox4 mediates TGF-beta-induced apoptosis in cultured mouse podocytes. Am J Physiol Renal Physiol 2014; 306: F155-F167.
51. Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis, mitochondrial dysfunction in cardiac myocytes. Circ Res 2010; 106: 1253-1264.
52. Watson ML, Macrae K, Marley AE, Hundal HS. Chronic effects of palmitate overload on nutrient-induced insulin secretion, autocrine signalling in pancreatic MIN6 beta cells. PLoS ONE 2011; 6: e25975.
53. Macrae K, Stretton C, Lipina C, Blachnio-Zabielska A, Baranowski M, Gorski J et al. Defining the role of DAG, mitochondrial function, , lipid deposition in palmitate-induced proinflammatory signaling, its counter-modulation by palmitoleate. J Lipid Res 2013; 54: 2366-2378.
54. Leamy AK, Egnatchik RA, Shiota M, Ivanova PT, Myers DS, Brown HA et al. Enhanced synthesis of saturated phospholipids is associated with ER stress, lipotoxicity in palmitate treated hepatic cells. J Lipid Res 2014; 55: 1478-1488.
55. Dikalov S. Cross talk between mitochondria, NADPH oxidases. Free Radic Biol Med 2011; 51: 1289-1301.
56. Lu G, Greene EL, Nagai T, Egan BM. Reactive oxygen species are critical in the oleic acid-mediated mitogenic signaling pathway in vascular smooth muscle cells. Hypertension 1998; 32: 1003-1010.
57. Koulajian K, Desai T, Liu GC, Ivovic A, Patterson JN, Tang C et al. NADPH oxidase inhibition prevents beta cell dysfunction induced by prolonged elevation of oleate in rodents. Diabetologia 2013; 56: 1078-1087.
58. Pang J, Cui J, Gong H, Xi C, Zhang TM. Effect of NAD on PARP-mediated insulin sensitivity in oleic acid treated hepatocytes. J Cell Physiol 2015; 230: 1607-1613.
59. Lamers D, Schlich R, Horrighs A, Cramer A, Sell H, Eckel J. Differential impact of oleate, palmitate, , adipokines on expression of NF-kappaB target genes in human vascular smooth muscle cells. Mol Cell Endocrinol 2012; 362: 194-201.
60. Park EJ, Lee AY, Chang SH, Yu KN, Kim JH, Cho MH. Role of p53 in the cellular response following oleic acid accumulation in Chang liver cells. Toxicol Lett 2014; 224: 114-120.
61. Yuzefovych L, Wilson G, Rachek L. Different effects of oleate vs. palmitate on mitochondrial function, apoptosis, , insulin signaling in L6 skeletal muscle cells: role of oxidative stress. Am J Physiol Endocrinol Metab 2010; 299: E1096-E1105.
62. Ellgaard L, Molinari M, Helenius A. Setting the standards: quality control in the secretory pathway. Science 1999; 286: 1882-1888.
63. Tu BP, Weissman JS. Oxidative protein folding in eukaryotes: mechanisms, consequences. J Cell Biol 2004; 164: 341-346.
64. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress, oxidative stress: a vicious cycle or a double-edged sword Antioxid Redox Signal 2007; 9: 2277-2293.
65. Cao SS, Kaufman RJ. Endoplasmic reticulum stress, oxidative stress in cell fate decision, human disease. Antioxid Redox Signal 2014; 21: 396-413.
66. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74: 739-789.
67. Back SH, Kaufman RJ. Endoplasmic reticulum stress, type 2 diabetes. Annu Rev Biochem 2012; 81: 767-793.
68. Cnop M, Ladriere L, Igoillo-Esteve M, Moura RF, Cunha DA. Causes, cures for endoplasmic reticulum stress in lipotoxic beta-cell dysfunction. Diabetes Obes Metab 2010; 12(Suppl 2): 76-82.
69. Hage Hassan R, Bourron O, Hajduch E. Defect of insulin signal in peripheral tissues: Important role of ceramide. World J Diabetes 2014; 5: 244-257.
70. Chaurasia B, Summers SA. Ceramides-lipotoxic inducers of metabolic disorders. Trends Endocrinol Metab 2015; 26: 538-550.
71. Ueda N. Ceramide-induced apoptosis in renal tubular cells: a role of mitochondria, sphingosine-1-phoshate. Int J Mol Sci 2015; 16: 5076-5124.
72. Raichur S, Wang ST, Chan PW, Li Y, Ching J, Chaurasia B et al. CerS2 haploinsufficiency inhibits beta-oxidation, confers susceptibility to diet-induced steatohepatitis, insulin resistance. Cell Metab 2014; 20: 687-695.
73. Liu Z, Xia Y, Li B, Xu H, Wang C, Liu Y et al. Induction of ER stress-mediated apoptosis by ceramide via disruption of ER Ca(2+) homeostasis in human adenoid cystic carcinoma cells. Cell Biosci 2014; 4: 71.
74. Soumura M, Kume S, Isshiki K, Takeda N, Araki S, Tanaka Y et al. Oleate, eicosapentaenoic acid attenuate palmitate-induced inflammation, apoptosis in renal proximal tubular cell. Biochem Biophys Res Commun 2010; 402: 265-271.
75. Sieber J, Lindenmeyer MT, Kampe K, Campbell KN, Cohen CD, Hopfer H et al. Regulation of podocyte survival, endoplasmic reticulum stress by fatty acids. Am J Physiol Renal Physiol 2010; 299: F821-F829.
76. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV Jr, Ory DS et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 2003; 100: 3077-3082.
77. Thorn K, Bergsten P. Fatty acid-induced oxidation, triglyceride formation is higher in insulin-producing MIN6 cells exposed to oleate compared to palmitate. J Cell Biochem 2010; 111: 497-507.
78. Henique C, Mansouri A, Fumey G, Lenoir V, Girard J, Bouillaud F et al. Increased mitochondrial fatty acid oxidation is sufficient to protect skeletal muscle cells from palmitate-induced apoptosis. J Biol Chem 2010; 285: 36818-36827.
79. Sieber J, Weins A, Kampe K, Gruber S, Lindenmeyer MT, Cohen CD et al. Susceptibility of podocytes to palmitic acid is regulated by stearoyl-CoA desaturases 1, 2. Am J Pathol 2013; 183: 735-744.
80. Heard A, Thompson J, Carver J, Bakey M, Wang XR. Targeting molecular chaperones for the treatment of cystic fibrosis: is it a viable approach Curr Drug Targets 2015; 16: 958-964.
81. Silverman GA, Pak SC, Perlmutter DH. Disorders of protein misfolding: alpha-1-antitrypsin deficiency as prototype. J Pediatr 2013; 163: 320-326.
82. Mukherjee A, Morales-Scheihing D, Butler PC, Soto C. Type 2 diabetes as a protein misfolding disease. Trends Mol Med 2015; 21: 439-449.
83. Moreno JA, Radford H, Peretti D, Steinert JR, Verity N, Martin MG et al. Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration. Nature 2012; 485: 507-511.
84. Pfaffenbach KT, Gentile CL, Nivala AM, Wang D, Wei Y, Pagliassotti MJ. Linking endoplasmic reticulum stress to cell death in hepatocytes: roles of C/EBP homologous protein, chemical chaperones in palmitatemediated cell death. Am J Physiol Endocrinol Metab 2010; 298: E1027-E1035.
85. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D et al. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 2005; 307: 935-939.
86. Cnop M, Ladriere L, Hekerman P, Ortis F, Cardozo AK, Dogusan Z et al. Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress, causes pancreatic beta-cell dysfunction, apoptosis. J Biol Chem 2007; 282: 3989-3997.
87. Ladriere L, Igoillo-Esteve M, Cunha DA, Brion JP, Bugliani M, Marchetti P et al. Enhanced signaling downstream of ribonucleic Acid-activated protein kinase-like endoplasmic reticulum kinase potentiates lipotoxic endoplasmic reticulum stress in human islets. J Clin Endocrinol Metab 2010; 95: 1442-1449.
88. Cunha DA, Hekerman P, Ladriere L, Bazarra-Castro A, Ortis F, Wakeham MC et al. Initiation, execution of lipotoxic ER stress in pancreatic beta-cells. J Cell Sci. 2008; 121(Pt 14): 2308-2318.
89. Malhi H, Kropp EM, Clavo VF, Kobrossi CR, Han J, Mauer AS et al. C/EBP homologous protein-induced macrophage apoptosis protects mice from steatohepatitis. J Biol Chem 2013; 288: 18624-18642.
90. Mekahli D, Bultynck G, Parys JB, De Smedt H, Missiaen L. Endoplasmicreticulum calcium depletion, disease. Cold Spring Harb Perspect Biol 2011; 3: a004317.
91. Gwiazda KS, Yang TL, Lin Y, Johnson JD. Effects of palmitate on ER, cytosolic Ca2+ homeostasis in beta-cells. Am J Physiol Endocrinol Metab 2009; 296: E690-E701.
92. Hara T, Mahadevan J, Kanekura K, Hara M, Lu S, Urano F. Calcium efflux from the endoplasmic reticulum leads to beta-cell death. Endocrinology 2014; 155: 758-768.
93. Fu S, Yang L, Li P, Hofmann O, Dicker L, Hide W et al. Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 2011; 473: 528-531.
94. Haynes CM, Titus EA, Cooper AA. Degradation of misfolded proteins prevents ER-derived oxidative stress, cell death. Mol Cell 2004; 15: 767-776.
95. Li G, Mongillo M, Chin KT, Harding H, Ron D, Marks AR et al. Role of ERO1-alpha-mediated stimulation of inositol 1, 4, 5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J Cell Biol 2009; 186: 783-792.
96. Weissmann N, Sydykov A, Kalwa H, Storch U, Fuchs B, Mederos y Schnitzler M et al. Activation of TRPC6 channels is essential for lung ischaemia-reperfusion induced oedema in mice. Nat Commun 2012; 3: 649.
97. Hong JH, Moon SJ, Byun HM, Kim MS, Jo H, Bae YS et al. Critical role of phospholipase Cgamma1 in the generation of H2O2-evoked [Ca2+]i oscillations in cultured rat cortical astrocytes. J Biol Chem 2006; 281: 13057-13067.
98. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T et al. BAX, BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 2003; 300: 135-139.
99. Demaurex N, Distelhorst C. Cell biology. Apoptosis-the calcium connection. Science 2003; 300: 65-67.
100. Csordas G, Renken C, Varnai P, Walter L, Weaver D, Buttle KF et al. Structural, functional features, significance of the physical linkage between ER, mitochondria. J Cell Biol 2006; 174: 915-921.
101. Arruda AP, Pers BM, Parlakgul G, Guney E, Inouye K, Hotamisligil GS. Chronic enrichment of hepatic endoplasmic reticulum-mitochondria contact leads to mitochondrial dysfunction in obesity. Nat Med 2014; 20: 1427-1435.
102. Tubbs E, Theurey P, Vial G, Bendridi N, Bravard A, Chauvin MA et al. Mitochondria-associated endoplasmic reticulum membrane (MAM) integrity is required for insulin signaling, is implicated in hepatic insulin resistance. Diabetes 2014; 63: 3279-3294.
103. Rizzuto R, De Stefani D, Raffaello A, Mammucari C. Mitochondria as sensors, regulators of calcium signalling. Nat Rev Mol Cell Biol 2012; 13: 566-578.
104. Arruda AP, Hotamisligil GS. Calcium homeostasis, organelle function in the pathogenesis of obesity, diabetes. Cell Metab 2015; 22: 381-397.
105. Choi SE, Kim HE, Shin HC, Jang HJ, Lee KW, Kim Y et al. Involvement of Ca2+-mediated apoptotic signals in palmitate-induced MIN6N8a beta cell death. Mol Cell Endocrinol 2007; 272: 50-62.
106. Park KS, Wiederkehr A, Kirkpatrick C, Mattenberger Y, Martinou JC, Marchetti P et al. Selective actions of mitochondrial fission/fusion genes on metabolism-secretion coupling in insulin-releasing cells. J Biol Chem 2008; 283: 33347-33356.
107. Wiederkehr A, Wollheim CB. Minireview: implication of mitochondria in insulin secretion, action. Endocrinology 2006; 147: 2643-2649.
108. Wiederkehr A, Wollheim CB. Impact of mitochondrial calcium on the coupling of metabolism to insulin secretion in the pancreatic beta-cell. Cell Calcium 2008; 44: 64-76.
109. Del Arco A, Contreras L, Pardo B, Satrustegui J. Calcium regulation of mitochondrial carriers. Biochim Biophys Acta 2016; 1863: 2413-2421.
110. De Marchi U, Thevenet J, Hermant A, Dioum E, Wiederkehr A. Calcium co-regulates oxidative metabolism, ATP synthase-dependent respiration in pancreatic beta cells. J Biol Chem 2014; 289: 9182-9194.
111. Quan X, Nguyen TT, Choi SK, Xu S, Das R, Cha SK et al. Essential role of mitochondrial Ca2+ uniporter in the generation of mitochondrial pH gradient, metabolism-secretion coupling in insulin-releasing cells. J Biol Chem 2015; 290: 4086-4096.
112. Pendin D, Greotti E, Pozzan T. The elusive importance of being a mitochondrial Ca(2+) uniporter. Cell Calcium 2014; 55: 139-145.
113. Pan X, Liu J, Nguyen T, Liu C, Sun J, Teng Y et al. The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter. Nat Cell Biol 2013; 15: 1464-1472.
114. Kwong JQ, Lu X, Correll RN, Schwanekamp JA, Vagnozzi RJ, Sargent MA et al. The mitochondrial calcium uniporter selectively matches metabolic output to acute contractile stress in the heart. Cell Rep 2015; 12: 15-22.
115. Yi M, Weaver D, Hajnoczky G. Control of mitochondrial motility, distribution by the calcium signal: a homeostatic circuit. J Cell Biol 2004; 167: 661-672.
116. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med 2000; 6: 513-519.
117. Turner N, Heilbronn LK. Is mitochondrial dysfunction a cause of insulin resistance Trends Endocrinol Metab 2008; 19: 324-330.
118. Szendroedi J, Phielix E, Roden M. The role of mitochondria in insulin resistance, type 2 diabetes mellitus. Nat Rev Endocrinol 2012; 8: 92-103.
119. Choi SE, Lee YJ, Hwang GS, Chung JH, Lee SJ, Lee JH et al. Supplement of TCA cycle intermediates protects against high glucose/palmitateinduced INS-1 beta cell death. Arch Biochem Biophys 2011; 505: 231-241.
120. Archer SL. Mitochondrial dynamics-mitochondrial fission, fusion in human diseases. N Engl J Med 2013; 369: 2236-2251.
121. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G et al. Fission, selective fusion govern mitochondrial segregation, elimination by autophagy. EMBO J 2008; 27: 433-446.
122. Molina AJ, Wikstrom JD, Stiles L, Las G, Mohamed H, Elorza A et al. Mitochondrial networking protects beta-cells from nutrient-induced apoptosis. Diabetes 2009; 58: 2303-2315.
123. Schuit FC, In't Veld PA, Pipeleers DG. Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells. Proc Natl Acad Sci USA 1988; 85: 3865-3869.
124. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-529.
125. Cardozo AK, Ortis F, Storling J, Feng YM, Rasschaert J, Tonnesen M et al. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b, deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes 2005; 54: 452-461.
126. Fonseca SG, Fukuma M, Lipson KL, Nguyen LX, Allen JR, Oka Y et al. WFS1 is a novel component of the unfolded protein response, maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells. J Biol Chem 2005; 280: 39609-39615.
127. Sandhu MS, Weedon MN, Fawcett KA, Wasson J, Debenham SL, Daly A et al. Common variants in WFS1 confer risk of type 2 diabetes. Nat Genet 2007; 39: 951-953.
128. Igoillo-Esteve M, Marselli L, Cunha DA, Ladriere L, Ortis F, Grieco FA et al. Palmitate induces a pro-inflammatory response in human pancreatic islets that mimics CCL2 expression by beta cells in type 2 diabetes. Diabetologia 2010; 53: 1395-1405.
129. Wiederkehr A, Wollheim CB. Mitochondrial signals drive insulin secretion in the pancreatic beta-cell. Mol Cell Endocrinol 2012; 353: 128-137.
130. Wiederkehr A, Wollheim CB. Linking fatty acid stress to beta-cell mitochondrial dynamics. Diabetes 2009; 58: 2185-2186.
131. Nobuhara M, Saotome M, Watanabe T, Urushida T, Katoh H, Satoh H et al. Mitochondrial dysfunction caused by saturated fatty acid loading induces myocardial insulin-resistance in differentiated H9c2 myocytes: a novel ex vivo myocardial insulin-resistance model. Exp Cell Res 2013; 319: 955-966.
132. Souto Padron de Figueiredo A, Salmon AB, Bruno F, Jimenez F, Martinez HG, Halade GV et al. Nox2 mediates skeletal muscle insulin resistance induced by a high fat diet. J Biol Chem 2015; 290: 13427-13439.
133. Yang L, Qian Z, Ji H, Yang R, Wang Y, Xi L et al. Inhibitory effect on protein kinase Ctheta by Crocetin attenuates palmitate-induced insulin insensitivity in 3T3-L1 adipocytes. Eur J Pharmacol 2010; 642: 47-55.
134. Martinez-Garcia C, Izquierdo-Lahuerta A, Vivas Y, Velasco I, Yeo TK, Chen S et al. Renal lipotoxicity-associated inflammation, insulin resistance affects actin cytoskeleton organization in podocytes. PLoS ONE 2015; 10: e0142291.
135. Mayer CM, Belsham DD. Palmitate attenuates insulin signaling, induces endoplasmic reticulum stress, apoptosis in hypothalamic neurons: rescue of resistance, apoptosis through adenosine 5 monophosphate-activated protein kinase activation. Endocrinology 2010; 151: 576-585.
136. Piro S, Maniscalchi ET, Monello A, Pandini G, Mascali LG, Rabuazzo AM et al. Palmitate affects insulin receptor phosphorylation, intracellular insulin signal in a pancreatic alpha-cell line. Endocrinology 2010; 151: 4197-4206.
137. Salvado L, Coll T, Gomez-Foix AM, Salmeron E, Barroso E, Palomer X et al. Oleate prevents saturated-fatty-acid-induced ER stress, inflammation, insulin resistance in skeletal muscle cells through an AMPK-dependent mechanism. Diabetologia 2013; 56: 1372-1382.
138. Kwon B, Lee HK, Querfurth HW. Oleate prevents palmitate-induced mitochondrial dysfunction, insulin resistance, inflammatory signaling in neuronal cells. Biochim Biophys Acta 2014; 1843: 1402-1413.
139. Perdomo L, Beneit N, Otero YF, Escribano O, Diaz-Castroverde S, Gomez-Hernandez A et al. Protective role of oleic acid against cardiovascular insulin resistance, in the early, late cellular atherosclerotic process. Cardiovasc Diabetol 2015; 14: 75.
140. Henriksen EJ, Diamond-Stanic MK, Marchionne EM. Oxidative stress, the etiology of insulin resistance, type 2 diabetes. Free Radic Biol Med 2011; 51: 993-999.
141. Galadari S, Rahman A, Pallichankandy S, Galadari A, Thayyullathil F. Role of ceramide in diabetes mellitus: evidence, mechanisms. Lipids Health Dis 2013; 12: 98.
142. Sathyanarayana P, Barthwal MK, Kundu CN, Lane ME, Bergmann A, Tzivion G et al. Activation of the Drosophila MLK by ceramide reveals TNF-alpha, ceramide as agonists of mammalian MLK3. Mol Cell 2002; 10: 1527-1533.
143. Lanner JT, Katz A, Tavi P, Sandstrom ME, Zhang SJ, Wretman C et al. The role of Ca2+ influx for insulin-mediated glucose uptake in skeletal muscle. Diabetes 2006; 55: 2077-2083.
144. Whitehead JP, Molero JC, Clark S, Martin S, Meneilly G, James DE. The role of Ca2+ in insulin-stimulated glucose transport in 3T3-L1 cells. J Biol Chem 2001; 276: 27816-27824.
145. Furuta A, Tanaka M, Omata W, Nagasawa M, Kojima I, Shibata H. Microtubule disruption with BAPTA, dimethyl BAPTA by a calcium chelation-independent mechanism in 3T3-L1 adipocytes. Endocr J 2009; 56: 235-243.
146. Contreras-Ferrat A, Llanos P, Vasquez C, Espinosa A, Osorio-Fuentealba C, Arias-Calderon M et al. Insulin elicits a ROS-activated, an IP(3)-dependent Ca(2)(+) release, which both impinge on GLUT4 translocation. J Cell Sci 2014; 127(Pt 9): 1911-1923.
147. Taddeo EP, Laker RC, Breen DS, Akhtar YN, Kenwood BM, Liao JA et al. Opening of the mitochondrial permeability transition pore links mitochondrial dysfunction to insulin resistance in skeletal muscle. Mol Metab 2014; 3: 124-134.
148. Wang CH, Tsai TF, Wei YH. Role of mitochondrial dysfunction, dysregulation of Ca(2+) homeostasis in insulin insensitivity of mammalian cells. Ann NY Acad Sci 2015; 1350: 66-76.
149. Brownlee M. Biochemistry, molecular cell biology of diabetic complications. Nature 2001; 414: 813-820.
150. Shah A, Xia L, Goldberg H, Lee KW, Quaggin SE, Fantus IG. Thioredoxin-interacting protein mediates high glucose-induced reactive oxygen species generation by mitochondria, the NADPH oxidase, Nox4, in mesangial cells. J Biol Chem 2013; 288: 6835-6848.
151. Manea A, Manea SA, Todirita A, Albulescu IC, Raicu M, Sasson S et al. High-glucose-increased expression, activation of NADPH oxidase in human vascular smooth muscle cells is mediated by 4-hydroxynonenalactivated PPARalpha, PPARbeta/delta. Cell Tissue Res 2015; 361: 593-604.
152. Cheng DW, Jiang Y, Shalev A, Kowluru R, Crook ED, Singh LP. An analysis of high glucose, glucosamine-induced gene expression, oxidative stress in renal mesangial cells. Arch Physiol Biochem 2006; 112: 189-218.
153. Daiber A. Redox signaling (cross-talk) from, to mitochondria involves mitochondrial pores, reactive oxygen species. Biochim Biophys Acta 2010; 1797: 897-906.
154. Kumar B, Kowluru A, Kowluru RA. Lipotoxicity augments glucotoxicity-induced mitochondrial damage in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci 2015; 56: 2985-2992.
155. Hong OK, Yoo SJ, Son JW, Kim MK, Baek KH, Song KH et al. High glucose, palmitate increases bone morphogenic protein 4 expression in human endothelial cells. Korean J Physiol Pharmacol 2016; 20: 169-175.
156. Lennon R, Pons D, Sabin MA, Wei C, Shield JP, Coward RJ et al. Saturated fatty acids induce insulin resistance in human podocytes: implications for diabetic nephropathy. Nephrol Dial Transplant 2009; 24: 3288-3296.
157. Shikama Y, Kudo Y, Ishimaru N, Funaki M. Possible Involvement of Palmitate in Pathogenesis of Periodontitis. J Cell Physiol 2015; 230: 2981-2989.