Endoplasmic reticulum stress may be involved in insulin resistance and lipid metabolism disorders of the white adipose tissues induced by high-fat diet containing industrial trans-fatty acids

References

• Wanders AJ , Zock PL , Brouwer IA . Trans fat intake and its dietary sources in general populations worldwide: a systematic review. Nutrients . 2017;9:840. doi:10.3390/nu9080840
   Web of Science ®Google Scholar
• Mazidi M , Cicero AF , Kengne AP , Banach M . Association between plasma trans-fatty acid concentrations and measures of glucose homeostasis and cardiovascular risk factors in adults in NHANES 1999-2000. Angiology . 2018;69:630–637. doi:10.1177/0003319717745987 29241351
   PubMed Web of Science ®Google Scholar
• Chajès V , Biessy C , Ferrari P , et al. Plasma elaidic acid level as biomarker of industrial trans fatty acids and risk of weight change: report from the EPIC study. PLoS One . 2015;10:e0118206. doi:10.1371/journal.pone.0118206 25675445
   PubMed Web of Science ®Google Scholar
• Wang Q , McKenna M , Borges ÁH , Duprez D , Neuhaus J , Neaton JD . Plasma phospholipid trans-fatty acids levels, cardiovascular diseases, and total mortality: the cardiovascular health study. J Am Heart Assoc . 2014;3. doi:10.1161/JAHA.114.000914.
   Web of Science ®Google Scholar
• Liu B , Sun Y , Snetselaar LG , et al. Association between plasma trans-fatty acid concentrations and diabetes in a nationally representative sample of US adults. J Diabetes . 2018;10:653–664. doi:10.1111/1753-0407.12652 29446544
   PubMed Web of Science ®Google Scholar
• Gomez de la Camara A , De Andrés Esteban E , Urrútia Cuchí G , et al. Variability of nutrients intake, lipid profile and cardiovascular mortality among geographical areas in Spain: the DRECE study. Geospat Health . 2017;12:524. doi:10.4081/gh.2017.524 29239557
   PubMed Web of Science ®Google Scholar
• Li C , He JZ , Zhou XD , Xu X . [Berberine regulates type 2 diabetes mellitus related with insulin resistance]. Zhongguo Zhong Yao Za Zhi . 2017;42:2254–2260. doi:10.19540/j.cnki.cjcmm.20170307.014 28822177
   PubMedGoogle Scholar
• Elagizi A , Kachur S , Lavie CJ , et al. An overview and update on obesity and the obesity paradox in cardiovascular diseases. Prog Cardiovasc Dis . 2018;61:142–150. doi:10.1016/j.pcad.2018.07.003 29981771
   PubMed Web of Science ®Google Scholar
• Sonmez A , Yumuk V , Haymana C , et al. Impact of obesity on the metabolic control of type 2 diabetes: results of the Turkish nationwide survey of glycemic and other metabolic parameters of patients with diabetes mellitus (TEMD obesity study). Obes Facts . 2019;12:167–178. doi:10.1159/000496624 30893706
   PubMed Web of Science ®Google Scholar
• Liu MQ , Chen Z , Chen LX . Endoplasmic reticulum stress: a novel mechanism and therapeutic target for cardiovascular diseases. Acta Pharmacol Sin . 2016;37:425–443. doi:10.1038/aps.2015.145 26838072
   PubMed Web of Science ®Google Scholar
• Flamment M , Hajduch E , Ferre P , Foufelle F . New insights into ER stress-induced insulin resistance. Trends Endocrinol Metab . 2012;23:381–390. doi:10.1016/j.tem.2012.06.003 22770719
   PubMed Web of Science ®Google Scholar
• Sharma NK , Das SK , Mondal AK , et al. Endoplasmic reticulum stress markers are associated with obesity in nondiabetic subjects. J Clin Endocrinol Metab . 2008;93:4532–4541. doi:10.1210/jc.2008-1001 18728164
   PubMed Web of Science ®Google Scholar
• Yu X , Ren L-P , Wang C , et al. Role of X-box binding protein-1 in fructose-induced de novo lipogenesis in HepG2 cells. Chin Med J (Engl) . 2018;131:2310–2319. doi:10.4103/0366-6999.241799 30246717
   PubMed Web of Science ®Google Scholar
• Yilmaz E . Endoplasmic reticulum stress and obesity. Adv Exp Med Biol . 2017;960:261–276. doi:10.1007/978-3-319-48382-5_11 28585203
   PubMed Web of Science ®Google Scholar
• Zobel EH , Hansen TW , Rossing P , von Scholten BJ . Global changes in food supply and the obesity epidemic. Curr Obes Rep . 2016;5:449–455. doi:10.1007/s13679-016-0233-8 27696237
   PubMed Web of Science ®Google Scholar
• Wang N , Wang J , Tang H-P , et al. Depot-specific inflammation with decreased expression of ATM2 in white adipose tissues induced by high-margarine/lard intake. PLoS One . 2017;12:e0188007. doi:10.1371/journal.pone.0188007 29141038
   PubMed Web of Science ®Google Scholar
• Jeyakumar SM , Vajreswari A , Giridharan NV . Chronic dietary vitamin A supplementation regulates obesity in an obese mutant WNIN/Ob rat model. Obesity (Silver Spring) . 2006;14:52–59. doi:10.1038/oby.2006.7 16493122
   PubMed Web of Science ®Google Scholar
• Shah SS , Rodriguez G , Musick A , et al. Targeting glioblastoma stem cells with 2-deoxy-D-glucose (2-DG) potentiates radiation-induced Unfolded Protein Response (UPR). Cancers (Basel) . 2019;11:159. doi:10.3390/cancers11020159
   Web of Science ®Google Scholar
• Zou C , Wang Y , Shen Z . 2-NBDG as a fluorescent indicator for direct glucose uptake measurement. J Biochem Biophys Methods . 2005;64:207–215. doi:10.1016/j.jbbm.2005.08.001 16182371
   PubMedGoogle Scholar
• Miyamoto JÉ , Ferraz ACG , Portovedo M , et al. Interesterified soybean oil promotes weight gain, impaired glucose tolerance and increased liver cellular stress markers. J Nutr Biochem . 2018;59:153–159. doi:10.1016/j.jnutbio.2018.05.014 30005920
   PubMed Web of Science ®Google Scholar
• Hung CS , Lee J-K , Yang C-Y , et al. Measurement of visceral fat: should we include retroperitoneal fat? PLoS One . 2014;9:e112355. doi:10.1371/journal.pone.0112355 25401949
   PubMed Web of Science ®Google Scholar
• Zhao X , Shen C , Zhu H , et al. Trans-fatty acids aggravate obesity, insulin resistance and hepatic steatosis in C57BL/6 mice, possibly by suppressing the IRS1 dependent pathway. Molecules . 2016;21:705. doi:10.3390/molecules21060705
   Web of Science ®Google Scholar
• Kavanagh K , Jones KL , Sawyer J , et al. Trans fat diet induces abdominal obesity and changes in insulin sensitivity in monkeys. Obesity (Silver Spring) . 2007;15:1675–1684. doi:10.1038/oby.2007.200 17636085
   PubMed Web of Science ®Google Scholar
• Brouwer IA , Wanders AJ , Katan MB . Effect of animal and industrial trans fatty acids on HDL and LDL cholesterol levels in humans–a quantitative review. PLoS One . 2010;5:e9434. doi:10.1371/journal.pone.0009434 20209147
   PubMed Web of Science ®Google Scholar
• Aronis KN , Joseph RJ , Blackburn GL , Mantzoros C . trans-Fatty acids, insulin resistance/diabetes, and cardiovascular disease risk: should policy decisions be based on observational cohort studies, or should we be waiting for results from randomized placebo-controlled trials? Metabolism . 2011;60:901–905. doi:10.1016/j.metabol.2011.04.003 21684360
   PubMed Web of Science ®Google Scholar
• Hunter JE . Dietary trans fatty acids: review of recent human studies and food industry responses. Lipids . 2006;41:967–992. doi:10.1007/s11745-006-5049-y 17263298
   PubMed Web of Science ®Google Scholar
• Micha R , King IB , Lemaitre RN , et al. Food sources of individual plasma phospholipid trans fatty acid isomers: the cardiovascular health study. Am J Clin Nutr . 2010;91:883–893. doi:10.3945/ajcn.2009.28877 20219966
   PubMed Web of Science ®Google Scholar
• Oshita T , Toh R , Shinohara M , et al. Elevated serum elaidic acid predicts risk of repeat revascularization after percutaneous coronary intervention in Japan. Circ J . 2019. doi:10.1253/circj.CJ-18-1175
   Web of Science ®Google Scholar
• Nishida C , Uauy R , Kumanyika S , Shetty P . The joint WHO/FAO expert consultation on diet, nutrition and the prevention of chronic diseases: process, product and policy implications. Public Health Nutr . 2004;7:245–250.14972063
   PubMed Web of Science ®Google Scholar
• Bendsen NT , Christensen R , Bartels EM , Astrup A . Consumption of industrial and ruminant trans fatty acids and risk of coronary heart disease: a systematic review and meta-analysis of cohort studies. Eur J Clin Nutr . 2011;65:773–783. doi:10.1038/ejcn.2011.34 21427742
   PubMed Web of Science ®Google Scholar
• Hwang E-Y , Yu M-H , Jung Y-S , Lee S-P , Shon JH , Lee S-O . Defatted safflower seed extract inhibits adipogenesis in 3T3-L1 preadipocytes and improves lipid profiles in C57BL/6J ob/ob mice fed a high-fat diet. Nutr Res . 2016;36:995–1003. doi:10.1016/j.nutres.2016.07.004 27632920
   PubMed Web of Science ®Google Scholar
• Rosenson RS , Brewer HB , Chapman MJ , et al. HDL measures, particle heterogeneity, proposed nomenclature, and relation to atherosclerotic cardiovascular events. Clin Chem . 2011;57:392–410. doi:10.1373/clinchem.2010.155333 21266551
   PubMed Web of Science ®Google Scholar
• Kosmas CE , Martinez I , Sourlas A , et al. High-density lipoprotein (HDL) functionality and its relevance to atherosclerotic cardiovascular disease. Drugs Context . 2018;7:212525. doi:10.7573/dic.212525 29623098
   PubMedGoogle Scholar
• Pagano ES , Spinedi E , Gagliardino JJ . White adipose tissue and circadian rhythm dysfunctions in obesity: pathogenesis and available therapies. Neuroendocrinology . 2017;104:347–363. doi:10.1159/000453317 27846625
   PubMed Web of Science ®Google Scholar
• Sun K , Kusminski CM , Scherer PE . Adipose tissue remodeling and obesity. J Clin Invest . 2011;121:2094–2101. doi:10.1172/JCI45887 21633177
   PubMed Web of Science ®Google Scholar
• Wang H , Sit WH , Tipoe GL , Liu Z , Wan JM . Comparative proteomic analysis of fibrotic liver of rats fed high fat diet contained lard versus corn oil. Clin Nutr . 2017;36:198–208. doi:10.1016/j.clnu.2015.10.015 26646359
   PubMed Web of Science ®Google Scholar
• Nakandakari S , Muñoz VR , Kuga GK , et al. Short-term high-fat diet modulates several inflammatory, ER stress, and apoptosis markers in the hippocampus of young mice. Brain Behav Immun . 2019. doi:10.1016/j.bbi.2019.02.016
   Web of Science ®Google Scholar
• Ozcan U , Cao Q , Yilmaz E , et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science . 2004;306:457–461. doi:10.1126/science.1103160 15486293
   PubMed Web of Science ®Google Scholar
• Chakrabarti A , Chen AW , Varner JD . A review of the mammalian unfolded protein response. Biotechnol Bioeng . 2011;108:2777–2793. doi:10.1002/bit.23282 21809331
   PubMed Web of Science ®Google Scholar
• Ibrahim IM , Abdelmalek DH , Elfiky AA . GRP78: A cell’s response to stress. Life Sci . 2019. doi:10.1016/j.lfs.2019.04.022
   Web of Science ®Google Scholar
• Gardner BM , Walter P . Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science . 2011;333:1891–1894. doi:10.1126/science.1209126 21852455
   PubMed Web of Science ®Google Scholar
• Bertolotti A , Zhang Y , Hendershot LM , Harding HP , Ron D . Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol . 2000;2:326–332. doi:10.1038/35014014 10854322
   PubMed Web of Science ®Google Scholar
• Zhang C , Kawauchi J , Adachi MT , et al. Activation of JNK and transcriptional repressor ATF3/LRF1 through the IRE1/TRAF2 pathway is implicated in human vascular endothelial cell death by homocysteine. Biochem Biophys Res Commun . 2001;289:718–724. doi:10.1006/bbrc.2001.6044 11726207
   PubMed Web of Science ®Google Scholar
• Shan B , Wang X , Wu Y , et al. The metabolic ER stress sensor IRE1alpha suppresses alternative activation of macrophages and impairs energy expenditure in obesity. Nat Immunol . 2017;18:519–529. doi:10.1038/ni.3709 28346409
   PubMed Web of Science ®Google Scholar
• Vinayagamoorthi R , Bobby Z , Sridhar MG . Antioxidants preserve redox balance and inhibit c-Jun-N-terminal kinase pathway while improving insulin signaling in fat-fed rats: evidence for the role of oxidative stress on IRS-1 serine phosphorylation and insulin resistance. J Endocrinol . 2008;197:287–296. doi:10.1677/JOE-08-0061 18434358
   PubMed Web of Science ®Google Scholar
• Rozo AV , Vijayvargia R , Weiss HR , Ruan H . Silencing Jnk1 and Jnk2 accelerates basal lipolysis and promotes fatty acid re-esterification in mouse adipocytes. Diabetologia . 2008;51:1493–1504. doi:10.1007/s00125-008-1036-6 18528680
   PubMed Web of Science ®Google Scholar
• Ito M , Nagasawa M , Omae N , et al. A novel JNK2/SREBP-1c pathway involved in insulin-induced fatty acid synthesis in human adipocytes. J Lipid Res . 2013;54:1531–1540. doi:10.1194/jlr.M031591 23515281
   PubMed Web of Science ®Google Scholar
• Boden G , Merali S . Measurement of the increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Methods Enzymol . 2011;489:67–82. doi:10.1016/B978-0-12-385116-1.00004-2 21266224
   PubMed Web of Science ®Google Scholar
• Han J , Kaufman RJ . The role of ER stress in lipid metabolism and lipotoxicity. J Lipid Res . 2016;57:1329–1338. doi:10.1194/jlr.R067595 27146479
   PubMed Web of Science ®Google Scholar
• Welch WJ , Brown CR . Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones . 1996;1:109–115. doi:10.1379/1466-1268(1996)001<0109:iomacc>2.3.co;2 9222596
   PubMed Web of Science ®Google Scholar
• Haberzettl P , Vladykovskaya E , Srivastava S , Bhatnagar A . Role of endoplasmic reticulum stress in acrolein-induced endothelial activation. Toxicol Appl Pharmacol . 2009;234:14–24. doi:10.1016/j.taap.2008.09.019 18951912
   PubMed Web of Science ®Google Scholar
• Inden M , Kitamura Y , Takeuchi H , et al. Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. J Neurochem . 2007;101:1491–1504. doi:10.1111/j.1471-4159.2006.04440.x 17459145
   PubMed Web of Science ®Google Scholar
• Gould GW , Holman GD . The glucose transporter family: structure, function and tissue-specific expression. Biochem J . 1993;295(Pt 2):329–341. doi:10.1042/bj2950329 8240230
   PubMed Web of Science ®Google Scholar
• Bryant NJ , Govers R , James DE . Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol . 2002;3:267–277. doi:10.1038/nrm782 11994746
   PubMed Web of Science ®Google Scholar
• Brewer PD , Habtemichael EN , Romenskaia I , Mastick CC , Coster AC . Glut4 is sorted from a Rab10 GTPase-independent constitutive recycling pathway into a highly insulin-responsive Rab10 GTPase-dependent sequestration pathway after adipocyte differentiation. J Biol Chem . 2016;291:773–789. doi:10.1074/jbc.M115.694919 26527681
   PubMed Web of Science ®Google Scholar
• Granados N , Amengual J , Ribot J , Palou A , Bonet ML . Distinct effects of oleic acid and its trans-isomer elaidic acid on the expression of myokines and adipokines in cell models. Br J Nutr . 2011;105:1226–1234. doi:10.1017/S0007114510004885 21208487
   PubMed Web of Science ®Google Scholar
• Saravanan N , Haseeb A , Ehtesham NZ ; Ghafoorunissa. Differential effects of dietary saturated and trans-fatty acids on expression of genes associated with insulin sensitivity in rat adipose tissue. Eur J Endocrinol . 2005;153:159–165. doi:10.1530/eje.1.01946.15998628
   PubMed Web of Science ®Google Scholar
• Li J , Houseknecht KL , Stenbit AE , Katz EB , Charron MJ . Reduced glucose uptake precedes insulin signaling defects in adipocytes from heterozygous GLUT4 knockout mice. Faseb J . 2000;14:1117–1125. doi:10.1096/fasebj.14.9.1117 10834933
   PubMed Web of Science ®Google Scholar
• Ozawa K , Miyazaki M , Matsuhisa M , et al. The endoplasmic reticulum chaperone improves insulin resistance in type 2 diabetes. Diabetes . 2005;54:657–663. doi:10.2337/diabetes.54.3.657 15734840
   PubMed Web of Science ®Google Scholar
• Nakatani Y , Kaneto H , Kawamori D , et al. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem . 2005;280:847–851. doi:10.1074/jbc.M411860200 15509553
   PubMed Web of Science ®Google Scholar
• Guo Q , Xu L , Li H , Sun H , Wu S , Zhou B . 4-PBA reverses autophagic dysfunction and improves insulin sensitivity in adipose tissue of obese mice via Akt/mTOR signaling. Biochem Biophys Res Commun . 2017;484:529–535. doi:10.1016/j.bbrc.2017.01.106 28153729
   PubMed Web of Science ®Google Scholar
• Copps KD , White MF . Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia . 2012;55:2565–2582. doi:10.1007/s00125-012-2644-8 22869320
   PubMed Web of Science ®Google Scholar
• Mahmutovic L , Bego T , Sterner M , et al. Association of IRS1 genetic variants with glucose control and insulin resistance in type 2 diabetic patients from Bosnia and Herzegovina. Drug Metab Pers Ther . 2019;34. doi:10.1515/dmpt-2018-0031.
   Google Scholar
• Bluher M , Michael MD , Peroni OD , et al. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev Cell . 2002;3:25–38.12110165
   PubMed Web of Science ®Google Scholar
• Favaretto F , Milan G , Collin GB , et al. GLUT4 defects in adipose tissue are early signs of metabolic alterations in Alms1GT/GT, a mouse model for obesity and insulin resistance. PLoS One . 2014;9:e109540. doi:10.1371/journal.pone.0109540 25299671
   PubMed Web of Science ®Google Scholar
• Rondinone CM , Wang LM , Lonnroth P , Wesslau C , Pierce JH , Smith U . Insulin receptor substrate (IRS) 1 is reduced and IRS-2 is the main docking protein for phosphatidylinositol 3-kinase in adipocytes from subjects with non-insulin-dependent diabetes mellitus. Proc Natl Acad Sci U S A . 1997;94:4171–4175. doi:10.1073/pnas.94.8.4171 9108124
   PubMed Web of Science ®Google Scholar
• Staubs PA , Nelson JG , Reichart DR , Olefsky JM . Platelet-derived growth factor inhibits insulin stimulation of insulin receptor substrate-1-associated phosphatidylinositol 3-kinase in 3T3-L1 adipocytes without affecting glucose transport. J Biol Chem . 1998;273:25139–25147. doi:10.1074/jbc.273.39.25139 9737973
   PubMed Web of Science ®Google Scholar
• Chiu TT , Sun Y , Koshkina A , Klip A . Rac-1 superactivation triggers insulin-independent glucose transporter 4 (GLUT4) translocation that bypasses signaling defects exerted by c-Jun N-terminal kinase (JNK)- and ceramide-induced insulin resistance. J Biol Chem . 2013;288:17520–17531. doi:10.1074/jbc.M113.467647 23640896
   PubMed Web of Science ®Google Scholar
• Brown MS , Goldstein JL . The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell . 1997;89:331–340. doi:10.1016/s0092-8674(00)80213-5 9150132
   PubMed Web of Science ®Google Scholar
• Jang J , Jung Y , Seo SJ , et al. Berberine activates AMPK to suppress proteolytic processing, nuclear translocation and target DNA binding of SREBP-1c in 3T3-L1 adipocytes. Mol Med Rep . 2017;15:4139–4147. doi:10.3892/mmr.2017.6513 28487951
   PubMed Web of Science ®Google Scholar
• Zhang C , Chen X , Zhu R-M , et al. Endoplasmic reticulum stress is involved in hepatic SREBP-1c activation and lipid accumulation in fructose-fed mice. Toxicol Lett . 2012;212:229–240. doi:10.1016/j.toxlet.2012.06.002 22698815
   PubMed Web of Science ®Google Scholar
• Fang DL , Wan Y , Shen W , et al. Endoplasmic reticulum stress leads to lipid accumulation through upregulation of SREBP-1c in normal hepatic and hepatoma cells. Mol Cell Biochem . 2013;381:127–137. doi:10.1007/s11010-013-1694-7 23703028
   PubMed Web of Science ®Google Scholar
• Ning J , Hong T , Ward A , et al. Constitutive role for IRE1alpha-XBP1 signaling pathway in the insulin-mediated hepatic lipogenic program. Endocrinology . 2011;152:2247–2255. doi:10.1210/en.2010-1036 21447637
   PubMed Web of Science ®Google Scholar
• Kim JB , Spiegelman BM . ADD1/SREBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes Dev . 1996;10:1096–1107. doi:10.1101/gad.10.9.1096 8654925
   PubMed Web of Science ®Google Scholar