Sequestration of fatty acids in triglycerides prevents endoplasmic reticulum stress in an in vitro model of cardiomyocyte lipotoxicity

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 12, 2014, Pages 1648-1655

  Bosma, Madeleen ^a,b   Dapito, Dianne H ^a   Drosatos Tampakaki, Zoi ^a   Huiping Son, Ni ^a   Huang, Li Shin ^a   Kersten, Sander ^b   Drosatos, Konstantinos ^c   Goldberg, Ira J ^a  

^a Division of Preventive Medicine and Nutrition Columbia University College of Physi and Surg ^*  (United States)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; FAT DROPLET; FATTY ACID; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; LIPID; LONG CHAIN FATTY ACID COENZYME A LIGASE; NON ESTERIFIED FREE FATTY ACID; OLEIC ACID; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ACETATE COENZYME A LIGASE; BIOLOGICAL MARKER; PALMITIC ACID DERIVATIVE; PNPLA2 PROTEIN, HUMAN; TRIACYLGLYCEROL LIPASE;

ARTICLE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; LIPID STORAGE; LIPOTOXICITY; PROTEIN PHOSPHORYLATION; UPREGULATION; WESTERN BLOTTING; ADULT; BIOLOGICAL MODEL; DRUG EFFECTS; HEK293 CELL LINE; INTRACELLULAR SPACE; METABOLISM; PATHOLOGY;

ACETATE-COA LIGASE; ADULT; BIOMARKERS; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS; HEK293 CELLS; HUMANS; INTRACELLULAR SPACE; LIPASE; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; PALMITATES; PPAR GAMMA; TRIGLYCERIDES;

EID: 84908530426     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.09.012     Document Type: Article

References (60)

1. G.J. van der Vusse, M. van Bilsen, and J.F. Glatz Cardiac fatty acid uptake and transport in health and disease Cardiovasc. Res. 45 2000 279 293
2. K. Drosatos, K.G. Bharadwaj, A. Lymperopoulos, S. Ikeda, R. Khan, Y. Hu, R. Agarwal, S. Yu, H. Jiang, S.F. Steinberg, W.S. Blaner, W.J. Koch, and I.J. Goldberg Cardiomyocyte lipids impair beta-adrenergic receptor function via PKC activation Am. J. Physiol. Endocrinol. Metab. 300 2011 E489 E499
3. D.J. Chess, and W.C. Stanley Role of diet and fuel overabundance in the development and progression of heart failure Cardiovasc. Res. 79 2008 269 278
4. J.C. Perman, P. Bostrom, M. Lindbom, U. Lidberg, M. StAhlman, D. Hagg, H. Lindskog, M. Scharin Tang, E. Omerovic, L. Mattsson Hulten, A. Jeppsson, P. Petursson, J. Herlitz, G. Olivecrona, D.K. Strickland, K. Ekroos, S.O. Olofsson, and J. Boren The VLDL receptor promotes lipotoxicity and increases mortality in mice following an acute myocardial infarction J. Clin. Invest. 121 2011 2625 2640
5. N.M. Borradaile, and J.E. Schaffer Lipotoxicity in the heart Curr. Hypertens. Rev. 7 2005 412 417
6. K. Terai, Y. Hiramoto, M. Masaki, S. Sugiyama, T. Kuroda, M. Hori, I. Kawase, and H. Hirota AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress Mol. Cell. Biol. 25 2005 9554 9575
7. D.J. Thuerauf, M. Marcinko, N. Gude, M. Rubio, M.A. Sussman, and C.C. Glembotski Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes Circ. Res. 99 2006 275 282
8. K. Okada, T. Minamino, Y. Tsukamoto, Y. Liao, O. Tsukamoto, S. Takashima, A. Hirata, M. Fujita, Y. Nagamachi, T. Nakatani, C. Yutani, K. Ozawa, S. Ogawa, H. Tomoike, M. Hori, and M. Kitakaze Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis Circulation 110 2004 705 712
9. N.M. Borradaile, X. Han, J.D. Harp, S.E. Gale, D.S. Ory, and J.E. Schaffer Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death J. Lipid Res. 47 2006 2726 2737
10. S. Doroudgar, and C.C. Glembotski New concepts of endoplasmic reticulum function in the heart: programmed to conserve J. Mol. Cell. Cardiol. 55 2013 85 91
11. J. Groenendyk, P.K. Sreenivasaiah, D.H. Kim, L.B. Agellon, and M. Michalak Biology of endoplasmic reticulum stress in the heart Circ. Res. 107 2010 1185 1197
12. G.S. Hotamisligil Role of endoplasmic reticulum stress and c-Jun NH2-terminal kinase pathways in inflammation and origin of obesity and diabetes Diabetes 54 2005 S73 S78
13. D.B. Ostrander, G.C. Sparagna, A.A. Amoscato, J.B. McMillin, and W. Dowhan Decreased cardiolipin synthesis corresponds with cytochrome c release in palmitate-induced cardiomyocyte apoptosis J. Biol. Chem. 276 2001 38061 38067
14. N.M. Borradaile, K.K. Buhman, L.L. Listenberger, C.J. Magee, E.T. Morimoto, D.S. Ory, and J.E. Schaffer A critical role for eukaryotic elongation factor 1A-1 in lipotoxic cell death Mol. Biol. Cell 17 2006 770 778
15. T.S. Park, H. Yamashita, W.S. Blaner, and I.J. Goldberg Lipids in the heart: a source of fuel and a source of toxins Curr. Opin. Lipidol. 18 2007 277 282
16. J.E. De Vries, M.M. Vork, T.H. Roemen, Y.F. de Jong, J.P. Cleutjens, G.J. van der Vusse, and M. van Bilsen Saturated but not mono-unsaturated fatty acids induce apoptotic cell death in neonatal rat ventricular myocytes J. Lipid Res. 38 1997 1384 1394
17. D. Dyntar, M. Eppenberger-Eberhardt, K. Maedler, M. Pruschy, H.M. Eppenberger, G.A. Spinas, and M.Y. Donath Glucose and palmitic acid induce degeneration of myofibrils and modulate apoptosis in rat adult cardiomyocytes Diabetes 50 2001 2105 2113
18. L.L. Listenberger, X. Han, S.E. Lewis, S. Cases, R.V. Farese Jr., D.S. Ory, and J.E. Schaffer Triglyceride accumulation protects against fatty acid-induced lipotoxicity Proc. Natl. Acad. Sci. U. S. A. 100 2003 3077 3082
19. L. Liu, X. Shi, K.G. Bharadwaj, S. Ikeda, H. Yamashita, H. Yagyu, J.E. Schaffer, Y.-H. Yu, and I.J. Goldberg DGAT1 expression increases heart triglyceride content but ameliorates lipotoxicity J. Biol. Chem. 284 2009 36312 36323
20. A.C. Aurich, B. Niemann, R. Pan, S. Gruenler, H. Issa, R.E. Silber, and S. Rohrbach Age-dependent effects of high fat-diet on murine left ventricles: role of palmitate Basic Res. Cardiol. 108 2013 369
21. A. Chokshi, K. Drosatos, F.H. Cheema, R. Ji, T. Khawaja, S. Yu, T. Kato, R. Khan, H. Takayama, R. Knoll, H. Milting, C.S. Chung, U. Jorde, Y. Naka, D.M. Mancini, I.J. Goldberg, and P.C. Schulze Ventricular assist device implantation corrects myocardial lipotoxicity, reverses insulin resistance, and normalizes cardiac metabolism in patients with advanced heart failure Circulation 125 2012 2844 2853
22. M.M. Davidson, C. Nesti, L. Palenzuela, W.F. Walker, E. Hernandez, L. Protas, M. Hirano, and N.D. Isaac Novel cell lines derived from adult human ventricular cardiomyocytes J. Mol. Cell. Cardiol. 39 2005 133 147
23. D.S. Straus, and C.K. Glass Anti-inflammatory actions of PPAR ligands: new insights on cellular and molecular mechanisms Trends Immunol. 28 2007 551 558
24. K. Drosatos, D. Sanoudou, K.E. Kypreos, D. Kardassis, and V.I. Zannis A dominant negative form of the transcription factor c-Jun affects genes that have opposing effects on lipid homeostasis in mice J. Biol. Chem. 282 2007 19556 19564
25. T.C. He, S. Zhou, L.T. da Costa, J. Yu, K.W. Kinzler, and B. Vogelstein A simplified system for generating recombinant adenoviruses Proc. Natl. Acad. Sci. U. S. A. 95 1998 2509 2514
26. B.N. Reid, G.P. Ables, O.A. Otlivanchik, G. Schoiswohl, R. Zechner, W.S. Blaner, I.J. Goldberg, R.F. Schwabe, S.C. Chua Jr., and L.S. Huang Hepatic overexpression of hormone-sensitive lipase and adipose triglyceride lipase promotes fatty acid oxidation, stimulates direct release of free fatty acids, and ameliorates steatosis J. Biol. Chem. 283 2008 13087 13099
27. A. Peter, C. Weigert, H. Staiger, F. Machicao, F. Schick, J. Machann, N. Stefan, C. Thamer, H. Häring, and E. Schleicher Individual stearoyl-CoA desaturase 1 expression modulates endoplasmic reticulum stress and inflammation in human myotubes and is associated with skeletal muscle lipid storage and insulin sensitivity in vivo Diabetes 58 2009 1757 1765
28. N.-H. Son, S. Yu, J. Tuinei, K. Arai, H. Hamai, S. Homma, G.I. Shulman, E.D. Abel, and I.J. Goldberg PPARy-induced cardiolipotoxicity in mice is ameliorated by PPARa deficiency despite increases in fatty acid oxidation J. Clin. Invest. 120 2010 3443 3454
29. N.H. Son, T.S. Park, H. Yamashita, M. Yokoyama, L.A. Huggins, K. Okajima, S. Homma, M.J. Szabolcs, L.S. Huang, and I.J. Goldberg Cardiomyocyte expression of PPARgamma leads to cardiac dysfunction in mice J. Clin. Invest. 117 2007 2791 2801
30. M. Wang, and R.J. Kaufman The impact of the endoplasmic reticulum protein-folding environment on cancer development Nat Rev Cancer 14 2014 581 597
31. H.C. Chiu, A. Kovacs, D.A. Ford, F.F. Hsu, R. Garcia, P. Herrero, J.E. Saffitz, and J.E. Schaffer A novel mouse model of lipotoxic cardiomyopathy J. Clin. Invest. 107 2001 813 822
32. R.M. Bell, and R.A. Coleman Enzymes of glycerolipid synthesis in eukaryotes Annu. Rev. Biochem. 49 1980 459 487
33. N. Mayorek, I. Grinstein, and J. Bar-Tana Triacylglycerol synthesis in cultured rat hepatocytes. The rate-limiting role of diacylglycerol acyltransferase Eur. J. Biochem. 182 1989 395 400
34. B.H. Goodpaster, R. Theriault, S.C. Watkins, and D.E. Kelley Intramuscular lipid content is increased in obesity and decreased by weight loss Metabolism 49 2000 467 472
35. D.A. Pan, S. Lillioja, A.D. Kriketos, M.R. Milner, L.A. Baur, C. Bogardus, A.B. Jenkins, and L.H. Storlien Skeletal muscle triglyceride levels are inversely related to insulin action Diabetes 46 1997 983 988
36. S. Sharma, J.V. Adrogue, L. Golfman, I. Uray, J. Lemm, K. Youker, G.P. Noon, O.H. Frazier, and H. Taegtmeyer Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart FASEB J. 18 2004 1692 1700
37. M. Bosma, M.K.C. Hesselink, L.M. Sparks, S. Timmers, M.J. Ferraz, F. Mattijssen, D. van Beurden, G. Schaart, M.H. de Baets, F.K. Verheyen, S. Kersten, and P. Schrauwen Perilipin 2 improves insulin sensitivity in skeletal muscle despite elevated intramuscular lipid levels Diabetes 61 2012 2679 2690
38. S. Schenk, and J.F. Horowitz Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance J. Clin. Invest. 117 2007 1690 1698
39. J.M. Brown, J.L. Betters, C. Lord, Y. Ma, X. Han, K. Yang, H.M. Alger, J. Melchior, J. Sawyer, R. Shah, M.D. Wilson, X. Liu, M.J. Graham, R. Lee, R. Crooke, G.I. Shulman, B. Xue, H. Shi, and L. Yu CGI-58 knockdown in mice causes hepatic steatosis but prevents diet-induced obesity and glucose intolerance J. Lipid Res. 51 2010 3306 3315
40. M. Bosma, S. Kersten, M.K.C. Hesselink, and P. Schrauwen Re-evaluating lipotoxic triggers in skeletal muscle: relating intramyocellular lipid metabolism to insulin sensitivity Prog. Lipid Res. 51 2012 36 49
41. S.A. Summers Ceramides in insulin resistance and lipotoxicity Prog. Lipid Res. 45 2006 42 72
42. D.M. Erion, and G.I. Shulman Diacylglycerol-mediated insulin resistance Nat. Med. 16 2010 400 402
43. L. Liu, S. Yu, R.S. Khan, S. Homma, P.C. Schulze, W.S. Blaner, Y. Yin, and I.J. Goldberg Diacylglycerol acyl transferase 1 overexpression detoxifies cardiac lipids in PPAR transgenic mice J. Lipid Res. 53 2012 1482 1492
44. J.B. Lockridge, M.L. Sailors, D.J. Durgan, O. Egbejimi, W.J. Jeong, M.S. Bray, W.C. Stanley, and M.E. Young Bioinformatic profiling of the transcriptional response of adult rat cardiomyocytes to distinct fatty acids J. Lipid Res. 49 2008 1395 1408
45. Y. Wei, D. Wang, F. Topczewski, and M.J. Pagliassotti Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells Am. J. Physiol. Endocrinol. Metab. 291 2006 E275 E281
46. D.L. Hickson-Bick, L.M. Buja, and J.B. McMillin Palmitate-mediated alterations in the fatty acid metabolism of rat neonatal cardiac myocytes J. Mol. Cell. Cardiol. 32 2000 511 519
47. I.C. Okere, M.P. Chandler, T.A. McElfresh, J.H. Rennison, V. Sharov, H.N. Sabbah, K.Y. Tserng, B.D. Hoit, P. Ernsberger, M.E. Young, and W.C. Stanley Differential effects of saturated and unsaturated fatty acid diets on cardiomyocyte apoptosis, adipose distribution, and serum leptin Am. J. Physiol. Heart Circ. Physiol. 291 2006 H38 H44
48. J.G. Duncan Lipotoxicity: what is the fate of fatty acids? J. Lipid Res. 49 2008 1375 1376
49. T.A. Miller, N.K. LeBrasseur, G.M. Cote, M.P. Trucillo, D.R. Pimentel, Y. Ido, N.B. Ruderman, and D.B. Sawyer Oleate prevents palmitate-induced cytotoxic stress in cardiac myocytes Biochem. Biophys. Res. Commun. 336 2005 309 315
50. D.M. Muoio, T.M. Lewin, P. Wiedmer, and R.A. Coleman Acyl-CoAs are functionally channeled in liver: potential role of acyl-CoA synthetase Am. J. Physiol. Endocrinol. Metab. 279 2000 E1366 E1373
51. I.J. Goldberg, C.M. Trent, and P.C. Schulze Lipid metabolism and toxicity in the heart Cell Metab. 15 2012 805 812
52. Y. Nakachi, K. Yagi, I. Nikaido, H. Bono, M. Tonouchi, C. Schonbach, and Y. Okazaki Identification of novel PPARgamma target genes by integrated analysis of ChIP-on-chip and microarray expression data during adipocyte differentiation Biochem. Biophys. Res. Commun. 372 2008 362 366
53. K. Drosatos, R.S. Khan, C.M. Trent, H. Jiang, N.H. Son, W.S. Blaner, S. Homma, P.C. Schulze, and I.J. Goldberg Peroxisome proliferator-activated receptor-gamma activation prevents sepsis-related cardiac dysfunction and mortality in mice Circ. Heart Fail. 6 2013 550 562
54. J.P. Morrow, A. Katchman, N.H. Son, C.M. Trent, R. Khan, T. Shiomi, H. Huang, V. Amin, J.M. Lader, C. Vasquez, G.E. Morley, J. D'Armiento, S. Homma, I.J. Goldberg, and S.O. Marx Mice with cardiac overexpression of peroxisome proliferator-activated receptor gamma have impaired repolarization and spontaneous fatal ventricular arrhythmias Circulation 124 2011 2812 2821
55. Y. Lee, R.H. Naseem, L. Duplomb, B.H. Park, D.J. Garry, J.A. Richardson, J.E. Schaffer, and R.H. Unger Hyperleptinemia prevents lipotoxic cardiomyopathy in acyl CoA synthase transgenic mice Proc. Natl. Acad. Sci. U. S. A. 101 2004 13624 13629
56. R.K. Vikramadithyan, K. Hirata, H. Yagyu, Y. Hu, A. Augustus, S. Homma, and I.J. Goldberg Peroxisome proliferator-activated receptor agonists modulate heart function in transgenic mice with lipotoxic cardiomyopathy J. Pharmacol. Exp. Ther. 313 2005 586 593
57. V.P. Bilan, E.M. Salah, S. Bastacky, H.B. Jones, R.M. Mayers, B. Zinker, S.M. Poucher, and S.P. Tofovic Diabetic nephropathy and long-term treatment effects of rosiglitazone and enalapril in obese ZSF1 rats J. Endocrinol. 210 2011 293 308
58. T.O. Eichmann, M. Kumari, J.T. Haas, R.V. Farese, R. Zimmermann, A. Lass, and R. Zechner Studies on the substrate and stereo/regioselectivity of adipose triglyceride lipase, hormone-sensitive lipase, and diacylglycerol-O-acyltransferases J. Biol. Chem. 287 2012 41446 41457
59. S.K. Das, S. Eder, S. Schauer, C. Diwoky, H. Temmel, B. Guertl, G. Gorkiewicz, K.P. Tamilarasan, P. Kumari, M. Trauner, R. Zimmermann, P. Vesely, G. Haemmerle, R. Zechner, and G. Hoefler Adipose triglyceride lipase contributes to cancer-associated cachexia Science 333 2011 233 238
60. G. Haemmerle, T. Moustafa, G. Woelkart, S. Buttner, A. Schmidt, T. van de Weijer, M. Hesselink, D. Jaeger, P.C. Kienesberger, K. Zierler, R. Schreiber, T. Eichmann, D. Kolb, P. Kotzbeck, M. Schweiger, M. Kumari, S. Eder, G. Schoiswohl, N. Wongsiriroj, N.M. Pollak, F.P.W. Radner, K. Preiss-Landl, T. Kolbe, T. Rulicke, B. Pieske, M. Trauner, A. Lass, R. Zimmermann, G. Hoefler, S. Cinti, E.E. Kershaw, P. Schrauwen, F. Madeo, B. Mayer, and R. Zechner ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-α and PGC-1 Nat. Med. 17 2011 1076 1085