Cardiac triglyceride accumulation following acute lipid excess occurs through activation of a FoxO1-iNOS-CD36 pathway

Free Radical Biology and Medicine

Volumn 51, Issue 2, 2011, Pages 352-363

  Puthanveetil, Prasanth ^a   Wang, Ying ^a   Zhang, Dahai ^a   Wang, Fang ^a   Kim, Min Suk ^a   Innis, Sheila ^a   Pulinilkunnil, Thomas ^b   Abrahani, Ashraf ^a   Rodrigues, Brian ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cardiac triglycerides; CD36; FoxO1; Free radicals; iNOS; Lipid excess; Saturated fatty acids

Indexed keywords

ALBUMIN; CD36 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTRALIPID; MITOGEN ACTIVATED PROTEIN KINASE P38; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN CDC42; TRANSCRIPTION FACTOR FKHR; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; TYROSINE;

ANIMAL CELL; ARTICLE; CARDIOLIPOTOXICITY; CELL INTERACTION; CELL ISOLATION; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; LIPID STORAGE; LIPOTOXICITY; MOUSE; NITRATION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD36; BLOTTING, WESTERN; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; LIPID METABOLISM; MALE; MYOCARDIUM; NERVE TISSUE PROTEINS; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, WISTAR; TRIGLYCERIDES;

RATTUS;

EID: 79959365710     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.04.009     Document Type: Article

References (63)

1. W. Yang, T. Kelly, and J. He Genetic epidemiology of obesity Epidemiol. Rev. 29 2007 49 61 (Pubitemid 47229640)
2. G.S. Hotamisligil Inflammation and metabolic disorders Nature 444 2006 860 867 (Pubitemid 46024993)
3. J.B. Morris, B. Kenney, H. Huynh, and E.A. Woodcock Regulation of the proapoptotic factor FOXO1 (FKHR) in cardiomyocytes by growth factors and alpha1-adrenergic agonists Endocrinology 146 2005 4370 4376 (Pubitemid 41324033)
4. H.J. Evans-Anderson, C.M. Alfieri, and K.E. Yutzey Regulation of cardiomyocyte proliferation and myocardial growth during development by FOXO transcription factors Circ. Res. 102 2008 686 694 (Pubitemid 351457856)
5. H. Huang, and D.J. Tindall Dynamic FoxO transcription factors J. Cell Sci. 120 2007 2479 2487 (Pubitemid 47323857)
6. D.A. Glauser, and W. Schlegel The emerging role of FOXO transcription factors in pancreatic beta cells J. Endocrinol. 193 2007 195 207
7. S. Asada, H. Daitoku, H. Matsuzaki, T. Saito, T. Sudo, H. Mukai, S. Iwashita, K. Kako, T. Kishi, Y. Kasuya, and A. Fukamizu Mitogen-activated protein kinases, Erk and p38, phosphorylate and regulate Foxo1 Cell Signalling 19 2007 519 527 (Pubitemid 46107803)
8. B. Shen, L. Chao, and J. Chao Pivotal role of JNK-dependent FOXO1 activation in downregulation of kallistatin expression by oxidative stress Am. J. Physiol. Heart Circ. Physiol. 298 2010 H1048 H1054
9. W. Bi, L. Xiao, Y. Jia, J. Wu, Q. Xie, J. Ren, G. Ji, and Z. Yuan c-Jun N-terminal kinase enhances MST1-mediated pro-apoptotic signaling through phosphorylation at serine 82 J. Biol. Chem. 285 2010 6259 6264
10. T. Hosaka, W.H. Biggs III, D. Tieu, A.D. Boyer, N.M. Varki, W.K. Cavenee, and K.C. Arden Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification Proc. Natl. Acad. Sci. U S A 101 2004 2975 2980 (Pubitemid 38327721)
11. Y.G. Ni, K. Berenji, N. Wang, M. Oh, N. Sachan, A. Dey, J. Cheng, G. Lu, D.J. Morris, D.H. Castrillon, R.D. Gerard, B.A. Rothermel, and J.A. Hill Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling Circulation 114 2006 1159 1168 (Pubitemid 44386480)
12. K.C. Arden FoxO: linking new signaling pathways Mol. Cell 14 2004 416 418 (Pubitemid 38648793)
13. E.W. Lam, R.E. Francis, and M. Petkovic FOXO transcription factors: key regulators of cell fate Biochem. Soc. Trans. 34 2006 722 726 (Pubitemid 44796405)
14. P. Puthanveetil, Y. Wang, F. Wang, M.S. Kim, A. Abrahani, and B. Rodrigues The increase in cardiac pyruvate dehydrogenase kinase-4 after short-term dexamethasone is controlled by an Akt-p38-forkhead box other factor-1 signaling axis Endocrinology 151 2010 2306 2318
15. M. Kuo, V. Zilberfarb, N. Gangneux, N. Christeff, and T. Issad O-glycosylation of FoxO1 increases its transcriptional activity towards the glucose 6-phosphatase gene FEBS Lett. 582 2008 829 834
16. J.M. Park, T.H. Kim, J.S. Bae, M.Y. Kim, K.S. Kim, and Y.H. Ahn Role of resveratrol in FOXO1-mediated gluconeogenic gene expression in the liver Biochem. Biophys. Res. Commun. 403 2010 329 334
17. Y.I. Kim, F.N. Lee, W.S. Choi, S. Lee, and J.H. Youn Insulin regulation of skeletal muscle PDK4 mRNA expression is impaired in acute insulin-resistant states Diabetes 55 2006 2311 2317 (Pubitemid 44743629)
18. H.S. Kwon, B. Huang, T.G. Unterman, and R.A. Harris Protein kinase B-alpha inhibits human pyruvate dehydrogenase kinase-4 gene induction by dexamethasone through inactivation of FOXO transcription factors Diabetes 53 2004 899 910 (Pubitemid 38436601)
19. C.C. Bastie, Z. Nahle, T. McLoughlin, K. Esser, W. Zhang, T. Unterman, and N.A. Abumrad FoxO1 stimulates fatty acid uptake and oxidation in muscle cells through CD36-dependent and -independent mechanisms J. Biol. Chem. 280 2005 14222 14229 (Pubitemid 40517324)
20. C. Christoffersen, E. Bollano, M.L. Lindegaard, E.D. Bartels, J.P. Goetze, C.B. Andersen, and L.B. Nielsen Cardiac lipid accumulation associated with diastolic dysfunction in obese mice Endocrinology 144 2003 3483 3490 (Pubitemid 36904426)
21. D. An, G. Kewalramani, J.K. Chan, D. Qi, S. Ghosh, T. Pulinilkunnil, A. Abrahani, S.M. Innis, and B. Rodrigues Metformin influences cardiomyocyte cell death by pathways that are dependent and independent of caspase-3 Diabetologia 49 2006 2174 2184 (Pubitemid 44168486)
22. M.S. Kim, F. Wang, P. Puthanveetil, G. Kewalramani, S. Innis, L. Marzban, S.F. Steinberg, T.D. Webber, T.J. Kieffer, A. Abrahani, and B. Rodrigues Cleavage of protein kinase D after acute hypoinsulinemia prevents excessive lipoprotein lipase-mediated cardiac triglyceride accumulation Diabetes 58 2009 2464 2475
23. C. Ballard-Croft, A.C. Locklar, B.J. Keith, R.M. Mentzer Jr., and R.D. Lasley Oxidative stress and adenosine A1 receptor activation differentially modulate subcellular cardiomyocyte MAPKs Am. J. Physiol. Heart Circ. Physiol. 294 2008 H263 H271
24. M.S. Kim, G. Kewalramani, P. Puthanveetil, V. Lee, U. Kumar, D. An, A. Abrahani, and B. Rodrigues Acute diabetes moderates trafficking of cardiac lipoprotein lipase through p38 mitogen-activated protein kinase-dependent actin cytoskeleton organization Diabetes 57 2008 64 76
25. D.W. Powell, M.J. Rane, B.A. Joughin, R. Kalmukova, J.H. Hong, B. Tidor, W.L. Dean, W.M. Pierce, J.B. Klein, M.B. Yaffe, and K.R. McLeish Proteomic identification of 14-3-3zeta as a mitogen-activated protein kinase-activated protein kinase 2 substrate: role in dimer formation and ligand binding Mol. Cell. Biol. 23 2003 5376 5387 (Pubitemid 36950892)
26. V. Obsilova, J. Silhan, E. Boura, J. Teisinger, and T. Obsil 14-3-3 proteins: a family of versatile molecular regulators Physiol. Res. 57 Suppl. 3 2008 S11 S21
27. T. Obsil, and V. Obsilova Structure/function relationships underlying regulation of FOXO transcription factors Oncogene 27 2008 2263 2275 (Pubitemid 351501778)
28. J. Tanaka, L. Qiang, A.S. Banks, C.L. Welch, M. Matsumoto, T. Kitamura, Y. Ido-Kitamura, R.A. DePinho, and D. Accili Foxo1 links hyperglycemia to LDL oxidation and endothelial nitric oxide synthase dysfunction in vascular endothelial cells Diabetes 58 2009 2344 2354
29. A. Musch, D. Cohen, G. Kreitzer, and E. Rodriguez-Boulan cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network EMBO J. 20 2001 2171 2179 (Pubitemid 32410587)
30. T. Koeck, B. Willard, J.W. Crabb, M. Kinter, D.J. Stuehr, and K.S. Aulak Glucose-mediated tyrosine nitration in adipocytes: targets and consequences Free Radic. Biol. Med. 46 2009 884 892
31. J. Zhou, N. Dehne, and B. Brune Nitric oxide causes macrophage migration via the HIF-1-stimulated small GTPases Cdc42 and Rac1 Free Radic. Biol. Med. 47 2009 741 749
32. W. Fan, H. Morinaga, J.J. Kim, E. Bae, N.J. Spann, S. Heinz, C.K. Glass, and J.M. Olefsky FoxO1 regulates Tlr4 inflammatory pathway signalling in macrophages EMBO J. 29 2010 4223 4236
33. K.S. Ahn, and B.B. Aggarwal Transcription factor NF-kappaB: a sensor for smoke and stress signals Ann. N.Y. Acad. Sci. 1056 2005 218 233 (Pubitemid 43030980)
34. M. Yang, J. Wu, C.M. Martin, P.R. Kvietys, and T. Rui Important role of p38 MAP kinase/NF-kappaB signaling pathway in the sepsis-induced conversion of cardiac myocytes to a proinflammatory phenotype Am. J. Physiol. Heart Circ. Physiol. 294 2008 H994 H1001
35. D. An, and B. Rodrigues Role of changes in cardiac metabolism in development of diabetic cardiomyopathy Am. J. Physiol. Heart Circ. Physiol. 291 2006 H1489 H1506
36. V.K. Mootha, C.M. Lindgren, K.F. Eriksson, A. Subramanian, S. Sihag, J. Lehar, P. Puigserver, E. Carlsson, M. Ridderstrale, E. Laurila, N. Houstis, M.J. Daly, N. Patterson, J.P. Mesirov, T.R. Golub, P. Tamayo, B. Spiegelman, E.S. Lander, J.N. Hirschhorn, D. Altshuler, and L.C. Groop PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes Nat. Genet. 34 2003 267 273 (Pubitemid 36792858)
37. S. Nemoto, M.M. Fergusson, and T. Finkel SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1α J. Biol. Chem. 280 2005 16456 16460 (Pubitemid 40616776)
38. E.H. Jeninga, K. Schoonjans, and J. Auwerx Reversible acetylation of PGC-1: connecting energy sensors and effectors to guarantee metabolic flexibility Oncogene 29 2010 4617 4624
39. A.R. Wende, and E.D. Abel Lipotoxicity in the heart Biochim. Biophys. Acta 1801 2010 311 319
40. C.C. Bastie, T. Hajri, V.A. Drover, P.A. Grimaldi, and N.A. Abumrad CD36 in myocytes channels fatty acids to a lipase-accessible triglyceride pool that is related to cell lipid and insulin responsiveness Diabetes 53 2004 2209 2216 (Pubitemid 39145573)
41. M. Febbraio, D.P. Hajjar, and R.L. Silverstein CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism J. Clin. Invest. 108 2001 785 791 (Pubitemid 32880285)
42. M. Febbraio, and R.L. Silverstein CD36: implications in cardiovascular disease Int. J. Biochem. Cell Biol. 39 2007 2012 2030 (Pubitemid 47376825)
43. A.N. Carley, and D.L. Severson What are the biochemical mechanisms responsible for enhanced fatty acid utilization by perfused hearts from type 2 diabetic db/db mice? Cardiovasc. Drugs Ther. 22 2008 83 89
44. Z. Nahle, M. Hsieh, T. Pietka, C.T. Coburn, P.A. Grimaldi, M.Q. Zhang, D. Das, and N.A. Abumrad CD36-dependent regulation of muscle FoxO1 and PDK4 in the PPAR delta/beta-mediated adaptation to metabolic stress J. Biol. Chem. 283 2008 14317 14326
45. Y. Behl, P. Krothapalli, T. Desta, S. Roy, and D.T. Graves FOXO1 plays an important role in enhanced microvascular cell apoptosis and microvascular cell loss in type 1 and type 2 diabetic rats Diabetes 58 2009 917 925
46. J.J. Kim, P. Li, J. Huntley, J.P. Chang, K.C. Arden, and J.M. Olefsky FoxO1 haploinsufficiency protects against high-fat diet-induced insulin resistance with enhanced peroxisome proliferator-activated receptor gamma activation in adipose tissue Diabetes 58 2009 1275 1282
47. S.C. Martinez, K. Tanabe, C. Cras-Meneur, N.A. Abumrad, E. Bernal-Mizrachi, and M.A. Permutt Inhibition of Foxo1 protects pancreatic islet beta-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis Diabetes 57 2008 846 859
48. S. Umar, and A. van der Laarse Nitric oxide and nitric oxide synthase isoforms in the normal, hypertrophic, and failing heart Mol. Cell. Biochem. 333 2010 191 201
49. J.H. Lipschutz, and K.E. Mostov Exocytosis: the many masters of the exocyst Curr. Biol. 12 2002 R212 R214
50. D.M. Nikolic, M.C. Gong, J. Turk, and S.R. Post Class A scavenger receptor-mediated macrophage adhesion requires coupling of calcium-independent phospholipase A(2) and 12/15-lipoxygenase to Rac and Cdc42 activation J. Biol. Chem. 282 2007 33405 33411 (Pubitemid 350159552)
51. K. Tsukamoto, K. Hirano, S. Yamashita, N. Sakai, C. Ikegami, Z. Zhang, F. Matsuura, H. Hiraoka, A. Matsuyama, M. Ishigami, and Y. Matsuzawa Retarded intracellular lipid transport associated with reduced expression of Cdc42, a member of Rho-GTPases, in human aged skin fibroblasts: a possible function of Cdc42 in mediating intracellular lipid transport Arterioscler. Thromb. Vasc. Biol. 22 2002 1899 1904 (Pubitemid 35315779)
52. C.L. Morin, R.H. Eckel, T. Marcel, and M.J. Pagliassotti High fat diets elevate adipose tissue-derived tumor necrosis factor-alpha activity Endocrinology 138 1997 4665 4671 (Pubitemid 27460901)
53. K. Chakir, S.K. Daya, R.S. Tunin, R.H. Helm, M.J. Byrne, V.L. Dimaano, A.C. Lardo, T.P. Abraham, G.F. Tomaselli, and D.A. Kass Reversal of global apoptosis and regional stress kinase activation by cardiac resynchronization Circulation 117 2008 1369 1377 (Pubitemid 351501490)
54. R.A. Kayal, M. Siqueira, J. Alblowi, J. McLean, N. Krothapalli, D. Faibish, T.A. Einhorn, L.C. Gerstenfeld, and D.T. Graves TNF-alpha mediates diabetes-enhanced chondrocyte apoptosis during fracture healing and stimulates chondrocyte apoptosis through FOXO1 J. Bone Miner. Res. 25 2010 1604 1615
55. W. Song, X. Lu, and Q. Feng Tumor necrosis factor-alpha induces apoptosis via inducible nitric oxide synthase in neonatal mouse cardiomyocytes Cardiovasc. Res. 45 2000 595 602 (Pubitemid 30047126)
56. M. Seddon, Y.H. Looi, and A.M. Shah Oxidative stress and redox signalling in cardiac hypertrophy and heart failure Heart 93 2007 903 907 (Pubitemid 47122034)
57. C.C. Hsieh, and J. Papaconstantinou Thioredoxin-ASK1 complex levels regulate ROS-mediated p38 MAPK pathway activity in livers of aged and long-lived Snell dwarf mice FASEB J. 20 2006 259 268 (Pubitemid 44933173)
58. J.E. Ricci, N. Waterhouse, and D.R. Green Mitochondrial functions during cell death, a complex (I-V) dilemma Cell Death Differ. 10 2003 488 492 (Pubitemid 36656637)
59. H. Wiseman, and B. Halliwell Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer Biochem. J. 313 Pt 1 1996 17 29 (Pubitemid 26013419)
60. P.J. White, A. Charbonneau, G.J. Cooney, and A. Marette Nitrosative modifications of protein and lipid signaling molecules by reactive nitrogen species Am. J. Physiol. Endocrinol. Metab. 299 2010 E868 E878
61. J.J. Luiken, F.G. Schaap, F.A. van Nieuwenhoven, G.J. van der Vusse, A. Bonen, and J.F. Glatz Cellular fatty acid transport in heart and skeletal muscle as facilitated by proteins Lipids 34 Suppl 1999 S169 S175
62. B. Binas Heart and liver fatty acid binding proteins and the metabolic syndrome Curr. Hypertens. Rep. 7 2005 401 406 (Pubitemid 43136934)
63. R.E. Gimeno, A.M. Ortegon, S. Patel, S. Punreddy, P. Ge, Y. Sun, H.F. Lodish, and A. Stahl Characterization of a heart-specific fatty acid transport protein J. Biol. Chem. 278 2003 16039 16044 (Pubitemid 36799724)