Cardiac expression of microsomal triglyceride transfer protein is increased in obesity and serves to attenuate cardiac triglyceride accumulation

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  Bartels, Emil D ^a   Nielsen, Jan M ^b   Hellgren, Lars I ^c   Ploug, Thorkil ^d   Nielsen, Lars B ^a,d  

^a International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; FATTY ACID; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; CARRIER PROTEIN; INSULIN; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; GENE OVEREXPRESSION; HEART FUNCTION; HEART PROTECTION; INSULIN SENSITIVITY; LIPID DIET; LIPID METABOLISM; LIPID STORAGE; MALE; MOUSE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; TRANSGENE; UPREGULATION; ANIMAL; C57BL MOUSE; GENETICS; HEART MUSCLE; HUMAN; METABOLISM; MOUSE MUTANT; MOUSE STRAIN; TRANSGENIC MOUSE;

MUS;

ANIMALS; APOLIPOPROTEINS B; CARRIER PROTEINS; HUMANS; INSULIN; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, OBESE; MICE, TRANSGENIC; MYOCARDIUM; OBESITY; TRIGLYCERIDES;

EID: 65449137930     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005300     Document Type: Article

References (61)

1. Kenchaiah S, Evans JC, Levy D, Wilson PW, Benjamin EJ, et al. (2002) Obesity and the risk of heart failure. N Engl J Med 347: 305-313.
2. Ford ES, Ajani UA, Croft JB, Critchley JA, Labarthe DR, et al. (2007) Explaining the decrease in U.S. deaths from coronary disease, 1980-2000. N Engl J Med 356: 2388-2398.
3. McGavock JM, Lingvay I, Zib I, Tillery T, Salas N, et al. (2007) Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 116: 1170-1175.
4. Szczepaniak LS, Dobbins RL, Metzger GJ, Sartoni-D'Ambrosia G, Arbique D, et al. (2003) Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magn Reson Med 49: 417-423.
5. Christoffersen C, Bollano E, Lindegaard ML, Bartels ED, Goetze JP, et al. (2003) Cardiac lipid accumulation associated with diastolic dysfunction in obese mice. Endocrinology 144: 3483-3490.
6. Zhou YT, Grayburn P, Karim A, Shimabukuro M, Higa M, et al. (2000) Lipotoxic heart disease in obese rats: implications for human obesity. Proc Natl Acad Sci U S A 97: 1784-1789.
7. Lee Y, Naseem RH, Duplomb L, Park BH, Garry DJ, et al. (2004) Hyperleptinemia prevents lipotoxic cardiomyopathy in acyl CoA synthase transgenic mice. Proc Natl Acad Sci U S A 101: 13624-13629.
8. Lopaschuk GD, Folmes CD, Stanley WC (2007) Cardiac energy metabolism in obesity. Circ Res 101: 335-347.
9. Szczepaniak LS, Victor RG, Orci L, Unger RH (2007) Forgotten but not gone: the rediscovery of fatty heart, the most common unrecognized disease in America. Circ Res 101: 759-767.
10. Stanley WC, Chandler MP (2002) Energy metabolism in the normal and failing heart: potential for therapeutic interventions. Heart Fail Rev 7: 115-130.
11. Unger RH (2003) Minireview: weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology 144: 5159-5165.
12. Stanley WC, Recchia FA, Lopaschuk GD (2005) Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 85: 1093-1129.
13. Somoza B, Guzman R, Cano V, Merino B, Ramos P, et al. (2007) Induction of cardiac uncoupling protein-2 expression and adenosine 5′-monophosphate-activated protein kinase phosphorylation during early states of diet-induced obesity in mice. Endocrinology 148: 924-931.
14. Bamba V, Rader DJ (2007) Obesity and atherogenic dyslipidemia. Gastroenterology 132: 2181-2190.
15. Koutsari C, Jensen MD (2006) Thematic review series: patient-oriented research. Free fatty acid metabolism in human obesity. J Lipid Res 47: 1643-1650.
16. Hammer S, van der Meer RW, Lamb HJ, Schar M, de RA, et al. (2008) Progressive caloric restriction induces dose-dependent changes in myocardial triglyceride content and diastolic function in healthy men. J Clin Endocrinol Metab 93: 497-503.
17. Wisneski JA, Gertz EW, Neese RA, Mayr M (1987) Myocardial metabolism of free fatty acids. Studies with 14C-labeled substrates in humans. J Clin Invest 79: 359-366.
18. Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, et al. (2003) Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest 111: 419-426.
19. Chiu HC, Kovacs A, Blanton RM, Han X, Courtois M, et al. (2005) Transgenic expression of fatty acid transport protein 1 in the heart causes lipotoxic cardiomyopathy. Circ Res 96: 225-233.
20. Finck BN, Lehman JJ, Leone TC, Welch MJ, Bennett MJ, et al. (2002) The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J Clin Invest 109: 121-130.
21. Chiu HC, Kovacs A, Ford DA, Hsu FF, Garcia R, et al. (2001) A novel mouse model of lipotoxic cardiomyopathy. J Clin Invest 107: 813-822.
22. Kurtz DM, Rinaldo P, Rhead WJ, Tian L, Millington DS, et al. (1998) Targeted disruption of mouse long-chain acyl-CoA dehydrogenase gene reveals crucial roles for fatty acid oxidation. Proc Natl Acad Sci U S A 95: 15592-15597.
23. Wilson CR, Tran MK, Salazar KL, Young ME, Taegtmeyer H (2007) Western diet, but not high fat diet, causes derangements of fatty acid metabolism and contractile dysfunction in the heart of Wistar rats. Biochem J 406: 457-467.
24. Saddik M, Lopaschuk GD (1991) Myocardial triglyceride turnover and contribution to energy substrate utilization in isolated working rat hearts. J Biol Chem 266: 8162-8170.
25. Strawford A, Antelo F, Christiansen M, Hellerstein MK (2004) Adipose tissue triglyceride turnover, de novo lipogenesis, and cell proliferation in humans measured with 2H2O. Am J Physiol Endocrinol Metab 286: E577-E588.
26. Nielsen LB, Veniant M, Boren J, Raabe M, Wong JS, et al. (1998) Genes for apolipoprotein B and microsomal triglyceride transfer protein are expressed in the heart: evidence that the heart has the capacity to synthesize and secrete lipoproteins. Circulation 98: 13-16.
27. Adiels M, Boren J, Caslake MJ, Stewart P, Soro A, et al. (2005) Overproduction of VLDL1 driven by hyperglycemia is a dominant feature of diabetic dyslipidemia. Arterioscler Thromb Vasc Biol 25: 1697-1703.
28. Mohler PJ, Zhu MY, Blade AM, Ham AJ, Shelness GS, et al. (2007) Identification of a novel isoform of microsomal triglyceride transfer protein. J Biol Chem 282: 26981-26988.
29. Dougan SK, Rava P, Hussain MM, Blumberg RS (2007) MTP regulated by an alternate promoter is essential for NKT cell development. J Exp Med 204: 533-545.
30. Boren J, Veniant MM, Young SG (1998) Apo B100-containing lipoproteins are secreted by the heart. J Clin Invest 101: 1197-1202.
31. Nielsen LB, Bartels ED, Bollano E (2002) Overexpression of apolipoprotein B in the heart impedes cardiac triglyceride accumulation and development of cardiac dysfunction in diabetic mice. J Biol Chem 277: 27014-27020.
32. Yokoyama M, Yagyu H, Hu Y, Seo T, Hirata K, et al. (2004) Apolipoprotein B production reduces lipotoxic cardiomyopathy: studies in heart-specific lipoprotein lipase transgenic mouse. J Biol Chem 279: 4204-4211.
33. Bjorkegren J, Veniant M, Kim SK, Withycombe SK, Wood PA, et al. (2001) Lipoprotein secretion and triglyceride stores in the heart. J Biol Chem 276: 38511-38517.
34. Raabe M, Veniant MM, Sullivan MA, Zlot CH, Bjorkegren J, et al. (1999) Analysis of the role of microsomal triglyceride transfer protein in the liver of tissue-specific knockout mice. J Clin Invest 103: 1287-1298.
35. Park SY, Cho YR, Kim HJ, Higashimori T, Danton C, et al. (2005) Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes 54: 3530-3540.
36. Petersen S, Russ M, Reinauer H, Eckel J (1991) Inverse regulation of glucose transporter Glut4 and G-protein Gs mRNA expression in cardiac myocytes from insulin resistant rats. FEBS Lett 286: 1-5.
37. Chess DJ, Stanley WC (2008) Role of diet and fuel overabundance in the development and progression of heart failure. Cardiovasc Res 79: 269-278.
38. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, et al. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461.
39. Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7: 1013-1030.
40. Hollander MC, Sheikh MS, Yu K, Zhan Q, Iglesias M, et al. (2001) Activation of Gadd34 by diverse apoptotic signals and suppression of its growth inhibitory effects by apoptotic inhibitors. Int J Cancer 96: 22-31.
41. Gordon DA, Jamil H, Sharp D, Mullaney D, Yao Z, et al. (1994) Secretion of apolipoprotein B-containing lipoproteins from HeLa cells is dependent on expression of the microsomal triglyceride transfer protein and is regulated by lipid availability. Proc Natl Acad Sci U S A 91: 7628-7632.
42. Raabe M, Flynn LM, Zlot CH, Wong JS, Veniant MM, et al. (1998) Knockout of the abetalipoproteinemia gene in mice: reduced lipoprotein secretion in heterozygotes and embryonic lethality in homozygotes. Proc Natl Acad Sci U S A 95: 8686-8691.
43. Ledmyr H, McMahon AD, Ehrenborg E, Nielsen LB, Neville M, et al. (2004) The microsomal triglyceride transfer protein gene-493T variant lowers cholesterol but increases the risk of coronary heart disease. Circulation 109: 2279-2284.
44. Jacob S, Machann J, Rett K, Brechtel K, Volk A, et al. (1999) Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes 48: 1113-1119.
45. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, et al. (2007) Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56: 2085-2092.
46. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, et al. (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7: 45-56.
47. Mazumder PK, O'Neill BT, Roberts MW, Buchanan J, Yun UJ, et al. (2004) Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes 53: 2366-2374.
48. Peterson LR, Herrero P, Schechtman KB, Racette SB, Waggoner AD (2004) Effect of obesity and insulin resistance on myocardial substrate metabolism and efficiency in young women. Circulation 109: 2191-2196.
49. Park TS, Hu Y, Noh HL, Drosatos K, Okajima K, et al. (2008) Ceramide is a cardiotoxin in lipotoxic cardiomyopathy. J Lipid Res 49: 2101-2112.
50. Ye G, Metreveli NS, Ren J, Epstein PN (2003) Metallothionein prevents diabetes-induced deficits in cardiomyocytes by inhibiting reactive oxygen species production. Diabetes 52: 777-783.
51. Finck BN, Han X, Courtois M, Aimond F, Nerbonne JM, et al. (2003) A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc Natl Acad Sci U S A 100: 1226-1231.
52. Buchanan J, Mazumder PK, Hu P, Chakrabarti G, Roberts MW, et al. (2005) Reduced cardiac efficiency and altered substrate metabolism precedes the onset of hyperglycemia and contractile dysfunction in two mouse models of insulin resistance and obesity. Endocrinology 146: 5341-5349.
53. Yang J, Sambandam N, Han X, Gross RW, Courtois M, et al. (2007) CD36 deficiency rescues lipotoxic cardiomyopathy. Circ Res 100: 1208-1217.
54. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, et al. (1998) A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 2: 559-569.
55. Bartels ED, Bang CA, Nielsen LB (2009) Early atherosclerosis and vascular inflammation in mice with diet-induced type 2 diabetes. Eur J Clin Invest 39: 190-199.
56. Pedersen TX, Bro S, Andersen MH, Etzerodt M, Jauhiainen M, et al. (2009) Effect of treatment with human apolipoprotein A-I on atherosclerosis in uremic apolipoprotein-E deficient mice. Atherosclerosis 202: 372-381.
57. Bang CA, Bro S, Bartels ED, Pedersen TX, Nielsen LB (2007) Effect of uremia on HDL composition, vascular inflammation, and atherosclerosis in wild-type mice. Am J Physiol Renal Physiol 293: F1325-F1331.
58. Lindegaard ML, Nielsen LB (2008) Maternal diabetes causes coordinated down-regulation of genes involved with lipid metabolism in the murine fetal heart. Metabolism 57: 766-773.
59. Georgakopoulos D, Mitzner WA, Chen CH, Byrne BJ, Millar HD, et al. (1998) In vivo murine left ventricular pressure-volume relations by miniaturized conductance micromanometry. Am J Physiol 274: H1416-H1422.
60. Nielsen JM, Kristiansen SB, Ringgaard S, Nielsen TT, Flyvbjerg A, et al. (2007) Left ventricular volume measurement in mice by conductance catheter: evaluation and optimization of calibration. Am J Physiol Heart Circ Physiol 293: H534-H540.
61. Bartels ED, Lauritsen M, Nielsen LB (2002) Hepatic expression of microsomal triglyceride transfer protein and in vivo secretion of triglyceride-rich lipoproteins are increased in obese diabetic mice. Diabetes 51: 1233-1239.