A murine model of isolated cardiac steatosis leads to cardiomyopathy

Hypertension

Volumn 57, Issue 2, 2011, Pages 216-222

  Glenn, Denis J ^a,b   Wang, Feng ^a   Nishimoto, Minobu ^a   Cruz, Michelle C ^a   Uchida, Yoshikazu ^c   Holleran, Walter M ^c   Zhang, Yan ^c   Yeghiazarians, Yerem ^c   Gardner, David G ^a  

^a Diabetes Center   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cardiac fibrosis; cardiomyopathy; diacylglycerol acyltransferase; lipotoxicity; mitochondrial biogenesis

Indexed keywords

CYTOCHROME C; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 1; DIACYLGLYCEROL ACYLTRANSFERASE 1; GELATINASE A; GLUCOSE; INSULIN; PROCOLLAGEN; PROCOLLAGEN TYPE 1A; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOGENESIS; BODY WEIGHT; CARDIAC STEATOSIS; CARDIOMYOPATHY; CONTROLLED STUDY; DECELERATION; DIASTOLIC DYSFUNCTION; DISEASE COURSE; DYSLIPIDEMIA; ECHOCARDIOGRAPHY; FEMALE; GLUCOSE HOMEOSTASIS; HEART DISEASE; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HISTOLOGY; HYPERGLYCEMIA; HYPOTHESIS; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIPID STORAGE; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEATOSIS; SYSTOLIC DYSFUNCTION; TRANSGENIC MOUSE; VELOCITY;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CARDIOMYOPATHIES; CELLS, CULTURED; CYTOCHROMES C; DIACYLGLYCEROL O-ACYLTRANSFERASE; DISEASE MODELS, ANIMAL; FATTY ACIDS; FEMALE; FIBROSIS; GENE EXPRESSION; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; MITOCHONDRIA; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; TRIGLYCERIDES;

EID: 79551498811     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.110.160655     Document Type: Article

References (54)

1. Kenchaiah S, Evans JC, Levy D, Wilson PW, Benjamin EJ, Larson MG, Kannel WB, Vasan RS. Obesity and the risk of heart failure. N Engl J Med. 2002;347:305-313.
2. Sharma S, Adrogue JV, Golfman L, Uray I, Lemm J, Youker K, Noon GP, Frazier OH, Taegtmeyer H. Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. FASEB J. 2004;18: 1692-1700.
3. McGavock JM, Victor RG, Unger RH, Szczepaniak LS. Adiposity of the heart, revisited. Ann Intern Med. 2006;144:517-524.
4. Brindley DN, Kok BPC, Kienesberger PC, Lehner R, Dyck JRB. Shedding light on the enigma of myocardial lipotoxicity: the involvement of known and putative regulators of fatty acid storage and mobilization. Am J Physiol Endocrinol Metab. 2010;298:E897-E908.
5. Unger RH. Lipotoxic diseases. Annu Rev Med. 2002;53:319-336.
6. Listenberger LL, Schaffer JE. Mechanisms of lipoapoptosis: implications for human heart disease. Trends Cardiovasc Med. 2002;12:134-138.
7. Ouwens DM, Boer C, Fodor M, de Galan P, Heine RJ, Maassen JA, Diamant M. Cardiac dysfunction induced by high-fat diet is associated with altered myocardial insulin signalling in rats. Diabetologia. 2005;48:1229-1237.
8. Thakker GD, Frangogiannis NG, Bujak M, Zymek P, Gaubatz JW, Reddy AK, Taffet G, Michael LH, Entman ML, Ballantyne CM. Effects of diet-induced obesity on inflammation and remodeling after myocardial infarction. Am J Physiol Heart Circ Physiol. 2006;291:H2504-H2514.
9. Christoffersen C, Bollano E, Lindegaard MLS, Bartels ED, Goetze JP, Andersen CB, Nielsen LB. Cardiac lipid accumulation associated with dia-stolic dysfunction in obese mice. Endocrinology. 2003;144:3483-3490.
10. Buchanan J, Mazumder PK, Hu P, Chakrabarti G, Roberts MW, Yun UJ, Cooksey RC, Litwin SE, Abel ED. 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. 2005;146:5341-5349.
11. Zhou Y-T, Grayburn P, Karim A, Shimabukuro M, Higa M, Baetens D, Orci L, Unger RH. Lipotoxic heart disease in obese rats: implications for human obesity. Proc Natl Acad Sci USA. 2000;97:1784-1789.
12. Chiu HC, Kovacs A, Ford DA, Hsu FF, Garcia R, Herrero P, Saffitz JE, Schaffer JE. A novel mouse model of lipotoxic cardiomyopathy. J Clin Invest. 2001;107:813-822.
13. Chiu HC, Kovacs A, Blanton RM, Han X, Courtois M, Weinheimer CJ, Yamada KA, Brunet S, Xu H, Nerbonne JM, Welch MJ, Fettig NM, Sharp TL, Sambandam N, Olson KM, Ory DS, Schaffer JE. Transgenic expression of fatty acid transport protein 1 in the heart causes lipotoxic cardiomyopathy. Circ Res. 2005;96:225-233.
14. Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, Kako Y, Seo T, Hu Y, Lutz EP, Merkel M, Bensadoun A, Homma S, Goldberg IJ. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest. 2003;111:419-426.
15. Haemmerle G, Lass A, Zimmermann R, Gorkiewicz G, Meyer C, Rozman J, Heldmaier G, Maier R, Theussl C, Eder S, Kratky D, Wagner EF, Klingenspor M, Hoefler G, Zechner R. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science. 2006;312:734-737.
16. Abel ED, Litwin SE, Sweeney G. Cardiac remodeling in obesity. Physiol Rev. 2008;88:389-419.
17. Cases S, Smith SJ, Zheng YW, Myers HM, Lear SR, Sande E, Novak S, Collins C, Welch CB, Lusis AJ, Erickson SK, Farese RV Jr. Identification of a gene encoding an acyl CoA:diacylglycerol acyltransferase, a key enzyme in triacylglycerol synthesis. Proc Natl Acad Sci USA. 1998;95:13018-13023.
18. Buhman KK, Smith SJ, Stone SJ, Repa JJ, Wong JS, Knapp FF Jr, Burri BJ, Hamilton RL, Abumrad NA, Farese RV Jr. DGAT1 is not essential for intestinal triacylglycerol absorption or chylomicron synthesis. J Biol Chem. 2002;277:25474-25479.
19. Cases S, Stone SJ, Zhou P, Yen E, Tow B, Lardizabal KD, Voelker T, Farese RV Jr. Cloning of DGAT2, a second mammalian diacylglycerol acyltransferase, and related family members. J Biol Chem. 2001;276: 38870-38876.
20. Chen HC, Smith SJ, Ladha Z, Jensen DR, Ferreira LD, Pulawa LK, McGuire JG, Pitas RE, Eckel RH, Farese RV Jr. Increased insulin and leptin sensitivity in mice lacking acyl CoA:diacylglycerol acyltransferase 1. J Clin Invest. 2002;109:1049-1055.
21. Chen N, Liu L, Zhang Y, Ginsberg HN, Yu YH. Whole-body insulin resistance in the absence of obesity in FVB mice with overexpression of dgat1 in adipose tissue. Diabetes. 2005;54:3379-3386.
22. Levin MC, Monetti M, Watt MJ, Sajan MP, Stevens RD, Bain JR, Newgard CB, Farese RV Sr, Farese RV Jr. Increased lipid accumulation and insulin resistance in transgenic mice expressing dgat2 in glycolytic (type II) muscle. Am J Physiol Endocrinol Metab. 2007;293:E1772-E1781.
23. Liu L, Zhang Y, Chen N, Shi X, Tsang B, Yu YH. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J Clin Invest. 2007; 117:1679-1689.
24. Rajabi M, Kassiotis C, Razeghi P, Taegtmeyer H. Return to the fetal gene program protects the stressed heart: a strong hypothesis. Heart Fail Rev. 2007;12:331-343.
25. Oh JK, Hatle L, Tajik AJ, Little WC. Diastolic heart failure can be diagnosed by comprehensive two-dimensional and Doppler echocardiog-raphy. J Am Coll Cardiol. 2006;47:500-506.
26. Querejeta R, Lopez B, Gonzalez A, Sanchez E, Larman M, Martinez Ubago JL, Diez J. Increased collagen type I synthesis in patients with heart failure of hypertensive origin: relation to myocardial fibrosis. Circulation. 2004;110: 1263-1268.
27. Haukipuro KA, Harju EJ, Risteli L. Effect of intravenous feeding on wound healing in starvation: an experimental study on the rabbit. In Vivo. 1991;5:43-47.
28. Peterson JT, Li H, Dillon L, Bryant JW. Evolution of matrix metallo-protease and tissue inhibitor expression during heart failure progression in the infarcted rat. Cardiovasc Res. 2000;46:307-315.
29. Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX, Aziz S, Johnson JI, Bugger H, Zaha VG, Abel ED. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes. 2007;56:2457-2466.
30. Tsutsui H, Kinugawa S, Matsushima S. Mitochondrial oxidative stress and dysfunction in myocardial remodelling. Cardiovasc Res. 2009;81:449-456.
31. Wang P, Liu J, Li Y, Wu S, Luo J, Yang H, Subbiah R, Chatham J, Zhelyabovska O, Yang Q. Peroxisome proliferator-activated receptor {delta} is an essential transcriptional regulator for mitochondrial protection and biogenesis in adult heart. Circ Res. 2010;106:911-919.
32. Hayashi M, Imanaka-Yoshida K, Yoshida T, Wood M, Fearns C, Tatake RJ, Lee JD. A crucial role of mitochondrial HSP40 in preventing dilated cardiomyopathy. Nat Med. 2006;12:128-132.
33. Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev. 2008;88:611-638.
34. Duncan JG, Fong JL, Medeiros DM, Finck BN, Kelly DP. Insulin-resistant heart exhibits a mitochondrial biogenic response driven by the peroxisome proliferator-activated receptor-alpha/PGC-1alpha gene regulatory pathway. Circulation. 2007;115:909-917.
35. Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY, Mootha VK, Jager S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, Lowell BB, Krainc D, Spiegelman BM. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell. 2004;119:121-135.
36. Leone TC, Lehman JJ, Finck BN, Schaeffer PJ, Wende AR, Boudina S, Courtois M, Wozniak DF, Sambandam N, Bernal-Mizrachi C, Chen Z, O. Holloszy J, Medeiros DM, Schmidt RE, Saffitz JE, Abel ED, Semen-kovich CF, Kelly DP. PGC-1a; deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 2005;3:e101.
37. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV Jr, Ory DS, Schaffer JE. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA. 2003;100:3077-3082.
38. Liu L, Shi X, Bharadwaj KG, Ikeda S, Yamashita H, Yagyu H, Schaffer JE, Yu Y-H, Goldberg IJ. Dgat1 expression increases heart triglyceride content but ameliorates lipotoxicity. J Biol Chem. 2009;284:36312-36323.
39. Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab. 2001;86:5755-5761.
40. Beggah AT, Escoubet B, Puttini S, Cailmail S, Delage V, Ouvrard-Pascaud A, Bocchi B, Peuchmaur M, Delcayre C, Farman N, Jaisser F. Reversible cardiac fibrosis and heart failure induced by conditional expression of an antisense mRNA of the mineralocorticoid receptor in cardiomyocytes. Proc Natl Acad Sci USA. 2002;99:7160-7165.
41. Anderson KR, Sutton MG, Lie JT. Histopathological types of cardiac fibrosis in myocardial disease. J Pathol. 1979;128:79-85.
42. Zaman AK, Fujii S, Goto D, Furumoto T, Mishima T, Nakai Y, Dong J, Imagawa S, Sobel BE, Kitabatake A. Salutary effects of attenuation of angiotensin II on coronary perivascular fibrosis associated with insulin resistance and obesity. J Mol Cell Cardiol. 2004;37:525-535.
43. Zaman AK, Fujii S, Sawa H, Goto D, Ishimori N, Watano K, Kaneko T, Furumoto T, Sugawara T, Sakuma I, Kitabatake A, Sobel BE. Angiotensin-converting enzyme inhibition attenuates hypofibrinolysis and reduces cardiac perivascular fibrosis in genetically obese diabetic mice. Circulation. 2001; 103:3123-3128.
44. Graier WF, Malli R, Kostner GM. Mitochondrial protein phosphorylation: instigator or target of lipotoxicity? Trends Endocrinol Metab. 2009; 20:186-193.
45. Goodpaster BH, Kelley DE. Skeletal muscle triglyceride: marker or mediator of obesity-induced insulin resistance in type 2 diabetes mellitus? Curr Diab Rep. 2002;2:216-222.
46. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes. 2002; 51:2944-2950.
47. Russell LK, Finck BN, Kelly DP. Mouse models of mitochondrial dysfunction and heart failure. J Mol Cell Cardiol. 2005;38:81-91.
48. Lin JD. Minireview: the PGC-1 coactivator networks: chromatin-remodeling and mitochondrial energy metabolism. Mol Endocrinol. 2009; 23:2-10.
49. Garnier A, Fortin D, Delomenie C, Momken I, Veksler V, Ventura-Clapier R. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. Physiol Rev. 2003;551:491-501.
50. Arany Z, He H, Lin J, Hoyer K, Handschin C, Toka O, Ahmad F, Matsui T, Chin S, Wu P-H, Rybkin II, Shelton JM, Manieri M, Cinti S, Schoen FJ, Bassel-Duby R, Rosenzweig A, Ingwall JS, Spiegelman BM. Transcriptional coactivator PGC-1a controls the energy state and contractile function of cardiac muscle. Cell Metabolism. 2005;1:259-271.
51. Sihag S, Cresci S, Li AY, Sucharov CC, Lehman JJ. PGC-1a and ERRa target gene downregulation is a signature of the failing human heart. J Mol Cell Cardiol. 2009;46:201-212.
52. Alpert MA, Terry BE, Mulekar PM, Cohen MV, Massey CV, Fan TM, Panayiotou H, Mukerji V. Cardiac morphology and left ventricular function in normotensive morbidly obese patients with and without congestive heart failure, and effect of weight loss. Am J Cardiol. 1997;80: 736-740.
53. Nichols GA, Hillier TA, Erbey JR, Brown JB. Congestive heart failure in type 2 diabetes. Diabetes Care. 2001;24:1614-1619.
54. McGavock JM, Lingvay I, Zib I, Tillery T, Salas N, Unger R, Levine BD, Raskin P, Victor RG, Szczepaniak LS. Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation. 2007;116:1170-1175.