Magnetic resonance imaging of progressive cardiomyopathic changes in the db/db mouse

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 292, Issue 5, 2007, Pages

  Yue, Patrick ^a,c   Arai, Takayasu ^a   Terashima, Masahiro ^a   Sheikh, Ahmad Y ^b   Cao, Feng ^a   Charo, David ^a   Hoyt, Grant ^b   Robbins, Robert C ^b   Ashley, Euan A ^a   Wu, Joseph ^a   Yang, Phillip C ^a   Tsao, Philip S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Diabetes mellitus; Heart failure; Insulin resistance; Metabolism

Indexed keywords

FLUORODEOXYGLUCOSE F 18; GLUCOSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOMYOPATHY; CONTROLLED STUDY; FEMALE; GLUCOSE TRANSPORT; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE MASS; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; STATISTICAL SIGNIFICANCE; ANIMAL; COMPUTER ASSISTED DIAGNOSIS; HEART LEFT VENTRICLE FUNCTION; HEART VENTRICLE; METHODOLOGY; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CARDIOMYOPATHIES; FEMALE; HEART VENTRICLES; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED STRAINS; VENTRICULAR DYSFUNCTION, LEFT;

EID: 34250835571     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00856.2006     Document Type: Article

References (66)

1. Aasum E, Hafstad AD, Severson DL, Larsen TS. Age-dependent changes in metabolism, contractile function, and ischemic sensitivity in hearts from db/db mice. Diabetes 52: 434-441, 2003.
2. Abe T, Ohga Y, Tabayashi N, Kobayashi S, Sakata S, Misawa H, Tsuji T, Kohzuki H, Suga H, Taniguchi S, Takaki M. Left ventricular diastolic dysfunction in type 2 diabetes mellitus model rats. Am J Physiol Heart Circ Physiol 282: H138-H148, 2002.
3. Al-Shafei AI, Wise RG, Gresham GA, Bronns G, Carpenter TA, Hall LD, Huang CL. Non-invasive magnetic resonance imaging assessment of myocardial changes and the effects of angiotensin-converting enzyme inhibition in diabetic rats. J Physiol 538: 541-553, 2002.
4. Al-Shafei AI, Wise RG, Gresham GA, Carpenter TA, Hall LD, Huang CL. Magnetic resonance imaging analysis of cardiac cycle events in diabetic rats: the effect of angiotensin-converting enzyme inhibition. J Physiol 538: 555-572, 2002.
5. An D, Rodrigues B. Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 291: H1489-H1506, 2006.
6. Bagi Z, Erdei N, Toth A, Li W, Hintze TH, Koller A, Kaley G. Type 2 diabetic mice have increased arteriolar tone and blood pressure: enhanced release of COX-2-derived constrictor prostaglandins. Arterioscler Thromb Vasc Biol 25: 1610-1616, 2005.
7. Barouch LA, Berkowitz DE, Harrison RW, O'Donnell CP, Hare JM. Disruption of leptin signaling contributes to cardiac hypertrophy independently of body weight in mice. Circulation 108: 754-759, 2003.
8. Barouch LA, Gao D, Chen L, Miller KL, Xu W, Phan AC, Kittleson MM, Minhas KM, Berkowitz DE, Wei C, Hare JM. Cardiac myocyte apoptosis is associated with increased DNA damage and decreased survival in murine models of obesity. Circ Res 98: 119-124, 2006.
9. Bauters C, Lamblin N, Mc Fadden EP, Van Belle E, Millaire A, de Groote P. Influence of diabetes mellitus on heart failure risk and outcome. Cardiovasc Diabetol 2: 1, 2003.
10. Belke DD, Larsen TS, Gibbs EM, Severson DL. Altered metabolism causes cardiac dysfunction in perfused hearts from diabetic (db/db) mice. Am J Physiol Endocrinol Metab 279: E1104-E1113, 2000.
11. Belke DD, Swanson EA, Dillmann WH. Decreased sarcoplasmic reticulum activity and contractility in diabetic db/db mouse heart. Diabetes 53: 3201-3208, 2004.
12. Berthiaume N, Mika AK, Zinker BA. Development of insulin resistance and endothelin-1 levels in the Zucker fatty rat. Metabolism 52: 845-849, 2003.
13. Bertoni AG, Tsai A, Kasper EK, Brancati FL. Diabetes and idiopathic cardiomyopathy: a nationwide case-control study. Diabetes Care 26: 2791-2795, 2003.
14. 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 146: 5341-5349, 2005.
15. Calderone A, Takahashi N, Izzo NJ Jr, Thaik CM, Colucci WS. Pressure- and volume-induced left ventricular hypertrophies are associated with distinct myocyte phenotypes and differential induction of peptide growth factor mRNAs. Circulation 92: 2385-2390, 1995.
16. Carley AN, Semeniuk LM, Shimoni Y, Aasum E, Larsen TS, Berger JP, Severson DL. Treatment of type 2 diabetic db/db mice with a novel PPARγ agonist improves cardiac metabolism but not contractile function. Am J Physiol Endocrinol Metab 286: E449-E455, 2004.
17. Carroll R, Carley AN, Dyck JR, Severson DL. Metabolic effects of insulin on cardiomyocytes from control and diabetic db/db mouse hearts. Am J Physiol Endocrinol Metab 288: E900-E906, 2005.
18. Chatham JC, Seymour AM. Cardiac carbohydrate metabolism in Zucker diabetic fatty rats. Cardiovasc Res 55: 104-112, 2002.
19. Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, Lakey ND, Culpepper J, Moore KJ, Breitbart RE, Duyk GM, Tepper RI, Morgenstern JP. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 84: 491-495, 1996.
20. Christoffersen C, Bartels ED, Nielsen LB. Heart specific up-regulation of genes for B-type and C-type natriuretic peptide receptors in diabetic mice. Eur J Clin Invest 36: 69-75, 2006.
21. Day ML, Schwartz D, Wiegand RC, Stockman PT, Brunnert SR, Tolunay HE, Currie MG, Standaert DG, Needleman P. Ventricular atriopeptin. Unmasking of messenger RNA and peptide synthesis by hypertrophy or dexamethasone. Hypertension 9: 485-491, 1987.
22. de Simone G, Devereux RB, Roman MJ, Alderman MH, Laragh JH. Relation of obesity and gender to left ventricular hypertrophy in normotensive and hypertensive adults. Hypertension 23: 600-606, 1994.
23. Devereux RB, Roman MJ, Paranicas M, O'Grady MJ, Lee ET, Welty TK, Fabsitz RR, Robbins D, Rhoades ER, Howard BV. Impact of diabetes on cardiac structure and function: the Strong Heart Study. Circulation 101: 2271-2276, 2000.
24. Dillmann WH. Biochemical basis of thyroid hormone action in the heart. Am J Med 88: 626-630, 1990.
25. Engelgau MM, Geiss LS, Saaddine JB, Boyle JP, Benjamin SM, Gregg EW, Tierney EF, Rios-Burrows N, Mokdad AH, Ford ES, Imperatore G, Narayan KM. The evolving diabetes burden in the United States. Ann Intern Med 140: 945-950, 2004.
26. Fang ZY, Yuda S, Anderson V, Short L, Case C, Marwick TH. Echocardiographic detection of early diabetic myocardial disease. J Am Coll Cardiol 41: 611-617, 2003.
27. Fredersdorf S, Thumann C, Ulucan C, Griese DP, Luchner A, Riegger GA, Kromer EP, Weil J. Myocardial hypertrophy and enhanced left ventricular contractility in Zucker diabetic fatty rats. Cardiovasc Pathol 13: 11-19, 2004.
28. Frustaci A, Kajstura J, Chimenti C, Jakoniuk I, Leri A, Maseri A, Nadal-Ginard B, Anversa P. Myocardial cell death in human diabetes. Circ Res 87: 1123-1132, 2000.
29. Galderisi M, Anderson KM, Wilson PW, Levy D. Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). Am J Cardiol 68: 85-89, 1991.
30. Gower WR Jr, San Miguel GI, Carter GM, Hassan I, Farese RV, Vesely DL. Atrial natriuretic hormone prohormone gene expression in cardiac and extra-cardiac tissues of diabetic Goto-Kakizaki rats. Mol Cell Biochem 252: 263-271, 2003.
31. How OJ, Aasum E, Severson DL, Chan WY, Essop MF, Larsen TS. Increased myocardial oxygen consumption reduces cardiac efficiency in diabetic mice. Diabetes 55: 466-473, 2006.
32. Huang Y, Walker KE, Hanley F, Narula J, Houser SR, Tulenko TN. Cardiac systolic and diastolic dysfunction after a cholesterol-rich diet. Circulation 109: 97-102, 2004.
33. Iltis I, Kober F, Desrois M, Dalmasso C, Lan C, Portha B, Cozzone PJ, Bernard M. Defective myocardial blood flow and altered function of the left ventricle in type 2 diabetic rats: a noninvasive in vivo study using perfusion and cine magnetic resonance imaging. Invest Radiol 40: 19-26, 2005.
34. Izumo S, Lompre AM, Matsuoka R, Koren G, Schwartz K, Nadal-Ginard B, Mahdavi V. Myosin heavy chain messenger RNA and protein isoform transitions during cardiac hypertrophy. Interaction between hemodynamic and thyroid hormone-induced signals. J Clin Invest 79: 970-977, 1987.
35. Katz AM. Heart Failure: Pathophysiology, Molecular Biology, and Clinical Management. Philadelphia, PA: Lippincott Williams and Wilkins, 2000.
36. Kosugi R, Shioi T, Watanabe-Maeda K, Yoshida Y, Takahashi K, Machida Y, Izumi T. Angiotensin II receptor antagonist attenuates expression of aging markers in diabetic mouse heart. Circ J 70: 482-488, 2006.
37. Langenickel T, Pagel I, Hohnel K, Dietz R, Willenbrock R. Differential regulation of cardiac ANP and BNP mRNA in different stages of experimental heart failure. Am J Physiol Heart Circ Physiol 278: H1500-H1506, 2000.
38. Lee M, Gardin JM, Lynch JC, Smith VE, Tracy RP, Savage PJ, Szklo M, Ward BJ. Diabetes mellitus and echocardiographic left ventricular function in free-living elderly men and women: the Cardiovascular Health Study. Am Heart J 133: 36-43, 1997.
39. 2+-ATPase and myosin heavy chain isozyme switch. Diabetologia 49: 1434-1446, 2006.
40. Like AA, Lavine RL, Poffenbarger PL, Chick WL. Studies in the diabetic mutant mouse. VI. Evolution of glomerular lesions and associated proteinuria. Am J Pathol 66: 193-224, 1972.
41. Loganathan R, Bilgen M, Al-Hafez B, Alenezy MD, Smirnova IV. Cardiac dysfunction in the diabetic rat: quantitative evaluation using high resolution magnetic resonance imaging. Cardiovasc Diabetol 5: 7, 2006.
42. Messerli FH, Sundgaard-Riise K, Reisin ED, Dreslinski GR, Ventura HO, Oigman W, Frohlich ED, Dunn FG. Dimorphic cardiac adaptation to obesity and arterial hypertension. Ann Intern Med 99: 757-761, 1983.
43. Oakes ND, Thalen P, Aasum E, Edgley A, Larsen T, Furler SM, Ljung B, Severson D. Cardiac metabolism in mice: tracer method developments and in vivo application revealing profound metabolic inflexibility in diabetes. Am J Physiol Endocrinol Metab 290: E870-E881, 2006.
44. Pang Y, Hunton DL, Bounelis P, Marchase RB. Hyperglycemia inhibits capacitative calcium entry and hypertrophy in neonatal cardiomyocytes. Diabetes 51: 3461-3467, 2002.
45. i transient decrease in cardiomyopathy of db/db type 2 diabetic mice. Diabetes 55: 608-615, 2006.
46. Raev DC. Which left ventricular function is impaired earlier in the evolution of diabetic cardiomyopathy? An echocardiographic study of young type I diabetic patients. Diabetes Care 17: 633-639, 1994.
47. Rajapurohitam V, Gan XT, Kirshenbaum LA, Karmazyn M. The obesity-associated peptide leptin induces hypertrophy in neonatal rat ventricular myocytes. Circ Res 93: 277-279, 2003.
48. Raju SV, Zheng M, Schuleri KH, Phan AC, Bedja D, Saraiva RM, Yiginer O, Vandegaer K, Gabrielson KL, O'Donnell CP, Berkowitz DE, Barouch LA, Hare JM. Activation of the cardiac ciliary neurotrophic factor receptor reverses left ventricular hypertrophy in leptin-deficient and leptin-resistant obesity. Proc Natl Acad Sci USA 103: 4222-4227, 2006.
49. Reyes M, Steinhelper ME, Alvarez JA, Escobedo D, Pearce J, Valvano JW, Pollock BH, Wei CL, Kottam A, Altman D, Bailey S, Thomsen S, Lee S, Colston JT, Oh JH, Freeman GL, Feldman MD. Impact of physiological variables and genetic background on myocardial frequency-resistivity relations in the intact beating murine heart. Am J Physiol Heart Circ Physiol 291: H1659-H1669, 2006.
50. Robertson DM, Sima AA. Diabetic neuropathy in the mutant mouse [C57BL/ks(db/db)]: a morphometric study. Diabetes 29: 60-67, 1980.
51. Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Branwood AW, Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 30: 595-602, 1972.
52. Sabbah HN, Sharov VG, Gupta RC, Mishra S, Rastogi S, Undrovinas AI, Chaudhry PA, Todor A, Mishima T, Tanhehco EJ, Suzuki G. Reversal of chronic molecular and cellular abnormalities due to heart failure by passive mechanical ventricular containment. Circ Res 93: 1095-1101, 2003.
53. Sack MN, Rader TA, Park S, Bastin J, McCune SA, Kelly DP. Fatty acid oxidation enzyme gene expression is downregulated in the failing heart. Circulation 94: 2837-2842, 1996.
54. Samuelsson AM, Bollano E, Mobini R, Larsson BM, Omerovic E, Fu M, Waagstein F, Holmang A. Hyperinsulinemia: effect on cardiac mass/function, angiotensin II receptor expression, and insulin signaling pathways. Am J Physiol Heart Circ Physiol 291: H787-H796, 2006.
55. Sato A, Tarnow L, Nielsen FS, Knudsen E, Parving HH. Left ventricular hypertrophy in normoalbuminuric type 2 diabetic patients not taking antihypertensive treatment. QJM 98: 879-884, 2005.
56. Schaffer SW, Mozaffari M. Abnormal mechanical function in diabetes: relation to myocardial calcium handling. Coron Artery Dis 7: 109-115, 1996.
57. Schaible TF, Malhotra A, Ciambrone G, Scheuer J. The effects of gonadectomy on left ventricular function and cardiac contractile proteins in male and female rats. Circ Res 54: 38-49, 1984.
58. Semeniuk LM, Kryski AJ, Severson DL. Echocardiographic assessment of cardiac function in diabetic db/db and transgenic db/db-hGLUT4 mice. Am J Physiol Heart Circ Physiol 283: H976-H982, 2002.
59. Taegtmeyer H, Overturf ML. Effects of moderate hypertension on cardiac function and metabolism in the rabbit. Hypertension 11: 416-426, 1988.
60. Tenenbaum A, Fisman EZ, Schwammenthal E, Adler Y, Benderly M, Motro M, Shemesh J. Increased prevalence of left ventricular hypertrophy in hypertensive women with type 2 diabetes mellitus. Cardiovasc Diabetol 2: 14, 2003.
61. Troisi RJ, Weiss ST, Parker DR, Sparrow D, Young JB, Landsberg L. Relation of obesity and diet to sympathetic nervous system activity. Hypertension 17: 669-677, 1991.
62. Van den Bergh A, Flameng W, Herijgers P. Type II diabetic mice exhibit contractile dysfunction but maintain cardiac output by favourable loading conditions. Eur J Heart Fail 8: 777-783, 2006.
63. Werner S, Breeden M, Hubner G, Greenhalgh DG, Longaker MT. Induction of keratinocyte growth factor expression is reduced and delayed during wound healing in the genetically diabetic mouse. J Invest Dermatol 103: 469-473, 1994.
64. Wu JC, Inubushi M, Sundaresan G, Schelbert HR, Gambhir SS. Positron emission tomography imaging of cardiac reporter gene expression in living rats. Circulation 106: 180-183, 2002.
65. Xu FP, Chen MS, Wang YZ, Yi Q, Lin SB, Chen AF, Luo JD. Leptin induces hypertrophy via endothelin-1-reactive oxygen species pathway in cultured neonatal rat cardiomyocytes. Circulation 110: 1269-1275, 2004.
66. Yang XP, Liu YH, Rhaleb NE, Kurihara N, Kim HE, Carretero OA. Echocardiographic assessment of cardiac function in conscious and anesthetized mice. Am J Physiol Heart Circ Physiol 277: H1967-H1974, 1999.