Metabolic stress - Induced activation of FoxO1 triggers diabetic cardiomyopathy in mice

Journal of Clinical Investigation

Volumn 122, Issue 3, 2012, Pages 1109-1118

  Battiprolu, Pavan K ^a   Hojayev, Berdymammet ^a   Jiang, Nan ^a   Wang, Zhao V ^a   Luo, Xiang ^a   Iglewski, Myriam ^a   Shelton, John M ^a   Gerard, Robert D ^a   Rothermel, Beverly A ^a   Gillette, Thomas G ^a   Lavandero, Sergio ^a,b   Hill, Joseph A ^a,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; GLUCOSE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; LIPID; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; DISEASE COURSE; DOWN REGULATION; HEART; HEART FUNCTION; HEART MUSCLE CELL; INFORMATION PROCESSING; INSULIN RESISTANCE; INSULIN RESPONSE; INTRACELLULAR SIGNALING; LIPID DIET; MALE; METABOLIC STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION;

ANIMALS; BODY WEIGHT; CELL SIZE; CELL SURVIVAL; DIABETIC CARDIOMYOPATHIES; FATTY ACIDS; FORKHEAD TRANSCRIPTION FACTORS; GLUCOSE; HEART FAILURE; INSULIN; MICE; MICE, INBRED C57BL; MYOCYTES, CARDIAC; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SOMATOMEDINS; SUBCELLULAR FRACTIONS;

EID: 84863283393     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI60329     Document Type: Article

References (58)

1. Roger VL, et al. Heart disease and stroke statistics - 2011 update: a report from the American Heart Association. Circulation. 2011;123(4):e18-e209.
2. Witteles RM, Fowler MB. Insulin-resistant cardiomyopathy clinical evidence, mechanisms, and treatment options. J Am Coll Cardiol. 2008;51(2):93-102.
3. Battiprolu PK, Gillette TG, Wang ZV, Lavandero S, Hill JA. Diabetic cardiomyopathy: mechanisms and therapeutic targets. Drug Discov Today Dis Mech. 2010;7(2):e135-e143.
4. Ferdous A, Battiprolu PK, Ni YG, Rothermel BA, Hill JA. FoxO, autophagy, and cardiac remodeling. J Cardiovasc Transl Res. 2010;3(4):355-364.
5. Cheng Z, White MF. Targeting Forkhead box O1 from the concept to metabolic diseases: lessons from mouse models. Antioxid Redox Signal. 2011;14(4):649-661.
6. Ronnebaum SM, Patterson C. The FoxO family in cardiac function and dysfunction. Annu Rev Physiol. 2010;72:81-94.
7. Ni YG, et al. FoxO transcription factors activate Akt and attenuate insulin signaling in heart by inhibiting protein phosphatases. Proc Natl Acad Sci U S A. 2007;104(51):20517-20522.
8. Tremblay ML, Giguere V. Phosphatases at the heart of FoxO metabolic control. Cell Metab. 2008;7(2):101-103. (Pubitemid 351168562)
9. Koitabashi N, et al. Avoidance of transient cardiomyopathy in cardiomyocyte-targeted tamoxifeninduced MerCreMer gene deletion models. Circ Res. 2009;105(1):12-15.
10. Ouwens DM, et al. Cardiac dysfunction induced by high-fat diet is associated with altered myocardial insulin signalling in rats. Diabetologia. 2005;48(6):1229-1237. (Pubitemid 40909661)
11. Park TS, et al. Ceramide is a cardiotoxin in lipotoxic cardiomyopathy. J Lipid Res. 2008;49(10):2101-2112.
12. Coort SL, et al. Enhanced sarcolemmal FAT/CD36 content and triacylglycerol storage in cardiac myocytes from obese zucker rats. Diabetes. 2004;53(7):1655-1663. (Pubitemid 38857021)
13. Zhang LY, Keung W, Samokhvalov V, Wang W, Lopaschuk GD. Role of fatty acid uptake and fatty acid beta-oxidation in mediating insulin resistance in heart and skeletal muscle. Biochim Biophys Acta. 2010;1801(1):1-22.
14. Yan J, Young ME, Cui L, Lopaschuk GD, Liao R, Tian R. Increased glucose uptake and oxidation in mouse hearts prevent high fatty acid oxidation but cause cardiac dysfunction in diet-induced obesity. Circulation. 2009;119(21):2818- 2828.
15. Carley AN, Kleinfeld AM. Fatty acid (FFA) transport in cardiomyocytes revealed by imaging unbound FFA is mediated by an FFA pump modulated by the CD36 protein. J Biol Chem. 2011;286(6):4589-4597.
16. Wright JJ, et al. Mechanisms for increased myocardial fatty acid utilization following short-term highfat feeding. Cardiovasc Res. 2009;82(2):351-360.
17. Chabowski A, et al. Insulin stimulates fatty acid transport by regulating expression of FAT/CD36 but not FABPpm. Am J Physiol Endocrinol Metab. 2004;287(4):E781-E789. (Pubitemid 39237909)
18. Zhao G, et al. Overexpression of pyruvate dehydrogenase kinase 4 in heart perturbs metabolism and exacerbates calcineurin-induced cardiomyopathy. Am J Physiol Heart Circ Physiol. 2008;294(2):H936-H943. (Pubitemid 351253306)
19. Long YC, Cheng Z, Copps KD, White MF. Insulin receptor substrates Irs1 and Irs2 coordinate skeletal muscle growth and metabolism via the Akt and AMPK pathways. Mol Cell Biol. 2011;31(3):430-441.
20. Chambers KT, et al. Chronic inhibition of pyruvate dehydrogenase in heart triggers an adaptive metabolic response. J Biol Chem. 2011;286(13):11155-11162.
21. Cheng Z, Tseng Y, White MF. Insulin signaling meets mitochondria in metabolism. Trends Endocrinol Metab. 2010;21(10):589-598.
22. Prudente S, Morini E, Trischitta V. Insulin signaling regulating genes: effect on T2DM and cardiovascular risk. Nat Rev Endocrinol. 2009;5(12):682-693.
23. Ueno M, et al. Regulation of insulin signalling by hyperinsulinaemia: role of IRS-1/2 serine phosphorylation and the mTOR/p70 S6K pathway. Diabetologia. 2005;48(3):506-518. (Pubitemid 40487298)
24. Guo S, Dunn SL, White MF. The reciprocal stability of FOXO1 and IRS2 creates a regulatory circuit that controls insulin signaling. Mol Endocrinol. 2006;20(12):3389-3399. (Pubitemid 44833578)
25. Pederson TM, Kramer DL, Rondinone CM. Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes. 2001;50(1):24-31. (Pubitemid 32047976)
26. Wang Y, Nishina PM, Naggert JK. Degradation of IRS1 leads to impaired glucose uptake in adipose tissue of the type 2 diabetes mouse model TALLYHO/Jng. J Endocrinol. 2009;203(1):65-74.
27. Lin Y, Sun Z. Current views on type 2 diabetes. J Endocrinol. 2010;204(1):1-11.
28. White MF. Insulin signaling in health and disease. Science. 2003;302(5651):1710-1711. (Pubitemid 37505726)
29. Meyer C, Stumvoll M, Nadkarni V, Dostou J, Mitrakou A, Gerich J. Abnormal renal and hepatic glucose metabolism in type 2 diabetes mellitus. J Clin Invest. 1998;102(3):619-624. (Pubitemid 28376164)
30. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res. 2006;98(5):596-605.
31. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414(6865):813-820. (Pubitemid 34000785)
32. Cai L, Li W, Wang G, Guo L, Jiang Y, Kang YJ. Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes. 2002;51(6):1938-1948. (Pubitemid 34564309)
33. Eliasson MJ, et al. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med. 1997;3(10):1089-1095. (Pubitemid 27444449)
34. Montagnani M. Diabetic cardiomyopathy: how much does it depend on AGE? Br J Pharmacol. 2008;154(4):725-726. (Pubitemid 351821582)
35. Galvez AS, et al. Aldose reductase induced by hyperosmotic stress mediates cardiomyocyte apoptosis: differential effects of sorbitol and mannitol. J Biol Chem. 2003;278(40):38484-38494. (Pubitemid 37221743)
36. Luiken JJ, et al. Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes. 2002;51(10):3113-3119.
37. Wende AR, Abel ED. Lipotoxicity in the heart. Biochim Biophys Acta. 2010;1801(3):311-319.
38. Kannel WB, Hjortland M, Castelli WP. Role of diabetes in congestive heart failure: the Framingham study. Am J Cardiol. 1974;34(1):29-34.
39. Sarwar N, et al. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375(9733):2215-2222.
40. Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Branwood AW, Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol. 1972;30(6):595-602.
41. Rodrigues B, Cam MC, McNeill JH. Metabolic disturbances in diabetic cardiomyopathy. Mol Cell Biochem. 1998;180(1-2):53-57. (Pubitemid 28118803)
42. An D, Rodrigues B. Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol. 2006;291(4):H1489-H1506. (Pubitemid 44497651)
43. Boudina S, Abel ED. Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord. 2010;11(1):31-39.
44. Dobrin JS, Lebeche D. Diabetic cardiomyopathy: signaling defects and therapeutic approaches. Expert Rev Cardiovasc Ther. 2010;8(3):373-391.
45. Hayat SA, Patel B, Khattar RS, Malik RA. Diabetic cardiomyopathy: mechanisms, diagnosis and treatment. Clin Sci (Lond). 2004;107(6):539-557. (Pubitemid 39627201)
46. Abel ED. Insulin signaling in heart muscle: lessons from genetically engineered mouse models. Curr Hypertens Rep. 2004;6(6):416-423. (Pubitemid 39600096)
47. Skurk C, et al. The FOXO3a transcription factor regulates cardiac myocyte size downstream of AKT signaling. J Biol Chem. 2005;280(21):20814-20823. (Pubitemid 40776786)
48. Ni YG, et al. Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling. Circulation. 2006;114(11):1159-1168. (Pubitemid 44386480)
49. Sengupta A, Molkentin JD, Yutzey KE. FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem. 2009;284(41):28319-28331.
50. Stahl M, et al. The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J Immunol. 2002;168(10):5024-5031. (Pubitemid 34495965)
51. Kops GJ, et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature. 2002;419(6904):316-321.
52. Puigserver P, et al. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature. 2003;423(6939):550-555. (Pubitemid 36648580)
53. Medema RH, Kops GJ, Bos JL, Burgering BM. AFXlike Forkhead transcription factors mediate cellcycle regulation by Ras and PKB through p27kip1. Nature. 2000;404(6779):782-787. (Pubitemid 30212408)
54. Ogg S, et al. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature. 1997;389(6654):994-999. (Pubitemid 27485694)
55. Horowitz JD, Chirkov YY, Kennedy JA, Sverdlov AL. Modulation of myocardial metabolism: an emerging therapeutic principle. Curr Opin Cardiol. 2010;25(4):329-334.
56. Collins KA, et al. Accuracy of echocardiographic estimates of left ventricular mass in mice. Am J Physiol Heart Circ Physiol. 2001;280(5):H1954- H1962.
57. Battiprolu PK, Harmon KJ, Rodnick KJ. Sex differences in energy metabolism and performance of teleost cardiac tissue. Am J Physiol Regul Integr Comp Physiol. 2007;292(2):R827-R836. (Pubitemid 46207736)
58. Wang Y, Cheng J, Joyner RW, Wagner MB, Hill JA. Remodeling of early-phase repolarization: a mechanism of abnormal impulse conduction in heart failure. Circulation. 2006;113(15):1849-1856. (Pubitemid 43739396)