Impaired translocation and activation of mitochondrial Akt1 mitigated mitochondrial oxidative phosphorylation Complex V activity in diabetic myocardium

Journal of Molecular and Cellular Cardiology

Volumn 59, Issue 1, 2013, Pages 167-175

  Yang, Jia Ying ^a,b   Deng, Wu ^a,b   Chen, Yumay ^a,b   Fan, Weiwei ^a,b   Baldwin, Kenneth M ^b   Jope, Richard S ^c   Wallace, Douglas C ^a,b,d   Wang, Ping H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CREATINE PHOSPHATE; ISOPROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN AKT1; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; ENZYME ACTIVITY; HEART MUSCLE CELL; IN VITRO STUDY; INSULIN RESISTANCE; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL TARGETING SIGNAL; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CARRIER PROTEINS; DIABETES MELLITUS, TYPE 2; INSULIN; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; MYOCARDIUM; OXIDATIVE PHOSPHORYLATION; PHOSPHOCREATINE; PROTO-ONCOGENE PROTEINS C-AKT; RATS;

EID: 84875917083     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.02.016     Document Type: Article

References (48)

1. Sale E.M., Sale G.J. Protein kinase B: signaling roles and therapeutic targeting. Cell Mol Life Sci 2008, 65:113-127.
2. Coffer P.J., Jin J., Woodgett J.R. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J 1998, 335:1-13.
3. Alessi D.R., Caudwell F.B., Andjelkovic M., Hemming B.A., Cohen P. Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett 1996, 399:333-338.
4. Manning B.D., Cantley L.C. Akt/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
5. Bertrand L., Horman S., Beaulove C., Vanoverschelde J.L. Insulin signaling in the heart. Cardiovasc Res 2008, 79:238-248.
6. Gottlob K., Majewski N., Kennedy S., Kandel E., Robey R.B., Hay N. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 2001, 15:1406-1418.
7. Hahn-Windgassen A., Nogueira V., Chen C.C., Skeen J.E., Soneeberg N., Hay N. Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J Biol Chem 2005, 280:32081-32089.
8. Yang J.Y., Yeh H.Y., Lin K., Wang P.H. Insulin stimulates Akt translocation to mitochondria: implications on dysregulation of mitochondrial oxidative phosphorylation in diabetic myocardium. J Mol Cell Cardiol 2009, 46:919-926.
9. Matheny R.W., Adamo M.L. Current perspectives on Akt Akt-ivation and Akt-ions. Exp Biol Med (Maywood) 2009, 234:1264-1270.
10. Masure S., Haefner B., Wesselink J.J., Hoefnagel E., Mortier E., Verhasselt P., et al. Molecular cloning, expression and characterization of the human serine/threonine kinase Akt-3. Eur J Biochem 1999, 265:353-360.
11. Cho H., Thorvaldsen J.L., Chu Q., Feng F., Birnbaum M.J. Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J Biol Chem 2001, 276:38349-38352.
12. Cho H., Mu J., Kim J.K., Thorvaldsen J.L., Chu Q., Crenshaw E.B., et al. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 2001, 292:1728-1731.
13. Garofalo R.S., Orena S.J., Rafidi K., Torchia A.J., Stock J.L., Hildebrandt A.L., et al. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J Clin Invest 2003, 112:197-208.
14. Easton R.M., Cho H., Roovers K., Shineman D.W., Mizrahi M., Forman M.S., et al. Role of Akt3/protein kinase Bgamma in attainment of normal brain size. Mol Cell Biol 2005, 25:1869-1878.
15. Tschopp O., Yang Z.Z., Brodbeck D., Dummler B.A., Hemmings-Mieszczak M., Watanabe T., et al. Essential role of protein kinase B gamma (PKB gamma/Akt3) in postnatal brain development but not in glucose homeostasis. Development 2005, 132:2943-2954.
16. O'Neill B.T., Kim J., Wende A.R., Theobald H.A., Tuinei J., Buchanan J., et al. A conserved role for phosphoinositide-3-kinase but not Akt signaling in mitochondrial adaptations that accompany physiological cardiac hypertrophy. Cell Metab 2007, 6:294-306.
17. Zinda M.J., Johnson M.A., Paul J.D., Horn C., Konicek B.W., Lu Z.H., et al. Akt-1, -2, and -3 are expressed in both normal and tumor tissue of lung, breast, prostate, and colon. Clin Cancer Res 2001, 7:2475-2479.
18. Rubler S., Dlugash J., Yuceoglu Y.Z., Kumral T., Branwood A.W., Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 1972, 30:595-602.
19. Bugger H., Abel E.D. Molecular mechanisms for myocardial mitochondrial dysfunction in the metabolic syndrome. Clin Sci (Lond) 2008, 114:195-210.
20. Scheuermann-Freestone M., Madsen P.L., Manners D., Blamire A.M., Buckingham R.E., Styles P., et al. Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes. Circulation 2003, 107:3040-3046.
21. Ye G., Metreveli N.S., Donthi R.V., Xia S., Xu M., Carlson E.C., et al. Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes 2004, 53:1336-1343.
22. Pierce G.N., Dhalla N.S. Heart mitochondrial function in chronic experimental diabetes in rats. Can J Cardiol 1985, 1:48-54.
23. Boudina S., Sena S., O'Neill B.T., Tathireddy P., Young M.E., Abel E.D. Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 2005, 112:2686-2695.
24. Savabi F. Mitochondrial creatine phosphokinase deficiency in diabetic rat heart. Biochem Biophys Res Commun 1988, 154:469-475.
25. Veksler V.I., Murat I., Ventura-Clapier R. Creatine kinase and mechanical and mitochondrial functions in hereditary and diabetic cardiomyopathies. Can J Physiol Pharmacol 1991, 69:852-858.
26. Su H., Samsamshariat A., Fu J., Shan Y.X., Chen Y.H., Piomelli D., et al. Oleylethanolamide activates Ras-Erk pathway and improves myocardial function in doxorubicin induced heart failure. Endocrinology 2006, 147:827-834.
27. Barrientos A. In vivo and in organello assessment of OXPHO activity. Methods 2002, 26:307-316.
28. Trounce I.A., Kim Y.L., Wallace D.C. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and trans-mitochondrial cell lines. Methods Enzymol 1996, 264:484-509.
29. Giger J.M., Bodell P.W., Baldwin K.M., Haddad F. The CAAT-binding transcription factor 1/nuclear factor 1 binding site is important in beta-myosin heavy chain antisense promoter regulation in rats. Exp Physiol 2009, 94:1163-1173.
30. Su C.C., Yang J.Y., Leu H.B., Chen Y., Wang P.H. Mitochondrial Akt regulated mitochondrial apoptosis signaling in cardiac muscle cells. Am J Physiol Heart Circ Physiol 2012, 302:H716-H723.
31. Huss J.M., Kelly D.P. Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest 2005, 115:543-555.
32. Szendroedi J., Roden M. Mitochondrial fitness and insulin sensitivity in humans. Diabetologia 2008, 51:2155-2167.
33. Boirie Y. Insulin regulation of mitochondrial proteins and oxidative phosphorylation in human muscle. Trends Endocrinol Metab 2003, 14:393-394.
34. Hermann J.M., Reimer J. The intramembrane space of mitochondria. Antioxid Redox Signal 2010, 13:1341-1358.
35. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
36. Pedersen P.L. Transport ATPase into the year 2009: a brief overview related to types, structures, functions and roles in health and disease. J Bioenerg Biomembr 2007, 39:349-355.
37. Shiojima I., Walsh K. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev 2006, 20:3347-3365.
38. DeBosch B., Treskov I., Lupu T.S., Weinheimer C., Kovacs A., Courtois M., et al. Akt1 is required for physiological cardiac growth. Circulation 2006, 113:2097-2104.
39. DeBosch B., Sambandam N., Weinheimer C., Courtois M., Muslin A.J. Akt2 regulates cardiac metabolism and cardiomyocyte survival. J Biol Chem 2006, 281:32841-32851.
40. Chen W.S., Peng X.D., Wang Y., Xu P.Z., Chen M.L., Luo Y., et al. Leptin deficiency and beta-cell dysfunction underlie type 2 diabetes in compound Akt knockout mice. Mol Cell Biol 2009, 29:3151-3162.
41. Hay N. Akt isoforms and glucose homeostasis-the leptin connection. Trends Endocrinol Metab 2011, 22:66-73.
42. Gonzalez E., McGraw T.E. Insulin-modulated Akt subcellular localization determines Akt isoform-specific signaling. Proc Natl Acad Sci 2009, 106:7004-7009.
43. Neubauer S., Horn M., Cramer M., Harre K., Newell J.B., Peters W., et al. Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation 1997, 96(7):2190-2196.
44. Salvi M., Brunati A.M., Toninello A. Tyrosine phosphorylation in mitochondria: a new frontier in mitochondrial signaling. Free Radic Biol Med 2005, 38:1267-1277.
45. Fang J.K., Prabu S.K., Sepuri N.B., Raza H., Anandatheerthavarada H.K., Galati D., et al. Site specific phosphorylation of cytochrome c oxidase subunits I IVi1 and Vb in rabbit hearts subjected to ischemia/reperfusion. FEBS Lett 2007, 58:11302-11310.
46. Lee I., Salomon A.R., Ficarro S., Mathes I., Lottspeich F., Grossman L.I., et al. cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J Biol Chem 2005, 280:6094-6100.
47. Li L., Lorenzo P.S., Bogi K., Blumberg P.M., Yuspa S.H. Protein kinase C delta targets mitochondria, alters mitochondrial membrane potential, and induces apoptosis in normal and neoplastic keratinocytes when overexpressed by an adenoviral vector. Mol Cell Biol 1999, 19:8547-8558.
48. Stanley W.C., Lopaschuk G.D., McCormack J.G. Regulation of energy substrate metabolism in the diabetes heart. Cardiovasc Res 1997, 34:25-33.