Mitochondria in cardiac disease

Translational Cardiology: Molecular Basis of Cardiac Metabolism, Cardiac Remodeling, Translational Therapies and Imaging Techniques

Volumn , Issue , 2012, Pages 63-82

  Gottlieb, Roberta A ^a   Quarato, GioVanni ^a   Abel, E Dale ^b  

^a Donald P Shiley BioScience Center   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIAC DISEASE;

EID: 84922276117     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-61779-891-7_3     Document Type: Chapter

References (135)

1. Lee JK, Belogrudov GI, Stroud RM. Crystal structure of bovine mitochondrial factor B at 0.96-A resolution. Proc Natl Acad Sci USA. 2008;105(36):13379-84.
2. Nicholls DG, Ferguson SJ. Bioenergetics 3. London: Academic; 2002.
3. Hoch FL. Cardiolipins and mitochondrial proton-selective leakage. J Bioenerg Biomembr. 1998;30(6):511-32.
4. Arselin G, Vaillier J, Salin B, et al. The modulation in subunits e and g amounts of yeast ATP synthase modi fi es mitochondrial cristae morphology. J Biol Chem. 2004;279(39):40392-9.
5. Minauro-Sanmiguel F, Wilkens S, Garcia JJ. Structure of dimeric mitochondrial ATP synthase: novel F0 bridging features and the structural basis of mitochondrial cristae biogenesis. Proc Natl Acad Sci USA. 2005;102(35):12356-8.
6. Lesnefsky EJ, Hoppel CL. Cardiolipin as an oxidative target in cardiac mitochondria in the aged rat. Biochim Biophys Acta. 2008;1777(7-8):1020-7.
7. Lesnefsky EJ, Minkler P, Hoppel CL. Enhanced modi fi cation of cardiolipin during ischemia in the aged heart. J Mol Cell Cardiol. 2009;46(6):1008-15.
8. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc). 2005;70(2):200-14.
9. Raffaello A, Rizzuto R. Mitochondrial longevity pathways. Biochim Biophys Acta. 2010;1813(1): 260-8.
10. Kushnareva Y, Murphy AN, Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem J. 2002;368(Pt 2):545-53.
11. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem. 2003;278(38):36027-31.
12. Fato R, Bergamini C, Leoni S, Lenaz G. Mitochondrial production of reactive oxygen species: role of complex I and quinone analogues. Biofactors. 2008;32(1-4):31-9.
13. Li N, Ragheb K, Lawler G, et al. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem. 2003;278(10):8516-25.
14. Fato R, Bergamini C, Bortolus M, et al. Differential effects of mitochondrial Complex I inhibitors on production of reactive oxygen species. Biochim Biophys Acta. 2009;1787(5):384-92.
15. Lesnefsky EJ, Chen Q, Moghaddas S, Hassan MO, Tandler B, Hoppel CL. Blockade of electron transport during ischemia protects cardiac mitochondria. J Biol Chem. 2004;279(46): 47961-7.
16. Seo BB, Marella M, Yagi T, Matsuno-Yagi A. The single subunit NADH dehydrogenase reduces generation of reactive oxygen species from complex I. FEBS Lett. 2006;580(26):6105-8.
17. Perry CN, Huang C, Liu W, Magee N, Carreira RS, Gottlieb RA. Xenotransplantation of mitochondrial electron transfer enzyme, Ndi1, in myocardial reperfusion injury. PLoS One. 2011;6(2):e16288.
18. Camara AK, Bienengraeber M, Stowe DF. Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury. Front Physiol. 2011;2:13.
19. Nicholls DG, Locke RM. Thermogenic mechanisms in brown fat. Physiol Rev. 1984;64(1): 1-64.
20. Ledesma A, de Lacoba MG, Rial E. The mitochondrial uncoupling proteins. Genome Biol. 2002;3(12):REVIEWS3015.
21. Boudina S, Abel ED. Mitochondrial uncoupling: a key contributor to reduced cardiac ef fi ciency in diabetes. Physiology (Bethesda). 2006;21:250-8.
22. Bugger H, Abel ED. Molecular mechanisms for myocardial mitochondrial dysfunction in the metabolic syndrome. Clin Sci (Lond). 2008;114(3):195-210.
23. Halestrap AP. What is the mitochondrial permeability transition pore? J Mol Cell Cardiol. 2009;46(6):821-31.
24. Kokoszka JE, Waymire KG, Levy SE, et al. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature. 2004;427(6973):461-5.
25. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol. 2007;9(5):550-5.
26. Baines CP, Kaiser RA, Purcell NH, et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature. 2005;434(7033):658-62.
27. Bernardi P, Krauskopf A, Basso E, et al. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J. 2006;273(10):2077-99.
28. Halestrap AP. A pore way to die: the role of mitochondria in reperfusion injury and cardioprotection. Biochem Soc Trans. 2010;38(4):841-60.
29. Di Lisa F, Carpi A, Giorgio V, Bernardi P. The mitochondrial permeability transition pore and cyclophilin D in cardioprotection. Biochim Biophys Acta. 2011;1813(7):1316-22.
30. Penna C, Mancardi D, Rastaldo R, Pagliaro P. Cardioprotection: a radical view Free radicals in pre and postconditioning. Biochim Biophys Acta. 2009;1787(7):781-93.
31. Carreira RS, Lee Y, Ghochani M, Gustafsson AB, Gottlieb RA. Cyclophilin D is required for mitochondrial removal by autophagy in cardiac cells. Autophagy. 2010;6(4):462-72.
32. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 2000;102(1):33-42.
33. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 1996;86(1):147-57.
34. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Mol Cell. 2010;37(3):299-310.
35. Rasola A, Sciacovelli M, Pantic B, Bernardi P. Signal transduction to the permeability transition pore. FEBS Lett. 2010;584(10):1989-96.
36. Brady NR, Hamacher-Brady A, Gottlieb RA. Proapoptotic BCL-2 family members and mitochondrial dysfunction during ischemia/reperfusion injury, a study employing cardiac HL-1 cells and GFP biosensors. Biochim Biophys Acta. 2006;1757(5-6):667-78.
37. Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta. 2006;1757(5-6):509-17.
38. Dhalla NS, Temsah RM, Netticadan T. Role of oxidative stress in cardiovascular diseases. J Hypertens. 2000;18(6):655-73.
39. Baines CP. The mitochondrial permeability transition pore and ischemia-reperfusion injury. Basic Res Cardiol. 2009;104(2):181-8.
40. Di Lisa F, Canton M, Menabo R, Kaludercic N, Bernardi P. Mitochondria and cardioprotection. Heart Fail Rev. 2007;12(3-4):249-60.
41. Cadenas S, Aragones J, Landazuri MO. Mitochondrial reprogramming through cardiac oxygen sensors in ischaemic heart disease. Cardiovasc Res. 2010;88(2):219-28.
42. Halestrap AP, Pasdois P. The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta. 2009;1787(11):1402-15.
43. Crow MT, Mani K, Nam YJ, Kitsis RN. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res. 2004;95(10):957-70.
44. Minatoguchi S, Kariya T, Uno Y, et al. Caspase-dependent and serine protease-dependent DNA fragmentation of myocytes in the ischemia-reperfused rabbit heart: these inhibitors do not reduce infarct size. Jpn Circ J. 2001;65(10):907-11.
45. Halestrap AP. Mitochondria and reperfusion injury of the heart-a holey death but not beyond salvation. J Bioenerg Biomembr. 2009;41(2):113-21.
46. Hausenloy DJ, Lim SY, Ong SG, Davidson SM, Yellon DM. Mitochondrial cyclophilin-D as a critical mediator of ischaemic preconditioning. Cardiovasc Res. 2010;88(1):67-74.
47. Clarke SJ, McStay GP, Halestrap AP. Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J Biol Chem. 2002;277(38):34793-9.
48. Halestrap AP, Clarke SJ, Javadov SA. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res. 2004;61(3): 372-85.
49. Argaud L, Gateau-Roesch O, Muntean D, et al. Speci fi c inhibition of the mitochondrial permeability transition prevents lethal reperfusion injury. J Mol Cell Cardiol. 2005;38(2):367-74.
50. Xie JR, Yu LN. Cardioprotective effects of cyclosporine A in an in vivo model of myocardial ischemia and reperfusion. Acta Anaesthesiol Scand. 2007;51(7):909-13.
51. Piot C, Croisille P, Staat P, et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med. 2008;359(5):473-81.
52. Hausenloy DJ, Yellon DM. Preconditioning and postconditioning: underlying mechanisms and clinical application. Atherosclerosis. 2009;204(2):334-41.
53. Granfeldt A, Lefer DJ, Vinten-Johansen J. Protective ischaemia in patients: preconditioning and postconditioning. Cardiovasc Res. 2009;83(2):234-46.
54. Peart JN, Headrick JP. Clinical cardioprotection and the value of conditioning responses. Am J Physiol Heart Circ Physiol. 2009;296(6):H1705-20.
55. Lim SY, Davidson SM, Hausenloy DJ, Yellon DM. Preconditioning and postconditioning: the essential role of the mitochondrial permeability transition pore. Cardiovasc Res. 2007;75(3): 530-5.
56. Takeda K, Yoshida T, Kikuchi S, et al. Synergistic roles of the proteasome and autophagy for mitochondrial maintenance and chronological lifespan in fi ssion yeast. Proc Natl Acad Sci USA. 2010;107(8):3540-5.
57. Sandoval H, Thiagarajan P, Dasgupta SK, et al. Essential role for Nix in autophagic maturation of erythroid cells. Nature. 2008;454(7201):232-5.
58. Zhang H, Bosch-Marce M, Shimoda LA, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 2008;283(16):10892-903.
59. Hamacher-Brady A, Brady NR, Logue SE, et al. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ. 2007;14(1):146-57.
60. Novak I, Kirkin V, McEwan DG, et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010;11(1):45-51.
61. Geisler S, Holmstrom KM, Skujat D, et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol. 2010;12(2):119-31.
62. Dagda RK, Cherra III SJ, Kulich SM, Tandon A, Park D, Chu CT. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fi ssion. J Biol Chem. 2009;284(20):13843-55.
63. Kitada T, Asakawa S, Hattori N, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 1998;392(6676):605-8.
64. Valente EM, Abou-Sleiman PM, Caputo V, et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science. 2004;304(5674):1158-60.
65. Vives-Bauza C, Zhou C, Huang Y, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci USA. 2010;107(1):378-83.
66. Pankiv S, Clausen TH, Lamark T, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282(33): 24131-45.
67. Lee JY, Nagano Y, Taylor JP, Lim KL, Yao TP. Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J Cell Biol. 2010;189(4):671-9.
68. Huang C, Yitzhaki S, Perry CN, et al. Autophagy induced by ischemic preconditioning is essential for cardioprotection. J Cardiovasc Transl Res. 2010;3(4):365-73.
69. Huang C, Andres AM, Ratliff EP, Hernandez G, Lee P, Gottlieb RA. Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS One. 2011;6(6):e20975.
70. Rakovic A, Grunewald A, Kottwitz J, et al. Mutations in PINK1 and Parkin impair ubiquitination of Mitofusins in human fi broblasts. PLoS One. 2011;6(3):e16746.
71. Yoshii SR, Kishi C, Ishihara N, Mizushima N. Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J Biol Chem. 2011;286(22): 19630-40.
72. Chan NC, Salazar AM, Pham AH, et al. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet. 2011;20(9):1726-37.
73. Kapelko VI, Lakomkin VL, Korchazhkina OV, Pisarenko OI. Cardiac pump function of the isolated rat heart at two modes of energy deprivation and effect of adrenergic stimulation. Mol Cell Biochem. 1996;163-164:131-6.
74. Scarpulla RC. Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann N Y Acad Sci. 2008;1147:321-34.
75. Rowe GC, Jiang A, Arany Z. PGC-1 coactivators in cardiac development and disease. Circ Res. 2010;107(7):825-38.
76. Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev. 2008;88(2):611-38.
77. Wende AR, Schaeffer PJ, Parker GJ, et al. A role for the transcriptional coactivator PGC- 1alpha in muscle refueling. J Biol Chem. 2007;282(50):36642-51.
78. Jeninga EH, Schoonjans K, Auwerx J. Reversible acetylation of PGC-1: connecting energy sensors and effectors to guarantee metabolic fl exibility. Oncogene. 2010;29(33):4617-24.
79. Iwabu M, Yamauchi T, Okada-Iwabu M, et al. Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1. Nature. 2010;464(7293):1313-9.
80. Sengupta A, Molkentin JD, Yutzey KE. FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem. 2009;284(41):28319-31.
81. Shin JH, Ko HS, Kang H, et al. PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell. 2011;144(5):689-702.
82. Crescenzo R, Lionetti L, Mollica MP, et al. Altered skeletal muscle subsarcolemmal mitochondrial compartment during catch-up fat after caloric restriction. Diabetes. 2006;55(8):2286-93.
83. Lo MC, Lu CI, Chen MH, Chen CD, Lee HM, Kao SH. Glycoxidative stress-induced mitophagy modulates mitochondrial fates. Ann N Y Acad Sci. 2010;1201:1-7.
84. Taneike M, Yamaguchi O, Nakai A, et al. Inhibition of autophagy in the heart induces agerelated cardiomyopathy. Autophagy. 2010;6(5):600-06.
85. Nakai A, Yamaguchi O, Takeda T, et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med. 2007;13(5):619-24.
86. Smirnova E, Griparic L, Shurland DL, van der Bliek AM. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell. 2001;12(8):2245-56.
87. Yoon Y, Krueger EW, Oswald BJ, McNiven MA. The mitochondrial protein hFis1 regulates mitochondrial fi ssion in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol. 2003;23(15):5409-20.
88. Ingerman E, Perkins EM, Marino M, et al. Dnm1 forms spirals that are structurally tailored to fi t mitochondria. J Cell Biol. 2005;170(7):1021-7.
89. Koshiba T, Detmer SA, Kaiser JT, Chen H, McCaffery JM, Chan DC. Structural basis of mitochondrial tethering by mitofusin complexes. Science. 2004;305(5685):858-62.
90. Cipolat S, Martins de Brito O, Dal Zilio B, Scorrano L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci USA. 2004;101(45):15927-32.
91. Okamoto K, Shaw JM. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu Rev Genet. 2005;39:503-36.
92. Twig G, Elorza A, Molina AJ, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008;27(2):433-46.
93. Karbowski M, Norris KL, Cleland MM, Jeong SY, Youle RJ. Role of Bax and Bak in mitochondrial morphogenesis. Nature. 2006;443(7112):658-62.
94. Sheridan C, Delivani P, Cullen SP, Martin SJ. Bax- or Bak-induced mitochondrial fi ssion can be uncoupled from cytochrome C release. Mol Cell. 2008;31(4):570-85.
95. Berman SB, Chen YB, Qi B, et al. Bcl-x L increases mitochondrial fi ssion, fusion, and biomass in neurons. J Cell Biol. 2009;184(5):707-19.
96. Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum Mol Genet. 2010;19(24):4861-70.
97. Tanaka A, Cleland MM, Xu S, et al. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol. 2011;191(7):1367-80.
98. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: signi fi cance for the molecular mechanism of Bcl-2 action. EMBO J. 2001;20(11):2690-701.
99. Jagasia R, Grote P, Westermann B, Conradt B. DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death in C. elegans. Nature. 2005;433(7027):754-60.
100. Nakamura T, Lipton SA. Redox regulation of mitochondrial fi ssion, protein misfolding, synaptic damage, and neuronal cell death: potential implications for Alzheimer's and Parkinson's diseases. Apoptosis. 2010;15(11):1354-63.
101. Chen L, Gong Q, Stice JP, Knowlton AA. Mitochondrial OPA1, apoptosis, and heart failure. Cardiovasc Res. 2009;84(1):91-9.
102. Ong SB, Subrayan S, Lim SY, Yellon DM, Davidson SM, Hausenloy DJ. Inhibiting mitochondrial fi ssion protects the heart against ischemia/reperfusion injury. Circulation. 2010;121(18):2012-22.
103. Dorn 2nd GW, Clark CF, Eschenbacher WH, et al. MARF and Opa1 control mitochondrial and cardiac function in Drosophila. Circ Res. 2011;108(1):12-7.
104. Terman A, Brunk UT. The aging myocardium: roles of mitochondrial damage and lysosomal degradation. Heart Lung Circ. 2005;14(2):107-14.
105. Gomes LC, Di Benedetto G, Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol. 2011;13(5):589-98.
106. Hansen M, Chandra A, Mitic LL, Onken B, Driscoll M, Kenyon C. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 2008;4(2):e24.
107. Partridge L, Alic N, Bjedov I, Piper MD. Ageing in Drosophila: the role of the insulin/Igf and TOR signalling network. Exp Gerontol. 2011;46(5):376-81.
108. Yang L, Li P, Fu S, Calay ES, Hotamisligil GS. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 2010;11(6):467-78.
109. Przyklenk K, Maynard M, Greiner DL, Whittaker P. Cardioprotection with postconditioning: loss of ef fi cacy in murine models of type-2 and type-1 diabetes. Antioxid Redox Signal. 2010;14(5):781-90.
110. Kupai K, Csonka C, Fekete V, et al. Cholesterol diet-induced hyperlipidemia impairs the cardioprotective effect of postconditioning: role of peroxynitrite. Am J Physiol Heart Circ Physiol. 2009;297(5):H1729-35.
111. Benjamin IJ, Guo Y, Srinivasan S, et al. CRYAB and HSPB2 Deficiency alters cardiac metabolism and paradoxically confers protection against myocardial ischemia in aging mice. Am J Physiol Heart Circ Physiol. 2007;293(5):H3201-9.
112. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation. 2007;115(25):3213-23.
113. Bugger H, Abel ED. Rodent models of diabetic cardiomyopathy. Dis Model Mech. 2009; 2(9-10):454-66.
114. Abel ED, Litwin SE, Sweeney G. Cardiac remodeling in obesity. Physiol Rev. 2008;88(2): 389-419.
115. Bugger H, Abel ED. Mitochondria in the diabetic heart. Cardiovasc Res. 2010;88(2):229-40.
116. Boudina S, Sena S, Theobald H, et al. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes. 2007;56(10):2457-66.
117. Bugger H, Chen D, Riehle C, et al. Tissue-speci fi c remodeling of the mitochondrial proteome in type 1 diabetic akita mice. Diabetes. 2009;58(9):1986-97.
118. Boudina S, Sena S, O'Neill BT, Tathireddy P, Young ME, Abel ED. Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation. 2005;112(17):2686-95.
119. Wende AR, Abel ED. Lipotoxicity in the heart. Biochim Biophys Acta. 2010;1801(3): 311-9.
120. Duncan JG, Fong JL, Medeiros DM, Finck BN, Kelly DP. Insulin-resistant heart exhibits a mitochondrial biogenic response driven by the peroxisome proliferator-activated receptoralpha/ PGC-1alpha gene regulatory pathway. Circulation. 2007;115(7):909-17.
121. Ye G, Metreveli NS, Donthi RV, et al. Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes. 2004;53(5):1336-43.
122. Shen X, Zheng S, Metreveli NS, Epstein PN. Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes. 2006;55(3):798-805.
123. O'Neill BT, Kim J, Wende AR, et al. A conserved role for phosphatidylinositol 3-kinase but not Akt signaling in mitochondrial adaptations that accompany physiological cardiac hypertrophy. Cell Metab. 2007;6(4):294-306.
124. Kim J, Wende AR, Sena S, et al. Insulin-like growth factor I receptor signaling is required for exercise-induced cardiac hypertrophy. Mol Endocrinol. 2008;22(11):2531-43.
125. Boudina S, Bugger H, Sena S, et al. Contribution of impaired myocardial insulin signaling to mitochondrial dysfunction and oxidative stress in the heart. Circulation. 2009;119(9): 1272-83.
126. Laustsen PG, Russell SJ, Cui L, et al. Essential role of insulin and insulin-like growth factor 1 receptor signaling in cardiac development and function. Mol Cell Biol. 2007;27(5):1649-64.
127. Abel ED, Doenst T. Mitochondrial adaptations to physiological vs. pathological cardiac hypertrophy. Cardiovasc Res. 2011;90(2):234-42.
128. Doenst T, Pytel G, Schrepper A, et al. Decreased rates of substrate oxidation ex vivo predict the onset of heart failure and contractile dysfunction in rats with pressure overload. Cardiovasc Res. 2010;86(3):461-70.
129. Riehle C, Wende AR, Zaha VG, et al. PGC-1(beta) Deficiency Accelerates the Transition to Heart Failure in Pressure Overload Hypertrophy. Circ Res. 2011;109(7):783-93.
130. Arany Z, Novikov M, Chin S, Ma Y, Rosenzweig A, Spiegelman BM. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc Natl Acad Sci USA. 2006;103(26):10086-91.
131. Saini-Chohan HK, Holmes MG, Chicco AJ, et al. Cardiolipin biosynthesis and remodeling enzymes are altered during development of heart failure. J Lipid Res. 2009;50(8):1600-8.
132. Houtkooper RH, Vaz FM. Cardiolipin, the heart of mitochondrial metabolism. Cell Mol Life Sci. 2008;65(16):2493-506.
133. Lu Z, Xu X, Hu X, et al. PGC-1 alpha regulates expression of myocardial mitochondrial antioxidants and myocardial oxidative stress after chronic systolic overload. Antioxid Redox Signal. 2010;13(7):1011-22.
134. Karamanlidis G, Nascimben L, Couper GS, Shekar PS, del Monte F, Tian R. Defective DNA replication impairs mitochondrial biogenesis in human failing hearts. Circ Res. 2010;106(9):1541-8.
135. Shiojima I, Sato K, Izumiya Y, et al. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest. 2005;115(8): 2108-18.