Cardiac mitochondrial proteome dynamics with heavy water reveals stable rate of mitochondrial protein synthesis in heart failure despite decline in mitochondrial oxidative capacity

Journal of Molecular and Cellular Cardiology

Volumn 75, Issue , 2014, Pages 88-97

  Shekar, Kadambari Chandra ^a   Li, Ling ^b   Dabkowski, Erinne R ^a   Xu, Wenhong ^a   Ribeiro, Rogerio Faustino ^a   Hecker, Peter A ^a   Recchia, Fabio A ^c,d   Sadygov, Rovshan G ^e   Willard, Belinda ^b   Kasumov, Takhar ^b   Stanley, William C ^a,f  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SCUOLA SUPERIORE SANT ANNA   (Italy)

^e University of Texas Medical Branch School of Medicine   (United States)

^f UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cardiac failure; Deuterium; Mitochondria; Proteome dynamics

Indexed keywords

ADENOSINE TRIPHOSPHATE; DEUTERIUM OXIDE; MITOCHONDRIAL PROTEIN; PROTEOME; PYRUVATE DEHYDROGENASE; CITRATE SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; BRAIN MITOCHONDRION; CELL ISOLATION; CELL SUBPOPULATION; CONTROLLED STUDY; DISEASE SEVERITY; FATTY ACID OXIDATION; GEL ELECTROPHORESIS; HEART FAILURE; INTERFIBRILLAR MITOCHONDRION; MALE; MASS SPECTROMETRY; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL RESPIRATION; NONHUMAN; PROTEIN CONTENT; PROTEIN METABOLISM; PROTEIN SYNTHESIS; RAT; RESPIRATORY CHAIN; SUBSARCOLEMMA MITOCHONDRION; ANIMAL; BIOSYNTHESIS; BODY WEIGHT; CELL RESPIRATION; HALF LIFE TIME; HEART MITOCHONDRION; HEART VENTRICLE; METABOLISM; ORGAN SIZE; OXIDATION REDUCTION REACTION; PATHOLOGY; PATHOPHYSIOLOGY; PRESSURE; PROTEIN STABILITY; SARCOLEMMA; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; BODY WEIGHT; CELL RESPIRATION; CITRATE (SI)-SYNTHASE; DEUTERIUM OXIDE; HALF-LIFE; HEART FAILURE; HEART VENTRICLES; MALE; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTEINS; ORGAN SIZE; OXIDATION-REDUCTION; PRESSURE; PROTEIN BIOSYNTHESIS; PROTEIN STABILITY; PROTEOME; RATS, SPRAGUE-DAWLEY; SARCOLEMMA;

EID: 84916635071     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.06.014     Document Type: Article

References (49)

1. 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. J Physiol 2003, 551:491-501.
2. Bugger H., Schwarzer M., Chen D., Schrepper A., Amorim P.A., Schoepe M., et al. Proteomic remodelling of mitochondrial oxidative pathways in pressure overload-induced heart failure. Cardiovasc Res 2010, 85:376-384.
3. Sabbah H.N., Sharov V., Riddle J.M., Kono T., Lesch M., Goldstein S. Mitochondrial abnormalities in myocardium of dogs with chronic heart failure. J Mol Cell Cardiol 1992, 24:1333-1347.
4. Schwarzer M., Schrepper A., Amorim P.A., Osterholt M., Doenst T. Pressure overload differentially affects respiratory capacity in interfibrillar and subsarcolemmal mitochondria. Am J Physiol Heart Circ Physiol 2013, 304:H529-H537.
5. Rachdaoui N., Austin L., Kramer E., Previs M.J., Anderson V.E., Kasumov T., et al. Measuring proteome dynamics in vivo: as easy as adding water?. Mol Cell Proteomics 2009, 8:2653-2663.
6. Li L., Willard B., Rachdaoui N., Kirwan J.P., Sadygov R.G., Stanley W.C., et al. Plasma proteome dynamics: analysis of lipoproteins and acute phase response proteins with 2H2O metabolic labeling. Mol Cell Proteomics 2012, 11. [M111 014209].
7. Price J.C., Holmes W.E., Li K.W., Floreani N.A., Neese R.A., Turner S.M., et al. Measurement of human plasma proteome dynamics with (2)H(2)O and liquid chromatography tandem mass spectrometry. Anal Biochem 2012, 420:73-83.
8. Kim T.Y., Wang D., Kim A.K., Lau E., Lin A.J., Liem D.A., et al. Metabolic labeling reveals proteome dynamics of mouse mitochondria. Mol Cell Proteomics 2012, 11:1586-1594.
9. Kasumov T., Dabkowski E.R., Shekar K.C., Li L., Ribeiro R.F., Walsh K., et al. Assessment of cardiac proteome dynamics with heavy water: slower protein synthesis rates in interfibrillar than subsarcolemmal mitochondria. Am J Physiol Heart Circ Physiol 2013, 304:H1201-H1214.
10. Lesnefsky E.J., Moghaddas S., Tandler B., Kerner J., Hoppel C.L. Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol 2001, 33:1065-1089.
11. Hofer T., Servais S., Seo A.Y., Marzetti E., Hiona A., Upadhyay S.J., et al. Bioenergetics and permeability transition pore opening in heart subsarcolemmal and interfibrillar mitochondria: effects of aging and lifelong calorie restriction. Mech Ageing Dev 2009, 130:297-307.
12. Williamson C.L., Dabkowski E.R., Baseler W.A., Croston T.L., Alway S.E., Hollander J.M. Enhanced apoptotic propensity in diabetic cardiac mitochondria: influence of subcellular spatial location. Am J Physiol Heart Circ Physiol 2010, 298:H633-H642.
13. Judge S., Jang Y.M., Smith A., Hagen T., Leeuwenburgh C. Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J 2005, 19:419-421.
14. Asemu G., O'Connell K.A., Cox J.W., Dabkowski E.R., Xu W., Ribeiro R.F., et al. Enhanced resistance to permeability transition in interfibrillar cardiac mitochondria in dogs: effects of aging and long-term aldosterone infusion. Am J Physiol Heart Circ Physiol 2013, 304:H514-H528.
15. Dabkowski E.R., Baseler W.A., Williamson C.L., Powell M., Razunguzwa T.T., Frisbee J.C., et al. Mitochondrial dysfunction in the type 2 diabetic heart is associated with alterations in spatially distinct mitochondrial proteomes. Am J Physiol Heart Circ Physiol 2010, 299:H529-H540.
16. Hoppel C.L., Tandler B., Parland W., Turkaly J.S., Albers L.D. Hamster cardiomyopathy. A defect in oxidative phosphorylation in the cardiac interfibrillar mitochondria. J Biol Chem 1982, 257:1540-1548.
17. Galvao T.F., Khairallah R.J., Dabkowski E.R., Brown B.H., Hecker P.A., O'Connell K.A., et al. Marine n3 polyunsaturated fatty acids enhance resistance to mitochondrial permeability transition in heart failure but do not improve survival. Am J Physiol Heart Circ Physiol 2013, 304:H12-H21.
18. Galvao T.F., Brown B.H., Hecker P.A., O'Connell K.A., O'Shea K.M., Sabbah H.N., et al. High intake of saturated fat, but not polyunsaturated fat, improves survival in heart failure despite persistent mitochondrial defects. Cardiovasc Res 2012, 93:24-32.
19. Dabkowski E.R., O'Connell K.A., Xu W., Ribeiro R.F., Hecker P.A., Shekar K.C., et al. Docosahexaenoic acid supplementation alters key properties of cardiac mitochondria and modestly attenuates development of left ventricular dysfunction in pressure overload-induced heart failure. Cardiovasc Drugs Ther 2013, 27:499-510.
20. Zaha V., Grohmann J., Gobel H., Geibel A., Beyersdorf F., Doenst T. Experimental model for heart failure in rats-induction and diagnosis. Thorac Cardiovasc Surg 2003, 51:211-215.
21. Duda M.K., O'Shea K.M., Tintinu A., Xu W., Khairallah R.J., Barrows B.R., et al. Fish oil, but not flaxseed oil, decreases inflammation and prevents pressure overload-induced cardiac dysfunction. Cardiovasc Res 2009, 81:319-327.
22. Palmer J.W., Tandler B., Hoppel C.L. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 1977, 252:8731-8739.
23. Kerner J., Minkler P.E., Lesnefsky E.J., Hoppel C.L. Fatty acid chain elongation in palmitate-perfused working rat heart: mitochondrial acetyl-CoA is the source of two-carbon units for chain elongation. J Biol Chem 2014, 289:10223-10234.
24. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
25. Khairallah R.J., O'Shea K.M., Brown B.H., Khanna N., Des Rosiers C., Stanley W.C. Treatment with docosahexaenoic acid, but not eicosapentaenoic acid, delays Ca2+-induced mitochondria permeability transition in normal and hypertrophied myocardium. J Pharmacol Exp Ther 2010, 335:155-162.
26. O'Shea K.M., Khairallah R.J., Sparagna G.C., Xu W., Hecker P.A., Robillard-Frayne I., et al. Dietary omega-3 fatty acids alter cardiac mitochondrial phospholipid composition and delay Ca2+-induced permeability transition. J Mol Cell Cardiol 2009, 47:819-827.
27. Panchal A.R., Stanley W.C., Kerner J., Sabbah H.N. Beta-receptor blockade decreases carnitine palmitoyl transferase I activity in dogs with heart failure. J Card Fail 1998, 4:121-126.
28. Price J.C., Khambatta C.F., Li K.W., Bruss M.D., Shankaran M., Dalidd M., et al. The effect of long term calorie restriction on in vivo hepatic proteostatis: a novel combination of dynamic and quantitative proteomics. Mol Cell Proteomics 2012, 11:1801-1814.
29. Doherty M.K., Hammond D.E., Clague M.J., Gaskell S.J., Beynon R.J. Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J Proteome Res 2009, 8:104-112.
30. Gonda D.K., Bachmair A., Wunning I., Tobias J.W., Lane W.S., Varshavsky A. Universality and structure of the N-end rule. J Biol Chem 1989, 264:16700-16712.
31. Dice J.F. Molecular determinants of protein half-lives in eukaryotic cells. FASEB J 1987, 1:349-357.
32. Stanley W.C., Recchia F.A., Lopaschuk G.D. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 2005, 85:1093-1129.
33. Lesnefsky E.J., Gudz T.I., Moghaddas S., Migita C.T., Ikeda-Saito M., Turkaly P.J., et al. Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site. J Mol Cell Cardiol 2001, 33:37-47.
34. Dai D.F., Hsieh E.J., Liu Y., Chen T., Beyer R.P., Chin M.T., et al. Mitochondrial proteome remodelling in pressure overload-induced heart failure: the role of mitochondrial oxidative stress. Cardiovasc Res 2012, 93:79-88.
35. Kasumov T., Willard B., Li L., Li M., Conger H., Buffa J.A., et al. 2H2O-based high-density lipoprotein turnover method for the assessment of dynamic high-density lipoprotein function in mice. Arterioscler Thromb Vasc Biol 2013, 33:1994-2003.
36. Osorio J.C., Stanley W.C., Linke A., Castellari M., Diep Q.N., Panchal A.R., et al. Impaired myocardial fatty acid oxidation and reduced protein expression of retinoid X receptor-alpha in pacing-induced heart failure. Circulation 2002, 106:606-612.
37. Rosca M.G., Hoppel C.L. Mitochondrial dysfunction in heart failure. Heart Fail Rev 2013, 18:607-622.
38. Rosca M.G., Vazquez E.J., Kerner J., Parland W., Chandler M.P., Stanley W., et al. Cardiac mitochondria in heart failure: decrease in respirasomes and oxidative phosphorylation. Cardiovasc Res 2008, 80:30-39.
39. Riehle C., Wende A.R., Zaha V.G., Pires K.M., Wayment B., Olsen C., et al. PGC-1beta deficiency accelerates the transition to heart failure in pressure overload hypertrophy. Circ Res 2011, 109:783-793.
40. Martin O.J., Lai L., Soundarapandian M.M., Leone T.C., Zorzano A., Keller M.P., et al. A role for peroxisome proliferator-activated receptor gamma coactivator-1 in the control of mitochondrial dynamics during postnatal cardiac growth. Circ Res 2014, 114:626-636.
41. Lehman J.J., Barger P.M., Kovacs A., Saffitz J.E., Medeiros D.M., Kelly D.P. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 2000, 106:847-856.
42. Lai L., Leone T.C., Zechner C., Schaeffer P.J., Kelly S.M., Flanagan D.P., et al. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev 2008, 22:1948-1961.
43. Arany Z., Novikov M., Chin S., Ma Y., Rosenzweig A., Spiegelman B.M. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc Natl Acad Sci U S A 2006, 103:10086-10091.
44. Abel E.D., Doenst T. Mitochondrial adaptations to physiological vs pathological cardiac hypertrophy. Cardiovasc Res 2011, 90:234-242.
45. Bursch W., Hochegger K., Torok L., Marian B., Ellinger A., Hermann R.S. Autophagic and apoptotic types of programmed cell death exhibit different fates of cytoskeletal filaments. J Cell Sci 2000, 113(Pt 7):1189-1198.
46. Powell S.R. The ubiquitin-proteasome system in cardiac physiology and pathology. Am J Physiol Heart Circ Physiol 2006, 291:H1-H19.
47. Varshavsky A., Bachmair A., Finley D. The N-end rule of selective protein turnover: mechanistic aspects and functional implications. Biochem Soc Trans 1987, 15:815-816.
48. Tompa P., Prilusky J., Silman I., Sussman J.L. Structural disorder serves as a weak signal for intracellular protein degradation. Proteins 2008, 71:903-909.
49. Lau E., Wang D., Zhang J., Yu H., Lam M.P., Liang X., et al. Substrate- and isoform-specific proteome stability in normal and stressed cardiac mitochondria. Circ Res 2012, 110:1174-1178.