Biphasic response of skeletal muscle mitochondria to chronic cardiac pressure overload - Role of respiratory chain complex activity

Journal of Molecular and Cellular Cardiology

Volumn 52, Issue 1, 2012, Pages 125-135

  Schrepper, Andrea ^a   Schwarzer, Michael ^a   Schöpe, Maria ^b   Amorim, Paulo A ^b   Doenst, Torsten ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Mitochondria; Oxidative capacity; Pressure overload induced heart failure; Skeletal muscle; Timeline

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE);

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; HEART EJECTION FRACTION; HEART FAILURE; HEART LEFT VENTRICLE OVERLOAD; HEART OUTPUT; HEART VENTRICLE HYPERTROPHY; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE ATROPHY; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RESPIRATORY CHAIN; SKELETAL MUSCLE; SOLEUS MUSCLE;

ANIMALS; AORTA; BLOOD PRESSURE; CARDIOMEGALY; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; HEART FAILURE; MALE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84155194899     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.10.022     Document Type: Article

References (44)

1. Ingwall J.S., Weiss R.G. Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ Res 2004, 95:135-145.
2. Neubauer S. The failing heart-an engine out of fuel. N Engl J Med 2007, 356:1140-1151.
3. Doenst T., Pytel G., Schrepper A., Amorim P., Farber G., Shingu Y., 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, 86:461-470.
4. Heather L.C., Carr C.A., Stuckey D.J., Pope S., Morten K.J., Carter E.E., et al. Critical role of complex III in the early metabolic changes following myocardial infarction. Cardiovasc Res 2010, 85:127-136.
5. 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.
6. 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.
7. 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.
8. Srere P. Citrate synthase. Methods Enzymol 1969, 13:3-11.
9. Chance B., Williams G.R. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem 1955, 217:383-393.
10. Estabrook R.W. Mitochondrial respiratory control and the polarigraphic measurement of ADP:O ratios. Methods Enzymol 1967, 10:41-47.
11. Janssen A.J., Trijbels F.J., Sengers R.C., Smeitink J.A., van den Heuvel L.P., Wintjes L.T., et al. Spectrophotometric assay for complex I of the respiratory chain in tissue samples and cultured fibroblasts. Clin Chem 2007, 53:729-734.
12. Krahenbuhl S., Chang M., Brass E.P., Hoppel C.L. Decreased activities of ubiquinol:ferricytochrome c oxidoreductase (complex III) and ferrocytochrome c:oxygen oxidoreductase (complex IV) in liver mitochondria from rats with hydroxycobalamin[c-lactam]-induced methylmalonic aciduria. J Biol Chem 1991, 266:20998-21003.
13. Wharton D.C., Tzagoloff A. Cytochrome oxidase from beef heart mitochondria. Methods Enzymol 1967, 10:245-250.
14. Schwarzer M., Faerber G., Rueckauer T., Blum D., Pytel G., Mohr F.W., et al. The metabolic modulators, Etomoxir and NVP-LAB121, fail to reverse pressure overload induced heart failure in vivo. Basic Res Cardiol 2009, 104:547-557.
15. Schwarzer M., Britton S.L., Koch L.G., Wisloff U., Doenst T. Low intrinsic aerobic exercise capacity and systemic insulin resistance are not associated with changes in myocardial substrate oxidation or insulin sensitivity. Basic Res Cardiol 2010, 105:357-364.
16. Wittig I., Braun H.P., Schagger H. Blue native PAGE. Nat Protoc 2006, 1:418-428.
17. Dalla Libera L., Ravara B., Gobbo V., Betto D.D., Germinario E., Angelini A., et al. Skeletal muscle proteins oxidation in chronic right heart failure in rats: can different beta-blockers prevent it to the same degree?. Int J Cardiol 2010, 143:192-199.
18. Mettauer B., Zoll J., Sanchez H., Lampert E., Ribera F., Veksler V., et al. Oxidative capacity of skeletal muscle in heart failure patients versus sedentary or active control subjects. J Am Coll Cardiol 2001, 38:947-954.
19. 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.
20. Rosca M.G., Okere I.A., Sharma N., Stanley W.C., Recchia F.A., Hoppel C.L. Altered expression of the adenine nucleotide translocase isoforms and decreased ATP synthase activity in skeletal muscle mitochondria in heart failure. J Mol Cell Cardiol 2009, 46:927-935.
21. Simonini A., Long C.S., Dudley G.A., Yue P., McElhinny J., Massie B.M. Heart failure in rats causes changes in skeletal muscle morphology and gene expression that are not explained by reduced activity. Circ Res 1996, 79:128-136.
22. Witte K., Hu K., Swiatek J., Mussig C., Ertl G., Lemmer B. Experimental heart failure in rats: effects on cardiovascular circadian rhythms and on myocardial beta-adrenergic signaling. Cardiovasc Res 2000, 47:350-358.
23. 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.
24. Schon E.A., Dencher N.A. Heavy breathing: energy conversion by mitochondrial respiratory supercomplexes. Cell Metab 2009, 9:1-3.
25. Paradies G., Petrosillo G., Pistolese M., Ruggiero F.M. The effect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart submitochondrial particles. FEBS Lett 2000, 466:323-326.
26. Sparagna G.C., Chicco A.J., Murphy R.C., Bristow M.R., Johnson C.A., Rees M.L., et al. Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure. J Lipid Res 2007, 48:1559-1570.
27. Adhihetty P.J., Uguccioni G., Leick L., Hidalgo J., Pilegaard H., Hood D.A. The role of PGC-1alpha on mitochondrial function and apoptotic susceptibility in muscle. Am J Physiol Cell Physiol 2009, 297:C217-C225.
28. 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.
29. Schreiber S.N., Emter R., Hock M.B., Knutti D., Cardenas J., Podvinec M., et al. The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc Natl Acad Sci USA 2004, 101:6472-6477.
30. Witte K.K., Clark A.L. Why does chronic heart failure cause breathlessness and fatigue?. Prog Cardiovasc Dis 2007, 49:366-384.
31. Drexler H., Riede U., Munzel T., Konig H., Funke E., Just H. Alterations of skeletal muscle in chronic heart failure. Circulation 1992, 85:1751-1759.
32. Garnier A., Fortin D., Zoll J., N'Guessan B., Mettauer B., Lampert E., et al. Coordinated changes in mitochondrial function and biogenesis in healthy and diseased human skeletal muscle. FASEB J 2005, 19:43-52.
33. Miller M.S., Vanburen P., Lewinter M.M., Lecker S.H., Selby D.E., Palmer B.M., et al. Mechanisms underlying skeletal muscle weakness in human heart failure: alterations in single fiber myosin protein content and function. Circ Heart Fail 2009, 2:700-706.
34. Momken I., Kahapip J., Bahi L., Badoual T., Hittinger L., Ventura-Clapier R., et al. Does angiotensin-converting enzyme inhibition improve the energetic status of cardiac and skeletal muscles in heart failure induced by aortic stenosis in rats?. J Mol Cell Cardiol 2003, 35:399-407.
35. Carvalho R.F., Cicogna A.C., Campos G.E., De Assis J.M., Padovani C.R., Okoshi M.P., et al. Myosin heavy chain expression and atrophy in rat skeletal muscle during transition from cardiac hypertrophy to heart failure. Int J Exp Pathol 2003, 84:201-206.
36. Coirault C., Langeron O., Lambert F., Blanc F.X., Lerebours G., Claude N., et al. Impaired skeletal muscle performance in the early stage of cardiac pressure overload in rabbits: beneficial effects of angiotensin-converting enzyme inhibition. J Pharmacol Exp Ther 1999, 291:70-75.
37. Iossa S., Mollica M.P., Lionetti L., Crescenzo R., Tasso R., Liverini G. A possible link between skeletal muscle mitochondrial efficiency and age-induced insulin resistance. Diabetes 2004, 53:2861-2866.
38. Marin-Garcia J., Ananthakrishnan R., Goldenthal M.J. Mitochondrial gene expression in rat heart and liver during growth and development. Biochem Cell Biol 1997, 75:137-142.
39. Vescovo G., Ceconi C., Bernocchi P., Ferrari R., Carraro U., Ambrosio G.B. Skeletal muscle myosin heavy chain expression in rats with monocrotaline-induced cardiac hypertrophy and failure. Relation to blood flow and degree of muscle atrophy. Cardiovasc Res 1998, 39:233-241.
40. Lunde P.K., Sjaastad I., Schiotz Thorud H.M., Sejersted O.M. Skeletal muscle disorders in heart failure. Acta Physiol Scand 2001, 171:277-294.
41. Hambrecht R., Adams V., Gielen S., Linke A., Mobius-Winkler S., Yu J., et al. Exercise intolerance in patients with chronic heart failure and increased expression of inducible nitric oxide synthase in the skeletal muscle. J Am Coll Cardiol 1999, 33:174-179.
42. Massie B.M., Conway M., Rajagopalan B., Yonge R., Frostick S., Ledingham J., et al. Skeletal muscle metabolism during exercise under ischemic conditions in congestive heart failure. Evidence for abnormalities unrelated to blood flow. Circulation 1988, 78:320-326.
43. Minotti J.R., Christoph I., Oka R., Weiner M.W., Wells L., Massie B.M. Impaired skeletal muscle function in patients with congestive heart failure. Relationship to systemic exercise performance. J Clin Invest 1991, 88:2077-2082.
44. Ariano M.A., Armstrong R.B., Edgerton V.R. Hindlimb muscle fiber populations of five mammals. J Histochem Cytochem 1973, 21:51-55.