Regulation of Mitochondrial Respiration in Heart Muscle

  • Ilmo Hassinen
Part of the Advances in Biochemistry in Health and Disease book series (ABHD, volume 2)


Heart muscle with its continual and heavy use of energy is strongly dependent on the most efficient biological energy provider, the process of oxidative phosphorylation, which is responsible for the aerobic conversion and conservation of the combustion energy of fuel substrates to ATP, the universal cellular energy currency. Its key reactions are localized in mitochondria. The myocardial mitochondrion may be regarded as an archetype of its kind and therefore is also a classical experimental model in research on oxidative phosphorylation.


Respiratory Chain Fatty Acid Oxidation Ubiquinone Oxidoreductase Flux Control Coefficient Electron Transfer Flavoprotein 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abrahams JP, Leslie AG, Lutter R, and Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370: 621–628PubMedGoogle Scholar
  2. Ala-Rämi A, Ylihautala M, Ingman P, Hassinen IE (2005) Influence of calcium-induced workload transitions and fatty acid supply on myocardial substrate selection. Metabolism 54: 410–420PubMedGoogle Scholar
  3. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290: 457–465PubMedGoogle Scholar
  4. Anthony G, Reimann A, Kadenbach B (1993) Tissue-specific regulation of bovine heart cytochrome-c oxidase activity by ADP via interaction with subunit VIa. Proc Natl Acad Sci USA 90: 1652–1656PubMedGoogle Scholar
  5. Arnold S, Kadenbach B (1997) Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome-c oxidase. Eur. J Biochem 249: 350–354PubMedGoogle Scholar
  6. Atkinson DE (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7: 4030–4034Google Scholar
  7. Beckmann JD, Frerman FE (1985) Electron-transfer flavoprotein-ubiquinone oxidoreductase from pig liver: purification and molecular, redox, and catalytic properties. Biochemistry 24: 3913–3921PubMedGoogle Scholar
  8. Belke DD, Wang LC, Lopaschuk GD (1998) Acetyl-CoA carboxylase control of fatty acid oxidation in hearts from hibernating Richardson’s ground squirrels. Biochim Biophys Acta 1391: 25–36PubMedGoogle Scholar
  9. Bender E, Kadenbach B (2000) The allosteric ATP-inhibition of cytochrome c oxidase activity is reversibly switched on by cAMP-dependent phosphorylation. FEBS Lett 466: 130–134PubMedGoogle Scholar
  10. Bessman SP, Geiger PJ (1981) Transport of energy in muscle: the phosphorylcreatine shuttle. Science 211: 448–452PubMedGoogle Scholar
  11. Brandt U (1997) Proton-translocation by membrane-bound NADH:ubiquinone-oxidoreductase (complex I) through redox-gated ligand conduction. Biochim Biophys Acta 1318: 79–91PubMedGoogle Scholar
  12. Cabezon E, Arechaga I, Jonathan P, Butler G, Walker JE (2000) Dimerization of bovine F1-ATPase by binding the inhibitor protein, IF1. J Biol Chem 275: 28353–28355PubMedGoogle Scholar
  13. Chance B, Leigh JS Jr, Clark BJ, Maris J, Kent J, Nioka S, Smith D (1985) Control of oxidative metabolism and oxygen delivery in human skeletal muscle: a steady-state analysis of the work/energy cost transfer function. Proc Natl Acad Sci U S A 82: 8384–8388PubMedGoogle Scholar
  14. Channer KS, Channer JL, Campbell MJ, Rees JR (1988) Cardiomyopathy in the Kearns-Sayre syndrome. Br Heart J 59: 486–490PubMedGoogle Scholar
  15. Denton RM, Randle PJ, Bridges BJ, Cooper RH, Kerbey AL, Pask HT, Severson DL, Stansbie D, Whitehouse S (1975) Regulation of mammalian pyruvate dehydrogenase. Mol Cell Biochem 9: 27–53PubMedGoogle Scholar
  16. Dutton PL, Moser CC, Sled VD, Daldal F, Ohnishi T (1998) A reductant-induced oxidation mechanism for complex I. Biochim Biophys Acta 1364: 245–257PubMedGoogle Scholar
  17. Dyck JR, Barr AJ, Barr RL, Kolattukudy PE, Lopaschuk GD (1998) Characterization of cardiac malonyl-CoA decarboxylase and its putative role in regulating fatty acid oxidation. Am J Physiol 275: H2122–H2129PubMedGoogle Scholar
  18. Ehrlich RS, Colman RF (1982) Interrelationships among nucleotide binding sites of pig heart NAD-dependent isocitrate dehydrogenase. J Biol Chem 257: 4769–4774PubMedGoogle Scholar
  19. Feliciello A, Gottesman ME, Avvedimento EV (2005) cAMP-PKA signaling to the mitochondria: protein scaffolds, mRNA and phosphatases. Cell Signal 17: 279–287PubMedGoogle Scholar
  20. Flemming D, Hellwig P, Friedrich T (2003) Involvement of tyrosines 114 and 139 of subunit NuoB in the proton pathway around cluster N2 in Escherichia coli NADH:ubiquinone oxidoreductase. J Biol Chem 278: 3055–3062PubMedGoogle Scholar
  21. Forsander OA (1970) Effects of ethanol on metabolic pathways. In: Tremoliers J, editor. International encyclopedia of paharmacology and therapeutics. New York: Pergamon Press pp. 117–135Google Scholar
  22. Frank V, Kadenbach B (1996) Regulation of the H+/e- stoichiometry of cytochrome c oxidase from bovine heart by intramitochondrial ATP/ADP ratios. FEBS Lett 382: 121–124PubMedGoogle Scholar
  23. Friedrich T, Weiss H (1997) Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules. J Theor Biol 187: 529–540PubMedGoogle Scholar
  24. Garofano A, Zwicker K, Kerscher S, Okun P, Brandt U (2003) Two aspartic acid residues in the PSST-homologous NUKM subunit of complex I from Yarrowia lipolytica are essential for catalytic activity. J Biol Chem 278: 42435–42440PubMedGoogle Scholar
  25. Green DW, Murray HN, Sleph PG, Wang FL, Baird AJ, Rogers WL, Grover GJ (1998) Preconditioning in rat hearts is independent of mitochondrial F1F0 ATPase inhibition. Am J Physiol 274: H90–H97PubMedGoogle Scholar
  26. Griffiths EJ, Halestrap AP (1993) Pyrophosphate metabolism in the perfused heart and isolated heart mitochondria and its role in regulation of mitochondrial function by calcium. Biochem J 290: 489–495PubMedGoogle Scholar
  27. Groen AK, Wanders RJ, Westerhoff HV, Van der MR, Tager JM (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257: 2754–2757Google Scholar
  28. Guenebaut V, Schlitt A, Weiss H, Leonard K, Friedrich T (1998) Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 276: 105–112PubMedGoogle Scholar
  29. Gupte SS, Hackenbrock CR (1988) Multidimensional diffusion modes and collision frequencies of cytochrome c with its redox partners. J Biol Chem 263: 5241–5247PubMedGoogle Scholar
  30. Hassinen I, Ito K, Nioka S, Chance B (1990) Mechanism of fatty acid effect on myocardial oxygen consumption. A phosphorus NMR study. Biochim Biophys Acta 1019: 73–80PubMedGoogle Scholar
  31. Hassinen IE (1986) Mitochondrial respiratory control in the myocardium. Biochim Biophys Acta 853: 135–151PubMedGoogle Scholar
  32. Hassinen IE, Hiltunen K (1975) Respiratory control in isolated perfused rat heart. Role of the equilibrium relations between the mitochondrial electron carriers and the adenylate system. Biochim Biophys Acta 408: 319–330PubMedGoogle Scholar
  33. Hassinen IE, Vuokila PT (1993) Reaction of dicyclohexylcarbodiimide with mitochondrial proteins. Biochim Biophys Acta 1144: 107–124PubMedGoogle Scholar
  34. Heineman FW, Balaban RS (1990) Control of mitochondrial respiration in the heart in vivo. Ann Rev Physiol 52: 523–542Google Scholar
  35. Holt PJ, Morgan DJ, Sazanov LA (2003) The location of NuoL and NuoM subunits in the membrane domain of the Escherichia coli complex I: implications for the mechanism of proton pumping. J Biol Chem 278: 43114–43120PubMedGoogle Scholar
  36. Honkakoski PJ, Hassinen IE (1986) Sensitivity to NN’-dicyclohexylcarbodi-imide of proton translocation by mitochondrial NADH:ubiquinone oxidoreductase. Biochem J 237: 927–930PubMedGoogle Scholar
  37. Houstek J, Cannon B, Lindberg O (1975) Glycerol-3-phosphate shuttle and its function in intermediary metabolism of hamster brown-adipose tissue. Eur J Biochem 54: 11–18PubMedGoogle Scholar
  38. Iwata S, Lee JW, Okada K, Lee JK, Iwata M, Rasmussen B, Link TA, Ramaswamy S, Jap BK (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281: 64–71PubMedGoogle Scholar
  39. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376: 660–669PubMedGoogle Scholar
  40. Jeneson JA, Wiseman RW, Westerhoff HV, Kushmerick MJ (1996) The signal transduction function for oxidative phosphorylation is at least second order in ADP. J Biol Chem 271: 27995–27998PubMedGoogle Scholar
  41. Kacser H (1983) The control of enzyme systems in vivo: elasticity analysis of the steady state. Biochem Soc Trans 11: 35–40PubMedGoogle Scholar
  42. Kacser H, Burns JA (1973) The control of flux. Symp Soc Exp Biol 27: 65–104PubMedGoogle Scholar
  43. Kato-Yamada Y, Noji H, Yasuda R, Kinosita K Jr, Yoshida M (1998) Direct observation of the rotation of epsilon subunit in F1-ATPase. J Biol Chem 273: 19375–19377PubMedGoogle Scholar
  44. Katz LA, Swain JA, Portman MA, Balaban RS (1989) Relation between phosphate metabolites and oxygen consumption of heart in vivo. Am J Physiol 256: H265–H274PubMedGoogle Scholar
  45. Kauppinen RA, Hiltunen JK, Hassinen IE (1980) Subcellular distribution of phosphagens in isolated perfused rat heart. FEBS Lett 112: 273–276PubMedGoogle Scholar
  46. Kauppinen RA, Hiltunen JK, Hassinen IE (1983) Mitochondrial membrane potential, transmembrane difference in the NAD+ redox potential and the equilibrium of the glutamate-aspartate translocase in the isolated perfused rat heart. Biochim Biophys Acta 725: 425–433PubMedGoogle Scholar
  47. Kervinen M, Patsi J, Finel M, Hassinen IE (2004) A pair of membrane-embedded acidic residues in the NuoK subunit of Escherichia coli NDH-1, a counterpart of the ND4L subunit of the mitochondrial complex I, are required for high ubiquinone reductase activity. Biochemistry 43: 773–781PubMedGoogle Scholar
  48. Klingenberg M (1970) Localization of the glycerol-phosphate dehydrogenase in the outer phase of the mitochondrial inner membrane. Eur J Biochem 13: 247–252PubMedGoogle Scholar
  49. Kornberg H (1966) Anaplerotic sequences and their role in metabolism. Essays Biochem 1–31Google Scholar
  50. Korzeniewski B (1998) Regulation of ATP supply during muscle contraction: theoretical studies. Biochem J 330: 1189–1195PubMedGoogle Scholar
  51. Korzeniewski B, Mazat JP (1996) Theoretical studies on the control of oxidative phosphorylation in muscle mitochondria: application to mitochondrial deficiencies. Biochem J 319: 143–148PubMedGoogle Scholar
  52. Korzeniewski B, Noma A, Matsuoka S (2005) Regulation of oxidative phosphorylation in intact mammalian heart in vivo. Biophys Chem 116: 145–157PubMedGoogle Scholar
  53. Kupriyanov VV, Ya SA, Ruuge EK, Kapel’ko VI, Yu ZM, Lakomkin VL, Smirnov VN, Saks VA (1984) Regulation of energy flux through the creatine kinase reaction in vitro and in perfused rat heart. 31P-NMR studies. Biochim Biophys Acta 805: 319–331Google Scholar
  54. Kurki S, Zickermann V, Kervinen M, Hassinen I, Finel M (2000). Mutagenesis of three conserved Glu residues in a bacterial homologue of the ND1 subunit of complex I affects ubiquinone reduction kinetics but not inhibition by dicyclohexylcarbodiimide. Biochemistry 39: 13496–13502PubMedGoogle Scholar
  55. LaNoue KF, Williamson JR (1971) Interrelationships between malate-aspartate shuttle and citric acid cycle in rat heart mitochondria. Metabolism 20: 119–140PubMedGoogle Scholar
  56. Lardy HA, Wellman H (1952) Oxidative phosphorylations; role of inorganic phosphate and acceptor systems in control of metabolic rates. J Biol Chem 195: 215–224PubMedGoogle Scholar
  57. Leisey JR, Grotyohann LW, Scott DA, Scaduto RC Jr (1993) Regulation of cardiac mitochondrial calcium by average extramitochondrial calcium. Am J Physiol 265: H1203–H1208PubMedGoogle Scholar
  58. Liimatta EV, Gödecke A, Schrader J, Hassinen IE (2004) Regulation of cellular respiration in myoglobin-deficient mouse heart. Mol Cell Biochem 256-257: 201–208PubMedGoogle Scholar
  59. MacDonald MJ (1981) High content of mitochondrial glycerol-3-phosphate dehydrogenase in pancreatic islets and its inhibition by diazoxide. J Biol Chem 256: 8287–8290PubMedGoogle Scholar
  60. MacGowan GA, Du C, Glonty V, Suhan JP, Koretsky AP, Farkas DL (2001) Rhod-2 based measurements of intracellular calcium in the perfused mouse heart: cellular and subcellular localization and response to positive inotropy. J Biomed Opt 6: 23–30PubMedGoogle Scholar
  61. Manneschi L, Federico A (1995) Polarographic analyses of subsarcolemmal and intermyofibrillar mitochondria from rat skeletal and cardiac muscle. J Neurol Sci 128: 151–156PubMedGoogle Scholar
  62. McCormack JG, Denton RM (1990) The role of mitochondrial Ca2+ transport and matrix Ca2+ in signal transduction in mammalian tissues. Biochim Biophys Acta 1018: 287–291PubMedGoogle Scholar
  63. McGarry JD, Foster DW (1979) In support of the roles of malonyl-CoA and carnitine acyltransferase I in the regulation of hepatic fatty acid oxidation and ketogenesis. J Biol Chem 254: 8163–8168PubMedGoogle Scholar
  64. Midgley PJ, Rutter GA, Thomas AP, Denton RM (1987) Effects of Ca2+ and Mg2+ on the activity of pyruvate dehydrogenase phosphate phosphatase within toluene-permeabilized mitochondria. Biochem J 241: 371–377PubMedGoogle Scholar
  65. Mitchell P (1975) The protonmotive Q cycle: a general formulation. FEBS Lett 59: 137–139PubMedGoogle Scholar
  66. Muller G, Bandlow W (1987) cAMP-dependent protein kinase activity in yeast mitochondria. Z. Naturforsch [C] 42: 1291–1302Google Scholar
  67. Nichols BJ, Rigoulet M, Denton RM (1994) Comparison of the effects of Ca2+, adenine nucleotides and pH on the kinetic properties of mitochondrial NAD+-isocitrate dehydrogenase and oxoglutarate dehydrogenase from the yeast Saccharomyces cerevisiae and rat heart. Biochem J 303: 461–465PubMedGoogle Scholar
  68. Nuutinen EM, Hiltunen K, Hassinen IE (1981) The glutamate dehydrogenase system and the redox state of mitochondrial free nicotinamide adenine dinucleotide in myocardium. FEBS Lett 128: 356–360PubMedGoogle Scholar
  69. Nuutinen EM (1984) Subcellular origin of the surface fluorescence of reduced nicotinamide nucleotides in the isolated perfused rat heart. Basic Res Cardiol 79: 49–58PubMedGoogle Scholar
  70. Ohnishi T, Salerno JC (2005) Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett 579:4555-4561PubMedGoogle Scholar
  71. Oster G, Wang H (2003) Rotary protein motors. Trends Cell Biol 13: 114–121PubMedGoogle Scholar
  72. Ostro MJ, Fondy TP (1977) Isolation and characterization of multiple molecular forms of cytosolic NAD-linked glycerol-3-phosphate dehydrogenase from normal and neoplastic rabbit tissues. J Biol Chem 252: 5575–5583PubMedGoogle Scholar
  73. Palmieri F, Bisaccia F, Capobianco L, Dolce V, Fiermonte G, Iacobazzi V, Zara V (1993) Transmembrane topology, genes, and biogenesis of the mitochondrial phosphate and oxoglutarate carriers. J Bioenerg Biomembr 25: 493–501PubMedGoogle Scholar
  74. Papa S, Sardanelli AM, Cocco T, Speranza F, Scacco SC, Technikova-Dobrova Z (1996) The nuclear-encoded 18 kDa (IP) AQDQ subunit of bovine heart complex I is phosphorylated by the mitochondrial cAMP-dependent protein kinase. FEBS Lett 379: 299–301PubMedGoogle Scholar
  75. Papa S, Sardanelli AM, Scacco S, Petruzzella V, Technikova-Dobrova Z, Vergari R, Signorile A (2002) The NADH: ubiquinone oxidoreductase (complex I) of the mammalian respiratory chain and the cAMP cascade. J Bioenerg Biomembr 34: 1–10PubMedGoogle Scholar
  76. Papa S, Sardanelli AM, Scacco S, Technikova-Dobrova Z (1999) cAMP-dependent protein kinase and phosphoproteins in mammalian mitochondria. An extension of the cAMP-mediated intracellular signal transduction. FEBS Lett 444: 245–249PubMedGoogle Scholar
  77. Penna C, Pagliaro P, Rastaldo R, Di Pancrazio F, Lippe G, Gattullo D, Mancardi D, Samaja M, Losano G, Mavelli I (2004) F0F1 ATP synthase activity is differently modulated by coronary reactive hyperemia before and after ischemic preconditioning in the goat. Am J Physiol Heart Circ Physiol 287: H2192–H2200PubMedGoogle Scholar
  78. Peters SJ (2003) Regulation of PDH activity and isoform expression: diet and exercise. Biochem Soc Trans 31: 1274–1280PubMedGoogle Scholar
  79. Peuhkurinen KJ, Hassinen IE (1982) Pyruvate carboxylation as an anaplerotic mechanism in the isolated perfused rat heart. Biochem J 202: 67–76PubMedGoogle Scholar
  80. Ragan CI (1987) Structure of NADH-ubiquinone reductase (complex I). Curr Top Bioenerg 15: 1–35Google Scholar
  81. Ravindran S, Radke GA, Guest JR, Roche TE (1996) Lipoyl domain-based mechanism for the integrated feedback control of the pyruvate dehydrogenase complex by enhancement of pyruvate dehydrogenase kinase activity. J Biol Chem 271: 653–662PubMedGoogle Scholar
  82. Reichmann H, Vogler L, Seibel P (1996) Ragged red or ragged blue fibers. Eur Neurol 36: 98–102PubMedGoogle Scholar
  83. Riva A, Tandler B, Loffredo F, Vazquez E, Hoppel C (2005) Structural differences in two biochemically defined populations of cardiac mitochondria. Am J Physiol Heart Circ Physiol 289: H868–H872PubMedGoogle Scholar
  84. Ruzicka FJ, Beinert H (1977) A new iron-sulfur flavoprotein of the respiratory chain. A component of the fatty acid beta oxidation pathway. J Biol Chem 252: 8440–8445PubMedGoogle Scholar
  85. Sazanov LA, Peak-Chew SY, Fearnley IM, Walker JE (2000) Resolution of the membrane domain of bovine complex I into subcomplexes: implications for the structural organization of the enzyme. Biochemistry 39: 7229–7235PubMedGoogle Scholar
  86. Schagger H (2002) Respiratory chain supercomplexes of mitochondria and bacteria. Biochim Biophys Acta 1555: 154–159PubMedGoogle Scholar
  87. Schilling B, Aggeler R, Schulenberg B, Murray J, Row RH, Capaldi RA, Gibson BW (2005) Mass spectrometric identification of a novel phosphorylation site in subunit NDUFA10 of bovine mitochondrial complex I. FEBS Lett 579: 2485–2490PubMedGoogle Scholar
  88. Schulz H (1991) Beta oxidation of fatty acids. Biochim Biophys Acta 1081: 109–120PubMedGoogle Scholar
  89. Siess EA, Kientsch-Engel RI, Wieland OH (1984) Concentration of free oxaloacetate in the mitochondrial compartment of isolated liver cells. Biochem J 218: 171–176PubMedGoogle Scholar
  90. Signorile A, Sardanelli AM, Nuzzi R, Papa S (2002) Serine (threonine) phosphatase(s) acting on cAMP-dependent phosphoproteins in mammalian mitochondria. FEBS Lett 512: 91–94PubMedGoogle Scholar
  91. Steenaart NA, Shore GC (1997) Mitochondrial cytochrome c oxidase subunit IV is phosphorylated by an endogenous kinase. FEBS Lett 415: 294–298PubMedGoogle Scholar
  92. Sundqvist KE, Heikkilä J, Hassinen IE, Hiltunen JK (1987) Role of NADP+-linked malic enzymes as regulators of the pool size of tricarboxylic acid-cycle intermediates in the perfused rat heart. Biochem J 243: 853–857PubMedGoogle Scholar
  93. Sundqvist KE, Hiltunen JK, Hassinen IE (1989) Pyruvate carboxylation in the rat heart. Role of biotin-dependent enzymes. Biochem J 257: 913–916Google Scholar
  94. Technikova-Dobrova Z, Sardanelli AM, Speranza F, Scacco S, Signorile A, Lorusso V, Papa S (2001) Cyclic adenosine monophosphate-dependent phosphorylation of mammalian mitochondrial proteins: enzyme and substrate characterization and functional role. Biochemistry 40: 13941–13947PubMedGoogle Scholar
  95. Todaka K, Wang J, Yi GH, Stennett R, Knecht M, Packer M, Burkhoff D (1996) Effects of levosimendan on myocardial contractility and oxygen consumption. J Pharmacol Exp Ther 279: 120–127PubMedGoogle Scholar
  96. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272: 1136–1144PubMedGoogle Scholar
  97. Ueno H, Suzuki T, Kinosita K Jr, Yoshida M (2005) ATP-driven stepwise rotation of FoF1-ATP synthase. Proc Natl Acad Sci USA 102: 1333–1338PubMedGoogle Scholar
  98. Vendelin M, Kongas O, Saks V (2000) Regulation of mitochondrial respiration in heart cells analyzed by reaction-diffusion model of energy transfer. Am J Physiol Cell Physiol 278: C747–C764PubMedGoogle Scholar
  99. Vuorinen K, Ylitalo K, Peuhkurinen K, Raatikainen P, Ala-Rämi A, Hassinen IE (1995a) Mechanisms of ischemic preconditioning in rat myocardium. Roles of adenosine, cellular energy state, and mitochondrial F1F0-ATPase. Circulation 91: 2810–2818PubMedGoogle Scholar
  100. Vuorinen KH, Ala-Rämi A, Yan Y, Ingman P, Hassinen IE (1995b) Respiratory control in heart muscle during fatty acid oxidation. Energy state or substrate-level regulation by Ca2+? J Mol Cell Cardiol 27: 1581–1591PubMedGoogle Scholar
  101. Weinstein ES, Benson DW, Fry DE (1986) Subpopulations of human heart mitochondria. J Surg Res 40: 495–498PubMedGoogle Scholar
  102. Wieland OH, Portenhauser R (1974) Regulation of pyruvate-dehydrogenase interconversion in rat-liver mitochondria as related to the phosphorylation state of intramitochondrial adenine nucleotides. Eur J Biochem 45: 577–588PubMedGoogle Scholar
  103. Wikström M (1984) Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett 169: 300–304PubMedGoogle Scholar
  104. Wikström M (1984) Pumping of protons from the mitochondrial matrix by cytochrome oxidase. Nature 308: 558–560PubMedGoogle Scholar
  105. Williamson JR, Ford C, Illingworth J, Safer B (1976) Coordination of citric acid cycle activity with electron transport flux. Circ Res 38: I39–I51PubMedGoogle Scholar
  106. Wilson DF, Owen CS, Holian A (1977) Control of mitochondrial respiration: a quantitative evaluation of the roles of cytochrome c and oxygen. Arch Biochem Biophys 182: 749–762PubMedGoogle Scholar
  107. Wilson DF, Stubbs M, Veech RL, Erecinska M, Krebs HA (1974) Equilibrium relations between the oxidation-reduction reactions and the adenosine triphosphate synthesis in suspensions of isolated liver cells. Biochem J 140: 57–64PubMedGoogle Scholar
  108. Wu ST, Kojima S, Parmley WW, Wikman-Coffelt J (1992) Relationship between cytosolic calcium and oxygen consumption in isolated rat hearts. Cell Calcium 13: 235–247PubMedGoogle Scholar
  109. Ylitalo K, Ala-Rämi A, Vuorinen K, Peuhkurinen K, Lepojärvi M, Kaukoranta P, Kiviluoma K, Hassinen IE (2001) Reversible ischemic inhibition of F1Fo-ATPase in rat and human myocardium. Biochim Biophys Acta 1504: 329–339PubMedGoogle Scholar
  110. Zeviani M, Tiranti V, Piantadosi C (1998) Mitochondrial disorders. Medicine (Baltimore) 77: 59–72Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Ilmo Hassinen

There are no affiliations available

Personalised recommendations