Regulation of respiration controlled by mitochondrial creatine kinase in permeabilized cardiac cells in situ. Importance of system level properties

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 9, 2009, Pages 1089-1105

  Guzun, Rita ^a   Timohhina, Natalja ^b   Tepp, Kersti ^b   Monge, Claire ^a   Kaambre, Tuuli ^b   Sikk, Peeter ^b   Kuznetsov, Andrey V ^c   Pison, Christophe ^a   Saks, Valdur ^a,b  

^a Domaine Universitaire   (France)

^b NATIONAL INSTITUTE OF CHEMICAL PHYSICS AND BIOPHYSICS   (Estonia)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Cardiomyocyte; Creatine; Creatine kinase; Mitochondria; Respiration

Indexed keywords

ADENOSINE TRIPHOSPHATASE (MAGNESIUM); ADENOSINE TRIPHOSPHATE MAGNESIUM; GLYCOLYTIC ENZYME; MITOCHONDRIAL CREATINE KINASE; PHOSPHOENOLPYRUVATE; PYRUVATE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CELL MEMBRANE PERMEABILITY; CELL STRUCTURE; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; DISSOCIATION CONSTANT; ENERGY TRANSFER; ENZYME KINETICS; GLYCOLYSIS; HEART MUSCLE CELL; IN VITRO STUDY; MITOCHONDRIAL RESPIRATION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN INTERACTION; RAT; RESPIRATION CONTROL; STEADY STATE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CARDIOTONIC AGENTS; CELL RESPIRATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CREATINE; CREATINE KINASE, MITOCHONDRIAL FORM; ENZYME ACTIVATION; KINETICS; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; OXYGEN CONSUMPTION; PHOSPHOCREATINE; PHOSPHOENOLPYRUVATE; PYRUVATE KINASE; RATS; RATS, WISTAR;

EID: 67649588894     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.03.024     Document Type: Article

References (135)

1. Engelhardt W.A. Life and science. Annu. Rev. Biochem. 51 (1982) 1-19
2. Vignais P. La biologie des origines à nos jours (2001), EDP Sciences, Les Ulis, France 478
3. Vignais P. Science expérimentale et connaissance du vivant. La méthode et les concepts (2006), EDP Sciences, Les Ulis, France 430
4. Belitzer V., and Tsybakova E. About mechanism of phosphorylation, respiratory coupling. Biochimia 4 (1939) 516-533 Moscow
5. Wallimann T., Wyss M., Brdiczka D., Nicolay K., and Eppenberger H.M. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem. J. 281 Pt 1 (1992) 21-40
6. Wallimann T., Tokarska-Schlattner M., Neumann D., Epand R.F., Andres R.H., Widmer H.R., Hornemann T., Saks V., Agarkova I., and Schlattner U. The phosphocreatine circuit: molecular and cellular physiology of creatine kinases, sensitivity to free radicals, and enhancement by creatine supplementation. In: Saks V. (Ed). Molecular System Bioenergetics. Energy for Life (2007), Wiley-VCH, Weinheim, GmbH, Germany
7. Wyss M., Smeitink J., Wevers R.A., and Wallimann T. Mitochondrial creatine kinase: a key enzyme of aerobic energy metabolism. Biochim. Biophys. Acta 1102 (1992) 119-166
8. Vendelin M., Lemba M., and Saks V.A. Analysis of functional coupling: mitochondrial creatine kinase and adenine nucleotide translocase. Biophys. J. 87 (2004) 696-713
9. Saks V.A., Kuznetsov A.V., Vendelin M., Guerrero K., Kay L., and Seppet E.K. Functional coupling as a basic mechanism of feedback regulation of cardiac energy metabolism. Mol. Cellular Biochem. 256-257 (2004) 185-199
10. Dolder M., Walzel B., Speer O., Schlattner U., and Wallimann T. Inhibition of the mitochondrial permeability transition by creatine kinase substrates. Requirement for microcompartmentation. J. Biol. Chem. 278 (2003) 17760-17766
11. Saks V., Dzeja P., Schlattner U., Vendelin M., Terzic A., and Wallimann T. Cardiac system bioenergetics: metabolic basis of the Frank-Starling law. J. Physiol. 571 (2006) 253-273
12. Saks V., Monge C., Anmann T., and Dzeja P. Integrated and organized cellular energetic systems: theories of cell energetics, compartmentation and metabolic channeling. In: Saks V. (Ed). Molecular System Bioenergetics. Energy for Life (2007), Wiley-VCH, Weinheim, GmbH, Germany 59-110
13. Saks V., Anmann T., Guzun R., Kaambre T., Sikk P., Schlattner U., Wallimann T., Aliev M., and Vendelin M. The creatine kinase phosphotransfer network: thermodynamic and kinetic considerations, the impact of the mitochondrial outer membrane and modelling approaches. In: Wyss M., and Salomons G. (Eds). Creatine and Creatine Kinase in Health and Disease. (2007), Springer, Dordrecht, Netherlands 27-66
14. Saks V., Beraud N., and Wallimann T. Metabolic compartmentation-a system level property of muscle cells. Int. J. Mol. Sci. (2008) 751-767
15. Schlattner U., and Wallimann T. Metabolite channeling: creatine kinase microcompartments. In: Lennarz W.J., and Lane M.D. (Eds). Encyclopedia of Biological Chemistry (2004), Academic Press, New York, USA 646-651
16. Schlattner U., Tokarska-Schlattner M., and Wallimann T. Mitochondrial creatine kinase in human health and disease. Biochim. Biophys. Acta 1762 (2006) 164-180
17. Beard D.A. A biophysical model of the mitochondrial respiratory system and oxidative phosphorylation. PLoS Comput. Biol. 1 (2005) e36
18. Beard D.A. Modeling of oxygen transport and cellular energetics explains observations on in vivo cardiac energy metabolism. PLoS Comput. Biol. 2 (2006) e107
19. van Beek J.H. Adenine nucleotide-creatine-phosphate module in myocardial metabolic system explains fast phase of dynamic regulation of oxidative phosphorylation. Am. J. Physiol. Cell Physiol. 293 (2007) C815-829
20. Van Beek J.H. Multiscale and modular analysis of cardiac energy metabolism: repairing the broken interfaces of isolated system components. Ann. N. Y. Acad. Sci. 1123 (2008) 155-168
21. Kemp G. Physiological implications of linear kinetics of mitochondrial respiration in vitro. Am. J. Physiol. Cell Physiol. 295 (2008) C844-846
22. Wu F., Yang F., Vinnakota K.C., and Beard D.A. Computer modeling of mitochondrial tricarboxylic acid cycle, oxidative phosphorylation, metabolite transport, and electrophysiology. J. Biol. Chem. 282 (2007) 24525-24537
23. Wu F., Zhang E.Y., Zhang J., Bache R.J., and Beard D.A. Phosphate metabolite concentrations and ATP hydrolysis potential in normal and ischaemic hearts. J. Physiol. 586 (2008) 4193-4208
24. Nicholls D.G., and Ferguson S.J. Bioenergetics (2002), Academic Press, London-New York 288
25. Balaban R.S. Cardiac energy metabolism homeostasis: role of cytosolic calcium. J. Mol. Cell. Cardiol. 34 (2002) 1259-1271
26. Korzeniewski B. Regulation of oxidative phosphorylation through parallel activation. Biophys. Chem. 129 (2007) 93-110
27. Korzeniewski B., Deschodt-Arsac V., Calmettes G., Franconi J.M., and Diolez P. Physiological heart activation by adrenaline involves parallel activation of ATP usage and supply. Biochem. J. 413 (2008) 343-347
28. Saks V., Dzeja P., Guzun R., Aliev M., Vendelin M., Terzic A., and Wallimann T. System analysis of cardiac energetics-excitation-contraction coupling: integration of mitochondrial respiration, phosphotransfer pathways, metabolic pacing, and substrate supply in the heart. In: Saks V. (Ed). Molecular System Bioenergetics. Energy for Life (2007), Wiley-VCH, Weinheim, GmbH, Germany
29. Saks V., Favier R., Guzun R., Schlattner U., and Wallimann T. Molecular system bioenergetics: regulation of substrate supply in response to heart energy demands. J. Physiol. 577 (2006) 769-777
30. Ingwall J.S. Energy metabolism in heart failure and remodelling. Cardiovasc. Res. 81 (2009) 412-414
31. Noble D. Modeling the heart-from genes to cells to the whole organ. Science (New York, N.Y 295 (2002) 1678-1682
32. Noble D. The music of life. Biology Beyond the Genome (2006), Oxford Univ. Press, Oxford, UK
33. Kitano H. Systems biology: a brief overview. Science (New York, N.Y.) 295 (2002) 1662-1664
34. Hunter P., and Nielsen P. A strategy for integrative computational physiology. Physiology (Bethesda, Md) 20 (2005) 316-325
35. Boogerd F.C., Bruggeman F.J., Hofmeyer J.S., and Westerhoff H.V. Systems Biology: Philosophical Foundations (2007), Elsevier Science 342
36. Alberghina L., and Westerhoff H.V. Systems Biology (2005), Definitions and Perspectives, Springer Verlag 401
37. Williamson J.R. Mitochondrial function in the heart. Annu. Rev. Physiol. 41 (1979) 485-506
38. Katz A.M. Ernest Henry Starling, his predecessors, and the "law of the heart". Circulation 106 (2002) 2986-2992
39. Neely J., and Morgan H. Relationship between carbohydrate and lipid metabolism and the energy balance of heart muscle. Annu. Rev. Physiol. (1974) 413-459
40. Balaban R.S., Kantor H.L., Katz L.A., and Briggs R.W. Relation between work and phosphate metabolite in the in vivo paced mammalian heart. Science (New York, N.Y) 232 (1986) 1121-1123
41. Shimizu J., Todaka K., and Burkhoff D. Load dependence of ventricular performance explained by model of calcium-myofilament interactions. Am. J. Physiol. Heart Circ. Physiol. 282 (2002) H1081-1091
42. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., and Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 287 (2004) C817-833
43. Bers D. Excitation-Contraction Coupling and Cardiac Contractile Force (2001), Kluwer Academic Publishers, Dordrecht, Netherlands
44. Brini M. Ca(2+) signalling in mitochondria: mechanism and role in physiology and pathology. Cell Calcium 34 (2003) 399-405
45. Meyer R.A., Sweeney H.L., and Kushmerick M.J. A simple analysis of the "phosphocreatine shuttle". Am. J. Physiol. 246 (1984) C365-377
46. Jeneson J.A., Wiseman R.W., Westerhoff H.V., and Kushmerick M.J. The signal transduction function for oxidative phosphorylation is at least second order in ADP. J. Biol. Chem. 271 (1996) 27995-27998
47. Jeneson J.A., Westerhoff H.V., and Kushmerick M.J. A metabolic control analysis of kinetic controls in ATP free energy metabolism in contracting skeletal muscle. Am. J. Physiol. Cell Physiol. 279 (2000) C813-832
48. Barros L.F., and Martinez C. An enquiry into metabolite domains. Biophys. J. 92 (2007) 3878-3884
49. Saks V., Kuznetsov A., Andrienko T., Usson Y., Appaix F., Guerrero K., Kaambre T., Sikk P., Lemba M., and Vendelin M. Heterogeneity of ADP diffusion and regulation of respiration in cardiac cells. Biophys. J. 84 (2003) 3436-3456
50. Kummel L. Ca, Mg-ATPase activity of permeabilised rat heart cells and its functional coupling to oxidative phosphorylation of the cells. Cardiovasc. Res. 22 (1988) 359-367
51. Saks V.A., Kapelko V.I., Kupriyanov V.V., Kuznetsov A.V., Lakomkin V.L., Veksler V.I., Sharov V.G., Javadov S.A., Seppet E.K., and Kairane C. Quantitative evaluation of relationship between cardiac energy metabolism and post-ischemic recovery of contractile function. J. Mol. Cell. Cardiol. 21 Suppl. 1 (1989) 67-78
52. Saks V.A., Belikova Y.O., and Kuznetsov A.V. In vivo regulation of mitochondrial respiration in cardiomyocytes: specific restrictions for intracellular diffusion of ADP. Biochim. Biophys. Acta 1074 (1991) 302-311
53. Saks V.A., Vasil eva E., Belikova Yu O., Kuznetsov A.V., Lyapina S., Petrova L., and Perov N.A. Retarded diffusion of ADP in cardiomyocytes: possible role of mitochondrial outer membrane and creatine kinase in cellular regulation of oxidative phosphorylation. Biochim. Biophys. Acta 1144 (1993) 134-148
54. Saks V., Dos Santos P., Gellerich F.N., and Diolez P. Quantitative studies of enzyme-substrate compartmentation, functional coupling and metabolic channelling in muscle cells. Mol. Cell. Biochem. 184 (1998) 291-307
55. Veksler V.I., Kuznetsov A.V., Anflous K., Mateo P., van Deursen J., Wieringa B., and Ventura-Clapier R. Muscle creatine kinase-deficient mice. II. Cardiac and skeletal muscles exhibit tissue-specific adaptation of the mitochondrial function. J. Biol. Chem. 270 (1995) 19921-19929
56. Kuznetsov A.V., Tiivel T., Sikk P., Kaambre T., Kay L., Daneshrad Z., Rossi A., Kadaja L., Peet N., Seppet E., and Saks V.A. Striking differences between the kinetics of regulation of respiration by ADP in slow-twitch and fast-twitch muscles in vivo. Eur. J. Biochem./FEBS 241 (1996) 909-915
57. Anflous K., Armstrong D.D., and Craigen W.J. Altered mitochondrial sensitivity for ADP and maintenance of creatine-stimulated respiration in oxidative striated muscles from VDAC1-deficient mice. J. Biol. Chem. 276 (2001) 1954-1960
58. Boudina S., Laclau M.N., Tariosse L., Daret D., Gouverneur G., Bonoron-Adele S., Saks V.A., and Dos Santos P. Alteration of mitochondrial function in a model of chronic ischemia in vivo in rat heart. Am. J. Physiol. Heart Circ. Physiol. 282 (2002) H821-831
59. Liobikas J., Kopustinskiene D.M., and Toleikis A. What controls the outer mitochondrial membrane permeability for ADP: facts for and against the role of oncotic pressure. Biochim. Biophys. Acta 1505 (2001) 220-225
60. Burelle Y., and Hochachka P.W. Endurance training induces muscle-specific changes in mitochondrial function in skinned muscle fibers. J. Appl. Physiol. 92 (2002) 2429-2438
61. Zoll J., Sanchez H., N Guessan B., Ribera F., Lampert E., Bigard X., Serrurier B., Fortin D., Geny B., Veksler V., Ventura-Clapier R., and Mettauer B. Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle. J. Physiol. 543 (2002) 191-200
62. Zoll J., Koulmann N., Bahi L., Ventura-Clapier R., and Bigard A.X. Quantitative and qualitative adaptation of skeletal muscle mitochondria to increased physical activity. J. Cell. Physiol. 194 (2003) 186-193
63. Zoll J., N Guessan B., Ribera F., Lampert E., Fortin D., Veksler V., Bigard X., Geny B., Lonsdorfer J., Ventura-Clapier R., and Mettauer B. Preserved response of mitochondrial function to short-term endurance training in skeletal muscle of heart transplant recipients. J. Am. Coll. Cardiol. 42 (2003) 126-132
64. Zoll J., Ponsot E., Doutreleau S., Mettauer B., Piquard F., Mazzucotelli J.P., Diemunsch P., and Geny B. Acute myocardial ischaemia induces specific alterations of ventricular mitochondrial function in experimental pigs. Acta Physiol. Scand. 185 (2005) 25-32
65. Guerrero K., Wuyam B., Mezin P., Vivodtzev I., Vendelin M., Borel J.C., Hacini R., Chavanon O., Imbeaud S., Saks V., and Pison C. Functional coupling of adenine nucleotide translocase and mitochondrial creatine kinase is enhanced after exercise training in lung transplant skeletal muscle. Am. J. Physiol. 289 (2005) R1144-1154
66. Vendelin M., Eimre M., Seppet E., Peet N., Andrienko T., Lemba M., Engelbrecht J., Seppet E.K., and Saks V.A. Intracellular diffusion of adenosine phosphates is locally restricted in cardiac muscle. Mol. Cell. Biochem. 256-257 (2004) 229-241
67. Selivanov V.A., Krause S., Roca J., and Cascante M. Modeling of spatial metabolite distributions in the cardiac sarcomere. Biophys. J. 92 (2007) 3492-3500
68. Abraham M.R., Selivanov V.A., Hodgson D.M., Pucar D., Zingman L.V., Wieringa B., Dzeja P.P., Alekseev A.E., and Terzic A. Coupling of cell energetics with membrane metabolic sensing. Integrative signaling through creatine kinase phosphotransfer disrupted by M-CK gene knock-out. J. Biol. Chem. 277 (2002) 24427-24434
69. Selivanov V.A., Alekseev A.E., Hodgson D.M., Dzeja P.P., and Terzic A. Nucleotide-gated KATP channels integrated with creatine and adenylate kinases: amplification, tuning and sensing of energetic signals in the compartmentalized cellular environment. Mol. Cell. Biochem. 256-257 (2004) 243-256
70. Weiss J.N., Yang L., and Qu Z. Systems biology approaches to metabolic and cardiovascular disorders: network perspectives of cardiovascular metabolism. J. Lipid Res. 47 (2006) 2355-2366
71. Saks V.A., Kaambre T., Sikk P., Eimre M., Orlova E., Paju K., Piirsoo A., Appaix F., Kay L., Regitz-Zagrosek V., Fleck E., and Seppet E. Intracellular energetic units in red muscle cells. Biochem. J. 356 (2001) 643-657
72. Seppet E.K., Kaambre T., Sikk P., Tiivel T., Vija H., Tonkonogi M., Sahlin K., Kay L., Appaix F., Braun U., Eimre M., and Saks V.A. Functional complexes of mitochondria with Ca,MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells. Biochim. Biophys. Acta 1504 (2001) 379-395
73. Dzeja P., Chung S., and Terzic A. Integration of adenylate kinase and glycolytic and clycogenolytic circuits in cellular energetics. In: Saks V. (Ed). Molecular System Bioenergetics. Energy for life (2007), Wiley-VCH, Weinheim, GmbH, Germany 195-264
74. Klingenberg M. The ADP and ATP transport in mitochondria and its carrier. Biochim. Biophys. Acta 1778 (2008) 1978-2021
75. Saks V.A., Chernousova G.B., Gukovsky D.E., Smirnov V.N., and Chazov E.I. Studies of energy transport in heart cells. Mitochondrial isoenzyme of creatine phosphokinase: kinetic properties and regulatory action of Mg2+ ions. Eur. J. Biochem./FEBS 57 (1975) 273-290
76. Kuznetsov A.V., Veksler V., Gellerich F.N., Saks V., Margreiter R., and Kunz W.S. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat. Protocols 3 (2008) 965-976
77. Saks V.A., Veksler V.I., Kuznetsov A.V., Kay L., Sikk P., Tiivel T., Tranqui L., Olivares J., Winkler K., Wiedemann F., and Kunz W.S. Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol. Cell. Biochem. 184 (1998) 81-100
78. Gnaiger E. Oxygen Solubility in Experimental Media., OROBOROS Bioenergetics Newsletter MiPNet 6.3 (2001), Innsbruck, Austria
79. Fuller E.O., Goldberg D.I., Starnes J.W., Sacks L.M., and Delivoria-Papadopoulos M. Mitochondrial respiration following acute hypoxia in the perfused rat heart. J. Mol. Cell. Cardiol. 17 (1985) 71-81
80. Monge C., Beraud N., Kuznetsov A.V., Rostovtseva T., Sackett D., Schlattner U., Vendelin M., and Saks V.A. Regulation of respiration in brain mitochondria and synaptosomes: restrictions of ADP diffusion in situ, roles of tubulin, and mitochondrial creatine kinase. Mol. Cell. Biochem. 318 (2008) 147-165
81. van Gelder B. On cytochrome c oxidase. I. The extinction coefficients of cytochrome a and cytochrome a3. Biochim. Biophys. Acta 118 (1966) 36-46
82. Jacobus W.E., and Saks V.A. Creatine kinase of heart mitochondria: changes in its kinetic properties induced by coupling to oxidative phosphorylation. Arch. Biochem. Biophys. 219 (1982) 167-178
83. McLeish M.J., and Kenyon G.L. Relating structure to mechanism in creatine kinase. Crit. Rev. Biochem. Mol. Biol. 40 (2005) 1-20
84. Gellerich F., and Saks V.A. Control of heart mitochondrial oxygen consumption by creatine kinase: the importance of enzyme localization. Biochem. Biophys. Res. Commun. 105 (1982) 1473-1481
85. Gellerich F.N., Schlame M., Bohnensack R., and Kunz W. Dynamic compartmentation of adenine nucleotides in the mitochondrial intermembrane space of rat-heart mitochondria. Biochim. Biophys. Acta 890 (1987) 117-126
86. Gellerich F.N., Trumbeckaite S., Opalka J.R., Seppet E., Rasmussen H.N., Neuhoff C., and Zierz S. Function of the mitochondrial outer membrane as a diffusion barrier in health and diseases. ` 28 (2000) 164-169
87. Gellerich F.N., Laterveer F.D., Zierz S., and Nicolay K. The quantitation of ADP diffusion gradients across the outer membrane of heart mitochondria in the presence of macromolecules. Bioch. Biophys. Acta 1554 (2002) 48-56
88. Klingenberg M. Mitochondria metabolite transport. FEBS letters 6 (1970) 145-154
89. Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol. Cell. Biochem. 256-257 (2004) 107-115
90. Saks V.A., Kuznetsov A.V., Khuchua Z.A., Vasilyeva E.V., Belikova J.O., Kesvatera T., and Tiivel T. Control of cellular respiration in vivo by mitochondrial outer membrane and by creatine kinase. A new speculative hypothesis: possible involvement of mitochondrial-cytoskeleton interactions. J. Mol. Cell. Cardiol. 27 (1995) 625-645
91. Appaix F., Kuznetsov A.V., Usson Y., Kay L., Andrienko T., Olivares J., Kaambre T., Sikk P., Margreiter R., and Saks V. Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria. Exp. Physiol. 88 (2003) 175-190
92. Rostovtseva T.K., and Bezrukov S.M. VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J. Bioenerg. Biomembr. 40 (2008) 163-170
93. Rostovtseva T.K., Sheldon K.L., Hassanzadeh E., Monge C., Saks V., Bezrukov S.M., and Sackett D.L. Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 18746-18751
94. Kuznetsov A.V., Khuchua Z.A., Vassil eva E.V., Medved eva N.V., and Saks V.A. Heart mitochondrial creatine kinase revisited: the outer mitochondrial membrane is not important for coupling of phosphocreatine production to oxidative phosphorylation. Arch. Biochem. Biophys. 268 (1989) 176-190
95. Saks V.A., Chernousova G.B., Voronkov, Smirnov V.N., and Chazov E.I. Study of energy transport mechanism in myocardial cells. Circ. Res. 35 Suppl. 3 (1974) 138-149
96. Saks V.A., Kuznetsov A.V., Kupriyanov V.V., Miceli M.V., and Jacobus W.E. Creatine kinase of rat heart mitochondria. The demonstration of functional coupling to oxidative phosphorylation in an inner membrane-matrix preparation. J. Biol. Chem. 260 (1985) 7757-7764
97. Aliev M.K., and Saks V.A. Compartmentalized energy transfer in cardiomyocytes: use of mathematical modeling for analysis of in vivo regulation of respiration. Biophys. J. 73 (1997) 428-445
98. Joubert F., Mateo P., Gillet B., Beloeil J.C., Mazet J.L., and Hoerter J.A. CK flux or direct ATP transfer: versatility of energy transfer pathways evidenced by NMR in the perfused heart. Mol. Cell. Biochem. 256-257 (2004) 43-58
99. Kay L., Nicolay K., Wieringa B., Saks V., and Wallimann T. Direct evidence for the control of mitochondrial respiration by mitochondrial creatine kinase in oxidative muscle cells in situ. The J. Biol. Chem. 275 (2000) 6937-6944
100. McFarland E.W., Kushmerick M.J., and Moerland T.S. Activity of creatine kinase in a contracting mammalian muscle of uniform fiber type. Biophys. J. 67 (1994) 1912-1924
101. Kushmerick M.J., and Conley K.E. Energetics of muscle contraction: the whole is less than the sum of its parts. Biochem. Soc. Trans. 30 (2002) 227-231
102. Ingwall J.S. ATP and the heart. ATP and the Heart (2002), Kluwer Academic Publishers, Dordrecht-Boston-London 1-244
103. Zweier J.L., and Jacobus W.E. Substrate-induced alterations of high energy phosphate metabolism and contractile function in the perfused heart. J. Biol. Chem. 262 (1987) 8015-8021
104. Saks V.A., and Aliev M.K. Is there the creatine kinase equilibrium in working heart cells?. Biochem. Biophys. Res. Commun. 227 (1996) 360-367
105. Lardy H.A., and Wellman H. Oxidative phosphorylations; role of inorganic phosphate and acceptor systems in control of metabolic rates. J. Biol. Chem. 195 (1952) 215-224
106. Chance B., and Williams G.R. A method for the localization of sites for oxidative phosphorylation. Nature 176 (1955) 250-254
107. Chance B., and Williams G.R. The respiratory chain and oxidative phosphorylation. Advan. Enzymol. Relat. subj. Biochem. 17 (1956) 65-134
108. Vignais P.V. Molecular and physiological aspects of adenine nucleotide transport in mitochondria. Biochim. Biophys. Acta 456 (1976) 1-38
109. Schlattner U., Forstner M., Eder M., Stachowiak O., Fritz-Wolf K., and Wallimann T. Functional aspects of the x-ray structure of mitochondrial creatine kinase: a molecular physiology approach. Mol. Cell. Biochem. 184 (1998) 125-140
110. Schlattner U., Dolder M., Wallimann T., and Tokarska-Schlattner M. Mitochondrial creatine kinase and mitochondrial outer membrane porin show a direct interaction that is modulated by calcium. J. Biol. Chem. 276 (2001) 48027-48030
111. Schlattner U., and Wallimann T. Molecular structure and function of mitochondrial creatine kinases. In: Uvarsky V.N. (Ed). Creatine Kinase-Biochemistry, Physiology, Structure and Function (2006), Nova Science Publishers, New York
112. Epand R.F., Tokarska-Schlattner M., Schlattner U., Wallimann T., and Epand R.M. Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. J. Mol. Biol. 365 (2007) 968-980
113. Bessman S.P., and Fonyo A. The possible role of the mitochondrial bound creatine kinase in regulation of mitochondrial respiration. Biochem. Biophys. Res. Commun. 22 (1966) 597-602
114. Jacobus W.E., and Lehninger A.L. Creatine kinase of rat heart mitochondria. Coupling of creatine phosphorylation to electron transport. J. Biol. Chem. 248 (1973) 4803-4810
115. Vial C., Godinot C., and Gautheron D. Membranes: creatine kinase (E.C.2.7.3.2.) in pig heart mitochondria. Properties and role in phosphate potential regulation. Biochimie 54 (1972) 843-852
116. Barbour R.L., Ribaudo J., and Chan S.H. Effect of creatine kinase activity on mitochondrial ADP/ATP transport. Evidence for a functional interaction. J. Biol. Chem. 259 (1984) 8246-8251
117. Erickson-Viitanen S., Geiger P.J., Viitanen P., and Bessman S.P. Compartmentation of mitochondrial creatine phosphokinase. II. The importance of the outer mitochondrial membrane for mitochondrial compartmentation. J. Biol. Chem. 257 (1982) 14405-14411
118. Erickson-Viitanen S., Viitanen P., Geiger P.J., Yang W.C., and Bessman S.P. Compartmentation of mitochondrial creatine phosphokinase. I. Direct demonstration of compartmentation with the use of labeled precursors. J. Biol. Chem. 257 (1982) 14395-14404
119. Saks V.A., Khuchua Z.A., and Kuznetsov A.V. Specific inhibition of ATP-ADP translocase in cardiac mitoplasts by antibodies against mitochondrial creatine kinase. Biochim. Biophys. Acta 891 (1987) 138-144
120. Kim I.H., and Lee H.J. Oxidative phosphorylation of creatine by respiring pig heart mitochondria in the absence of added adenine nucleotides. Biochem. Int. 14 (1987) 103-110
121. Meyer L.E., Machado L.B., Santiago A.P., da-Silva W.S., De Felice F.G., Holub O., Oliveira M.F., and Galina A. Mitochondrial creatine kinase activity prevents reactive oxygen species generation: antioxidant role of mitochondrial kinase-dependent ADP re-cycling activity. J. Biol. Chem. 281 (2006) 37361-37371
122. Kaasik A., Veksler V., Boehm E., Novotova M., Minajeva A., and Ventura-Clapier R. Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ. Res. 89 (2001) 153-159
123. Hornikova D., Herman P., Mejsnar J., Vecer J., and Zurmanova J. Creatine kinase structural changes induced by substrates. Biochim. Biophys. Acta (2009) 270-274
124. Saks V., Kaambre T., Guzun R., Anmann T., Sikk P., Schlattner U., Wallimann T., Aliev M., and Vendelin M. The creatine kinase phosphotransfer network: thermodynamic and kinetic considerations, the impact of the mitochondrial outer membrane and modelling approaches. Sub-cell. Biochem. 46 (2007) 27-65
125. Neubauer S. The failing heart-an engine out of fuel. New Engl. J. Med. 356 (2007) 1140-1151
126. Vendelin M., Kongas O., and Saks V. Regulation of mitochondrial respiration in heart cells analyzed by reaction-diffusion model of energy transfer. Am. J. Physiol. Cell Physiol. 278 (2000) C747-764
127. Bose S., French S., Evans F.J., Joubert F., and Balaban R.S. Metabolic network control of oxidative phosphorylation: multiple roles of inorganic phosphate. J. Biol. Chem. 278 (2003) 39155-39165
128. Saks V.A., Ventura-Clapier R., and Aliev M.K. Metabolic control and metabolic capacity: two aspects of creatine kinase functioning in the cells. Biochim. Biophys. Acta 1274 (1996) 81-88
129. Chance B., Im J., Nioka S., and Kushmerick M. Skeletal muscle energetics with PNMR: personal views and historic perspectives. NMR Biomed. 19 (2006) 904-926
130. Vendelin M., Bovendeerd P.H., Engelbrecht J., and Arts T. Optimizing ventricular fibers: uniform strain or stress, but not ATP consumption, leads to high efficiency. Am. J. Physiol. Heart Circ. Physiol. 283 (2002) H1072-1081
131. Honda H., Tanaka K., Akita N., and Haneda T. Cyclical changes in high-energy phosphates during the cardiac cycle by pacing-gated 31P nuclear magnetic resonance. Circ. J. 66 (2002) 80-86
132. Spindler M., Illing B., Horn M., de Groot M., Ertl G., and Neubauer S. Temporal fluctuations of myocardia high-energy phosphate metabolite with the cardiac cycle. Basic Res. Cardiol. 96 (2001) 553-556
133. Saks V.A., Kongas O., Vendelin M., and Kay L. Role of the creatine/phosphocreatine system in the regulation of mitochondrial respiration. Acta Physiol. Scand. 168 (2000) 635-641
134. Beer M., Seyfarth T., Sandstede J., Landschutz W., Lipke C., Kostler H., von Kienlin M., Harre K., Hahn D., and Neubauer S. Absolute concentrations of high-energy phosphate metabolites in normal, hypertrophied, and failing human myocardium measured noninvasively with (31)P-SLOOP magnetic resonance spectroscopy. J. Am. Coll. Cardiol. 40 (2002) 1267-1274
135. Nascimben L., Ingwall J.S., Pauletto P., Friedrich J., Gwathmey J.K., Saks V., Pessina A.C., and Allen P.D. Creatine kinase system in failing and nonfailing human myocardium. Circulation 94 (1996) 1894-1901