Formation of highly organized intracellular structure and energy metabolism in cardiac muscle cells during postnatal development of rat heart

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1837, Issue 8, 2014, Pages 1350-1361

  Anmann, Tiia ^a   Varikmaa, Minna ^a,b   Timohhina, Natalja ^a   Tepp, Kersti ^a   Shevchuk, Igor ^a   Chekulayev, Vladimir ^a   Saks, Valdur ^a,c   Kaambre, Tuuli ^a,d  

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

^b TALLINN UNIVERSITY OF TECHNOLOGY   (Estonia)

^c Domaine Universitaire   (France)

^d TALLINN UNIVERSITY   (Estonia)

Author keywords

Bioenergetics; Cardiomyocyte; Development; Intracellular architecture; Mitochondria; Tubulin

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ALPHA4 TUBULIN; BETA 2 TUBULIN; CREATINE KINASE; TUBULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENERGY METABOLISM; FEEDBACK SYSTEM; HEART DEVELOPMENT; HEART MUSCLE CELL; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; MUSCLE FIBRIL; NEWBORN; NONHUMAN; OUTER MEMBRANE; OXIDATIVE PHOSPHORYLATION; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN; RESPIROMETRY;

RATTUS;

BIOENERGETICS; CARDIOMYOCYTE; DEVELOPMENT; INTRACELLULAR ARCHITECTURE; MITOCHONDRIA; TUBULIN;

ADENOSINE DIPHOSPHATE; ANIMALS; CYTOSKELETON; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENERGY METABOLISM; HUMANS; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANES; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; TUBULIN;

EID: 84901112706     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2014.03.015     Document Type: Article

References (76)

1. A.M. Gordon, M. Regnier, and E. Homsher Skeletal and cardiac muscle contractile activation: tropomyosin "rocks and rolls" News Physiol. Sci. 16 2001 49 55 (Pubitemid 33578322)
2. M. Vendelin, N. Beraud, K. Guerrero, T. Andrienko, A.V. Kuznetsov, J. Olivares, L. Kay, and V.A. Saks Mitochondrial regular arrangement in muscle cells: a "crystal-like" pattern Am. J. Physiol. Cell Physiol. 288 2005 C757 C767
3. T. Anmann, M. Eimre, A.V. Kuznetsov, T. Andrienko, T. Kaambre, P. Sikk, E. Seppet, T. Tiivel, M. Vendelin, and V.A. Saks Calcium-induced contraction of sarcomeres changes the regulation of mitochondrial respiration in permeabilized cardiac cells FEBS J. 272 2005 3145 3161 (Pubitemid 40904700)
4. V.A. Saks, T. Kaambre, P. Sikk, M. Eimre, E. Orlova, K. Paju, A. Piirsoo, F. Appaix, L. Kay, V. Regitz-Zagrosek, E. Fleck, and E. Seppet Intracellular energetic units in red muscle cells Biochem. J. 356 2001 643 657 (Pubitemid 32532379)
5. E.K. Seppet, T. Kaambre, P. Sikk, T. Tiivel, H. Vija, M. Tonkonogi, K. Sahlin, L. Kay, F. Appaix, U. Braun, M. Eimre, and V.A. Saks Functional complexes of mitochondria with Ca,MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells Biochim. Biophys. Acta 1504 2001 379 395 (Pubitemid 32201910)
6. A. Kaasik, V. Veksler, E. Boehm, M. Novotova, A. Minajeva, and R. Ventura-Clapier Energetic crosstalk between organelles: architectural integration of energy production and utilization Circ. Res. 89 2001 153 159 (Pubitemid 34135823)
7. V. Saks, A.V. Kuznetsov, M. Gonzalez-Granillo, K. Tepp, N. Timohhina, M. Karu-Varikmaa, T. Kaambre, P. Dos Santos, F. Boucher, and R. Guzun Intracellular energetic units regulate metabolism in cardiac cells J. Mol. Cell. Cardiol. 52 2012 419 436
8. V. Saks, R. Guzun, N. Timohhina, K. Tepp, M. Varikmaa, C. Monge, N. Beraud, T. Kaambre, A. Kuznetsov, L. Kadaja, M. Eimre, and E. Seppet Structure-function relationships in feedback regulation of energy fluxes in vivo in health and disease: mitochondrial interactosome Biochim. Biophys. Acta 1797 2010 678 697
9. V. Saks, T. Kaambre, R. Guzun, T. Anmann, P. Sikk, U. Schlattner, T. Wallimann, M. Aliev, and M. Vendelin The creatine kinase phosphotransfer network: thermodynamic and kinetic considerations, the impact of the mitochondrial outer membrane and modelling approaches Subcell. Biochem. 46 2007 27 65
10. N. Timohhina, R. Guzun, K. Tepp, C. Monge, M. Varikmaa, H. Vija, P. Sikk, T. Kaambre, D. Sackett, and V. Saks Direct measurement of energy fluxes from mitochondria into cytoplasm in permeabilized cardiac cells in situ: some evidence for mitochondrial interactosome J. Bioenerg. Biomembr. 41 2009 259 275
11. F. Appaix, A.V. Kuznetsov, Y. Usson, L. Kay, T. Andrienko, J. Olivares, T. Kaambre, P. Sikk, R. Margreiter, and V. Saks Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria Exp. Physiol. 88 2003 175 190 (Pubitemid 36150070)
12. T. Anmann, R. Guzun, N. Beraud, S. Pelloux, A.V. Kuznetsov, L. Kogerman, T. Kaambre, P. Sikk, K. Paju, N. Peet, E. Seppet, C. Ojeda, Y. Tourneur, and V. Saks Different kinetics of the regulation of respiration in permeabilized cardiomyocytes and in HL-1 cardiac cells. Importance of cell structure/organization for respiration regulation Biochim. Biophys. Acta 1757 2006 1597 1606 (Pubitemid 44838483)
13. J.R. Wilding, F. Joubert, C. de Araujo, D. Fortin, M. Novotova, V. Veksler, and R. Ventura-Clapier Altered energy transfer from mitochondria to sarcoplasmic reticulum after cytoarchitectural perturbations in mice hearts J. Physiol. 575 2006 191 200 (Pubitemid 44178137)
14. V.A. Saks, Y.O. Belikova, and A.V. Kuznetsov In vivo regulation of mitochondrial respiration in cardiomyocytes: specific restrictions for intracellular diffusion of ADP Biochim. Biophys. Acta 1074 1991 302 311
15. R. Guzun, N. Timohhina, K. Tepp, C. Monge, T. Kaambre, P. Sikk, A.V. Kuznetsov, C. Pison, and V. Saks Regulation of respiration controlled by mitochondrial creatine kinase in permeabilized cardiac cells in situ. Importance of system level properties Biochim. Biophys. Acta 1787 2009 1089 1105
16. K. Tepp, I. Shevchuk, V. Chekulayev, N. Timohhina, A.V. Kuznetsov, R. Guzun, V. Saks, and T. Kaambre High efficiency of energy flux controls within mitochondrial interactosome in cardiac intracellular energetic units Biochim. Biophys. Acta 1807 2011 1549 1561
17. L. Kay, Z. Li, M. Mericskay, J. Olivares, L. Tranqui, E. Fontaine, T. Tiivel, P. Sikk, T. Kaambre, J.L. Samuel, L. Rappaport, Y. Usson, X. Leverve, D. Paulin, and V.A. Saks Study of regulation of mitochondrial respiration in vivo. An analysis of influence of ADP diffusion and possible role of cytoskeleton Biochim. Biophys. Acta 1322 1997 41 59 (Pubitemid 27497127)
18. K.L. Sheldon, E.N. Maldonado, J.J. Lemasters, T.K. Rostovtseva, and S.M. Bezrukov Phosphorylation of voltage-dependent anion channel by serine/threonine kinases governs its interaction with tubulin PLoS One 6 2011 e25539
19. T.K. Rostovtseva, K.L. Sheldon, E. Hassanzadeh, C. Monge, V. Saks, S.M. Bezrukov, and D.L. Sackett Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration Proc. Natl. Acad. Sci. U. S. A. 105 2008 18746 18751
20. M. Carre, N. Andre, G. Carles, H. Borghi, L. Brichese, C. Briand, and D. Braguer Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel J. Biol. Chem. 277 2002 33664 33669
21. C. Monge, N. Beraud, A.V. Kuznetsov, T. Rostovtseva, D. Sackett, U. Schlattner, M. Vendelin, and V.A. Saks 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
22. E.N. Maldonado, J. Patnaik, M.R. Mullins, and J.J. Lemasters Free tubulin modulates mitochondrial membrane potential in cancer cells Cancer Res. 70 2010 10192 10201
23. M. Varikmaa, R. Bagur, T. Kaambre, A. Grichine, N. Timohhina, K. Tepp, I. Shevchuk, V. Chekulayev, M. Metsis, F. Boucher, V. Saks, A.V. Kuznetsov, and R. Guzun Role of mitochondria-cytoskeleton interactions in respiration regulation and mitochondrial organization in striated muscles Biochim. Biophys. Acta 1837 2014 232 245
24. A.V. Kuznetsov, S. Javadov, R. Guzun, M. Grimm, and V. Saks Cytoskeleton and regulation of mitochondrial function: the role of beta-tubulin II Front. Physiol. 4 2013 82
25. A. Banerjee, M.C. Roach, K.A. Wall, M.A. Lopata, D.W. Cleveland, and R.F. Luduena A monoclonal antibody against the type II isotype of beta-tubulin. Preparation of isotypically altered tubulin J. Biol. Chem. 263 1988 3029 3034 (Pubitemid 18062960)
26. X.H. Jaglin, and J. Chelly Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects Trends Genet. 25 2009 555 566
27. G.A. Porter Jr., J. Hom, D. Hoffman, R. Quintanilla, K. de Mesy Bentley, and S.S. Sheu Bioenergetics, mitochondria, and cardiac myocyte differentiation Prog. Pediatr. Cardiol. 31 2011 75 81
28. T. Tiivel, L. Kadaya, A. Kuznetsov, T. Kaambre, N. Peet, P. Sikk, U. Braun, R. Ventura-Clapier, V. Saks, and E.K. Seppet Developmental changes in regulation of mitochondrial respiration by ADP and creatine in rat heart in vivo Mol. Cell. Biochem. 208 2000 119 128 (Pubitemid 30451462)
29. A. Bass, M. Stejskalova, A. Stieglerova, B. Ostadal, and M. Samanek Ontogenetic development of energy-supplying enzymes in rat and guinea-pig heart Physiol. Res. 50 2001 237 245 (Pubitemid 32720593)
30. G.D. Lopaschuk, and J.S. Jaswal Energy metabolic phenotype of the cardiomyocyte during development, differentiation, and postnatal maturation J. Cardiovasc. Pharmacol. 56 2010 130 140
31. A. Fischer, M. Ten Hove, L. Sebag-Montefiore, H. Wagner, K. Clarke, H. Watkins, C.A. Lygate, and S. Neubauer Changes in creatine transporter function during cardiac maturation in the rat BMC Dev. Biol. 10 2010 70
32. R.J. Ascuitto, and N.T. Ross-Ascuitto Substrate metabolism in the developing heart Semin. Perinatol. 20 1996 542 563 (Pubitemid 27147001)
33. A.O. Makinde, P.F. Kantor, and G.D. Lopaschuk Maturation of fatty acid and carbohydrate metabolism in the newborn heart Mol. Cell. Biochem. 188 1998 49 56 (Pubitemid 28493317)
34. A. Boneh Regulation of mitochondrial oxidative phosphorylation by second messenger-mediated signal transduction mechanisms Cell. Mol. Life Sci. 63 2006 1236 1248 (Pubitemid 43939010)
35. M.R. Duchen, A. Leyssens, and M. Crompton Transient mitochondrial depolarizations reflect focal sarcoplasmic reticular calcium release in single rat cardiomyocytes J. Cell Biol. 142 1998 975 988 (Pubitemid 28402053)
36. R. Garesse, and C.G. Vallejo Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes Gene 263 2001 1 16 (Pubitemid 32167049)
37. A. Ikenishi, H. Okayama, N. Iwamoto, S. Yoshitome, S. Tane, K. Nakamura, T. Obayashi, T. Hayashi, and T. Takeuchi Cell cycle regulation in mouse heart during embryonic and postnatal stages Dev. Growth Differ. 54 2012 731 738
38. N. Hall, and M. DeLuca Developmental changes in creatine phosphokinase isoenzymes in neonatal mouse hearts Biochem. Biophys. Res. Commun. 66 1975 988 994
39. J.S. Ingwall, W.R. Roeske, and K. Wildenthal The fetal mouse heart in organ culture: maintenance of the differentiated state Methods Cell Biol. 21A 1980 167 186
40. R.T. Dowell Mitochondrial component of the phosphorylcreatine shuttle is enhanced during rat heart perinatal development Biochem. Biophys. Res. Commun. 141 1986 319 325 (Pubitemid 17002077)
41. R.V. Trask, and J.J. Billadello Tissue-specific distribution and developmental regulation of M and B creatine kinase mRNAs Biochim. Biophys. Acta 1049 1990 182 188 (Pubitemid 20183656)
42. R.T. Dowell, and M.C. Fu Heterogeneous cellular expression of creatine kinase isoenzyme during normal rat heart development Mol. Cell. Biochem. 178 1998 87 94 (Pubitemid 28121746)
43. J. Piquereau, M. Novotova, D. Fortin, A. Garnier, R. Ventura-Clapier, V. Veksler, and F. Joubert Postnatal development of mouse heart: formation of energetic microdomains J. Physiol. 588 2010 2443 2454
44. A.V. Kuznetsov, V. Veksler, F.N. Gellerich, V. Saks, R. Margreiter, and W.S. Kunz Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells Nat. Protoc. 3 2008 965 976 (Pubitemid 351818685)
45. V.A. Saks, V.I. Veksler, A.V. Kuznetsov, L. Kay, P. Sikk, T. Tiivel, L. Tranqui, J. Olivares, K. Winkler, F. Wiedemann, and W.S. Kunz Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo Mol. Cell. Biochem. 184 1998 81 100 (Pubitemid 28398602)
46. M. Eimre, K. Paju, S. Pelloux, N. Beraud, M. Roosimaa, L. Kadaja, M. Gruno, N. Peet, E. Orlova, R. Remmelkoor, A. Piirsoo, V. Saks, and E. Seppet Distinct organization of energy metabolism in HL-1 cardiac cell line and cardiomyocytes Biochim. Biophys. Acta 1777 2008 514 524
47. C. Monge, N. Beraud, K. Tepp, S. Pelloux, S. Chahboun, T. Kaambre, L. Kadaja, M. Roosimaa, A. Piirsoo, Y. Tourneur, A.V. Kuznetsov, V. Saks, and E. Seppet Comparative analysis of the bioenergetics of adult cardiomyocytes and nonbeating HL-1 cells: respiratory chain activities, glycolytic enzyme profiles, and metabolic fluxes Can. J. Physiol. Pharmacol. 87 2009 318 326
48. R. Guzun, N. Timohhina, K. Tepp, M. Gonzalez-Granillo, I. Shevchuk, V. Chekulayev, A.V. Kuznetsov, T. Kaambre, and V.A. Saks Systems bioenergetics of creatine kinase networks: physiological roles of creatine and phosphocreatine in regulation of cardiac cell function Amino Acids 40 2011 1333 1348
49. J. Sambrook, and D.W. Russell Molecular Cloning: A Laboratory Manual 3rd ed. 2001 Cold Spring Harbor Laboratory Press Cold Spring Harbor, N.Y.
50. I. Romero-Calvo, B. Ocon, P. Martinez-Moya, M.D. Suarez, A. Zarzuelo, O. Martinez-Augustin, and F.S. de Medina Reversible Ponceau staining as a loading control alternative to actin in Western blots Anal. Biochem. 401 2010 318 320
51. R. Guzun, M. Gonzalez-Granillo, M. Karu-Varikmaa, A. Grichine, Y. Usson, T. Kaambre, K. Guerrero-Roesch, A. Kuznetsov, U. Schlattner, and V. Saks Regulation of respiration in muscle cells in vivo by VDAC through interaction with the cytoskeleton and MtCK within mitochondrial interactosome Biochim. Biophys. Acta 1818 2012 1545 1554
52. J. Wolff Plasma membrane tubulin Biochim. Biophys. Acta 1788 2009 1415 1433
53. J. Cassereau, A. Chevrollier, N. Gueguen, V. Desquiret, C. Verny, G. Nicolas, F. Dubas, P. Amati-Bonneau, P. Reynier, D. Bonneau, and V. Procaccio Mitochondrial dysfunction and pathophysiology of Charcot-Marie-Tooth disease involving GDAP1 mutations Exp. Neurol. 227 1 2011 31 41
54. T. Narishige, K.L. Blade, Y. Ishibashi, T. Nagai, M. Hamawaki, D.R. Menick, D. Kuppuswamy, and G.t. Cooper Cardiac hypertrophic and developmental regulation of the beta-tubulin multigene family J. Biol. Chem. 274 1999 9692 9697
55. M. Hallman, P. Maenpaa, and I. Hassinen Levels of cytochromes in heart, liver, kidney and brain in the developing rat Experientia 28 1972 1408 1410
56. V.L. Kinnula, and I. Hassinen Effect of hypoxia on mitochondrial mass and cytochrome concentrations in rat heart and liver during postnatal development Acta Physiol. Scand. 99 1977 462 466 (Pubitemid 8084623)
57. J.J. Lehman, P.M. Barger, A. Kovacs, J.E. Saffitz, D.M. Medeiros, and D.P. Kelly Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis J. Clin. Invest. 106 2000 847 856
58. B.N. Finck The PPAR regulatory system in cardiac physiology and disease Cardiovasc. Res. 73 2007 269 277 (Pubitemid 44937693)
59. Z. Wu, P. Puigserver, U. Andersson, C. Zhang, G. Adelmant, V. Mootha, A. Troy, S. Cinti, B. Lowell, R.C. Scarpulla, and B.M. Spiegelman Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1 Cell 98 1999 115 124 (Pubitemid 29331201)
60. L.K. Russell, C.M. Mansfield, J.J. Lehman, A. Kovacs, M. Courtois, J.E. Saffitz, D.M. Medeiros, M.L. Valencik, J.A. McDonald, and D.P. Kelly Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner Circ. Res. 94 2004 525 533 (Pubitemid 38326288)
61. G. Lenaz, and M.L. Genova Structural and functional organization of the mitochondrial respiratory chain: a dynamic super-assembly Int. J. Biochem. Cell Biol. 41 2009 1750 1772
62. E. Bonora, A.M. Porcelli, G. Gasparre, A. Biondi, A. Ghelli, V. Carelli, A. Baracca, G. Tallini, A. Martinuzzi, G. Lenaz, M. Rugolo, and G. Romeo Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III Cancer Res. 66 2006 6087 6096
63. H.Y. Lim, Q.S. Ho, J. Low, M. Choolani, and K.P. Wong Respiratory competent mitochondria in human ovarian and peritoneal cancer Mitochondrion 11 2011 437 443
64. M. Puurand, N. Peet, A. Piirsoo, M. Peetsalu, J. Soplepmann, M. Sirotkina, A. Peetsalu, A. Hemminki, and E. Seppet Deficiency of the complex I of the mitochondrial respiratory chain but improved adenylate control over succinate-dependent respiration are human gastric cancer-specific phenomena Mol. Cell. Biochem. 370 2012 69 78
65. H. Simonnet, J. Demont, K. Pfeiffer, L. Guenaneche, R. Bouvier, U. Brandt, H. Schagger, and C. Godinot Mitochondrial complex I is deficient in renal oncocytomas Carcinogenesis 24 2003 1461 1466 (Pubitemid 37160836)
66. R.J. Scheubel, M. Tostlebe, A. Simm, S. Rohrbach, R. Prondzinsky, F.N. Gellerich, R.E. Silber, and J. Holtz Dysfunction of mitochondrial respiratory chain complex I in human failing myocardium is not due to disturbed mitochondrial gene expression J. Am. Coll. Cardiol. 40 2002 2174 2181 (Pubitemid 36005905)
67. S. Papa The NDUFS4 nuclear gene of complex I of mitochondria and the cAMP cascade Biochim. Biophys. Acta 1555 2002 147 153 (Pubitemid 35251822)
68. J. Marin-Garcia Thyroid hormone and myocardial mitochondrial biogenesis Vascul. Pharmacol. 52 2010 120 130
69. P.P. Dzeja, and A. Terzic Phosphotransfer networks and cellular energetics J. Exp. Biol. 206 2003 2039 2047 (Pubitemid 36761807)
70. W.E. Jacobus, and V.A. Saks Creatine kinase of heart mitochondria: changes in its kinetic properties induced by coupling to oxidative phosphorylation Arch. Biochem. Biophys. 219 1982 167 178
71. K. Anflous, D.D. Armstrong, and W.J. Craigen 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 (Pubitemid 32109673)
72. X. Xu, W. Decker, M.J. Sampson, W.J. Craigen, and M. Colombini Mouse VDAC isoforms expressed in yeast: channel properties and their roles in mitochondrial outer membrane permeability J. Membr. Biol. 170 1999 89 102 (Pubitemid 29367689)
73. S. Das, R. Wong, N. Rajapakse, E. Murphy, and C. Steenbergen Glycogen synthase kinase 3 inhibition slows mitochondrial adenine nucleotide transport and regulates voltage-dependent anion channel phosphorylation Circ. Res. 103 2008 983 991
74. M. Roosimaa, T. Podramagi, L. Kadaja, A. Ruusalepp, K. Paju, R. Puhke, M. Eimre, E. Orlova, A. Piirsoo, N. Peet, F.N. Gellerich, and E. Seppet Dilation of human atria: increased diffusion restrictions for ADP, overexpression of hexokinase 2 and its coupling to oxidative phosphorylation in cardiomyocytes Mitochondrion 13 2013 399 409
75. H. Sato, T. Nagai, D. Kuppuswamy, T. Narishige, M. Koide, D.R. Menick, and G.t. Cooper Microtubule stabilization in pressure overload cardiac hypertrophy J. Cell Biol. 139 1997 963 973 (Pubitemid 27508566)
76. E.K. Seppet, M. Eimre, T. Anmann, E. Seppet, A. Piirsoo, N. Peet, K. Paju, R. Guzun, N. Beraud, S. Pelloux, Y. Tourneur, A.V. Kuznetsov, T. Kaambre, P. Sikk, and V.A. Saks Structure-function relationships in the regulation of energy transfer between mitochondria and ATPases in cardiac cells Exp. Clin. Cardiol. 11 2006 189 194 (Pubitemid 44540862)