Restricted ADP movement in cardiomyocytes: Cytosolic diffusion obstacles are complemented with a small number of open mitochondrial voltage-dependent anion channels

Journal of Molecular and Cellular Cardiology - Tập 97 - Trang 197-203 - 2016
Päivo Simson1, Natalja Jepihhina1, Martin Laasmaa1, Pearu Peterson1, Rikke Birkedal1, Marko Vendelin1
1Laboratory of Systems Biology, Institute of Cybernetics, Tallinn University of Technology, Akadeemia Rd 21, 12618 Tallinn, Estonia

Tài liệu tham khảo

Weiss, 2001, The cytoplasm: no longer a well-mixed bag, Circ. Res., 89, 108, 10.1161/res.89.2.108 Ventura-Clapier, 2011, Bioenergetics of the failing heart, BBA-Mol. Cell Res., 1813, 1360 Kushmerick, 1969, Ionic mobility in muscle cells, Science, 166, 1297, 10.1126/science.166.3910.1297 Meyer, 1984, A simple analysis of the “phosphocreatine shuttle”, AJP: Cell Physiol., 246, C365 Kinsey, 2011, Molecules in motion: influences of diffusion on metabolic structure and function in skeletal muscle, J. Exp. Biol., 214, 263, 10.1242/jeb.047985 Bessman, 1981, Transport of energy in muscle: the phosphorylcreatine shuttle, Science, 211, 448, 10.1126/science.6450446 Glancy, 2015, Mitochondrial reticulum for cellular energy distribution in muscle, Nature, 523, 617, 10.1038/nature14614 Akki, 2012, Creatine kinase overexpression improves ATP kinetics and contractile function in postischemic myocardium, Am. J. Physiol. Heart Circ. Physiol., 303, H844, 10.1152/ajpheart.00268.2012 Eisner, 2014, Mitochondrial fusion is frequent in skeletal muscle and supports excitation–contraction coupling, J. Cell Biol., 205, 179, 10.1083/jcb.201312066 Gudbjarnason, 1970, Functional compartmentation of ATP and creatine phosphate in heart muscle, J. Mol. Cell. Cardiol., 1, 325, 10.1016/0022-2828(70)90009-X Fischmeister, 2006, Compartmentation of cyclic nucleotide signaling in the heart the role of cyclic nucleotide phosphodiesterases, Circ. Res., 99, 816, 10.1161/01.RES.0000246118.98832.04 Csordás, 2009, Sr/er–mitochondrial local communication: calcium and ros, BBA-Bioenerg., 1787, 1352, 10.1016/j.bbabio.2009.06.004 Silverman, 2003, Is there a transient rise in sub-sarcolemmal Na and activation of Na/K pump current following activation of I(Na) in ventricular myocardium?, Cardiovasc. Res., 57, 1025, 10.1016/S0008-6363(02)00645-4 Abraham, 2002, Coupling of cell energetics with membrane metabolic sensing, J. Biol. Chem., 277, 24427, 10.1074/jbc.M201777200 Veksler, 1987, Mitochondrial respiratory parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibers, BBA, 892, 191 Kümmel, 1988, Ca,Mg-ATPase activity of permeabilized rat heart cells and its functional coupling to oxidative phosphorylation of the cells, Cardiovasc. Res., 22, 359, 10.1093/cvr/22.5.359 Kuznetsov, 2008, Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells, Nat. Protoc., 3, 965, 10.1038/nprot.2008.61 Jepihhina, 2011, Permeabilized rat cardiomyocyte response demonstrates intracellular origin of diffusion obstacles, Biophys. J., 101, 2112, 10.1016/j.bpj.2011.09.025 Branovets, 2013, Unchanged mitochondrial organization and compartmentation of high-energy phosphates in creatine-deficient GAMT−/− mouse hearts, Am. J. Physiol. Heart Circ. Physiol., 305, H506, 10.1152/ajpheart.00919.2012 Seppet, 2001, Functional complexes of mitochondria with Ca,MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells, BBA, 1504, 379 Kaasik, 2001, Energetic crosstalk between organelles: architectural integration of energy production and utilization, Circ. Res., 89, 153, 10.1161/hh1401.093440 Saks, 2001, Intracellular energetic units in red muscle cells, Biochem. J., 356, 643, 10.1042/bj3560643 Sepp, 2014, Tight coupling of Na+/K+-ATPase with glycolysis demonstrated in permeabilized rat cardiomyocytes, PLoS One, 9, 10.1371/journal.pone.0099413 Saks, 2003, Heterogeneity of adp diffusion and regulation of respiration in cardiac cells, Biophys. J., 84, 3436, 10.1016/S0006-3495(03)70065-4 Vendelin, 2004, Intracellular diffusion of adenosine phosphates is locally restricted in cardiac muscle, Mol. Cell. Biochem., 256, 229, 10.1023/B:MCBI.0000009871.04141.64 Kay, 1997, Early alteration of the control of mitochondrial function in myocardial ischemia, J. Mol. Cell. Cardiol., 29, 3399, 10.1006/jmcc.1997.0564 Kay, 1997, Alteration in the control of mitochondrial respiration by outer mitochondrial membrane and creatine during heart preservation, Cardiovasc. Res., 34, 547, 10.1016/S0008-6363(97)00058-8 Boudina, 2002, Alteration of mitochondrial function in a model of chronic ischemia in vivo in rat heart, Am. J. Physiol. Heart Circ. Physiol., 282, H821, 10.1152/ajpheart.00471.2001 Laclau, 2001, Cardioprotection by ischemic preconditioning preserves mitochondrial function and functional coupling between adenine nucleotide translocase and creatine kinase, J. Mol. Cell. Cardiol., 33, 947, 10.1006/jmcc.2001.1357 Rostovtseva, 2008, Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration, PNAS, 105, 18746, 10.1073/pnas.0806303105 Gurnev, 2011, Tubulin-blocked state of VDAC studied by polymer and ATP partitioning, FEBS Lett., 585, 2363, 10.1016/j.febslet.2011.06.008 Gonzalez-Granillo, 2012, Studies of the role of tubulin beta II isotype in regulation of mitochondrial respiration in intracellular energetic units in cardiac cells, J. Mol. Cell. Cardiol., 52, 437, 10.1016/j.yjmcc.2011.07.027 Guzun, 2011, Mitochondria-cytoskeleton interaction: distribution of beta-tubulins in cardiomyocytes and HL-1 cells, BBA, 1807, 458 Vendelin, 2004, Intracellular diffusion of adenosine phosphates is locally restricted in cardiac muscle, Mol. Cell. Biochem., 256–257, 229, 10.1023/B:MCBI.0000009871.04141.64 Birkedal, 2014, The location of energetic compartments affects energetic communication in cardiomyocytes, Front. Physiol., 5, 376, 10.3389/fphys.2014.00376 Illaste, 2012, Analysis of molecular movement reveals latticelike obstructions to diffusion in heart muscle cells, Biophys. J., 102, 739, 10.1016/j.bpj.2012.01.012 Ramay, 2009, Diffusion restrictions surrounding mitochondria: a mathematical model of heart muscle fibers, Biophys. J., 97, 443, 10.1016/j.bpj.2009.04.062 Sepp, 2010, ADP compartmentation analysis reveals coupling between pyruvate kinase and ATPases in heart muscle, Biophys. J., 98, 2785, 10.1016/j.bpj.2010.03.025 Schöberl, 1997, Netgen an advancing front 2d/3d-mesh generator based on abstract rules, Comput. Vis. Sci., 1, 41, 10.1007/s007910050004 Logg, 2012 Laasmaa, 2011, Application of regularized Richardson-Lucy algorithm for deconvolution of confocal microscopy images, J. Microsc., 243, 124, 10.1111/j.1365-2818.2011.03486.x Aliev, 2002, Water content and its intracellular distribution in intact and saline perfused rat hearts revisited, Cardiovasc. Res., 53, 48, 10.1016/S0008-6363(01)00474-6 Birkedal, 2006, Three-dimensional mitochondrial arrangement in ventricular myocytes: from chaos to order, Am. J. Physiol. Cell. Physiol., 291, C1148, 10.1152/ajpcell.00236.2006 Rostovtseva, 1996, ATP flux is controlled by a voltage-gated channel from the mitochondrial outer membrane, J. Biol. Chem., 271, 28006, 10.1074/jbc.271.45.28006 Lemasters, 1762, Voltage-dependent anion channel (VDAC) as mitochondrial governator—thinking outside the box, BBA-Mol. Basis Dis., 2006, 181 Rostovtseva, 1997, VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function, Biophys. J., 72, 1954, 10.1016/S0006-3495(97)78841-6 Maldonado, 2013, Voltage-dependent anion channels modulate mitochondrial metabolism in cancer cells regulation by free tubulin and erastin, J. Biol. Chem., 288, 11920, 10.1074/jbc.M112.433847 Seppet, 2001, Functional complexes of mitochondria with Ca,MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells, BBA-Bioenerg., 1504, 379, 10.1016/S0005-2728(00)00269-3 de Graaf, 2000, In vivo 31P-NMR diffusion spectroscopy of ATP and phosphocreatine in rat skeletal muscle, Biophys. J., 78, 1657, 10.1016/S0006-3495(00)76717-8 Vendelin, 2008, Anisotropic diffusion of fluorescently labeled ATP in rat cardiomyocytes determined by raster image correlation spectroscopy, Am. J. Physiol. Cell. Physiol., 295, C1302, 10.1152/ajpcell.00313.2008 Samartsev, 2003, Temperature dependence of rat liver mitochondrial respiration with uncoupling of oxidative phosphorylation by fatty acids. Influence of inorganic phosphate, Biochem. Mosc., 68, 618, 10.1023/A:1024657507814 Biró, 2010, Comparing the temperature-dependent conductance of the two structurally similar E. coli porins OmpC and OmpF, Biophys. J., 98, 1830, 10.1016/j.bpj.2010.01.026 Nestorovich, 2012, Kinetics and thermodynamics of binding reactions as exemplified by anthrax toxin channel blockage with a cationic cyclodextrin derivative, PNAS, 109, 18453, 10.1073/pnas.1208771109 Vendelin, 2000, Regulation of mitochondrial respiration in heart cells analyzed by reaction-diffusion model of energy transfer, Am. J. Physiol. Cell. Physiol., 278, C747, 10.1152/ajpcell.2000.278.4.C747 Vendelin, 2010, Modulation of energy transfer pathways between mitochondria and myofibrils by changes in performance of perfused heart, J. Biol. Chem., 285, 37240, 10.1074/jbc.M110.147116 Schneider, 2008, Cardiac structure and function during ageing in energetically compromised guanidinoacetate N-methyltransferase (GAMT)-knockout mice - a one year longitudinal mri study, J. Cardiovasc. Magn. Reson., 10, 9, 10.1186/1532-429X-10-9 Lygate, 2013, Living without creatine: unchanged exercise capacity and response to chronic myocardial infarction in creatine-deficient mice, Circ. Res., 112, 945, 10.1161/CIRCRESAHA.112.300725 Suga, 1990, Ventricular energetics, Physiol. Rev., 70, 247, 10.1152/physrev.1990.70.2.247 Tan, 2007, Vdac closure increases calcium ion flux, Biochim. Biophys. Acta Biomembr., 1768, 2510, 10.1016/j.bbamem.2007.06.002 Vendelin, 2000, Cardiac mechanoenergetics replicated by cross-bridge model, Ann. Biomed. Eng., 28, 629, 10.1114/1.1305910 Kalda, 2015, Cross-bridge group ensembles describing cooperativity in thermodynamically consistent way, PLoS One, 10, 10.1371/journal.pone.0137438