Mitochondrial dynamics in heart cells: Very low amplitude high frequency fluctuations in adult cardiomyocytes and flow motion in non beating Hl-1 cells

Agutter PS, Malone PC, Wheatley DN (1995) Intracellular transport mechanisms: a critique of diffusion theory. J Theor Biol 176:261–272 Agutter PS, Malone PC, Wheatley DN (2000) Diffusion theory in biology: a relic of mechanistic materialism. J Hist Biol 33:71–111 Amchenkova AA, Bakeeva LE, Chentsov YS, Skulachev VP, Zorov DB (1988) Coupling membranes as energy-transmitting cables. Filamentous mitochondria in fibroblasts and mitochondrial clusters in cardiomyocytes. J Cell Biol 107:481–495 Anesti V, Scorrano L (2006) The relationship between mitochondrial shape and function and the cytoskeleton. Biochim Biophys Acta 1757:692–699 Anmann T, Guzun R, Beraud N, Pelloux S, Kuznetsov AV, Kogerman L, Kaambre T, Sikk P, Paju K, Peet N, Seppet E, Ojeda C, Tourneur Y, Saks V (2006) 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 1757:1597–1606 Aon MA, Cortassa S, Marban E, O’Rourke B (2003) Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J Biol Chem 278:44735–44744 Aon MA, Cortassa S, O’Rourke B (2004) Percolation and criticality in a mitochondrial network. Proc Natl Acad Sci USA 101:4447–4452 Aon MA, Cortassa SC, O’Rourke B (2006) The fundamental organization of cardiac mitochondria as a network of coupled oscillators. Biophys J 91:4317–4327 Aon MA, Cortassa S, O’Rourke B (2007) On the network properties of mitochondria. In: Saks V (ed) Molecular system bioenergetics, energy for life. Wiley-VCH, Weinheim, Germany, pp 111–135 Appaix F, Kuznetsov AV, Usson Y, Kay L, Andrienko T, Olivares J, Kaambre T, Sikk P, Margreiter R, Saks V (2003) Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria. Exp Physiology 88:175–190 Ball EH, Singer SJ (1982) Mitochondria are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc Natl Acad Sci USA 79:123–126 Benard G, Rossignol R (2008) Ultrastucture of mitochondria and its bearing on function and bioenergetics. Antioxid Redox Signal 10:1313–1342 Bereiter-Hahn J (1990) Behaviour of mitochondria in the living cell. Int Rev Cytol 122:1–63 Bereiter-Hahn J, Voth M (1994) Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc Res Tech 27:198–219 Birkedal R, Shiels HA, Vendelin M (2006) Three-dimensional mitochondrial arrangement in ventricular myocytes: from chaos to order. Am J Physiol Cell Physiol 291:C1148–C1158 Capetenaki Y (2002) Desmin cytoskeleton: a potential regulator of muscle mitochondrial behaviour and function. Trends Cardiovasc Med 12:339–348 Chan DC (2006) Mitochondria: dynamic organelles in disease, aging, and development. Cell 125:1241–1252 Chance B, Yoshioka T (1966) Sustained oscillations of ionic constituents of mitochondria. Arch Biochem Biophys 117:51–465 Chen H, Chomyn A, Chan DC (2005) Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 280:26185–26192 Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A, Terzic A (2007) Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med Suppl 1:S60–7 Chung S, Dzeja PP, Faustino RS, Terzic A (2008) Developmental restructuring of the creatine kinase system integrates mitochondrial energetics with stem cell cardiogenesis. Ann N Y Acad Sci 1147:254–63 Claycomb WC, Lanson NA Jr, Stallworth BS, Eeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr (1998) HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Nat Acad Sci USA 95:2979–2984 Collins TJ, Bootman MD (2003) Mitochondria are morphologically heterogeneous within cells. J Exp Biol 206:1993–2000 Collins TJ, Berridge MJ, Lipp P, Bootman MD (2002) Mitochondria are morphologically and functionally heterogeneous within cells. Embo J 21:1616–1627 Cortassa S, Aon MA, Marban E, Winslow RL, O’Rourke B (2003) An integrated model of cardiac mitochondrial energy metabolism and calcium dynamics. Biophys J 84:2734–2755 Cortassa S, Aon MA, Winslow RL, O’Rourke B (2004) A mitochondrial oscillator dependent on reactive oxygen species. Biophys J 87:2060–73 Csordás G, Renken C, Várnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnóczky G (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174:915–921 Dedov VN, Roufogalis BD (1999) Organisation of mitochondria in living sensory neurons. FEBS Lett 456:171–174 Dimmer KS, Scorrano L (2006) (De) constructing mitochondria: what for? Physiology (Bethesda) 21:233–241 Dzeja PP, Chung S, Terzic A (2007) Integration of adenylate kinase and glycolytic and glycogenolytic circuits in cellular energetics. In: Saks V (ed) Molecular system bioenergetics, energy for life. Wiley-VCH, Weinheim, Germany, pp 265–301 Eimre M, Paju K, Pelloux S, Beraud N, Roosimaa M, Kadaja L, Gruno M, Peet N, Orlova E, Remmelkoor R, Piirsoo A, Saks V, Seppet E (2008) Distinct organization of energy metabolism in HL-1 cardiac cell line and cardiomyocytes. Biochim Biophys Acta 1777:514–524 Einstein A (1905) Von der molerulärkinetichen theorie der wärme gefordete bewegung von in ruhenden flüssigkeiten suspendierten teilchen. Ann Phys (Leipzig) 17:549–560 Evtodienko YV (2000) Sustained oscillations of transmembrane Ca2+ fluxes in mitochondria and their possible significance. Membr Cell Biol 14:1–17 Floryk D, Houstĕk J (1999) Tetramethyl rhodamine methyl ester (TMRM) is suitable for cytofluorometric measurements of mitochondrial membrane potential in cells treated with digitonin. Biosci Rep 19:27–34 Fukuda N, Sasaki D, Ishiwata S, Kurihara S (2001) Length dependence of tension generation in rat skinned cardiac muscle: role of titin in the Frank-Starling mechanism of the heart. Circulation 104:1639–1645 Fukunaga K, Hostetler LD (1975) The estimation of the gradient of a density function, with applications in pattern recognition. IEEE Trans Inf Theory 21(2):32–39 Gerencser AA, Nicholls DG (2008) Measurement of instantaneous vectors of organelle transport: mitochondrial transport and bioenergetics in hippocampal neurons. Biophys J 95:3079–3099 Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80:853–924 Gordon AM, Regnier M, Homsher E (2001) Skeletal and cardiac muscle contractile activation: tropomyosin "rocks and rolls". News Physiol Sci 16:49–55 Hackenbrock CR (1966) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J Cell Biol 3:269–297 Hackenbrock CR (1968a) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. II. Electron transport-linked ultrastructural transformations in mitochondria. J Cell Biol 37:345–369 Hackenbrock CR (1968b) Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states. Proc Natl Acad Sci USA 61:598–605 Hajnóczky G, Csordás G, Madesh M, Pacher P (2000) The machinery of local Ca2+ signalling between sarco-endoplasmic reticulum and mitochondria. J Physiol 529:69–81 Hattori T, Watanabe K, Uechi Y, Yoshioka H, Ohta Y (2005) Repetitive transient depolarizations of the inner mitochondrial membrane induced by proton pumping. Biophys J 88:2340–9 Heggeness MH, Simon M, Singer SJ (1978) Association of mitochondria with microtubules in cultured cells. Proc Natl Acad Sci USA 75:3863–3866 Islam MA (2004) Einstein-Smoluchowski diffusion equation: a discussion. Physica Scripta 70:120–125 Karbowski M, Youle RJ (2003) Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ 10:870–80 Kay L, Li Z, Mericskay M, Olivares J, Tranqui L, Fontaine E, Tiivel T, Sikk P, Kaambre T, Samuel JL, Rappaport L, Usson Y, Leverve X, Paulin D, Saks VA (1997) Study of regulation of mitochondrial respiration in vivo. an analysis of influence of ADP diffusion and possible role of cytoskeleton. Biochim Biophys Acta 1322:41–59 Klingenberg M (2007) Transport viewed as a catalytic process. Biochimie 89:1042–1048 Klingenberg M (2008) The ADP and ATP transport in mitochondria and its carrier. Biochim Biophys acta 778:1978–2021 Kuznetsov AV (2007) Structural organization and dynamics of mitochondria in the cells in vivo. In: Saks V (ed) Molecular system bioenergetics, energy for life. Wiley-VCH, Weinheim, Germany, pp 137–162 Kuznetsov AV, Tiivel T, Sikk P, Käämbre T, Kay L, Daneshrad Z, Rossi A, Kadaja L, Peet N, Seppet E, Saks V (1996) Striking difference between slow and fast twitch muscles in the kinetics of regulation of respiration by ADP in the cells in vivo. Eur J Biochem 241:909–915 Kuznetsov AV, Troppmair J, Sucher R, Hermann M, Saks V, Margreiter R (2006) Mitochondrial subpopulations and heterogeneity revealed by confocal imaging: possible physiological role? Biochim Biophys Acta Bioener\getics 1757:686–691 Loew LM (1993) Confocal microscopy of potentiometric fluorescent dyes. Methods Cell Biol 38:194–209 Mannella CA (2001) The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Biophys Acta 1762:140–147 Mannella CA (2006) Structure and dynamics of the mitochondrial inner membrane cristae. Biochim Biophys Acta 1763:542–548 Mannella CA, Buttle K, Marko M (1997) Reconsidering mitochondrial structure: new views of an old organelle. Trends Biochem Sci 22:37–38 Margieantu D, Capaldi RA, Markus AH (2000) Dynamics of the mitochondrial reticulum in live cells using Fourier image correlation spectroscopy and digital video microscopy. Biophys J 79:1833–1849 McBride HM, Neuspiel M, Wasiak S (2006) Mitochondria: more than just a powerhouse. Curr Biol 16:R551–560 Milner DJ, Mavroidis M, Weisleder N, Capetanaki Y (2000) Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J Cell Biol 150:1283–1298 O'Reilly CM, Fogarty KE, Drummond RM, Tuft RA, Walsh JV Jr (2003) Quantitative analysis of spontaneous mitochondrial depolarizations. Biophys J 85:3350–3357 Pacher P, Csordás P, Schneider T, Hajnóczky G (2000) Quantification of calcium signal transmission from sarco-endoplasmic reticulum to the mitochondria. J Physiol 529:553–564 Pelloux S, Ojeda C, Tourneur Y (2005) An original method to quantify mitochondria movement in cultured cardiomyocytes. Comput Cardiol 32:813–816 Pelloux S, Robillard J, Ferrera R, Bilbaut A, Ojeda C, Saks V, Ovize M, Tourneur Y (2006) Non-beating HL-1 cells for confocal microscopy: application to mitochondrial functions during cardiac preconditioning. Progr Biophys Mol Biol 90:270–298 Petronilli V, Penzo D, Scorrano L, Bernardi P, Di Lisa F (2001) The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J Biol Chem 276:12030–4 Philbert J (2006) One and a half century of diffusion: Fick, Einstein, before and beyond. Diffus Fundam 4:6.1–6.19 Presley AD, Fuller KM, Arriaga EA (2003) MitoTracker Green labelling of mitochondrial proteins and their subsequent analysis by capillary electrophoresis with laser-induced fluorescence detection. J Chromatogr 793:141–150 Rasmussen UF, Vielwerth SE, Rasmussen HN (2004) Skeletal muscle bioenergetics: a comparative study of mitochondria isolated from pigeon pectoralis, rat soleus, rat biceps brachii, pig biceps femoris and human quadriceps. Comp Biochem Physiol A Mol Integr Physiol 137:435–46 Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280:1763–1766 Romashko DN, Marban E, O’Rourke B (1998) Subcellular metabolic transients and mitochondrial redox waves in heart cells. Proc Natl Acad Sci 95:1618–1623 Rostovtseva TK, Bezrukov S (2008) VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J Bioenerg Biomembr 40:163–170 Rostovtseva TK, Hassanzadeh E, Sheldon K, Monge C, Saks V, Bezrukov SM, Sackett S (2008) New role for an old protein: tubulin binding blocks the mitochondrial outer membrane voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci USA 105:18746–18751 Saks VA, Kuznetsov AV, Khuchua ZA, Vasilyeva EV, Belikova JO, Kesvatera T, Tiivel T (1995) 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 27:625–645 Saks VA, Kaambre T, Sikk P, Eimre M, Orlova E, Paju K, Piirsoo A, Appaix F, Kay L, Regitz-Zagrosek V, Fleck E, Seppet E (2001) Intracellular energetic units in red muscle cells. Biochem J 356:643–657 Saks V, Kuznetsov A, Andrienko T, Usson Y, Appaix F, Guerrero K, Kaambre T, Sikk P, Lemba M, Vendelin M (2003) Heterogeneity of ADP diffusion and regulation of respiration in cardiac cells. Biophys J 84:3436–3456 Saks V, Dzeja P, Schlattner U, Vendelin M, Terzic A, Wallimann T (2006) Cardiac system bioenergetics: metabolic basis of frank-starling law. J Physiol 571:253–273 Saks V, Monge C, Anmann T, Dzeja P (2007) Integrated and organized cellular energetic systems: theories of cell energetics, compartmentation and metabolic channeling. In: Saks V (ed) Molecular system bioenergetics, energy for life. Wiley-VCH, Weinheim, Germany, pp 59–110 Saks V, Beraud N, Wallimann T (2008) Metabolic compartmentation−a system level property of muscle cells: real problems of diffusion in living cells. Int J. Mol Sci 9:751–767 Scherer B, Klingenberg M (1974) Demonstration of the relationship between adenine nucleotide carrier and the structural changes of mitochondria as induced by adenosine 5’-diphosphate. Biochem 13:161–170 Seppet EK, Kaambre T, Sikk P, Tiivel T, Vija H, Tonkonogi M, Sahlin K, Kay L, Appaix F, Braun U, Eimre M, Saks VA (2001) Functional comlexes of mitochondria with Ca, MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells. Biochim Biophys Acta 1504:379–395 Shen T, Zhen M, Cao C, Chen C, Tang J, Zhang W, Cheng H, Chen KH, Xiao RP (2007) Mitofusin-2 is a major determinant of oxidative stress-mediated heart muscle cell apoptosis. J Biol Chem 282:23354–23361 Skulachev VP (1990) Power transmission along biological membranes. J Membr Biol 114:97–112 Skulachev VP (2001) Mitochondrial filaments and clusters as intracellular powertransmitting cables. Trends in Biochem Sci 26:23–29 Skulachev VP, Bakeeva LE, Chernyak BV, Domnina LV, Minin AA, Pletjushkina OY, Saprunova VB, Skulachev IV, Tsyplenkova VG, Vasiliev JM, Yaguzhinsky LS, Zorov DB (2004) Thread-grain transition of mitochondrial reticulum as a step of mitoptosis and apoptosis. Mol Cell Biochem 256–257:341–58 Sommer JR, Jennings RB (1986) Ultrastructure of cardiac muscle. In: Fozzard HA, Jennings RB, Haber E, Katz AM, Morgan H (eds) The heart and cardiovascular system. Scientific foundations. Raven, New York, pp 61–100 Stoner CD, Sirak HD (1973) Adenine nucleotide induced contraction of the inner mitochondrial membrane. J Cell Biol 56:51–64 Sun CN, Dhalla NS, Olson RE (1969) Formation of gigantic mitochondria in hypoxic isolated perfused rat hearts. Experimentia 25:763–764 Twig G, Graf SA, Wikstrom JD, Mohamed H, Haigh SE, Elorza A, Deutsch M, Zurgil N, Reynolds N, Shirihai OS (2006) Tagging and tracking individual networks within a complex mitochondrial web with photoactivatable GFP. Am J Physiol Cell Physiol 291:C176–C184 Twig G, Hyde B, And Shirihai OS (2008b) Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta 1777:1092–1097 Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS (2008a) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27:433–46 Vale RD (2003) The molecular motor toolbox for intracellular transport. Cell 112:467–480 Vale RD, Funatsu T, Pierce DW, Romberg L, Harada Y, Yanagida T (1996) Direct observation of single kinesin molecules moving along microtubules. Nature 380:451–453 Vendelin M, Birkedal R (2008) Anisotropic diffusion of fluorescently labeled ATP in rat cardiomyocytes determined by raster image correlation spectroscopy. Am J Physiol Cell Physiol 295:C1302–C1315 Vendelin M, Eimre M, Seppet E, Peet N, Andrienko T, Lemba M, Engelbrecht J, Seppet EK, Saks VA (2004) Intracellular diffusion of adenosine phosphates is locally restricted in cardiac muscle. Mol Cell Biochem 256(257):229–241 Vendelin M, Beraud N, Guerrero K, Andrienko T, Kuznetsov AV, Olivares J, Kay L, Saks VA (2005) Mitochondrial regular arrangement in muscle cells: a ‘‘crystal-like’’ pattern. Am J Physiol Cell Physiol 288:C757–767 Vergun O, Votyakova TV, Reynolds IJ (2003) Spontaneous changes in mitochondrial membrane potential in single isolated brain mitochondria. Biophys J 85:3358–3366 von Smoluchowski M (1906) Zür kinetichen theorie der brownschen molekulärbewegung und der suspensionen. Ann Der Physik 21:756–780 Wallimann T, Tokarska-Schlattner M, Neumann D, Epand R, Andres RH, Widmer HR, Hornemann T, Saks V, Agarkova I, Schlattner U (2007) 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. Wiley-VCH, Weinheim, Germany, pp 195–264 Wang W, Fang H, Groom L, Cheng A, Zhang W, Liu J, Wang X, Li K, Han P, Zheng M, Yin J, Wang W, Mattson MP, Kao JPY, Lakatta EK, Sheu SS, Ouyang K, Chen J, Dirksen RT, Cheng H (2008) Superoxide flashes in single mitochondrion. Cell 134:279–290 Weber NE, Blair PV (1970) Ultrastructural studies of beef heart mitochondria. II. Adenine nucleotide induced modifications of mitochondrial morphology. Biochem Biophys Res Commun 41:821–829 Weiss JN, Yang L, Qu Z (2006) Network perspectives of cardiovascular metabolism. J Lipid Research 47:2355–2366 White SM, Constantin PE, Claycomb WC (2006) Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am J Physiol Heart Circ Physiol 286:H823–829 Wiseman PW, Petersen NO (1999) Image correlation spectroscopy. II. Optimisation for ultrasensitive detection of pre-existing platelet-derived growth factor-beta receptor oligomers on intact cells. Biophys J 76:963–977 Wiseman PW, Brown CM, Webb DJ, Hebert B, Johnson NL, Squier JA, Ellisman MH, Horwitz AF (2005) Spatial mapping of integrin interactions and dynamics during cell migration by Image Correlation Microscopy. J Cell Sci 117:5521–5534 Yaffe MP (1999) The machinery of mitochondrial inheritance and behavior. Science 283:1493–1497 Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ (2000) Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192:1001–1014 Zorov DB, Kobrinsky E, Juhaszova M, Sollott SJ (2004) Examining intracellular organelle function using fluorescent probes: from animalcules to quantum dots. Circ Res 95:239–252