Journal of Molecular and Cellular Cardiology
Volume 49, Issue 4 , Pages 565-575 , October 2010

Optical imaging of mitochondrial function uncovers actively propagating waves of mitochondrial membrane potential collapse across intact heart

  • Alexander R. Lyon

      Affiliations

    • Cardiovascular Research Center, Mount Sinai School of Medicine, New York, NY, USA
    • ,
  • Paul J. Joudrey

      Affiliations

    • Cardiovascular Research Center, Mount Sinai School of Medicine, New York, NY, USA
    • ,
  • Dongzhu Jin

      Affiliations

    • Cardiovascular Research Center, Mount Sinai School of Medicine, New York, NY, USA
    • ,
  • Robert D. Nass

      Affiliations

    • Cardiovascular Research Center, Mount Sinai School of Medicine, New York, NY, USA
    • ,
  • Miguel A. Aon

      Affiliations

    • Division of Cardiology, Johns Hopkins University, Baltimore, MD, USA
    • ,
  • Brian O'Rourke

      Affiliations

    • Division of Cardiology, Johns Hopkins University, Baltimore, MD, USA
    • ,
  • Fadi G. Akar

      Affiliations

    • Cardiovascular Research Center, Mount Sinai School of Medicine, New York, NY, USA
    • Division of Cardiology, Johns Hopkins University, Baltimore, MD, USA
    • Corresponding Author InformationCorresponding author. Pharmacology and Systems Biology, Cardiovascular Research Center, Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, NY 10029, USA. Tel.: +1 212 241 9251; fax: +1 212 241 4080.

Received 19 November 2009 ,Revised 29 June 2010 ,Accepted 2 July 2010.

References 

  1. Gustafsson AB, Gottlieb RA. Heart mitochondria: gates of life and death. Cardiovasc Res. Jan 15 2008;77(2):334–343
  2. Honda HM, Korge P, Weiss JN. Mitochondria and ischemia/reperfusion injury. Ann NY Acad Sci. Jun 2005;1047:248–258
  3. Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature. Oct 19 2006;443(7113):787–795
  4. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia–reperfusion injury. Physiol Rev. Apr 2008;88(2):581–609
  5. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. Jan 23 2004;116(2):205–219
  6. Fatokun AA, Stone TW, Smith RA. Oxidative stress in neurodegeneration and available means of protection. Front Biosci. 2008;13:3288–3311
  7. Scaduto RC, Grotyohann LW. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J. Jan 1999;76(1 Pt 1):469–477
  8. Zorov DB, Kobrinsky E, Juhaszova M, Sollott SJ. Examining intracellular organelle function using fluorescent probes: from animalcules to quantum dots. Circ Res. Aug 6 2004;95(3):239–252
  9. Matsumoto-Ida M, Akao M, Takeda T, Kato M, Kita T. Real-time 2-photon imaging of mitochondrial function in perfused rat hearts subjected to ischemia/reperfusion. Circulation. Oct 3 2006;114(14):1497–1503
  10. Brown DA, Aon MA, Akar FG, Liu T, Sorarrain N, O'Rourke B. Effects of 4′-chlorodiazepam on cellular excitation–contraction coupling and ischaemia–reperfusion injury in rabbit heart. Cardiovasc Res. Jul 1 2008;79(1):141–149
  11. Akar FG, Aon MA, Tomaselli GF, O'Rourke B. Spatial heterogeneity of the mitochondrial membrane potential underlies reperfusion related arrhythmias. Circulation. 2006;114(18):269
  12. Jin HWCE, Lyon A, Stocks J, Akar FG. Spatial heterogeneity of the mitochondrial membrane potential underlying arrhythmias in pressure overload hypertrophy. Circulation. 2008;118(18):S531
  13. Lyon ARPJ, Liang LF, Hajjar RJ, Akar FG. Gene transfer of the peripheral type benzodiazepine receptor alters the spatio-temporal dynamics of the mitochondrial membrane potential (delta psi(M)) across the intact heart. Circulation. 2008;118(18):S528
  14. Kusuoka H, Marban E. Cellular mechanisms of myocardial stunning. Annu Rev Physiol. 1992;54:243–256
  15. Inserte J, Garcia-Dorado D, Ruiz-Meana M, Solares J, Soler J. The role of Na+–H+ exchange occurring during hypoxia in the genesis of reoxygenation-induced myocardial oedema. J Mol Cell Cardiol. Apr 1997;29(4):1167–1175
  16. Schneider S, Chen W, Hou J, Steenbergen C, Murphy E. Inhibition of p38 MAPK alpha/beta reduces ischemic injury and does not block protective effects of preconditioning. Am J Physiol. Feb 2001;280(2):H499–H508
  17. Severs NJ. The cardiac muscle cell. Bioessays. Feb 2000;22(2):188–199
  18. Weiss JN, Korge P, Honda HM, Ping P. Role of the mitochondrial permeability transition in myocardial disease. Circ Res. Aug 22 2003;93(4):292–301
  19. O'Rourke B. Mitochondrial ion channels. Annu Rev Physiol. 2007;69:19–49
  20. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med. Oct 2 2000;192(7):1001–1014
  21. Brady NR, Elmore SP, van Beek JJ, Krab K, Courtoy PJ, Hue L, et al. Coordinated behavior of mitochondria in both space and time: a reactive oxygen species-activated wave of mitochondrial depolarization. Biophys J. Sep 2004;87(3):2022–2034
  22. Aon MA, Cortassa S, Marban E, O'Rourke B. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J Biol Chem. Nov 7 2003;278(45):44735–44744
  23. Aon MA, Cortassa S, O'Rourke B. The fundamental organization of cardiac mitochondria as a network of coupled oscillators. Biophys J. Dec 1 2006;91(11):4317–4327
  24. Weiss JN, Venkatesh N. Metabolic regulation of cardiac ATP-sensitive K+ channels. Cardiovasc Drugs Ther. Aug 1993;7(Suppl 3):499–505
  25. Akar FG, Aon MA, Tomaselli GF, O'Rourke B. The mitochondrial origin of postischemic arrhythmias. J Clin Invest. Dec 2005;115(12):3527–3535
  26. Park M, Shen YT, Gaussin V, Heyndrickx GR, Bartunek J, Resuello RR, et al. Apoptosis predominates in nonmyocytes in heart failure. Am J Physiol. Aug 2009;297(2):H785–H791
  27. Scarabelli T, Stephanou A, Rayment N, Pasini E, Comini L, Curello S, et al. Apoptosis of endothelial cells precedes myocyte cell apoptosis in ischemia/reperfusion injury. Circulation. Jul 17 2001;104(3):253–256
  28. Aon MA, Cortassa S, Akar FG, O'Rourke B. Mitochondrial criticality: a new concept at the turning point of life or death. Biochim Biophys Acta. Feb 2006;1762(2):232–240
  29. Weiss JN, Yang L, Qu Z. Systems biology approaches to metabolic and cardiovascular disorders: network perspectives of cardiovascular metabolism. J Lipid Res. Nov 2006;47(11):2355–2366
  30. Girouard SD, Laurita KR, Rosenbaum DS. Unique properties of cardiac action potentials recorded with voltage-sensitive dyes. J Cardiovasc Electrophysiol. Nov 1996;7(11):1024–1038
  31. Akar FG, Rosenbaum DS. Transmural electrophysiological heterogeneities underlying arrhythmogenesis in heart failure. Circ Res. Oct 3 2003;93(7):638–645
  32. Akar FG, Yan GX, Antzelevitch C, Rosenbaum DS. Unique topographical distribution of M cells underlies reentrant mechanism of torsade de pointes in the long-QT syndrome. Circulation. Mar 12 2002;105(10):1247–1253
  33. Salama G, Lombardi R, Elson J. Maps of optical action potentials and NADH fluorescence in intact working hearts. Am J Physiol. Feb 1987;252(2 Pt 2):H384–H394
  34. Lu LS, Liu YB, Sun CW, Lin LC, Su MJ, Wu CC. Optical mapping of myocardial reactive oxygen species production throughout the reperfusion of global ischemia. J Biomed Opt. Mar–Apr 2006;11(2):021012

PII: S0022-2828(10)00251-8

doi: 10.1016/j.yjmcc.2010.07.002

Journal of Molecular and Cellular Cardiology
Volume 49, Issue 4 , Pages 565-575 , October 2010

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