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

Journal of Molecular and Cellular Cardiology

Volumn 49, Issue 4, 2010, Pages 565-575

  Lyon, Alexander R ^a   Joudrey, Paul J ^a   Jin, Dongzhu ^a   Nass, Robert D ^a   Aon, Miguel A ^b   'Rourke, Brian ^b   Akar, Fadi G ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Energetics; Mitochondria; Mitochondrial membrane potential; Oxidative stress

Indexed keywords

LACTATE DEHYDROGENASE;

ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL ENERGY; CELL MEMBRANE DEPOLARIZATION; CELL METABOLISM; CONTROLLED STUDY; ENZYME RELEASE; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; IMAGING; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY;

ANIMALS; CARDIAC ELECTROPHYSIOLOGY; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; OXIDATIVE STRESS; RATS;

EID: 77956178165     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2010.07.002     Document Type: Article

References (34)

1. Gustafsson A.B., Gottlieb R.A. Heart mitochondria: gates of life and death. Cardiovasc Res 2008, 77(2):334-343.
2. Honda H.M., Korge P., Weiss J.N. Mitochondria and ischemia/reperfusion injury. Ann NY Acad Sci 2005, 1047:248-258.
3. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443(7113):787-795.
4. Murphy E., Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 2008, 88(2):581-609.
5. Danial N.N., Korsmeyer S.J. Cell death: critical control points. Cell 2004, 116(2):205-219.
6. Fatokun A.A., Stone T.W., Smith R.A. Oxidative stress in neurodegeneration and available means of protection. Front Biosci 2008, 13:3288-3311.
7. Scaduto R.C., Grotyohann L.W. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 1999, 76(1 Pt 1):469-477.
8. Zorov D.B., Kobrinsky E., Juhaszova M., Sollott S.J. Examining intracellular organelle function using fluorescent probes: from animalcules to quantum dots. Circ Res 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 2006, 114(14):1497-1503.
10. Brown D.A., Aon M.A., Akar F.G., 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 2008, 79(1):141-149.
11. Akar F.G., Aon M.A., Tomaselli G.F., O'Rourke B. Spatial heterogeneity of the mitochondrial membrane potential underlies reperfusion related arrhythmias. Circulation 2006, 114(18):269.
12. Jin H.W.C.E., Lyon A., Stocks J., Akar F.G. Spatial heterogeneity of the mitochondrial membrane potential underlying arrhythmias in pressure overload hypertrophy. Circulation 2008, 118(18):S531.
13. Lyon A.R.P.J., Liang L.F., Hajjar R.J., Akar F.G. 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 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 2001, 280(2):H499-H508.
17. Severs N.J. The cardiac muscle cell. Bioessays 2000, 22(2):188-199.
18. Weiss J.N., Korge P., Honda H.M., Ping P. Role of the mitochondrial permeability transition in myocardial disease. Circ Res 2003, 93(4):292-301.
19. O'Rourke B. Mitochondrial ion channels. Annu Rev Physiol 2007, 69:19-49.
20. Zorov D.B., Filburn C.R., Klotz L.O., Zweier J.L., Sollott S.J. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 2000, 192(7):1001-1014.
21. Brady N.R., Elmore S.P., van Beek J.J., Krab K., Courtoy P.J., Hue L., et al. Coordinated behavior of mitochondria in both space and time: a reactive oxygen species-activated wave of mitochondrial depolarization. Biophys J 2004, 87(3):2022-2034.
22. Aon M.A., 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 2003, 278(45):44735-44744.
23. Aon M.A., Cortassa S., O'Rourke B. The fundamental organization of cardiac mitochondria as a network of coupled oscillators. Biophys J 2006, 91(11):4317-4327.
24. Weiss J.N., Venkatesh N. Metabolic regulation of cardiac ATP-sensitive K+ channels. Cardiovasc Drugs Ther 1993, 7(Suppl 3):499-505.
25. Akar F.G., Aon M.A., Tomaselli G.F., O'Rourke B. The mitochondrial origin of postischemic arrhythmias. J Clin Invest 2005, 115(12):3527-3535.
26. Park M., Shen Y.T., Gaussin V., Heyndrickx G.R., Bartunek J., Resuello R.R., et al. Apoptosis predominates in nonmyocytes in heart failure. Am J Physiol 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 2001, 104(3):253-256.
28. Aon M.A., Cortassa S., Akar F.G., O'Rourke B. Mitochondrial criticality: a new concept at the turning point of life or death. Biochim Biophys Acta 2006, 1762(2):232-240.
29. Weiss J.N., Yang L., Qu Z. Systems biology approaches to metabolic and cardiovascular disorders: network perspectives of cardiovascular metabolism. J Lipid Res 2006, 47(11):2355-2366.
30. Girouard S.D., Laurita K.R., Rosenbaum D.S. Unique properties of cardiac action potentials recorded with voltage-sensitive dyes. J Cardiovasc Electrophysiol 1996, 7(11):1024-1038.
31. Akar F.G., Rosenbaum D.S. Transmural electrophysiological heterogeneities underlying arrhythmogenesis in heart failure. Circ Res 2003, 93(7):638-645.
32. Akar F.G., Yan G.X., Antzelevitch C., Rosenbaum D.S. Unique topographical distribution of M cells underlies reentrant mechanism of torsade de pointes in the long-QT syndrome. Circulation 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 1987, 252(2 Pt 2):H384-H394.
34. Lu L.S., Liu Y.B., Sun C.W., Lin L.C., Su M.J., Wu C.C. Optical mapping of myocardial reactive oxygen species production throughout the reperfusion of global ischemia. J Biomed Opt 2006, 11(2):021012.