Mitochondrial oscillations in physiology and pathophysiology.
Oscillations in chemical reactions and metabolic pathways have historically served as prototypes for understanding the dynamics of complex nonlinear systems. This chapter reviews the oscillatory behavior of mitochondria, with a focus on the mitochondrial oscillator dependent on reactive oxygen species (ROS), as first described in heart cells. Experimental and theoretical evidence now indicates that mitochondrial energetic variables oscillate autonomously as part of a network of coupled oscillators under both physiological and pathological conditions. The physiological domain is characterized by small-amplitude oscillations in mitochondrial membrane potential (delta psi(m)) showing correlated behavior over a wide range of frequencies, as determined using Power Spectral Analysis and Relative Dispersion Analysis of long term recordings of delta psi(m). Under metabolic stress, when the balance between ROS generation and ROS scavenging is perturbed, the mitochondrial network throughout the cell locks to one main low-frequency, high-amplitude oscillatory mode. This behavior has major pathological implications because the energy dissipation and cellular redox changes that occur during delta psi(m) depolarization result in suppression of electrical excitability and Ca2+ handling, the two main functions of the cardiac cell. In an ischemia/reperfusion scenario these alterations scale up to the level of the whole organ, giving rise to fatal arrhythmias.
Aon
Miguel A
MA
Division of Cardiology, Institute of Molecular Cardiobiology, The Johns Hopkins University Baltimore, Maryland, USA.
Cortassa
Sonia
S
O'Rourke
Brian
B
D000818:Animals; D001145:Arrhythmias, Cardiac / Q000503:physiopathology; D001683:Biological Clocks / Q000502:physiology*; D006801:Humans; D007473:Ion Channels / Q000378:metabolism; D017136:Ion Transport; D008928:Mitochondria / Q000378:metabolism*; D008929:Mitochondria, Heart / Q000378:metabolism; D008954:Models, Biological; D032383:Myocytes, Cardiac / Q000378:metabolism; D018384:Oxidative Stress; D017382:Reactive Oxygen Species / Q000378:metabolism
D007473:Ion Channels; D017382:Reactive Oxygen Species
J Biol Chem. 1965 Jul;240:3170-81
14342349
Physiol Rev. 2004 Apr;84(2):431-88
15044680
Biochim Biophys Acta. 2006 Feb;1762(2):232-40
16242921
J Bioenerg Biomembr. 1992 Feb;24(1):77-90
1380509
Biochim Biophys Acta. 2006 May-Jun;1757(5-6):509-17
16829228
J Exp Med. 2000 Oct 2;192(7):1001-14
11015441
Biophys J. 2004 Sep;87(3):2060-73
15345581
Eur J Biochem. 1982 Nov;128(1):159-61
6293824
Arch Biochem Biophys. 1974 Aug;163(2):759-68
4414954
FEBS Lett. 1994 Jul 11;348(2):211-5
8034044
Biochim Biophys Acta. 1974 Dec 30;346(3-4):245-60
4280315
Biochem Biophys Res Commun. 1966 Aug 12;24(3):381-5
4961151
Cell Calcium. 1994 Feb;15(2):143-52
8149414
J Biol Chem. 1989 Jan 25;264(3):1508-15
2492277
Mitochondrion. 2003 Nov;3(3):139-46
16120353
J Physiol. 2001 May 15;533(Pt 1):227-36
11351030
Proc Natl Acad Sci U S A. 1964 Jun;51:1244-51
14215650
J Biol Chem. 1988 Mar 25;263(9):4254-8
2831225
Biophys J. 2003 Apr;84(4):2734-55
12668482
FEBS Lett. 2006 May 22;580(12):2830-5
16545376
Biophys J. 2003 Nov;85(5):3350-7
14581236
Biophys Chem. 1998 May 5;72(1-2):111-21
9652089
Biofizika. 1964;9:306-11
14206238
Mol Cell Biochem. 2004 Jan-Feb;256-257(1-2):169-84
14977179
Proc Natl Acad Sci U S A. 1964 Aug;52:337-41
14206600
Biophys J. 2006 Dec 1;91(11):4317-27
16980364
Biochem J. 1999 Oct 15;343 Pt 2:311-7
10510294
J Exp Biol. 1979 Aug;81:281-306
390081
Eur J Biochem. 1985 Dec 16;153(3):503-7
3935438
Membr Cell Biol. 2000;14(1):1-17
11051078
Biochim Biophys Acta. 1971 Aug 6;245(1):17-20
5132470
FEBS Lett. 1976 Jul 1;66(1):44-7
6337
J Physiol. 1999 Apr 1;516 ( Pt 1):1-17
10066918
Biochem Biophys Res Commun. 1965 Dec 9;21(5):497-502
4286527
J Biol Chem. 1987 Nov 5;262(31):15085-93
2444594
Biophys J. 1998 Apr;74(4):2129-37
9545072
Cell. 1995 Aug 11;82(3):415-24
7634331
Cell Biophys. 1984 Dec;6(4):263-77
6085560
Am J Physiol Cell Physiol. 2004 May;286(5):C1139-51
15075213
Annu Rev Biochem. 1971;40:237-58
4330578
FEBS J. 2005 Jun;272(11):2648-60
15943800
Arch Biochem Biophys. 1968 Apr;125(1):157-65
4296954
Biochem Soc Symp. 1999;66:167-79
10989666
Biochim Biophys Acta. 1957 Apr;24(1):19-26
13426197
Biophys J. 2004 Nov;87(5):3585-93
15315954
Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4447-52
15070738
Arch Biochem Biophys. 1966 Nov;117(2):381-93
4961739
Arch Biochem Biophys. 1968 Apr;125(1):166-74
4296955
Science. 1994 Aug 12;265(5174):962-6
8052856
Biochim Biophys Acta. 1964 May 11;86:427-8
14171029
Biochim Biophys Acta. 1965 Aug 24;105(2):265-78
4954638
Adv Exp Med Biol. 1995;382:165-74
8540393
J Cell Biol. 1998 Aug 24;142(4):975-88
9722610
Am J Physiol. 1998 Apr;274(4):C1174-84
9575814
Biophys J. 2003 Nov;85(5):3358-66
14581237
J Neurosci. 2001 Jul 15;21(14):5054-65
11438581
ScientificWorldJournal. 2001 Apr 04;1:133-45
12805697
FEMS Microbiol Rev. 2003 Oct;27(4):547-57
14550945
J Clin Invest. 2005 Dec;115(12):3527-35
16284648
Biophys J. 2005 Jul;89(1):107-19
15834002
Arch Biochem Biophys. 1966 Nov;117(2):451-65
5972828
J Biol Chem. 2003 Nov 7;278(45):44735-44
12930841
Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1618-23
9465065
Arch Biochem Biophys. 1968 Apr;125(1):151-6
4296953
Physiol Rev. 1999 Apr;79(2):609-34
10221990
Physiology (Bethesda). 2005 Oct;20:303-15
16174870
Biophys J. 1993 Dec;65(6):2396-407
8312478
J Physiol. 2000 Nov 15;529 Pt 1:23-36
11080248
J Exp Biol. 1979 Aug;81:217-79
390080