Multistationary and Oscillatory Modes of Free Radicals Generation by the Mitochondrial Respiratory Chain Revealed by a Bifurcation Analysis

PLoS Computational Biology

Volumn 8, Issue 9, 2012, Pages

  Selivanov, Vitaly A ^a,b   Cascante, Marta ^a   Friedman, Mark ^c   Schumaker, Mark F ^d   Trucco, Massimo ^e   Votyakova, Tatyana V ^e  

^a UNIVERSITY OF BARCELONA   (Spain)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF ALABAMA IN HUNTSVILLE   (United States)

^d WASHINGTON STATE UNIVERSITY   (United States)

^e CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIFURCATION (MATHEMATICS); BIOELECTRIC POTENTIALS; CHAINS; ELECTRON TRANSPORT PROPERTIES; FREE RADICAL REACTIONS; FREE RADICALS; MITOCHONDRIA; ORDINARY DIFFERENTIAL EQUATIONS; PHYSIOLOGY;

BIFURCATION ANALYSIS; ENERGY; FREE RADICAL GENERATION; MITOCHONDRIAL ELECTRON TRANSPORT CHAIN; MITOCHONDRIAL RESPIRATORY CHAIN; MITOCHONDRIAS; OSCILLATORY MODE; REACTIVE OXYGEN SPECIES; RESPIRATORY CHAINS; RESPIRATORY COMPLEX;

METABOLISM;

FREE RADICAL; REACTIVE OXYGEN METABOLITE; SUCCINIC ACID;

ALGORITHM; ARTICLE; AUTOREGULATION; BIFURCATION ANALYSIS; CELL METABOLISM; CITRIC ACID CYCLE; MATHEMATICAL ANALYSIS; MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION SWELLING; OSCILLATION; OXIDATION REDUCTION STATE; PREDICTION; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; TIME;

EID: 84866950334     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002700     Document Type: Article

References (37)

1. Mitchell P, (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191: 144-148.
2. Turrens JF, Alexandre A, Lehninger AL, (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237: 408-414.
3. Li C, Jackson RM, (2002) Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol 282: C227-C241.
4. Bottino R, Balamurugan AN, Tse H, Thirunavukkarasu C, Ge X, et al. (2004) Response of human islets to isolation stress and the effect of antioxidant treatment. Diabetes 53: 2559-2568.
5. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, et al. (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1: 401-408.
6. Cai J, Jones DP, (1999) Mitochondrial redox signaling during apoptosis. J Bioenerg Biomembr 31: 327-334.
7. Griffiths HR, Dunston CR, Bennett SJ, Grant MM, Phillips DC, et al. (2011) Free radicals and redox signalling in T-cells during chronic inflammation and ageing. Biochem Soc Trans 39: 1273-1278.
8. Gupta S, Dhiman M, Wen JJ, Garg NJ, (2011) ROS signalling of inflammatory cytokines during Trypanosoma cruzi infection. Adv Parasitol 76: 153-170.
9. Brand MD, Nicholls DG, (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435: 297-312.
10. Selivanov VA, Votyakova TV, Zeak JA, Trucco M, Roca J, et al. (2009) Bistability of mitochondrial respiration underlies paradoxical reactive oxygen species generation induced by anoxia. PLoS Comput Biol 5: e1000619.
11. Loor G, Kondapalli J, Iwase H, Chandel NS, Waypa GB, et al. (2011) Mitochondrial oxidant stress triggers cell death in simulated ischemia-reperfusion. Biochim Biophys Acta 1813: 1382-1394.
12. Selivanov VA, Votyakova TV, Pivtoraiko VN, Zeak J, Sukhomlin T, et al. (2011) Reactive oxygen species production by forward and reverse electron fluxes in the mitochondrial respiratory chain. PLoS Comput Biol 7: e1001115.
13. 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.
14. Zorov DB, Juhaszova M, Sollott SJ, (2006) Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta 1757: 509-517.
15. Aon MA, Cortassa S, Marbán 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.
16. Kummer U, Olsen LF, Dixon CJ, Green AK, Bornberg-Bauer E, et al. (2000) Switching from simple to complex oscillations in calcium signaling. Biophys J 79: 1188-1195.
17. Bindel D, Demmel J, Friedman M, Govaerts W, Kuznetsov YuA (2005) Bifurcation analysis of large equilibrium systems in Matlab. In: Sunderam VS, editor. Proceedings of the International Conference on Computational Science ICCS. Part I. Atlanta: Springer Verlag. pp. 50-57.
18. Bindel D, Demmel J, Friedman M, (2008) Continuation of Invariant Subspaces in Large Scale Bifurcation Problems,. SIAM J Sci Comp 30: 637-656.
19. Li K, Zhang W, Fang H, Xie W, Liu J, et al. (2012) Superoxide flashes reveal novel properties of mitochondrial reactive oxygen species excitability in cardiomyocytes. Biophys J 102: 1011-1021.
20. Wang X, Jian C, Zhang X, Huang Z, Xu J, et al. (2012) Superoxide flashes: Elemental events of mitochondrial ROS signaling in the heart. J Mol Cell Cardiol 52: 940-948.
21. Ma Q, Fang H, Shang W, Liu L, Xu Z, et al. (2011) Superoxide flashes: early mitochondrial signals for oxidative stress-induced apoptosis. J Biol Chem 286: 27573-27581.
22. Fang H, Chen M, Ding Y, Shang W, Xu J, et al. (2011) Imaging superoxide flash and metabolism-coupled mitochondrial permeability transition in living animals. Cell Res 21: 1295-1304.
23. Sheu SS, Wang W, Cheng H, Dirksen RT, (2008) Superoxide flashes: illuminating new insights into cardiac ischemia/reperfusion injury. Future Cardiol 4: 551-554.
24. Slodzinski MK, Aon MA, O'Rourke B, (2008) Glutathione oxidation as a trigger of mitochondrial depolarization and oscillation in intact hearts. J Mol Cell Cardiol 45: 650-660.
25. Wang W, Fang H, Groom L, Cheng A, Zhang W, et al. (2008) Superoxide flashes in single mitochondria. Cell 134: 279-290.
26. Zhou L, Aon MA, Almas T, Cortassa S, Winslow RL, et al. (2010) A reaction-diffusion model of ROS-induced ROS release in a mitochondrial network. PLoS Comput Biol 6: e1000657.
27. Selivanov VA, Ichas F, Holmuhamedov EL, Jouaville LS, Evtodienko YV, et al. (1998) A model of mitochondrial Ca(2+)-induced Ca2+ release simulating the Ca2+ oscillations and spikes generated by mitochondria. Biophys Chem 72: 111-121.
28. Khalfaoui-Hassani B, Lanciano P, Lee DW, Darrouzet E, Daldal F, (2012) Recent advances in cytochrome bc(1): Inter monomer electronic communication? FEBS Lett 586: 617-621.
29. Shinkarev VP, Wraight CA, (2007) Intermonomer electron transfer in the bc1 complex dimer is controlled by the energized state and by impaired electron transfer between low and high potential hemes. FEBS Lett 581: 1535-1541.
30. Orii Y, Miki T, (1997) Oxidation process of bovine heart ubiquinol-cytochrome c reductase as studied by stopped-flow rapid-scan spectrophotometry and simulations based on the mechanistic Q cycle model. J Biol Chem 272: 17594-17604.
31. Moser CC, Page CC, Dutton PL, (2006) Darwin at the molecular scale: selection and variance in electron tunneling proteins including cytochrome c oxidase. Philos Trans R Soc Lond B Biol Sci 361: 1295-305.
32. Marcus RA, Sutin N, (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811: 265-322.
33. Huang L-S, Cobessi D, Tung EY, Berry EA, (2005) Binding of the respiratory chain inhibitor antimycin to the mitochondrial bc1 complex: a new crystal structure reveals an altered intramolecular hydrogen-bonding pattern. J Mol Biol 351: 573-597.
34. Beeckmans S, Kanarek L, (1981) Demonstration of physical interactions between consecutive enzymes of the citric acid cycle and of the aspartate-malate shuttle. A study involving fumarase, malate dehydrogenase, citrate synthesis and aspartate aminotransferase. Eur J Biochem 117: 527-535.
35. Beeckmans S, Van Driessche E, Kanarek L, (1989) The visualization by affinity electrophoresis of a specific association between the consecutive citric acid cycle enzymes fumarase and malate dehydrogenase. Eur J Biochem 183: 449-454.
36. Petzold LR (1983) A description of DASSL: A differential/algebraic system solver. In: Stepleman RS, editor. Scientific Computing. Amsterdam: North- Holland. pp. 65-68.
37. Votyakova TV, Reynolds IJ, (2005) Ca2+-induced permeabilization promotes free radical release from rat brain mitochondria with partially inhibited complex I. J Neurochem 93: 526-537.