Complex oscillatory redox dynamics with signaling potential at the edge between normal and pathological mitochondrial function

Frontiers in Physiology

Volumn 5 JUL, Issue , 2014, Pages

  Kembro, Jackelyn M ^a   Cortassa, Sonia ^b   Aon, Miguel A ^b  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Complex oscillations; Hopf bifurcations; Mitochondrial energetic redox; Physiological and pathophysiological behavior; Redox environment; ROS signaling

Indexed keywords

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; THIOREDOXIN;

ARTICLE; CELL ENERGY; CELL FUNCTION; CONCENTRATION (PARAMETERS); DISORDERS OF MITOCHONDRIAL FUNCTIONS; EXTRACELLULAR MATRIX; MATHEMATICAL MODEL; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL ENERGETIC REDOX COMPUTATIONAL MODEL; MOLECULAR PATHOLOGY; OSCILLATORY POTENTIAL; OXIDATIVE STRESS; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; SIMULATION; SPECTROSCOPY; STEADY STATE;

EID: 84904326680     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00257     Document Type: Article

References (73)

1. Antila, E., and Westermarck, T. (1989). On the etiopathogenesis and therapy of Down syndrome. Int. J. Dev. Biol. 33, 183-188.
2. Aon, M. A. (2013). "Complex systems biology of networks: the riddle and the challenge". in Systems Biology of Metabolic and Signaling Networks. Energy, Mass and Information Transfer, eds M. A. Aon, V. Saks, and U. Schlattner (Heidelberg; New York; Dordrecht; London: Springer-Verlag Berlin Heidelberg), 19-35.
3. Aon, M. A., and Cortassa, S. (1997). Dynamic Biological Organization. Fundamentals as Applied to Cellular Systems. London: Chapman and Hall.
4. Aon, M. A., and Cortassa, S. (2012). Mitochondrial network energetics in the heart. Wiley Interdiscip. Rev. Syst. Biol. Med. 4, 599-613. doi: 10.1002/wsbm.1188.
5. Aon, M. A., Cortassa, S., Lemar, K. M., Hayes, A. J., and Lloyd, D. (2007b). Single and cell population respiratory oscillations in yeast: a 2-photon scanning laser microscopy study. FEBS Lett. 581, 8-14. doi: 10.1016/j.febslet.2006.11.068.
6. Aon, M. A., Cortassa, S., Marban, E., and 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. doi: 10.1074/jbc.M302673200.
7. Aon, M. A., Cortassa, S., and O'Rourke, B. (2004). Percolation and criticality in a mitochondrial network. Proc. Natl. Acad. Sci. U.S.A. 101:4447-4452. doi: 10.1073/pnas.0307156101.
8. Aon, M. A., Cortassa, S., and O'Rourke, B. (2006). The fundamental organization of cardiac mitochondria as a network of coupled oscillators. Biophys. J. 91, 4317-4327. doi: 10.1073/pnas.0307156101.
9. Aon, M. A., Cortassa, S., and O'Rourke, B. (2007a). On the Network Properties of Mitochondria, in Molecular System Bioenergetics: Energy for Life, ed V. Saks (KGaA, Weinheim: Wiley-VCH Verlag GmbH & Co.), 111-135. doi: 10.1002/9783527621095.ch4.
10. Aon, M. A., Cortassa, S., and O'Rourke, B. (2008b). Mitochondrial oscillations in physiology and pathophysiology. Adv. Exp. Med. Biol. 641, 98-117. doi: 10.1007/978-0-387-09794-7_8.
11. Aon, M. A., Cortassa, S., and O'Rourke, B. (2008c). "Is there a mitochondrial clock?" in Ultradian Rhythms from Molecules to Mind. A New Vision of Life, eds D. Lloyd and E. L. Rossi (New York, NY: Springer-Verlag), 129-144.
12. Aon, M. A., Roussel, M. R., Cortassa, S., O'Rourke, B., Murray, D. B., Beckmann, M., et al. (2008a). The scale-free dynamics of eukaryotic cells. PLoS ONE 3:e3624. doi: 10.1371/journal.pone.0003624.
13. Aon, M. A., Stanley, B. A., Sivakumaran, V., Kembro, J. M., O'Rourke, B., Paolocci, N., et al. (2012). Glutathione/thioredoxin systems modulate mitochondrial H2O2 emission: an experimental-computational study. J. Gen. Physiol. 139, 479-491. doi: 10.1085/jgp.201210772.
14. Balaban, R. S., Nemoto, S., and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483-495. doi: 10.1016/j.cell.2005.02.001.
15. Boveris, A., Oshino, N., and Chance, B. (1972). The cellular production of hydrogen peroxide. Biochem. J. 128, 617-630.
16. Chance, B., Sies, H., and Boveris, A. (1979). Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59, 527-605.
17. Cortassa, S., and Aon, M. A. (2013). "Dynamics of mitochondrial redox and energy networks: insights from an experimental-computational synergy". in Systems Biology of Metabolic and Signaling Networks. Energy, Mass and Information Transfer, eds M. A. Aon, V. Saks, and U. Schlattner (Heidelberg; New York; Dordrecht; London: Springer-Verlag Berlin Heidelberg), 115-144.
18. Cortassa, S., Aon, M. A., Winslow, R. L., and O'Rourke, B. (2004). A mitochondrial oscillator dependent on reactive oxygen species. Biophys. J. 87, 2060-2073. doi: 10.1529/biophysj.104.041749.
19. Cortassa, S., O'Rourke, B., and Aon, M. A. (2014). Redox-optimized ROS balance and the relationship between mitochondrial respiration and ROS. Biochim. Biophys. Acta 1837, 287-295. doi: 10.1016/j.bbabio.2013.11.007.
20. Craven, P. A., Melhem, M. F., Phillips, S. L., and DeRubertis, F. R. (2001a). Overexpression of Cu2+/Zn2+ superoxide dismutase protects against early diabetic glomerular injury in transgenic mice. Diabetes 50, 2114-2125. doi: 10.2337/diabetes.50.9.2114.
21. Craven, P. A., Phillips, S. L., Melhem, M. F., Liachenko, J., and DeRubertis, F. R. (2001b). Overexpression of manganese superoxide dismutase suppresses increases in collagen accumulation induced by culture of mesangial cells in high-media glucose. Metabolism 50, 1043-1048. doi: 10.1053/meta.2001.25802.
22. DeRubertis, F. R., Craven, P. A., Melhem, M. F., and Salah, E. M. (2004). Attenuation of renal injury in db/db mice overexpressing superoxide dismutase: evidence for reduced superoxide-nitric oxide interaction. Diabetes 53, 762-768. doi: 10.2337/diabetes.53.3.762.
23. Dhooge, A., Govaerts, W., Kuznetsov, Y. A., Meijer, H. G. E., and Sautois, B. (2008). New features of the software MATCONT for bifurcation analysis of dynamical systems. Math. Comp. Model Dyn. 14, 147-175. doi: 10.1080/13873950701742754.
24. Fannin, S. W., Lesnefsky, E. J., Slabe, T. J., Hassan, M. O., and Hoppel, C. L. (1999). Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch. Biochem. Biophys. 372, 399-407. doi: 10.1006/abbi.1999.1508.
25. Finkel, T. (2000). Redox-dependent signal transduction. FEBS Lett. 476, 52-54. doi: 10.1016/S0014-5793(00)01669-0.
26. Fukai, T., and Ushio-Fukai, M. (2011). Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid. Redox Signal. 15, 1583-1606. doi: 10.1089/ars.2011.3999.
27. Hoffman, D. L., and Brookes, P. S. (2009). Oxygen sensitivity of mitochondrial reactive oxygen species generation depends on metabolic conditions. J. Biol. Chem. 284, 16236-16245. doi: 10.1074/jbc.M809512200.
28. Hsu, J. L., Hsieh, Y., Tu, C., O'Connor, D., Nick, H. S., and Silverman, D. N. (1996). Catalytic properties of human manganese superoxide dismutase. J. Biol. Chem. 271, 17687-17691. doi: 10.1074/jbc.271.30.17687.
29. Jones, D. P., and Go, Y. M. (2010). Redox compartmentalization and cellular stress. Diabetes Obes. Metab. 12(Suppl. 2), 116-125. doi: 10.1111/j.1463-1326.2010.01266.x.
30. Judge, S., Jang, Y. M., Smith, A., Hagen, T., and Leeuwenburgh, C. (2005a). Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J. 19, 419-421. doi: 10.1096/fj.04-2622fje.
31. Judge, S., Jang, Y. M., Smith, A., Selman, C., Phillips, T., Speakman, J. R., et al. (2005b). Exercise by lifelong voluntary wheel running reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1564-R1572. doi: 10.1152/ajpregu.00396.2005.
32. Kanasewich, E. R. (1981). Time Sequence Analysis in Geophysics. Edmonton, AB: The University of Alberta Press.
33. Kaneko, K., and Tsuda, I. (2003). Chaotic itinerancy. Chaos 13, 926-936. doi: 10.1063/1.1607783.
34. Kembro, J. M., Aon, M. A., Winslow, R. L., O'Rourke, B., and Cortassa, S. (2013). Integrating mitochondrial energetics, redox and ROS metabolic networks: a two-compartment model. Biophys. J. 104, 332-343. doi: 10.1016/j.bpj.2012.11.3808.
35. Kembro, J. M., Cortassa, S., and Aon, M. A. (2014). "Mitochondrial reactive oxygen species and arrhythmias". in Systems Biology of Free Radicals and Antioxidants, ed I. Laher (Berlin-Heidelberg: Springer-Verla), 1047-1076.
36. Kierzenka, J., and Shampine, L. F. (eds.). (2011). deval.meditor. Natick, MA: The The MathWorks, Inc.
37. Kowluru, R. A., Atasi, L., and Ho, Y. S. (2006a). Role of mitochondrial superoxide dismutase in the development of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 47, 1594-1599. doi: 10.1167/iovs.05-1276.
38. Kowluru, R. A., Kowluru, V., Xiong, Y., and Ho, Y. S. (2006b). Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress. Free Radic. Biol. Med. 41, 1191-1196. doi: 10.1016/j.freeradbiomed.2006.01.012.
39. Kurz, F. T., Aon, M. A., O'Rourke, B., and Armoundas, A. A. (2010a). Spatio-temporal oscillations of individual mitochondria in cardiac myocytes reveal modulation of synchronized mitochondrial clusters. Proc. Natl. Acad. Sci. U.S.A. 107, 14315-14320. doi: 10.1073/pnas.1007562107.
40. Lakatta, E. G., and Sollott, S. J. (2002). Perspectives on mammalian cardiovascular aging: humans to molecules. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 132, 699-721. doi: 10.1016/S1095-6433(02)00124-1.
41. Lloyd, D., Aon, M. A., and Cortassa, S. (2001). Why homeodynamics, not homeostasis? Sci. World J. 1, 133-145. doi: 10.1100/tsw.2001.20.
42. Lloyd, D., Cortassa, S., O'Rourke, B., and Aon, M. A. (2012). What yeast and cardiomyocytes share: ultradian oscillatory redox mechanisms of cellular coherence and survival. Integr. Biol. (Camb) 4, 65-74. doi: 10.1039/c1ib00124h.
43. Lloyd, D., and Murray, D. B. (2007). Redox rhythmicity: clocks at the core of temporal coherence. Bioessays 29, 465-473. doi: 10.1002/bies.20575.
44. Lloyd, D., and Rossi, E. L. (2008). "Epilogue: a new vision of life". in Ultradian Rhythms from Molecules to Mind, ed E. L. Lloyd DaR (New York, NY: Springer Science+Business Media B.V), 431-439.
45. Lu, L., Oveson, B. C., Jo, Y. J., Lauer, T. W., Usui, S., Komeima, K., et al. (2009). Increased expression of glutathione peroxidase 4 strongly protects retina from oxidative damage. Antioxid. Redox Signal. 11, 715-724. doi: 10.1089/ars.2008.2171.
46. Massaad, C. A., Pautler, R. G., and Klann, E. (2009a). Mitochondrial superoxide: a key player in Alzheimer's disease. Aging (Albany NY) 1, 758-761.
47. Massaad, C. A., Washington, T. M., Pautler, R. G., and Klann, E. (2009b). Overexpression of SOD-2 reduces hippocampal superoxide and prevents memory deficits in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 106, 13576-13581. doi: 10.1073/pnas.0902714106.
48. McAdam, M. E., Levelle, F., Fox, R. A., and Fielden, E. M. (1977). A pulse-radiolysis study of the manganese-containing superoxide dismutase from Bacillus stearothermophilus. Biochem. J. 165, 81-87.
49. Melov, S., Doctrow, S. R., Schneider, J. A., Haberson, J., Patel, M., Coskun, P. E., et al. (2001). Lifespan extension and rescue of spongiform encephalopathy in superoxide dismutase 2 nullizygous mice treated with superoxide dismutase-catalase mimetics. J. Neurosci. 21, 8348-8353.
50. Misra, A., Haudek, S. B., Knuefermann, P., Vallejo, J. G., Chen, Z. J., Michael, L. H., et al. (2003). Nuclear factor-kappaB protects the adult cardiac myocyte against ischemia-induced apoptosis in a murine model of acute myocardial infarction. Circulation 108, 3075-3078. doi: 10.1161/01.CIR.0000108929.93074.0B.
51. Morel, Y., and Barouki, R. (1999). Repression of gene expression by oxidative stress. Biochem. J. 342(Pt 3), 481-496. doi: 10.1042/0264-6021:3420481.
52. Murray, D. B., and Lloyd, D. (2007). A tuneable attractor underlies yeast respiratory dynamics. Biosystems 90, 287-294. doi: 10.1016/j.biosystems.2006.09.032.
53. Paulsen, C. E., and Carroll, K. S. (2010). Orchestrating redox signaling networks through regulatory cysteine switches. ACS Chem. Biol. 5, 47-62. doi: 10.1021/cb900258z.
54. Prindle, A., Samayoa, P., Razinkov, I., Danino, T., Tsimring, L. S., and Hasty, J. (2012). A sensing array of radically coupled genetic 'biopixels'. Nature 481, 39-44. doi: 10.1038/nature10722.
55. Qu, Z. (2013). "Network dynamics in cardiac electrophysiology". in Systems Biology of Metabolic and Signaling Networks. Energy, Mass and Information Transfer, eds M. A. Aon, V. Saks, and U. Schlattner (Heidelberg; New York; Dordrecht; London: Springer-Verlag Berlin Heidelberg), 243-260.
56. Rodriguez, C., Mayo, J. C., Sainz, R. M., Antolin, I., Herrera, F., Martin, V., et al. (2004). Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res. 36, 1-9. doi: 10.1046/j.1600-079X.2003.00092.x.
57. Rolfe, D. F., and Brown, G. C. (1997). Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731-758.
58. Roussel, M. R., and Lloyd, D. (2007). Observation of a chaotic multioscillatory metabolic attractor by real-time monitoring of a yeast continuous culture. FEBS J. 274, 1011-1018. doi: 10.1111/j.1742-4658.2007.05651.x.
59. Sasidharan, K., Tomita, M., Aon, M., Lloyd, D., and Murray, D. B. (2012). Time-structure of the yeast metabolism in vivo. Adv. Exp. Med. Biol. 736, 359-379. doi: 10.1007/978-1-4419-7210-1_21.
60. Shigenaga, M. K., Hagen, T. M., and Ames, B. N. (1994). Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U.S.A. 91, 10771-10778. doi: 10.1073/pnas.91.23.10771.
61. Stanley, B. A., Sivakumaran, V., Shi, S., McDonald, I., Lloyd, D., Watson, W. H., et al. (2011). Thioredoxin reductase-2 is essential for keeping low levels of H(2)O(2) emission from isolated heart mitochondria. J. Biol. Chem. 286, 33669-33677. doi: 10.1074/jbc.M111.284612.
62. St-Pierre, J., Buckingham, J. A., Roebuck, S. J., and Brand, M. D. (2002). Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277, 44784-44790. doi: 10.1074/jbc.M207217200.
63. Suh, J. H., Heath, S. H., and Hagen, T. M. (2003). Two subpopulations of mitochondria in the aging rat heart display heterogenous levels of oxidative stress. Free Radic. Biol. Med. 35, 1064-1072. doi: 10.1016/S0891-5849(03)00468-4.
64. Sun, J., Molitor, J., and Tower, J. (2004). Effects of simultaneous over-expression of Cu/ZnSOD and MnSOD on Drosophila melanogaster life span. Mech. Ageing Dev. 125, 341-349. doi: 10.1016/j.mad.2004.01.009.
65. Sun, J., and Tower, J. (1999). FLP recombinase-mediated induction of Cu/Zn-superoxide dismutase transgene expression can extend the life span of adult Drosophila melanogaster flies. Mol. Cell. Biol. 19, 216-228.
66. Tribble, D. L., Gong, E. L., Leeuwenburgh, C., Heinecke, J. W., Carlson, E. L., Verstuyft, J. G., et al. (1997). Fatty streak formation in fat-fed mice expressing human copper-zinc superoxide dismutase. Arterioscler. Thromb. Vasc. Biol. 17, 1734-1740. doi: 10.1161/01.ATV.17.9.1734.
67. Usui, S., Komeima, K., Lee, S. Y., Jo, Y. J., Ueno, S., Rogers, B. S., et al. (2009). Increased expression of catalase and superoxide dismutase 2 reduces cone cell death in retinitis pigmentosa. Mol. Ther. 17, 778-786. doi: 10.1038/mt.2009.47.
68. Usui, S., Oveson, B. C., Iwase, T., Lu, L., Lee, S. Y., Jo, Y. J., et al. (2011). Overexpression of SOD in retina: need for increase in H2O2-detoxifying enzyme in same cellular compartment. Free Radic. Biol. Med. 51, 1347-1354. doi: 10.1016/j.freeradbiomed.2011.06.010.
69. Wei, A. C., Aon, M. A., O'Rourke, B., Winslow, R. L., and Cortassa, S. (2011). Mitochondrial energetics, pH regulation, and ion dynamics: a computational-experimental approach. Biophys. J. 100, 2894-2903. doi: 10.1016/j.bpj.2011.05.027.
70. West, B. J. (1999). Physiology, Promiscuity and Prophecy at the Millennium: A Tale of Tails. Singapore: World Scientific.
71. Yates, F. E. (1992). Fractal applications in biology: scaling time in biochemical networks. Methods Enzymol. 210, 636-675. doi: 10.1016/0076-6879(92)10032-9.
72. Zhou, L., Aon, M. A., Almas, T., Cortassa, S., Winslow, R. L., and O'Rourke, B. (2010). A reaction-diffusion model of ROS-induced ROS release in a mitochondrial network. PLoS Comput. Biol. 6:e1000657. doi: 10.1371/journal.pcbi.1000657.
73. Zorov, D. B., Filburn, C. R., Klotz, L. O., Zweier, J. L., and Sollott, S. J. (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. doi: 10.1084/jem.192.7.1001.