Mitochondrial flashes: New insights into mitochondrial ROS signalling and beyond

Journal of Physiology

Volumn 592, Issue 17, 2014, Pages 3703-3713

  Hou, Tingting ^a   Wang, Xianhua ^a   Ma, Qi ^a   Cheng, Heping ^a  

^a Peking University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

AGING; ARTICLE; CELL PH; CELL PROLIFERATION; GENE MUTATION; HUMAN; HUNTINGTON CHOREA; HYPEROSMOTIC STRESS; LIFESPAN; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL FLASH; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION SWELLING; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; ACTION POTENTIAL; ANIMAL; METABOLISM; MITOCHONDRION;

ACTION POTENTIALS; ANIMALS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84906815063     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.275735     Document Type: Article

References (68)

1. Adler V, Yin Z, Tew KD & Ronai Z (1999). Role of redox potential and reactive oxygen species in stress signaling. Oncogene 18, 6104-6111.
2. 2+-induced permeabilization of rat liver mitochondria. Biochem J 239, 19-29.
3. Andreyev AY, Kushnareva YE & Starkov AA (2005). Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 70, 200-214.
4. Aon MA, Cortassa S & O'Rourke B (2004). Percolation and criticality in a mitochondrial network. Proc Natl Acad Sci U S A 101, 4447-4452.
5. Aon MA, Cortassa S & O'Rourke B (2008). Mitochondrial oscillations in physiology and pathophysiology. Adv Exp Med Biol 641, 98-117.
6. Azarias G & Chatton JY (2011). Selective ion changes during spontaneous mitochondrial transients in intact astrocytes. PLoS One 6, e28505.
7. Balaban RS, Nemoto S & Finkel T (2005). Mitochondria, oxidants, and aging. Cell 120, 483-495.
8. Basso E, Petronilli V, Forte MA & Bernardi P (2008). Phosphate is essential for inhibition of the mitochondrial permeability transition pore by cyclosporin A and by cyclophilin D ablation. J Biol Chem 283, 26307-26311.
9. Bernardi P (1992). Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J Biol Chem 267, 8834-8839.
10. 2+ of the hydrolysis and the synthesis of ATP in Ehrlich ascites tumour mitochondria: relation to the Crabtree effect. Biochim Biophys Acta 1228, 261-266.
11. Boveris A & Chance B (1973). The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134, 707-716.
12. Breckwoldt MO, Pfister FM, Bradley PM, Marinkovic P, Williams PR, Brill MS, Plomer B, Schmalz A, St Clair DK, Naumann R, Griesbeck O, Schwarzländer M, Godinho L, Bareyre FM, Dick TP, Kerschensteiner M & Misgeld T (2014). Multiparametric optical analysis of mitochondrial redox signals during neuronal physiology and pathology in vivo. Nat Med 20, 555-560.
13. Cao Y, Zhang X, Shang W, Xu J, Wang X, Hu X, Ao Y & Cheng H (2013). Proinflammatory cytokines stimulate mitochondrial superoxide flashes in articular chondrocytes in vitro and in situ. PLoS One 8, e66444.
14. Chance B, Sies H & Boveris A (1979). Hydroperoxide metabolism in mammalian organs. Physiol Rev 59, 527-605.
15. Cheng H & Lederer WJ (2008). Calcium sparks. Physiol Rev 88, 1491-1545.
16. 2+-dependent pore activated by oxidative stress in heart mitochondria. Biochem J 245, 915-918.
17. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 255, 357-360.
18. Di Lisa F & Bernardi P (2009). A CaPful of mechanisms regulating the mitochondrial permeability transition. J Mol Cell Cardiol 46, 775-780.
19. Droge W (2002). Free radicals in the physiological control of cell function. Physiol Rev 82, 47-95.
20. Duchen MR (2000). Mitochondria and calcium: from cell signalling to cell death. J Physiol 529, 57-68.
21. 2+-induced mitochondrial oscillations. A study on permeabilised Ehrlich ascites tumour cells. Cell Calcium 15, 143-152.
22. Fang H, Chen M, Ding Y, Shang W, Xu J, Zhang X, Zhang W, Li K, Xiao Y, Gao F, Shang S, Li JC, Tian XL, Wang SQ, Zhou J, Weisleder N, Ma J, Ouyang K, Chen J, Wang X, Zheng M, Wang W & Cheng H (2011). Imaging superoxide flash and metabolism-coupled mitochondrial permeability transition in living animals. Cell Res 21, 1295-1304.
23. Green DR (1998). Apoptotic pathways: the roads to ruin. Cell 94, 695-698.
24. Halliwell B (2001). Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18, 685-716.
25. 2+ trigger site. Arch Biochem Biophys 195, 460-467.
26. 2+ uniport and basal reactive oxygen species elevation. J Biol Chem 288, 4602-4612.
27. Hou Y, Ghosh P, Wan R, Ouyang X, Cheng H, Mattson MP & Cheng A (2014). Permeability transition pore-mediated mitochondrial superoxide flashes mediate an early inhibitory effect of amyloid beta1-42 on neural progenitor cell proliferation. Neurobiol Aging 35, 975-989.
28. Hou Y, Ouyang X, Wan R, Cheng H, Mattson MP & Cheng A (2012). Mitochondrial superoxide production negatively regulates neural progenitor proliferation and cerebral cortical development. Stem Cells 30, 2535-2547.
29. Huang Z, Zhang W, Fang H, Zheng M, Wang X, Xu J, Cheng H, Gong G, Wang W, Dirksen RT & Sheu SS (2011). Response to 'A critical evaluation of cpYFP as a probe for superoxide'. Free Radic Biol Med 51, 1937-1940.
30. 2+-induced membrane transition in mitochondria. I. The protective mechanisms. Arch Biochem Biophys 195, 453-459.
31. 2+ release. Arch Biochem Biophys 195, 468-477.
32. Ichas F, Jouaville LS & Mazat JP (1997). Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89, 1145-1153.
33. Ichas F & Mazat JP (1998). From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366, 33-50.
34. Jensen PK (1966). Antimycin-insensitive oxidation of succinate and reduced nicotinamide-adenine dinucleotide in electron-transport particles. I. pH dependency and hydrogen peroxide formation. Biochim Biophys Acta 122, 157-166.
35. Jian C, Hou T, Yin R, Cheng H & Wang X (2013). Regulation of superoxide flashes by steady-state and transient elevations of mitochondrial calcium. Scientia Sinica Vitae 43, 869-876.
36. Kinnally KW, Campo ML & Tedeschi H (1989). Mitochondrial channel activity studied by patch-clamping mitoplasts. J Bioenerg Biomembr 21, 497-506.
37. Li K, Zhang W, Fang H, Xie W, Liu J, Zheng M, Wang X, Wang W, Tan W & Cheng H (2012). Superoxide flashes reveal novel properties of mitochondrial reactive oxygen species excitability in cardiomyocytes. Biophys J 102, 1011-1021.
38. 2 production in pigeon heart mitochondria. FEBS Lett 18, 261-264.
39. Ma Q, Fang H, Shang W, Liu L, Xu Z, Ye T, Wang X, Zheng M, Chen Q & Cheng H (2011). Superoxide flashes: early mitochondrial signals for oxidative stress-induced apoptosis. J Biol Chem 286, 27573-27581.
40. Maryanovich M & Gross A (2013). A ROS rheostat for cell fate regulation. Trends Cell Biol 23, 129-134.
41. Murphy MP (2009). How mitochondria produce reactive oxygen species. Biochem J 417, 1-13.
42. 2+. Proc Natl Acad Sci U S A 98, 3197-3202.
43. Newsholme P, Haber EP, Hirabara SM, Rebelato EL, Procopio J, Morgan D, Oliveira-Emilio HC, Carpinelli AR & Curi R (2007). Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity. J Physiol 583, 9-24.
44. Nunnari J & Suomalainen A (2012). Mitochondria: in sickness and in health. Cell 148, 1145-1159.
45. Owusu-Ansah E & Banerjee U (2009). Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461, 537-541.
46. Petronilli V, Szabo I & Zoratti M (1989). The inner mitochondrial membrane contains ion-conducting channels similar to those found in bacteria. FEBS Lett 259, 137-143.
47. Poburko D, Santo-Domingo J & Demaurex N (2011). Dynamic regulation of the mitochondrial proton gradient during cytosolic calcium elevations. J Biol Chem 286, 11672-11684.
48. Pouvreau S (2010). Superoxide flashes in mouse skeletal muscle are produced by discrete arrays of active mitochondria operating coherently. PLoS One 5, e13035.
49. Quatresous E, Legrand C & Pouvreau S (2012). Mitochondria-targeted cpYFP: pH or superoxide sensor? J Gen Physiol 140, 567-570.
50. Santo-Domingo J, Giacomello M, Poburko D, Scorrano L & Demaurex N (2013). OPA1 promotes pH flashes that spread between contiguous mitochondria without matrix protein exchange. EMBO J 32, 1927-1940.
51. Schwarzländer M, Logan DC, Fricker MD & Sweetlove LJ (2011). The circularly permuted yellow fluorescent protein cpYFP that has been used as a superoxide probe is highly responsive to pH but not superoxide in mitochondria: implications for the existence of superoxide 'flashes'. Biochem J 437, 381-387.
52. Schwarzländer M, Logan DC, Johnston IG, Jones NS, Meyer AJ, Fricker MD & Sweetlove LJ (2012a). Pulsing of membrane potential in individual mitochondria: a stress-induced mechanism to regulate respiratory bioenergetics in Arabidopsis. Plant Cell 24, 1188-1201.
53. Schwarzländer M, Murphy MP, Duchen MR, Logan DC, Fricker MD, Halestrap AP, Müller FL, Rizzuto R, Dick TP, Meyer AJ & Sweetlove LJ (2012b). Mitochondrial 'flashes': a radical concept repHined. Trends Cell Biol 22, 503-508.
54. Shen EZ, Song CQ, Lin Y, Zhang WH, Su PF, Liu WY, Zhang P, Xu J, Lin N, Zhan C, Wang X, Shyr Y, Cheng H & Dong MQ (2014). Mitoflash frequency in early adulthood predicts lifespan in Caenorhabditis elegans. Nature 508, 128-132.
55. 2 generation: redox signaling and oxidative stress. J Biol Chem 289, 8735-8741.
56. Starkov AA (2008). The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci 1147, 37-52.
57. Szabo I, Bernardi P & Zoratti M (1992). Modulation of the mitochondrial megachannel by divalent cations and protons. J Biol Chem 267, 2940-2946.
58. Szabo I & Zoratti M (1991). The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A. J Biol Chem 266, 3376-3379.
59. Wallace DC (2012). Mitochondria and cancer. Nat Rev Cancer 12, 685-698.
60. Wang JQ, Chen Q, Wang X, Wang QC, Wang Y, Cheng HP, Guo C, Sun Q & Tang TS (2013). Dysregulation of mitochondrial calcium signaling and superoxide flashes cause mitochondrial genomic DNA damage in Huntington disease. J Biol Chem 288, 3070-3084.
61. Wang W, Fang H, Groom L, Cheng A, Zhang W, Liu J, Wang X, Li K, Han P, Zheng M, Yin J, Mattson MP, Kao JP, Lakatta EG, Sheu SS, Ouyang K, Chen J, Dirksen RT & Cheng H (2008). Superoxide flashes in single mitochondria. Cell 134, 279-290.
62. Wang X, Jian C, Zhang X, Huang Z, Xu J, Hou T, Shang W, Ding Y, Zhang W, Ouyang M, Wang Y, Yang Z, Zheng M & Cheng H (2012). Superoxide flashes: elemental events of mitochondrial ROS signaling in the heart. J Mol Cell Cardiol 52, 940-948.
63. Wang X, Ma Q, Wang W & Cheng H (2014). Mitochondrial superoxide flashes: From Signaling to disease. In Systems Biology of Free Radicals and Anti-Oxidants, 2014 edn, ed. Laher I. Springer-Verlag, Berlin Heidelberg.
64. Wei L & Dirksen RT (2012). Mitochondrial superoxide flashes: From discovery to new controversies. J Gen Physiol 139, 425-434.
65. Wei L, Salahura G, Boncompagni S, Kasischke KA, Protasi F, Sheu SS & Dirksen RT (2011). Mitochondrial superoxide flashes: metabolic biomarkers of skeletal muscle activity and disease. FASEB J 25, 3068-3078.
66. Wei-LaPierre L, Gong G, Gerstner BJ, Ducreux S, Yule DI, Pouvreau S, Wang X, Sheu SS, Cheng H, Dirksen RT & Wang W (2013). Respective contribution of mitochondrial superoxide and pH to mitochondria-targeted circularly permuted yellow fluorescent protein (mt-cpYFP) flash activity. J Biol Chem 288, 10567-10577.
67. Zhang X, Huang Z, Hou T, Xu J, Wang Y, Shang W, Ye T, Cheng H, Gao F & Wang X (2013). Superoxide constitutes a major signal of mitochondrial superoxide flash. Life Sci 93, 178-186.
68. 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.