Imaging mitochondrial reactive oxygen species with fluorescent probes: Current applications and challenges

References

• Bashan N, Kovsan J, Kachko I, Ovadia H, Rudich A. Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol Rev 2009;89:27–71.
   PubMed Web of Science ®Google Scholar
• Grisham MB. Reactive oxygen species in immune responses. Free Radic Biol Med 2004;36:1479–1480.
   PubMed Web of Science ®Google Scholar
• Gutterman DD, Miura H, Liu Y. Redox modulation of vascular tone: focus of potassium channel mechanisms of dilation. Arterioscler Thromb Vasc Biol 2005;25:671–678.
   PubMed Web of Science ®Google Scholar
• Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87:245–313.
   PubMed Web of Science ®Google Scholar
• Feng Y, Liu Y, Wang D, Zhang X, Liu W, Fu F, et al. Insulin alleviates posttrauma cardiac dysfunction by inhibiting tumor necrosis factor-alpha-mediated reactive oxygen species production. Crit Care Med 2013;41:e74–84.
   Web of Science ®Google Scholar
• Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science 2006;312:1882–1883.
   PubMed Web of Science ®Google Scholar
• Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003;552:335–344.
   PubMed Web of Science ®Google Scholar
• Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 2014;94:909–950.
   PubMed Web of Science ®Google Scholar
• Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010;45:466–472.
   PubMed Web of Science ®Google Scholar
• Figueira TR, Barros MH, Camargo AA, Castilho RF, Ferreira JC, Kowaltowski AJ, et al. Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antioxid Redox Signal 2013; 18:2029–2074
   PubMed Web of Science ®Google Scholar
• Venditti P, Di Stefano L, Di Meo S. Mitochondrial metabolism of reactive oxygen species. Mitochondrion 2013;13: 71–82.
   PubMed Web of Science ®Google Scholar
• Fisher-Wellman KH, Gilliam LA, Lin CT, Cathey BL, Lark DS, Neufer PD. Mitochondrial glutathione depletion reveals a novel role for the pyruvate dehydrogenase complex as a key H2O2-emitting source under conditions of nutrient overload. Free Radic Biol Med 2013;65:1201–1208.
   PubMed Web of Science ®Google Scholar
• Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS, Beal MF. Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J Neurosci 2004;24:7779–7788.
   PubMed Web of Science ®Google Scholar
• Kaludercic N, Carpi A, Menabo R, Di Lisa F, Paolocci N. Monoamine oxidases (MAO) in the pathogenesis of heart failure and ischemia/reperfusion injury. Biochim Biophys Acta 2011;1813:1323–1332
   PubMed Web of Science ®Google Scholar
• Quinlan CL, Goncalves RL, Hey-Mogensen M, Yadava N, Bunik VI, Brand MD. The 2-oxoacid dehydrogenase complexes in mitochondria can produce superoxide/hydrogen peroxide at much higher rates than complex I. J Biol Chem 2014;289:8312–8325.
   PubMed Web of Science ®Google Scholar
• Hamanaka RB, Chandel NS. Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 2010;35:505–513.
   PubMed Web of Science ®Google Scholar
• Page MM, Robb EL, Salway KD, Stuart JA. Mitochondrial redox metabolism: aging, longevity and dietary effects. Mech Ageing Dev 2010;131:242–252.
   Google Scholar
• Cardoso AR, Chausse B, da Cunha FM, Luevano-Martinez LA, Marazzi TB, Pessoa PS, Queliconi BB, Kowaltowski AJ. Mitochondrial compartmentalization of redox processes. Free Radic Biol Med 2012;52:2201–2208.
   PubMed Web of Science ®Google Scholar
• Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 2008;4:278–286.
   PubMed Web of Science ®Google Scholar
• Gutowski M, Kowalczyk S. A study of free radical chemistry: their role and pathophysiological significance. Acta Biochim Pol 2013;60:1–16.
   PubMed Web of Science ®Google Scholar
• Yousif LF, Stewart KM, Kelley SO. Targeting mitochondria with organelle-specific compounds: strategies and applications. Chembiochem 2009;10:1939–1950.
   PubMed Web of Science ®Google Scholar
• Juhaszova M, Zorov DB, Kim SH, Pepe S, Fu Q, Fishbein KW, et al. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest 2004;113:1535–1549.
   PubMed Web of Science ®Google Scholar
• Zhang X, Huang Z, Hou T, Xu J, Wang Y, Shang W, et al. Superoxide constitutes a major signal of mitochondrial superoxide flash. Life Sci 2013;93:178–186.
   PubMed Web of Science ®Google Scholar
• Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 2012;52:1–6.
   PubMed Web of Science ®Google Scholar
• Wang X, Fang H, Huang Z, Shang W, Hou T, Cheng A, Cheng H. Imaging ROS signaling in cells and animals. J Mol Med (Berl) 2013;91:917–927.
   PubMed Web of Science ®Google Scholar
• Qian SY, Buettner GR. Iron and dioxygen chemistry is an important route to initiation of biological free radical oxidations: an electron paramagnetic resonance spin trapping study. Free Radic Biol Med 1999;26:1447–1456.
   PubMed Web of Science ®Google Scholar
• Folkes LK, Patel KB, Wardman P, Wrona M. Kinetics of reaction of nitrogen dioxide with dihydrorhodamine and the reaction of the dihydrorhodamine radical with oxygen: implications for quantifying peroxynitrite formation in cells. Arch Biochem Biophys 2009;484:122–126.
   PubMed Web of Science ®Google Scholar
• Curtin JF, Donovan M, Cotter TG. Regulation and measurement of oxidative stress in apoptosis. J Immunol Methods 2002;265:49–72.
   PubMed Web of Science ®Google Scholar
• Zmijewski JW, Moellering DR, Le Goffe C, Landar A, Ramachandran A, Darley-Usmar VM. Oxidized LDL induces mitochondrially associated reactive oxygen/nitrogen species formation in endothelial cells. Am J Physiol Heart Circ Physiol 2005;289:H852–861.
   PubMed Web of Science ®Google Scholar
• Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 2000; 192:1001–1014.
   PubMed Web of Science ®Google Scholar
• Zhao H, Joseph J, Fales HM, Sokoloski EA, Levine RL, Vasquez-Vivar J, Kalyanaraman B. Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proc Natl Acad Sci U S A 2005;102:5727–5732.
   PubMed Web of Science ®Google Scholar
• Zielonka J, Kalyanaraman B. Hydroethidine- and MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation: another inconvenient truth. Free Radic Biol Med 2010;48:983–1001.
   PubMed Web of Science ®Google Scholar
• Zielonka J, Srinivasan S, Hardy M, Ouari O, Lopez M, Vasquez-Vivar J, Avadhani NG, Kalyanaraman B. Cytochrome c-mediated oxidation of hydroethidine and mito-hydroethidine in mitochondria: identification of homo- and heterodimers. Free Radic Biol Med 2008;44:835–846.
   PubMed Web of Science ®Google Scholar
• Fernandes DC, Wosniak J Jr, Pescatore LA, Bertoline MA, Liberman M, Laurindo FR, Santos CX. Analysis of DHE-derived oxidation products by HPLC in the assessment of superoxide production and NADPH oxidase activity in vascular systems. Am J Physiol Cell Physiol 2007;292:C413–422.
   PubMed Web of Science ®Google Scholar
• Meany DL, Thompson L, Arriaga EA. Simultaneously monitoring the superoxide in the mitochondrial matrix and extramitochondrial space by micellar electrokinetic chromatography with laser-induced fluorescence. Anal Chem 2007; 79:4588–4594.
   PubMed Web of Science ®Google Scholar
• Zielonka J, Sarna T, Roberts JE, Wishart JF, Kalyanaraman B. Pulse radiolysis and steady-state analyses of the reaction between hydroethidine and superoxide and other oxidants. Arch Biochem Biophys 2006;456:39–47.
   PubMed Web of Science ®Google Scholar
• Robinson KM, Janes MS, Pehar M, Monette JS, Ross MF, Hagen TM, Murphy MP, Beckman JS. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci U S A 2006;103:15038–15043.
   PubMed Web of Science ®Google Scholar
• Zielonka J, Vasquez-Vivar J, Kalyanaraman B. Detection of 2-hydroxyethidium in cellular systems: a unique marker product of superoxide and hydroethidine. Nat Protoc 2008;3:8–21.
   PubMed Web of Science ®Google Scholar
• Galougahi KK, Liu CC, Gentile C, Kok C, Nunez A, Garcia A, et al. Glutathionylation mediates angiotensin II-induced eNOS uncoupling, amplifying NADPH oxidase- dependent endothelial dysfunction. J Am Heart Assoc 2014;3: e000731.
   Web of Science ®Google Scholar
• Kaludercic N, Deshwal S, Di Lisa F. Reactive oxygen species and redox compartmentalization. Front Physiol 2014; 5:285.
   PubMed Web of Science ®Google Scholar
• Gomes A, Fernandes E, Lima JL. Fluorescence probes used for detection of reactive oxygen species. J Biochem Biophys Methods 2005;65:45–80.
   PubMedGoogle Scholar
• Dikalov SI, Harrison DG. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid Redox Signal 2014;20:372–382.
   PubMed Web of Science ®Google Scholar
• Wardman P. Methods to measure the reactivity of peroxynitrite-derived oxidants toward reduced fluoresceins and rhodamines. Methods Enzymol 2008;441:261–282.
   PubMed Web of Science ®Google Scholar
• Koide Y, Urano Y, Kenmoku S, Kojima H, Nagano T. Design and synthesis of fluorescent probes for selective detection of highly reactive oxygen species in mitochondria of living cells. J Am Chem Soc 2007;129:10324–10325.
   PubMed Web of Science ®Google Scholar
• Sikora A, Zielonka J, Lopez M, Joseph J, Kalyanaraman B. Direct oxidation of boronates by peroxynitrite: mechanism and implications in fluorescence imaging of peroxynitrite. Free Radic Biol Med 2009;47:1401–1407.
   PubMed Web of Science ®Google Scholar
• Zielonka J, Sikora A, Joseph J, Kalyanaraman B. Peroxynitrite is the major species formed from different flux ratios of co-generated nitric oxide and superoxide: direct reaction with boronate-based fluorescent probe. J Biol Chem 2010;285: 14210–14216.
   PubMed Web of Science ®Google Scholar
• Winterbourn CC. The challenges of using fluorescent probes to detect and quantify specific reactive oxygen species in living cells. Biochim Biophys Acta 2014;1840:730–738.
   PubMed Web of Science ®Google Scholar
• Dickinson BC, Huynh C, Chang CJ. A palette of fluorescent probes with varying emission colors for imaging hydrogen peroxide signaling in living cells. J Am Chem Soc 2010;132: 5906–5915.
   PubMed Web of Science ®Google Scholar
• Dickinson BC, Chang CJ. A targetable fluorescent probe for imaging hydrogen peroxide in the mitochondria of living cells. J Am Chem Soc 2008;130:9638–9639.
   PubMed Web of Science ®Google Scholar
• Fang H, Chen M, Ding Y, Shang W, Xu J, Zhang X, et al. Imaging superoxide flash and metabolism-coupled mitochondrial permeability transition in living animals. Cell Res 2011; 21:1295–1304.
   PubMed Web of Science ®Google Scholar
• Guzman JN, Sanchez-Padilla J, Wokosin D, Kondapalli J, Ilijic E, Schumacker PT, Surmeier DJ. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 2010;468:696–700.
   PubMed Web of Science ®Google Scholar
• Liu Z, Celotto AM, Romero G, Wipf P, Palladino MJ. Genetically encoded redox sensor identifies the role of ROS in degenerative and mitochondrial disease pathogenesis. Neurobiol Dis 2012;45:362–368
   PubMed Web of Science ®Google Scholar
• Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV, Lukyanov S. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 2006;3:281–286.
   PubMed Web of Science ®Google Scholar
• Espinosa A, Garcia A, Hartel S, Hidalgo C, Jaimovich E. NADPH oxidase and hydrogen peroxide mediate insulin- induced calcium increase in skeletal muscle cells. J Biol Chem 2009;284:2568–2575.
   PubMed Web of Science ®Google Scholar
• Poburko D, Santo-Domingo J, Demaurex N. Dynamic regulation of the mitochondrial proton gradient during cytosolic calcium elevations. J Biol Chem 2011;286:11672–11684.
   PubMed Web of Science ®Google Scholar
• Lukyanov KA, Belousov VV. Genetically encoded fluorescent redox sensors. Biochim Biophys Acta 2014;1840: 745–756
   PubMed Web of Science ®Google Scholar
• Stone JR, Yang S. Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal 2006;8:243–270.
   PubMed Web of Science ®Google Scholar
• Ezerina D, Morgan B, Dick TP. Imaging dynamic redox processes with genetically encoded probes. J Mol Cell Cardiol 2014;73:43–49.
   PubMed Web of Science ®Google Scholar
• Bilan DS, Pase L, Joosen L, Gorokhovatsky AY, Ermakova YG, Gadella TW, et al. HyPer-3: a genetically encoded H(2)O(2) probe with improved performance for ratiometric and fluorescence lifetime imaging. ACS Chem Biol 2013;8: 535–542
   PubMed Web of Science ®Google Scholar
• Markvicheva KN, Bilan DS, Mishina NM, Gorokhovatsky AY, Vinokurov LM, Lukyanov S, Belousov VV. A genetically encoded sensor for H2O2 with expanded dynamic range. Bioorg Med Chem 2010;19:1079–1084.
   PubMed Web of Science ®Google Scholar
• Ermakova YG, Bilan DS, Matlashov ME, Mishina NM, Markvicheva KN, Subach OM, et al. Red fluorescent genetically encoded indicator for intracellular hydrogen peroxide. Nat Commun 2014;5. Doi:10.1038/ncomms6222
   PubMed Web of Science ®Google Scholar
• Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 2004;279:22284–22293.
   PubMed Web of Science ®Google Scholar
• Hanson GT, Aggeler R, Oglesbee D, Cannon M, Capaldi RA, Tsien RY, Remington SJ. Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 2004;279:13044–13053.
   PubMed Web of Science ®Google Scholar
• Meyer AJ, Dick TP. Fluorescent protein-based redox probes. Antioxid Redox Signal 2010;13:621–650.
   PubMed Web of Science ®Google Scholar
• Gutscher M, Sobotta MC, Wabnitz GH, Ballikaya S, Meyer AJ, Samstag Y, Dick TP. Proximity-based protein thiol oxidation by H2O2-scavenging peroxidases. J Biol Chem 2009;284: 31532–31540.
   PubMed Web of Science ®Google Scholar
• Wang W, Fang H, Groom L, Cheng A, Zhang W, Liu J. Superoxide flashes in single mitochondria. Cell 2008;134:279–290.
   PubMed Web of Science ®Google Scholar
• Li K, Zhang W, Fang H, Xie W, Liu J, Zheng M, et al. Superoxide flashes reveal novel properties of mitochondrial reactive oxygen species excitability in cardiomyocytes. Biophys J 2012;102:1011–1021.
   PubMed Web of Science ®Google Scholar
• Pouvreau S. Superoxide flashes in mouse skeletal muscle are produced by discrete arrays of active mitochondria operating coherently. PLoS One 2010;5:e13035.
   Web of Science ®Google Scholar
• Shen EZ, Song CQ, Lin Y, Zhang WH, Su PF, Liu WY, et al. Mitoflash frequency in early adulthood predicts lifespan in Caenorhabditis elegans. Nature 2014;508:128–132.
   PubMed Web of Science ®Google Scholar
• Wang JQ Chen Q, Wang X, Wang QC, Wang Y, Cheng HP, et al. Dysregulation of Mitochondrial Calcium Signaling and Superoxide Flashes Cause Mitochondrial Genomic DNA Damage in Huntington's Disease. J Biol Chem. 2012. Doi:10.1074/jbc.M112.407726
   Web of Science ®Google Scholar
• Hou T, Zhang X, Xu J, Jian C, Huang Z, Ye T, et al. Synergistic triggering of superoxide flashes by mitochondrial Ca2 + uniport and Basal reactive oxygen species elevation. J Biol Chem 2013;288:4602–4612.
   PubMed Web of Science ®Google Scholar
• Sheu SS, Wang W, Cheng H, Dirksen RT. Superoxide flashes: illuminating new insights into cardiac ischemia/reperfusion injury. Future Cardiol 2008;4:551–554.
   PubMedGoogle Scholar
• Wang X, Jian C, Zhang X, Huang Z, Xu J, Hou T, et al. Superoxide flashes: elemental events of mitochondrial ROS signaling in the heart. J Mol Cell Cardiol 2012;52:940–948.
   PubMed Web of Science ®Google Scholar
• Hou T, Wang X, Ma Q, Cheng H. Mitochondrial flashes: new insights into mitochondrial ROS signaling and beyond. J Physiol 2014;592:3703–3713.
   PubMed Web of Science ®Google Scholar
• Wei L, Salahura G, Boncompagni S, Kasischke KA, Protasi F, Sheu SS, Dirksen RT. Mitochondrial superoxide flashes: metabolic biomarkers of skeletal muscle activity and disease. FASEB J 2011;25:3068–3078.
   PubMed Web of Science ®Google Scholar
• Santo-Domingo J, Giacomello M, Poburko D, Scorrano L, Demaurex N. OPA1 promotes pH flashes that spread between contiguous mitochondria without matrix protein exchange. EMBO J 2013;32:1927–1940.
   PubMed Web of Science ®Google Scholar
• Schwarzlander M, Logan DC, Fricker MD, Sweetlove LJ. 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 2011;437:381–387.
   PubMed Web of Science ®Google Scholar
• Muller FL. A critical evaluation of cpYFP as a probe for superoxide. Free Radic Biol Med 2009;47:1779–1780.
   PubMed Web of Science ®Google Scholar
• Schwarzlander M, Murphy MP, Duchen MR, Logan DC, Fricker MD, Halestrap AP, et al. Mitochondrial ‘flashes’: a radical concept repHined. Trends Cell Biol 2012;22:503–508.
   Google Scholar
• Wei-LaPierre L, Gong G, Gerstner BJ, Ducreux S, Yule DI, Pouvreau S, et al. Respective contribution of mitochondrial superoxide and pH to mitochondria-targeted circularly permuted yellow fluorescent protein (mt-cpYFP) flash activity. J Biol Chem 2013;288:10567–10577.
   PubMed Web of Science ®Google Scholar
• Breckwoldt MO, Pfister FM, Bradley PM, Marinkovic P, Williams PR, Brill MS, et al. Multiparametric optical analysis of mitochondrial redox signals during neuronal physiology and pathology in vivo. Nat Med 2014;20:555–560.
   PubMed Web of Science ®Google Scholar
• Cheng H, Wang W, Wang X, Sheu SS, Dirksen RT, Dong MQ. Cheng et al. reply. Nature 2014;514:E14–15.
   PubMedGoogle Scholar
• Ma Q, Fang H, Shang W, Liu L, Xu Z, Ye T, et al. Superoxide flashes: early mitochondrial signals for oxidative stress-induced apoptosis. J Biol Chem 2011;286:27573–27581.
   PubMed Web of Science ®Google Scholar
• Kolossov VL, Spring BQ, Sokolowski A, Conour JE, Clegg RM, Kenis PJ, Gaskins HR. Engineering redox-sensitive linkers for genetically encoded FRET-based biosensors. Exp Biol Med (Maywood) 2008;233:238–248.
   PubMed Web of Science ®Google Scholar
• Yano T, Oku M, Akeyama N, Itoyama A, Yurimoto H, Kuge S, Fujiki Y, Sakai Y. A novel fluorescent sensor protein for visualization of redox states in the cytoplasm and in peroxisomes. Mol Cell Biol 2010;30:3758–3766.
   PubMed Web of Science ®Google Scholar
• Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, et al. Mitochondrial complex III is required for hypoxia- induced ROS production and cellular oxygen sensing. Cell Metab 2005;1:401–408.
   PubMed Web of Science ®Google Scholar
• Enyedi B, Zana M, Donko A, Geiszt M. Spatial and temporal analysis of NADPH oxidase-generated hydrogen peroxide signals by novel fluorescent reporter proteins. Antioxid Redox Signal 2013;19:523–534
   PubMed Web of Science ®Google Scholar