Redox Imaging Using Cardiac Myocyte-Specific Transgenic Biosensor Mice

Circulation Research

Volumn 119, Issue 9, 2016, Pages 1004-1016

  Swain, Lija ^a   Kesemeyer, Andrea ^a   Meyer Roxlau, Stefanie ^b   Vettel, Christiane ^c   Zieseniss, Anke ^a   Güntsch, Annemarie ^a   Jatho, Aline ^a   Becker, Andreas ^a   Nanadikar, Maithily S ^a   Morgan, Bruce ^d   Dennerlein, Sven ^a   Shah, Ajay M ^e   El Armouche, Ali ^b   Nikolaev, Viacheslav O ^f,g   Katschinski, Dörthe M ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^g Heart Institute Lahr   (Germany)

Author keywords

angiotensin II; cytoplasm; diamide; ischemia; reactive oxygen species

Indexed keywords

ANGIOTENSIN II; DIAMIDE; DITHIOTHREITOL; GLUTAREDOXIN; GREEN FLUORESCENT PROTEIN; HYDROGEN PEROXIDE; ISOPRENALINE; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ARTICLE; BIOSENSOR; CARDIAC MUSCLE CELL; CYTOSOL; HYPOXIA; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REOXYGENATION; STIMULATION; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETIC PROCEDURES; GENETICS; HEART; METABOLISM; ORGAN CULTURE TECHNIQUE; OXYGEN CONSUMPTION; PHYSIOLOGY; PROCEDURES;

ANIMALS; BIOSENSING TECHNIQUES; CELLS, CULTURED; GREEN FLUORESCENT PROTEINS; HEART; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCYTES, CARDIAC; ORGAN CULTURE TECHNIQUES; OXIDATION-REDUCTION; OXYGEN CONSUMPTION;

EID: 84984704751     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.309551     Document Type: Article

References (41)

1. Kemp M, Go YM, Jones DP. Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology. Free Radic Biol Med. 2008;44:921-937. doi: 10.1016/j.freeradbiomed.2007.11.008
2. Jones DP, Sies H. The Redox Code. Antioxid Redox Signal. 2015;23:734-746. doi: 10.1089/ars.2015.6247
3. Sag CM, Santos CX, Shah AM. Redox regulation of cardiac hypertrophy. J Mol Cell Cardiol. 2014;73:103-111. doi: 10.1016/j.yjmcc.2014.02.002
4. Kaludercic N, Deshwal S, Di Lisa F. Reactive oxygen species and redox compartmentalization. Front Physiol. 2014;5:285. doi: 10.3389/ fphys.2014.00285
5. Christians ES, Benjamin IJ. Proteostasis and REDOX state in the heart. Am J Physiol Heart Circ Physiol. 2012;302:H24-H37. doi: 10.1152/ ajpheart.00903.2011
6. Gutscher M, Pauleau AL, Marty L, Brach T, Wabnitz GH, Samstag Y, Meyer AJ, Dick TP. Real-time imaging of the intracellular glutathione redox potential. Nat Methods. 2008;5:553-559. doi: 10.1038/nmeth.1212
7. Schwarzländer M, Dick TP, Meyer AJ, Morgan B. Dissecting Redox Biology Using fluorescent protein sensors. Antioxid Redox Signal. 2016;24:680-712. doi: 10.1089/ars.2015.6266
8. Morgan B, Sobotta MC, Dick TP. Measuring E(GSH) and H2O2 with roGFP2-based redox probes. Free Radic Biol Med. 2011;51:1943-1951. doi: 10.1016/j.freeradbiomed.2011.08.035
9. 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. doi: 10.1038/nature09536
10. Breckwoldt MO, Pfister FM, Bradley PM, et al. Multiparametric optical analysis of mitochondrial redox signals during neuronal physiology and pathology in vivo. Nat Med. 2014;20:555-560. doi: 10.1038/nm.3520
11. Xu X, Löhneysen K, Soldau K, Noack D, Vu A, Friedman JS. A novel approach for in vivo measurement of mouse red cell redox status. Blood. 2011;118:3694-3697. doi: 10.1182/blood-2011-03-342113
12. Wolf AM, Nishimaki K, Kamimura N, Ohta S. Real-time monitoring of oxidative stress in live mouse skin. J Invest Dermatol. 2014;134:1701-1709. doi: 10.1038/jid.2013.428
13. Fujikawa Y, Roma LP, Sobotta MC, Rose AJ, Diaz MB, Locatelli G, Breckwoldt MO, Misgeld T, Kerschensteiner M, Herzig S, Müller-Decker K, Dick TP. Mouse redox histology using genetically encoded probes. Sci Signal. 2016;9:rs1. doi: 10.1126/scisignal.aad3895
14. Vogler M, Zieseniss A, Hesse AR, Levent E, Tiburcy M, Heinze E, Burzlaff N, Schley G, Eckardt KU, Willam C, Katschinski DM. Pre-and post-conditional inhibition of prolyl-4-hydroxylase domain enzymes protects the heart from an ischemic insult. Pflugers Arch. 2015;467:2141-2149. doi: 10.1007/s00424-014-1667-z
15. Silter M, Kögler H, Zieseniss A, Wilting J, Schäfer K, Toischer K, Rokita AG, Breves G, Maier LS, Katschinski DM. Impaired Ca(2+)-handling in HIF-1alpha(+/-) mice as a consequence of pressure overload. Pflugers Arch. 2010;459:569-577. doi: 10.1007/ s00424-009-0748-x
16. Meyer AJ, Dick TP. Fluorescent protein-based redox probes. Antioxid Redox Signal. 2010;13:621-650. doi: 10.1089/ars.2009.2948
17. 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. doi: 10.1074/jbc.M312846200
18. Wittig I, Braun HP, Schägger H. Blue native PAGE. Nat Protoc. 2006;1:418-428. doi: 10.1038/nprot.2006.62
19. Schwarzländer M, Fricker MD, Müller C, Marty L, Brach T, Novak J, Sweetlove LJ, Hell R, Meyer AJ. Confocal imaging of glutathione redox potential in living plant cells. J Microsc. 2008;231:299-316. doi: 10.1111/j.1365-2818.2008.02030.x
20. Schwarzländer 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. doi: 10.1042/BJ20110883
21. Llopis J, McCaffery JM, Miyawaki A, Farquhar MG, Tsien RY. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc Natl Acad Sci U S A. 1998;95:6803-6808
22. Wagner S, Dantz C, Flebbe H, Azizian A, Sag CM, Engels S, Möllencamp J, Dybkova N, Islam T, Shah AM, Maier LS. NADPH oxidase 2 mediates angiotensin II-dependent cellular arrhythmias via PKA and CaMKII. J Mol Cell Cardiol. 2014;75:206-215. doi: 10.1016/j. yjmcc.2014.07.011
23. Bendall JK, Cave AC, Heymes C, Gall N, Shah AM. Pivotal role of a gp91(phox)-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation. 2002;105:293-296
24. Forkink M, Smeitink JA, Brock R, Willems PH, Koopman WJ. Detection and manipulation of mitochondrial reactive oxygen species in mammalian cells. Biochim Biophys Acta. 2010;1797:1034-1044. doi: 10.1016/j. bbabio.2010.01.022
25. Boulton S, Anderson A, Swalwell H, Henderson JR, Manning P, Birch-Machin MA. Implications of using the fluorescent probes, dihydrorhodamine 123 and 2',7'-dichlorodihydrofluorescein diacetate, for the detection of UVA-induced reactive oxygen species. Free Radic Res. 2011;45:139-146. doi: 10.3109/10715762.2010.517751
26. Tetz LM, Kamau PW, Cheng AA, Meeker JD, Loch-Caruso R. Troubleshooting the dichlorofluorescein assay to avoid artifacts in measurement of toxicant-stimulated cellular production of reactive oxidant species. J Pharmacol Toxicol Methods. 2013;67:56-60. doi: 10.1016/j. vascn.2013.01.195
27. Lukyanov KA, Belousov VV. Genetically encoded fluorescent redox sensors. Biochim Biophys Acta. 2014;1840:745-756. doi: 10.1016/j. bbagen.2013.05.030
28. Morgan B, Van Laer K, Owusu TN, Ezerina D, Pastor-Flores D, Amponsah PS, Tursch A, Dick TP. Real-time monitoring of basal ho levels with peroxiredoxin-based probes. Nat Chem Biol. 2016 doi: 10:1038/ nchembio.2067
29. Shen D, Dalton TP, Nebert DW, Shertzer HG. Glutathione redox state regulates mitochondrial reactive oxygen production. J Biol Chem. 2005;280:25305-25312. doi: 10.1074/jbc.M500095200
30. Rebrin I, Zicker S, Wedekind KJ, Paetau-Robinson I, Packer L, Sohal RS. Effect of antioxidant-enriched diets on glutathione redox status in tissue homogenates and mitochondria of the senescence-accelerated mouse. Free Radic Biol Med. 2005;39:549-557. doi: 10.1016/j. freeradbiomed.2005.04.008
31. 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. doi: 10.1074/jbc.M312847200
32. Giustarini D, Dalle-Donne I, Milzani A, Fanti P, Rossi R. Analysis of GSH and GSSG after derivatization with N-ethylmaleimide. Nat Protoc. 2013;8:1660-1669. doi: 10.1038/nprot.2013.095
33. Go YM, Jones DP. Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta. 2008;1780:1273-1290. doi: 10.1016/j.bbagen.2008.01.011
34. Ribas V, García-Ruiz C, Fernández-Checa JC. Glutathione and mitochondria. Front Pharmacol. 2014;5:151. doi: 10.3389/fphar.2014.00151
35. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552:335-344. doi: 10.1113/jphysiol.2003.049478
36. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120:483-495. doi: 10.1016/j.cell.2005.02.001
37. Chen Z, Lash LH. Evidence for mitochondrial uptake of glutathione by dicarboxylate and 2-oxoglutarate carriers. J Pharmacol Exp Ther. 1998;285:608-618
38. Garcia J, Han D, Sancheti H, Yap LP, Kaplowitz N, Cadenas E. Regulation of mitochondrial glutathione redox status and protein glutathionylation by respiratory substrates. J Biol Chem. 2010;285:39646-39654. doi: 10.1074/jbc.M110.164160
39. Cortassa S, O'Rourke B, Aon MA. Redox-optimized ROS balance and the relationship between mitochondrial respiration and ROS. Biochim Biophys Acta. 2014;1837:287-295. doi: 10.1016/j.bbabio.2013. 11.007
40. Aon MA, Cortassa S, O'Rourke B. Redox-optimized ROS balance: a unifying hypothesis. Biochim Biophys Acta. 2010;1797:865-877. doi: 10.1016/j.bbabio.2010.02.016
41. Nickel AG, von Hardenberg A, Hohl M, et al. Reversal of Mitochondrial Transhydrogenase Causes Oxidative Stress in Heart Failure. Cell Metab. 2015;22:472-484. doi: 10.1016/j.cmet.2015.07.008