Red fluorescent genetically encoded indicator for intracellular hydrogen peroxide

Nature Communications

Volumn 5, Issue , 2014, Pages

  Ermakova, Yulia G ^a   Bilan, Dmitry S ^a,b   Matlashov, Mikhail E ^a,b   Mishina, Natalia M ^a   Markvicheva, Ksenia N ^a   Subach, Oksana M ^b   Subach, Fedor V ^b   Bogeski, Ivan ^c   Hoth, Markus ^c   Enikolopov, Grigori ^b,d   Belousov, Vsevolod V ^a,b  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^c SAARLAND UNIVERSITY   (Germany)

^d Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; GLUTATHIONE DISULFIDE; GROWTH FACTOR; HYDROGEN PEROXIDE; RED FLUORESCENT PROTEIN; SUPEROXIDE; CALCIUM; FLUORESCENT DYE; PHOTOPROTEIN; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN;

CONCENTRATION (COMPOSITION); CYTOPLASM; DETECTION METHOD; FLUORESCENCE; HYDROGEN PEROXIDE; OXYGEN; PROBE; RECOMBINATION; REDOX CONDITIONS; SENSOR;

ARTICLE; CALCIUM TRANSPORT; CELL CULTURE; CELL STIMULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; FEMALE; GENETIC CODE; HELA CELL LINE; HUMAN; HUMAN CELL; MITOCHONDRION; MOLECULAR SENSOR; SIGNAL TRANSDUCTION; CHEMISTRY; ELECTRON TRANSPORT; FLUORESCENCE MICROSCOPY; HEK293 CELL LINE; KINETICS; METABOLISM; OXIDATION REDUCTION REACTION; SPECTROPHOTOMETRY; TIME FACTOR;

CALCIUM; CYTOPLASM; ELECTRON TRANSPORT; FLUORESCENT DYES; HEK293 CELLS; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; KINETICS; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SPECTROPHOTOMETRY; TIME FACTORS;

EID: 84923381507     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6222     Document Type: Article

References (49)

1. Sies, H. & Cadenas, E. Oxidative stress: damage to intact cells and organs. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 311, 617-631 (1985).
2. Droge, W. Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95 (2002).
3. Winterbourn, C. C. Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4, 278-286 (2008).
4. D'Autreaux, B. & Toledano, M. B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell. Biol. 8, 813-824 (2007).
5. Belousov, V. V. et al. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3, 281-286 (2006).
6. Bilan, D. S. et al. HyPer-3: a genetically encoded H2O2 probe with improved performance for ratiometric and fluorescence lifetime imaging. ACS Chem. Biol. 8, 535-542 (2013).
7. Gutscher, M. et al. Proximity-based protein thiol oxidation by H2O2-scavenging peroxidases. J. Biol. Chem. 284, 31532-31540 (2009).
8. Markvicheva, K. N. et al. A genetically encoded sensor for H2O2 with expanded dynamic range. Bioorg. Med. Chem. 19, 1079-1084 (2011).
9. Lukyanov, K. A. & Belousov, V. V. Genetically encoded fluorescent redox sensors. Biochim. Biophys. Acta. 1840, 745-756 (2014).
10. Aslund, F., Zheng, M., Beckwith, J. & Storz, G. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl Acad. Sci. USA 96, 6161-6165 (1999).
11. Choi, H. et al. Structural basis of the redox switch in the OxyR transcription factor. Cell 105, 103-113 (2001).
12. Zheng, M., Aslund, F. & Storz, G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279, 1718-1721 (1998).
13. Zhao, Y. et al. An expanded palette of genetically encoded Ca(2)(+) indicators. Science 333, 1888-1891 (2011).
14. Shui, B. et al. Circular permutation of red fluorescent proteins. PLoS ONE 6, e20505 (2011).
15. Shemiakina, I. I. et al. A monomeric red fluorescent protein with low cytotoxicity. Nat. Commun. 3, 1204 (2012).
16. Markvicheva, K. N., Bogdanova, E. A., Staroverov, D. B., Lukyanov, S. & Belousov, V. V. Imaging of intracellular hydrogen peroxide production with HyPer upon stimulation of HeLa cells with epidermal growth factor. Methods Mol. Biol. 476, 76-83 (2009).
17. Mishina, N. M. et al. Visualization of intracellular hydrogen peroxide with HyPer, a genetically encoded fluorescent probe. Methods Enzymol. 526, 45-59 (2013).
18. Mishina, N. M. et al. Does cellular hydrogen peroxide diffuse or act locally? Antioxid. Redox. Signal. 14, 1-7 (2011).
19. Albrecht, S. C., Barata, A. G., Grosshans, J., Teleman, A. A. & Dick, T. P. In vivo mapping of hydrogen peroxide and oxidized glutathione reveals chemical and regional specificity of redox homeostasis. Cell. Metab. 14, 819-829 (2012).
20. West, A. P., Shadel, G. S. & Ghosh, S. Mitochondria in innate immune responses. Nat. Rev. Immunol. 11, 389-402 (2011).
21. Starkov, A. A. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann. N. Y. Acad. Sci. 1147, 37-52 (2008).
22. Gomes, A., Fernandes, E. & Lima, J.L.F.C. Fluorescence probes used for detection of reactive oxygen species. J. Biochem. Biophys. Methods 65, 45-80 (2005).
23. Kalyanaraman, B. et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic. Biol. Med. 52, 1-6 (2012).
24. Adam-Vizi, V. & Starkov, A. A. Calcium and mitochondrial reactive oxygen species generation: how to read the facts. J. Alzheimer's Dis. 20(Suppl 2): S413-S426.
25. Hansson, M. J. et al. Calcium-induced generation of reactive oxygen species in brain mitochondria is mediated by permeability transition. Free Radic. Biol. Med. 45, 284-294 (2008).
26. Kowaltowski, A. J., Castilho, R. F. & Vercesi, A. E. Ca(2+)-induced mitochondrial membrane permeabilization: role of coenzyme Q redox state. Am. J. Physiol. 269, C141-C147 (1995).
27. Dykens, J. A. Isolated cerebral and cerebellar mitochondria produce free radicals when exposed to elevated CA2+ and Na+: implications for neurodegeneration. J. Neurochem. 63, 584-591 (1994).
28. Starkov, A. A., Polster, B. M. & Fiskum, G. Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J. Neurochem. 83, 220-228 (2002).
29. Gyulkhandanyan, A. V. & Pennefather, P. S. Shift in the localization of sites of hydrogen peroxide production in brain mitochondria by mitochondrial stress. J. Neurochem. 90, 405-421 (2004).
30. Komary, Z., Tretter, L. & Adam-Vizi, V. H2O2 generation is decreased by calcium in isolated brain mitochondria. Biochim. Biophys. Acta. 1777, 800-807 (2008).
31. Ralevic, V. & Burnstock, G. Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413-492 (1998).
32. Treiman, M., Caspersen, C. & Christensen, S. B. A tool coming of age: thapsigargin as an inhibitor of sarco-endoplasmic reticulum Ca(2+)-ATPases. Trends. Pharmacol. Sci. 19, 131-135 (1998).
33. Poburko, D., Santo-Domingo, J. & Demaurex, N. Dynamic regulation of the mitochondrial proton gradient during cytosolic calcium elevations. J. Biol. Chem. 286, 11672-11684 (2011).
34. Gutscher, M. et al. Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 5, 553-559 (2008).
35. Jones, K. T. & Sharpe, G. R. Thapsigargin raises intracellular free calcium levels in human keratinocytes and inhibits the coordinated expression of differentiation markers. Exp. Cell Res. 210, 71-76 (1994).
36. Chen, Q., Vazquez, E. J., Moghaddas, S., Hoppel, C. L. & Lesnefsky, E. J. Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 278, 36027-36031 (2003).
37. Du, C., Fang, M., Li, Y., Li, L. & Wang, X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102, 33-42 (2000).
38. Nagai, T., Sawano, A., Park, E. S. & Miyawaki, A. Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc. Natl Acad. Sci. USA 98, 3197-3202 (2001).
39. Berg, J., Hung, Y. P. & Yellen, G. A genetically encoded fluorescent reporter of ATP:ADP ratio. Nat. Methods 6, 161-166 (2009).
40. Hung, Y. P., Albeck, J. G., Tantama, M. & Yellen, G. Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor. Cell Metab. 14, 545-554 (2011).
41. Marvin, J. S. et al. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat. Methods 10, 162-170 (2013).
42. Li, Y., Sierra, A. M., Ai, H. W. & Campbell, R. E. Identification of sites within a monomeric red fluorescent protein that tolerate peptide insertion and testing of corresponding circular permutations. Photochem. Photobiol. 84, 111-119 (2008).
43. Meyer, A. J. & Dick, T. P. Fluorescent protein-based redox probes. Antioxid. Redox. Signal. 13, 621-650 (2010).
44. Mekahli, D., Bultynck, G., Parys, J. B., De Smedt, H. & Missiaen, L. Endoplasmic-reticulum calcium depletion and disease. Cold Spring Harb. Perspect. Biol. 3, a004317 (2011).
45. Jobsis, F. F. Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science 198, 1264-1267 (1977).
46. Filonov, G. S. et al. Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat. Biotechnol. 29, 757-761 (2011).
47. Piatkevich, K. D., Subach, F. V. & Verkhusha, V. V. Engineering of bacterial phytochromes for near-infrared imaging, sensing, and light-control in mammals. Chem. Soc. Rev. 42, 3441-3452 (2013).
48. Shu, X. et al. Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 324, 804-807 (2009).
49. Bogeski, I. et al. Differential redox regulation of ORAI ion channels: a mechanism to tune cellular calcium signaling. Sci. Signal. 3, ra24 (2010).