Bright and fast multicoloured voltage reporters via electrochromic FRET

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zou, Peng ^a   Zhao, Yongxin ^b   Douglass, Adam D ^c   Hochbaum, Daniel R ^a   Brinks, Daan ^a   Werley, Christopher A ^a   Harrison, D Jed ^b   Campbell, Robert E ^b   Cohen, Adam E ^a,d  

^a HARVARD STEM CELL INSTITUTE   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RHODOPSIN; PHOTOPROTEIN;

ARRAY; FLUORESCENCE; NEUROLOGY; PROTEIN; SENSITIVITY ANALYSIS;

ABSORPTION SPECTROSCOPY; ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BRIGHTNESS; COLOR; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; ENERGY TRANSFER; FEMALE; FLUORESCENCE; HIPPOCAMPUS; HUMAN; HUMAN CELL; ILLUMINATION; MEMBRANE POTENTIAL; NERVE CELL; NERVE CELL CULTURE; NERVE POTENTIAL; NONHUMAN; RAT; RESPONSE TIME; SIGNAL NOISE RATIO; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELL LINE; KIDNEY; MOLECULAR GENETICS; PHYSIOLOGY; PROCEDURES;

ACTION POTENTIALS; AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; COLOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HIPPOCAMPUS; HUMANS; KIDNEY; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; NEURONS; RATS; RHODOPSIN;

EID: 84907059872     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5625     Document Type: Article

References (43)

1. Cohen, A. E. & Venkatachalam, V. Bringing bioelectricity to light. Annu. Rev. Biophys. 43, 11.1-11.22 (2014).
2. Bezanilla, F. How membrane proteins sense voltage. Nat. Rev. Mol. Cell Biol. 9, 323-332 (2008). (Pubitemid 351430853)
3. Kralj, J. M., Hochbaum, D. R., Douglass, A. D. & Cohen, A. E. Electrical spiking in Escherichia coli probed with a fluorescent voltage indicating protein. Science 333, 345-348 (2011).
4. Slayman, C. L. & Slayman, C. W. Depolarization of the plasma membrane of Neurospora during active transport of glucose: evidence for a protondependent cotransport system. Proc. Natl Acad. Sci. USA 71, 1935-1939 (1974).
5. Mousavi, S. A., Chauvin, A., Pascaud, F., Kellenberger, S. & Farmer, E. E. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500, 422-426 (2013).
6. Siegel, M. S. & Isacoff, E. Y. A genetically encoded optical probe of membrane voltage. Neuron 19, 735-741 (1997). (Pubitemid 27471378)
7. Jin, L. et al. Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 75, 779-785 (2012).
8. Cao, G. et al. Genetically targeted optical electrophysiology in intact neural circuits. Cell 154, 904-913 (2013).
9. St-Pierre, F. et al. High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat. Neurosci. 17, 884-889 (2014).
10. Baker, B. J. et al. Genetically encoded fluorescent voltage sensors using the voltage-sensing domain of Nematostella and Danio phosphatases exhibit fast kinetics. J. Neurosci. Methods 208, 190-196 (2012).
11. Mutoh, H., Akemann, W. & Knöpfel, T. Genetically engineered fluorescent voltage reporters.. ACS Chem. Neuro. 3, 585-592 (2012).
12. Lam, A. J. et al. Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005-1012 (2012).
13. Hochbaum, D. R. et al. All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat. Methods 11, 825-833 (2014).
14. Kralj, J. M., Douglass, A. D., Hochbaum, D. R., Maclaurin, D. & Cohen, A. E. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 9, 90-95 (2012).
15. Chen, T. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
16. Marvin, J. S. et al. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat. Methods 10, 162-170 (2013).
17. Tantama, M., Martínez-François, J. R., Mongeon, R. & Yellen, G. Imaging energy status in live cells with a fluorescent biosensor of the intracellular ATPto-ADP ratio. Nat. Commun. 4, 2550 (2013).
18. Kuner, T. & Augustine, G. J. A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons. Neuron 27, 447-459 (2000).
19. San Martín, A. et al. Imaging mitochondrial flux in single cells with a FRET sensor for pyruvate. PLoS ONE 9, e85780 (2014).
20. Bayraktar, H. et al. Ultrasensitive measurements of microbial rhodopsin photocycles using photochromic FRET. Photochem. Photobiol. 88, 90-97 (2011).
21. Barker, S. L., Kopelman, R., Meyer, T. E. & Cusanovich, M. A. Fiber-optic nitric oxide-selective biosensors and nanosensors. Anal. Chem. 70, 971-976 (1998).
22. Kuznetsova, S. et al. The enzyme mechanism of nitrite reductase studied at single-molecule level. Proc. Natl Acad. Sci. USA 105, 3250-3255 (2008). (Pubitemid 351723539)
23. Gong, Y., Wagner, M. J., Li, J. Z. & Schnitzer, M. J. Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nat. Commun. 5, 3674 (2014).
24. Maclaurin, D., Venkatachalam, V., Lee, H. & Cohen, A. E. Mechanism of voltage-sensitive fluorescence in a microbial rhodopsin. Proc. Natl Acad. Sci. USA 110, 5939-5944 (2013).
25. Shaner, N. C. et al. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat. Methods 5, 545-551 (2008). (Pubitemid 351761763)
26. Enami, N. et al. Crystal structures of archaerhodopsin-1 and-2: common structural motif in archaeal light-driven proton pumps. J. Mol. Biol. 358, 675-685 (2006).
27. Shu, X., Shaner, N. C., Yarbrough, C. A., Tsien, R. Y. & Remington, S. J. Novel chromophores and buried charges control colour in mFruits. Biochemistry 45, 9639-9647 (2006). (Pubitemid 44257411)
28. Gradinaru, V. et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154-165 (2010).
29. Heim, R. & Tsien, R. Y. Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr. Biol. 6, 178-182 (1996).
30. Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A. & Tsien, R. Y. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276, 29188-29194 (2001).
31. Shcherbo, D. et al. Far-red fluorescent tags for protein imaging in living tissues. Biochem. J. 418, 567-574 (2009).
32. Chung, Y. G., Schwartz, J. A. & Sawaya, R. E. Diagnostic potential of laserinduced autofluorescence emission in brain tissue. J. Korean Med. Sci. 12.2, 135-142 (1997). (Pubitemid 127711464)
33. Lin, W., Toms, S. A., Motamedi, M., Jansen, E. D. & Mahadevan-Jansen, A. Brain tumor demarcation using optical spectroscopy; an in vitro study. J. Biomed. Opt. 5, 214-220 (2000).
34. Flock, S. T., Jacques, S. L., Wilson, B. C., Star, W. M. & van Gemert, M. J. Optical properties of Intralipid: a phantom medium for light propagation studies. Lasers Surg. Med. 12, 510-519 (1992).
35. Zhang, J., Davidson, R. M., Wei, M. & Loew, L. M. Membrane electric properties by combined patch clamp and fluorescence ratio imaging in single neurons. Biophys. J. 74, 48-53 (1998). (Pubitemid 28041735)
36. Hou, J. H., Venkatachalam, V. & Cohen, A. E. Temporal dynamics of microbial rhodopsin fluorescence reports absolute membrane voltage. Biophys. J. 106, 639-648 (2014).
37. Fisher, J. A. et al. Two-photon excitation of potentiometric probes enables optical recording of action potentials from mammalian nerve terminals in situ. J. Neurophysiol. 99, 1545-1553 (2008). (Pubitemid 351413729)
38. Akemann, W. et al. Two-photon voltage imaging using a genetically encoded voltage indicator. Sci. Rep. 3, 2231 (2013).
39. Beja, O., Spudich, E. N., Spudich, J. L., Leclerc, M. & Delong, E. F. Proteorhodopsin phototrophy in the ocean. Nature 411, 786-789 (2001). (Pubitemid 32588098)
40. Spudich, J. L. The multitalented microbial sensory rhodopsins. Trends Microbiol. 14, 480-487 (2006). (Pubitemid 44537810)
41. Bujard, H. et al. A T5 promoter-based transcription-translation system for the analysis of proteins in vitro and in vivo. Meth. Enzymol. 155, 416-433 (1987).
42. Hille, B. in Ion Channels of Excitable Membranes (Sinauer, 2001).
43. Chen, G., Harata, N. C. & Tsien, R. W. Paired-pulse depression of unitary quantal amplitude at single hippocampal synapses. Proc. Natl Acad. Sci. USA 101, 1063-1068 (2004). (Pubitemid 38160584)