The evolving capabilities of rhodopsin-based genetically encoded voltage indicators

Current Opinion in Chemical Biology

Volumn 27, Issue , 2015, Pages 84-89

  Gong, Yiyang ^a  

^a Duke University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; RHODOPSIN; FLUORESCENT DYE; HYBRID PROTEIN; PHOTOPROTEIN;

ACTION POTENTIAL; ELECTRIC POTENTIAL; FLUORESCENCE; KINETICS; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; REVIEW; SENSOR; SIGNAL NOISE RATIO; SPIKE; ANIMAL; CELL CULTURE; CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC PROCEDURES; GENETICS; HUMAN; PHYSIOLOGY; PROCEDURES; VOLTAGE SENSITIVE DYE IMAGING;

ANIMALIA;

ACTION POTENTIALS; ANIMALS; BIOSENSING TECHNIQUES; CELLS, CULTURED; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HUMANS; KINETICS; LUMINESCENT PROTEINS; NEURONS; RECOMBINANT FUSION PROTEINS; RHODOPSIN; VOLTAGE-SENSITIVE DYE IMAGING;

EID: 84934764172     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2015.05.006     Document Type: Review

References (31)

1. Peterka D.S., Takahashi H., Yuste R. Imaging voltage in neurons. Neuron 2011, 69:9-21.
2. Mutoh H., Akemann W., Knopfel T. Genetically engineered fluorescent voltage reporters. ACS Chem Neurosci 2012, 3:585-592.
3. Akerboom J., Chen T.W., Wardill T.J., Tian L., Marvin J.S., Mutlu S., Calderon N.C., Esposti F., Borghuis B.G., Sun X.R., et al. Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 2012, 32:13819-13840.
4. Chen T.W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
5. Lundby A., Mutoh H., Dimitrov D., Akemann W., Knopfel T. Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci-VSP voltage-sensing movements. PLoS One 2008, 3:e2514.
6. Tsutsui H., Karasawa S., Okamura Y., Miyawaki A. Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 2008, 5:683-685.
7. Lundby A., Akemann W., Knopfel T. Biophysical characterization of the fluorescent protein voltage probe VSFP2.3 based on the voltage-sensing domain of Ci-VSP. Eur Biophys J 2010, 39:1625-1635.
8. Lam A.J., St-Pierre F., Gong Y., Marshall J.D., Cranfill P.J., Baird M.A., McKeown M.R., Wiedenmann J., Davidson M.W., Schnitzer M.J., et al. Improving FRET dynamic range with bright green and red fluorescent proteins. Nat Methods 2012, 9:1005-1012.
9. Akemann W., Mutoh H., Perron A., Park Y.K., Iwamoto Y., Knopfel T. Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein. J Neurophysiol 2012, 108:2323-2337.
10. Mishina Y., Mutoh H., Song C., Knöpfel T. Exploration of genetically encoded voltage indicators based on a chimeric voltage sensing domain. Front Mol Neurosci 2014, 7.
11. Jin L., Han Z., Platisa J., Wooltorton J.R., Cohen L.B., Pieribone V.A. Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 2012, 75:779-785.
12. Cao G., Platisa J., Pieribone V.A., Raccuglia D., Kunst M., Nitabach M.N. Genetically targeted optical electrophysiology in intact neural circuits. Cell 2013, 154:904-913.
13. St-Pierre F., Marshall J.D., Yang Y., Gong Y., Schnitzer M.J., Lin M.Z. High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat Neurosci 2014, 17:884-889.
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 2012, 9:90-95.
15. Lanyi J.K. Proton transfer and energy coupling in the bacteriorhodopsin photocycle. J Bioenerg Biomembr 1992, 24:169-179.
16. Lanyi J.K. Bacteriorhodopsin. Annu Rev Physiol 2004, 66:665-688.
17. Kolodner P., Lukashev E.P., Ching Y.C., Rousseau D.L. Electric-field-induced Schiff-base deprotonation in D85N mutant bacteriorhodopsin. Proc Natl Acad Sci U S A 1996, 93:11618-11621.
18. Marinetti T., Subramaniam S., Mogi T., Marti T., Khorana H.G. Replacement of aspartic residues 85, 96, 115, or 212 affects the quantum yield and kinetics of proton release and uptake by bacteriorhodopsin. Proc Natl Acad Sci U S A 1989, 86:529-533.
19. Moltke S., Krebs M.P., Mollaaghababa R., Khorana H.G., Heyn M.P. Intramolecular charge transfer in the bacteriorhodopsin mutants Asp85-->Asn and Asp212-->Asn: effects of pH and anions. Biophys J 1995, 69:2074-2083.
20. --dependent photovoltage responses of bacteriorhodopsin: comparison of the D85T and D85S mutants and wild-type acid purple form. FEBS Lett 1997, 418:239-242.
21. Gong Y., Li J.Z., Schnitzer M.J. Enhanced archaerhodopsin fluorescent protein voltage indicators. PLoS One 2013, 8:e66959.
22. Maclaurin D., Venkatachalam V., Lee H., Cohen A.E. Mechanism of voltage-sensitive fluorescence in a microbial rhodopsin. Proc Natl Acad Sci U S A 2013, 110:5939-5944.
23. Park J., Werley C.A., Venkatachalam V., Kralj J.M., Dib-Hajj S.D., Waxman S.G., Cohen A.E. Screening fluorescent voltage indicators with spontaneously spiking HEK cells. PLoS One 2013, 8:e85221.
24. Venkatachalam V., Brinks D., Maclaurin D., Hochbaum D., Kralj J., Cohen A.E. Flash memory: photochemical imprinting of neuronal action potentials onto a microbial rhodopsin. J Am Chem Soc 2014, 136:2529-2537.
25. Hochbaum D.R., Zhao Y., Farhi S.L., Klapoetke N., Werley C.A., Kapoor V., Zou P., Kralj J.M., Maclaurin D., Smedemark-Margulies N., et al. All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat Meth 2014, 11:825-833.
26. Flytzanis N.C., Bedbrook C.N., Chiu H., Engqvist M.K., Xiao C., Chan K.Y., Sternberg P.W., Arnold F.H., Gradinaru V. Archaerhodopsin variants with enhanced voltage-sensitive fluorescence in mammalian and Caenorhabditis elegans neurons. Nat Commun 2014, 5:4894.
27. Bayraktar H., Fields A.P., Kralj J.M., Spudich J.L., Rothschild K.J., Cohen A.E. Ultrasensitive measurements of microbial rhodopsin photocycles using photochromic FRET. Photochem Photobiol 2012, 88:90-97.
28. Gong Y., Wagner M.J., Zhong Li J., Schnitzer M.J. Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nat Commun 2014, 5:3674.
29. Zou P., Zhao Y., Douglass A.D., Hochbaum D.R., Brinks D., Werley C.A., Harrison D.J., Campbell R.E., Cohen A.E. Bright and fast multicoloured voltage reporters via electrochromic FRET. Nat Commun 2014, 5.
30. Waschuk S.A., Bezerra A.G., Shi L., Brown L.S. Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc Natl Acad Sci U S A 2005, 102:6879-6883.
31. Wilt B.A., Fitzgerald J.E., Schnitzer M.J. Photon shot noise limits on optical detection of neuronal spikes and estimation of spike timing. Biophys J 2013, 104:51-62.