Designs and sensing mechanisms of genetically encoded fluorescent voltage indicators

Current Opinion in Chemical Biology

Volumn 27, Issue , 2015, Pages 31-38

  St Pierre, François ^a,b   Chavarha, Mariya ^a,b   Lin, Michael Z ^a,b,c  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; RHODOPSIN; FLUORESCENT DYE; PHOTOPROTEIN; PROTEIN BINDING;

CONFORMATIONAL TRANSITION; ELECTRIC POTENTIAL; FLUORESCENCE; NONHUMAN; PHYSICAL PHENOMENA; REVIEW; SENSOR; ACTION POTENTIAL; ANIMAL; CELL MEMBRANE; CHEMISTRY; DEVICES; GENETIC PROCEDURES; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; PROCEDURES; VOLTAGE SENSITIVE DYE IMAGING;

ACTION POTENTIALS; ANIMALS; BIOSENSING TECHNIQUES; CELL MEMBRANE; FLUORESCENT DYES; HUMANS; LUMINESCENT PROTEINS; NEURONS; PROTEIN BINDING; VOLTAGE-SENSITIVE DYE IMAGING;

EID: 84930959289     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2015.05.003     Document Type: Review

References (61)

1. Mutoh H., Akemann W., Knöpfel T. Genetically engineered fluorescent voltage reporters. ACS Chem Neurosci 2012, 3:585-592.
2. Chemla S., Chavane F. Voltage-sensitive dye imaging: technique review and models. J Physiol Paris 2010, 104:40-50.
3. Jensen M.O., Jogini V., Borhani D.W., Leffler A.E., Dror R.O., Shaw D.E. Mechanism of voltage gating in potassium channels. Science 2012, 336:229-233.
4. Li Q., Wanderling S., Paduch M., Medovoy D., Singharoy A., McGreevy R., Villalba-Galea C.A., Hulse R.E., Roux B., Schulten K., et al. Structural mechanism of voltage-dependent gating in an isolated voltage-sensing domain. Nat Struct Mol Biol 2014, 21:244-252.
5. + channel. Cell 2005, 123:463-475.
6. Ataka K., Pieribone V.A. A genetically targetable fluorescent probe of channel gating with rapid kinetics. Biophys J 2002, 82:509-516.
7. Guerrero G., Siegel M.S., Roska B., Loots E., Isacoff E.Y. Tuning FlaSh: redesign of the dynamics, voltage range, and color of the genetically encoded optical sensor of membrane potential. Biophys J 2002, 83:3607-3618.
8. Sakai R., Repunte-Canonigo V., Raj C.D., Knöpfel T. Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. Eur J Neurosci 2001, 13:2314-2318.
9. Baker B.J., Lee H., Pieribone V.A., Cohen L.B., Isacoff E.Y., Knöpfel T., Kosmidis E.K. Three fluorescent protein voltage sensors exhibit low plasma membrane expression in mammalian cells. J Neurosci Methods 2007, 161:32-38.
10. Dimitrov D., He Y., Mutoh H., Baker B.J., Cohen L., Akemann W., Knöpfel T. Engineering and characterization of an enhanced fluorescent protein voltage sensor. PLoS One 2007, 2:e440.
11. Murata Y., Iwasaki H., Sasaki M., Inaba K., Okamura Y. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 2005, 435:1239-1243.
12. Kohout S.C., Ulbrich M.H., Bell S.C., Isacoff E.Y. Subunit organization and functional transitions in Ci-VSP. Nat Struct Mol Biol 2008, 15:106-108.
13. Villalba-Galea C.A., Frezza L., Sandtner W., Bezanilla F. Sensing charges of the Ciona intestinalis voltage-sensing phosphatase. J Gen Physiol 2013, 142:543-555.
14. Baker B.J., Jin L., Han Z., Cohen L.B., Popovic M., Platisa J., Pieribone V. Genetically encoded fluorescent voltage sensors using the voltage-sensing domain of Nematostella and Danio phosphatases exhibit fast kinetics. J Neurosci Methods 2012, 208:190-196.
15. 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.
16. Tsutsui H., Karasawa S., Okamura Y., Miyawaki A. Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 2008, 5:683-685.
17. Tsutsui H., Jinno Y., Tomita A., Niino Y., Yamada Y., Mikoshiba K., Miyawaki A., Okamura Y. Improved detection of electrical activity with a voltage probe based on a voltage-sensing phosphatase. J Physiol 2013, 591:4427-4437.
18. Akemann W., Mutoh H., Perron A., Park Y.K., Iwamoto Y., Knöpfel T. Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein. J Neurophysiol 2012, 108:2323-2337.
19. Akemann W., Mutoh H., Perron A., Rossier J., Knöpfel T. Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat Methods 2010, 7:643-649.
20. Perron A., Mutoh H., Akemann W., Gautam S.G., Dimitrov D., Iwamoto Y., Knöpfel T. Second and third generation voltage-sensitive fluorescent proteins for monitoring membrane potential. Front Mol Neurosci 2009, 2:5.
21. Mishina Y., Mutoh H., Knöpfel T. Transfer of Kv3.1 voltage sensor features to the isolated Ci-VSP voltage-sensing domain. Biophys J 2012, 103:669-676.
22. 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, 7:78.
23. Villalba-Galea C.A., Sandtner W., Dimitrov D., Mutoh H., Knöpfel T., Bezanilla F. Charge movement of a voltage-sensitive fluorescent protein. Biophys J 2009, 96:L19-L21.
24. Villalba-Galea C.A., Sandtner W., Starace D.M., Bezanilla F. S4-based voltage sensors have three major conformations. Proc Natl Acad Sci U S A 2008, 105:17600-17607.
25. Perron A., Mutoh H., Launey T., Knöpfel T. Red-shifted voltage-sensitive fluorescent proteins. Chem Biol 2009, 16:1268-1277.
26. Lundby A., Mutoh H., Dimitrov D., Akemann W., Knöpfel T. Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci-VSP voltage-sensing movements. PLoS One 2008, 3:e2514.
27. 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.
28. Han Z., Jin L., Chen F., Loturco J.J., Cohen L.B., Bondar A., Lazar J., Pieribone V.A. Mechanistic studies of the genetically encoded fluorescent protein voltage probe ArcLight. PLoS One 2014, 9:e113873.
29. Thompson S.M., Masukawa L.M., Prince D.A. Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal CA1 neurons in vitro. J Neurosci 1985, 5:817-824.
30. Piao H.H., Rajakumar D., Kang B.E., Kim E.H., Baker B.J. Combinatorial mutagenesis of the voltage-sensing domain enables the optical resolution of action potentials firing at 60Hz by a genetically encoded fluorescent sensor of membrane potential. J Neurosci 2015, 35:372-385.
31. Han Z., Jin L., Platisa J., Cohen L.B., Baker B.J., Pieribone V.A. Fluorescent protein voltage probes derived from ArcLight that respond to membrane voltage changes with fast kinetics. PLoS One 2013, 8:e81295.
32. Baird G.S., Zacharias D.A., Tsien R.Y. Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci U S A 1999, 96:11241-11246.
33. Barnett L., Platisa J., Popovic M., Pieribone V.A., Hughes T. A fluorescent, genetically-encoded voltage probe capable of resolving action potentials. PLoS One 2012, 7:e43454.
34. Gautam S.G., Perron A., Mutoh H., Knöpfel T. Exploration of fluorescent protein voltage probes based on circularly permuted fluorescent proteins. Front Neuroeng 2009, 2:14.
35. 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.
36. 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, 5:4625.
37. Haupts U., Maiti S., Schwille P., Webb W.W. Dynamics of fluorescence fluctuations in green fluorescent protein observed by fluorescence correlation spectroscopy. Proc Natl Acad Sci U S A 1998, 95:13573-13578.
38. Ernst O.P., Lodowski D.T., Elstner M., Hegemann P., Brown L.S., Kandori H. Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem Rev 2013, 114:126-163.
39. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 2005, 8:1263-1268.
40. 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.
41. 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 2011, 333:345-348.
42. 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.
43. Chow B.Y., Han X., Dobry A.S., Qian X., Chuong A.S., Li M., Henninger M.A., Belfort G.M., Lin Y., Monahan P.E., Boyden E.S. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 2010, 463:98-102.
44. 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.
45. Gong Y., Li J.Z., Schnitzer M.J. Enhanced Archaerhodopsin fluorescent protein voltage indicators. PLoS One 2013, 8:e66959.
46. 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 Methods 2014, 11:825-833.
47. McIsaac R.S., Engqvist M.K., Wannier T., Rosenthal A.Z., Herwig L., Flytzanis N.C., Imasheva E.S., Lanyi J.K., Balashov S.P., Gradinaru V., Arnold F.H. Directed evolution of a far-red fluorescent rhodopsin. Proc Natl Acad Sci U S A 2014, 111:13034-13039.
48. 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.
49. 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.
50. Peterka D.S., Takahashi H., Yuste R. Imaging voltage in neurons. Neuron 2011, 69:9-21.
51. 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.
52. Carandini M., Shimaoka D., Rossi L.F., Sato T.K., Benucci A., Knöpfel T. Imaging the awake visual cortex with a genetically encoded voltage indicator. J Neurosci 2015, 35:53-63.
53. Akemann W., Sasaki M., Mutoh H., Imamura T., Honkura N., Knöpfel T. Two-photon voltage imaging using a genetically encoded voltage indicator. Sci Rep 2013, 3:2231.
54. Scott G., Fagerholm E.D., Mutoh H., Leech R., Sharp D.J., Shew W.L., Knöpfel T. Voltage imaging of waking mouse cortex reveals emergence of critical neuronal dynamics. J Neurosci 2014, 34:16611-16620.
55. Ahrens K.F., Heider B., Lee H., Isacoff E.Y., Siegel R.M. Two-photon scanning microscopy of in vivo sensory responses of cortical neurons genetically encoded with a fluorescent voltage sensor in rat. Front Neural Circuits 2012, 6:15.
56. Leyton-Mange J.S., Mills R.W., Macri V.S., Jang M.Y., Butte F.N., Ellinor P.T., Milan D.J. Rapid cellular phenotyping of human pluripotent stem cell-derived cardiomyocytes using a genetically encoded fluorescent voltage sensor. Stem Cell Reports 2014, 2:163-170.
57. Hou J.H., Kralj J.M., Douglass A.D., Engert F., Cohen A.E. Simultaneous mapping of membrane voltage and calcium in zebrafish heart in vivo reveals chamber-specific developmental transitions in ionic currents. Front Physiol 2014, 5:344.
58. Tsutsui H., Higashijima S., Miyawaki A., Okamura Y. Visualizing voltage dynamics in zebrafish heart. J Physiol 2010, 588:2017-2021.
59. Hou J.H., Venkatachalam V., Cohen A.E. Temporal dynamics of microbial rhodopsin fluorescence reports absolute membrane voltage. Biophys J 2014, 106:639-648.
60. Tsutsui H., Jinno Y., Tomita A., Okamura Y. Rapid evaluation of a protein-based voltage probe using a field-induced membrane potential change. Biochim Biophys Acta 2014, 1838:1730-1737.
61. 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.