Exploration of genetically encoded voltage indicators based on a Chimeric voltage sensing domain

Frontiers in Molecular Neuroscience

Volumn 7, Issue SEP, 2014, Pages

  Mishina, Yukiko ^a,b   Mutoh, Hiroki ^a,c   Song, Chenchen ^d   Knopfel, Thomas ^d  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

FRET sensors; Mouse model; Optical imaging; Optogenetics; Voltage imaging

Indexed keywords

CHIMERIC PROTEIN; FLUORESCENT DYE; GENETICALLY ENCODED VOLTAGE INDICATOR; OPSIN; SHAW POTASSIUM CHANNEL; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE SENSING DOMAIN; VOLTAGE SENSITIVE FLUORESCENT PROTEIN; VOLTAGE SENSITIVE PHOSPHATASE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CIONA INTESTINALIS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DNA SEQUENCE; ELECTROPHYSIOLOGY; ELECTROPORATION; EVOKED CORTICAL RESPONSE; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; MOUSE; NERVOUS SYSTEM POTENTIAL; NONHUMAN; PC12 CELL LINE; POLYMERASE CHAIN REACTION; RAT; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; SOMATOSENSORY CORTEX; VISUAL CORTEX; VOLTAGE CLAMP TECHNIQUE;

EID: 84907526483     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2014.00078     Document Type: Article

References (34)

1. Akemann, W., Mutoh, H., Perron, A., Park, Y. K., Iwamoto, Y., and Knopfel, T. (2012). Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein. J. Neurophysiol. 108, 2323-2337. doi: 10.1152/jn.00452.2012
2. Akemann, W., Mutoh, H., Perron, A., Rossier, J., and Knopfel, T. (2010). Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat. Methods 7, 643-649. doi: 10.1038/nmeth.1479
3. Alford, S. C., Wu, J., Zhao, Y., Campbell, R. E., and Knopfel, T. (2013). Optogenetic reporters. Biol. Cell 105, 14-29. doi: 10.1111/boc.201200054
4. Diez-Garcia, J., Akemann, W., and Knopfel, T. (2007) In vivo calcium imaging from genetically specified target cells in mouse cerebellum. Neuroimage 34, 859-869. doi: 10.1016/j.neuroimage.2006.10.021
5. Dimitrov, D., He, Y., Mutoh, H., Baker, B. J., Cohen, L., Akemann, W., et al. (2007). Engineering and characterization of an enhanced fluorescent protein voltage sensor. PLoS ONE 2:e440. doi: 10.1371/journal.pone.0000440
6. Gong, Y., Wagner, M. J., Zhong, L. J., and Schnitzer, M. J. (2014). Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nat. Commun. 5, 3674. doi: 10.1038/ncomms4674
7. Grinvald, A., and Hildesheim, R. (2004). VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 5, 874-885. doi: 10.1038/ nrn1536
8. Grinvald, A., Salzberg, B. M., and Cohen, L. B. (1977). Simultaneous recording from several neurones in an invertebrate central nervous system. Nature 268, 140-142. doi: 10.1038/268140a0
9. Han, Z., Jin, L., Platisa, J., Cohen, L. B., Baker, B. J., and Pieribone, V. A. (2013). Fluorescent protein voltage probes derived from ArcLight that respond to membrane voltage changes with fast kinetics. PLoS ONE 8:e81295. doi: 10.1371/journal.pone.0081295
10. Jin, L., Han, Z., Platisa, J., Wooltorton, J. R., Cohen, L. B., and Pieribone, V. A. (2012). Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 75, 779-785. doi: 10.1016/j.neuron.2012.06.040
11. Kenet, T., Bibitchkov, D., Tsodyks, M., Grinvald, A., and Arieli, A. (2003). Spontaneously emerging cortical representations of visual attributes. Nature 425, 954-956. doi: 10.1038/nature02078
12. Knopfel, T. (2012). Genetically encoded optical indicators for the analysis of neuronal circuits. Nat. Rev. Neurosci. 13, 687-700. doi: 10.1038/nrn3293
13. Kralj, J. M., Douglass, A. D., Hochbaum, D. R., Maclaurin, D., and Cohen, A. E. (2012). Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 9, 90-95. doi: 10.1038/nmeth.1782
14. Lam, A. J., St-Pierre, F., Gong, Y., Marshall, J. D., Cranfill, P. J., Baird, M. A., etal. (2012). Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005-1012. doi: 10.1038/nmeth.2171
15. Lundby, A., Akemann, W., and Knopfel, T. (2010). Biophysical characterization of the fluorescent protein voltage probe VSFP2.3 based on the voltage-sensing domain of Ci-VSP. Eur. Biophys. J. 39, 1625-1635. doi: 10.1007/s00249-010-0620-0
16. Lundby, A., Mutoh, H., Dimitrov, D., Akemann, W., and Knopfel, T. (2008). Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci-VSP voltage-sensing movements. PLoS ONE 3:e2514. doi: 10.1371/jour-nal.pone.0002514
17. Maclaurin, D., Venkatachalam, V., Lee, H., and Cohen, A. E. (2013). Mechanism of voltage-sensitive fluorescence in a microbial rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 110, 5939-5944. doi: 10.1073/pnas.1215595110
18. Mishina, Y., Mutoh, H., and Knopfel, T. (2012). Transfer of Kv3.1 voltage sensor features to the isolated Ci-VSP voltage-sensing domain. Biophys. J. 103, 669-676. doi: 10.1016/j.bpj.2012.07.031
19. Mutoh, H., Akemann, W., andKnopfel, T. (2012). Geneticallyengineered fluorescent voltage reporters. ACS Chem. Neurosci. 3, 585-592. doi: 10.1021/cn300041b
20. Mutoh, H., and Knopfel, T. (2013). Probing neuronal activities with genetically encoded optical indicators: from a historical to a forward-looking perspective. Pflugers Arch. 465, 361-371. doi: 10.1007/s00424-012-1202-z
21. Mutoh, H., Perron, A., Dimitrov, D., Iwamoto, Y., Akemann, W., Chudakov, D. M., et al. (2009). Spectrally-resolved response properties of the three most advanced FRET based fluorescent protein voltage probes. PLoS ONE 4:e4555. doi: 10.1371/journal.pone.0004555
22. Perron, A., Mutoh, H., Akemann, W., Gautam, S. G., Dimitrov, D., Iwamoto, Y., et al. (2009a). Second and third generation voltage-sensitive fluorescent proteins for monitoring membrane potential. Front. Mol. Neurosci. 2:5. doi: 10.3389/neuro.02.005.2009
23. Perron, A., Mutoh, H., Launey, T., and Knopfel, T. (2009b). Red-shifted voltage-sensitive fluorescent proteins. Chem. Biol. 16, 1268-1277. doi: 10.1016/j.chembiol.2009.11.014
24. Petersen, C. C., Grinvald, A., and Sakmann, B. (2003a). Spatiotemporal dynamics of sensoryresponses in layer 2/3 of rat barrel cortex measured in vivo byvoltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J. Neurosci. 23, 1298-1309.
25. Petersen, C. C., Hahn, T. T., Mehta, M., Grinvald, A., and Sakmann, B. (2003b). Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. U.S.A. 100, 13638-13643. doi: 10.1073/pnas.2235811100
26. Ross, W. N., Salzberg, B. M., Cohen, L. B., and Davila, H. V. (1974). A large change in dye absorption during the action potential. Biophys. J. 14, 983-986. doi: 10.1016/S0006-3495(74)85963-1
27. Sakai, R., Repunte-Canonigo, V., Raj, C. D., and Knopfel, T. (2001). Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. Eur. J. Neurosci. 13, 2314-2318. doi: 10.1046/j.0953-816x.2001.01617.x
28. Shoham, D., Glaser, D. E., Arieli, A., Kenet, T., Wijnbergen, C., Toledo, Y., et al. (1999). Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24, 791-802. doi: 10.1016/S0896-6273(00)81027-2
29. St-Pierre, F., Marshall, J. D., Yang, Y., Gong, Y., Schnitzer, M.J., andLin, M.Z. (2014). High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat. Neurosci. 17, 884-889. doi: 10.1038/nn.3709
30. Tsutsui, H., Jinno, Y., Tomita, A., Niino, Y., Yamada, Y., Mikoshiba, K., etal. (2013). Improved detection of electrical activity with a voltage probe based on a voltage-sensing phosphatase. J. Physiol. 591, 4427-4437. doi: 10.1113/jphysiol.2013.257048
31. Tsutsui, H., Karasawa, S., Okamura, Y., and Miyawaki, A. (2008). Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat. Methods 5, 683-685. doi: 10.1038/nmeth.1235
32. Vargas, E., Yarov-Yarovoy, V., Khalili-Araghi, F., Catterall, W. A., Klein, M. L., Tarek, M., et al. (2012).An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations. J. Gen. Physiol. 140, 587-594. doi: 10.1085/jgp.201210873
33. Villalba-Galea, C. A., Sandtner, W., Starace, D. M., and Bezanilla, F. (2008). S4-based voltage sensors have three major conformations. Proc. Natl. Acad. Sci. U.S.A. 105, 17600-17607. doi: 10.1073/pnas.0807387105
34. Zou, P., Zhao, Y., Douglass, A. D., Hochbaum, D. R., Brinks, D., Werley, C. A., et al. (2014). Bright andfast multicolouredvoltage reporters via electrochromic FRET. Nat. Commun. 5, 4625. doi: 10.1038/ncomms5625