Genetically encoded voltage indicator

Genetically encoded voltage indicator (or GEVI) is a protein that can sense membrane potential in a cell and relate the change in voltage to a form of output, often fluorescent level.[1] It is a promising optogenetic recording tool that enables exporting electrophysiological signals from cultured cells, live animals, and ultimately human brain. Examples of notable GEVIs include ArcLight, ASAP1,[2] ASAP2s, [3] and Ace2N-mNeon.

History

Despite that the idea of optical measurement of neuronal activity was proposed in the late 1960s,[4] the first successful GEVI that was convenient enough to put into actual use was not developed until technologies of genetic engineering had become mature in the late 1990s. The first GEVI, coined FlaSh,[5] was constructed by fusing a modified green fluorescent protein with a voltage-sensitive K+ channel (Shaker). Unlike fluorescent proteins, the discovery of new GEVIs were seldomly inspired by the nature, for it is hard to find an organism which naturally has the ability to change its fluorescence based on voltage. Therefore, new GEVIs are mostly the products of genetic and protein engineering.

Two methods can be utilized to find novel GEVIs: rational design and directed evolution. The former method contributes to the most of new GEVI variants, but recent researches using directed evolution have shown promising results in GEVI optimization.[6]

Structure

GEVI can have many configuration designs in order to realize voltage sensing function.[7] An essential feature of GEVI structure is that it must situate on the cell membrane. Conceptually, the structure of a GEVI should permit the function of sensing the voltage difference and reporting it by change in fluorescence. Usually, the voltage-sensing domain (VSD) of a GEVI spans across the membrane, and is connected to the fluorescent protein(s). However, it is not necessary that sensing and reporting should happen in different structures, e.g. Arch.

By structure, GEVIs can be classified into four categories based on the current findings: (1) GEVIs contain a fluorescent protein FRET pair, e.g. VSFP1, (2) Single opsion GEVIs, e.g. Arch, (3) Opsin-FP FRET pair GEVIs, e.g. MacQ-mCitrine, (4) single FP with special types of voltage sensing domains, e.g. ASAP1. A majority of GEVIs are based on the Ciona intestinalis voltage sensitive phosphatase (Ci-VSP or Ci-VSD (domain)), which was discovered in 2005 from the genomic survey of the organism.[8] Some GEVIs might have similar components, but with different positioning of them. For example, ASAP1 and ArcLight both use a VSD and one FP, but the FP of ASAP1 is on the outside of the cell whereas that of ArcLight is on the inside, and the two FPs of VSFP-Butterfly are separated by the VSD, while the two FPs of Mermaid are relatively close to each other.

Table of GEVIs and their structure
GEVI[A] Year Sensing Reporting Precursor
FlaSh[5] 1997 Shaker (K+ channel) GFP -
VSFP1[9] 2001 Rat Kv2.1 (K+ channel) FRET pair: CFP and YFP -
SPARC[10] 2002 Rat Na+ channel GFP -
VSFP2's[11] 2007 Ci-VSD FRET pair: CFP (Cerulean) and YFP (Citrine) VSFP1
Flare[12] 2007 Kv1.4 (K+ channel) YFP FlaSh
VSFP3.1[13] 2008 Ci-VSD CFP VSFP2's
Mermaid[14] 2008 Ci-VSD FRET pair: Marine GFP (mUKG) and OFP (mKOκ) VSFP2's
hVOS[15] 2008 Dipicrylamine GFP -
Red-shifted VSFP's[16] 2009 Ci-VSD RFP/YFP (Citrine, mOrange2, TagRFP, or mKate2) VSFP3.1
PROPS[17] 2011 Modified green-absorbing proteorhodopsin (GPR) Same as left -
Zahra, Zahra 2[18] 2012 Nv-VSD, Dr-VSD FRET pair: CFP (Cerulean) and YFP (Citrine) VSFP2's
ArcLight[19] 2012 Ci-VSD Modified super ecliptic pHluorin -
Arch[20] 2012 Archaerhodopsin 3 Same as left -
ElectricPk[21] 2012 Ci-VSD Circularly permuted EGFP VSFP3.1
VSFP-Butterfly[22] 2012 Ci-VSD FRET pair: YFP (mCitrine) and RFP (mKate2) VSFP2's
VSFP-CR[23] 2013 Ci-VSD FRET pair: GFP (Clover) and RFP(mRuby2) VSFP2.3
Mermaid2[24] 2013 Ci-VSD FRET pair: CFP (seCFP2) and YFP Mermaid
Mac GEVIs[25] 2014 Mac rhodopsin (FRET acceptor) FRET doner: mCitrine, or mOrange2 -
QuasAr1, QuasAr2[26] 2014 Modified Archaerhodopsin 3 Same as left Arch
Archer[27] 2014 Modified Archaerhodopsin 3 Same as left Arch
ASAP1[2] 2014 Modified Gg-VSD Circularly permuted GFP -
Ace GEVIs[28] 2015 Modified Ace rhodopsin FRET doner: mNeonGreen Mac GEVIs
Pado[29] 2016 Voltage-gated proton channel Super ecliptic pHluorin -
ASAP2f[30] 2016 Modified Gg-VSD Circularly permuted GFP ASAP1
FlicR1[31] 2016 Ci-VSD Circularly permuted RFP (mApple) VSFP3.1
Bongwoori[32] 2017 Ci-VSD Modified super ecliptic pHluorin ArcLight
ASAP2s[33] 2017 Modified Gg-VSD Circularly permuted GFP ASAP1
  1. ↑Names in italic denote GEVIs not named.

Characteristics

A GEVI can be evaluated by its many characteristics. These traits can be classified into two categories: performance and compatibility. The performance properties include brightness, photostability, sensitivity, kinetics (speed), linearity of response, etc., while the compatibility properties cover toxicity (phototoxicity), plasma membrane localization, adaptability of deep-tissue imaging, etc.[34] For now, no existing GEVI meets all the desired properties, so searching for a perfect GEVI is still a quite competitive research area.

Applications and advantages

Different types of GEVIs are seen being used in many biological or physiological research areas. It is thought to be superior to conventional voltage detecting methods like electrode-based electrophysiological recordings, calcium imaging, or voltage sensitive dyes. It can show neuron signals with subcellular spatial resolution.[35] It has fast temporal resolution (sub-millisecond[28]), matching or surpassing that of the electrode recordings, and about one magnitude faster than calcium imaging. Researchers have used it to probe neural communications of an intact brain (of Drosophila[36] or mouse[37]), electrical spiking of bacteria (E. coli[17]), and human stem-cell derived cardiomyocyte.[38]

References

  1. ↑ "Genetically-Encoded Voltage Indicators - OpenOptogenetics.org". www.openoptogenetics.org. Retrieved 2017-05-08.
  2. 1 2 St-Pierre, François; Marshall, Jesse D; Yang, Ying; Gong, Yiyang; Schnitzer, Mark J; Lin, Michael Z. "High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor". Nature Neuroscience. 17 (6): 884–889. doi:10.1038/nn.3709. PMC 4494739. PMID 24755780.
  3. ↑ Chamberland, Simon; Yang, Helen H; Pan, Michael M; Evans, Stephen W; Guan, Sihui; Chavarha, Mariya; Yang, Ying; Salesse, Charleen; Wu, Haodi (2017-07-27). "Fast two-photon imaging of subcellular voltage dynamics in neuronal tissue with genetically encoded indicators". eLife. 6. doi:10.7554/eLife.25690. ISSN 2050-084X.
  4. ↑ Cohen, L. B.; Keynes, R. D.; Hille, B. (1968-05-04). "Light scattering and birefringence changes during nerve activity". Nature. 218 (5140): 438–441. ISSN 0028-0836. PMID 5649693.
  5. 1 2 Siegel, M. S.; Isacoff, E. Y. (1997-10-01). "A genetically encoded optical probe of membrane voltage". Neuron. 19 (4): 735–741. ISSN 0896-6273. PMID 9354320.
  6. ↑ Platisa, Jelena; Vasan, Ganesh; Yang, Amy; Pieribone, Vincent A. (2017-03-15). "Directed Evolution of Key Residues in Fluorescent Protein Inverses the Polarity of Voltage Sensitivity in the Genetically Encoded Indicator ArcLight". ACS Chemical Neuroscience. 8 (3): 513–523. doi:10.1021/acschemneuro.6b00234. ISSN 1948-7193. PMC 5355904. PMID 28045247.
  7. ↑ Gong, Yiyang (2015-08-01). "The evolving capabilities of rhodopsin-based genetically encoded voltage indicators". Current Opinion in Chemical Biology. 27: 84–89. doi:10.1016/j.cbpa.2015.05.006. ISSN 1879-0402. PMC 4571180. PMID 26143170.
  8. ↑ Murata, Yoshimichi; Iwasaki, Hirohide; Sasaki, Mari; Inaba, Kazuo; Okamura, Yasushi (2005-06-30). "Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor". Nature. 435 (7046): 1239–1243. doi:10.1038/nature03650. ISSN 1476-4687. PMID 15902207.
  9. ↑ Sakai, R.; Repunte-Canonigo, V.; Raj, C. D.; Knöpfel, T. (2001-06-01). "Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein". The European Journal of Neuroscience. 13 (12): 2314–2318. ISSN 0953-816X. PMID 11454036.
  10. ↑ Ataka, Kazuto; Pieribone, Vincent A. (2002-01-01). "A genetically targetable fluorescent probe of channel gating with rapid kinetics". Biophysical Journal. 82 (1 Pt 1): 509–516. doi:10.1016/S0006-3495(02)75415-5. ISSN 0006-3495. PMC 1302490. PMID 11751337.
  11. ↑ Dimitrov, Dimitar; He, You; Mutoh, Hiroki; Baker, Bradley J.; Cohen, Lawrence; Akemann, Walther; Knöpfel, Thomas (2007-05-09). "Engineering and characterization of an enhanced fluorescent protein voltage sensor". PLoS One. 2 (5): e440. doi:10.1371/journal.pone.0000440. ISSN 1932-6203. PMC 1857823. PMID 17487283.
  12. ↑ Baker, B. J.; Lee, H.; Pieribone, V. A.; Cohen, L. B.; Isacoff, E. Y.; Knopfel, T.; Kosmidis, E. K. (2007-03-30). "Three fluorescent protein voltage sensors exhibit low plasma membrane expression in mammalian cells". Journal of Neuroscience Methods. 161 (1): 32–38. doi:10.1016/j.jneumeth.2006.10.005. ISSN 0165-0270. PMID 17126911.
  13. ↑ Lundby, Alicia; Mutoh, Hiroki; Dimitrov, Dimitar; Akemann, Walther; Knöpfel, Thomas (2008-06-25). "Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci-VSP voltage-sensing movements". PLoS One. 3 (6): e2514. doi:10.1371/journal.pone.0002514. ISSN 1932-6203. PMC 2429971. PMID 18575613.
  14. ↑ Tsutsui, Hidekazu; Karasawa, Satoshi; Okamura, Yasushi; Miyawaki, Atsushi (2008-08-01). "Improving membrane voltage measurements using FRET with new fluorescent proteins". Nature Methods. 5 (8): 683–685. doi:10.1038/nmeth.1235. ISSN 1548-7105. PMID 18622396.
  15. ↑ Sjulson, Lucas; Miesenböck, Gero (2008-05-21). "Rational optimization and imaging in vivo of a genetically encoded optical voltage reporter". The Journal of Neuroscience. 28 (21): 5582–5593. doi:10.1523/JNEUROSCI.0055-08.2008. ISSN 1529-2401. PMC 2714581. PMID 18495892.
  16. ↑ Perron, Amelie; Mutoh, Hiroki; Launey, Thomas; Knöpfel, Thomas (2009-12-24). "Red-shifted voltage-sensitive fluorescent proteins". Chemistry & Biology. 16 (12): 1268–1277. doi:10.1016/j.chembiol.2009.11.014. ISSN 1879-1301. PMC 2818747. PMID 20064437.
  17. 1 2 Kralj, Joel M.; Hochbaum, Daniel R.; Douglass, Adam D.; Cohen, Adam E. (2011-07-15). "Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein". Science. 333 (6040): 345–348. doi:10.1126/science.1204763. ISSN 1095-9203. PMID 21764748.
  18. ↑ Baker, Bradley J.; Jin, Lei; Han, Zhou; Cohen, Lawrence B.; Popovic, Marko; Platisa, Jelena; Pieribone, Vincent (2012-07). "Genetically encoded fluorescent voltage sensors using the voltage-sensing domain of Nematostella and Danio phosphatases exhibit fast kinetics". Journal of Neuroscience Methods. 208 (2): 190–196. doi:10.1016/j.jneumeth.2012.05.016. ISSN 0165-0270. Check date values in: |date= (help)
  19. ↑ Jin, Lei; Han, Zhou; Platisa, Jelena; Wooltorton, Julian R. A.; Cohen, Lawrence B.; Pieribone, Vincent A. (2012-09-06). "Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe". Neuron. 75 (5): 779–785. doi:10.1016/j.neuron.2012.06.040. ISSN 1097-4199. PMC 3439164. PMID 22958819.
  20. ↑ Kralj, Joel M.; Douglass, Adam D.; Hochbaum, Daniel R.; Maclaurin, Dougal; Cohen, Adam E. (2011-11-27). "Optical recording of action potentials in mammalian neurons using a microbial rhodopsin". Nature Methods. 9 (1): 90–95. doi:10.1038/nmeth.1782. ISSN 1548-7105. PMC 3248630. PMID 22120467.
  21. ↑ Barnett, Lauren; Platisa, Jelena; Popovic, Marko; Pieribone, Vincent A.; Hughes, Thomas (2012-01-01). "A fluorescent, genetically-encoded voltage probe capable of resolving action potentials". PLoS One. 7 (9): e43454. doi:10.1371/journal.pone.0043454. ISSN 1932-6203. PMC 3435330. PMID 22970127.
  22. ↑ Akemann, Walther; Mutoh, Hiroki; Perron, Amélie; Park, Yun Kyung; Iwamoto, Yuka; Knöpfel, Thomas (2012-10-01). "Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein". Journal of Neurophysiology. 108 (8): 2323–2337. doi:10.1152/jn.00452.2012. ISSN 1522-1598. PMID 22815406.
  23. ↑ Lam, Amy J.; St-Pierre, François; Gong, Yiyang; Marshall, Jesse D.; McKeown, Michael R.; Schnitzer, Mark J.; Tsien, Roger Y.; Lin, Michael Z. (2013-01). "Improving FRET Dynamic Range with Bright Green and Red Fluorescent Proteins". Biophysical Journal. 104 (2): 683a. doi:10.1016/j.bpj.2012.11.3773. ISSN 0006-3495. Check date values in: |date= (help)
  24. ↑ Tsutsui, Hidekazu; Jinno, Yuka; Tomita, Akiko; Niino, Yusuke; Yamada, Yoshiyuki; Mikoshiba, Katsuhiko; Miyawaki, Atsushi; Okamura, Yasushi (2013-09-15). "Improved detection of electrical activity with a voltage probe based on a voltage-sensing phosphatase". The Journal of Physiology. 591 (18): 4427–4437. doi:10.1113/jphysiol.2013.257048. ISSN 1469-7793. PMC 3784191. PMID 23836686.
  25. ↑ Gong, Yiyang; Wagner, Mark J.; Zhong Li, Jin; Schnitzer, Mark J. (2014-04-22). "Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors". Nature Communications. 5: 3674. doi:10.1038/ncomms4674. ISSN 2041-1723. PMC 4247277. PMID 24755708.
  26. ↑ Hochbaum, Daniel R.; Zhao, Yongxin; Farhi, Samouil L.; Klapoetke, Nathan; Werley, Christopher A.; Kapoor, Vikrant; Zou, Peng; Kralj, Joel M.; Maclaurin, Dougal (2014-08-01). "All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins". Nature Methods. 11 (8): 825–833. doi:10.1038/nmeth.3000. ISSN 1548-7105. PMC 4117813. PMID 24952910.
  27. ↑ Flytzanis, Nicholas C.; Bedbrook, Claire N.; Chiu, Hui; Engqvist, Martin K. M.; Xiao, Cheng; Chan, Ken Y.; Sternberg, Paul W.; Arnold, Frances H.; Gradinaru, Viviana (2014-09-15). "Archaerhodopsin variants with enhanced voltage-sensitive fluorescence in mammalian and Caenorhabditis elegans neurons". Nature Communications. 5: 4894. doi:10.1038/ncomms5894. ISSN 2041-1723. PMC 4166526. PMID 25222271.
  28. 1 2 Gong, Yiyang; Huang, Cheng; Li, Jin Zhong; Grewe, Benjamin F.; Zhang, Yanping; Eismann, Stephan; Schnitzer, Mark J. (2015-12-11). "High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor". Science. 350 (6266): 1361–1366. doi:10.1126/science.aab0810. ISSN 1095-9203. PMC 4904846. PMID 26586188.
  29. ↑ Kang, Bok Eum; Baker, Bradley J. (2016-04-04). "Pado, a fluorescent protein with proton channel activity can optically monitor membrane potential, intracellular pH, and map gap junctions". Scientific Reports. 6: 23865. doi:10.1038/srep23865. ISSN 2045-2322. PMC 4878010. PMID 27040905.
  30. ↑ Yang, Helen H.; St-Pierre, François; Sun, Xulu; Ding, Xiaozhe; Lin, Michael Z.; Clandinin, Thomas R. (2016-06-30). "Subcellular Imaging of Voltage and Calcium Signals Reveals Neural Processing In Vivo". Cell. 166 (1): 245–257. doi:10.1016/j.cell.2016.05.031. ISSN 1097-4172. PMID 27264607.
  31. ↑ Abdelfattah, Ahmed S.; Farhi, Samouil L.; Zhao, Yongxin; Brinks, Daan; Zou, Peng; Ruangkittisakul, Araya; Platisa, Jelena; Pieribone, Vincent A.; Ballanyi, Klaus (2016-02-24). "A Bright and Fast Red Fluorescent Protein Voltage Indicator That Reports Neuronal Activity in Organotypic Brain Slices". The Journal of Neuroscience. 36 (8): 2458–2472. doi:10.1523/JNEUROSCI.3484-15.2016. ISSN 1529-2401. PMC 4764664. PMID 26911693.
  32. ↑ Lee, Sungmoo; Geiller, Tristan; Jung, Arong; Nakajima, Ryuichi; Song, Yoon-Kyu; Baker, Bradley J. (2017-08-15). "Improving a genetically encoded voltage indicator by modifying the cytoplasmic charge composition". Scientific Reports. 7 (1). doi:10.1038/s41598-017-08731-2. ISSN 2045-2322.
  33. ↑ Chamberland, Simon; Yang, Helen H; Pan, Michael M; Evans, Stephen W; Guan, Sihui; Chavarha, Mariya; Yang, Ying; Salesse, Charleen; Wu, Haodi (2017-07-27). "Fast two-photon imaging of subcellular voltage dynamics in neuronal tissue with genetically encoded indicators". eLife. 6. doi:10.7554/eLife.25690. ISSN 2050-084X.
  34. ↑ Yang, Helen H.; St-Pierre, François (2016-09-28). "Genetically Encoded Voltage Indicators: Opportunities and Challenges". The Journal of Neuroscience. 36 (39): 9977–9989. doi:10.1523/JNEUROSCI.1095-16.2016. ISSN 1529-2401. PMC 5039263. PMID 27683896.
  35. ↑ Kaschula, Richard; Salecker, Iris (2016-06-30). "Neuronal Computations Made Visible with Subcellular Resolution". Cell. 166 (1): 18–20. doi:10.1016/j.cell.2016.06.022. ISSN 1097-4172. PMID 27368098.
  36. ↑ Cao, Guan; Platisa, Jelena; Pieribone, Vincent A.; Raccuglia, Davide; Kunst, Michael; Nitabach, Michael N. (2013-08-15). "Genetically targeted optical electrophysiology in intact neural circuits". Cell. 154 (4): 904–913. doi:10.1016/j.cell.2013.07.027. ISSN 1097-4172. PMC 3874294. PMID 23932121.
  37. ↑ Knöpfel, Thomas; Gallero-Salas, Yasir; Song, Chenchen (2015-08-01). "Genetically encoded voltage indicators for large scale cortical imaging come of age". Current Opinion in Chemical Biology. 27: 75–83. doi:10.1016/j.cbpa.2015.06.006. ISSN 1879-0402. PMID 26115448.
  38. ↑ Kaestner, Lars; Tian, Qinghai; Kaiser, Elisabeth; Xian, Wenying; Müller, Andreas; Oberhofer, Martin; Ruppenthal, Sandra; Sinnecker, Daniel; Tsutsui, Hidekazu (2015-09-08). "Genetically Encoded Voltage Indicators in Circulation Research". International Journal of Molecular Sciences. 16 (9): 21626–21642. doi:10.3390/ijms160921626. ISSN 1422-0067. PMC 4613271. PMID 26370981.
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