Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Synergistic Ensemble of Optogenetic Actuators and Dynamic Indicators in Cell Biology

  • Kim, Jihoon (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Heo, Won Do (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST))
  • Received : 2018.07.10
  • Accepted : 2018.08.07
  • Published : 2018.09.30
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Abstract

Discovery of the naturally evolved fluorescent proteins and their genetically engineered biosensors have enormously contributed to current bio-imaging techniques. These reporters to trace dynamic changes of intracellular protein activities have continuously transformed according to the various demands in biological studies. Along with that, light-inducible optogenetic technologies have offered scientists to perturb, control and analyze the function of intracellular machineries in spatiotemporal manner. In this review, we present an overview of the molecular strategies that have been exploited for producing genetically encoded protein reporters and various optogenetic modules. Finally, in particular, we discuss the current efforts for combined use of these reporters and optogenetic modules as a powerful tactic for the control and imaging of signaling events in cells and tissues.

Keywords

References

  1. Ai, H.W., Henderson, J.N., Remington, S.J., and Campbell, R.E. (2006). Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochem. J. 400, 531-540. https://doi.org/10.1042/BJ20060874
  2. Alford, S.C., Abdelfattah, A.S., Ding, Y., and Campbell, R.E. (2012a). A fluorogenic red fluorescent protein heterodimer. Chem. Biol. 19, 353-360. https://doi.org/10.1016/j.chembiol.2012.01.006
  3. Alford, S.C., Ding, Y., Simmen, T., and Campbell, R.E. (2012b). Dimerization-dependent green and yellow fluorescent proteins. ACS Synthetic Biol. 1, 569-575. https://doi.org/10.1021/sb300050j
  4. Alford, S.C., Wu, J., Zhao, Y., Campbell R.E., and Knopfel, T. (2012). Optogenetic reporters. Biol. Cell 105, 14-29.
  5. Aoki, K., Nakamura, T., and Matsuda, M. (2004). Spatio-temporal regulation of Rac1 and Cdc42 activity during nerve growth factorinduced neurite outgrowth in PC12 cells. J. Biol. Chem. 279, 713-719. https://doi.org/10.1074/jbc.M306382200
  6. Baird, G.S., Zacharias, D.A., and Tsien, R.Y. (1999). Circular permutation and receptor insertion within green fluorescent proteins. Proc. Natl. Acad. Sci. USA 96, 11241-11246. https://doi.org/10.1073/pnas.96.20.11241
  7. Banaszynski, L.A., Sellmyer, M.A., Contag, C.H., Wandless, T.J., and Thorne, S.H. (2008). Chemical control of protein stability and function in living mice. Nat. Med. 14, 1123-1127. https://doi.org/10.1038/nm.1754
  8. Berndt, A., Schoenenberger, P., Mattis, J., Tye, K.M., Deisseroth, K., Hegemann, P., and Oertner, T.G. (2011). High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels. Proc. Natl. Acad. Sci. USA 108, 7595-7600. https://doi.org/10.1073/pnas.1017210108
  9. Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G., and Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268. https://doi.org/10.1038/nn1525
  10. Bugaj, L.J., Choksi, A.T., Mesuda, C.K., Kane, R.S., and Schaffer, D.V. (2013). Optogenetic protein clustering and signaling activation in mammalian cells. Nat. Methods 10, 249-252. https://doi.org/10.1038/nmeth.2360
  11. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y. (2002). A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 7877. https://doi.org/10.1073/pnas.082243699
  12. Chang, K.Y., Woo, D., Jung, H., Lee, S., Kim, S., Won, J., Kyung, T., Park, H., Kim, N., Yang, H.W., et al. (2014). Light-inducible receptor tyrosine kinases that regulate neurotrophin signalling. Nat. Commun. 5, 4057. https://doi.org/10.1038/ncomms5057
  13. 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., et al. (2010). High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98-102. https://doi.org/10.1038/nature08652
  14. Christie, J.M., Salomon, M., Nozue, K., Wada, M., and Briggs, W.R. (1999). LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): Binding sites for the chromophore flavin mononucleotide. Proc. Natl. Acad. Sci. USA 96, 8779-8783. https://doi.org/10.1073/pnas.96.15.8779
  15. Chu, J., Zhang, Z., Zheng, Y., Yang, J., Qin, L., Lu, J., Huang, Z.-L., Zeng, S., and Luo, Q. (2009). A novel far-red bimolecular fluorescence complementation system that allows for efficient visualization of protein interactions under physiological conditions. Biosens. Bioelectron. 25, 234-239. https://doi.org/10.1016/j.bios.2009.06.008
  16. Crefcoeur, R.P., Yin, R., Ulm, R., and Halazonetis, T.D. (2013). Ultraviolet-B-mediated induction of protein-protein interactions in mammalian cells. Nat. Commun. 4, 1779. https://doi.org/10.1038/ncomms2800
  17. Davidson, M.W., and Campbell, R.E. (2009). Engineered fluorescent proteins: innovations and applications. Nat. Methods 6, 713-717. https://doi.org/10.1038/nmeth1009-713
  18. Day, R.N., Booker, C.F., and Periasamy, A. (2008). Characterization of an improved donor fluorescent protein for Forster resonance energy transfer microscopy (SPIE). J. Biomed. Optics 13, 031203. https://doi.org/10.1117/1.2939094.
  19. Demeautis, C., Sipieter, F., Roul, J., Chapuis, C., Padilla-Parra, S., Riquet, F.B., and Tramier, M. (2017). Multiplexing PKA and ERK1&2 kinases FRET biosensors in living cells using single excitation wavelength dual colour FLIM. Sci. Rep. 7, 41026. https://doi.org/10.1038/srep41026
  20. Dimitrov, D., He, Y., Mutoh, H., Baker, B.J., Cohen, L., Akemann, W., and Knopfel, T. (2007). Engineering and characterization of an enhanced fluorescent protein voltage sensor. PloS One 2, e440. https://doi.org/10.1371/journal.pone.0000440
  21. Ding, Z., Liang, J., Lu, Y., Yu, Q., Songyang, Z., Lin, S.-Y., and Mills, G.B. (2006). A retrovirus-based protein complementation assay screen reveals functional AKT1-binding partners. Proc. Natl. Acad. Sci. USA 103, 15014-15019. https://doi.org/10.1073/pnas.0606917103
  22. Ding, Y., Li, J., Enterina, J.R., Shen, Y., Zhang, I., Tewson, P.H., Mo, G.C., Zhang, J., Quinn, A.M., Hughes, T.E., et al. (2015). Ratiometric biosensors based on dimerization-dependent fluorescent protein exchange. Nat. Methods 12, 195-198. https://doi.org/10.1038/nmeth.3261
  23. Doupe, D.P., and Perrimon, N. (2014). Visualizing and manipulating temporal signaling dynamics with fluorescence-based tools. Sci. Signal. 7, re1. https://doi.org/10.1126/scisignal.2005077
  24. Fan, J.Y., Cui, Z.Q., Wei, H.P., Zhang, Z.-P., Zhou, Y.F., Wang, Y.P., and Zhang, X.E. (2008). Split mCherry as a new red bimolecular fluorescence complementation system for visualizing protein-protein interactions in living cells. Biochem. Biophys. Res. Commun. 367, 47-53. https://doi.org/10.1016/j.bbrc.2007.12.101
  25. Fosbrink, M., Aye-Han, N.-N., Cheong, R., Levchenko, A., and Zhang, J. (2010). Visualization of JNK activity dynamics with a genetically encoded fluorescent biosensor. Proc. Natl. Acad. Sci. USA 107, 5459-5464. https://doi.org/10.1073/pnas.0909671107
  26. Fritz, R.D., Letzelter, M., Reimann, A., Martin, K., Fusco, L., Ritsma, L., Ponsioen, B., Fluri, E., Schulte-Merker, S., Rheenen, J.V., et al. (2013). A versatile toolkit to produce sensitive FRET biosensors to visualize signaling in time and space. Sci. Signal. 6, 2-13.
  27. Goedhart, J., van Weeren, L., Hink, M.A., Vischer, N.O.E., Jalink, K., and Gadella Jr, T.W.J. (2010). Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nat. Methods 7, 137-139. https://doi.org/10.1038/nmeth.1415
  28. Gradinaru, V., Thompson, K.R., Zhang, F., Mogri, M., Kay, K., Schneider, M.B., and Deisseroth, K. (2007). Targeting and readout strategies for fast optical neural control in vitro and in vivo. J. Neurosci. 27, 14231-14238. https://doi.org/10.1523/JNEUROSCI.3578-07.2007
  29. Grant, D.M., Zhang, W., McGhee, E.J., Bunney, T.D., Talbot, C.B., Kumar, S., Munro, I., Dunsby, C., Neil, M.A.A., Katan, M., et al. (2008). Multiplexed FRET to image multiple signaling events in live cells. Biophys. J. 95, L69-L71. https://doi.org/10.1529/biophysj.108.139204
  30. Habuchi, S., Ando, R., Dedecker, P., Verheijen, W., Mizuno, H., Miyawaki, A., and Hofkens, J. (2005). Reversible single-molecule photoswitching in the GFP-like fluorescent protein Dronpa. Proc. Natl. Acad. Sci. USA 102, 9511-9516. https://doi.org/10.1073/pnas.0500489102
  31. Han, X., and Boyden, E.S. (2007). Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PloS One 2, e299. https://doi.org/10.1371/journal.pone.0000299
  32. Harper, S.M., Neil, L.C., and Gardner, K.H. (2003). Structural basis of a phototropin light switch. Science 301, 1541. https://doi.org/10.1126/science.1086810
  33. Harvey, C.D., Ehrhardt, A.G., Cellurale, C., Zhong, H., Yasuda, R., Davis, R.J., and Svoboda, K. (2008a). A genetically encoded fluorescent sensor of ERK activity. Proc. Natl. Acad. Sci. USA 105, 19264-19269. https://doi.org/10.1073/pnas.0804598105
  34. Harvey, C.D., Yasuda, R., Zhong, H., and Svoboda, K. (2008b). The spread of Ras activity triggered by activation of a single dendritic spine. Science 321, 136-140. https://doi.org/10.1126/science.1159675
  35. Heim, R., and Tsien, R.Y. (1996). Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr. Biol. 6, 178-182. https://doi.org/10.1016/S0960-9822(02)00450-5
  36. Heim, R., Cubitt, A.B., and Tsien, R.Y. (1995). Improved green fluorescence. Nature 373, 663.
  37. Ibraheem, A., and Campbell, R.E. (2010). Designs and applications of fluorescent protein-based biosensors. Curr. Opin. Chem. Biol. 14, 30-36. https://doi.org/10.1016/j.cbpa.2009.09.033
  38. Ishizuka, T., Kakuda, M., Araki, R., and Yawo, H. (2006). Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels. Neurosci. Res. 54, 85-94. https://doi.org/10.1016/j.neures.2005.10.009
  39. Jach, G., Pesch, M., Richter, K., Frings, S., and Uhrig, J.F. (2006). An improved mRFP1 adds red to bimolecular fluorescence complementation. Nat. Methods 3, 597-600. https://doi.org/10.1038/nmeth901
  40. Kennedy, M.J., Hughes, R.M., Peteya, L.A., Schwartz, J.W., Ehlers, M.D., and Tucker, C.L. (2010). Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Method 7, 973-975. https://doi.org/10.1038/nmeth.1524
  41. Kerppola, T.K. (2008). Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Ann. Rev. Biophys. 37, 465-487. https://doi.org/10.1146/annurev.biophys.37.032807.125842
  42. Khanna, R., Huq, E., Kikis, E.A., Al-Sady, B., Lanzatella, C., and Quail, P.H. (2004). A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic Helix-Loop-Helix transcription factors. Plant Cell 16, 3033-3044. https://doi.org/10.1105/tpc.104.025643
  43. Kim, N., Kim, J.M., Lee, M., Kim, C.Y., Chang, K.Y., and Heo, W.D. (2014). Spatiotemporal control of fibroblast growth factor receptor signals by blue light. Chem. Biol. 21, 903-912. https://doi.org/10.1016/j.chembiol.2014.05.013
  44. Kiyokawa, E., Aoki, K., Nakamura, T., and Matsuda, M. (2011). Spatiotemporal regulation of small GTPases as revealed by probes based on the principle of Forster Resonance Energy Transfer (FRET): Implications for signaling and pharmacology. Annu. Rev. Pharmacol. Toxicol. 51, 337-358. https://doi.org/10.1146/annurev-pharmtox-010510-100234
  45. Kojima, T., Karasawa, S., Miyawaki, A., Tsumuraya, T., and Fujii, I. (2011). Novel screening system for protein-protein interactions by bimolecular fluorescence complementation in Saccharomyces cerevisiae. J. Biosci. Bioeng. 111, 397-401. https://doi.org/10.1016/j.jbiosc.2010.12.013
  46. Komatsu, N., Aoki, K., Yamada, M., Yukinaga, H., Fujita, Y., Kamioka, Y., and Matsuda, M. (2011). Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol. Biol. Cell 22, 4647-4656. https://doi.org/10.1091/mbc.e11-01-0072
  47. Kyung, T., Lee, S., Kim, J.E., Cho, T., Park, H., Jeong, Y.-M., Kim, D., Shin, A., Kim, S., Baek, J., et al. (2015). Optogenetic control of endogenous $Ca^{2+}$ channels in vivo. Nat.Biotechnol. 33, 1092-1096. https://doi.org/10.1038/nbt.3350
  48. 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. (2012). Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005-1012. https://doi.org/10.1038/nmeth.2171
  49. Lee, S., Park, H., Kyung, T., Kim, N.Y., Kim, S., Kim, J., and Heo, W.D. (2014). Reversible protein inactivation by optogenetic trapping in cells. Nat. Methods 11, 633-636. https://doi.org/10.1038/nmeth.2940
  50. Levskaya, A., Weiner, O.D., Lim, W.A., and Voigt, C.A. (2009). Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461, 997-1001. https://doi.org/10.1038/nature08446
  51. Li, X., Gutierrez, D.V., Hanson, M.G., Han, J., Mark, M.D., Chiel, H., Hegemann, P., Landmesser, L.T., and Herlitze, S. (2005). Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc. Natl. Acad. Sci. USA 102, 17816-17821. https://doi.org/10.1073/pnas.0509030102
  52. Miyawaki, A., Llopis, J., Heim, R., McCaffery, J.M., Adams, J.A., Ikura, M., and Tsien, R.Y. (1997). Fluorescent indicators for $Ca^{2+}$ based on green fluorescent proteins and calmodulin. Nature 388, 882-887. https://doi.org/10.1038/42264
  53. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P., and Bamberg, E. (2003). Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100, 13940-13945. https://doi.org/10.1073/pnas.1936192100
  54. Nakai, J., Ohkura, M., and Imoto, K. (2001). A high signal-to-noise $Ca^{2+}$ probe composed of a single green fluorescent protein. Nat. Biotechnol. 19, 137-141. https://doi.org/10.1038/84397
  55. Nagai, T., Sawano, A., Park, E.S., and Miyawaki, A. (2001). Circularly permuted green fluorescent proteins engineered to sense $Ca^{2+}$. Proc. Natl. Acad. Sci. USA 98, 3197-3202. https://doi.org/10.1073/pnas.051636098
  56. Nguyen, A.W., and Daugherty, P.S. (2005). Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat. Biotechnol. 23, 355-360. https://doi.org/10.1038/nbt1066
  57. Nguyen, M.K., Kim, C.Y., Kim, J.M., Park, B.O., Lee, S., Park, H., and Heo, W.D. (2016). Optogenetic oligomerization of Rab GTPases regulates intracellular membrane trafficking. Nat. Chem. Biol. 12, 431-436. https://doi.org/10.1038/nchembio.2064
  58. Nishioka, T., Frohman, M.A., Matsuda, M., and Kiyokawa, E. (2010). Heterogeneity of phosphatidic acid levels and distribution at the plasma membrane in living cells as visualized by a Foster resonance energy transfer (FRET) biosensor. J. Biol. Chem. 285, 35979-35987. https://doi.org/10.1074/jbc.M110.153007
  59. Ohkura, M., Sasaki, T., Kobayashi, C., Ikegaya, Y., and Nakai, J. (2012). An improved genetically encoded red fluorescent $Ca^{2+}$ indicator for detecting optically evoked action potentials. PloS one 7, e39933. https://doi.org/10.1371/journal.pone.0039933
  60. Ouyang, M., Sun, J., Chien, S., and Wang, Y. (2008). Determination of hierarchical relationship of Src and Rac at subcellular locations with FRET biosensors. Proc. Natl. Acad. Sci. USA 105, 14353-14358. https://doi.org/10.1073/pnas.0807537105
  61. Ouyang, M., Huang, H., Shaner, N.C., Remacle, A.G., Shiryaev, S.A., Strongin, A.Y., Tsien, R.Y., and Wang, Y. (2010). Simultaneous visualization of protumorigenic Src and MT1-MMP activities with fluorescence resonance energy transfer. Cancer Res. 70, 2204-2212. https://doi.org/10.1158/0008-5472.CAN-09-3698
  62. Park, H., Kim, N.Y., Lee, S., Kim, N., Kim, J., and Heo, W.D. (2017). Optogenetic protein clustering through fluorescent protein tagging and extension of CRY2. Nat. Commun. 8, 30. https://doi.org/10.1038/s41467-017-00060-2
  63. Pertz, O., Hodgson, L., Klemke, R.L., and Hahn, K.M. (2006). Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440, 1069-1072. https://doi.org/10.1038/nature04665
  64. Regot, S., Hughey, Jacob J., Bajar, Bryce T., Carrasco, S., and Covert, Markus W. (2014). High-sensitivity measurements of multiple kinase activities in live single cells. Cell 157, 1724-1734. https://doi.org/10.1016/j.cell.2014.04.039
  65. Santos, S.D.M., Verveer, P.J., and Bastiaens, P.I.H. (2007). Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat. Cell Biol. 9, 324-330. https://doi.org/10.1038/ncb1543
  66. Schroder-Lang, S., Schwarzel, M., Seifert, R., Strunker, T., Kateriya, S., Looser, J., Watanabe, M., Kaupp, U.B., Hegemann, P., and Nagel, G. (2006). Fast manipulation of cellular cAMP level by light in vivo. Nat. Methods 4, 39-42.
  67. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N.G., Palmer, A.E., and Tsien, R.Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572. https://doi.org/10.1038/nbt1037
  68. Shcherbakova, D.M., and Verkhusha, V.V. (2013). Near-infrared fluorescent proteins for multicolor in vivo imaging. Nat. Methods 10, 751-754. https://doi.org/10.1038/nmeth.2521
  69. Shcherbo, D., Merzlyak, E.M., Chepurnykh, T.V., Fradkov, A.F., Ermakova, G.V., Solovieva, E.A., Lukyanov, K.A., Bogdanova, E.A., Zaraisky, A.G., Lukyanov, S., et al. (2007). Bright far-red fluorescent protein for whole-body imaging. Nat. Methods 4, 741-746. https://doi.org/10.1038/nmeth1083
  70. Siegel, M.S., and Isacoff, E.Y. (1997). A genetically encoded optical probe of membrane voltage. Neuron 19, 735-741. https://doi.org/10.1016/S0896-6273(00)80955-1
  71. Shimomura, O., Johnson Frank, H., and Saiga, Y. (1962). Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, aequorea. J. Cell. Comp. Physiol. 59, 223-239. https://doi.org/10.1002/jcp.1030590302
  72. Stockwell, B.R. (2004). Exploring biology with small organic molecules. Nature 432, 846-854. https://doi.org/10.1038/nature03196
  73. Strickland, D., Yao, X., Gawlak, G., Rosen, M.K., Gardner, K.H., and Sosnick, T.R. (2010). Rationally improving LOV domain-based photoswitches. Nat. Methods 7, 623-626. https://doi.org/10.1038/nmeth.1473
  74. Taslimi, A., Vrana, J.D., Chen, D., Borinskaya, S., Mayer, B.J., Kennedy, M.J., and Tucker, C.L. (2014). An optimized optogenetic clustering tool for probing protein interaction and function. Nat. Commun. 5, 4925. https://doi.org/10.1038/ncomms5925
  75. Tomosugi, W., Matsuda, T., Tani, T., Nemoto, T., Kotera, I., Saito, K., Horikawa, K., and Nagai, T. (2009). An ultramarine fluorescent protein with increased photostability and pH insensitivity. Nat. Methods 6, 351-353. https://doi.org/10.1038/nmeth.1317
  76. Turgeon, B., and Meloche, S. (2009). Interpreting neonatal lethal phenotypes in mouse mutants: insights into gene function and human diseases. Physiol. Rev. 89, 1-26. https://doi.org/10.1152/physrev.00040.2007
  77. Vinkenborg Jan, L., Evers Toon, H., Reulen Sanne, W.A., Meijer, E.W., and Merkx, M. (2007). Enhanced sensitivity of FRET-based protease sensors by redesign of the GFP dimerization interface. ChemBioChem 8, 1119-1121. https://doi.org/10.1002/cbic.200700109
  78. Welch, C.M., Elliott, H., Danuser, G., and Hahn, K.M. (2011). Imaging the coordination of multiple signalling activities in living cells. Nat. Rev. Mol. Cell Biol. 12, 749-756. https://doi.org/10.1038/nrm3212
  79. Wu, Y.I., Frey, D., Lungu, O.I., Jaehrig, A., Schlichting, I., Kuhlman, B., and Hahn, K.M. (2009). A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461, 104-108. https://doi.org/10.1038/nature08241
  80. Yasuda, R., Harvey, C.D., Zhong, H., Sobczyk, A., van Aelst, L., and Svoboda, K. (2006). Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging. Nat. Neurosci. 9, 283-291. https://doi.org/10.1038/nn1635
  81. Zhang, K., and Cui, B. (2015). Optogenetic control of intracellular signaling pathways. Trends Biotechnol. 33, 92-100. https://doi.org/10.1016/j.tibtech.2014.11.007
  82. Zhang, F., Wang, L.-P., Boyden, E.S., and Deisseroth, K. (2006). Channelrhodopsin-2 and optical control of excitable cells. Nat. Methods 3, 785-792. https://doi.org/10.1038/nmeth936
  83. Zhang, K., Duan, L., Ong, Q., Lin, Z., Varman, P.M., Sung, K., and Cui, B. (2014). Light-mediated kinetic control reveals the temporal effect of the Raf/MEK/ERK pathway in PC12 cell neurite outgrowth. PloS one 9, e92917. https://doi.org/10.1371/journal.pone.0092917
  84. Zhao, Y., Araki, S., Wu, J., Teramoto, T., Chang, Y.F., Nakano, M., Abdelfattah, A.S., Fujiwara, M., Ishihara, T., Nagai, T., et al. (2011). An expanded palette of genetically encoded $Ca^{2+}$ indicators. Science 333, 1888-1891. https://doi.org/10.1126/science.1208592
  85. Zhou, X.X., Chung, H.K., Lam, A.J., and Lin, M.Z. (2012). Optical control of protein activity by fluorescent protein domains. Science 338, 810-814. https://doi.org/10.1126/science.1226854

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