Photoreceptor engineering

Frontiers in Molecular Biosciences

Volumn 2, Issue JUN, 2015, Pages

  Ziegler, Thea ^a,b   Möglich, Andreas ^a,b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Allostery; Light; Optogenetics; Protein engineering; Sensory photoreceptor; Signal transduction

Indexed keywords

EID: 85014680349     PISSN: None     EISSN: 2296889X     Source Type: Journal    
DOI: 10.3389/fmolb.2015.00030     Document Type: Review

References (167)

1. Airan, R. D., Thompson, K. R., Fenno, L. E., Bernstein, H., and Deisseroth, K. (2009). Temporally precise in vivo control of intracellular signalling. Nature 458, 1025-1029. doi: 10.1038/nature07926
2. Anantharaman, V., Balaji, S., and Aravind, L. (2006). The signaling helix: a common functional theme in diverse signaling proteins. Biol. Direct 1:25. doi: 10.1186/1745-6150-1-25
3. Aoki, K., Kumagai, Y., Sakurai, A., Komatsu, N., Fujita, Y., Shionyu, C., et al. (2013). Stochastic ERK activation induced by noise and cell-to-cell propagation regulates cell density-dependent proliferation. Mol. Cell 52, 529-540. doi: 10.1016/j.molcel.2013.09.015
4. Avelar, G. M., Schumacher, R. I., Zaini, P. A., Leonard, G., Richards, T. A., and Gomes, S. L. (2014). A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr. Biol. 24, 1234-1240. doi: 10.1016/j.cub.2014.04.009
5. Beel, B., Prager, K., Spexard, M., Sasso, S., Weiss, D., Müller, N., Heinnickel, M., et al. (2012). A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell 24, 2992-3008. doi: 10.1105/tpc.112.098947
6. Berndt, A., Yizhar, O., Gunaydin, L. A., Hegemann, P., and Deisseroth, K. (2009). Bi-stable neural state switches. Nat. Neurosci. 12, 229-234. doi: 10.1038/nn.2247
7. Beyer, H. M., Juillot, S., Herbst, K., Samodelov, S. L., Müller, K., Schamel, W. W., et al. (2015a). Red light-regulated reversible nuclear localization of proteins in mammalian cells and zebrafish. ACS Synth. Biol. doi: 10.1021/acssynbio.5b00004
8. Beyer, H. M., Naumann, S., Weber, W., and Radziwill, G. (2015b). Optogenetic control of signaling in mammalian cells. Biotechnol. J. 10, 273-283. doi: 10.1002/biot.201400077
9. Blackshaw, S., and Snyder, S. H. (1997). Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family. J. Neurosci. 17, 8083-8092
10. Bonger, K. M., Rakhit, R., Payumo, A. Y., Chen, J. K., and Wandless, T. J. (2014). General method for regulating protein stability with light. ACS Chem. Biol. 9, 111-115. doi: 10.1021/cb400755b
11. Brown, B. A., Cloix, C., Jiang, G. H., Kaiserli, E., Herzyk, P., Kliebenstein, D. J., et al. (2005). A UV-B-specific signaling component orchestrates plant UV protection. Proc. Natl. Acad. Sci. U.S.A. 102, 18225-18230. doi: 10.1073/pnas.0507187102
12. 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. doi: 10.1038/nmeth.2360
13. Burgie, E. S., Bussell, A. N., Walker, J. M., Dubiel, K., and Vierstra, R. D. (2014). Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome. Proc. Natl. Acad. Sci. U.S.A. 111, 10179-10184. doi: 10.1073/pnas.1403096111
14. Burgie, E. S., and Vierstra, R. D. (2014). Phytochromes: an atomic perspective on photoactivation and signaling. Plant Cell 26, 4568-4583. doi: 10.1105/tpc.114.131623
15. Burgie, E. S., Walker, J. M., Phillips, G. N. Jr., and Vierstra, R. D. (2013). A photo-labile thioether linkage to phycoviolobilin provides the foundation for the blue/green photocycles in DXCF-cyanobacteriochromes. Structure 21, 88-97. doi: 10.1016/j.str.2012.11.001
16. Chang, K.-Y., Woo, D., Jung, H., Lee, S., Kim, S., Won, J., et al. (2014). Light-inducible receptor tyrosine kinases that regulate neurotrophin signalling. Nat. Commun. 5, 4057. doi: 10.1038/ncomms5057
17. Chapman, S., Faulkner, C., Kaiserli, E., Garcia-Mata, C., Savenkov, E. I., Roberts, A. G., et al. (2008). The photoreversible fluorescent protein iLOV outperforms GFP as a reporter of plant virus infection. Proc. Natl. Acad. Sci. U.S.A. 105, 20038-20043. doi: 10.1073/pnas.0807551105
18. Chen, D., Gibson, E. S., and Kennedy, M. J. (2013). A light-triggered protein secretion system. J. Cell Biol. 201, 631-640. doi: 10.1083/jcb.201210119
19. Christie, J. M., Arvai, A. S., Baxter, K. J., Heilmann, M., Pratt, A. J., O'Hara, A., et al. (2012). Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335, 1492-1496. doi: 10.1126/science.1218091
20. Christie, J. M., Corchnoy, S. B., Swartz, T. E., Hokenson, M., Han, I.-S., Briggs, W. R., et al. (2007). Steric interactions stabilize the signaling state of the LOV2 domain of phototropin 1. Biochemistry 46, 9310-9319. doi: 10.1021/bi700852w
21. Chung, K., Wallace, J., Kim, S.-Y., Kalyanasundaram, S., Andalman, A. S., Davidson, T. J., et al. (2013). Structural and molecular interrogation of intact biological systems. Nature 497, 332-337. doi: 10.1038/nature12107
22. Conrad, K. S., Bilwes, A. M., and Crane, B. R. (2013). Light-induced subunit dissociation by a light-oxygen-voltage domain photoreceptor from Rhodobacter sphaeroides. Biochemistry 52, 378-391. doi: 10.1021/bi3015373
23. Conrad, K. S., Manahan, C. C., and Crane, B. R. (2014). Photochemistry of flavoprotein light sensors. Nat. Chem. Biol. 10, 801-809. doi: 10.1038/nchembio.1633
24. 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. doi: 10.1038/ncomms2800
25. Deisseroth, K., Feng, G., Majewska, A. K., Miesenböck, G., Ting, A., and Schnitzer, M. J. (2006). Next-generation optical technologies for illuminating genetically targeted brain circuits. J. Neurosci. 26, 10380-10386. doi: 10.1523/JNEUROSCI.3863-06.2006
26. Diensthuber, R. P., Bommer, M., Gleichmann, T., and Möglich, A. (2013). Full-length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators. Structure 21, 1127-1136. doi: 10.1016/j.str.2013.04.024
27. Diensthuber, R. P., Engelhard, C., Lemke, N., Gleichmann, T., Ohlendorf, R., Bittl, R., et al. (2014). Biophysical, mutational, and functional investigation of the chromophore-binding pocket of light-oxygen-voltage photoreceptors. ACS Synth. Biol. 3, 811-819. doi: 10.1021/sb400205x
28. Dixon, R. E., Yuan, C., Cheng, E. P., Navedo, M. F., and Santana, L. F. (2012). Ca2+ signaling amplification by oligomerization of L-type Cav1.2 channels. Proc. Natl. Acad. Sci. U.S.A. 109, 1749-1754. doi: 10.1073/pnas.1116731109
29. Drepper, T., Eggert, T., Circolone, F., Heck, A., Krauss, U., Guterl, J.-K., et al. (2007). Reporter proteins for in vivo fluorescence without oxygen. Nat. Biotechnol. 25, 443-445. doi: 10.1038/nbt1293
30. Ernst, O. P., Lodowski, D. T., Elstner, M., Hegemann, P., Brown, L. S., and Kandori, H. (2014). Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem. Rev. 114, 126-163. doi: 10.1021/cr4003769
31. Fan, H. Y., Morgan, S.-A., Brechun, K. E., Chen, Y.-Y., Jaikaran, A. S. I., and Woolley, G. A. (2011). Improving a designed photocontrolled DNA-binding protein. Biochemistry 50, 1226-1237. doi: 10.1021/bi101432p
32. Fan, L. Z., and Lin, M. Z. (2015). Optical control of biological processes by light-switchable proteins. Wiley Interdiscip. Rev. Dev. Biol. doi: 10.1002/wdev.188. [Epub ahead of print]
33. Feynman, R. P. (1963). The Feynman Lectures on Physics. Menlo-Park, CA: Addison-Wesley
34. Filonov, G. S., Piatkevich, K. D., Ting, L.-M., Zhang, J., Kim, K., and Verkhusha, V. V. (2011). Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat. Biotechnol. 29, 757-761. doi: 10.1038/nbt.1918
35. Freedman, M. S., Lucas, R. J., Soni, B., von Schantz, M., Muñoz, M., David-Gray, Z., et al. (1999). Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284, 502-504
36. Gasser, C., Taiber, S., Yeh, C.-M., Wittig, C. H., Hegemann, P., Ryu, S., et al. (2014). Engineering of a red-light-activated human cAMP/cGMP-specific phosphodiesterase. Proc. Natl. Acad. Sci. U.S.A. 111, 8803-8808. doi: 10.1073/pnas.1321600111
37. Gleichmann, T., Diensthuber, R. P., and Möglich, A. (2013). Charting the signal trajectory in a light-oxygen-voltage photoreceptor by random mutagenesis and covariance analysis. J. Biol. Chem. 288, 29345-29355. doi: 10.1074/jbc. M113.506139
38. Grusch, M., Schelch, K., Riedler, R., Reichhart, E., Differ, C., Berger, W., et al. (2014). Spatio-temporally precise activation of engineered receptor tyrosine kinases by light. EMBO J. 33, 1713-1726. doi: 10.15252/embj.201387695
39. Guntas, G., Hallett, R. A., Zimmerman, S. P., Williams, T., Yumerefendi, H., Bear, J. E., et al. (2015). Engineering an improved light-induced dimer (iLID) for controlling the localization and activity of signaling proteins. Proc. Natl. Acad. Sci. U.S.A. 112, 112-117. doi: 10.1073/pnas.1417910112
40. Halavaty, A. S., and Moffat, K. (2007). N-and C-terminal flanking regions modulate light-induced signal transduction in the LOV2 domain of the blue light sensor phototropin 1 from Avena sativa. Biochemistry 46, 14001-14009. doi: 10.1021/bi701543e
41. Harper, S. M., Neil, L. C., and Gardner, K. H. (2003). Structural basis of a phototropin light switch. Science 301, 1541-1544. doi: 10.1126/science.1086810
42. Hegemann, P. (2008). Algal sensory photoreceptors. Annu. Rev. Plant Biol. 59, 167-189. doi: 10.1146/annurev.arplant.59.032607.092847
43. Hell, S. W., and Wichmann, J. (1994). Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19, 780-782. doi: 10.1364/OL.19.000780
44. Hirose, Y., Shimada, T., Narikawa, R., Katayama, M., and Ikeuchi, M. (2008). Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein. Proc. Natl. Acad. Sci. U.S.A. 105, 9528-9533. doi: 10.1073/pnas.0801826105
45. Hochbaum, D. R., Zhao, Y., Farhi, S. L., Klapoetke, N., Werley, C. A., Kapoor, V., et al. (2014). All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat. Methods 11, 825-833. doi: 10.1038/nmeth.3000
46. Hughes, J., Lamparter, T., Mittmann, F., Hartmann, E., Gärtner, W., Wilde, A., et al. (1997). A prokaryotic phytochrome. Nature 386, 663. doi: 10.1038/386663a0
47. Idevall-Hagren, O., Dickson, E. J., Hille, B., Toomre, D. K., and De Camilli, P. (2012). Optogenetic control of phosphoinositide metabolism. Proc. Natl. Acad. Sci. U.S.A. 109, E2316-E2323. doi: 10.1073/pnas.1211305109
48. Ikeuchi, M., and Ishizuka, T. (2008). Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem. Photobiol. Sci. 7, 1159-1167. doi: 10.1039/b802660m
49. Ishizuka, T., Kamiya, A., Suzuki, H., Narikawa, R., Noguchi, T., Kohchi, T., et al. (2011). The cyanobacteriochrome, TePixJ, isomerizes its own chromophore by converting phycocyanobilin to phycoviolobilin. Biochemistry 50, 953-961. doi: 10.1021/bi101626t
50. Jansen, V., Alvarez, L., Balbach, M., Strünker, T., Hegemann, P., Kaupp, U. B., et al. (2015). Controlling fertilization and cAMP signaling in sperm by optogenetics. Elife 4:e05161. doi: 10.7554/eLife.05161
51. Kakumoto, T., and Nakata, T. (2013). Optogenetic control of PIP3: PIP3 is sufficient to induce the actin-based active part of growth cones and is regulated via endocytosis. PLoS ONE 8:e70861. doi: 10.1371/journal.pone.0070861
52. Karunarathne, W. K. A., Giri, L., Kalyanaraman, V., and Gautam, N. (2013). Optically triggering spatiotemporally confined GPCR activity in a cell and programming neurite initiation and extension. Proc. Natl. Acad. Sci. U.S.A. 110, E1565-E1574. doi: 10.1073/pnas.1220697110
53. Kawano, F., Suzuki, H., Furuya, A., and Sato, M. (2015). Engineered pairs of distinct photoswitches for optogenetic control of cellular proteins. Nat. Commun. 6:6256. doi: 10.1038/ncomms7256
54. 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. Methods 7, 973-975. doi: 10.1038/nmeth.1524
55. Kim, J.-M., Hwa, J., Garriga, P., Reeves, P. J., RajBhandary, U. L., and Khorana, H. G. (2005). Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops. Biochemistry 44, 2284-2292. doi: 10.1021/bi048328i
56. 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. doi: 10.1016/j.chembiol.2014.05.013
57. Klapoetke, N. C., Murata, Y., Kim, S. S., Pulver, S. R., Birdsey-Benson, A., Cho, Y. K., et al. (2014). Independent optical excitation of distinct neural populations. Nat. Methods 11, 338-346. doi: 10.1038/nmeth.2836
58. Klemm, J. D., Schreiber, S. L., and Crabtree, G. R. (1998). Dimerization as a regulatory mechanism in signal transduction. Annu. Rev. Immunol. 16, 569-592. doi: 10.1146/annurev.immunol.16.1.569
59. Konermann, S., Brigham, M. D., Trevino, A. E., Hsu, P. D., Heidenreich, M., Cong, L., et al. (2013). Optical control of mammalian endogenous transcription and epigenetic states. Nature 500, 472-476. doi: 10.1038/nature12466
60. Koyanagi, M., Kawano, E., Kinugawa, Y., Oishi, T., Shichida, Y., Tamotsu, S., et al. (2004). Bistable UV pigment in the lamprey pineal. Proc. Natl. Acad. Sci. U.S.A. 101, 6687-6691. doi: 10.1073/pnas.0400819101
61. 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
62. Kralj, J. M., Hochbaum, D. R., Douglass, A. D., and Cohen, A. E. (2011). Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333, 345-348. doi: 10.1126/science.1204763
63. Lamb, J. S., Zoltowski, B. D., Pabit, S. A., Crane, B. R., and Pollack, L. (2008). Time-resolved dimerization of a PAS-LOV protein measured with photocoupled small angle X-ray scattering. J. Am. Chem. Soc. 130, 12226-12227. doi: 10.1021/ja804236f
64. Lee, J., Natarajan, M., Nashine, V. C., Socolich, M., Vo, T., Russ, W. P., et al. (2008). Surface sites for engineering allosteric control in proteins. Science 322, 438-442. doi: 10.1126/science.1159052
65. Lee, S., Park, H., Kyung, T., Kim, N. Y., Kim, S., Kim, J., et al. (2014). Reversible protein inactivation by optogenetic trapping in cells. Nat. Methods 11, 633-636. doi: 10.1038/nmeth.2940
66. Leibiger, I. B., and Berggren, P.-O. (2015). Regulation of glucose homeostasis using radiogenetics and magnetogenetics in mice. Nat. Med. 21, 14-16. doi: 10.1038/nm.3782
67. Levskaya, A., Chevalier, A. A., Tabor, J. J., Simpson, Z. B., Lavery, L. A., Levy, M., et al. (2005). Synthetic biology: engineering Escherichia coli to see light. Nature 438, 441-442. doi: 10.1038/nature04405
68. 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. doi: 10.1038/nature08446
69. Liu, H., Gomez, G., Lin, S., Lin, S., and Lin, C. (2012). Optogenetic control of transcription in zebrafish. PLoS ONE 7:e50738. doi: 10.1371/journal.pone.0050738
70. Liu, H., Yu, X., Li, K., Klejnot, J., Yang, H., Lisiero, D., et al. (2008). Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322, 1535-1539. doi: 10.1126/science.1163927
71. Losi, A., Gärtner, W., Raffelberg, S., Cella Zanacchi, F., Bianchini, P., Diaspro, A., et al. (2013). A photochromic bacterial photoreceptor with potential for super-resolution microscopy. Photochem. Photobiol. Sci. 12, 231-235. doi: 10.1039/C2PP25254F
72. Luck, M., Mathes, T., Bruun, S., Fudim, R., Hagedorn, R., Tran Nguyen, T. M., et al. (2012). A photochromic histidine kinase rhodopsin (HKR1) that is bimodally switched by ultraviolet and blue light. J. Biol. Chem. 287, 40083-40090. doi: 10.1074/jbc. M112.401604
73. Lungu, O. I., Hallett, R. A., Choi, E. J., Aiken, M. J., Hahn, K. M., and Kuhlman, B. (2012). Designing photoswitchable peptides using the AsLOV2 domain. Chem. Biol. 19, 507-517. doi: 10.1016/j.chembiol.2012.02.006
74. Makhlynets, O. V., Raymond, E. A., and Korendovych, I. V. (2015). Design of allosterically regulated protein catalysts. Biochemistry 54, 1444-1456. doi: 10.1021/bi5015248
75. Mills, E., Chen, X., Pham, E., Wong, S., and Truong, K. (2012). Engineering a photoactivated caspase-7 for rapid induction of apoptosis. ACS Synth. Biol. 1, 75-82. doi: 10.1021/sb200008j
76. Moffat, K., Zhang, F., Hahn, K. M., and Möglich, A. (2013). "The biophysics and engineering of signaling photoreceptors". in Optogenetics, eds P. Hegemann and S. Sigrist (Berlin: Walter de Gruyter), 7-22
77. Möglich, A., Ayers, R. A., and Moffat, K. (2009a). Design and signaling mechanism of light-regulated histidine kinases. J. Mol. Biol. 385, 1433-1444. doi: 10.1016/j.jmb.2008.12.017
78. Möglich, A., Ayers, R. A., and Moffat, K. (2009b). Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17, 1282-1294. doi: 10.1016/j.str.2009.08.011
79. Möglich, A., Ayers, R. A., and Moffat, K. (2010a). Addition at the molecular level: signal integration in designed Per-ARNT-Sim receptor proteins. J. Mol. Biol. 400, 477-486. doi: 10.1016/j.jmb.2010.05.019
80. Möglich, A., and Moffat, K. (2010). Engineered photoreceptors as novel optogenetic tools. Photochem. Photobiol. Sci. 9, 1286-1300. doi: 10.1039/c0pp00167h
81. Möglich, A., Yang, X., Ayers, R. A., and Moffat, K. (2010b). Structure and function of plant photoreceptors. Annu. Rev. Plant Biol. 61, 21-47. doi: 10.1146/annurev-arplant-042809-112259
82. Monod, J., Wyman, J., and Changeux, J. P. (1965). On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118. doi: 10.1016/S0022-2836(65)80285-6
83. Motlagh, H. N., Wrabl, J. O., Li, J., and Hilser, V. J. (2014). The ensemble nature of allostery. Nature 508, 331-339. doi: 10.1038/nature13001
84. Motta-Mena, L. B., Reade, A., Mallory, M. J., Glantz, S., Weiner, O. D., Lynch, K. W., et al. (2014). An optogenetic gene expression system with rapid activation and deactivation kinetics. Nat. Chem. Biol. 10, 196-202. doi: 10.1038/nchembio.1430
85. Müller, K., Engesser, R., Metzger, S., Schulz, S., Kämpf, M. M., Busacker, M., et al. (2013a). A red/far-red light-responsive bi-stable toggle switch to control gene expression in mammalian cells. Nucleic Acids Res. 41, e77. doi: 10.1093/nar/gkt002
86. Müller, K., Engesser, R., Schulz, S., Steinberg, T., Tomakidi, P., Weber, C. C., et al. (2013b). Multi-chromatic control of mammalian gene expression and signaling. Nucleic Acids Res. 41, e124. doi: 10.1093/nar/gkt340
87. Müller, K., Engesser, R., Timmer, J., Nagy, F., Zurbriggen, M. D., and Weber, W. (2013c). Synthesis of phycocyanobilin in mammalian cells. Chem. Commun. (Camb.) 49, 8970-8972. doi: 10.1039/c3cc45065a
88. Nagel, G., Ollig, D., Fuhrmann, M., Kateriya, S., Musti, A. M., Bamberg, E., et al. (2002). Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296, 2395-2398. doi: 10.1126/science.1072068
89. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., et al. (2003). Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. U.S.A. 100, 13940-13945. doi: 10.1073/pnas.1936192100
90. Narikawa, R., Enomoto, G., Ni-Ni-Win Fushimi, K., and Ikeuchi, M. (2014). A new type of dual-Cys cyanobacteriochrome GAF domain found in cyanobacterium Acaryochloris marina, which has an unusual red/blue reversible photoconversion cycle. Biochemistry 53, 5051-5059. doi: 10.1021/bi500376b
91. Narikawa, R., Ishizuka, T., Muraki, N., Shiba, T., Kurisu, G., and Ikeuchi, M. (2013). Structures of cyanobacteriochromes from phototaxis regulators AnPixJ and TePixJ reveal general and specific photoconversion mechanism. Proc. Natl. Acad. Sci. U.S.A. 110, 918-923. doi: 10.1073/pnas.1212098110
92. Narikawa, R., Nakajima, T., Aono, Y., Fushimi, K., Enomoto, G., Ni-Ni-Win, et al. (2015). A biliverdin-binding cyanobacteriochrome from the chlorophyll d-bearing cyanobacterium Acaryochloris marina. Sci. Rep. 5:7950. doi: 10.1038/srep07950
93. Nash, A. I., McNulty, R., Shillito, M. E., Swartz, T. E., Bogomolni, R. A., Luecke, H., et al. (2011). Structural basis of photosensitivity in a bacterial light-oxygen-voltage/helix-turn-helix (LOV-HTH) DNA-binding protein. Proc. Natl. Acad. Sci. U.S.A. 108, 9449-9454. doi: 10.1073/pnas.1100262108
94. Nihongaki, Y., Suzuki, H., Kawano, F., and Sato, M. (2014). Genetically engineered photoinducible homodimerization system with improved dimer-forming efficiency. ACS Chem. Biol. 9, 617-621. doi: 10.1021/cb400836k
95. Nihongaki, Y., Yamamoto, S., Kawano, F., Suzuki, H., and Sato, M. (2015). CRISPR-Cas9-based photoactivatable transcription system. Chem. Biol. 22, 169-174. doi: 10.1016/j.chembiol.2014.12.011
96. Niopek, D., Benzinger, D., Roensch, J., Draebing, T., Wehler, P., Eils, R., et al. (2014). Engineering light-inducible nuclear localization signals for precise spatiotemporal control of protein dynamics in living cells. Nat. Commun. 5, 4404. doi: 10.1038/ncomms5404
97. Oh, E., Maejima, T., Liu, C., Deneris, E., and Herlitze, S. (2010). Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor. J. Biol. Chem. 285, 30825-30836. doi: 10.1074/jbc. M110.147298
98. Ohlendorf, R., Vidavski, R. R., Eldar, A., Moffat, K., and Möglich, A. (2012). From dusk till dawn: one-plasmid systems for light-regulated gene expression. J. Mol. Biol. 416, 534-542. doi: 10.1016/j.jmb.2012.01.001
99. Pashaie, R., Anikeeva, P., Lee, J. H., Prakash, R., Yizhar, O., Prigge, M., et al. (2014). Optogenetic brain interfaces. IEEE Rev. Biomed. Eng. 7, 3-30. doi: 10.1109/RBME.2013.2294796
100. Pathak, G. P., Strickland, D., Vrana, J. D., and Tucker, C. L. (2014). Benchmarking of optical dimerizer systems. ACS Synth. Biol. 3, 832-838. doi: 10.1021/sb500291r
101. Patterson, G. H., and Lippincott-Schwartz, J. (2002). A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297, 1873-1877. doi: 10.1126/science.1074952
102. Paz, J. T., Davidson, T. J., Frechette, E. S., Delord, B., Parada, I., Peng, K., et al. (2013). Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat. Neurosci. 16, 64-70. doi: 10.1038/nn.3269
103. Pham, E., Mills, E., and Truong, K. (2011). A synthetic photoactivated protein to generate local or global Ca(2+) signals. Chem. Biol. 18, 880-890. doi: 10.1016/j.chembiol.2011.04.014
104. Piatkevich, K. D., Subach, F. V., and Verkhusha, V. V. (2013a). Engineering of bacterial phytochromes for near-infrared imaging, sensing, and light-control in mammals. Chem. Soc. Rev. 42, 3441-3452. doi: 10.1039/c3cs35458j
105. Piatkevich, K. D., Subach, F. V., and Verkhusha, V. V. (2013b). Far-red light photoactivatable near-infrared fluorescent proteins engineered from a bacterial phytochrome. Nat. Commun. 4, 2153. doi: 10.1038/ncomms3153
106. Pollock, R., and Clackson, T. (2002). Dimerizer-regulated gene expression. Curr. Opin. Biotechnol. 13, 459-467. doi: 10.1016/S0958-1669(02)00373-7
107. Polstein, L. R., and Gersbach, C. A. (2012). Light-inducible spatiotemporal control of gene activation by customizable zinc finger transcription factors. J. Am. Chem. Soc. 134, 16480-16483. doi: 10.1021/ja3065667
108. Polstein, L. R., and Gersbach, C. A. (2015). A light-inducible CRISPR-Cas9 system for control of endogenous gene activation. Nat. Chem. Biol. 11, 198-200. doi: 10.1038/nchembio.1753
109. Pudasaini, A., El-Arab, K. K., and Zoltowski, B. D. (2015). LOV-based optogenetic devices: light-driven modules to impart photoregulated control of cellular signaling. Front. Mol. Biosci 2:18. doi: 10.3389/fmolb.2015.00018
110. Qi, Y. B., Garren, E. J., Shu, X., Tsien, R. Y., and Jin, Y. (2012). Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singlet oxygen generating protein miniSOG. Proc. Natl. Acad. Sci. U.S.A. 109, 7499-7504. doi: 10.1073/pnas.1204096109
111. Raffelberg, S., Wang, L., Gao, S., Losi, A., Gärtner, W., and Nagel, G. (2013). A LOV-domain-mediated blue-light-activated adenylate (adenylyl) cyclase from the cyanobacterium Microcoleus chthonoplastes PCC 7420. Biochem. J. 455, 359-365. doi: 10.1042/BJ20130637
112. Reis, J. M., Burns, D. C., and Woolley, G. A. (2014). Optical control of protein-protein interactions via blue light-induced domain swapping. Biochemistry 53, 5008-5016. doi: 10.1021/bi500622x
113. Renicke, C., Schuster, D., Usherenko, S., Essen, L.-O., and Taxis, C. (2013). A LOV2 domain-based optogenetic tool to control protein degradation and cellular function. Chem. Biol. 20, 619-626. doi: 10.1016/j.chembiol.2013.03.005
114. Richter, F., Scheib, U. S., Mehlhorn, J., Schubert, R., Wietek, J., Gernetzki, O., et al. (2015). Upgrading a microplate reader for photobiology and all-optical experiments. Photochem. Photobiol. Sci. 14, 270-279. doi: 10.1039/C4PP00361F
115. Rockwell, N. C., Duanmu, D., Martin, S. S., Bachy, C., Price, D. C., Bhattacharya, D., et al. (2014). Eukaryotic algal phytochromes span the visible spectrum. Proc. Natl. Acad. Sci. U.S.A. 111, 3871-3876. doi: 10.1073/pnas.1401871111
116. Rockwell, N. C., and Lagarias, J. C. (2010). A brief history of phytochromes. Chemphyschem 11, 1172-1180. doi: 10.1002/cphc.200900894
117. Rockwell, N. C., Martin, S. S., Feoktistova, K., and Lagarias, J. C. (2011). Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes. Proc. Natl. Acad. Sci. U.S.A. 108, 11854-11859. doi: 10.1073/pnas.1107844108
118. Rockwell, N. C., Ohlendorf, R., and Möglich, A. (2013). Cyanobacteriochromes in full color and three dimensions. Proc. Natl. Acad. Sci. U.S.A. 110, 806-807. doi: 10.1073/pnas.1220690110
119. Rockwell, N. C., Su, Y.-S., and Lagarias, J. C. (2006). Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57, 837-858. doi: 10.1146/annurev.arplant.56.032604.144208
120. Ryu, M.-H., Kang, I.-H., Nelson, M. D., Jensen, T. M., Lyuksyutova, A. I., Siltberg-Liberles, J., et al. (2014). Engineering adenylate cyclases regulated by near-infrared window light. Proc. Natl. Acad. Sci. U.S.A. 111, 10167-10172. doi: 10.1073/pnas.1324301111
121. Ryu, M.-H., Moskvin, O. V., Siltberg-Liberles, J., and Gomelsky, M. (2010). Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J. Biol. Chem. 285, 41501-41508. doi: 10.1074/jbc. M110.177600
122. Schmidt, D., and Cho, Y. K. (2015). Natural photoreceptors and their application to synthetic biology. Trends Biotechnol. 33, 80-91. doi: 10.1016/j.tibtech.2014.10.007
123. Schmidt, D., Tillberg, P. W., Chen, F., and Boyden, E. S. (2014). A fully genetically encoded protein architecture for optical control of peptide ligand concentration. Nat. Commun. 5, 3019. doi: 10.1038/ncomms4019
124. Schröder-Lang, S., Schwärzel, M., Seifert, R., Strünker, T., Kateriya, S., Looser, J., et al. (2007). Fast manipulation of cellular cAMP level by light in vivo. Nat. Methods 4, 39-42. doi: 10.1038/nmeth975
125. Shcherbakova, D. M., Shemetov, A. A., Kaberniuk, A. A., and Verkhusha, V. V. (2015). Natural photoreceptors as a source of fluorescent proteins, biosensors, and optogenetic tools. Annu. Rev. Biochem. 5, 519-550. doi: 10.1146/annurev-biochem-060614-034411
126. Shimizu-Sato, S., Huq, E., Tepperman, J. M., and Quail, P. H. (2002). A light-switchable gene promoter system. Nat. Biotechnol. 20, 1041-1044. doi: 10.1038/nbt734
127. Shu, X., Royant, A., Lin, M. Z., Aguilera, T. A., Lev-Ram, V., Steinbach, P. A., et al. (2009). Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 324, 804-807. doi: 10.1126/science.1168683
128. Spoida, K., Masseck, O. A., Deneris, E. S., and Herlitze, S. (2014). Gq/5-HT2c receptor signals activate a local GABAergic inhibitory feedback circuit to modulate serotonergic firing and anxiety in mice. Proc. Natl. Acad. Sci. U.S.A. 111, 6479-6484. doi: 10.1073/pnas.1321576111
129. Stanley, S. A., Gagner, J. E., Damanpour, S., Yoshida, M., Dordick, J. S., and Friedman, J. M. (2012). Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice. Science 336, 604-608. doi: 10.1126/science.1216753
130. Stanley, S. A., Sauer, J., Kane, R. S., Dordick, J. S., and Friedman, J. M. (2015). Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat. Med. 21, 92-98. doi: 10.1038/nm.3730
131. Stein, V., and Alexandrov, K. (2015). Synthetic protein switches: design principles and applications. Trends Biotechnol. 33, 101-110. doi: 10.1016/j.tibtech.2014.11.010
132. Stierl, M., Stumpf, P., Udwari, D., Gueta, R., Hagedorn, R., Losi, A., et al. (2011). Light-modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium beggiatoa. J. Biol. Chem. 286, 1181-1188. doi: 10.1074/jbc. M110.185496
133. Strauss, H. M., Schmieder, P., and Hughes, J. (2005). Light-dependent dimerisation in the N-terminal sensory module of cyanobacterial phytochrome 1. FEBS Lett. 579, 3970-3974. doi: 10.1016/j.febslet.2005.06.025
134. Strickland, D., Lin, Y., Wagner, E., Hope, C. M., Zayner, J., Antoniou, C., et al. (2012). TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nat. Methods 9, 379-384. doi: 10.1038/nmeth.1904
135. Strickland, D., Moffat, K., and Sosnick, T. R. (2008). Light-activated DNA binding in a designed allosteric protein. Proc. Natl. Acad. Sci. U.S.A. 105, 10709-10714. doi: 10.1073/pnas.0709610105
136. 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. doi: 10.1038/nmeth.1473
137. Takahashi, F., Yamagata, D., Ishikawa, M., Fukamatsu, Y., Ogura, Y., Kasahara, M., et al. (2007). AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc. Natl. Acad. Sci. U.S.A. 104, 19625-19630. doi: 10.1073/pnas.0707692104
138. Takala, H., Björling, A., Berntsson, O., Lehtivuori, H., Niebling, S., Hoernke, M., et al. (2014). Signal amplification and transduction in phytochrome photosensors. Nature 509, 245-248. doi: 10.1038/nature13310
139. Taslimi, A., Vrana, J. D., Chen, D., Borinskaya, S., Mayer, B. J., Kennedy, M. J., et al. (2014). An optimized optogenetic clustering tool for probing protein interaction and function. Nat. Commun. 5, 4925. doi: 10.1038/ncomms5925
140. Terakita, A., and Nagata, T. (2014). Functional properties of opsins and their contribution to light-sensing physiology. Zool. Sci. 31, 653-659. doi: 10.2108/zs140094
141. Toettcher, J. E., Weiner, O. D., and Lim, W. A. (2013). Using optogenetics to interrogate the dynamic control of signal transmission by the Ras/Erk module. Cell 155, 1422-1434. doi: 10.1016/j.cell.2013.11.004
142. Tsien, R. Y. (2009). Constructing and exploiting the fluorescent protein paintbox (Nobel Lecture). Angew. Chem. Int. Ed. Engl. 48, 5612-5626. doi: 10.1002/anie.200901916
143. Tyszkiewicz, A. B., and Muir, T. W. (2008). Activation of protein splicing with light in yeast. Nat. Methods 5, 303-305. doi: 10.1038/nmeth.1189
144. Vaidya, A. T., Chen, C.-H., Dunlap, J. C., Loros, J. J., and Crane, B. R. (2011). Structure of a light-activated LOV protein dimer that regulates transcription. Sci. Signal. 4, ra50. doi: 10.1126/scisignal.2001945
145. Van Bergeijk, P., Adrian, M., Hoogenraad, C. C., and Kapitein, L. C. (2015). Optogenetic control of organelle transport and positioning. Nature 518, 111-114. doi: 10.1038/nature14128
146. Van Wyk, M., Pielecka-Fortuna, J., Löwel, S., and Kleinlogel, S. (2015). Restoring the ON switch in blind retinas: opto-mGluR6, a next-generation, cell-tailored optogenetic tool. PLoS Biol. 13:e1002143. doi: 10.1371/journal.pbio.1002143
147. Volkman, B. F., Lipson, D., Wemmer, D. E., and Kern, D. (2001). Two-state allosteric behavior in a single-domain signaling protein. Science 291, 2429-2433. doi: 10.1126/science.291.5512.2429
148. Wang, X., Chen, X., and Yang, Y. (2012). Spatiotemporal control of gene expression by a light-switchable transgene system. Nat. Methods 9, 266-269. doi: 10.1038/nmeth.1892
149. Wend, S., Wagner, H. J., Müller, K., Zurbriggen, M. D., Weber, W., and Radziwill, G. (2014). Optogenetic control of protein kinase activity in mammalian cells. ACS Synth. Biol. 3, 280-285. doi: 10.1021/sb400090s
150. Wolgemuth, C. W., and Sun, S. X. (2006). Elasticity of alpha-helical coiled coils. Phys. Rev. Lett. 97, 248101. doi: 10.1103/PhysRevLett.97.248101
151. Wu, D., Hu, Q., Yan, Z., Chen, W., Yan, C., Huang, X., et al. (2012). Structural basis of ultraviolet-B perception by UVR8. Nature 484, 214-219. doi: 10.1038/nature10931
152. Wu, Y. I., Frey, D., Lungu, O. I., Jaehrig, A., Schlichting, I., Kuhlman, B., et al. (2009). A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461, 104-108. doi: 10.1038/nature08241
153. Wyman, J., and Gill, S. J. (1990). Binding and Linkage: Functional Chemistry of Biological Macromolecules. Mill Valley, CA: University Science Books
154. Yang, X., Jost, A. P.-T., Weiner, O. D., and Tang, C. (2013). A light-inducible organelle-targeting system for dynamically activating and inactivating signaling in budding yeast. Mol. Biol. Cell 24, 2419-2430. doi: 10.1091/mbc. E13-03-0126
155. Yang, X., Stojkovic, E. A., Kuk, J., and Moffat, K. (2007). Crystal structure of the chromophore binding domain of an unusual bacteriophytochrome, RpBphP3, reveals residues that modulate photoconversion. Proc. Natl. Acad. Sci. U.S.A. 104, 12571-12576. doi: 10.1073/pnas.0701737104
156. Yao, X., Rosen, M. K., and Gardner, K. H. (2008). Estimation of the available free energy in a LOV2-J alpha photoswitch. Nat. Chem. Biol. 4, 491-497. doi: 10.1038/nchembio.99
157. Yazawa, M., Sadaghiani, A. M., Hsueh, B., and Dolmetsch, R. E. (2009). Induction of protein-protein interactions in live cells using light. Nat. Biotechnol. 27, 941-945. doi: 10.1038/nbt.1569
158. Yi, J. J., Wang, H., Vilela, M., Danuser, G., and Hahn, K. M. (2014). Manipulation of endogenous kinase activity in living cells using photoswitchable inhibitory peptides. ACS Synth. Biol. 3, 788-795. doi: 10.1021/sb5001356
159. Yu, X., Sayegh, R., Maymon, M., Warpeha, K., Klejnot, J., Yang, H., et al. (2009). Formation of nuclear bodies of Arabidopsis CRY2 in response to blue light is associated with its blue light-dependent degradation. Plant Cell 21, 118-130. doi: 10.1105/tpc.108.061663
160. Zalocusky, K. A., Fenno, L. E., and Deisseroth, K. (2013). "Current challenges in optogenetics". in Optogenetics, eds P. Hegemann and S. Sigrist (Berlin: Walter de Gruyter), 23-33
161. Zayner, J. P., Antoniou, C., and Sosnick, T. R. (2012). The amino-terminal helix modulates light-activated conformational changes in AsLOV2. J. Mol. Biol. 419, 61-74. doi: 10.1016/j.jmb.2012.02.037
162. Zhang, K., and Cui, B. (2015). Optogenetic control of intracellular signaling pathways. Trends Biotechnol. 33, 92-100. doi: 10.1016/j.tibtech.2014.11.007
163. Zhang, K., Duan, L., Ong, Q., Lin, Z., Varman, P. M., Sung, K., et al. (2014). Light-mediated kinetic control reveals the temporal effect of the Raf/MEK/ERK pathway in PC12 cell neurite outgrowth. PLoS ONE 9:e92917. doi: 10.1371/journal.pone.0092917
164. 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. doi: 10.1126/science.1226854
165. Zoltowski, B. D., and Crane, B. R. (2008). Light activation of the LOV protein vivid generates a rapidly exchanging dimer. Biochemistry 47, 7012-7019. doi: 10.1021/bi8007017
166. Zoltowski, B. D., Schwerdtfeger, C., Widom, J., Loros, J. J., Bilwes, A. M., Dunlap, J. C., et al. (2007). Conformational switching in the fungal light sensor vivid. Science 316, 1054-1057. doi: 10.1126/science.1137128
167. Zoltowski, B. D., Vaccaro, B., and Crane, B. R. (2009). Mechanism-based tuning of a LOV domain photoreceptor. Nat. Chem. Biol. 5, 827-834. doi: 10.1038/nchembio.210