1932

Abstract

Cells are bombarded by extrinsic signals that dynamically change in time and space. Such dynamic variations can exert profound effects on behaviors, including cellular signaling, organismal development, stem cell differentiation, normal tissue function, and disease processes such as cancer. Although classical genetic tools are well suited to introduce binary perturbations, new approaches have been necessary to investigate how dynamic signal variation may regulate cell behavior. This fundamental question is increasingly being addressed with optogenetics, a field focused on engineering and harnessing light-sensitive proteins to interface with cellular signaling pathways. Channelrhodopsins initially defined optogenetics; however, through recent use of light-responsive proteins with myriad spectral and functional properties, practical applications of optogenetics currently encompass cell signaling, subcellular localization, and gene regulation. Now, important questions regarding signal integration within branch points of signaling networks, asymmetric cell responses to spatially restricted signals, and effects of signal dosage versus duration can be addressed. This review summarizes emerging technologies and applications within the expanding field of optogenetics.

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2017-06-07
2024-12-06
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Literature Cited

  1. Fenno L, Yizhar O, Deisseroth K. 1.  2011. The development and application of optogenetics. Annu. Rev. Neurosci. 34:389–412 [Google Scholar]
  2. Ellis-Davies GC. 2.  2007. Caged compounds: photorelease technology for control of cellular chemistry and physiology. Nat. Methods 4:619–28 [Google Scholar]
  3. Nerbonne JM. 3.  1996. Caged compounds: tools for illuminating neuronal responses and connections. Curr. Opin. Neurobiol. 6:379–86 [Google Scholar]
  4. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 4.  2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8:1263–68 [Google Scholar]
  5. Hegemann P, Nagel G. 5.  2013. From channelrhodopsins to optogenetics. EMBO Mol. Med. 5:173–76 [Google Scholar]
  6. Zemelman BV, Lee GA, Ng M, Miesenböck G. 6.  2002. Selective photostimulation of genetically charged neurons. Neuron 33:15–22 [Google Scholar]
  7. Zhang K, Cui B. 7.  2015. Optogenetic control of intracellular signaling pathways. Trends Biotechnol 33:92–100 [Google Scholar]
  8. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K. 8.  2011. Optogenetics in neural systems. Neuron 71:9–34 [Google Scholar]
  9. Tischer D, Weiner OD. 9.  2014. Illuminating cell signalling with optogenetic tools. Nat. Rev. Mol. Cell Biol. 15:551–58 [Google Scholar]
  10. Deisseroth K. 10.  2011. Optogenetics. Nat. Methods 8:26–29 [Google Scholar]
  11. Boyden ES. 11.  2011. A history of optogenetics: the development of tools for controlling brain circuits with light. F1000 Biol. Rep. 3:11 [Google Scholar]
  12. Gorostiza P, Isacoff E. 12.  2007. Optical switches and triggers for the manipulation of ion channels and pores. Mol. Biosyst. 3:686–704 [Google Scholar]
  13. Zhang F, Vierock J, Yizhar O, Fenno LE, Tsunoda S. 13.  et al. 2011. The microbial opsin family of optogenetic tools. Cell 147:1446–57 [Google Scholar]
  14. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Mustl AM. 14.  et al. 2002. Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–98 [Google Scholar]
  15. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N. 15.  et al. 2003. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. PNAS 100:13940–45 [Google Scholar]
  16. Kato HE, Zhang F, Yizhar O, Ramakrishnan C, Nishizawa T. 16.  et al. 2012. Crystal structure of the channelrhodopsin light-gated cation channel. Nature 482:369–74 [Google Scholar]
  17. Lin JY, Lin MZ, Steinbach P, Tsien RY. 17.  2009. Characterization of engineered channel rhodopsin variants with improved properties and kinetics. Biophys. J. 96:1803–14 [Google Scholar]
  18. Tsunoda SP, Hegemann P. 18.  2009. Glu 87 of channelrhodopsin-1 causes pH-dependent color tuning and fast photocurrent inactivation. Photochem. Photobiol. 85:564–69 [Google Scholar]
  19. Berndt A, Lee SY, Ramakrishnan C, Deisseroth K. 19.  2014. Structure-guided transformation of channelrhodopsin into a light-activated chloride channel. Science 344:420–24 [Google Scholar]
  20. Christie JM, Salomon M, Nozue K, Wada M, Briggs WR. 20.  1999. LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. PNAS 96:8779–83 [Google Scholar]
  21. Huala E, Oeller PW, Liscum E, Han IS, Larsen E, Briggs WR. 21.  1997. Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278:2120–23 [Google Scholar]
  22. Christie JM, Swartz TE, Bogomolni RA, Briggs WR. 22.  2002. Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J 32:205–19 [Google Scholar]
  23. Christie JM, Gawthorne J, Young G, Fraser NJ, Roe AJ. 23.  2012. LOV to BLUF: flavoprotein contributions to the optogenetic toolkit. Mol. Plant 5:533–44 [Google Scholar]
  24. Harper SM, Neil LC, Gardner KH. 24.  2003. Structural basis of a phototropin light switch. Science 301:1541–44 [Google Scholar]
  25. Harper SM, Christie JM, Gardner KH. 25.  2004. Disruption of the LOV-Jα helix interaction activates phototropin kinase activity. Biochemistry 43:16184–92 [Google Scholar]
  26. Strickland D, Yao X, Gawlak G, Rosen MK, Gardner KH, Sosnick TR. 26.  2010. Rationally improving LOV domain-based photoswitches. Nat. Methods 7:623–26 [Google Scholar]
  27. Strickland D, Moffat K, Sosnick TR. 27.  2008. Light-activated DNA binding in a designed allosteric protein. PNAS 105:10709–14 [Google Scholar]
  28. Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I. 28.  et al. 2009. A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461:104–8 [Google Scholar]
  29. Wu YI, Wang X, He L, Montell D, Hahn KM. 29.  2011. Spatiotemporal control of small GTPases with light using the LOV domain. Methods Enzymol 497:393–407 [Google Scholar]
  30. Levskaya A, Weiner OD, Lim WA, Voigt CA. 30.  2009. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461:997–1001 [Google Scholar]
  31. Quail PH. 31.  2010. Phytochromes. Curr. Biol. 20:pR504–7 [Google Scholar]
  32. Quail PH. 32.  2002. Phytochrome photosensory signalling networks. Nat. Rev. Mol. Cell Biol. 3:85–93 [Google Scholar]
  33. Ni M, Tepperman JM, Quail PH. 33.  1999. Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400:781–84 [Google Scholar]
  34. Khanna R, Huq E, Kikis EA, Al-Sady B, Lanzatella C, Quail PH. 34.  2004. A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 16:3033–44 [Google Scholar]
  35. Kaberniuk AA, Shemetov AA, Verkhusha VV. 35.  2016. A bacterial phytochrome-based optogenetic system controllable with near-infrared light. Nat. Methods 13:591–97 [Google Scholar]
  36. Toettcher JE, Gong D, Lim WA, Weiner OD. 36.  2011. Light control of plasma membrane recruitment using the Phy-PIF system. Methods Enzymol 497:409–23 [Google Scholar]
  37. Buckley CE, Moore RE, Reade A, Goldberg AR, Weiner OD, Clarke J. 37.  2016. Reversible optogenetic control of subcellular protein localization in a live vertebrate embryo. Dev. Cell 36:117–26 [Google Scholar]
  38. Toettcher JE, Gong D, Lim WA, Weiner OD. 38.  2011. Light-based feedback for controlling intracellular signaling dynamics. Nat. Methods 8:837–39 [Google Scholar]
  39. Kennedy MJ, Hughes RM, Peteya LA, Schwartz JW, Ehlers MD, Tucker CL. 39.  2010. Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Methods 7:973–75 [Google Scholar]
  40. Taslimi A, Zoltowski B, Miranda JG, Pathak GP, Hughes RM, Tucker CL. 40.  2016. Optimized second-generation CRY2-CIB dimerizers and photoactivatable Cre recombinase. Nat. Chem. Biol. 12:425–30 [Google Scholar]
  41. Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A. 41.  et al. 2009. Interaction of COP1 and UVR8 regulates UV‐B‐induced photomorphogenesis and stress acclimation in Arabidopsis. . EMBO J. 28:591–601 [Google Scholar]
  42. Heijde M, Ulm R. 42.  2012. UV-B photoreceptor-mediated signalling in plants. Trends Plant Sci 17:230–37 [Google Scholar]
  43. Wu D, Hu Q, Yan Z, Chen W, Yan C. 43.  et al. 2012. Structural basis of ultraviolet-B perception by UVR8. Nature 484:214–19 [Google Scholar]
  44. Cloix C, Kaiserli E, Heilmann M, Baxter KJ, Brown BA. 44.  et al. 2012. C-terminal region of the UV-B photoreceptor UVR8 initiates signaling through interaction with the COP1 protein. PNAS 109:16366–70 [Google Scholar]
  45. Müller K, Engesser R, Schulz S, Steinberg T, Tomakidi P. 45.  et al. 2013. Multi-chromatic control of mammalian gene expression and signaling. Nucleic Acids Res 41:e124 [Google Scholar]
  46. Crefcoeur RP, Yin R, Ulm R, Halazonetis TD. 46.  2013. Ultraviolet-B-mediated induction of protein-protein interactions in mammalian cells. Nat. Commun. 4:1779 [Google Scholar]
  47. Sawa M, Nusinow DA, Kay SA, Imaizumi T. 47.  2007. FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–65 [Google Scholar]
  48. Zikihara K, Iwata T, Matsuoka D, Kandori H, Todo T, Tokutomi S. 48.  2006. Photoreaction cycle of the light, oxygen, and voltage domain in FKF1 determined by low-temperature absorption spectroscopy. Biochemistry 45:10828–37 [Google Scholar]
  49. Yazawa M, Sadaghiani AM, Hsueh B, Dolmetsch RE. 49.  2009. Induction of protein-protein interactions in live cells using light. Nat. Biotechnol. 27:941–45 [Google Scholar]
  50. Nash AI, McNulty R, Shillito ME, Swartz TE, Bogomolni RA. 50.  et al. 2011. Structural basis of photosensitivity in a bacterial light-oxygen-voltage/helix-turn-helix (LOV-HTH) DNA-binding protein. PNAS 108:9449–54 [Google Scholar]
  51. Rivera-Cancel G, Motta-Mena LB, Gardner KH. 51.  2012. Identification of natural and artificial DNA substrates for light-activated LOV-HTH transcription factor EL222. Biochemistry 51:10024–34 [Google Scholar]
  52. Motta-Mena LB, Reade A, Mallory MJ, Glantz S, Weiner OD. 52.  et al. 2014. An optogenetic gene expression system with rapid activation and deactivation kinetics. Nat. Chem. Biol. 10:196–202 [Google Scholar]
  53. Zoltowski BD, Schwerdtfeger C, Widom J, Loros JJ, Bilwes AM. 53.  et al. 2007. Conformational switching in the fungal light sensor Vivid. Science 316:1054–57 [Google Scholar]
  54. Lamb JS, Zoltowski BD, Pabit SA, Crane BR, Pollack L. 54.  2008. Time-resolved dimerization of a PAS-LOV protein measured with photocoupled small angle X-ray scattering. J. Am. Chem. Soc. 130:12226–27 [Google Scholar]
  55. Wang X, Chen X, Yang Y. 55.  2012. Spatiotemporal control of gene expression by a light-switchable transgene system. Nat. Methods 9:266–69 [Google Scholar]
  56. Kawano F, Suzuki H, Furuya A, Sato M. 56.  2015. Engineered pairs of distinct photoswitches for optogenetic control of cellular proteins. Nat. Commun. 6:6256 [Google Scholar]
  57. Zoltowski BD, Vaccaro B, Crane BR. 57.  2009. Mechanism-based tuning of a LOV domain photoreceptor. Nat. Chem. Biol. 5:827–34 [Google Scholar]
  58. Strickland D, Lin Y, Wagner E, Hope CM, Zayner J. 58.  et al. 2012. TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nat. Methods 9:379–84 [Google Scholar]
  59. Huang J, Koide A, Makabe K, Koide S. 59.  2008. Design of protein function leaps by directed domain interface evolution. PNAS 105:6578–83 [Google Scholar]
  60. Lee H-J, Zheng JJ. 60.  2010. PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun. Signal. 8:1–18 [Google Scholar]
  61. Guntas G, Hallett RA, Zimmerman SP, Williams T, Yumerefendi H. 61.  et al. 2015. Engineering an improved light-induced dimer (iLID) for controlling the localization and activity of signaling proteins. PNAS 112:112–17 [Google Scholar]
  62. Bugaj LJ, Choksi AT, Mesuda CK, Kane RS, Schaffer DV. 62.  2013. Optogenetic protein clustering and signaling activation in mammalian cells. Nat. Meth 10:249–52 [Google Scholar]
  63. Hallett RA, Zimmerman SP, Yumerefendi H, Bear JE, Kuhlman B. 63.  2016. Correlating in vitro and in vivo activities of light-inducible dimers: a cellular optogenetics guide. ACS Synth. Biol. 5:53–64 [Google Scholar]
  64. Taslimi A, Vrana JD, Chen D, Borinskaya S, Mayer BJ. 64.  et al. 2014. An optimized optogenetic clustering tool for probing protein interaction and function. Nat. Commun. 5:4925 [Google Scholar]
  65. Bugaj LJ, Spelke DP, Mesuda CK, Varedi M, Kane RS, Schaffer DV. 65.  2015. Regulation of endogenous transmembrane receptors through optogenetic Cry2 clustering. Nat. Commun. 6:6898 [Google Scholar]
  66. Stirman JN, Crane MM, Husson SJ, Wabnig S, Schultheis C. 66.  et al. 2011. Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. . Nat. Methods 8:153–58 [Google Scholar]
  67. Bernstein JG, Boyden ES. 67.  2011. Optogenetic tools for analyzing the neural circuits of behavior. Trends Cogn. Sci. 15:592–600 [Google Scholar]
  68. Grosenick L, Marshel JH, Deisseroth K. 68.  2015. Closed-loop and activity-guided optogenetic control. Neuron 86:106–39 [Google Scholar]
  69. Reutsky-Gefen I, Golan L, Farah N, Schejter A, Tsur L. 69.  et al. 2013. Holographic optogenetic stimulation of patterned neuronal activity for vision restoration. Nat. Commun. 4:9 [Google Scholar]
  70. Krook-Magnuson E, Armstrong C, Oijala M, Soltesz I. 70.  2013. On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat. Commun. 4:8 [Google Scholar]
  71. Hochbaum DR, Zhao Y, Farhi SL, Klapoetke N, Werley CA. 71.  et al. 2014. All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat. Methods 11:825–33 [Google Scholar]
  72. Adhikari A, Lerner TN, Finkelstein J, Pak S, Jennings JH. 72.  et al. 2015. Basomedial amygdala mediates top-down control of anxiety and fear. Nature 527:179–85 [Google Scholar]
  73. Ferenczi EA, Zalocusky KA, Liston C, Grosenick L, Warden MR. 73.  et al. 2016. Prefrontal cortical regulation of brainwide circuit dynamics and reward-related behavior. Science 351:aac9698 [Google Scholar]
  74. Shimizu-Sato S, Huq E, Tepperman JM, Quail PH. 74.  2002. A light-switchable gene promoter system. Nat. Biotechnol. 20:1041–44 [Google Scholar]
  75. Hughes RM, Bolger S, Tapadia H, Tucker CL. 75.  2012. Light-mediated control of DNA transcription in yeast. Methods 58:385–91 [Google Scholar]
  76. Cao JC, Arha M, Sudrik C, Bugaj LJ, Schaffer DV, Kane RS. 76.  2013. Light-inducible activation of target mRNA translation in mammalian cells. Chem. Commun. 49:8338–40 [Google Scholar]
  77. Cao JC, Arha M, Sudrik C, Schaffer DV, Kane RS. 77.  2014. Bidirectional regulation of mRNA translation in mammalian cells by using PUF domains. Angew. Chem. 53:4900–4 [Google Scholar]
  78. Polstein LR, Gersbach CA. 78.  2012. Light-inducible spatiotemporal control of gene activation by customizable zinc finger transcription factors. J. Am. Chem. Soc. 134:16480–83 [Google Scholar]
  79. Konermann S, Brigham MD, Trevino AE, Hsu PD, Heidenreich M. 79.  et al. 2013. Optical control of mammalian endogenous transcription and epigenetic states. Nature 500:472–76 [Google Scholar]
  80. Doudna JA, Charpentier E. 80.  2014. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096 [Google Scholar]
  81. Nihongaki Y, Yamamoto S, Kawano F, Suzuki H, Sato M. 81.  2015. CRISPR-Cas9-based photoactivatable transcription system. Chem. Biol. 22:169–74 [Google Scholar]
  82. Polstein LR, Gersbach CA. 82.  2015. A light-inducible CRISPR-Cas9 system for control of endogenous gene activation. Nat. Chem. Biol. 11:198–200 [Google Scholar]
  83. Nihongaki Y, Kawano F, Nakajima T, Sato M. 83.  2015. Photoactivatable CRISPR-Cas9 for optogenetic genome editing. Nat. Biotechnol. 33:755–60 [Google Scholar]
  84. Hemphill J, Borchardt EK, Brown K, Asokan A, Deiters A. 84.  2015. Optical control of CRISPR/Cas9 gene editing. J. Am. Chem. Soc. 137:5642–45 [Google Scholar]
  85. Yang X, Jost AP, Weiner OD, Tang C. 85.  2013. A light-inducible organelle-targeting system for dynamically activating and inactivating signaling in budding yeast. Mol. Biol. Cell 24:2419–30 [Google Scholar]
  86. Idevall-Hagren O, Dickson EJ, Hille B, Toomre DK, Camilli P. 86.  2012. Optogenetic control of phosphoinositide metabolism. PNAS 109:23 [Google Scholar]
  87. Katsura Y, Kubota H, Kunida K, Kanno A, Kuroda S, Ozawa T. 87.  2015. An optogenetic system for interrogating the temporal dynamics of Akt. Sci. Rep. 5:14589 [Google Scholar]
  88. O'Neill PR, Gautam N. 88.  2014. Subcellular optogenetic inhibition of G proteins generates signaling gradients and cell migration. Mol. Biol. Cell 25:2305–14 [Google Scholar]
  89. Ishii T, Sato K, Kakumoto T, Miura S, Touhara K. 89.  et al. 2015. Light generation of intracellular Ca2+ signals by a genetically encoded protein BACCS. Nat. Commun. 6:8021 [Google Scholar]
  90. Pham E, Mills E, Truong K. 90.  2011. A synthetic photoactivated protein to generate local or global Ca2+ signals. Chem. Biol. 18:880–90 [Google Scholar]
  91. Kyung T, Lee S, Kim J, Cho T, Park H. 91.  et al. 2015. Optogenetic control of endogenous Ca2+ channels in vivo. Nat. Biotechnol. 33:1092–96 [Google Scholar]
  92. 92.  Deleted in proof
  93. Gomez EJ, Gerhardt K, Judd J, Tabor JJ, Suh J. 93.  2015. Light-activated nuclear translocation of adeno-associated virus nanoparticles using phytochrome B for enhanced, tunable, and spatially programmable gene delivery. ACS Nano 10:225–37 [Google Scholar]
  94. Nguyen M, Kim C, Kim J, Park B, Lee S. 94.  et al. 2016. Optogenetic oligomerization of Rab GTPases regulates intracellular membrane trafficking. Nat. Chem. Biol. 12:431–36 [Google Scholar]
  95. Chen D, Gibson ES, Kennedy MJ. 95.  2013. A light-triggered protein secretion system. J. Cell Biol. 201:631–40 [Google Scholar]
  96. Spiltoir JI, Strickland D, Glotzer M, Tucker CL. 96.  2015. Optical control of peroxisomal trafficking. ACS Synth. Biol. 15:554–60 [Google Scholar]
  97. Hayashi-Takagi A, Yagishita S, Nakamura M, Shirai F, Wu YI. 97.  et al. 2015. Labelling and optical erasure of synaptic memory traces in the motor cortex. Nature 525:333–38 [Google Scholar]
  98. Toettcher JE, Weiner OD, Lim WA. 98.  2013. Using optogenetics to interrogate the dynamic control of signal transmission by the Ras/Erk module. Cell 155:1422–34 [Google Scholar]
  99. Zhang K, Duan L, Ong Q, Lin Z, Varman PM. 99.  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 [Google Scholar]
  100. Tucker CL, Vrana JD, Kennedy MJ. 100.  2014. Tools for controlling protein interactions using light. Curr. Protoc. Cell Biol. 64:17.16.1–20 [Google Scholar]
  101. Inglés-Prieto Á, Reichhart E, Muellner MK, Nowak M, Nijman SM. 101.  et al. 2015. Light-assisted small-molecule screening against protein kinases. Nat. Chem. Biol. 11:12952–54 [Google Scholar]
  102. Yoo SK, Deng Q, Cavnar PJ, Wu YI, Hahn KM. 102.  2010. Differential regulation of protrusion and polarity by PI(3)K during neutrophil motility in live zebrafish. Dev. Cell 18:226–36 [Google Scholar]
  103. Bansal V, Saggau P. 103.  2013. Digital micromirror devices: principles and applications in imaging. Cold Spring Harb. Protoc. 2013:404–11 [Google Scholar]
  104. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A. 104.  2005. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15:2279–84 [Google Scholar]
  105. Zhang F, Wang L-PP, Brauner M, Liewald JF, Kay K. 105.  et al. 2007. Multimodal fast optical interrogation of neural circuitry. Nature 446:633–39 [Google Scholar]
  106. Lima SQ, Miesenböck G. 106.  2005. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141–52 [Google Scholar]
  107. Guo ZV, Hart AC, Ramanathan S. 107.  2009. Optical interrogation of neural circuits in Caenorhabditis elegans. . Nat. Methods 6:891–96 [Google Scholar]
  108. Zhang F, Wang L-P, Boyden ES, Deisseroth K. 108.  2006. Channelrhodopsin-2 and optical control of excitable cells. Nat. Methods 3:785–92 [Google Scholar]
  109. Ayling OGS, Harrison TC, Boyd JD, Goroshkov A. 109.  2009. Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice. Nat. Methods 6:219–24 [Google Scholar]
  110. Hira R, Honkura N, Noguchi J, Maruyama Y. 110.  2009. Transcranial optogenetic stimulation for functional mapping of the motor cortex. J. Neurosci. Methods 179:258–63 [Google Scholar]
  111. Huber D, Petreanu L, Ghitani N, Ranade S, Hromádka T. 111.  et al. 2008. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451:61–64 [Google Scholar]
  112. Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K. 112.  et al. 2007. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54:205–18 [Google Scholar]
  113. Yazdan-Shahmorad A, Diaz-Botia C, Hanson TL, Kharazia V, Ledochowitsch P. 113.  et al. 2016. A large-scale interface for optogenetic stimulation and recording in nonhuman primates. Neuron 89:927–39 [Google Scholar]
  114. Chuong AS, Miri ML, Busskamp V, Matthews GA, Acker LC. 114.  et al. 2014. Noninvasive optical inhibition with a red-shifted microbial rhodopsin. Nat. Neurosci. 17:1123–29 [Google Scholar]
  115. Lin JY, Knutsen P, Muller A, Kleinfeld D, Tsien RY. 115.  2013. ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat. Neurosci. 16:1499–508 [Google Scholar]
  116. Prakash R, Yizhar O, Grewe B, Ramakrishnan C, Wang N. 116.  et al. 2012. Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nat. Methods 9:1171–79 [Google Scholar]
  117. Papagiakoumou E, Anselmi F, Bègue A, de Sars V, Glückstad J. 117.  et al. 2010. Scanless two-photon excitation of channelrhodopsin-2. Nat. Methods 7:848–54 [Google Scholar]
  118. Packer AM, Russell LE, Dalgleish HW, Hausser M. 118.  2015. Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo. Nat Methods 12:140–46 [Google Scholar]
  119. Bovetti S, Fellin T. 119.  2015. Optical dissection of brain circuits with patterned illumination through the phase modulation of light. J. Neurosci. Methods 241:66–77 [Google Scholar]
  120. Aravanis AM, Wang L-PP, Zhang F, Meltzer LA, Mogri MZ. 120.  et al. 2007. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J. Neural Eng. 4:56 [Google Scholar]
  121. Zhang F, Gradinaru V, Adamantidis AR, Durand R, Airan RD. 121.  et al. 2010. Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat. Protoc. 5:439–56 [Google Scholar]
  122. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. 122.  2007. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450:420–24 [Google Scholar]
  123. Wang J, Borton DA, Zhang J, Burwell RD, Nurmikko AV. 123.  2010. A neurophotonic device for stimulation and recording of neural microcircuits. Proc. IEEE Eng. Med. Biol. Sci 2010:2935–38 [Google Scholar]
  124. Anikeeva P, Andalman AS, Witten I, Warden M, Goshen I. 124.  et al. 2011. Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat. Neurosci. 15:163–70 [Google Scholar]
  125. Lee J, Ozden I, Song Y-K, Nurmikko AV. 125.  2015. Transparent intracortical microprobe array for simultaneous spatiotemporal optical stimulation and multichannel electrical recording. Nat. Methods 12:1157–62 [Google Scholar]
  126. Kim T-i, McCall JG, Jung YH, Huang X, Siuda ER. 126.  et al. 2013. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science 340:211–16 [Google Scholar]
  127. McCall JG, Kim T-i, Shin G, Huang X, Jung YH. 127.  et al. 2013. Fabrication and application of flexible, multimodal light-emitting devices for wireless optogenetics. Nat. Protoc. 8:2413–28 [Google Scholar]
  128. Park SI, Brenner DS, Shin G, Morgan CD, Copits BA. 128.  et al. 2015. Soft, stretchable, fully implantable miniaturized optoelectronic systems for wireless optogenetics. Nat. Biotechnol. 33:1280–86 [Google Scholar]
  129. Montgomery KL, Yeh AJ, Ho JS, Tsao V, Iyer S. 129.  et al. 2015. Wirelessly powered, fully internal optogenetics for brain, spinal and peripheral circuits in mice. Nat. Methods 12:969–74 [Google Scholar]
  130. Chow BY, Boyden ES. 130.  2013. Optogenetics and translational medicine. Sci. Transl. Med. 5:177ps5 [Google Scholar]
  131. Wu F, Stark E, Im M, Cho IJ, Yoon ES. 131.  et al. 2013. An implantable neural probe with monolithically integrated dielectric waveguide and recording electrodes for optogenetics applications. J. Neural Eng. 10:056012 [Google Scholar]
  132. Packer AM, Roska B, Hausser M. 132.  2013. Targeting neurons and photons for optogenetics. Nat. Neurosci. 16:805–15 [Google Scholar]
  133. Vaziri A, Emiliani V. 133.  2012. Reshaping the optical dimension in optogenetics. Curr. Opin. Neurobiol. 22:128–37 [Google Scholar]
  134. Wojtovich AP, Foster TH. 134.  2014. Optogenetic control of ROS production. Redox Biol 2:368–76 [Google Scholar]
  135. Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R. 135.  et al. 2010. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141:154–65 [Google Scholar]
  136. Muller K, Engesser R, Timmer J, Zurbriggen MD, Weber W. 136.  2014. Orthogonal optogenetic triple-gene control in Mammalian cells. ACS Synth. Biol. 3:796–801 [Google Scholar]
  137. Tonnesen J, Parish CL, Sorensen AT, Andersson A, Lundberg C. 137.  et al. 2011. Functional integration of grafted neural stem cell-derived dopaminergic neurons monitored by optogenetics in an in vitro Parkinson model. PLOS ONE 6:e17560 [Google Scholar]
  138. Zeng H, Madisen L. 138.  2012. Mouse transgenic approaches in optogenetics. Prog. Brain Res. 196:193–213 [Google Scholar]
  139. Del Bene F, Wyart C. 139.  2012. Optogenetics: a new enlightenment age for zebrafish neurobiology. Dev. Neurobiol. 72:404–14 [Google Scholar]
  140. Zalocusky K, Deisseroth K. 140.  2013. Optogenetics in the behaving rat: integration of diverse new technologies in a vital animal model. Optogenetics 1:1–17 [Google Scholar]
  141. Ruiz O, Lustig BR, Nassi JJ, Cetin A, Reynolds JH. 141.  et al. 2013. Optogenetics through windows on the brain in the nonhuman primate. J. Neurophysiol. 110:1455–67 [Google Scholar]
  142. Kotterman MA, Schaffer DV. 142.  2014. Engineering adeno-associated viruses for clinical gene therapy. Nat. Rev. Genet. 15:445–51 [Google Scholar]
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