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Annual Review of Biomedical Engineering

Volume 23, 2021

Signaling, Deconstructed: Using Optogenetics to Dissect and Direct Information Flow in Biological Systems

Abstract

Cells receive enormous amounts of information from their environment. How they act on this information—by migrating, expressing genes, or relaying signals to other cells—comprises much of the regulatory and self-organizational complexity found across biology. The “parts list” involved in cell signaling is generally well established, but how do these parts work together to decode signals and produce appropriate responses? This fundamental question is increasingly being addressed with optogenetic tools: light-sensitive proteins that enable biologists to manipulate the interaction, localization, and activity state of proteins with high spatial and temporal precision. In this review, we summarize how optogenetics is being used in the pursuit of an answer to this question, outlining the current suite of optogenetic tools available to the researcher and calling attention to studies that increase our understanding of and improve our ability to engineer biology.

Keyword(s): cell signaling, developmental biology, optogenetics, synthetic biology
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/content/journals/10.1146/annurev-bioeng-083120-111648
2021-07-13
2024-05-13
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Literature Cited

  1. 1. 
    Hartwell LH, Hopfield JJ, Leibler S, Murray AW 1999. From molecular to modular cell biology. Nature 402:C47–52
     [Google Scholar]
  2. 2. 
    Marr D. 1982. Vision: A Computational Investigation into the Human Representation and Processing of Visual Information Cambridge, MA: MIT Press
  3. 3. 
    Berg HC. 1993. Random Walks in Biology Princeton, NJ: Princeton Univ. Press
  4. 4. 
    Yi TM, Huang Y, Simon MI, Doyle J 2000. Robust perfect adaptation in bacterial chemotaxis through integral feedback control. PNAS 97:4649–53
     [Google Scholar]
  5. 5. 
    Alon U, Surette MG, Barkai N, Leibler S 1999. Robustness in bacterial chemotaxis. Nature 397:168–71
     [Google Scholar]
  6. 6. 
    Segall JE, Block SM, Berg HC 1986. Temporal comparisons in bacterial chemotaxis. PNAS 83:8987–91
     [Google Scholar]
  7. 7. 
    Fenno L, Yizhar O, Deisseroth K 2011. The development and application of optogenetics. Annu. Rev. Neurosci. 34:389–412
     [Google Scholar]
  8. 8. 
    Kolar K, Knobloch C, Stork H, Zindaric M, Weber W 2018. Optobase: a web platform for molecular optogenetics. ACS Synth. Biol. 7:1825–28
     [Google Scholar]
  9. 9. 
    Tye KM, Deisseroth K 2012. Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat. Rev. Neurosci. 13:251–66
     [Google Scholar]
  10. 10. 
    Zhang F, Vierock J, Yizhar O, Fenno LE, Tsunoda S et al. 2011. The microbial opsin family of optogenetic tools. Cell 147:1446–57
     [Google Scholar]
  11. 11. 
    Govorunova EG, Sineshchekov OA, Li H, Spudich JL 2017. Microbial rhodopsins: diversity, mechanisms, and optogenetic applications. Annu. Rev. Biochem. 86:845–72
     [Google Scholar]
  12. 12. 
    Crosson S, Rajagopal S, Moffat K 2003. The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42:2–10
     [Google Scholar]
  13. 13. 
    Harper SM, Neil LC, Gardner KH 2003. Structural basis of a phototropin light switch. Science 301:1541–44
     [Google Scholar]
  14. 14. 
    Yao X, Rosen MK, Gardner KH 2008. Estimation of the available free energy in a LOV2-Jα photoswitch. Nat. Chem. Biol. 4:491–97
     [Google Scholar]
  15. 15. 
    Sawa M, Nusinow DA, Kay SA, Imaizumi T 2007. FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–65
     [Google Scholar]
  16. 16. 
    Zoltowski BD, Vaccaro B, Crane BR 2009. Mechanism-based tuning of a LOV domain photoreceptor. Nat. Chem. Biol. 5:827–34
     [Google Scholar]
  17. 17. 
    Zoltowski BD, Crane BR 2008. Light activation of the LOV protein vivid generates a rapidly exchanging dimer. Biochemistry 47:7012–19
     [Google Scholar]
  18. 18. 
    Harper SM, Christie JM, Gardner KH 2004. Disruption of the LOV-Jα helix interaction activates phototropin kinase activity. Biochemistry 43:16184–92
     [Google Scholar]
  19. 19. 
    Glantz ST, Berlew EE, Jaber Z, Schuster BS, Gardner KH, Chow BY 2018. Directly light-regulated binding of RGS-LOV photoreceptors to anionic membrane phospholipids. PNAS 115:E7720–27
     [Google Scholar]
  20. 20. 
    Nash AI, McNulty R, Shillitob ME, Swartz TE, Bogomolnic RA 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]
  21. 21. 
    Weber AM, Kaiser J, Ziegler T, Pilsl S, Renzl C et al. 2019. A blue light receptor that mediates RNA binding and translational regulation. Nat. Chem. Biol. 15:1085–92
     [Google Scholar]
  22. 22. 
    Liu H, Yu X, Li K, Klejnot J, Yang H et al. 2008. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322:1535–39
     [Google Scholar]
  23. 23. 
    Zuo Z, Meng Y, Yu X, Zhang Z, Feng D et al. 2012. A study of the blue-light-dependent phosphorylation, degradation, and photobody formation of Arabidopsis CRY2. Mol. Plant 5:726–33
     [Google Scholar]
  24. 24. 
    Ma L, Guan Z, Wang Q, Yan X, Wang J et al. 2020. Structural insights into the photoactivation of Arabidopsis CRY2. Nat. Plants 6:1432–38
     [Google Scholar]
  25. 25. 
    Ma L, Wang X, Guan Z, Wang L, Wang Y et al. 2020. Structural insights into BIC-mediated inactivation of Arabidopsis cryptochrome 2. Nat. Struct. Mol. Biol. 27:472–79
     [Google Scholar]
  26. 26. 
    Liu B, Liu H, Zhong D, Lin C 2010. Searching for a photocycle of the cryptochrome photoreceptors. Curr. Opin. Plant Biol. 13:578–86
     [Google Scholar]
  27. 27. 
    Li P, Wang Q, Yu X, Liu H, Yang H et al. 2011. Arabidopsis cryptochrome 2 (CRY2) functions by the photoactivation mechanism distinct from the tryptophan (Trp) triad-dependent photoreduction. PNAS 108:20844–49
     [Google Scholar]
  28. 28. 
    Giovani B, Byrdin M, Ahmad M, Brettel K 2003. Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat. Struct. Mol. Biol. 10:489–90
     [Google Scholar]
  29. 29. 
    Rockwell NC, Martin SS, Feoktistova K, Lagarias JC 2011. Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes. PNAS 108:11854–59
     [Google Scholar]
  30. 30. 
    Fushimi K, Narikawa R 2019. Cyanobacteriochromes: photoreceptors covering the entire UV-to-visible spectrum. Curr. Opin. Struct. Biol. 57:39–46
     [Google Scholar]
  31. 31. 
    Fushimi K, Hasegawa M, Ito T, Rockwell NC, Enomoto G et al. 2020. Evolution-inspired design of multicolored photoswitches from a single cyanobacteriochrome scaffold. PNAS 117:15573–80
     [Google Scholar]
  32. 32. 
    Quail PH, Boylan MT, Parks BM, Short TW, Xu Y, Wagner D 1995. Phytochromes: photosensory perception and signal transduction. Science 268:675–80
     [Google Scholar]
  33. 33. 
    Burgie ES, Bussell AN, Walker JM, Dubiel K, Vierstra RD 2014. Crystal structure of the photosensing module from a red/far-red light–absorbing plant phytochrome. PNAS 111:10179–84
     [Google Scholar]
  34. 34. 
    Ni M, Tepperman JM, Quail PH 1999. Binding of Phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400:781–84
     [Google Scholar]
  35. 35. 
    Kaberniuk AA, Shemetov AA, Verkhusha VV 2016. A bacterial phytochrome-based optogenetic system controllable with near-infrared light. Nat. Methods 13:591–97
     [Google Scholar]
  36. 36. 
    Strauss HM, Schmieder P, Hughes J 2005. Light-dependent dimerisation in the N-terminal sensory module of cyanobacterial phytochrome 1. FEBS Lett. 579:3970–74
     [Google Scholar]
  37. 37. 
    Yuan H, Bauer CE 2008. PixE promotes dark oligomerization of the BLUF photoreceptor PixD. PNAS 105:11715–19
     [Google Scholar]
  38. 38. 
    Cloix C, Kaiserli E, Heilmann M, Baxter KJ, Brown BA 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]
  39. 39. 
    Kainrath S, Stadler M, Reichhart E, Distel M, Janovjak H 2017. Green-light-induced inactivation of receptor signaling using cobalamin-binding domains. Angew. Chem. Int. Ed. 56:4608–11
     [Google Scholar]
  40. 40. 
    Woolley GA, Morgan SA 2010. A photoswitchable DNA-binding protein based on a truncated GCN4-photoactive yellow protein chimera. Photochem. Photobiol. Sci. 9:1320–26
     [Google Scholar]
  41. 41. 
    Reis JM, Xu X, McDonald S, Woloschuk RM, Jaikaran ASI et al. 2018. Discovering selective binders for photoswitchable proteins using phage display. ACS Synth. Biol. 7:2355–64
     [Google Scholar]
  42. 42. 
    Zhou XX, Chung HK, Lam AJ, Lin MZ 2012. Optical control of protein activity by fluorescent protein domains. Science 338:810–14
     [Google Scholar]
  43. 43. 
    Zhang W, Lohman AW, Zhuravlova Y, Lu X, Wiens MD et al. 2017. Optogenetic control with a photocleavable protein, PHOCl. Nat. Methods 14:391–94
     [Google Scholar]
  44. 44. 
    Niopek D, Benzinger D, Roensch J, Draebing T, Wehler P et al. 2014. Engineering light-inducible nuclear localization signals for precise spatiotemporal control of protein dynamics in living cells. Nat. Commun. 5:4404
     [Google Scholar]
  45. 45. 
    Yumerefendi H, Dickinson DJ, Wang H, Zimmerman SP, Bear JE et al. 2015. Control of protein activity and cell fate specification via light-mediated nuclear translocation. PLOS ONE 10:e0128443
     [Google Scholar]
  46. 46. 
    Niopek D, Wehler P, Roensch J, Eils R, Di Ventura B 2016. Optogenetic control of nuclear protein export. Nat. Commun. 7:10624
     [Google Scholar]
  47. 47. 
    Yumerefendi H, Lerner AM, Zimmerman SP, Hahn K, Bear JE et al. 2016. Light-induced nuclear export reveals rapid dynamics of epigenetic modifications. Nat. Chem. Biol. 12:399–401
     [Google Scholar]
  48. 48. 
    Renicke C, Schuster D, Usherenko S, Essen L, Taxis C 2013. A LOV2 domain–based optogenetic tool to control protein degradation and cellular function. Chem. Biol. 20:619–26
     [Google Scholar]
  49. 49. 
    Guntas G, Hallett RA, Zimmerman SP, Williams T, Yumerefendi H 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]
  50. 50. 
    Strickland D, Lin Y, Wagner E, Hope CM, Zayner J et al. 2012. TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nat. Methods 9:379–84
     [Google Scholar]
  51. 51. 
    Patel AL, Yeung E, McGuire SE, Wu AY, Toettcher JE et al. 2019. Optimizing photoswitchable MEK. PNAS 116:25756–63
     [Google Scholar]
  52. 52. 
    Shimizu-Sato S, Huq E, Tepperman JM, Quail PH 2002. A light-switchable gene promoter system. Nat. Biotechnol. 20:1041–44
     [Google Scholar]
  53. 53. 
    Kennedy MJ, Hughes RM, Peteya LA, Schwartz JW, Ehlers MD, Tucker CL 2010. Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Methods 7:973–75
     [Google Scholar]
  54. 54. 
    Levskaya A, Weiner OD, Lim WA, Voigt CA 2009. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461:997–1001
     [Google Scholar]
  55. 55. 
    Kawano F, Suzuki H, Furuya A, Sato M 2015. Engineered pairs of distinct photoswitches for optogenetic control of cellular proteins. Nat. Commun. 6:6256
     [Google Scholar]
  56. 56. 
    Duan L, Hope J, Ong Q, Lou HY, Kim N et al. 2017. Understanding CRY2 interactions for optical control of intracellular signaling. Nat. Commun. 8:547
     [Google Scholar]
  57. 57. 
    Uda Y, Miura H, Goto Y, Aoki K 2020. Improvement of phycocyanobilin synthesis for genetically encoded phytochrome-based optogenetics. ACS Chem. Biol. 15:2896–906
     [Google Scholar]
  58. 58. 
    Kawano F, Okazaki R, Yazawa M, Sato M 2016. A photoactivatable Cre–LoxP recombination system for optogenetic genome engineering. Nat. Chem. Biol. 12:1059–64
     [Google Scholar]
  59. 59. 
    Meador K, Wysoczynski CL, Norris AJ, Aoto J, Bruchas MR, Tucker CL 2019. Achieving tight control of a photoactivatable Cre recombinase gene switch: new design strategies and functional characterization in mammalian cells and rodent. Nucleic Acids Res. 47:e97
     [Google Scholar]
  60. 60. 
    Bugaj LJ, Choksi AT, Mesuda CK, Kane RS, Schaffer DV 2013. Optogenetic protein clustering and signaling activation in mammalian cells. Nat. Methods 10:249–52
     [Google Scholar]
  61. 61. 
    Lee S, Park H, Kyung T, Kim NY, Kim S et al. 2014. Reversible protein inactivation by optogenetic trapping in cells. Nat. Methods 11:633–36
     [Google Scholar]
  62. 62. 
    Taslimi A, Vrana JD, Chen D, Borinskaya S, Mayer BJ et al. 2014. An optimized optogenetic clustering tool for probing protein interaction and function. Nat. Commun. 5:4925
     [Google Scholar]
  63. 63. 
    Park H, Kim NY, Lee S, Kim N, Kim J, Heo WD 2017. Optogenetic protein clustering through fluorescent protein tagging and extension of CRY2. Nat. Commun. 8:30
     [Google Scholar]
  64. 64. 
    Masuda S, Nakatani Y, Ren S, Tanaka M 2013. Blue light–mediated manipulation of transcription factor activity in vivo. ACS Chem. Biol. 8:2649–53
     [Google Scholar]
  65. 65. 
    Nakamura H, Lee AA, Afshar AS, Watanabe S, Rho E et al. 2018. Intracellular production of hydrogels and synthetic RNA granules by multivalent molecular interactions. Nat. Mater. 17:79–89
     [Google Scholar]
  66. 66. 
    Woo D, Seo Y, Jung H, Kim S, Kim N et al. 2019. Locally activating TrkB receptor generates actin waves and specifies axonal fate. Cell Chem. Biol. 26:1652–63
     [Google Scholar]
  67. 67. 
    Viswanathan R, Necakov A, Trylinski M, Harish RK, Krueger D et al. 2019. Optogenetic inhibition of Delta reveals digital Notch signalling output during tissue differentiation. EMBO Rep. 20:e47999
     [Google Scholar]
  68. 68. 
    Shin Y, Berry J, Pannucci N, Haataja MP, Toettcher JE, Brangwynne CP 2017. Spatiotemporal control of intracellular phase transitions using light-activated optodroplets. Cell 168:159–71
     [Google Scholar]
  69. 69. 
    Dine E, Gil AA, Uribe G, Brangwynne CP, Toettcher JE 2018. Protein phase separation provides long-term memory of transient spatial stimuli. Cell Syst. 6:655–63
     [Google Scholar]
  70. 70. 
    Bracha D, Walls MT, Wei MT, Zhu L, Kurian M et al. 2018. Mapping local and global liquid phase behavior in living cells using photo-oligomerizable seeds. Cell 175:1467–80
     [Google Scholar]
  71. 71. 
    Shin Y, Chang YC, Lee DSW, Berry J, Sanders DW et al. 2018. Liquid nuclear condensates mechanically sense and restructure the genome. Cell 175:1481–91
     [Google Scholar]
  72. 72. 
    Reed EH, Schuster BS, Good MC, Hammer DA 2020. SPLIT: stable protein coacervation using a light induced transition. ACS Synth. Biol. 9:500–7
     [Google Scholar]
  73. 73. 
    Dagliyan O, Tarnawski M, Chu P, Shirvanyants D, Schlichting I et al. 2016. Engineering extrinsic disorder to control protein activity in living cells. Science 354:1441–44
     [Google Scholar]
  74. 74. 
    Gil AA, Carrasco-López C, Zhu L, Zhao EM, Ravindran PT et al. 2020. Optogenetic control of protein binding using light-switchable nanobodies. Nat. Commun. 11:4044
     [Google Scholar]
  75. 75. 
    Carrasco-López C, Zhao EM, Gil AA, Alam N, Toettcher JE, Avalos JL 2020. Development of light-responsive protein binding in the monobody non-immunoglobulin scaffold. Nat. Commun. 11:4045
     [Google Scholar]
  76. 76. 
    Graziano BR, Gong D, Anderson KE, Pipathsouk A, Goldberg AR, Weiner OD 2017. A module for RAC temporal signal integration revealed with optogenetics. J. Cell Biol. 216:2515–31
     [Google Scholar]
  77. 77. 
    DeFelice MM, Clark HR, Hughey JJ, Maayan I, Kudo T et al. 2019. NF-κB signaling dynamics is controlled by a dose-sensing autoregulatory loop. Sci. Signal. 12:eaau3568
     [Google Scholar]
  78. 78. 
    Purvis JE, Lahav G 2013. Encoding and decoding cellular information through signaling dynamics. Cell 152:945–56
     [Google Scholar]
  79. 79. 
    Deneke VE, Di Talia S 2018. Chemical waves in cell and developmental biology. J. Cell Biol. 217:1193–204
     [Google Scholar]
  80. 80. 
    Marshall C 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal–regulated kinase activation. Cell 80:179–85
     [Google Scholar]
  81. 81. 
    Santos SD, Verveer PJ, Bastiaens PI 2007. Growth factor–induced MAPK network topology shapes ERK response determining PC-12 cell fate. Nat. Cell Biol. 9:324–30
     [Google Scholar]
  82. 82. 
    Albeck JG, Mills GB, Brugge JS 2013. Frequency-modulated pulses of ERK activity transmit quantitative proliferation signals. Mol. Cell 49:249–61
     [Google Scholar]
  83. 83. 
    Aoki K, Kumagai Y, Sakurai A, Komatsu N, Fujita Y et al. 2013. Stochastic ERK activation induced by noise and cell-to-cell propagation regulates cell density–dependent proliferation. Mol. Cell 52:529–40
     [Google Scholar]
  84. 84. 
    Kim N, Kim JM, Lee M, Kim CY, Chang KY, Do Heo W 2014. Spatiotemporal control of fibroblast growth factor receptor signals by blue light. Chem. Biol. 21:903–12
     [Google Scholar]
  85. 85. 
    Toettcher JE, Weiner OD, Lim WA 2013. Using optogenetics to interrogate the dynamic control of signal transmission by the RAS/ERK module. Cell 155:1422–34
     [Google Scholar]
  86. 86. 
    Wilson MZ, Ravindran PT, Lim WA, Toettcher JE 2017. Tracing information flow from ERK to target gene induction reveals mechanisms of dynamic and combinatorial control. Mol. Cell 67:757–69
     [Google Scholar]
  87. 87. 
    Bugaj L, Sabnis A, Mitchell A, Garbarino J, Toettcher JE et al. 2018. Cancer mutations and targeted drugs can disrupt dynamic signal encoding by the Ras-Erk pathway. Science 361:eaao3048
     [Google Scholar]
  88. 88. 
    Goglia AG, Wilson MZ, Jena SG, Silbert J, Basta LP et al. 2020. A live-cell screen for altered ERK dynamics reveals principles of proliferative control. Cell Syst. 10:240–53
     [Google Scholar]
  89. 89. 
    Tischer DK, Weiner OD 2019. Light-based tuning of ligand half-life supports kinetic proofreading model of T cell signaling. eLife 8:e42498
     [Google Scholar]
  90. 90. 
    Yousefi OS, Günther M, Hörner M, Chalupsky J, Wess M et al. 2019. Optogenetic control shows that kinetic proofreading regulates the activity of the T cell receptor. eLife 8:e42475
     [Google Scholar]
  91. 91. 
    Wang H, Vilela M, Winkler A, Tarnawski M, Schlichting I et al. 2016. LOVTRAP: an optogenetic system for photoinduced protein dissociation. Nat. Methods 13:755–58
     [Google Scholar]
  92. 92. 
    Hannanta-anan P, Chow BY 2016. Optogenetic control of calcium oscillation waveform defines NFAT as an integrator of calcium load. Cell Syst. 2:283–88
     [Google Scholar]
  93. 93. 
    Imayoshi I, Isomura A, Harima Y, Kawaguchi K, Kori H et al. 2013. Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342:1203–8
     [Google Scholar]
  94. 94. 
    Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I et al. 2009. A genetically encoded photoactivatable RAC controls the motility of living cells. Nature 461:104–8
     [Google Scholar]
  95. 95. 
    Toettcher JE, Gong D, Lim WA, Weiner OD 2011. Light-based feedback for controlling intracellular signaling dynamics. Nat. Methods 8:837–39
     [Google Scholar]
  96. 96. 
    Idevall-Hagren O, Dickson EJ, Hille B, Toomre DK, De Camilli P 2012. Optogenetic control of phosphoinositide metabolism. PNAS 109:E2316–23
     [Google Scholar]
  97. 97. 
    Stone OJ, Pankow N, Liu B, Sharma VP, Eddy RJ et al. 2019. Optogenetic control of cofilin and αTAT in living cells using Z-lock. Nat. Chem. Biol. 15:1183–90
     [Google Scholar]
  98. 98. 
    van Haren J, Charafeddine RA, Ettinger A, Wang H, Hahn KM, Wittmann T 2018. Local control of intracellular microtubule dynamics by EB1 photodissociation. Nat. Cell Biol. 20:252–61
     [Google Scholar]
  99. 99. 
    Cavanaugh KE, Staddon MF, Munro E, Banerjee S, Gardel ML 2020. RhoA mediates epithelial cell shape changes via mechanosensitive endocytosis. Dev. Cell 52:152–66
     [Google Scholar]
  100. 100. 
    Oakes PW, Wagner E, Brand CA, Probst D, Linke M et al. 2017. Optogenetic control of RhoA reveals zyxin-mediated elasticity of stress fibres. Nat. Commun. 8:15817
     [Google Scholar]
  101. 101. 
    Valon L, Marín-Llauradó A, Wyatt T, Charras G, Trepat X 2017. Optogenetic control of cellular forces and mechanotransduction. Nat. Commun. 8:14396
     [Google Scholar]
  102. 102. 
    Uroz M, Wistorf S, Serra-Picamal X, Conte V, Sales-Pardo M et al. 2018. Regulation of cell cycle progression by cell–cell and cell–matrix forces. Nat. Cell Biol. 20:646–54
     [Google Scholar]
  103. 103. 
    Hiratsuka T, Fujita Y, Naoki H, Aoki K, Kamioka Y, Matsuda M 2015. Intercellular propagation of extracellular signal–regulated kinase activation revealed by in vivo imaging of mouse skin. eLife 4:e05178
     [Google Scholar]
  104. 104. 
    Nikolic DL, Boettiger AN, Bar-Sagi D, Carbeck JD, Shvartsman SY 2006. Role of boundary conditions in an experimental model of epithelial wound healing. Am. J. Physiol. Cell Physiol. 291:C68–75
     [Google Scholar]
  105. 105. 
    Aoki K, Kondo Y, Naoki H, Hiratsuka T, Itoh RE, Matsuda M 2017. Propagating wave of ERK activation orients collective cell migration. Dev. Cell 43:305–17
     [Google Scholar]
  106. 106. 
    Hino N, Rossetti L, Marín-Llauradó A, Aoki K, Trepat X et al. 2020. ERK-mediated mechanochemical waves direct collective cell polarization. Dev. Cell 53:646–60
     [Google Scholar]
  107. 107. 
    Huang A, Amourda C, Zhang S, Tolwinski NS, Saunders TE 2017. Decoding temporal interpretation of the morphogen Bicoid in the early Drosophila embryo. eLife 6:e26258
     [Google Scholar]
  108. 108. 
    Irizarry J, McGehee J, Kim G, Stein D, Stathopoulos A 2020. Twist-dependent ratchet functioning downstream from Dorsal revealed using a light-inducible degron. Genes Dev. 34:965–72
     [Google Scholar]
  109. 109. 
    Johnson HE, Goyal Y, Pannucci NL, Schüpbach T, Shvartsman SY, Toettcher JE 2017. The spatiotemporal limits of developmental ERK signaling. Dev. Cell 40:185–92
     [Google Scholar]
  110. 110. 
    McDaniel SL, Gibson TJ, Schulz KN, Garcia MF, Nevil M et al. 2019. Continued activity of the pioneer factor Zelda is required to drive zygotic genome activation. Mol. Cell 74:185–95
     [Google Scholar]
  111. 111. 
    Kaur P, Saunders TE, Tolwinski NS 2017. Coupling optogenetics and light-sheet microscopy, a method to study Wnt signaling during embryogenesis. Sci. Rep. 7:16636
     [Google Scholar]
  112. 112. 
    Sako K, Pradhan SJ, Barone V, Inglés-Prieto Á, Müller P et al. 2016. Optogenetic control of nodal signaling reveals a temporal pattern of nodal signaling regulating cell fate specification during gastrulation. Cell Rep. 16:866–77
     [Google Scholar]
  113. 113. 
    Johnson HE, Toettcher JE 2019. Signaling dynamics control cell fate in the early Drosophila embryo. Dev. Cell 48:361–70
     [Google Scholar]
  114. 114. 
    Johnson HE, Djabrayan NJ, Shvartsman SY, Toettcher JE. 2020. Optogenetic rescue of a patterning mutant. Curr. Biol. 30:3414–24.e3
     [Google Scholar]
  115. 115. 
    Čapek D, Smutny M, Tichy AM, Morri M, Janovjak H, Heisenberg CP 2019. Light-activated Frizzled7 reveals a permissive role of non-canonical Wnt signaling in mesendoderm cell migration. eLife 8:e42093
     [Google Scholar]
  116. 116. 
    Murphy LO, Smith S, Chen RH, Fingar DC, Blenis J 2002. Molecular interpretation of ERK signal duration by immediate early gene products. Nat. Cell Biol. 4:556–64
     [Google Scholar]
  117. 117. 
    Keenan SE, Blythe SA, Marmion RA, Djabrayan NJV, Wieschaus EF, Shvartsman SY 2020. Rapid dynamics of signal-dependent transcriptional repression by Capicua. Dev. Cell 52:794–801
     [Google Scholar]
  118. 118. 
    Izquierdo E, Quinkler T, De Renzis S 2018. Guided morphogenesis through optogenetic activation of Rho signalling during early Drosophila embryogenesis. Nat. Commun. 9:2366
     [Google Scholar]
  119. 119. 
    Krueger D, Tardivo P, Nguyen C, De Renzis S 2018. Downregulation of basal myosin-II is required for cell shape changes and tissue invagination. EMBO J. 37:e100170
     [Google Scholar]
  120. 120. 
    Guglielmi G, Barry JD, Huber W, De Renzis S 2015. An optogenetic method to modulate cell contractility during tissue morphogenesis. Dev. Cell 35:646–60
     [Google Scholar]
  121. 121. 
    Eritano AS, Bromley CL, Albero AB, Schütz L, Wen FL et al. 2020. Tissue-scale mechanical coupling reduces morphogenetic noise to ensure precision during epithelial folding. Dev. Cell 53:212–28
     [Google Scholar]
  122. 122. 
    Krueger D, Quinkler T, Mortensen SA, Sachse C, De Renzis S 2019. Cross-linker-mediated regulation of actin network organization controls tissue morphogenesis. J. Cell Biol. 218:2743–61
     [Google Scholar]
  123. 123. 
    Qin X, Park BO, Liu J, Chen B, Choesmel-Cadamuro V et al. 2017. Cell-matrix adhesion and cell-cell adhesion differentially control basal myosin oscillation and Drosophila egg chamber elongation. Nat. Commun. 8:14708
     [Google Scholar]
  124. 124. 
    Teague BP, Guye P, Weiss R 2016. Synthetic morphogenesis. Cold Spring Harb. Perspect. Biol. 8:a023929
     [Google Scholar]
  125. 125. 
    Sakar MS, Neal D, Boudou T, Borochin MA, Li Y et al. 2012. Formation and optogenetic control of engineered 3D skeletal muscle bioactuators. Lab Chip 12:4976–85
     [Google Scholar]
  126. 126. 
    Staddon MF, Cavanaugh KE, Munro EM, Gardel ML, Banerjee S 2019. Mechanosensitive junction remodeling promotes robust epithelial morphogenesis. Biophys. J. 117:1739–50
     [Google Scholar]
  127. 127. 
    Repina NA, Bao X, Zimmermann JA, Joy DA, Kane RS, Schaffer DV. 2019. Optogenetic control of Wnt signaling for modeling early embryogenic patterning with human pluripotent stem cells. bioRxiv 665695. https://doi.org/10.1101/665695
    [Crossref]
  128. 128. 
    Chervyachkova E, Wegner SV 2018. Reversible social self-sorting of colloidal cell-mimics with blue light switchable proteins. ACS Synth. Biol. 7:1817–24
     [Google Scholar]
  129. 129. 
    Mueller M, Rasoulinejad S, Garg S, Wegner SV 2019. The importance of cell–cell interaction dynamics in bottom-up tissue engineering: concepts of colloidal self-assembly in the fabrication of multicellular architectures. Nano Lett. 20:2257–63
     [Google Scholar]
  130. 130. 
    Toda S, Blauch LR, Tang SK, Morsut L, Lim WA 2018. Programming self-organizing multicellular structures with synthetic cell-cell signaling. Science 361:156–62
     [Google Scholar]
  131. 131. 
    Milias-Argeitis A, Summers S, Stewart-Ornstein J, Zuleta I, Pincus D et al. 2011. In silico feedback for in vivo regulation of a gene expression circuit. Nat. Biotechnol. 29:1114–16
     [Google Scholar]
  132. 132. 
    Milias-Argeitis A, Rullan M, Aoki SK, Buchmann P, Khammash M 2016. Automated optogenetic feedback control for precise and robust regulation of gene expression and cell growth. Nat. Commun. 7:12546
     [Google Scholar]
  133. 133. 
    Harrigan P, Madhani HD, El-Samad H 2018. Real-time genetic compensation defines the dynamic demands of feedback control. Cell 175:877–86
     [Google Scholar]
  134. 134. 
    Perkins ML, Benzinger D, Arcak M, Khammash M 2020. Cell-in-the-loop pattern formation with optogenetically emulated cell-to-cell signaling. Nat. Commun. 11:1355
     [Google Scholar]
  135. 135. 
    Benninger RK, Piston DW. 2013. Two-photon excitation microscopy for the study of living cells and tissues. Curr. Protoc. Cell Biol. 59:4.11.1–24
     [Google Scholar]
  136. 136. 
    Kinjo T, Terai K, Horita S, Nomura N, Sumiyama K et al. 2019. Fret-assisted photoactivation of flavoproteins for in vivo two-photon optogenetics. Nat. Methods 16:1029–36
     [Google Scholar]
  137. 137. 
    Dempsey WP, Georgieva L, Helbling PM, Sonay AY, Truong TV et al. 2015. In vivo single-cell labeling by confined primed conversion. Nat. Methods 12:645–48
     [Google Scholar]
/content/journals/10.1146/annurev-bioeng-083120-111648
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Signaling, Deconstructed: Using Optogenetics to Dissect and Direct Information Flow in Biological Systems
Annual Review of Biomedical Engineering 23, 61 (2021); https://doi.org/10.1146/annurev-bioeng-083120-111648
/content/journals/10.1146/annurev-bioeng-083120-111648
/content/journals/10.1146/annurev-bioeng-083120-111648
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