Quantitative Biology

, Volume 5, Issue 2, pp 111–123 | Cite as

Engineering synthetic optogenetic networks for biomedical applications

  • Meiyan Wang
  • Yuanhuan Yu
  • Jiawei Shao
  • Boon Chin Heng
  • Haifeng Ye
Review

Abstract

Background

Recently, optogenetics based on genetically encoded photosensitive proteins has emerged as an innovative technology platform to revolutionize manipulation of cellular behavior through light stimulation. It has enabled user defined control of various cellular behaviors with spatiotemporal precision and minimal invasiveness, creating unprecedented opportunities for biomedical applications.

Results

This article reviews current advances in optogenetic networks designed for the treatment of human diseases. We highlight the advantages of these optogenetic networks, as well as emerging questions and future perspectives.

Conclusions

Various optogenetic systems have been engineered to control biological processes at all levels using light and applied for numerous diseases, such as metabolic disorders, cancer, and immune diseases. Continued development of optogenetic modules will be necessary to precisely control of gene expression magnitude towards clinical medical practice in the context of real-world problems.

Keywords

synthetic biology mammalian designer cells optogenetics synthetic gene circuits gene- and cell-based therapy 

Notes

Acknowledgements

This work was financially supported by the National Key Research and Development Program of China, Stem Cell and Translational Research (No. 2016YFA0100300), by the National Natural Science Foundation of China (Nos. 31522017, 31470834 and 31670869), by the Science and Technology Commission of Shanghai Municipality (Nos. 15QA1401500 and 14JC1401700), and by the Thousand Youth Talents Plan of China to H.Y.

References

  1. 1.
    Church, G. M., Elowitz, M. B., Smolke, C. D., Voigt, C. A. and Weiss, R. (2014) Realizing the potential of synthetic biology. Nat. Rev. Mol. Cell Biol., 15, 289–294PubMedCrossRefGoogle Scholar
  2. 2.
    Xie, M. Q., Haellman, V. and Fussenegger, M. (2016) Synthetic biology — application-oriented cell engineering. Curr. Opin. Biotechnol., 40, 139–148PubMedCrossRefGoogle Scholar
  3. 3.
    Khalil, A. S. and Collins, J. J. (2010) Synthetic biology: applications come of age. Nat. Rev. Genet., 11, 367–379PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Gardner, T. S., Cantor, C. R. and Collins, J. J. (2000) Construction of a genetic toggle switch in Escherichia coli. Nature, 403, 339–342PubMedCrossRefGoogle Scholar
  5. 5.
    Ye, H. F., Xie, M. Q., Xue, S., Hamri, G. C., Yin, J. L., Zulewski, H., and Fussenegger, M. (2016) Self-adjusting synthetic gene circuit for correcting insulin resistance. Nat. Biomed. Eng. 1, 0005PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Stricker, J., Cookson, S., Bennett, M. R., Mather, W. H., Tsimring, L. S. and Hasty, J. (2008) A fast, robust and tunable synthetic gene oscillator. Nature, 456, 516–519PubMedCrossRefGoogle Scholar
  7. 7.
    Fung, E., Wong, W. W., Suen, J. K., Bulter, T., Lee, S. G. and Liao, J. C. (2005) A synthetic gene-metabolic oscillator. Nature, 435, 118–122PubMedCrossRefGoogle Scholar
  8. 8.
    Tabor, J. J., Salis, H. M., Simpson, Z. B., Chevalier, A. A., Levskaya, A., Marcotte, E. M., Voigt, C. A. and Ellington, A. D. (2009) A synthetic genetic edge detection program. Cell, 137, 1272–1281PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Bulter, T., Lee, S. G., Wong, W. W. C., Fung, E., Connor, M. R. and Liao, J. C. (2004) Design of artificial cell-cell communication using gene and metabolic networks. Proc. Natl. Acad. Sci. USA, 101, 2299–2304PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Pathak, G. P., Vrana, J. D. and Tucker, C. L. (2013) Optogenetic control of cell function using engineered photoreceptors. Biol. Cell, 105, 59–72PubMedCrossRefGoogle Scholar
  11. 11.
    Chen, X. J., Li, T., Wang, X., Du, Z. M., Liu, R. M. and Yang, Y. (2016) Synthetic dual-input mammalian genetic circuits enable tunable and stringent transcription control by chemical and light. Nucleic Acids Res., 44, 2677–2690PubMedCrossRefGoogle Scholar
  12. 12.
    Chen, X., Li, T., Wang, X. and Yang, Y. (2015) A light-switchable bidirectional expression module allowing simultaneous regulation of multiple genes. Biochem. Biophys. Res. Commun., 465, 769–776PubMedCrossRefGoogle Scholar
  13. 13.
    Kemmer, C., Gitzinger, M., Daoud-El Baba, M., Djonov, V., Stelling, J. and Fussenegger, M. (2010) Self-sufficient control of urate homeostasis in mice by a synthetic circuit. Nat. Biotechnol., 28, 355–360PubMedCrossRefGoogle Scholar
  14. 14.
    Rössger, K., Charpin-El Hamri, G. and Fussenegger, M. (2013) Reward-based hypertension control by a synthetic brain-dopamine interface. Proc. Natl. Acad. Sci. USA, 110, 18150–18155PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Nihongaki, Y., Kawano, F., Nakajima, T. and Sato, M. (2015) Photoactivatable CRISPR-Cas9 for optogenetic genome editing. Nat. Biotechnol., 33, 755–760PubMedCrossRefGoogle Scholar
  16. 16.
    Zhang, K. and Cui, B. X. (2015) Optogenetic control of intracellular signaling pathways. Trends Biotechnol., 33, 92–100PubMedCrossRefGoogle Scholar
  17. 17.
    Weitzman, M. and Hahn, K. M. (2014) Optogenetic approaches to cell migration and beyond. Curr. Opin. Cell Biol., 30, 112–120PubMedCrossRefGoogle Scholar
  18. 18.
    Okuno, D., Asaumi, M. and Muneyuki, E. (1999) Chloride concentration dependency of the electrogenic activity of halorhodopsin. Biochemistry, 38, 5422–5429PubMedCrossRefGoogle Scholar
  19. 19.
    Zemelman, B. V., Lee, G. A., Ng, M. and Miesenbock, G. (2002) Selective photostimulation of genetically ChARGed neurons. Neuron, 33, 15–22PubMedCrossRefGoogle Scholar
  20. 20.
    Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P. and Bamberg, E. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA, 100, 13940–13945PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. and Deisseroth, K. (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci., 8, 1263–1268PubMedCrossRefGoogle Scholar
  22. 22.
    Kato, H. E., Zhang, F., Yizhar, O., Ramakrishnan, C., Nishizawa, T., Hirata, K., Ito, J., Aita, Y., Tsukazaki, T., Hayashi, S., et al. (2012) Crystal structure of the channelrhodopsin light-gated cation channel. Nature, 482, 369–374PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Oesterhelt, D. (1998) The structure and mechanism of the family of retinal proteins from halophilic archaea. Curr. Opin. Struct. Biol., 8, 489–500PubMedCrossRefGoogle Scholar
  24. 24.
    Haupts, U., Tittor, J. and Oesterhelt, D. (1999) Closing in on bacteriorhodopsin: progress in understanding the molecule. Annu. Rev. Biophys. Biomol. Struct., 28, 367–399PubMedCrossRefGoogle Scholar
  25. 25.
    Nagel, G., Brauner, M., Liewald, J. F., Adeishvili, N., Bamberg, E. and Gottschalk, A. (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid Behavioral responses. Curr. Biol., 15, 2279–2284PubMedCrossRefGoogle Scholar
  26. 26.
    Editorial (2011) Method of the Year 2010. Nat. Methods, 8, 1CrossRefGoogle Scholar
  27. 27.
    News, S. (2010) Stepping away from the trees for a look at the forest. Science, 330, 1612–1613CrossRefGoogle Scholar
  28. 28.
    Christie, J. M., Gawthorne, J., Young, G., Fraser, N. J. and Roe, A. J. (2012) LOV to BLUF: flavoprotein contributions to the optogenetic toolkit. Mol. Plant, 5, 533–544PubMedCrossRefGoogle Scholar
  29. 29.
    Muller, K., Engesser, R., Metzger, S., Schulz, S., Kampf, M. M., Busacker, M., Steinberg, T., Tomakidi, P., Ehrbar, M., Nagy, F., et al. (2013) A red/far-red light-responsive bi-stable toggle switch to control gene expression in mammalian cells. Nucleic Acids Res., 41, e77PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Wieland, M., Muller, M., Kyburz, A., Heissig, P., Wekenmann, S., Stolz, F., Auslander, S. and Fussenegger, M. (2014) Engineered UV-A light-responsive gene expression system for measuring sun cream efficacy in mammalian cell culture. J. Biotechnol., 189, 150–153PubMedCrossRefGoogle Scholar
  31. 31.
    Kawano, F., Suzuki, H., Furuya, A. and Sato, M. (2015) Engineered pairs of distinct photoswitches for optogenetic control of cellular proteins. Nat. Commun., 6, 6256PubMedCrossRefGoogle Scholar
  32. 32.
    Folcher, M., Oesterle, S., Zwicky, K., Thekkottil, T., Heymoz, J., Hohmann, M., Christen, M., Daoud-El-Baba, M. D., Buchmann, P. and Fussenegger, M. (2014) Mind-controlled transgene expression by a wireless-powered optogenetic designer cell implant. Nat. Commun., 5, 5392PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Fraikin, G. Y., Strakhovskaya, M. G., Belenikina, N. S. and Rubin, A. B. (2015) Bacterial photosensory proteins: regulatory functions and optogenetic applications. Microbiology, 84, 461–472CrossRefGoogle Scholar
  34. 34.
    Montgomery, K. L., Iyer, S. M., Christensen, A. J., Deisseroth, K. and Delp, S. L. (2016) Beyond the brain: optogenetic control in the spinal cord and peripheral nervous system. Sci. Transl. Med., 8, 337rv5CrossRefGoogle Scholar
  35. 35.
    Laakso, M. and Kuusisto, J. (2014) Insulin resistance and hyperglycaemia in cardiovascular disease development. Nat. Rev. Endocrinol., 10, 293–302PubMedCrossRefGoogle Scholar
  36. 36.
    Chen, L., Magliano, D. J. and Zimmet, P. Z. (2012) The worldwide epidemiology of type 2 diabetes mellitus — present and future perspectives. Nat. Rev. Endocrinol., 8, 228–236CrossRefGoogle Scholar
  37. 37.
    Grundy, S. M. (2006) Drug therapy of the metabolic syndrome: minimizing the emerging crisis in polypharmacy. Nat. Rev. Drug Discov., 5, 295–309PubMedCrossRefGoogle Scholar
  38. 38.
    Ye, H. F., Doaud-El Baba, M., Peng, R. W. and Fussenegger, M. (2011) A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science, 332, 1565–1568PubMedCrossRefGoogle Scholar
  39. 39.
    Wang, X., Chen, X. J. and Yang, Y. (2012) Spatiotemporal control of gene expression by a light-switchable transgene system. Nat. Methods, 9, 266–269PubMedCrossRefGoogle Scholar
  40. 40.
    Waldmann, T. A. (2003) Immunotherapy: past, present and future. Nat. Med., 9, 269–277PubMedCrossRefGoogle Scholar
  41. 41.
    Kalos, M. and June, C. H. (2013) Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology. immunity, 39, 49–60PubMedCrossRefGoogle Scholar
  42. 42.
    Restifo, N. P., Dudley, M. E. and Rosenberg, S. A. (2012) Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol., 12, 269–281PubMedCrossRefGoogle Scholar
  43. 43.
    Vivier, E., Ugolini, S., Blaise, D., Chabannon, C. and Brossay, L. (2012) Targeting natural killer cells and natural killer T cells in cancer. Nat. Rev. Immunol., 12, 239–252PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    He, L., Zhang, Y.W., Ma, G. L., Tan, P., Li, Z. J., Zang, S. B., Wu, X., Jing, J., Fang, S. H., Zhou, L. J., et al. (2015) Near-infrared photoactivatable control of Ca2+ signaling and optogenetic immunomodulation. eLife, 4, 25CrossRefGoogle Scholar
  45. 45.
    Xu, Y. X., Hyun, Y. M., Lim, K., Lee, H., Cummings, R. J., Gerber, S. A., Bae, S., Cho, T. Y., Lord, E. M. and Kim, M. (2014) Optogenetic control of chemokine receptor signal and T-cell migration. Proc. Natl. Acad. Sci. USA, 111, 6371–6376PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Boissonnas, A., Fetler, L., Zeelenberg, I. S., Hugues, S. and Amigorena, S. (2007) In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med., 204, 345–356PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Breart, B., Lemaitre, F., Celli, S. and Bousso, P. (2008) Twophoton imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice. J. Clin. Invest., 118, 1390–1397PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Cipolotti, L., Shallice, T., Chan, D., Fox, N., Scahill, R., Harrison, G., Stevens, J. and Rudge, P. (2001) Long-term retrograde amnesia... the crucial role of the hippocampus. Neuropsychologia, 39, 151–172PubMedGoogle Scholar
  49. 49.
    Nadel, L. and Moscovitch, M. (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol., 7, 217–227PubMedCrossRefGoogle Scholar
  50. 50.
    Buccione, I., Fadda, L., Serra, L., Caltagirone, C. and Carlesimo, G. A. (2008) Retrograde episodic and semantic memory impairment correlates with side of temporal lobe damage. J. Int. Neuropsychol. Soc., 14, 1083–1094PubMedCrossRefGoogle Scholar
  51. 51.
    Liu, X., Ramirez, S., Pang, P. T., Puryear, C. B., Govindarajan, A., Deisseroth, K. and Tonegawa, S. (2012) Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature, 484, 381–385.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Ramirez, S., Liu, X., Lin, P. A., Suh, J., Pignatelli, M., Redondo, R. L., Ryan, T. J. and Tonegawa, S. (2013) Creating a false memory in the hippocampus. Science, 341, 387–391PubMedCrossRefGoogle Scholar
  53. 53.
    Redondo, R. L., Kim, J., Arons, A. L., Ramirez, S., Liu, X. and Tonegawa, S. (2014) Bidirectional switch of the valence associated with a hippocampal contextual memory engram. Nature, 513, 426–430PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Denny, C. A., Kheirbek, M. A., Alba, E. L., Tanaka, K. F., Brachman, R. A., Laughman, K. B., Tomm, N. K., Turi, G. F., Losonczy, A. and Hen, R. (2014) Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis. Neuron, 83, 189–201PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Tanaka, K. Z., Pevzner, A., Hamidi, A. B., Nakazawa, Y., Graham, J. and Wiltgen, B. J. (2014) Cortical representations are reinstated by the hippocampus during memory retrieval. Neuron, 84, 347–354PubMedCrossRefGoogle Scholar
  56. 56.
    Cowansage, K. K., Shuman, T., Dillingham, B. C., Chang, A., Golshani, P. and Mayford, M. (2014) Direct reactivation of a coherent neocortical memory of context. Neuron, 84, 432–441PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Ryan, T. J., Roy, D. S., Pignatelli, M., Arons, A. and Tonegawa, S. (2015) Engram cells retain memory under retrograde amnesia. Science, 348, 1007–1013PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Nader, K., Schafe, G. E. and Le Doux, J. E. (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature, 406, 722–726PubMedCrossRefGoogle Scholar
  59. 59.
    Schroll, C., Riemensperger, T., Bucher, D., Ehmer, J., Voller, T., Erbguth, K., Gerber, B., Hendel, T., Nagel, G., Buchner, E., et al. (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol., 16, 1741–1747PubMedCrossRefGoogle Scholar
  60. 60.
    Bellmann, D., Richardt, A., Freyberger, R., Nuwal, N., Schwarzel, M., Fiala, A. and Stortkuhl, K. F. (2010) Optogenetically induced olfactory stimulation in Drosophila larvae reveals the neuronal basis of odor-aversion behavior. Front. Behav. Neurosci., 4, 10CrossRefGoogle Scholar
  61. 61.
    Hull, E. M., Du, J. F., Lorrain, D. S. and Matuszewich, L. (1995) Extracellular dopamine in the medial preoptic area — implications for sexual motivation and hormonal-control of copulation. J. Neurosci., 15, 7465–7471PubMedCrossRefGoogle Scholar
  62. 62.
    Sadeghipour, H., Ghasemi, M., Ebrahimi, F. and Dehpour, A. R. (2007) Effect of lithium on endothelium-dependent and neurogenic relaxation of rat corpus cavernosum: role of nitric oxide pathway. Nitric Oxide, 16, 54–63PubMedCrossRefGoogle Scholar
  63. 63.
    Melis, M. R., Spano, M. S., Succu, S. and Argiolas, A. (2000) Activation of γ-aminobutyric acidA receptors in the paraventricular nucleus of the hypothalamus reduces apomorphine-, Nmethyl-D-aspartic acid-and oxytocin-induced penile erection and yawning in male rats. Neurosci. Lett., 281, 127–130CrossRefGoogle Scholar
  64. 64.
    Melis, M. R., Succu, S. and Argiolas, A. (1997) Prevention by morphine of N-methyl-D-aspartic acid-induced penile erection and yawning: involvement of nitric oxide. Brain Res. Bull., 44, 689–694PubMedCrossRefGoogle Scholar
  65. 65.
    Melis, M. R., Succu, S., Iannucci, U. and Argiolas, A. (1997) Nmethyl-D-aspartic acid-induced penile erection and yawning: role of hypothalamic paraventricular nitric oxide. Eur. J. Pharmacol., 328, 115–123PubMedCrossRefGoogle Scholar
  66. 66.
    Toda, N., Ayajiki, K. and Okamura, T. (2005) Nitric oxide and penile erectile function. Pharmacol. Ther., 106, 233–266PubMedCrossRefGoogle Scholar
  67. 67.
    Melis, M. R. and Argiolas, A. (1999) Yawning: role of hypothalamic paraventricular nitric oxide. Acta Pharmacol. Sin., 20, 778–788Google Scholar
  68. 68.
    Melis, M. R. and Argiolas, A. (1997) Role of central nitric oxide in the control of penile erection and yawning. Prog. Neuropsychopharmacol. Biol. Psychiatry, 21, 899–922PubMedCrossRefGoogle Scholar
  69. 69.
    Nunes, K. P., Labazi, H. and Webb, R. C. (2012) New insights into hypertension-associated erectile dysfunction. Curr. Opin. Nephrol. Hypertens., 21, 163–170PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Fraga-Silva, R. A., Costa-Fraga, F. P., Faye, Y., Sturny, M., Santos, R. A., Dasilva, R. F. and Stergiopulos, N. (2014) An increased arginase activity is associated with corpus cavernosum impairment induced by hypercholesterolemia. J. Sex. Med., 11, 1173–1181PubMedCrossRefGoogle Scholar
  71. 71.
    Pauker-Sharon, Y., Arbel, Y., Finkelstein, A., Halkin, A., Herz, I., Banai, S. and Justo, D. (2013) Cardiovascular risk factors in men with ischemic heart disease and erectile dysfunction. Urology, 82, 377–381PubMedCrossRefGoogle Scholar
  72. 72.
    Huang, S. S., Lin, C. H., Chan, C. H., Loh, E. W. and Lan, T. H. (2013) Newly diagnosed major depressive disorder and the risk of erectile dysfunction: a population-based cohort study in Taiwan. Psychiatry Res., 210, 601–606PubMedCrossRefGoogle Scholar
  73. 73.
    Kim, T., Folcher, M., Doaud-El Baba, M. and Fussenegger, M. (2015) A synthetic erectile optogenetic stimulator enabling bluelight-inducible penile erection. Angew. Chem. Int. Ed., 54, 5933–5938CrossRefGoogle Scholar
  74. 74.
    Champion, H. C., Bivalacqua, T. J., Hyman, A. L., Ignarro, L. J., Hellstrom, W. J. G. and Kadowitz, P. J. (1999) Gene transfer of endothelial nitric oxide synthase to the penis augments erectile responses in the aged rat. Proc. Natl. Acad. Sci. USA, 96, 11648–11652PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Bennett, N. E., Kim, J. H., Wolfe, D. P., Sasaki, K., Yoshimura, N., Goins, W. F., Huang, S., Nelson, J. B., de Groat, W. C. and Glorioso, J. C. (2005) Improvement in erectile dysfunction after neurotrophic factor gene therapy in diabetic rats. J. Urol., 173, 1820–1824PubMedCrossRefGoogle Scholar
  76. 76.
    Christ, G. J., Day, N., Santizo, C., Sato, Y. S., Zhao, W. X., Sclafani, T., Bakal, R., Salman, M., Davies, K. and Melman, A. (2004) Intracorporal injection of hSlo cDNA restores erectile capacity in STZ-diabetic F-344 rats in vivo. Heart Circul. Physiol., 287, H1544–H1553CrossRefGoogle Scholar
  77. 77.
    Magee, T. R., Ferrini, M., Garban, H. J., Vernet, D., Mitani, K., Rajfer, J. and Gonzalez-Cadavid, F. (2002) Gene therapy of erectile dysfunction in the rat with penile neuronal nitric oxide synthase. Biol. Reprod., 67, 20–28PubMedCrossRefGoogle Scholar
  78. 78.
    Chancellor, M. B., Tirney, S., Mattes, C. E., Tzeng, E., Birder, L. A., Kanai, A. J., de Groat, W. C., Huard, J. and Yoshimura, N. (2003) Nitric oxide synthase gene transfer for erectile dysfunction in a rat model. BJU Int., 91, 691–696PubMedCrossRefGoogle Scholar
  79. 79.
    Antonenkov, V. D., Grunau, S., Ohlmeier, S. and Hiltunen, J. K. (2010) Peroxisomes are oxidative organelles. Antioxid. Redox Signal., 13, 525–537PubMedCrossRefGoogle Scholar
  80. 80.
    Millecamps, S. and Julien, J. P. (2013) Axonal transport deficits and neurodegenerative diseases. Nat. Rev. Neurosci., 14, 161–176PubMedCrossRefGoogle Scholar
  81. 81.
    Niopek, D., Benzinger, D., Roensch, J., Draebing, T., Wehler, P., Eils, R. and Di Ventura, B. (2014) Engineering light-inducible nuclear localization signals for precise spatiotemporal control of protein dynamics in living cells. Nat. Commun., 5, 4404PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Crefcoeur, R. P., Yin, R. H., Ulm, R. and Halazonetis, T. D. (2013) Ultraviolet-B-mediated induction of protein-protein interactions in mammalian cells. Nat. Commun., 4, 1779PubMedCrossRefGoogle Scholar
  83. 83.
    Yang, X. J., 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, 2419–2430PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Yumerefendi, H., Dickinson, D. J., Wang, H., Zimmerman, S. P., Bear, J. E., Goldstein, B., Hahn, K. and Kuhlman, B. (2015) Control of protein activity and cell fate specification via lightmediated nuclear translocation. PLoS One, 10, e0128443PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Spiltoir, J. I., Strickland, D., Glotzer, M. and Tucker, C. L. (2016) Optical control of peroxisomal trafficking. ACS Synth. Biol., 5, 554–560PubMedCrossRefGoogle Scholar
  86. 86.
    van Bergeijk, P., Adrian, M., Hoogenraad, C. C. and Kapitein, L. C. (2015) Optogenetic control of organelle transport and positioning. Nature, 518, 111–114PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Ishikawa, K., Tamura, Y. and Maruta, S. (2014) Photocontrol of mitotic kinesin Eg5 facilitated by thiol-reactive photochromic molecules incorporated into the loop L5 functional loop. J. Biochem., 155, 195–206PubMedCrossRefGoogle Scholar
  88. 88.
    Kamei, T., Fukaminato, T. and Tamaoki, N. (2012) A photochromic ATP analogue driving a motor protein with reversible light-controlled motility: controlling velocity and binding manner of a kinesin-microtubule system in an in vitro motility assay. Chem. Commun. (Camb.), 48, 7625–7627CrossRefGoogle Scholar
  89. 89.
    Nakamura, M., Chen, L., Howes, S. C., Schindler, T. D., Nogales, E. and Bryant, Z. (2014) Remote control of myosin and kinesin motors using light-activated gearshifting. Nat. Nanotechnol., 9, 693–697PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Duan, L. T., Che, D., Zhang, K., Ong, Q. X., Guo, S. L. and Cui, B. X. (2015) Optogenetic control of molecular motors and organelle distributions in cells. Chem. Biol., 22, 671–682PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Jena, B., Dotti, G. and Cooper, L. J. N. (2010) Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor. Blood, 116, 1035–1044PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    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, 941–945PubMedCrossRefGoogle Scholar
  93. 93.
    Park, J. S., Rhau, B., Hermann, A., McNally, K. A., Zhou, C., Gong, D., Weiner, O. D., Conklin, B. R., Onuffer, J. and Lim, W. A. (2014) Synthetic control of mammalian-cell motility by engineering chemotaxis to an orthogonal bioinert chemical signal. Proc. Natl. Acad. Sci. USA, 111, 5896–5901PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Taslimi, A., Zoltowski, B., Miranda, J. G., Pathak, G. P., Hughes, R. M. and Tucker, C. L. (2016) Optimized second-generation CRY2-CIB dimerizers and photoactivatable cre recombinase. Nat. Chem. Biol., 12, 425–430PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Konermann, S., Brigham, M. D., Trevino, A. E., Hsu, P. D., Heidenreich, M., Cong, L., Platt, R. J., Scott, D. A., Church, G. M. and Zhang, F. (2013) Optical control of mammalian endogenous transcription and epigenetic states. Nature, 500, 472.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A. and Bonas, U. (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science, 326, 1509–1512PubMedCrossRefGoogle Scholar
  97. 97.
    Moscou, M. J. and Bogdanove, A. J. (2009) A simple cipher governs DNA recognition by TAL effectors. Science, 326, 1501PubMedCrossRefGoogle Scholar
  98. 98.
    Zhang, F., Cong, L., Lodato, S., Kosuri, S., Church, G. M. and Arlotta, P. (2011) Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat. Biotechnol., 29, 149–153PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    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, 973–975PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Liu, H. T., Yu, X. H., Li, K. W., Klejnot, J., Yang, H. Y., Lisiero, D. and Lin, C. T. (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science, 322, 1535–1539PubMedCrossRefGoogle Scholar
  101. 101.
    Holkers, M., Maggio, I., Liu, J., Janssen, J. M., Miselli, F., Mussolino, C., Recchia, A., Cathomen, T. and Goncalves, M. (2013) Differential integrity of TALE nuclease genes following adenoviral and lentiviral vector gene transfer into human cells. Nucleic Acids Res., 41, e63PubMedCrossRefGoogle Scholar
  102. 102.
    Nihongaki, Y., Yamamoto, S., Kawano, F., Suzuki, H. and Sato, M. (2015) CRISPR-Cas9-based photoactivatable transcription system. Chem. Biol., 22, 169–174PubMedCrossRefGoogle Scholar
  103. 103.
    Hemphill, J., Borchardt, E. K., Brown, K., Asokan, A. and Deiters, A. (2015) Optical control of CRISPR/Cas9 gene editing. J. Am. Chem. Soc., 137, 5642–5645PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Lin, F., Dong, L., Wang, W., Liu, Y., Huang, W. and Cai, Z. (2016) An efficient light-inducible P53 expression system for inhibiting proliferation of bladder cancer cell. Int. J. Biol. Sci., 12, 1273–1278PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Schiml, S., Fauser, F. and Puchta, H. (2014) The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J., 80, 1139–1150PubMedCrossRefGoogle Scholar
  106. 106.
    Ran, F. A., Hsu, P. D., Lin, C. Y., Gootenberg, J. S., Konermann, S., Trevino, A. E., Scott, D. A., Inoue, A., Matoba, S., Zhang, Y., et al. (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 154, 1380–1389PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Slaymaker, I. M., Gao, L. Y., Zetsche, B., Scott, D. A., Yan,W. X. and Zhang, F. (2016) Rationally engineered Cas9 nucleases with improved specificity. Science, 351, 84–88PubMedCrossRefGoogle Scholar
  108. 108.
    Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P. and Lim, W. A. (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152, 1173–1183PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Weber, W. and Fussenegger, M. (2012) Emerging biomedical applications of synthetic biology. Nat. Rev. Genet., 13, 21–35.CrossRefGoogle Scholar
  110. 110.
    Xue, S., Yin, J. L., Shao, J. W., Yu, Y. H., Yang, L. F., Wang, Y. D., Xie, M. Q., Fussenegger, M. and Ye, H. F. (2016) A synthetic biology-inspired therapeutic strategy for targeting and treating hepatogenous diabetes. Mol. Ther., 443–455Google Scholar
  111. 111.
    Muller, K., Engesser, R., Metzger, S., Schulz, S., Kampf, M. M., Busacker, M., Steinberg, T., Tomakidi, P., Ehrbar, M., Nagy, F., et al. (2013) A red/far-red light-responsive bi-stable toggle switch to control gene expression in mammalian cells. Nucleic Acids Res., 41, e77PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Motta-Mena, L. B., Reade, A., Mallory, M. J., Glantz, S., Weiner, O. D., Lynch, K. W. and Gardner, K. H. (2014) An optogenetic gene expression system with rapid activation and deactivation kinetics. Nat. Chem. Biol., 10, 196–202PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Müller, K., Zurbriggen, M. D. and Weber, W. (2014) Control of gene expression using a red-and far-red light-responsive bi-stable toggle switch. Nat. Protoc., 9, 622–632PubMedCrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag GmbH 2017

Authors and Affiliations

  • Meiyan Wang
    • 1
  • Yuanhuan Yu
    • 1
  • Jiawei Shao
    • 1
  • Boon Chin Heng
    • 2
  • Haifeng Ye
    • 1
  1. 1.Shanghai Key Laboratory of Regulatory Biology, Institute of Biomedical Sciences and School of Life SciencesEast China Normal UniversityShanghaiChina
  2. 2.Department of Endodontology, Faculty of DentistryThe University of Hong KongHong Kong SARChina

Personalised recommendations