Red Light-Regulated Reversible Nuclear Localization of Proteins in Mammalian Cells and Zebrafish

ACS Synthetic Biology

Volumn 4, Issue 9, 2015, Pages 951-958

  Beyer, Hannes M ^a   Juillot, Samuel ^a   Herbst, Kathrin ^b,c   Samodelov, Sophia L ^a   Müller, Konrad ^a   Schamel, Wolfgang W ^a,d   Römer, Winfried ^a   Schäfer, Eberhard ^a   Nagy, Ferenc ^a,e   Strähle, Uwe ^b   Weber, Wilfried ^a   Zurbriggen, Matias D ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

light inducible nuclear transport; mammalian synthetic biology; optogenetics; phytochrome; plant synthetic biology

Indexed keywords

PHYTOCHROME B; PHYTOCHROME INTERACTING FACTOR 3; PROTEIN; SYNTHETIC PEPTIDE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN;

ANIMAL CELL; ARABIDOPSIS; ARTICLE; CELL NUCLEUS; CHO CELL LINE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; MAMMAL CELL; NONHUMAN; NUCLEAR IMPORT; OPTOGENETICS; PHOTOACTIVATION; PRIORITY JOURNAL; RED LIGHT; TRANSGENE; TRANSPORT KINETICS; ZEBRA FISH; 3T3 CELL LINE; ACTIVE TRANSPORT; ANIMAL; CRICETULUS; GENETIC ENGINEERING; GENETICS; LIGHT; METABOLISM; MOUSE; RADIATION RESPONSE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; CHO CELLS; CRICETULUS; GENETIC ENGINEERING; LIGHT; MICE; NIH 3T3 CELLS; PHYTOCHROME B; TRANSCRIPTION FACTORS; ZEBRAFISH;

EID: 84938328155     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.5b00004     Document Type: Article

References (37)

1. Epstein, J. A. and Neel, B. G. (2003) Signal transduction: an eye on organ development Nature 426, 238-239
2. Barry, E. R., Morikawa, T., Butler, B. L., Shrestha, K., de la Rosa, R., Yan, K. S., Fuchs, C. S., Magness, S. T., Smits, R., Ogino, S., Kuo, C. J., and Camargo, F. D. (2013) Restriction of intestinal stem cell expansion and the regenerative response by YAP Nature 493, 106-110
3. Geisberger, R., Rada, C., and Neuberger, M. S. (2009) The stability of AID and its function in class-switching are critically sensitive to the identity of its nuclear-export sequence Proc. Natl. Acad. Sci. U. S. A. 106, 6736-6741
4. Kau, T. R., Way, J. C., and Silver, P. A. (2004) Nuclear transport and cancer: from mechanism to intervention Nat. Rev. Cancer 4, 106-117
5. Yang, W., Xia, Y., Ji, H., Zheng, Y., Liang, J., Huang, W., Gao, X., Aldape, K., and Lu, Z. (2011) Nuclear PKM2 regulates beta-catenin transactivation upon EGFR activation Nature 480, 118-122
6. Beyer, H. M., Naumann, S., Weber, W., and Radziwill, G. (2014) Optogenetic control of signaling in mammalian cells Biotechnol. J. 10, 273-283
7. Tischer, D. and Weiner, O. D. (2014) Illuminating cell signalling with optogenetic tools Nat. Rev. Mol. Cell Biol. 15, 551-558
8. 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
9. 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
10. Wend, S., Wagner, H. J., Muller, K., Zurbriggen, M. D., Weber, W., and Radziwill, G. (2013) Optogenetic Control of Protein Kinase Activity in Mammalian Cells ACS Synth. Biol. 3, 280-285
11. 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
12. Chen, D., Gibson, E. S., and Kennedy, M. J. (2013) A light-triggered protein secretion system J. Cell Biol. 201, 631-640
13. Yang, X., Jost, A. P., 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
14. 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
15. 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, 4404
16. Usherenko, S., Stibbe, H., Musco, M., Essen, L. O., Kostina, E. A., and Taxis, C. (2014) Photo-sensitive degron variants for tuning protein stability by light BMC Syst. Biol. 8, 128
17. 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
18. Wu, Y. I., Frey, D., Lungu, O. I., Jaehrig, A., Schlichting, I., Kuhlman, B., and Hahn, K. M. (2009) A genetically encoded photoactivatable Rac controls the motility of living cells Nature 461, 104-108
19. Müller, K., Engesser, R., Metzger, S., Schulz, S., Kampf, M. M., Busacker, M., Steinberg, T., Tomakidi, P., Ehrbar, M., Nagy, F., Timmer, J., Zubriggen, M. D., and Weber, W. (2013) A red/far-red light-responsive bi-stable toggle switch to control gene expression in mammalian cells Nucleic Acids Res. 41, e77
20. Wang, X., Chen, X., and Yang, Y. (2012) Spatiotemporal control of gene expression by a light-switchable transgene system Nat. Methods 9, 266-269
21. Müller, K., Engesser, R., Schulz, S., Steinberg, T., Tomakidi, P., Weber, C. C., Ulm, R., Timmer, J., Zurbriggen, M. D., and Weber, W. (2013) Multi-chromatic control of mammalian gene expression and signaling Nucleic Acids Res. 41, e124
22. Müller, K., Engesser, R., Timmer, J., Zurbriggen, M. D., and Weber, W. (2014) Orthogonal optogenetic triple-gene control in Mammalian cells ACS Synth. Biol. 3, 796-801
23. Müller, K., Naumann, S., Weber, W., and Zurbriggen, M. D. (2014) Optogenetics for gene expression in mammalian cells Biol. Chem. 396, 145-152
24. Casal, J. J. (2013) Photoreceptor signaling networks in plant responses to shade Annu. Rev. Plant Biol. 64, 403-427
25. Rizzini, L., Favory, J. J., Cloix, C., Faggionato, D., O'Hara, A., Kaiserli, E., Baumeister, R., Schafer, E., Nagy, F., Jenkins, G. I., and Ulm, R. (2011) Perception of UV-B by the Arabidopsis UVR8 protein Science 332, 103-106
26. Ito, S., Song, Y. H., and Imaizumi, T. (2012) LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis Mol. Plant 5, 573-582
27. Chen, M., Tao, Y., Lim, J., Shaw, A., and Chory, J. (2005) Regulation of phytochrome B nuclear localization through light-dependent unmasking of nuclear-localization signals Curr. Biol. 15, 637-642
28. Pfeiffer, A., Nagel, M. K., Popp, C., Wust, F., Bindics, J., Viczian, A., Hiltbrunner, A., Nagy, F., Kunkel, T., and Schafer, E. (2012) Interaction with plant transcription factors can mediate nuclear import of phytochrome B Proc. Natl. Acad. Sci. U. S. A. 109, 5892-5897
29. Engelke, H., Chou, C., Uprety, R., Jess, P., and Deiters, A. (2014) Control of protein function through optochemical translocation ACS Synth. Biol. 3, 731-736
30. Ni, W., Xu, S. L., Chalkley, R. J., Pham, T. N., Guan, S., Maltby, D. A., Burlingame, A. L., Wang, Z. Y., and Quail, P. H. (2013) Multisite light-induced phosphorylation of the transcription factor PIF3 is necessary for both its rapid degradation and concomitant negative feedback modulation of photoreceptor phyB levels in Arabidopsis Plant Cell 25, 2679-2698
31. Müller, K., Engesser, R., Timmer, J., Nagy, F., Zurbriggen, M. D., and Weber, W. (2013) Synthesis of phycocyanobilin in mammalian cells Chem. Commun. 49, 8970-8972
32. Ghosh, I., Hamilton, A. D., and Regan, L. (2000) Antiparallel Leucine Zipper-Directed Protein Reassembly: Application to the Green Fluorescent Protein J. Am. Chem. Soc. 122, 5658-5659
33. Gasser, C., Taiber, S., Yeh, C. M., Wittig, C. H., Hegemann, P., Ryu, S., Wunder, F., and Moglich, A. (2014) Engineering of a red-light-activated human cAMP/cGMP-specific phosphodiesterase Proc. Natl. Acad. Sci. U. S. A. 111, 8803-8808
34. Ryu, M. H., Kang, I. H., Nelson, M. D., Jensen, T. M., Lyuksyutova, A. I., Siltberg-Liberles, J., Raizen, D. M., and Gomelsky, M. (2014) Engineering adenylate cyclases regulated by near-infrared window light Proc. Natl. Acad. Sci. U. S. A. 111, 10167-10172
35. Folcher, M., Oesterle, S., Zwicky, K., Thekkottil, T., Heymoz, J., Hohmann, M., Christen, M., Daoud El-Baba, M., Buchmann, P., and Fussenegger, M. (2014) Mind-controlled transgene expression by a wireless-powered optogenetic designer cell implant Nat. Commun. 5, 5392
36. 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, 622-632
37. Jacobs, J. L. and Dinman, J. D. (2004) Systematic analysis of bicistronic reporter assay data Nucleic Acids Res. 32, e160