Near-Infrared Optogenetic Genome Engineering Based on Photon-Upconversion Hydrogels
Yoichi Sasaki
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
Search for more papers by this authorDr. Mio Oshikawa
Center for Brain Integration Research (CBIR), Tokyo Medical and Dental University (TMDU), 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113–8510 Japan
Search for more papers by this authorDr. Pankaj Bharmoria
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
Search for more papers by this authorHironori Kouno
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
Search for more papers by this authorProf. Akiko Hayashi-Takagi
Laboratory of Medical Neuroscience, Institute for Molecular and Cellular Regulation, Gunma University, Maebashi-city, Gunma, 371-8512 Japan
PRESTO, JST, Honcho 4-1-8, Kawaguchi, Saitama, 332-0012 Japan
Search for more papers by this authorProf. Moritoshi Sato
Graduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro-ku, Tokyo, 153-8902 Japan
Search for more papers by this authorCorresponding Author
Prof. Itsuki Ajioka
Center for Brain Integration Research (CBIR), Tokyo Medical and Dental University (TMDU), 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113–8510 Japan
PRESTO, JST, Honcho 4-1-8, Kawaguchi, Saitama, 332-0012 Japan
Search for more papers by this authorCorresponding Author
Prof. Nobuhiro Yanai
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
PRESTO, JST, Honcho 4-1-8, Kawaguchi, Saitama, 332-0012 Japan
Search for more papers by this authorCorresponding Author
Prof. Nobuo Kimizuka
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
Search for more papers by this authorYoichi Sasaki
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
Search for more papers by this authorDr. Mio Oshikawa
Center for Brain Integration Research (CBIR), Tokyo Medical and Dental University (TMDU), 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113–8510 Japan
Search for more papers by this authorDr. Pankaj Bharmoria
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
Search for more papers by this authorHironori Kouno
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
Search for more papers by this authorProf. Akiko Hayashi-Takagi
Laboratory of Medical Neuroscience, Institute for Molecular and Cellular Regulation, Gunma University, Maebashi-city, Gunma, 371-8512 Japan
PRESTO, JST, Honcho 4-1-8, Kawaguchi, Saitama, 332-0012 Japan
Search for more papers by this authorProf. Moritoshi Sato
Graduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro-ku, Tokyo, 153-8902 Japan
Search for more papers by this authorCorresponding Author
Prof. Itsuki Ajioka
Center for Brain Integration Research (CBIR), Tokyo Medical and Dental University (TMDU), 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113–8510 Japan
PRESTO, JST, Honcho 4-1-8, Kawaguchi, Saitama, 332-0012 Japan
Search for more papers by this authorCorresponding Author
Prof. Nobuhiro Yanai
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
PRESTO, JST, Honcho 4-1-8, Kawaguchi, Saitama, 332-0012 Japan
Search for more papers by this authorCorresponding Author
Prof. Nobuo Kimizuka
Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395 Japan
Search for more papers by this authorGraphical Abstract
Near-infrared (NIR) light-triggered optogenetics with triplet–triplet annihilation-based photon upconversion (TTA-UC) is demonstrated. Triplet-lifetime extension by the covalent conjugation of donor and acceptor and a heat-induced conformational change of the hydrogel that prevents oxygen diffusion enables the formation of dendritic-spine-like structures by hippocampal neurons, induced by NIR-to-blue TTA-UC.
Abstract
Photon upconversion (UC) from near-infrared (NIR) light to visible light has enabled optogenetic manipulations in deep tissues. However, materials for NIR optogenetics have been limited to inorganic UC nanoparticles. Herein, NIR-light-triggered optogenetics using biocompatible, organic TTA-UC hydrogels is reported. To achieve triplet sensitization even in highly viscous hydrogel matrices, a NIR-absorbing complex is covalently linked with energy-pooling acceptor chromophores, which significantly elongates the donor triplet lifetime. The donor and acceptor are solubilized in hydrogels formed from biocompatible Pluronic F127 micelles, and heat treatment endows the excited triplets in the hydrogel with remarkable oxygen tolerance. Combined with photoactivatable Cre recombinase technology, NIR-light stimulation successfully performs genome engineering resulting in the formation of dendritic-spine-like structures of hippocampal neurons.
Conflict of interest
The authors declare no conflict of interest.
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References
- 1C. K. Kim, A. Adhikari, K. Deisseroth, Nat. Rev. Neurosci. 2017, 18, 222–235.
- 2J. Zhou, Q. Liu, W. Feng, Y. Sun, F. Li, Chem. Rev. 2015, 115, 395–465.
- 3
- 3aS. Baluschev, T. Miteva, V. Yakutkin, G. Nelles, A. Yasuda, G. Wegner, Phys. Rev. Lett. 2006, 97, 143903;
- 3bT. N. Singh-Rachford, F. N. Castellano, Coord. Chem. Rev. 2010, 254, 2560–2573;
- 3cJ. Zhao, S. Ji, H. Guo, RSC Adv. 2011, 1, 937–950;
- 3dY. C. Simon, C. Weder, J. Mater. Chem. 2012, 22, 20817–20830;
- 3eA. Monguzzi, R. Tubino, S. Hoseinkhani, M. Campione, F. Meinardi, Phys. Chem. Chem. Phys. 2012, 14, 4322–4332;
- 3fV. Gray, K. Moth-Poulsen, B. Albinsson, M. Abrahamsson, Coord. Chem. Rev. 2018, 362, 54–71;
- 3gJ. C. Wang, S. P. Hill, T. Dilbeck, O. O. Ogunsolu, T. Banerjee, K. Hanson, Chem. Soc. Rev. 2018, 47, 104–148.
- 4
- 4aZ. Huang, X. Li, M. Mahboub, K. M. Hanson, V. M. Nichols, H. Le, M. L. Tang, C. J. Bardeen, Nano Lett. 2015, 15, 5552–5557;
- 4bM. Mahboub, Z. Huang, M. L. Tang, Nano Lett. 2016, 16, 7169–7175;
- 4cS. Amemori, Y. Sasaki, N. Yanai, N. Kimizuka, J. Am. Chem. Soc. 2016, 138, 8702–8705.
- 5Y. Sasaki, S. Amemori, H. Kouno, N. Yanai, N. Kimizuka, J. Mater. Chem. C 2017, 5, 5063–5067.
- 6
- 6aJ.-H. Kim, F. Deng, F. N. Castellano, J.-H. Kim, Chem. Mater. 2012, 24, 2250–2252;
- 6bD. C. Thévenaz, A. Monguzzi, D. Vanhecke, R. Vadrucci, F. Meinardi, Y. C. Simon, C. Weder, Mater. Horiz. 2016, 3, 602–607;
- 6cP. Bharmoria, S. Hisamitsu, H. Nagatomi, T. Ogawa, M.-a. Morikawa, N. Yanai, N. Kimizuka, J. Am. Chem. Soc. 2018, 140, 10848–10855;
- 6dC. Ye, J. Ma, S. Chen, J. Ge, W. Yang, Q. Zheng, X. Wang, Z. Liang, Y. Zhou, J. Phys. Chem. C 2017, 121, 20158–20164.
- 7
- 7aW. E. Ford, M. A. J. Rodgers, J. Phys. Chem. 1992, 96, 2917–2920;
- 7bD. S. Tyson, F. N. Castellano, J. Phys. Chem. A 1999, 103, 10955–10960;
- 7cX.-y. Wang, A. Del Guerzo, R. H. Schmehl, J. Photochem. Photobiol. C 2004, 5, 55–77;
- 7dN. D. McClenaghan, Y. Leydet, B. Maubert, M. T. Indelli, S. Campagna, Coord. Chem. Rev. 2005, 249, 1336–1350;
- 7eD. Liu, Y. Zhao, Z. Wang, K. Xu, J. Zhao, Dalton Trans. 2018, 47, 8619–8628;
- 7fQ. Chen, Y. Liu, X. Guo, J. Peng, S. Garakyaraghi, C. M. Papa, F. N. Castellano, D. Zhao, Y. Ma, J. Phys. Chem. A 2018, 122, 6673–6682;
- 7gC. Mongin, P. Moroz, M. Zamkov, F. N. Castellano, Nat. Chem. 2018, 10, 225–230.
- 8F. Kawano, R. Okazaki, M. Yazawa, M. Sato, Nat. Chem. Biol. 2016, 12, 1059–1064.
- 9T. N. Singh-Rachford, F. N. Castellano, J. Phys. Chem. Lett. 2010, 1, 195–200.
- 10T. N. Singh-Rachford, F. N. Castellano, J. Phys. Chem. A 2008, 112, 3550–3556.
- 11Y. Y. Cheng, B. Fückel, T. Khoury, R. G. C. R. Clady, N. J. Ekins-Daukes, M. J. Crossley, T. W. Schmidt, J. Phys. Chem. A 2011, 115, 1047–1053.
- 12N. A. K. Meznarich, K. A. Juggernauth, K. M. Batzli, B. J. Love, Macromolecules 2011, 44, 7792–7798.
- 13A. Turshatov, D. Busko, S. Baluschev, T. Miteva, K. Landfester, New J. Phys. 2011, 13, 083035.
- 14N. Yanai, N. Kimizuka, Acc. Chem. Res. 2017, 50, 2487–2495.
- 15M. Oshikawa, K. Okada, K. Nakajima, I. Ajioka, Development 2013, 140, 2310–2320.
- 16B. Leuner, J. Falduto, T. J. Shors, J. Neurosci. 2003, 23, 659–665.
- 17N. Lamarche, N. Tapon, L. Stowers, P. D. Burbelo, P. Aspenström, T. Bridges, J. Chant, A. Hall, Cell 1996, 87, 519–529.
- 18L. Luo, T. K. Hensch, L. Ackerman, S. Barbel, L. Y. Jan, Y. N. Jan, Nature 1996, 379, 837–840.