Enabling Photo-Crosslinking and Photo-Sensitizing Properties for Synthetic Fluorescent Protein Chromophores
Huan Feng
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
University of Chinese Academy of Sciences, Beijing, 100049 China
These authors contributed equally to this work.
Search for more papers by this authorProf. Qun Zhao
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
These authors contributed equally to this work.
Search for more papers by this authorBeirong Zhang
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
University of Chinese Academy of Sciences, Beijing, 100049 China
Search for more papers by this authorHang Hu
Department of Chemistry, University of Washington, Seattle, WA 98195 USA
Search for more papers by this authorMeng Liu
University of Chinese Academy of Sciences, Beijing, 100049 China
State Key Laboratory of Molecular Reaction Dynamics, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
Search for more papers by this authorProf. Kaifeng Wu
State Key Laboratory of Molecular Reaction Dynamics, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
Search for more papers by this authorProf. Xiaosong Li
Department of Chemistry, University of Washington, Seattle, WA 98195 USA
Search for more papers by this authorCorresponding Author
Prof. Xin Zhang
Department of Chemistry and Westlake Laboratory of Life Sciences and Biomedicine, Westlake University, 18 Shilongshan Road, Hangzhou, 310024 China
Search for more papers by this authorCorresponding Author
Prof. Lihua Zhang
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
Search for more papers by this authorCorresponding Author
Prof. Yu Liu
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
Search for more papers by this authorHuan Feng
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
University of Chinese Academy of Sciences, Beijing, 100049 China
These authors contributed equally to this work.
Search for more papers by this authorProf. Qun Zhao
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
These authors contributed equally to this work.
Search for more papers by this authorBeirong Zhang
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
University of Chinese Academy of Sciences, Beijing, 100049 China
Search for more papers by this authorHang Hu
Department of Chemistry, University of Washington, Seattle, WA 98195 USA
Search for more papers by this authorMeng Liu
University of Chinese Academy of Sciences, Beijing, 100049 China
State Key Laboratory of Molecular Reaction Dynamics, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
Search for more papers by this authorProf. Kaifeng Wu
State Key Laboratory of Molecular Reaction Dynamics, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
Search for more papers by this authorProf. Xiaosong Li
Department of Chemistry, University of Washington, Seattle, WA 98195 USA
Search for more papers by this authorCorresponding Author
Prof. Xin Zhang
Department of Chemistry and Westlake Laboratory of Life Sciences and Biomedicine, Westlake University, 18 Shilongshan Road, Hangzhou, 310024 China
Search for more papers by this authorCorresponding Author
Prof. Lihua Zhang
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
Search for more papers by this authorCorresponding Author
Prof. Yu Liu
CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, 457 Zhongshan Road, Dalian, 116023 China
Search for more papers by this authorAbstract
Synthetic fluorescent protein chromophores have been reported for their singlet state fluorescence properties and applications in bioimaging, but rarely for the triplet state chemistries. Herein, we enabled their photo-sensitizing and photo-crosslinking properties through rational modulations. Extension of molecular conjugation and introduction of heavy atoms promoted the generation of reactive oxygen species. Unlike other photosensitizers, these chromophores selectively photo-crosslinked aggregated proteins and uncovered the interactome profiles. We also exemplified their general applications in chromophore-assisted light inactivation, photodynamic therapy and photo induced polymerization. Theoretical calculation, pathway analysis and transient absorption spectroscopy provided mechanistic insights for this triplet state chemistry. Overall, this work expands the function and application of synthetic fluorescent protein chromophores by enabling their triplet excited state properties.
Conflict of interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available in the supplementary material of this article.
Supporting Information
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| Filename | Description |
|---|---|
| ange202215215-sup-0001-misc_information.pdf5.7 MB | Supporting Information |
| ange202215215-sup-0001-SI_Data_1_for_Fig.4B-oxidation.xlsx21.4 MB | Supporting Information |
| ange202215215-sup-0001-SI_Data_2_for_Fig.4B-crosslinking.xlsx649.8 KB | Supporting Information |
| ange202215215-sup-0001-SI_Data_3_for_Fig.4C-oxidation.xlsx63.4 MB | Supporting Information |
| ange202215215-sup-0001-SI_Data_4_for_Fig.4C-crosslinking.xlsx632.9 KB | Supporting Information |
| ange202215215-sup-0001-SI_Data_5_for_Fig.5B.xlsx29.1 MB | Supporting Information |
| ange202215215-sup-0001-SI_Data_6_for_Fig.5E-5G.xlsx1.2 MB | Supporting Information |
| ange202215215-sup-0001-SI_Data_7_for_Fig.5H-5I.xlsx21.3 KB | Supporting Information |
| ange202215215-sup-0001-SI_Data_8_for_Fig.S11-oxidation.xlsx41.8 MB | Supporting Information |
| ange202215215-sup-0001-SI_Data_9_for_Fig.S11-crosslinking.xlsx3.5 MB | Supporting Information |
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References
- 1H. Deng, S. Yan, Y. Huang, C. Lei, Z. Nie, TrAC Trends Anal. Chem. 2020, 122, 115757.
- 2R. Heim, D. C. Prasher, R. Y. Tsien, Proc. Natl. Acad. Sci. USA 1994, 91, 12501–12504.
- 3G. Zhang, V. Gurtu, S. R. Kain, Biochem. Biophys. Res. Commun. 1996, 227, 707–711.
- 4A. W. Nguyen, P. S. Daugherty, Nat. Biotechnol. 2005, 23, 355–360.
- 5N. C. Shaner, R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, R. Y. Tsien, Nat. Biotechnol. 2004, 22, 1567–1572.
- 6R. Ando, H. Mizuno, A. Miyawaki, Science 2004, 306, 1370–1373.
- 7R. Ando, H. Hama, M. Yamamoto-Hino, H. Mizuno, A. Miyawaki, Proc. Natl. Acad. Sci. USA 2002, 99, 12651–12656.
- 8M. S. Baranov, K. A. Lukyanov, A. O. Borissova, J. Shamir, D. Kosenkov, L. V. Slipchenko, L. M. Tolbert, I. V. Yampolsky, K. M. Solntsev, J. Am. Chem. Soc. 2012, 134, 6025–6032.
- 9J. S. Paige, K. Y. Wu, S. R. Jaffrey, Science 2011, 333, 642–646.
- 10G. Feng, C. Luo, H. Yi, L. Yuan, B. Lin, X. Luo, X. Hu, H. Wang, C. Lei, Z. Nie, S. Yao, Nucleic Acids Res. 2017, 45, 10380–10392.
- 11Y. Liu, C. H. Wolstenholme, G. C. Carter, H. Liu, H. Hu, L. S. Grainger, K. Miao, M. Fares, C. A. Hoelzel, H. P. Yennawar, G. Ning, M. Du, L. Bai, X. Li, X. Zhang, J. Am. Chem. Soc. 2018, 140, 7381–7384.
- 12D. E. Williams, E. A. Dolgopolova, P. J. Pellechia, A. Palukoshka, T. J. Wilson, R. Tan, J. M. Maier, A. B. Greytak, M. D. Smith, J. A. Krause, N. B. Shustova, J. Am. Chem. Soc. 2015, 137, 2223–2226.
- 13M. E. Bulina, K. A. Lukyanov, O. V. Britanova, D. Onichtchouk, S. Lukyanov, D. M. Chudakov, Nat. Protoc. 2006, 1, 947–953.
- 14K. Takemoto, T. Matsuda, N. Sakai, D. Fu, M. Noda, S. Uchiyama, I. Kotera, Y. Arai, M. Horiuchi, K. Fukui, T. Ayabe, F. Inagaki, H. Suzuki, T. Nagai, Sci. Rep. 2013, 3, 2629.
- 15X. Liu, F. Kang, C. Hu, L. Wang, Z. Xu, D. Zheng, W. Gong, Y. Lu, Y. Ma, J. Wang, Nat. Chem. 2018, 10, 1201–1206.
- 16S. Ye, H. Zhang, J. Fei, C. H. Wolstenholme, X. Zhang, Angew. Chem. Int. Ed. 2021, 60, 1339–1346; Angew. Chem. 2021, 133, 1359–1366.
- 17N. M. Webber, S. R. Meech, Photochem. Photobiol. Sci. 2007, 6, 976–981.
- 18W. Wan, Y. Huang, Q. Xia, Y. Bai, Y. Chen, W. Jin, M. Wang, D. Shen, H. Lyu, Y. Tang, X. Dong, Z. Gao, Q. Zhao, L. Zhang, Y. Liu, Angew. Chem. Int. Ed. 2021, 60, 11335–11343; Angew. Chem. 2021, 133, 11436–11444.
- 19X. Zhao, Y. Dai, F. Ma, S. Misal, K. Hasrat, H. Zhu, Z. Qi, Chem. Eng. J. 2021, 410, 128133.
- 20C. H. Wolstenholme, H. Hu, S. Ye, B. E. Funk, D. Jain, C. H. Hsiung, G. Ning, Y. Liu, X. Li, X. Zhang, J. Am. Chem. Soc. 2020, 142, 17515–17523.
- 21S. Xu, W. Wu, X. Cai, C. J. Zhang, Y. Yuan, J. Liang, G. Feng, P. Manghnani, B. Liu, Chem. Commun. 2017, 53, 8727–8730.
- 22S. Gan, S. Hu, X. L. Li, J. Zeng, D. Zhang, T. Huang, W. Luo, Z. Zhao, L. Duan, S. J. Su, B. Z. Tang, ACS Appl. Mater. Interfaces 2018, 10, 17327–17334.
- 23W. Wan, W. Jin, Y. Huang, Q. Xia, Y. Bai, H. Lyu, D. Liu, X. Dong, W. Li, Y. Liu, Anal. Chem. 2021, 93, 1717–1724.
- 24D. Shen, W. Jin, Y. Bai, Y. Huang, H. Lyu, L. Zeng, M. Wang, Y. Tang, W. Wan, X. Dong, Z. Gao, H. L. Piao, X. Liu, Y. Liu, Angew. Chem. Int. Ed. 2021, 60, 16067–16076; Angew. Chem. 2021, 133, 16203–16212.
- 25W. E. Balch, R. I. Morimoto, A. Dillin, J. W. Kelly, Science 2008, 319, 916–919.
- 26B. Jiang, A. Aliyan, N. P. Cook, A. Augustine, G. Bhak, R. Maldonado, A. D. Smith McWilliams, E. M. Flores, N. Mendez, M. Shahnawaz, F. J. Godoy, J. Montenegro, I. Moreno-Gonzalez, A. A. Marti, J. Am. Chem. Soc. 2019, 141, 15605–15610.
- 27H. Jozawa, M. G. Kabir, T. Zako, M. Maeda, K. Chiba, Y. Kuroda, FEBS Lett. 2016, 590, 3501–3509.
- 28H. Luo, W. Tang, H. Liu, X. Zeng, W. S. C. Ngai, R. Gao, H. Li, R. Li, H. Zheng, J. Guo, F. Qin, G. Wang, K. Li, X. Fan, P. Zou, P. R. Chen, Angew. Chem. Int. Ed. 2022, 61, e202202008; Angew. Chem. 2022, 134, e202202008.
- 29F. Chu, D. T. Thornton, H. T. Nguyen, Methods 2018, 144, 53–63.
- 30M. Bern, J. Saladino, J. S. Sharp, Rapid Commun. Mass Spectrom. 2010, 24, 768–772.
- 31M. Wensien, F. R. von Pappenheim, L. M. Funk, P. Kloskowski, U. Curth, U. Diederichsen, J. Uranga, J. Ye, P. Fang, K. T. Pan, H. Urlaub, R. A. Mata, V. Sautner, K. Tittmann, Nature 2021, 593, 460–464.
- 32P. Du, W. Liu, H. Cao, H. Zhao, C. H. Huang, Water Res.: X 2018, 1, 100002.
- 33M. Liu, Z. Zhang, J. Cheetham, D. Ren, Z. S. Zhou, Anal. Chem. 2014, 86, 4940–4948.
- 34X. R. Liu, M. M. Zhang, B. Zhang, D. L. Rempel, M. L. Gross, Anal. Chem. 2019, 91, 9238–9245.
- 35L. Ludvíková, P. Stacko, J. Sperry, P. Klan, J. Org. Chem. 2018, 83, 10835–10844.
- 36A. Aliyan, N. P. Cook, A. A. Marti, Chem. Rev. 2019, 119, 11819–11856.
- 37D. M. Walther, P. Kasturi, M. Zheng, S. Pinkert, G. Vecchi, P. Ciryam, R. I. Morimoto, C. M. Dobson, M. Vendruscolo, M. Mann, F. U. Hartl, Cell 2015, 161, 919–932.
- 38F. W. Hoff, W. Hu, Y. Qiu, A. S. Gamis, R. Aplenc, E. A. Kolb, T. A. Alonzo, A. A. Qutub, E. S. de Bont, S. W. M. Bruggeman, S. M. Kornblau, T. M. Horton, Blood 2018, 132, 293.
- 39C. P. Guimaraes, M. D. Witte, C. S. Theile, G. Bozkurt, L. Kundrat, A. E. Blom, H. L. Ploegh, Nat. Protoc. 2013, 8, 1787–1799.
- 40A. Kumar, M. Zhang, L. Zhu, R. P. Liao, C. Mutai, S. Hafsat, D. R. Sherman, M. W. Wang, PLoS One 2012, 7, e39961.
- 41X. Zhao, J. Liu, J. Fan, H. Chao, X. Peng, Chem. Soc. Rev. 2021, 50, 4185–4219.
- 42J. Dai, X. Wu, S. Ding, X. Lou, F. Xia, S. Wang, Y. Hong, J. Med. Chem. 2020, 63, 1996–2012.
- 43W. Strober, Curr. Protoc. Immunol. 2001, Appendix 3, Appendix 3B.
- 44Y. Bai, J. Zhao, S. Wang, T. Lin, F. Ye, S. Zhao, ACS Appl. Mater. Interfaces 2021, 13, 35365–35375.
- 45F. Xu, H. Ge, N. Xu, C. Yang, Q. Yao, S. Long, W. Sun, J. Fan, X. Xu, X. Peng, Sci. China Chem. 2021, 64, 488–498.
- 46J. J. Li, Y. N. Zhou, Z. H. Luo, Prog. Polym. Sci. 2018, 87, 1–33.
- 47H. A. Patel, M. S. Yavuz, C. T. Yavuz, RSC Adv. 2014, 4, 24320–24323.
- 48Y. Bu, X. Zhu, H. Wang, J. Zhang, L. Wang, Z. Yu, Y. Tian, H. Zhou, Y. Xie, Anal. Chem. 2021, 93, 12059–12066.
- 49K. X. Teng, W. K. Chen, L. Y. Niu, W. H. Fang, G. Cui, Q. Z. Yang, Angew. Chem. Int. Ed. 2021, 60, 19912–19920; Angew. Chem. 2021, 133, 20065–20073.
- 50Z. Zhao, C. B. Swartchick, J. Chan, Chem. Soc. Rev. 2022, 51, 829–868.
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