In Situ Self-Assembled J-Aggregate Nanofibers of Glycosylated Aza-BODIPY for Synergetic Cell Membrane Disruption and Type I Photodynamic Therapy
Yi-chen Liu
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorDr. Guang-jian Liu
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorWei Zhou
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorGai-li Feng
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorQing-yu Ma
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorProf. Yuan Zhang
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorCorresponding Author
Prof. Guo-wen Xing
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorYi-chen Liu
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorDr. Guang-jian Liu
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorWei Zhou
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorGai-li Feng
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorQing-yu Ma
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorProf. Yuan Zhang
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorCorresponding Author
Prof. Guo-wen Xing
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorAbstract
The in situ self-assembly of exogenous molecules is a powerful strategy for manipulating cellular behavior. However, the direct self-assembly of photochemically inert constituents into supramolecular nano-photosensitizers (PSs) within cancer cells for precise photodynamic therapy (PDT) remains a challenge. Herein, we developed a glycosylated Aza-BODIPY compound (LMBP) capable of self-assembling into J-aggregate nanofibers in situ for cell membrane destruction and type I PDT. LMBP selectively entered human hepatocellular carcinoma HepG2 cells and subsequently self-assembled into intracellular J-aggregate nanovesicles and nanofibers through supramolecular interactions. Detailed studies revealed that these J-aggregate nanostructures generated superoxide radicals (O2−⋅) exclusively through photoinduced electron transfer, thus enabling effective PDT. Furthermore, the intracellular nanofibers exhibited an aggregation-induced retention effect, which resulted in selective toxicity to HepG2 cells by disrupting their cellular membranes and synergizing with PDT for powerful tumor suppression efficacy in vivo.
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
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
| Filename | Description |
|---|---|
| ange202309786-sup-0001-MBP.cif713.1 KB | Supporting Information |
| ange202309786-sup-0001-misc_information.pdf4.8 MB | Supporting Information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1
- 1aB. M. Luby, D. M. Charron, C. M. MacLaughlin, G. Zheng, Adv. Drug Delivery Rev. 2017, 113, 97–121;
- 1bG. Li, S. Yuan, D. Deng, T. Ou, Y. Li, R. Sun, Q. Lei, X. Wang, W. Shen, Y. Cheng, Z. Liu, S. Wu, Adv. Funct. Mater. 2019, 29, 1901932;
- 1cW. Piao, K. Hanaoka, T. Fujisawa, S. Takeuchi, T. Komatsu, T. Ueno, T. Terai, T. Tahara, T. Nagano, Y. Urano, J. Am. Chem. Soc. 2017, 139, 13713–13719;
- 1dK.-Xu Teng, W.-K. Chen, L.-Y. Niu, W.-H. Fang, G. Cui, Q.-Z. Yang, Angew. Chem. Int. Ed. 2021, 60, 19912–19920;
- 1eS. Zhou, X. Hu, R. Xia, S. Liu, Q. Pei, G. Chen, Z. Xie, X. Jing, Angew. Chem. Int. Ed. 2020, 59, 23198–23205.
- 2
- 2aM. R. Ke, S. F. Chen, X. H. Peng, Q. F. Zheng, B. Y. Zheng, C. K. Yeh, J. D. Huang, Eur. J. Med. Chem. 2017, 127, 200–209;
- 2bK.-X. Teng, L.-Y. Niu, Y.-F. Kang, Q.-Z. Yang, Chem. Sci. 2020, 11, 9703–9711.
- 3
- 3aS. S. Lucky, K. C. Soo, Y. Zhang, Chem. Rev. 2015, 115, 1990–2042;
- 3bV.-N. Nguyen, Y. Yan, J. Zhao, J. Yoon, Acc. Chem. Res. 2021, 54, 207–220;
- 3cH. Maeda, J. Wu, T. Sawa, Y. Matsumura, K. Hori, J. Controlled Release 2000, 65, 271–284.
- 4
- 4aG. B. Qi, Y. J. Gao, L. Wang, H. Wang, Adv. Mater. 2018, 30, 170344;
- 4bQ. Zou, M. Abbas, L. Zhao, S. Li, G. Shen, H. Yan, J. Am. Chem. Soc. 2017, 139, 1921–1927;
- 4cD. Zhang, K. X. Teng, L. Zhao, L. Y. Niu, Q. Z. Yang, Adv. Mater. 2023, 35, 2209789.
- 5
- 5aH. Kang, S. Rho, W. R. Stiles, S. Hu, Y. Baek, D. W. Hwang, S. Kashiwagi, M. S. Kim, H. S. Choi, Adv. Healthcare Mater. 2020, 9, 1901223;
- 5bX. Jiang, B. Du, J. Zheng, Nat. Nanotechnol. 2019, 14, 874–882.
- 6
- 6aS. Chagri, D. Y. W. Ng, T. Weil, Nat. Chem. Rev. 2022, 6, 320–338;
- 6bJ. Zhan, Y. Cai, S. He, L. Wang, Z. Yang, Angew. Chem. Int. Ed. 2018, 57, 1813–1816;
- 6cY. Yuan, J. Zhang, X. Qi, S. Li, G. Liu, S. Siddhanta, I. Barman, X. Song, M. T. McMahon, J. W. M. Bulte, Nat. Mater. 2019, 18, 1376–1383.
- 7
- 7aQ. Yao, C. Wang, M. Fu, L. Dai, J. Li, Y. Gao, ACS Nano 2020, 14, 4882–4889;
- 7bZ. Zheng, P. Chen, M. Xie, C. Wu, Y. Luo, W. Wang, J. Jiang, G. Liang, J. Am. Chem. Soc. 2016, 138, 11128–11131;
- 7cX. X. Zhao, L. L. Li, Y. Zhao, H. W. An, Q. Cai, J. Y. Lang, X. X. Han, B. Peng, Y. Fei, H. Liu, H. Qin, G. Nie, H. Wang, Angew. Chem. Int. Ed. 2019, 58, 15287–15294.
- 8
- 8aS. Yamamoto, K. Nishimura, K. Morita, S. Kanemitsu, Y. Nishida, T. Morimoto, T. Aoi, A. Tamura, T. Maruyama, Biomacromolecules 2021, 22, 2524–2531;
- 8bY. Deng, W. Zhan, G. Liang, Adv. Healthcare Mater. 2021, 10, 2001211;
- 8cM. Dergham, S. Lin, J. Geng, Angew. Chem. Int. Ed. 2022, 61, e202114267.
- 9
- 9aQ. Zhang, P. Yu, Y. Fan, C. Sun, H. He, X. Liu, L. Lu, M. Zhao, H. Zhang, F. Zhang, Angew. Chem. Int. Ed. 2021, 60, 3967–3973;
- 9bC. Sun, B. Li, M. Zhao, S. Wang, Z. Lei, L. Lu, H. Zhang, L. Feng, C. Dou, D. Yin, H. Xu, Y. Cheng, F. Zhang, J. Am. Chem. Soc. 2019, 141, 19221–19225.
- 10
- 10aK. Li, X. Duan, Z. Jiang, D. Ding, Y. Chen, G. Q. Zhang, Z. Liu, Nat. Commun. 2021, 12, 2376;
- 10bG. Yang, J. S. Ni, Y. Li, M. Zha, Y. Tu, K. Li, Angew. Chem. Int. Ed. 2021, 60, 5386–5393.
- 11N. J. Hestand, F. C. Spano, Chem. Rev. 2018, 118, 7069–7163.
- 12
- 12aZ. Feng, H. Wang, S. Wang, Q. Zhang, X. Zhang, A. A. Rodal, B. Xu, J. Am. Chem. Soc. 2018, 140, 9566–9573;
- 12bY. Li, T. Ma, H. Jiang, W. Li, D. Tian, J. Zhu, Z. Li, Angew. Chem. Int. Ed. 2022, 61, e2022030.
- 13
- 13aB. Sun, R. Chang, S. Cao, C. Yuan, L. Zhao, H. Yang, J. Li, X. Yan, J. C. M. Hest, Angew. Chem. Int. Ed. 2020, 59, 20582–20588;
- 13bJ. Du, T. Shi, S. Long, P. Chen, W. Sun, J. Fan, X. Peng, Coord. Chem. Rev. 2021, 427, 213604.
- 14
- 14aY.-Y. Wang, Y.-C. Liu, H. Sun, D.-S. Guo, Coord. Chem. Rev. 2019, 395, 46–62;
- 14bJ. Sun, K. Du, J. Diao, X. Cai, F. Feng, S. Wang, Angew. Chem. Int. Ed. 2020, 59, 12122–12128;
- 14cJ. Dai, Y. Li, Z. Long, R. Jiang, Z. Zhuang, Z. Wang, Z. Zhao, X. Lou, F. Xia, B. Z. Tang, ACS Nano 2020, 14, 854–866;
- 14dH. Shigemitsu, K. Ohkubo, K. Sato, A. Bunno, T. Mori, Y. Osakada, M. Fujitsuka, T. Kida, JACS Au 2022, 2, 1472–1478;
- 14eK. X. Teng, L. Y. Niu, Q. Z. Yang, J. Am. Chem. Soc. 2023, 145, 4081–4087.
- 15
- 15aD. Chen, Z. Wang, H. Dai, X. Lv, Q. Ma, D. Yang, J. Shao, Z. Xu, X. Dong, Small Methods 2020, 4, 2000013;
- 15bK.-X. Teng, L.-Y. Niu, Q.-Z. Yang, Chem. Sci. 2022, 13, 5951–5956;
- 15cK.-X. Teng, L.-Y. Niu, N. Xie, Q.-Z. Yang, Nat. Commun. 2022, 13, 6179.
- 16
- 16aZ. Shi, X. Han, W. Hu, H. Bai, B. Peng, L. Ji, Q. Fan, L. Li, W. Huang, Chem. Soc. Rev. 2020, 49, 7533–7567;
- 16bA. Gorman, J. Killoran, C. O'Shea, T. Kenna, W. M. Gallagher, D. F. O'Shea, J. Am. Chem. Soc. 2004, 126, 10619–10631.
- 17P. Chinna Ayya Swamy, G. Sivaraman, R. N. Priyanka, S. O. Raja, K. Ponnuvel, J. Shanmugpriya, A. Gulyani, Coord. Chem. Rev. 2020, 411, 213233.
- 18
- 18aM. Delbianco, P. Bharate, S. Varela-Aramburu, P. H. Seeberger, Chem. Rev. 2016, 116, 1693–1752;
- 18bS. A. Torres-Pérez, C. E. Torres-Pérez, M. Pedraza-Escalona, S. M. Pérez-Tapia, E. Ramón-Gallegos, Front. Oncol. 2020, 10, 605037.
- 19
- 19aY. Liu, Y. Zhang, G. Liu, G. Xing, Dyes Pigm. 2023, 208, 110813;
- 19bX. Bao, S. Zheng, L. Zhang, A. Shen, G. Zhang, S. Liu, J. Hu, Angew. Chem. Int. Ed. 2022, 61, e202207250.
- 20Deposition number 2240846 (for MBP) contains the supplementary crystallographic data for this paper. These data are provided free of charge by the joint Cambridge Crystallographic Data Centre and Fachinformationszentrum Karlsruhe Access Structures service.
- 21J. H. Kim, T. Schembri, D. Bialas, M. Stolte, F. Würthner, Adv. Mater. 2022, 34, 2104678.
- 22N. J. Hestand, C. Zheng, A. R. Penmetcha, B. Cona, J. A. Cody, F. C. Spano, C. J. Collison, J. Phys. Chem. C 2015, 119, 18964–18974.
- 23A. Lohr, M. Lysetska, F. Würthner, Angew. Chem. Int. Ed. 2005, 44, 5071–5074.
- 24
- 24aG. Yang, W. Zheng, G. Tao, L. Wu, Q. F. Zhou, Z. Kochovski, T. Ji, H. Chen, X. Li, Y. Lu, H. M. Ding, H. B. Yang, G. Chen, M. Jiang, ACS Nano 2019, 13, 13474–13485;
- 24bG. Yu, Y. Ma, C. Han, Y. Yao, G. Tang, Z. Mao, C. Gao, F. Huang, J. Am. Chem. Soc. 2013, 135, 10310–10313;
- 24cL. Y. Jia, G. J. Liu, Y. M. Ji, Y. Zhang, G. W. Xing, ChemNanoMat 2020, 6, 368–372;
- 24dY. M. Ji, G. J. Liu, C. Y. Li, Y. C. Liu, M. Hou, G. W. Xing, Chem. Asian J. 2019, 14, 3295–3300.
- 25T. Lu, F. Chen, J. Comput. Chem. 2012, 33, 580–592.
- 26
- 26aD. K. Ji, Y. Zhang, Y. Zang, J. Li, G. R. Chen, X. P. He, H. Tian, Adv. Mater. 2016, 28, 9356–9363;
- 26bA. A. D'Souza, P. V. Devarajan, J. Controlled Release 2015, 203, 126–139.
- 27
- 27aZ. M. Yang, K. M. Xu, Z. F. Guo, Z. H. Guo, B. Xu, Adv. Mater. 2007, 19, 3152–3156;
- 27bM. Pieszka, S. Han, C. Volkmann, R. Graf, I. Lieberwirth, K. Landfester, D. Y. W. Ng, T. Weil, J. Am. Chem. Soc. 2020, 142, 15780–15789.
- 28
- 28aY. Wang, W. Gao, X. Shi, J. Ding, W. Liu, H. He, K. Wang, F. Shao, Nature 2017, 547, 99–103;
- 28bS. Rühl, K. Shkarina, B. Demarco, R. Heilig, J. C. Santo, P. Broz, Science 2018, 362, 956–960.
- 29
- 29aL. Yu, Y. Xu, Z. Pu, H. Kang, M. Li, J. L. Sessler, J. S. Kim, J. Am. Chem. Soc. 2022, 144, 11326–11337;
- 29bM. Wu, X. Liu, H. Chen, Y. Duan, J. Liu, Y. Pan, B. Liu, Angew. Chem. Int. Ed. 2021, 60, 9093–9098.
Citing Literature
This is the
German version
of Angewandte Chemie.
Note for articles published since 1962:
Do not cite this version alone.
Take me to the International Edition version with citable page numbers, DOI, and citation export.
We apologize for the inconvenience.
