An Ion-Enhanced Oncolytic Virus-Like Nanoparticle for Tumor Immunotherapy
Fan Wu
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Department of Materials Science and State Key Laboratory of Molecular Engineering of Polymers, Fudan University, Shanghai, 200433 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorProf. Yanli Li
Guangzhou Municipal and Guangdong Provincial Key Laboratory of Molecular Target & Clinical Pharmacology, the NMPA and State Key Laboratory of Respiratory Disease, School of Pharmaceutical Sciences and the Fifth Affiliated Hospital, Guangzhou Medical University, Guangzhou, 511436 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorYun Meng
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorDr. Xuechao Cai
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorJieyun Shi
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorJinjin Li
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorDr. Yang Chen
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorDr. Li Zhang
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorDr. Xianfu Meng
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorDr. Huiyan Li
Department of Materials Science and State Key Laboratory of Molecular Engineering of Polymers, Fudan University, Shanghai, 200433 P. R. China
Search for more papers by this authorProf. Xingwu Jiang
Department of Materials Science and State Key Laboratory of Molecular Engineering of Polymers, Fudan University, Shanghai, 200433 P. R. China
Search for more papers by this authorProf. Zhenxiao Fu
State Key Laboratory of Advanced Materials and Electronic Components, Zhaoqing, 526020 P. R. China
Search for more papers by this authorCorresponding Author
Prof. Yelin Wu
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorCorresponding Author
Prof. Wenbo Bu
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Department of Materials Science and State Key Laboratory of Molecular Engineering of Polymers, Fudan University, Shanghai, 200433 P. R. China
Search for more papers by this authorFan Wu
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Department of Materials Science and State Key Laboratory of Molecular Engineering of Polymers, Fudan University, Shanghai, 200433 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorProf. Yanli Li
Guangzhou Municipal and Guangdong Provincial Key Laboratory of Molecular Target & Clinical Pharmacology, the NMPA and State Key Laboratory of Respiratory Disease, School of Pharmaceutical Sciences and the Fifth Affiliated Hospital, Guangzhou Medical University, Guangzhou, 511436 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorYun Meng
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorDr. Xuechao Cai
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorJieyun Shi
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorJinjin Li
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorDr. Yang Chen
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorDr. Li Zhang
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorDr. Xianfu Meng
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorDr. Huiyan Li
Department of Materials Science and State Key Laboratory of Molecular Engineering of Polymers, Fudan University, Shanghai, 200433 P. R. China
Search for more papers by this authorProf. Xingwu Jiang
Department of Materials Science and State Key Laboratory of Molecular Engineering of Polymers, Fudan University, Shanghai, 200433 P. R. China
Search for more papers by this authorProf. Zhenxiao Fu
State Key Laboratory of Advanced Materials and Electronic Components, Zhaoqing, 526020 P. R. China
Search for more papers by this authorCorresponding Author
Prof. Yelin Wu
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Search for more papers by this authorCorresponding Author
Prof. Wenbo Bu
Tongji University Cancer Center, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, 200072 P. R. China
Department of Materials Science and State Key Laboratory of Molecular Engineering of Polymers, Fudan University, Shanghai, 200433 P. R. China
Search for more papers by this authorGraphical Abstract
An oncolytic virus-mimicking strategy is proposed to enhance T cell-mediated tumor immunotherapy by synthesizing an ion-enhanced nanoplatform PolyIC@ZIF-8. This nanoplatform not only mimics an oncolytic virus-like function by inducing cell apoptosis to recruit T cells in a tumor antigen-dependent manner but also releases Zn2+ to enhance T cell recruitment and activation in a tumor antigen-independent manner.
Abstract
T lymphocytes (T cells) are essential for tumor immunotherapy. However, the insufficient number of activated T cells greatly limits the efficacy of tumor immunotherapy. Herein, we proposed an oncolytic virus-mimicking strategy to enhance T cell recruitment and activation for tumor treatment. We constructed an oncolytic virus-like nanoplatform (PolyIC@ZIF-8) that was degraded in the acidic tumor environment to release PolyIC and Zn2+. The released PolyIC exhibited an oncolytic virus-like function that induced tumor cell apoptosis and promoted T cell recruitment and activation through a tumor antigen-dependent manner. More importantly, the released Zn2+ not only enhanced T cell recruitment by inducing CXCL9/10/11 expression but also promoted T cell activation to increase interferon-γ (INF-γ) expression by inducing the phosphorylation of ZAP-70 via a tumor antigen-independent manner. This Zn2+-enhanced oncolytic virus-mimicking strategy provides a new approach for tumor immunotherapy.
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 from the corresponding author upon reasonable request.
Supporting Information
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References
- 1
- 1aM. Wang, B. Yin, H. Y. Wang, R. F. Wang, Immunotherapy 2014, 6, 1265–1278;
- 1bL. E. Klevorn, R. M. Teague, Trends Immunol. 2016, 37, 354–363.
- 2A. Xia, Y. Zhang, J. Xu, T. Yin, X. J. Lu, Front. Immunol. 2020, 10, 1719.
- 3
- 3aX. Cao, S. F. Cai, T. A. Fehniger, J. Song, L. I. Collins, D. R. Piwnica-Worms, T. J. Ley, Immunity 2007, 27, 635–646;
- 3bH. F. Aqbi, M. Wallace, S. Sappal, K. K. Payne, M. H. Manjili, J. Leukocyte Biol. 2018, 103, 1219–1223;
- 3cS. F. Ngiow, B. von Scheidt, H. Akiba, H. Yagita, M. W. Teng, M. J. Smyth, Cancer Res. 2011, 71, 3540–3551.
- 4
- 4aE. J. Wherry, Nat. Immunol. 2011, 12, 492–499;
- 4bE. J. Wherry, M. Kurachi, Nat. Rev. Immunol. 2015, 15, 486–499.
- 5
- 5aH. Fukuhara, Y. Ino, T. Todo, Cancer Sci. 2016, 107, 1373–1379;
- 5bS. J. Russell, K. W. Peng, Trends Pharmacol. Sci. 2007, 28, 326–333.
- 6
- 6aF. Benencia, M. C. Courrèges, N. W. Fraser, G. Coukos, Cancer Biol. Ther. 2008, 7, 1194–1205;
- 6bBenencia, M. C. Courrèges, J. R. Conejo-García, A. Mohamed-Hadley, L. Zhang, R. J. Buckanovich, R. Carroll, N. Fraser, G. Coukos, Mol. Ther. 2005, 12, 789–802.
- 7
- 7aH. L. Kaufman, F. J. Kohlhapp, A. Zloza, Nat. Rev. Drug Discovery 2015, 14, 642–662;
- 7bK. Twumasi-Boateng, J. L. Pettigrew, Y. Y. E. Kwok, J. C. Bell, B. H. Nelson, Nat. Rev. Cancer 2018, 18, 419–432.
- 8
- 8aA. Melcher, K. Parato, C. M. Rooney, J. C. Bell, Mol. Ther. 2011, 19, 1008–1016;
- 8bB. D. Lichty, C. J. Breitbach, D. F. Stojdl, J. C. Bell, Nat. Rev. Cancer 2014, 14, 559–567.
- 9N. Jayawardena, L. N. Burga, J. T. Poirier, M. Bostina, Oncolytic Virother 2019, 8, 39–56.
- 10
- 10aR. M. Verdijk, T. Mutis, B. Esendam, J. Kamp, C. J. Melief, A. Brand, E. Goulmy, J. Immunol. 1999, 163, 57–61;
- 10bM. Matsumoto, T. Seya, Adv. Drug Delivery Rev. 2008, 60, 805–812.
- 11
- 11aD. Tormo, A. Checinska, D. Alonso-Curbelo, E. Perez-Guijarro, E. Canon, E. Riveiro-Falkenbach, T. G. Calvo, L. Larribere, D. Megias, F. Mulero, M. A. Piris, R. Dash, P. M. Barral, J. L. Rodriguez-Peralto, P. Ortiz-Romero, T. Tuting, P. B. Fisher, M. S. Soengas, Cancer Cell 2009, 16, 103–114;
- 11bF. Bianchi, S. Pretto, E. Tagliabue, A. Balsari, L. Sfondrini, Cancer Biol. Ther. 2017, 18, 747–756.
- 12
- 12aA. M. Hafner, B. Corthesy, H. P. Merkle, Adv. Drug Delivery Rev. 2013, 65, 1386–1399;
- 12bB. Jin, R. Y. Wang, Q. Qiu, F. Sugauchi, T. Grandinetti, H. J. Alter, J. W. Shih, Immunology 2007, 122, 15–27.
- 13
- 13aH. Wang, L. Han, D. Zheng, M. Yang, Y. H. Andaloussi, P. Cheng, Z. Zhang, S. Ma, M. J. Zaworotko, Y. Feng, Y. Chen, Angew. Chem. Int. Ed. 2020, 59, 6263–6267; Angew. Chem. 2020, 132, 6322–6326;
- 13bG. Chen, S. Huang, X. Kou, S. Wei, S. Huang, S. Jiang, J. Shen, F. Zhu, G. Ouyang, Angew. Chem. Int. Ed. 2019, 58, 1463–1467; Angew. Chem. 2019, 131, 1477–1481;
- 13cG. Guo, T. Gong, H. Shen, Q. Wang, F. Jiang, J. Tang, X. Jiang, J. Wang, X. Zhang, W. Bu, Adv. Funct. Mater. 2021, 31, 2100795.
- 14
- 14aH. Wang, Y. Chen, H. Wang, X. Liu, X. Zhou, F. Wang, Angew. Chem. Int. Ed. 2019, 58, 7380–7384; Angew. Chem. 2019, 131, 7458–7462;
- 14bY. Li, P. Zhao, T. Gong, H. Wang, X. Jiang, H. Cheng, Y. Liu, Y. Wu, W. Bu, Angew. Chem. Int. Ed. 2020, 59, 22537–22543; Angew. Chem. 2020, 132, 22726–22732.
- 15
- 15aC. He, K. Lu, D. Liu, W. Lin, J. Am. Chem. Soc. 2014, 136, 5181–5184;
- 15bS. Peng, B. Bie, Y. Sun, M. Liu, H. Cong, W. Zhou, Y. Xia, H. Tang, H. Deng, X. Zhou, Nat. Commun. 2018, 9, 1293.
- 16
- 16aF. Y. Li, B. Chaigne-Delalande, C. Kanellopoulou, J. C. Davis, H. F. Matthews, D. C. Douek, J. I. Cohen, G. Uzel, H. C. Su, M. J. Lenardo, Nature 2011, 475, 471–476;
- 16bX. Shi, Y. Bi, W. Yang, X. Guo, Y. Jiang, C. Wan, L. Li, Y. Bai, J. Guo, Y. Wang, X. Chen, B. Wu, H. Sun, W. Liu, J. Wang, C. Xu, Nature 2013, 493, 111–115;
- 16cS. Hojyo, T. Fukada, J. Immunol. Res. 2016, 2016, 6762343.
- 17Y. Li, T. Gong, H. Gao, Y. Chen, H. Li, P. Zhao, Y. Jiang, K. Wang, Y. Wu, X. Zheng, W. Bu, Angew. Chem. Int. Ed. 2021, 60, 15472–15481; Angew. Chem. 2021, 133, 15600–15609.
- 18A. G. Dias Junior, N. G. Sampaio, J. Rehwinkel, Trends Microbiol. 2019, 27, 75–85.
- 19E. Swanton, P. Savory, S. Cosulich, P. Clarke, P. Woodman, Oncogene 1999, 18, 1781–1787.
- 20R. Tokunaga, W. Zhang, M. Naseem, A. Puccini, M. D. Berger, S. Soni, M. McSkane, H. Baba, H. J. Lenz, Cancer Treat. Rev. 2018, 63, 40–47.
- 21M. Yu, W. W. Lee, D. Tomar, S. Pryshchep, M. Czesnikiewicz-Guzik, D. L. Lamar, G. Li, K. Singh, L. Tian, C. M. Weyand, J. J. Goronzy, J. Exp. Med. 2011, 208, 775–785.
- 22T. Yokosuka, K. Sakata-Sogawa, W. Kobayashi, M. Hiroshima, A. Hashimoto-Tane, M. Tokunaga, M. L. Dustin, T. Saito, Nat. Immunol. 2005, 6, 1253–1262.
- 23
- 23aM. Zhang, R. Song, Y. Liu, Z. Yi, X. Meng, J. Zhang, Z. Tang, Z. Yao, Y. Liu, X. Liu, W. Bu, Chem 2019, 5, 2171–2182;
- 23bY. Liu, M. Zhang, W. Bu, View 2020, 1, e18.
