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Vol. 14 (2022)

Red Blood Cell-Mimic Nanocatalyst Triggering Radical Storm to Augment Cancer Immunotherapy

https://doi.org/10.1007/s40820-022-00801-z
Jiong Li
Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Biomedical Photonics and Sensing, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, People’s Republic of China
Sijia Wang
Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Biomedical Photonics and Sensing, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, People’s Republic of China
Xinyi Lin
Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Biomedical Photonics and Sensing, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, People’s Republic of China
Yanbing Cao
The United Innovation of Mengchao Hepatobiliary Technology Key Laboratory of Fujian Province, Mengchao Hepatobiliary Hospital of Fujian Medical University, Fuzhou 350025, People’s Republic of China
Zhixiong Cai
The United Innovation of Mengchao Hepatobiliary Technology Key Laboratory of Fujian Province, Mengchao Hepatobiliary Hospital of Fujian Medical University, Fuzhou 350025, People’s Republic of China
Jing Wang
Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Biomedical Photonics and Sensing, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, People’s Republic of China
Zhenxi Zhang
Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Biomedical Photonics and Sensing, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, People’s Republic of China
Xiaolong Liu
The United Innovation of Mengchao Hepatobiliary Technology Key Laboratory of Fujian Province, Mengchao Hepatobiliary Hospital of Fujian Medical University, Fuzhou 350025, People’s Republic of China
Ming Wu
The United Innovation of Mengchao Hepatobiliary Technology Key Laboratory of Fujian Province, Mengchao Hepatobiliary Hospital of Fujian Medical University, Fuzhou 350025, People’s Republic of China
Cuiping Yao
Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Biomedical Photonics and Sensing, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, People’s Republic of China

Corresponding Author: Cuiping Yao

zsycp@xjtu.edu.cn

Nano-Micro Letters, Vol. 14 (2022), Article Number: 57

Abstract

Red blood cells (RBCs) have recently emerged as promosing candidates for cancer treatment in terms of relieving tumor hypoxia and inducing oxidative damage against cancer cells, but they are still far from satisfactory due to their limited oxygen transport and reactive oxygen species generation rate in tumor tissue. Herein, artificial RBCs (designated FTP@RBCM) with radical storm production ability were developed for oncotherapy through multidimensional reactivity pathways of Fe-protoporphyrin-based hybrid metal–organic frameworks (FTPs, as the core), including photodynamic/chemodynamic-like, catalase-like and glutathione peroxidase-like activities. Meanwhile, owing to the advantages of long circulation abilities of RBCs provided by their cell membranes (RBCMs), FTP with a surface coated with RBCMs (FTP@RBCM) could enormously accumulate at tumor site to achieve remarkably enhanced therapeutic efficiency. Intriguingly, this ROS-mediated dynamic therapy was demonstrated to induce acute local inflammation and high immunogenic cancer death, which evoked a systemic antitumor immune response when combined with the newly identified T cell immunoglobulin and mucin-containing molecule 3 (Tim-3) checkpoint blockade, leading to not only effective elimination of primary tumors but also an abscopal effect of growth suppression of distant tumors. Therefore, such RBC-mimic nanocatalysts with multidimensional catalytic capacities might provide a promising new insight into synergistic cancer treatment.


Highlights:


1 A red blood cell-mimic nanocatalyst with photodynamic/chemodynamic-like, catalase-like and glutathione peroxidase-like activities was developed to boost radical storms for tumor eradication.
2 Combined with the Tim-3 immune checkpoint blockade, such radical therapy can systematically evoke a robust systemic antitumor immune response to eliminate residual cancer cells.

Keywords

Red blood cell mimic Metal–organic framework Nanocatalyst Radical storm Cancer immunotherapy
Li, Jiong, Sijia Wang, Xinyi Lin, Yanbing Cao, Zhixiong Cai, Jing Wang, Zhenxi Zhang, Xiaolong Liu, Ming Wu, and Cuiping Yao. 2022. “Red Blood Cell-Mimic Nanocatalyst Triggering Radical Storm to Augment Cancer Immunotherapy”. Nano-Micro Letters 14 (February):57. https://doi.org/10.1007/s40820-022-00801-z.
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References
  1. H. Minasyan, Phagocytosis and oxycytosis: two arms of human innate immunity. Immunol. Res. 66, 271–280 (2018). https://doi.org/10.1007/s12026-018-8988-5
  2. A. Ukidve, Z. Zhao, A. Fehnel, V. Krishnan, D.C. Pan et al., Erythrocyte-driven immunization via biomimicry of their natural antigen-presenting function. PNAS 117(30), 17727–17736 (2020). https://doi.org/10.1073/pnas.2002880117
  3. X. Liu, M.M. Jansman, L. Hosta-Rigau, Haemoglobin-loaded metal organic framework-based nanoparticles camouflaged with a red blood cell membrane as potential oxygen delivery systems. Biomater. Sci. 8(21), 5859–5873 (2020). https://doi.org/10.1039/D0BM01118E
  4. K. Ni, T. Aung, S. Li, N. Fatuzzo, X. Liang et al., Nanoscale metal-organic framework mediates radical therapy to enhance cancer immunotherapy. Chem 5(7), 1892–1913 (2019). https://doi.org/10.1016/j.chempr.2019.05.013
  5. H. Yang, R. Liu, Y. Xu, L. Qian, Z. Dai, Photosensitizer nanoparticles boost photodynamic therapy for pancreatic cancer treatment. Nano-Micro Lett. 13, 35 (2021). https://doi.org/10.1007/s40820-020-00561-8
  6. Q. Liu, A. Zhang, R. Wang, Q. Zhang, D. Cui, A review on metal- and metal oxide-based nanozymes: properties, mechanisms, and applications. Nano-Micro Lett. 13, 154 (2021). https://doi.org/10.1007/s40820-021-00674-8
  7. Y. Liu, W. Zhen, Y. Wang, S. Song, H. Zhang, Na2S2O8 nanoparticles trigger antitumor immunotherapy through reactive oxygen species storm and surge of tumor osmolarity. J. Am. Chem. Soc. 142(52), 21751–21757 (2020). https://doi.org/10.1021/jacs.0c09482
  8. G. Lan, K. Ni, Z. Xu, S.S. Veroneau, Y. Song et al., Nanoscale metal–organic framework overcomes hypoxia for photodynamic therapy primed cancer immunotherapy. J. Am. Chem. Soc. 140(17), 5670–5673 (2018). https://doi.org/10.1021/jacs.8b01072
  9. D. Zhang, Z. Ye, L. Wei, H. Luo, L. Xiao, Cell membrane-coated porphyrin metal–organic frameworks for cancer cell targeting and O2-evolving photodynamic therapy. ACS Appl. Mater. Interfaces 11(43), 39594–39602 (2019). https://doi.org/10.1021/acsami.9b14084
  10. Z. He, X. Huang, C. Wang, X. Li, Y. Liu et al., A catalase-like metal-organic framework nanohybrid for O2-evolving synergistic chemoradiotherapy. Angew. Chem. Int. Ed. 58(26), 8752–8756 (2019). https://doi.org/10.1002/anie.201902612
  11. S. Fu, R. Yang, J. Ren, J. Liu, L. Zhang et al., Catalytically active CoFe2O4 nanoflowers for augmented sonodynamic and chemodynamic combination therapy with elicitation of robust immune response. ACS Nano 15(7), 11953–11969 (2021). https://doi.org/10.1021/acsnano.1c03128
  12. D. Zhang, Z. Lin, Y. Zheng, J. Song, J. Li et al., Ultrasound-driven biomimetic nanosystem suppresses tumor growth and metastasis through sonodynamic therapy, CO therapy, and indoleamine 2,3-dioxygenase inhibition. ACS Nano 14(7), 8985–8999 (2020). https://doi.org/10.1021/acsnano.0c03833
  13. S. Koyama, E.A. Akbay, Y.Y. Li, G.S. Herter-Sprie, K.A. Buczkowski et al., Adaptive resistance to therapeutic PD-1 blockade is associated with upregulation of alternative immune checkpoints. Nat. Commun. 7, 10501 (2016). https://doi.org/10.1038/ncomms10501
  14. D.Y. Torrejon, G. Abril-Rodriguez, A.S. Champhekar, J. Tsoi, K.M. Campbell et al., Overcoming genetically based resistance mechanisms to PD-1 blockade. Cancer Discov. 10, 1140–1157 (2020). https://doi.org/10.1158/2159-8290.CD-19-1409
  15. M. Das, C. Zhu, V.K. Kuchroo, Tim-3 and its role in regulating anti-tumor immunity. Immunol. Rev. 276(1), 97–111 (2017). https://doi.org/10.1111/imr.12520
  16. S.F. Ngiow, B.V. Scheidt, H. Akiba, H. Yagita, M.W. Teng et al., Anti-TIM3 antibody promotes T cell IFN-γ-mediated antitumor immunity and suppresses established tumors. Cancer Res. 71(10), 3540–3551 (2011). https://doi.org/10.1158/0008-5472.CAN-11-0096
  17. Y. Wolf, A.C. Anderson, V.K. Kuchroo, TIM3 comes of age as an inhibitory receptor. Nat. Rev. Immunol. 20, 173–185 (2020). https://doi.org/10.1038/s41577-019-0224-6
  18. J.F. Liu, L. Wu, L.L. Yang, W.W. Deng, L. Mao et al., Blockade of TIM3 relieves immunosuppression through reducing regulatory T cells in head and neck cancer. J. Exp. Clin. Cancer Res. 37, 44 (2018). https://doi.org/10.1186/s13046-018-0713-7
  19. K.O. Dixon, M. Tabaka, M.A. Schramm, S. Xiao, R. Tang et al., TIM-3 restrains anti-tumour immunity by regulating inflammasome activation. Nature 595, 101–106 (2021). https://doi.org/10.1038/s41586-021-03626-9
  20. C. Zhu, A.C. Anderson, A. Schubart, H. Xiong, J. Imitola et al., The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 6, 1245–1252 (2005). https://doi.org/10.1038/ni1271
  21. F. Liu, Y. Liu, Z. Chen, Tim-3 expression and its role in hepatocellular carcinoma. J. Hematol. Oncol. 11, 126 (2018). https://doi.org/10.1186/s13045-018-0667-4
  22. X. Fang, Q. Shang, Y. Wang, L. Jiao, T. Yao et al., Single Pt atoms confined into a metal-organic framework for efficient photocatalysis. Adv. Mater. 30(7), 1705112 (2018). https://doi.org/10.1002/adma.201705112
  23. B. Wang, Y. Dai, Y. Kong, W. Du, H. Ni et al., Tumor microenvironment-responsive Fe(III)-porphyrin nanotheranostics for tumor imaging and targeted chemodynamic-photodynamic therapy. ACS Appl. Mater. Interfaces 12(48), 53634–53645 (2020). https://doi.org/10.1021/acsami.0c14046
  24. T. Yamashita, P. Hayes, Analysis of XPS spectra of Fe2+ and Fe3+ ions in oxide materials. Appl. Surf. Sci. 254(8), 2441–2449 (2008). https://doi.org/10.1016/j.apsusc.2007.09.063
  25. L. Rao, L.L. Bu, J.H. Xu, B. Cai, G.T. Yu et al., Red blood cell membrane as a biomimetic nanocoating for prolonged circulation time and reduced accelerated blood clearance. Small 11(46), 6225–6236 (2015). https://doi.org/10.1002/smll.201502388
  26. M. Xuan, J. Shao, J. Zhao, Q. Li, L. Dai et al., Magnetic mesoporous silica nanoparticles cloaked by red blood cell membranes: applications in cancer therapy. Angew. Chem. Int. Ed. 57(21), 6049–6053 (2018). https://doi.org/10.1002/anie.201712996
  27. D. Zheng, P. Yu, Z. Wei, C. Zhong, M. Wu et al., RBC membrane camouflaged semiconducting polymer nanoparticles for near-infrared photoacoustic imaging and photothermal therapy. Nano-Micro Lett. 12, 94 (2020). https://doi.org/10.1007/s40820-020-00429-x
  28. K. Lin, Y. Cao, D. Zheng, Q. Li, H. Liu et al., Facile phase transfer of hydrophobic Fe3O4@Cu2-xS nanoparticles by red blood cell membrane for MRI and phototherapy in the second near-infrared window. J. Mater. Chem. B 8(6), 1202–1211 (2020). https://doi.org/10.1039/c9tb02766a
  29. K. Ni, T. Luo, G. Lan, A. Culbert, Y. Song, A nanoscale metal–organic framework to mediate photodynamic therapy and deliver CpG oligodeoxynucleotides to enhance antigen presentation and cancer immunotherapy. Angew. Chem. Int. Ed. 59, 1108–1112 (2019). https://doi.org/10.1002/anie.201911429
  30. C. Zhang, F. Gao, W. Wu, W.X. Qiu, L. Zhang et al., Enzyme-driven membrane-targeted chimeric peptide for enhanced tumor photodynamic immunotherapy. ACS Nano 13, 11249–11262 (2019). https://doi.org/10.1021/acsnano.9b04315
  31. Z. Meng, X. Zhou, J. Xu, X. Han, Z. Dong et al., Light-triggered in situ gelation to enable robust photodynamic- immunotherapy by repeated stimulations. Adv. Mater. 31(24), 1900927 (2019). https://doi.org/10.1002/adma.201900927
  32. C. He, X. Duan, N. Guo, C. Chan, C. Poon et al., Core-shell nanoscale coordination polymers combine chemotherapy and photodynamic therapy to potentiate checkpoint blockade cancer immunotherapy. Nat. Commun. 7, 12499 (2016). https://doi.org/10.1038/ncomms12499
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