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Research Article

Ferric iron coordinated cisplatin prodrug reprograms the immune-cold tumor microenvironment through tumor hypoxia relief for enhanced cancer photodynamic-immunotherapy

Yinchu Ma1,2,§( ), Yingli Luo1,§, Xinfeng Tang3, Wei Jiang3, Hongjun Li4( ), Jilong Wang5( )
Wuxi School of Medicine, Jiangnan University, Wuxi 214122, China
Zhuhai Interventional Medical Center, Zhuhai Precision Medical Center, Zhuhai People's Hospital, Zhuhai Hospital Affiliated with Jinan University, Zhuhai 519000, China
School of Life Sciences, University of Science and Technology of China, Hefei 230027, China
Key Laboratory of Advanced Drug Delivery Systems of Zhejiang Province, College of Pharmaceutical Sciences, Zhejiang University, Hangzhou 310058, China
Joint Centre of Translational Medicine, Wenzhou Institute, University of Chinese Academy of Sciences, Wenzhou 325000, China

§ Yinchu Ma and Yingli Luo contributed equally to this work.

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Graphical Abstract

Nanoparticle assembled from the Fe3+ and cisplatin prodrug can catalyze oxygen production from hydrogen peroxide in tumor cells, which in turn sensitizes the photodynamic effect of Ce6 to initiate the immunogenic cell death and activate the anti-tumor immune response.

Abstract

The microenvironment of hypoxia and immune-cold limits the therapeutic outcomes of immune checkpoint blockade (ICB) therapy in solid tumors. It is important and imperative to search new strategies to relieve tumor hypoxia and reverse immunosuppression of cold tumors. In this study, the oxygen (O2) self-replenishing nano-enabled coordination platform can be used to induce potent antitumor immune response in cold tumors. The nanoplatform can produce O2 by catalyzing hydrogen peroxide (H2O2) in tumor site effectively, showing excellent photodynamic therapy (PDT) performance. Meanwhile, it can further trigger immunogenic cell death (ICD), enhance T cell infiltration, reverse immunosuppression, and reprogram the immune-cold tumor microenvironment. In vitro and in vivo results demonstrate that the nanoplatform has potential for eradicating tumors and long-term immunological memory effect. The nanoplatform opens up a strategy for reprograming the immunosuppressive microenvironment in cold tumors.

Keywords

immunogenic cell deathimmune responsereprograming cold tumor microenvironmentlong-term immunological memory effect

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References

[1]

Chowell, D.; Yoo, S. K.; Valero, C.; Pastore, A.; Krishna, C.; Lee, M.; Hoen, D.; Shi, H. Y.; Kelly, D. W.; Patel, N. et al. Improved prediction of immune checkpoint blockade efficacy across multiple cancer types. Nat. Biotechnol. 2022, 40, 499–506.
Crossref Google Scholar
[2]

Huang, A. C.; Zappasodi, R. A decade of checkpoint blockade immunotherapy in melanoma: Understanding the molecular basis for immune sensitivity and resistance. Nat. Immunol. 2022, 23, 660–670.
Crossref Google Scholar
[3]

Anagnostou, V.; Bardelli, A.; Chan, T. A.; Turajlic, S. The status of tumor mutational burden and immunotherapy. Nat. Cancer 2022, 3, 652–656.
Crossref Google Scholar
[4]

de Miguel, M.; Calvo, E. Clinical challenges of immune checkpoint inhibitors. Cancer Cell 2020, 38, 326–333.
Crossref Google Scholar
[5]

Kalbasi, A.; Ribas, A. Tumour-intrinsic resistance to immune checkpoint blockade. Nat. Rev. Immunol. 2020, 20, 25–39.
Crossref Google Scholar
[6]

Li, L.; Li, Y. C.; Yang, C. H.; Radford, D. C.; Wang, J. W.; Janát-Amsbury, M.; Kopeček, J.; Yang, J. Y. Inhibition of immunosuppressive tumors by polymer-assisted inductions of immunogenic cell death and multivalent PD-L1 crosslinking. Adv. Funct. Mater. 2020, 30, 1908961.
Crossref Google Scholar
[7]

Galon, J.; Bruni, D. Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat. Rev. Drug Discov. 2019, 18, 197–218.
Crossref Google Scholar
[8]

Yang, Z.; Gao, D.; Guo, X. Q.; Jin, L.; Zheng, J. J.; Wang, Y.; Chen, S. J.; Zheng, X. W.; Zeng, L.; Guo, M. et al. Fighting immune cold and reprogramming immunosuppressive tumor microenvironment with red blood cell membrane-camouflaged nanobullets. ACS Nano 2020, 14, 17442–17457.
Crossref Google Scholar
[9]

Li, Y. H.; Liu, X. H.; Zhang, X.; Pan, W.; Li, N.; Tang, B. Immune cycle-based strategies for cancer immunotherapy. Adv. Funct. Mater. 2021, 31, 2107540.
Crossref Google Scholar
[10]

Haanen, J. B. A. G. Converting cold into hot tumors by combining immunotherapies. Cell 2017, 170, 1055–1056.
Crossref Google Scholar
[11]

Chen, G. J.; Chen, Z. T.; Wen, D.; Wang, Z. J.; Li, H. J.; Zeng, Y.; Dotti, G.; Wirz, R. E.; Gu, Z. Transdermal cold atmospheric plasma-mediated immune checkpoint blockade therapy. Proc. Natl. Acad. Sci. USA 2020, 117, 3687–3692.
Crossref Google Scholar
[12]

Wang, C.; Wang, J. Q.; Zhang, X. D.; Yu, S. J.; Wen, D.; Hu, Q. Y.; Ye, Y. Q.; Bomba, H.; Hu, X. L.; Liu, Z. et al. In situ formed reactive oxygen species-responsive scaffold with gemcitabine and checkpoint inhibitor for combination therapy. Sci. Transl. Med. 2018, 10, eaan3682.
Crossref Google Scholar
[13]

Galluzzi, L.; Buqué, A.; Kepp, O.; Zitvogel, L.; Kroemer, G. Immunogenic cell death in cancer and infectious disease. Nat. Rev. Immunol. 2017, 17, 97–111.
Crossref Google Scholar
[14]

Xie, L. S.; Wang, G. H.; Sang, W.; Li, J.; Zhang, Z.; Li, W. X.; Yan, J.; Zhao, Q.; Dai, Y. L. Phenolic immunogenic cell death nanoinducer for sensitizing tumor to PD-1 checkpoint blockade immunotherapy. Biomaterials 2021, 269, 120638.
Crossref Google Scholar
[15]

Yang, W. J.; Zhang, F. W.; Deng, H. Z.; Lin, L. S.; Wang, S.; Kang, F.; Yu, G. C.; Lau, J.; Tian, R.; Zhang, M. R. et al. Smart nanovesicle-mediated immunogenic cell death through tumor microenvironment modulation for effective photodynamic immunotherapy. ACS Nano 2020, 14, 620–631.
Crossref Google Scholar
[16]

Li, J. B.; Cai, W. X.; Yu, J.; Zhou, S.; Li, X. L.; He, Z. G.; Ouyang, D. F.; Liu, H. Z.; Wang, Y. J. Autophagy inhibition recovers deficient ICD-based cancer immunotherapy. Biomaterials 2022, 287, 121651.
Crossref Google Scholar
[17]

Jin, L. J.; Shen, S.; Huang, Y. J.; Li, D. D.; Yang, X. Z. Corn-like Au/Ag nanorod-mediated NIR-II photothermal/photodynamic therapy potentiates immune checkpoint antibody efficacy by reprogramming the cold tumor microenvironment. Biomaterials 2021, 268, 120582.
Crossref Google Scholar
[18]

Tang, H. L.; Xu, X. J.; Chen, Y. X.; Xin, H. H.; Wan, T.; Li, B. W.; Pan, H. M.; Li, D.; Ping, Y. Reprogramming the tumor microenvironment through second-near-infrared-window photothermal genome editing of PD-L1 mediated by supramolecular gold nanorods for enhanced cancer immunotherapy. Adv. Mater. 2021, 33, 2006003.
Crossref Google Scholar
[19]

Ding, F. X.; Li, F.; Tang, D. S.; Wang, B.; Liu, J. Y.; Mao, X. Y.; Yin, J. Y.; Xiao, H. H.; Wang, J.; Liu, Z. Q. Restoration of the immunogenicity of tumor cells for enhanced cancer therapy via nanoparticle-mediated copper chaperone inhibition. Angew. Chem., Int. Ed. 2022, 61, e202203546.
Crossref Google Scholar
[20]

Jiang, W.; Wang, L.; Wang, Q.; Zhou, H.; Ma, Y. C.; Dong, W.; Xu, H. X.; Wang, Y. C. Reversing immunosuppression in hypoxic and immune-cold tumors with ultrathin oxygen self-supplementing polymer nanosheets under near infrared light irradiation. Adv. Funct. Mater. 2021, 31, 2100354.
Crossref Google Scholar
[21]

Ma, Y. C.; Zhang, Y. X.; Li, X. Q.; Zhao, Y. Y.; Li, M.; Jiang, W.; Tang, X. F.; Dou, J. X.; Lu, L. G.; Wang, F. et al. Near-infrared II phototherapy induces deep tissue immunogenic cell death and potentiates cancer immunotherapy. ACS Nano 2019, 13, 11967–11980.
Crossref Google Scholar
[22]

Sun, S.; Chen, Q.; Tang, Z. D.; Liu, C.; Li, Z. J.; Wu, A. G.; Lin, H. W. Tumor microenvironment stimuli-responsive fluorescence imaging and synergistic cancer therapy by carbon-dot-Cu2+ nanoassemblies. Angew. Chem., Int. Ed. 2020, 59, 21041–21048.
Crossref Google Scholar
[23]

Wang, Y. X.; Ding, Y. W.; Yao, D.; Dong, H.; Ji, C. W.; Wu, J. H.; Hu, Y. Q.; Yuan, A. H. Copper-based nanoscale coordination polymers augmented tumor radioimmunotherapy for immunogenic cell death induction and T-cell infiltration. Small 2021, 17, 2006231.
Crossref Google Scholar
[24]

Zhao, L. P.; Zheng, R. R.; Liu, L. S.; Chen, X. Y.; Guan, R. T.; Yang, N.; Chen, A. L.; Yu, X. Y.; Cheng, H.; Li, S. Y. Self-delivery oxidative stress amplifier for chemotherapy sensitized immunotherapy. Biomaterials 2021, 275, 120970.
Crossref Google Scholar
[25]

Xie, Q.; Li, Z.; Liu, Y.; Zhang, D. W.; Su, M.; Niitsu, H.; Lu, Y. Y.; Coffey, R. J.; Bai, M. F. Translocator protein-targeted photodynamic therapy for direct and abscopal immunogenic cell death in colorectal cancer. Acta Biomater. 2021, 134, 716–729.
Crossref Google Scholar
[26]

Liu, H. J.; Hu, Y.; Sun, Y. J.; Wan, C.; Zhang, Z. J.; Dai, X. M.; Lin, Z. H.; He, Q. Y.; Yang, Z.; Huang, P. et al. Co-delivery of bee venom melittin and a photosensitizer with an organic-inorganic hybrid nanocarrier for photodynamic therapy and immunotherapy. ACS Nano 2019, 13, 12638–12652.
Crossref Google Scholar
[27]

Jin, F. Y.; Qi, J.; Liu, D.; You, Y. C.; Shu, G. F.; Du, Y.; Wang, J.; Xu, X. L.; Ying, X. Y.; Ji, J. S. et al. Cancer-cell-biomimetic Upconversion nanoparticles combining chemo-photodynamic therapy and CD73 blockade for metastatic triple-negative breast cancer. J. Control. Release 2021, 337, 90–104.
Crossref Google Scholar
[28]

Wei, D. S.; Chen, Y. B.; Huang, Y.; Li, P.; Zhao, Y.; Zhang, X. H.; Wan, J.; Yin, X. Y.; Liu, T.; Yin, J. Y. et al. NIR-light triggered dual-cascade targeting core-shell nanoparticles enhanced photodynamic therapy and immunotherapy. Nano Today 2021, 41, 101288.
Crossref Google Scholar
[29]

Liu, X.; Liu, Y.; Li, X.; Huang, J. X.; Guo, X. M.; Zhang, J. L.; Luo, Z. Y.; Shi, Y. Y.; Jiang, M. S.; Qin, B. et al. ER-targeting PDT converts tumors into in situ therapeutic tumor vaccines. ACS Nano 2022, 16, 9240–9253.
Crossref Google Scholar
[30]

Huang, J.; Xiao, Z. C.; Chen, G. J.; Li, T.; Peng, Y.; Shuai, X. T. A pH-sensitive nanomedicine incorporating catalase gene and photosensitizer augments photodynamic therapy and activates antitumor immunity. Nano Today 2022, 43, 101390.
Crossref Google Scholar
[31]

Hu, L. Q.; Cao, Z. Y.; Ma, L. L.; Liu, Z. Q.; Liao, G. C.; Wang, J. X.; Shen, S.; Li, D. D.; Yang, X. Z. The potentiated checkpoint blockade immunotherapy by ROS-responsive nanocarrier-mediated cascade chemo-photodynamic therapy. Biomaterials 2019, 223, 119469.
Crossref Google Scholar
[32]

Lou, X.; Wang, H.; Liu, Y.; Huang, Y. W.; Liu, Z. H.; Zhang, W.; Wang, T. Perylene-based reactive oxygen species supergenerator for immunogenic photochemotherapy against hypoxic tumors. Angew. Chem., Int. Ed. 2023, 62, e202214586.
Crossref Google Scholar
[33]

Liu, L. L.; He, H. M.; Luo, Z. Y.; Zhou, H. M.; Liang, R. J.; Pan, H.; Ma, Y. F.; Cai, L. T. In situ photocatalyzed oxygen generation with photosynthetic bacteria to enable robust immunogenic photodynamic therapy in triple-negative breast cancer. Adv. Funct. Mater. 2020, 30, 1910176.
Crossref Google Scholar
[34]

Zhou, Z. G.; Liu, Y.; Song, W.; Jiang, X.; Deng, Z. A.; Xiong, W.; Shen, J. L. Metabolic reprogramming mediated PD-L1 depression and hypoxia reversion to reactivate tumor therapy. J. Control. Release 2022, 352, 793–812.
Crossref Google Scholar
[35]

Zhang, S. W.; Wang, J.; Kong, Z. Q.; Sun, X. X.; He, Z. G.; Sun, B. J.; Luo, C.; Sun, J. Emerging photodynamic nanotherapeutics for inducing immunogenic cell death and potentiating cancer immunotherapy. Biomaterials 2022, 282, 121433.
Crossref Google Scholar
[36]

You, Q.; Zhang, K. Y.; Liu, J. Y.; Liu, C. L.; Wang, H. Y.; Wang, M. T.; Ye, S. Y.; Gao, H. Q.; Lv, L. T.; Wang, C. et al. Persistent regulation of tumor hypoxia microenvironment via a bioinspired Pt-based oxygen nanogenerator for multimodal imaging-guided synergistic phototherapy. Adv. Sci. 2020, 7, 1903341.
Crossref Google Scholar
[37]

Hou, G. H.; Qian, J. M.; Guo, M.; Xu, W. J.; Wang, J. L.; Wang, Y. P.; Suo, A. L. Copper coordinated nanozyme-assisted photodynamic therapy for potentiating PD-1 blockade through amplifying oxidative stress. Chem. Eng. J. 2022, 435, 134778.
Crossref Google Scholar
[38]

Zhang, Y. F.; Liao, Y. Y.; Tang, Q. N.; Lin, J.; Huang, P. Biomimetic nanoemulsion for synergistic photodynamic-immunotherapy against hypoxic breast tumor. Angew. Chem., Int. Ed. 2021, 60, 10647–10653.
Crossref Google Scholar
[39]

He, L. Y.; Wang, J. F.; Zhu, P. Y.; Chen, J. M.; Zhao, S. J.; Liu, X. X.; Li, Y. N.; Guo, X. L.; Yan, Z. H.; Shen, X. et al. Intelligent manganese dioxide nanocomposites induce tumor immunogenic cell death and remould tumor microenvironment. Chem. Eng. J. 2023, 461, 141369.
Crossref Google Scholar
[40]

Huang, C.; Lin, B. Q.; Chen, C. Y.; Wang, H. M.; Lin, X. S.; Liu, J. M.; Ren, Q. F.; Tao, J.; Zhao, P.; Xu, Y. K. Synergistic reinforcing of immunogenic cell death and transforming tumor-associated macrophages via a multifunctional cascade bioreactor for optimizing cancer immunotherapy. Adv. Mater. 2022, 34, 2207593.
Crossref Google Scholar
[41]

Liu, L. H.; Zhang, Y. H.; Qiu, W. X.; Zhang, L.; Gao, F.; Li, B.; Xu, L.; Fan, J. X.; Li, Z. H.; Zhang, X. Z. Dual-stage light amplified photodynamic therapy against hypoxic tumor based on an O2 self-sufficient nanoplatform. Small 2017, 13, 1701621.
Crossref Google Scholar
[42]

Huang, L.; Zhao, S. J.; Wu, J. S.; Yu, L.; Singh, N.; Yang, K.; Lan, M. H.; Wang, P. F.; Kim, J. S. Photodynamic therapy for hypoxic tumors: Advances and perspectives. Coordin. Chem. Rev. 2021, 438, 213888.
Crossref Google Scholar
[43]

Shi, C.; Li, M. L.; Zhang, Z.; Yao, Q. C.; Shao, K.; Xu, F.; Xu, N.; Li, H. D.; Fan, J. L.; Sun, W. et al. Catalase-based liposomal for reversing immunosuppressive tumor microenvironment and enhanced cancer chemo-photodynamic therapy. Biomaterials 2020, 233, 119755.
Crossref Google Scholar
[44]

Hao, H. S.; Yu, M.; Yi, Y. F.; Sun, S. J.; Huang, X. Y.; Huang, C. Y.; Liu, Y. Q.; Huang, W. X.; Wang, J. Q.; Zhao, J. et al. Mesoporous calcium peroxide-ignited NO generation for amplifying photothermal immunotherapy of breast cancer. Chem. Eng. J. 2022, 437, 135371.
Crossref Google Scholar
[45]

Wu, W. C.; Pu, Y. Y.; Zhou, B. G.; Shen, Y. C.; Gao, S.; Zhou, M.; Shi, J. L. Photoactivatable immunostimulatory nanomedicine for immunometabolic cancer therapy. J. Am. Chem. Soc. 2022, 144, 19038–19050.
Crossref Google Scholar
[46]

Wang, D. D.; Wu, H. H.; Phua, S. Z. F.; Yang, G. B.; Lim, W. Q.; Gu, L.; Qian, C.; Wang, H. B.; Guo, Z.; Chen, H. Z. et al. Self-assembled single-atom nanozyme for enhanced photodynamic therapy treatment of tumor. Nat. Commun. 2020, 11, 357.
Crossref Google Scholar
[47]

Zhang, L.; Yang, Z.; Ren, J. H.; Ba, L.; He, W. S.; Wong, C. Y. Multifunctional oxygen-enriching nano-theranostics for cancer-specific magnetic resonance imaging and enhanced photodynamic/photothermal therapy. Nano Res. 2020, 13, 1389–1398.
Crossref Google Scholar
[48]

Liu, J. J.; Wu, M.; Pan, Y. T.; Duan, Y. K.; Dong, Z. L.; Chao, Y.; Liu, Z.; Liu, B. Biodegradable nanoscale coordination polymers for targeted tumor combination therapy with oxidative stress amplification. Adv. Funct. Mater. 2020, 30, 1908865.
Crossref Google Scholar
[49]

He, C. B.; Liu, D. M.; Lin, W. B. Nanomedicine applications of hybrid nanomaterials built from metal-ligand coordination bonds: Nanoscale metal-organic frameworks and nanoscale coordination polymers. Chem. Rev. 2015, 115, 11079–11108.
Crossref Google Scholar
[50]

Lan, G. X.; Ni, K. Y.; Lin, W. B. Nanoscale metal-organic frameworks for phototherapy of cancer. Coordin. Chem. Rev. 2019, 379, 65–81.
Crossref Google Scholar
[51]

Huang, Z. S.; Wang, Y. X.; Yao, D.; Wu, J. H.; Hu, Y. Q.; Yuan, A. H. Nanoscale coordination polymers induce immunogenic cell death by amplifying radiation therapy mediated oxidative stress. Nat. Commun. 2021, 12, 145.
Crossref Google Scholar
[52]

Liu, P.; Zhu, H. J.; Wang, M. Z.; Wei, M. J.; Liu, B. X.; Hu, P. W.; Lin, J. X.; Niu, X. H. Bimodal ratiometric fluorescence and colorimetric sensing of paraoxon based on trifunctional Ce, Tb co-coordinated polymers. Sens. Actuat. B: Chem. 2022, 360, 131616.
Crossref Google Scholar
[53]

Meng, T. J.; Shang, N. Z.; Zhao, J. N.; Su, M.; Wang, C.; Zhang, Y. F. Facile one-pot synthesis of Co coordination polymer spheres doped macroporous carbon and its application for electrocatalytic oxidation of glucose. J. Colloid Interf Sci. 2021, 589, 135–146.
Crossref Google Scholar
[54]

Zhang, Y. Z.; Cui, H. G.; Zhang, R. Q.; Zhang, H. B.; Huang, W. Nanoparticulation of prodrug into medicines for cancer therapy. Adv. Sci. 2021, 8, 2101454.
Crossref Google Scholar
[55]

Liu, J. J.; Chen, Q.; Zhu, W. W.; Yi, X.; Yang, Y.; Dong, Z. L.; Liu, Z. Nanoscale-coordination-polymer-shelled manganese dioxide composite nanoparticles: A multistage redox/pH/H2O2-responsive cancer theranostic nanoplatform. Adv. Funct. Mater. 2017, 27, 1605926.
Crossref Google Scholar
[56]

Wang, J. L.; Huang, M. W.; Chen, S. B.; Luo, Y. L.; Shen, S.; Du, X. J. Nanomedicine-mediated ubiquitination inhibition boosts antitumor immune response via activation of dendritic cells. Nano Res. 2021, 14, 3900–3906.
Crossref Google Scholar
[57]

Jiang, W.; Dong, W.; Li, M.; Guo, Z. X.; Wang, Q.; Liu, Y.; Bi, Y. H.; Zhou, H.; Wang, Y. C. Nitric oxide induces immunogenic cell death and potentiates cancer immunotherapy. ACS Nano 2022, 16, 3881–3894.
Crossref Google Scholar
Nano Research
Volume 16 Issue 7,
July 2023
Pages 9930-9939
DOI: 10.1007/s12274-023-5919-0
Cite this article:
Ma Y, Luo Y, Tang X, et al. Ferric iron coordinated cisplatin prodrug reprograms the immune-cold tumor microenvironment through tumor hypoxia relief for enhanced cancer photodynamic-immunotherapy. Nano Research, 2023, 16(7): 9930-9939. https://doi.org/10.1007/s12274-023-5919-0
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Received: 23 March 2023
Revised: 09 June 2023
Accepted: 12 June 2023
Published: 30 June 2023
© Tsinghua University Press 2023
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