Metal-phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stresses

Hypoxia, a prevalent characteristic of solid tumors, substantially impairs the efficacy of cancer treatments. However, there are no feasible clinical approaches for treating hypoxic tumors. Here, we develop metal-phenolic networks (CuGI) utilizing the natural glycolysis inhibitor (epigallocatechin g...

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Main Authors: Jia Liu, Zuoyu Chen, Lixue Deng, Chundong Yao, Zhixin Zhou, Cheng Zhou, Yawen Bin, Miaodeng Liu, Liping Wang, Lin Wang, Zheng Wang
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2025-05-01
Series:Bioactive Materials
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Online Access:http://www.sciencedirect.com/science/article/pii/S2452199X25000222
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author Jia Liu
Zuoyu Chen
Lixue Deng
Chundong Yao
Zhixin Zhou
Cheng Zhou
Yawen Bin
Miaodeng Liu
Liping Wang
Lin Wang
Zheng Wang
author_facet Jia Liu
Zuoyu Chen
Lixue Deng
Chundong Yao
Zhixin Zhou
Cheng Zhou
Yawen Bin
Miaodeng Liu
Liping Wang
Lin Wang
Zheng Wang
author_sort Jia Liu
collection DOAJ
description Hypoxia, a prevalent characteristic of solid tumors, substantially impairs the efficacy of cancer treatments. However, there are no feasible clinical approaches for treating hypoxic tumors. Here, we develop metal-phenolic networks (CuGI) utilizing the natural glycolysis inhibitor (epigallocatechin gallate) and the essential metal element in the human body (copper ions), specifically targeting and annihilating hypoxic cancer cells. CuGI redirects the metabolic pathway of hypoxic cancer cells from anaerobic glycolysis to oxidative phosphorylation, thereby enhancing reactive oxygen species production and promoting oligomerization of lipoylated proteins in the tricarboxylic acid cycle. Through targeted induction of oxidative and proteotoxic stresses, CuGI induces apoptosis and cuproptosis specifically in cancer cells under hypoxic conditions while sparing normal cells. Moreover, cancer cell membrane-coated CuGI (CuGI@CM) exhibits enhanced tumor penetration effect and demonstrates commendable biocompatibility, effectively suppressing colorectal tumor growth. Importantly, CuGI@CM, when combined with vascular disruptors or radiotherapy which aggravate tumor hypoxia, synergistically potentiates therapeutic efficacy. Thus, CuGI represents a specific and potent nanotherapeutic capable of selectively eliminating hypoxic tumors, offering promise in combination therapies to address tumor hypoxia.
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spelling doaj-art-8fc3c264532a4d2595e25bf3f8596a972025-08-20T03:12:38ZengKeAi Communications Co., Ltd.Bioactive Materials2452-199X2025-05-014736137710.1016/j.bioactmat.2025.01.022Metal-phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stressesJia Liu0Zuoyu Chen1Lixue Deng2Chundong Yao3Zhixin Zhou4Cheng Zhou5Yawen Bin6Miaodeng Liu7Liping Wang8Lin Wang9Zheng Wang10Research Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Hubei Key Laboratory of Regenerative Medicine and Multi-disciplinary Translational Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Hubei Provincial Engineering Research Center of Clinical Laboratory and Active Health Smart Equipment, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Corresponding author. Hubei Key Laboratory of Regenerative Medicine and Multi-disciplinary Translational Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China.Department of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, ChinaResearch Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Department of Clinical Laboratory, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, ChinaResearch Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Department of Clinical Laboratory, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, ChinaResearch Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Department of Clinical Laboratory, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, ChinaDepartment of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, ChinaHubei Key Laboratory of Precision Radiation Oncology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, ChinaResearch Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Department of Clinical Laboratory, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, ChinaResearch Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Department of Clinical Laboratory, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, ChinaResearch Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Department of Clinical Laboratory, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Hubei Key Laboratory of Regenerative Medicine and Multi-disciplinary Translational Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Hubei Provincial Engineering Research Center of Clinical Laboratory and Active Health Smart Equipment, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Corresponding author. Department of Clinical Laboratory, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China.Research Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Department of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Hubei Key Laboratory of Regenerative Medicine and Multi-disciplinary Translational Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Hubei Provincial Engineering Research Center of Clinical Laboratory and Active Health Smart Equipment, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Corresponding author. Research Center for Tissue Engineering and Regenerative Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China.Hypoxia, a prevalent characteristic of solid tumors, substantially impairs the efficacy of cancer treatments. However, there are no feasible clinical approaches for treating hypoxic tumors. Here, we develop metal-phenolic networks (CuGI) utilizing the natural glycolysis inhibitor (epigallocatechin gallate) and the essential metal element in the human body (copper ions), specifically targeting and annihilating hypoxic cancer cells. CuGI redirects the metabolic pathway of hypoxic cancer cells from anaerobic glycolysis to oxidative phosphorylation, thereby enhancing reactive oxygen species production and promoting oligomerization of lipoylated proteins in the tricarboxylic acid cycle. Through targeted induction of oxidative and proteotoxic stresses, CuGI induces apoptosis and cuproptosis specifically in cancer cells under hypoxic conditions while sparing normal cells. Moreover, cancer cell membrane-coated CuGI (CuGI@CM) exhibits enhanced tumor penetration effect and demonstrates commendable biocompatibility, effectively suppressing colorectal tumor growth. Importantly, CuGI@CM, when combined with vascular disruptors or radiotherapy which aggravate tumor hypoxia, synergistically potentiates therapeutic efficacy. Thus, CuGI represents a specific and potent nanotherapeutic capable of selectively eliminating hypoxic tumors, offering promise in combination therapies to address tumor hypoxia.http://www.sciencedirect.com/science/article/pii/S2452199X25000222Tumor hypoxiaMetal-organic networksCell metabolismReactive oxygen speciesCuproptosis
spellingShingle Jia Liu
Zuoyu Chen
Lixue Deng
Chundong Yao
Zhixin Zhou
Cheng Zhou
Yawen Bin
Miaodeng Liu
Liping Wang
Lin Wang
Zheng Wang
Metal-phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stresses
Bioactive Materials
Tumor hypoxia
Metal-organic networks
Cell metabolism
Reactive oxygen species
Cuproptosis
title Metal-phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stresses
title_full Metal-phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stresses
title_fullStr Metal-phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stresses
title_full_unstemmed Metal-phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stresses
title_short Metal-phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stresses
title_sort metal phenolic networks specifically eliminate hypoxic tumors by instigating oxidative and proteotoxic stresses
topic Tumor hypoxia
Metal-organic networks
Cell metabolism
Reactive oxygen species
Cuproptosis
url http://www.sciencedirect.com/science/article/pii/S2452199X25000222
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