Switchable ROS generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic/immune therapy

Acute kidney injury (AKI) induced by cisplatin (DDP), which is accompanied with the generation of reactive oxygen species (ROS), is a severe side effect during treatment and restricts the application of DDP. In this study, we develop ultrasmall Mn3O4 nanozyme (UMON) with tumor microenvironment (TME)...

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Main Authors: Yanan Ren, Fei Wu, Linlin Huo, Xiao Wang, Yong Zhang, Mengke Fan, Mingya Tan, Jiayi Zhao, Jingliang Cheng, Zhenghuan Zhao, Jianfeng Bao
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Materials Today Bio
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Online Access:http://www.sciencedirect.com/science/article/pii/S2590006424003892
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author Yanan Ren
Fei Wu
Linlin Huo
Xiao Wang
Yong Zhang
Mengke Fan
Mingya Tan
Jiayi Zhao
Jingliang Cheng
Zhenghuan Zhao
Jianfeng Bao
author_facet Yanan Ren
Fei Wu
Linlin Huo
Xiao Wang
Yong Zhang
Mengke Fan
Mingya Tan
Jiayi Zhao
Jingliang Cheng
Zhenghuan Zhao
Jianfeng Bao
author_sort Yanan Ren
collection DOAJ
description Acute kidney injury (AKI) induced by cisplatin (DDP), which is accompanied with the generation of reactive oxygen species (ROS), is a severe side effect during treatment and restricts the application of DDP. In this study, we develop ultrasmall Mn3O4 nanozyme (UMON) with tumor microenvironment (TME) responsive ROS scavenging and generating as adjuvant to alleviate DDP induced AKI with improved efficacy. In kidney, UMON with superoxide dismutase and catalase activity acts as ROS scavenger to eliminate ROS generated by DDP, successfully protecting the renal cells/tissue and alleviating AKI during DDP treatment. Alternatively, UMON rapidly responses to the high GSH level in TME and release Mn2+ in tumor. This unique feature endows it to generate hydroxyl radicals (∙OH) through a Fenton-like reaction and deplete GSH in tumor cell and tissue, achieving high efficient chemodynamic therapy (CDT). More importantly, the Mn2+ successfully activates the cGAS-STING pathway, initiating the immune response and effectively inhibiting the tumor metastases. The synergistic CDT and immune therapy effectively improve the anti-tumor efficacy of DDP in vitro and in vivo. This study demonstrates that TME responsive ROS scavenger/generator shows the potential to reduce side effects of DDP while improve its therapeutic efficacy, providing a new avenue to achieve efficient chemotherapy and promoting the progress of clinical chemotherapy.
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spelling doaj-art-5320faec67b949fb9d8052f4f5c4a7c92024-12-14T06:32:18ZengElsevierMaterials Today Bio2590-00642024-12-0129101328Switchable ROS generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic/immune therapyYanan Ren0Fei Wu1Linlin Huo2Xiao Wang3Yong Zhang4Mengke Fan5Mingya Tan6Jiayi Zhao7Jingliang Cheng8Zhenghuan Zhao9Jianfeng Bao10Functional Magnetic Resonance and Molecular Imaging Key Laboratory of Henan Province, Department of Magnetic Resonance Imaging, First Affiliated Hospital of Zhengzhou University, Zhengzhou University, Zhengzhou, 450001, ChinaFunctional Magnetic Resonance and Molecular Imaging Key Laboratory of Henan Province, Department of Magnetic Resonance Imaging, First Affiliated Hospital of Zhengzhou University, Zhengzhou University, Zhengzhou, 450001, ChinaCollege of Basic Medical Sciences, Chongqing Medical University, Chongqing, 400016, ChinaFunctional Magnetic Resonance and Molecular Imaging Key Laboratory of Henan Province, Department of Magnetic Resonance Imaging, First Affiliated Hospital of Zhengzhou University, Zhengzhou University, Zhengzhou, 450001, ChinaFunctional Magnetic Resonance and Molecular Imaging Key Laboratory of Henan Province, Department of Magnetic Resonance Imaging, First Affiliated Hospital of Zhengzhou University, Zhengzhou University, Zhengzhou, 450001, ChinaCollege of Basic Medical Sciences, Chongqing Medical University, Chongqing, 400016, ChinaCollege of Basic Medical Sciences, Chongqing Medical University, Chongqing, 400016, ChinaCollege of Basic Medical Sciences, Chongqing Medical University, Chongqing, 400016, ChinaFunctional Magnetic Resonance and Molecular Imaging Key Laboratory of Henan Province, Department of Magnetic Resonance Imaging, First Affiliated Hospital of Zhengzhou University, Zhengzhou University, Zhengzhou, 450001, China; Corresponding author.College of Basic Medical Sciences, Chongqing Medical University, Chongqing, 400016, China; Corresponding author.Functional Magnetic Resonance and Molecular Imaging Key Laboratory of Henan Province, Department of Magnetic Resonance Imaging, First Affiliated Hospital of Zhengzhou University, Zhengzhou University, Zhengzhou, 450001, China; Corresponding author.Acute kidney injury (AKI) induced by cisplatin (DDP), which is accompanied with the generation of reactive oxygen species (ROS), is a severe side effect during treatment and restricts the application of DDP. In this study, we develop ultrasmall Mn3O4 nanozyme (UMON) with tumor microenvironment (TME) responsive ROS scavenging and generating as adjuvant to alleviate DDP induced AKI with improved efficacy. In kidney, UMON with superoxide dismutase and catalase activity acts as ROS scavenger to eliminate ROS generated by DDP, successfully protecting the renal cells/tissue and alleviating AKI during DDP treatment. Alternatively, UMON rapidly responses to the high GSH level in TME and release Mn2+ in tumor. This unique feature endows it to generate hydroxyl radicals (∙OH) through a Fenton-like reaction and deplete GSH in tumor cell and tissue, achieving high efficient chemodynamic therapy (CDT). More importantly, the Mn2+ successfully activates the cGAS-STING pathway, initiating the immune response and effectively inhibiting the tumor metastases. The synergistic CDT and immune therapy effectively improve the anti-tumor efficacy of DDP in vitro and in vivo. This study demonstrates that TME responsive ROS scavenger/generator shows the potential to reduce side effects of DDP while improve its therapeutic efficacy, providing a new avenue to achieve efficient chemotherapy and promoting the progress of clinical chemotherapy.http://www.sciencedirect.com/science/article/pii/S2590006424003892Switchable ROS scavenger/generatorCisplatin adjuvantAcute kidney injuryImproved therapeutic efficacy
spellingShingle Yanan Ren
Fei Wu
Linlin Huo
Xiao Wang
Yong Zhang
Mengke Fan
Mingya Tan
Jiayi Zhao
Jingliang Cheng
Zhenghuan Zhao
Jianfeng Bao
Switchable ROS generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic/immune therapy
Materials Today Bio
Switchable ROS scavenger/generator
Cisplatin adjuvant
Acute kidney injury
Improved therapeutic efficacy
title Switchable ROS generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic/immune therapy
title_full Switchable ROS generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic/immune therapy
title_fullStr Switchable ROS generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic/immune therapy
title_full_unstemmed Switchable ROS generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic/immune therapy
title_short Switchable ROS generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic/immune therapy
title_sort switchable ros generator and scavenger to prevent the cisplatin induced acute kidney injury and improve efficacy via synergistic chemodynamic immune therapy
topic Switchable ROS scavenger/generator
Cisplatin adjuvant
Acute kidney injury
Improved therapeutic efficacy
url http://www.sciencedirect.com/science/article/pii/S2590006424003892
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