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Single-Atom Nanocatalytic Therapy for Suppression of Neuroinflammation by Inducing Autophagy of Abnormal Mitochondria

  • Bowen Li
    Bowen Li
    Academy of Medical Engineering and Translational Medicine, Tianjin Key Laboratory of Brain Science and Neural Engineering, Xincheng Hospital of Tianjin University, Tianjin University, Tianjin 300072, China
    More by Bowen Li
  • Yang Bai
    Yang Bai
    Department of Stomatology, Tianjin Medical University General Hospital, 154 Anshan Road, Heping District, Tianjin 300052, China
    More by Yang Bai
  • Chan Yion
    Chan Yion
    Academy of Medical Engineering and Translational Medicine, Tianjin Key Laboratory of Brain Science and Neural Engineering, Xincheng Hospital of Tianjin University, Tianjin University, Tianjin 300072, China
    More by Chan Yion
  • Hua Wang
    Hua Wang
    School of Pharmaceutical Science and Technology, Tianjin University, 92 Weijin Road, Nankai District, Tianjin 300072, China
    More by Hua Wang
  • Xin Su
    Xin Su
    School of Life Sciences, Tianjin University, 92 Weijin Road, Nankai District, Tianjin 300072, China
    More by Xin Su
  • Guoqing Feng
    Guoqing Feng
    Academy of Medical Engineering and Translational Medicine, Tianjin Key Laboratory of Brain Science and Neural Engineering, Xincheng Hospital of Tianjin University, Tianjin University, Tianjin 300072, China
    More by Guoqing Feng
  • Mingming Guo
    Mingming Guo
    Academy of Medical Engineering and Translational Medicine, Tianjin Key Laboratory of Brain Science and Neural Engineering, Xincheng Hospital of Tianjin University, Tianjin University, Tianjin 300072, China
    More by Mingming Guo
  • Wenchang Peng
    Wenchang Peng
    Academy of Medical Engineering and Translational Medicine, Tianjin Key Laboratory of Brain Science and Neural Engineering, Xincheng Hospital of Tianjin University, Tianjin University, Tianjin 300072, China
  • Boxi Shen
    Boxi Shen
    School of Pharmaceutical Science and Technology, Tianjin University, 92 Weijin Road, Nankai District, Tianjin 300072, China
    More by Boxi Shen
  • , and 
  • Bin Zheng*
    Bin Zheng
    Academy of Medical Engineering and Translational Medicine, Tianjin Key Laboratory of Brain Science and Neural Engineering, Xincheng Hospital of Tianjin University, Tianjin University, Tianjin 300072, China
    Healthina Academy of Cellular Intelligence Manufacturing & Neurotrauma Repair of Tianjin Economic-Technological Development Area, Healthina Biomedicine (Tianjin) Co. Ltd., No. 286 AnShan West Road, NanKai District, Tianjin 300190, China
    *E-mail: [email protected]
    More by Bin Zheng
Cite this: ACS Nano 2023, 17, 8, 7511–7529
Publication Date (Web):April 5, 2023
https://doi.org/10.1021/acsnano.2c12614
Copyright © 2023 American Chemical Society

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    Abstract

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    Catalysts have achieved efficacy in scavenging reactive oxygen species (ROS) to eliminate neuroinflammation, but it ignores the essential fact of blocking the source of ROS regeneration. Here, we report the single-atom catalysts (SACs) Pt/CeO2, which can effectively catalyze the breakdown of existing ROS and induce mitochondrial membrane potential (Δψm) depolarization by interfering with the α-glycerophosphate shuttle pathway and malate-aspartate shuttle pathway, indirectly triggering the self-clearance of dysfunctional mitochondria and thus eradicating the source of ROS generation. In a therapeutic model of Parkinson’s disease (PD), Pt/CeO2 wrapped by neutrophil-like (HL-60) cell membranes and modified by rabies virus glycoprotein (RVG29) effectively crosses the blood–brain barrier (BBB), enters dopaminergic neurons entering the neuroinflammatory region breaking down existing ROS and inducing mitophagy by electrostatic adsorption targeting mitochondria to prevent ROS regeneration after catalyst discharge. This strategy of efficiently eliminating ROS at the lesion and fundamentally blocking the source of ROS production can address both symptoms and root causes and provides a mechanism of explanation and action target for the treatment of inflammation-related diseases.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsnano.2c12614.

    • Results from a diverse range of experimental techniques, such as transmission electron microscopy (TEM) images, dynamic light scattering (DLS) data, scanning electron microscopy (SEM) and X-ray photoelectron spectroscopy (XPS) results, as well as cytotoxicity and cell confocal experiments (PDF)

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    Cited By

    This article is cited by 3 publications.

    1. Peng Jiang, Yu Xiao, Xinmei Hu, Cancan Wang, Hongjun Gao, Hongri Huang, Junming Lv, Zhongquan Qi, Zhanxiang Wang. RVG29 Peptide-Modified Exosomes Loaded with Mir-133b Mediate the RhoA-ROCK Pathway to Improve Motor and Neurological Symptoms in Parkinson’s Disease. ACS Biomaterials Science & Engineering 2024, 10 (5) , 3069-3085. https://doi.org/10.1021/acsbiomaterials.3c01622
    2. Shuai Zha, Haitao Liu, Hengde Li, Haolan Li, Ka-Leung Wong, Angelo Homayoun All. Functionalized Nanomaterials Capable of Crossing the Blood–Brain Barrier. ACS Nano 2024, 18 (3) , 1820-1845. https://doi.org/10.1021/acsnano.3c10674
    3. Xiaoyu Xia, Han Li, Xianbing Xu, Guanghua Zhao, Ming Du. Facilitating Pro-survival Mitophagy for Alleviating Parkinson’s Disease via Sequence-Targeted Lycopene Nanodots. ACS Nano 2023, 17 (18) , 17979-17995. https://doi.org/10.1021/acsnano.3c04308