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Targeted Therapy of Atherosclerosis by a Broad-Spectrum Reactive Oxygen Species Scavenging Nanoparticle with Intrinsic Anti-inflammatory Activity

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    Targeted Therapy of Atherosclerosis by a Broad-Spectrum Reactive Oxygen Species Scavenging Nanoparticle with Intrinsic Anti-inflammatory Activity
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    • Yuquan Wang
      Yuquan Wang
      Department of Cardiology, Southwest Hospital  and  Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      Department of Cardiology, Affiliated Hospital of North Sichuan Medical College, Nanchong 637000, China
      More by Yuquan Wang
    • Lanlan Li
      Lanlan Li
      Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      More by Lanlan Li
    • Weibo Zhao
      Weibo Zhao
      Department of Cardiology, Southwest Hospital, Third Military Medical University, Chongqing 400038, China
      More by Weibo Zhao
    • Yin Dou
      Yin Dou
      Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      More by Yin Dou
    • Huijie An
      Huijie An
      Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      More by Huijie An
    • Hui Tao
      Hui Tao
      Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      More by Hui Tao
    • Xiaoqiu Xu
      Xiaoqiu Xu
      Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      More by Xiaoqiu Xu
    • Yi Jia
      Yi Jia
      Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      More by Yi Jia
    • Shan Lu
      Shan Lu
      Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      More by Shan Lu
    • Jianxiang Zhang*
      Jianxiang Zhang
      Department of Pharmaceutics, College of Pharmacy, Third Military Medical University, Chongqing 400038, China
      *E-mail: [email protected] or [email protected]
      More by Jianxiang Zhang
      Orcidhttp://orcid.org/0000-0002-0984-2947
    • Houyuan Hu*
      Houyuan Hu
      Department of Cardiology, Southwest Hospital, Third Military Medical University, Chongqing 400038, China
      *E-mail: [email protected]
      More by Houyuan Hu
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    ACS Nano

    Cite this: ACS Nano 2018, 12, 9, 8943–8960
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    https://doi.org/10.1021/acsnano.8b02037
    Published August 16, 2018
    Copyright © 2018 American Chemical Society
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    Abstract

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    Atherosclerosis is a leading cause of vascular diseases worldwide. Whereas antioxidative therapy has been considered promising for the treatment of atherosclerosis in view of a critical role of reactive oxygen species (ROS) in the pathogenesis of atherosclerosis, currently available antioxidants showed considerably limited clinical outcomes. Herein, we hypothesize that a broad-spectrum ROS-scavenging nanoparticle can serve as an effective therapy for atherosclerosis, taking advantage of its antioxidative stress activity and targeting effects. As a proof of concept, a broad-spectrum ROS-eliminating material was synthesized by covalently conjugating a superoxide dismutase mimetic agent Tempol and a hydrogen-peroxide-eliminating compound of phenylboronic acid pinacol ester onto a cyclic polysaccharide β-cyclodextrin (abbreviated as TPCD). TPCD could be easily processed into a nanoparticle (TPCD NP). The obtained nanotherapy TPCD NP could be efficiently and rapidly internalized by macrophages and vascular smooth muscle cells (VSMCs). TPCD NPs significantly attenuated ROS-induced inflammation and cell apoptosis in macrophages, by eliminating overproduced intracellular ROS. Also, TPCD NPs effectively inhibited foam cell formation in macrophages and VSMCs by decreasing internalization of oxidized low-density lipoprotein. After intravenous (i.v.) administration, TPCD NPs accumulated in atherosclerotic lesions of apolipoprotein E-deficient (ApoE–/–) mice by passive targeting through the dysfunctional endothelium and translocation via inflammatory cells. TPCD NPs significantly inhibited the development of atherosclerosis in ApoE–/– mice after i.v. delivery. More importantly, therapy with TPCD NPs afforded stabilized plaques with less cholesterol crystals, a smaller necrotic core, thicker fibrous cap, and lower macrophages and matrix metalloproteinase-9, compared with those treated with control drugs previously developed for antiatherosclerosis. The therapeutic benefits of TPCD NPs mainly resulted from reduced systemic and local oxidative stress and inflammation as well as decreased inflammatory cell infiltration in atherosclerotic plaques. Preliminary in vivo tests implied that TPCD NPs were safe after long-term treatment via i.v. injection. Consequently, TPCD NPs can be developed as a potential antiatherosclerotic nanotherapy.

    Copyright © 2018 American Chemical Society

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.8b02037.

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    Cite this: ACS Nano 2018, 12, 9, 8943–8960
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