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Reshaping Prostate Tumor Microenvironment To Suppress Metastasis via Cancer-Associated Fibroblast Inactivation with Peptide-Assembly-Based Nanosystem

  • Jiayan Lang
    Jiayan Lang
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
    Sino-Danish Center for Education and Research, Sino-Danish College of UCAS, Beijing 100190, China
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  • , 
  • Xiao Zhao
    Xiao Zhao
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
    More by Xiao Zhao
  • , 
  • Yingqiu Qi
    Yingqiu Qi
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    School of Basic Medical Sciences, Zhengzhou University, Henan 450001, China
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  • , 
  • Yinlong Zhang
    Yinlong Zhang
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
    More by Yinlong Zhang
  • , 
  • Xuexiang Han
    Xuexiang Han
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
    More by Xuexiang Han
    Orcidhttp://orcid.org/0000-0003-0011-5222
  • , 
  • Yanping Ding
    Yanping Ding
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
    More by Yanping Ding
  • , 
  • Jiajing Guan
    Jiajing Guan
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    More by Jiajing Guan
  • , 
  • Tianjiao Ji*
    Tianjiao Ji
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
    *E-mail: [email protected]
    More by Tianjiao Ji
    Orcidhttp://orcid.org/0000-0002-4479-4821
  • , 
  • Ying Zhao*
    Ying Zhao
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
    *E-mail: [email protected]
    More by Ying Zhao
  • , and 
  • Guangjun Nie*
    Guangjun Nie
    CAS Key Laboratory for Biomedical Effects of Nanomaterials & Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology, Beijing 100190, China
    Center of Materials Science and Optoelectronics Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
    *E-mail: [email protected]
    More by Guangjun Nie
    Orcidhttp://orcid.org/0000-0001-5040-9793
Cite this: ACS Nano 2019, 13, 11, 12357–12371
Publication Date (Web):September 23, 2019
https://doi.org/10.1021/acsnano.9b04857
Copyright © 2019 American Chemical Society
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    Abstract

    Abstract Image

    Prostate cancer is one of the most common malignant tumors in men, and inhibiting metastasis is a key event but still a major challenge in prostate cancer treatment. Cancer-associated fibroblasts (CAFs) play an important role in prostate tumor metastasis by shaping the malignant tumor microenvironment. Herein, we constructed a CAF-targeting siRNA delivery system by loading the fibroblast activation protein-α (FAP-α) antibody onto the cell-penetrating peptide (CPP)-based nanoparticles, which specifically downregulated C–X–C motif chemokine ligand 12 (CXCL12) expression in CAFs. This regulation generated a series of changes through inactivating CAFs so that the malignant prostate tumor microenvironment was reshaped. The tumor cell invasion, migration, and tumor angiogenesis were significantly inhibited, which all contributed to the suppression of the metastasis of an orthotopic prostate tumor. This tumor microenvironment reshaping strategy via CAF targeting and inactivation provides an alternative approach for malignant prostate tumor metastasis inhibition.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.9b04857.

    • Additional experimental data such as DLS characterization, expression changes of cytokines, cytotoxicity, and blood clearance rate shown in Tables S1–S3 and Figure S1–S9 (PDF)

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