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In Situ Nanoadjuvant-Assembled Tumor Vaccine for Preventing Long-Term Recurrence

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    In Situ Nanoadjuvant-Assembled Tumor Vaccine for Preventing Long-Term Recurrence
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    • Quoc-Viet Le
      Quoc-Viet Le
      College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul 08826, Republic of Korea
      More by Quoc-Viet Le
    • Juhan Suh
      Juhan Suh
      College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul 08826, Republic of Korea
      More by Juhan Suh
    • Jin Joo Choi
      Jin Joo Choi
      College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul 08826, Republic of Korea
      More by Jin Joo Choi
    • Gyu Thae Park
      Gyu Thae Park
      College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul 08826, Republic of Korea
      More by Gyu Thae Park
    • Jung Weon Lee
      Jung Weon Lee
      College of Pharmacy and Research Institute of Pharmaceutical Sciences,  Interdisciplinary Program in Genetic Engineering  and  Medicinal Bioconvergence Research Center, Seoul National University, Seoul 08826, Republic of Korea
      More by Jung Weon Lee
    • Gayong Shim*
      Gayong Shim
      College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul 08826, Republic of Korea
      *E-mail: [email protected]
      More by Gayong Shim
    • Yu-Kyoung Oh*
      Yu-Kyoung Oh
      College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul 08826, Republic of Korea
      *E-mail: [email protected]
      More by Yu-Kyoung Oh
      Orcidhttp://orcid.org/0000-0002-0969-3339
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    ACS Nano

    Cite this: ACS Nano 2019, 13, 7, 7442–7462
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    https://doi.org/10.1021/acsnano.9b02071
    Published June 10, 2019
    Copyright © 2019 American Chemical Society
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    Abstract

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    Although immune checkpoint inhibitors have emerged as a breakthrough in cancer therapy, a monotherapy approach is not sufficient. Here, we report an immune checkpoint inhibitor-modified nanoparticle for an in situ-assembled tumor vaccine that can activate immune systems in the tumor microenvironment and prevent the long-term recurrence of tumors. Adjuvant-loaded nanoparticles were prepared by entrapping imiquimod (IQ) in photoresponsive polydopamine nanoparticles (IQ/PNs). The surfaces of IQ/PNs were then modified with anti-PDL1 antibody (PDL1Ab-IQ/PNs) for in situ assembly with inactivated tumor cells and immune checkpoint blocking of PDL1 (programmed cell death 1 ligand 1). The presence of anti-PDL1 antibodies on IQ/PNs increased the binding of nanoparticles to CT26 cancer cells overexpressing PDL1. Subsequent near-infrared (NIR) irradiation induced a greater photothermal anticancer effect against cells treated with PDL1Ab-IQ/PNs than cells treated with plain PNs or unmodified IQ/PNs. To mimic the tumor microenvironment, we cocultured bone marrow-derived dendritic cells with CT26 cells treated with various nanoparticle formulations and NIR irradiated. This coculture study revealed that NIR-inactivated, PDL1Ab-IQ/PN-bound CT26 cells induced maturation of dendritic cells to the greatest extent. Following a single intravenous administration of different nanoparticle formulations in CT26 tumor-bearing mice, PDL1Ab-IQ/PNs showed greater tumor tissue accumulation than unmodified nanoparticles. Subsequent NIR irradiation of mice treated with PDL1Ab-IQ/PNs resulted in tumor ablation. In addition to primary tumor ablation, PDL1Ab-IQ/PNs completely prevented the growth of a secondarily challenged CT26 tumor at a distant site, producing 100% survival for up to 150 days. A long-term protection study revealed that treatment with PDL1Ab-IQ/PNs followed by NIR irradiation inhibited the growth of distant, secondarily challenged CT26 tumors 150 days after the first tumor inoculation. Moreover, increased infiltration of T cells was observed in tumor tissues treated with PDL1Ab-IQ/PNs and NIR-irradiated, and T cells isolated from splenocytes of mice in which tumor recurrence was prevented showed active killing of CT26 cells. These results suggest that PDL1Ab-IQ/PNs in conjunction with NIR irradiation induce a potent, in situ-assembled, all-in-one tumor vaccine with adjuvant-containing nanoparticle-bound, inactivated tumor cells. Such in situ nanoadjuvant-assembled tumor vaccines can be further developed for long-term prevention of tumor recurrence without the need for chemotherapy.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    Video file S1 (MPG): Video file S2 (MPG): The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.9b02071.

    • Figures S1–S13 (PDF)

    • Video file S1: Phagocytosis of PDL1Ab-IQ/PN-treated tumor cells by BMDCs (MPG)

    • Video file S2a: CT26 cell-killing effect of untreated T cells (MPG)

    • Video file S2b: CT26 cell-killing effect of PDL1Ab-IQ/PN-treated T cells (MPG)

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    Cite this: ACS Nano 2019, 13, 7, 7442–7462
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