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      Tumor cell membrane-camouflaged responsive nanoparticles enable MRI-guided immuno-chemodynamic therapy of orthotopic osteosarcoma

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          Abstract

          Osteosarcoma is a refractory bone disease in young people that needs the updating and development of effective treatment. Although nanotechnology is widely applied in cancer therapy, poor targeting and inadequate efficiency hinder its development. In this study, we prepared alendronate (ALD)/K7M2 cell membranes-coated hollow manganese dioxide (HMnO 2) nanoparticles as a nanocarrier to load Ginsenoside Rh2 (Rh2) for Magnetic Resonance imaging (MRI)-guided immuno-chemodynamic combination osteosarcoma therapy. Subsequently, the ALD and K7M2 cell membranes were successively modified on the surface of HMnO 2 and loaded with Rh2. The tumor microenvironment (TME)-activated Rh2@HMnO 2-AM nanoparticles have good bone tumor-targeting and tumor-homing capabilities, excellent GSH-sensitive drug release profile and MRI capability, and attractive immuno-chemodynamic combined therapeutic efficiency. The Rh2@HMnO 2-AM nanoparticles can effectively trigger immunogenic cell death (ICD), activate CD4 +/CD8 + T cells in vivo, and upregulate BAX, BCL-2 and Caspase-3 in cellular level. Further results revealed that Rh2@HMnO 2-AM enhanced the secretion of IL-6, IFN-γ and TNF-α in serum and inhibited the generation of FOXP3 + T cells (Tregs) in tumors. Moreover, the Rh2@HMnO 2-AM treatment significant restricted tumor growth in-situ tumor-bearing mice. Therefore, Rh2@HMnO 2-AM may serve as an effective and bio-friendly nanoparticle platform combined with immunotherapy and chemodynamic therapy to provide a novel approach to osteosarcoma therapy.

          Graphical abstract

          Construction of tumor microenvironment-responsive nanoplatform for MRI-guided immuno-chemodynamic combination osteosarcoma targeted therapy.

          Highlights

          • •

            Ginsenoside Rh2 was loaded in Hollow MnO 2 NPs for enhancing its bioavailability.

          • •

            The orthotopic tumor model exhibits a convincing therapeutic effect of nanosystems.

          • •

            Alendronate/cell membranes enhance osteosarcoma targeting and tumor-homing ability.

          • •

            Tumor microenvironment-induced NPs degradation can release immune stimulant and Mn 2+.

          • •

            The NPs had excellent immuno-chemodynamic combination osteosarcoma therapy effect.

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          Most cited references48

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          Chemodynamic Therapy: Tumour Microenvironment-Mediated Fenton and Fenton-like Reactions

          Zhongmin Tang, Yanyan Liu, Mingyuan He … (2019)
          Tailored to the specific tumour microenvironment, which involves acidity and the overproduction of hydrogen peroxide, advanced nanotechnology has been introduced to generate the hydroxyl radical (. OH) primarily for tumour chemodynamic therapy (CDT) through the Fenton and Fenton-like reactions. Numerous studies have investigated the enhancement of CDT efficiency, primarily the increase in the amount of . OH generated. Notably, various strategies based on the Fenton reaction have been employed to enhance . OH generation, including nanomaterials selection, modulation of the reaction environment, and external energy fields stimulation, which are discussed systematically in this Minireview. Furthermore, the potential challenges and the methods used to facilitate CDT effectiveness are also presented to support this cutting-edge research area.
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            Cancer Cell Membrane-Coated Nanoparticles for Anticancer Vaccination and Drug Delivery

            Ronnie Fang, Che-Ming Hu, Brian T Luk … (2014)
            Cell-derived nanoparticles have been garnering increased attention due to their ability to mimic many of the natural properties displayed by their source cells. This top-down engineering approach can be applied toward the development of novel therapeutic strategies owing to the unique interactions enabled through the retention of complex antigenic information. Herein, we report on the biological functionalization of polymeric nanoparticles with a layer of membrane coating derived from cancer cells. The resulting core–shell nanostructures, which carry the full array of cancer cell membrane antigens, offer a robust platform with applicability toward multiple modes of anticancer therapy. We demonstrate that by coupling the particles with an immunological adjuvant, the resulting formulation can be used to promote a tumor-specific immune response for use in vaccine applications. Moreover, we show that by taking advantage of the inherent homotypic binding phenomenon frequently observed among tumor cells the membrane functionalization allows for a unique cancer targeting strategy that can be utilized for drug delivery applications.
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              Simultaneous Fenton-like Ion Delivery and Glutathione Depletion by MnO2 -Based Nanoagent to Enhance Chemodynamic Therapy

              Zhen Yang, Wei Tang, Gang Niu … (2018)
              Chemodynamic therapy (CDT) utilizes iron-initiated Fenton chemistry to destroy tumor cells by converting endogenous H2 O2 into the highly toxic hydroxyl radical (. OH). There is a paucity of Fenton-like metal-based CDT agents. Intracellular glutathione (GSH) with . OH scavenging ability greatly reduces CDT efficacy. A self-reinforcing CDT nanoagent based on MnO2 is reported that has both Fenton-like Mn2+ delivery and GSH depletion properties. In the presence of HCO3- , which is abundant in the physiological medium, Mn2+ exerts Fenton-like activity to generate . OH from H2 O2 . Upon uptake of MnO2 -coated mesoporous silica nanoparticles (MS@MnO2 NPs) by cancer cells, the MnO2 shell undergoes a redox reaction with GSH to form glutathione disulfide and Mn2+ , resulting in GSH depletion-enhanced CDT. This, together with the GSH-activated MRI contrast effect and dissociation of MnO2 , allows MS@MnO2 NPs to achieve MRI-monitored chemo-chemodynamic combination therapy.
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                Author and article information

                Contributors
                Chuanglong He
                Journal
                Journal ID (nlm-ta): Bioact Mater
                Journal ID (iso-abbrev): Bioact Mater
                Title: Bioactive Materials
                Publisher: KeAi Publishing
                ISSN (Electronic): 2452-199X
                Publication date PMC-release: 26 January 2022
                Publication date Collection: November 2022
                Publication date (Electronic): 26 January 2022
                Volume: 17
                Pages: 221-233
                Affiliations
                [a ]State Key Laboratory for Modification of Chemical Fibers and Polymer Materials, College of Chemistry, Chemical Engineering and Biotechnology, Donghua University, Shanghai, 201620, China
                [b ]Department of Thoracic Oncology, Jiujiang Cancer Hospital, Jiangxi Province, China
                [c ]Health Management Center, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China
                Author notes
                [∗ ]Corresponding author. hcl@ 123456dhu.edu.cn
                [∗∗ ]Corresponding author.
                Article
                Publisher Item ID: S2452-199X(22)00043-3
                DOI: 10.1016/j.bioactmat.2022.01.035
                PMC ID: 8965157
                PubMed ID: 35386464
                SO-VID: bec58a93-762c-4087-a1b6-ad6ea57babf3
                Copyright © © 2022 The Authors
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 1 December 2021
                Date revision received : 11 January 2022
                Date accepted : 19 January 2022
                Categories
                Subject: Article

                Keywords: ginsenoside rh2,hollow manganese dioxide,magnetic resonance imaging,chemodynamic therapy,immunotherapy
                Data availability:
                Keywords: ginsenoside rh2, hollow manganese dioxide, magnetic resonance imaging, chemodynamic therapy, immunotherapy

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