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Macrophage Membrane-Camouflaged Responsive Polymer Nanogels Enable Magnetic Resonance Imaging-Guided Chemotherapy/Chemodynamic Therapy of Orthotopic Glioma
Development of innovative nanomedicine formulations to traverse the blood–brain barrier (BBB) for effective theranostics of glioma remains a great challenge. Herein, we report the creation of macrophage membrane-camouflaged multifunctional polymer nanogels coloaded with manganese dioxide (MnO2) and...
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Published in: | ACS nano 2021-12, Vol.15 (12), p.20377-20390 |
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description | Development of innovative nanomedicine formulations to traverse the blood–brain barrier (BBB) for effective theranostics of glioma remains a great challenge. Herein, we report the creation of macrophage membrane-camouflaged multifunctional polymer nanogels coloaded with manganese dioxide (MnO2) and cisplatin for magnetic resonance (MR) imaging-guided chemotherapy/chemodynamic therapy (CDT) of orthotopic glioma. Redox-responsive poly(N-vinylcaprolactam) (PVCL) nanogels (NGs) formed via precipitation polymerization were in situ loaded with MnO2 and physically encapsulated with cisplatin to have a mean size of 106.3 nm and coated with macrophage membranes to have a good colloidal stability. The generated hybrid NGs display dual pH- and redox-responsive cisplatin and Mn(II) release profiles and can deplete glutathione (GSH) rich in tumor microenvironment through reaction with disulfide-containing cross-linkers within the NGs and MnO2. The thus created Mn(II) enables enhanced CDT through a Fenton-like reaction and T 1-weighted MR imaging, while the loaded cisplatin not only exerts its chemotherapy effect but also promotes the reactive oxygen species generation to enhance the CDT efficacy. Importantly, the macrophage membrane coating rendered the hybrid NGs with prolonged blood circulation time and ability to traverse BBB for specific targeted chemotherapy/CDT of orthotopic glioma. Our study demonstrates a promising self-adaptive and cooperative NG-based nanomedicine platform for highly efficient theranostics of glioma, which may be extended to tackle other difficult cancer types. |
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Herein, we report the creation of macrophage membrane-camouflaged multifunctional polymer nanogels coloaded with manganese dioxide (MnO2) and cisplatin for magnetic resonance (MR) imaging-guided chemotherapy/chemodynamic therapy (CDT) of orthotopic glioma. Redox-responsive poly(N-vinylcaprolactam) (PVCL) nanogels (NGs) formed via precipitation polymerization were in situ loaded with MnO2 and physically encapsulated with cisplatin to have a mean size of 106.3 nm and coated with macrophage membranes to have a good colloidal stability. The generated hybrid NGs display dual pH- and redox-responsive cisplatin and Mn(II) release profiles and can deplete glutathione (GSH) rich in tumor microenvironment through reaction with disulfide-containing cross-linkers within the NGs and MnO2. The thus created Mn(II) enables enhanced CDT through a Fenton-like reaction and T 1-weighted MR imaging, while the loaded cisplatin not only exerts its chemotherapy effect but also promotes the reactive oxygen species generation to enhance the CDT efficacy. Importantly, the macrophage membrane coating rendered the hybrid NGs with prolonged blood circulation time and ability to traverse BBB for specific targeted chemotherapy/CDT of orthotopic glioma. Our study demonstrates a promising self-adaptive and cooperative NG-based nanomedicine platform for highly efficient theranostics of glioma, which may be extended to tackle other difficult cancer types.</description><identifier>ISSN: 1936-0851</identifier><identifier>EISSN: 1936-086X</identifier><identifier>DOI: 10.1021/acsnano.1c08689</identifier><identifier>PMID: 34860014</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Cell Line, Tumor ; Glioma - diagnostic imaging ; Glioma - drug therapy ; Humans ; Macrophages ; Magnetic Resonance Imaging ; Magnetic Resonance Spectroscopy ; Manganese Compounds ; Nanogels ; Nanoparticles ; Oxides ; Polymers ; Theranostic Nanomedicine ; Tumor Microenvironment</subject><ispartof>ACS nano, 2021-12, Vol.15 (12), p.20377-20390</ispartof><rights>2021 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a333t-e66eb44d03e4e3df1ba4374e66496e72c518263be5e0abde15eeec14f04582e33</citedby><cites>FETCH-LOGICAL-a333t-e66eb44d03e4e3df1ba4374e66496e72c518263be5e0abde15eeec14f04582e33</cites><orcidid>0000-0001-8042-1232 ; 0000-0002-1065-0854 ; 0000-0001-6785-6645</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34860014$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xiao, Tingting</creatorcontrib><creatorcontrib>He, Meijuan</creatorcontrib><creatorcontrib>Xu, Fang</creatorcontrib><creatorcontrib>Fan, Yu</creatorcontrib><creatorcontrib>Jia, Bingyang</creatorcontrib><creatorcontrib>Shen, Mingwu</creatorcontrib><creatorcontrib>Wang, Han</creatorcontrib><creatorcontrib>Shi, Xiangyang</creatorcontrib><title>Macrophage Membrane-Camouflaged Responsive Polymer Nanogels Enable Magnetic Resonance Imaging-Guided Chemotherapy/Chemodynamic Therapy of Orthotopic Glioma</title><title>ACS nano</title><addtitle>ACS Nano</addtitle><description>Development of innovative nanomedicine formulations to traverse the blood–brain barrier (BBB) for effective theranostics of glioma remains a great challenge. Herein, we report the creation of macrophage membrane-camouflaged multifunctional polymer nanogels coloaded with manganese dioxide (MnO2) and cisplatin for magnetic resonance (MR) imaging-guided chemotherapy/chemodynamic therapy (CDT) of orthotopic glioma. Redox-responsive poly(N-vinylcaprolactam) (PVCL) nanogels (NGs) formed via precipitation polymerization were in situ loaded with MnO2 and physically encapsulated with cisplatin to have a mean size of 106.3 nm and coated with macrophage membranes to have a good colloidal stability. The generated hybrid NGs display dual pH- and redox-responsive cisplatin and Mn(II) release profiles and can deplete glutathione (GSH) rich in tumor microenvironment through reaction with disulfide-containing cross-linkers within the NGs and MnO2. The thus created Mn(II) enables enhanced CDT through a Fenton-like reaction and T 1-weighted MR imaging, while the loaded cisplatin not only exerts its chemotherapy effect but also promotes the reactive oxygen species generation to enhance the CDT efficacy. Importantly, the macrophage membrane coating rendered the hybrid NGs with prolonged blood circulation time and ability to traverse BBB for specific targeted chemotherapy/CDT of orthotopic glioma. Our study demonstrates a promising self-adaptive and cooperative NG-based nanomedicine platform for highly efficient theranostics of glioma, which may be extended to tackle other difficult cancer types.</description><subject>Cell Line, Tumor</subject><subject>Glioma - diagnostic imaging</subject><subject>Glioma - drug therapy</subject><subject>Humans</subject><subject>Macrophages</subject><subject>Magnetic Resonance Imaging</subject><subject>Magnetic Resonance Spectroscopy</subject><subject>Manganese Compounds</subject><subject>Nanogels</subject><subject>Nanoparticles</subject><subject>Oxides</subject><subject>Polymers</subject><subject>Theranostic Nanomedicine</subject><subject>Tumor Microenvironment</subject><issn>1936-0851</issn><issn>1936-086X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp1kV1LwzAYhYMofl97J70UpFvSpFl7KWPOwfxAFLwrb9u3XaVJatIK-y3-WaObu_MqyeE5J8l7CLlgdMRoxMZQOA3ajFhBE5mke-SYpVyG_vC2v9vH7IicOPdOaTxJJvKQHHGRSEqZOCZf91BY062gxuAeVW5BYzgFZYaq9VoZPKPrjHbNJwZPpl0rtMGDv7HG1gUzDXnrfVBr7JvihzX-OQUGCwV1o-twPjSlD5muUJl-hRa69fj3UK41KG952YiBqYJH269MbzqvztvGKDgjBxW0Ds-36yl5vZ29TO_C5eN8Mb1ZhsA570OUEnMhSspRIC8rloPgE-FlkUqcREXMkkjyHGOkkJfIYkQsmKioiJMIOT8lV5vczpqPAV2fqcYV2LZ-FmZwWSSpTKNURsyj4w3qh-acxSrrbKPArjNGs59Gsm0j2bYR77jchg-5wnLH_1XggesN4J3Zuxms9n_9N-4bFKKa8Q</recordid><startdate>20211228</startdate><enddate>20211228</enddate><creator>Xiao, Tingting</creator><creator>He, Meijuan</creator><creator>Xu, Fang</creator><creator>Fan, Yu</creator><creator>Jia, Bingyang</creator><creator>Shen, Mingwu</creator><creator>Wang, Han</creator><creator>Shi, Xiangyang</creator><general>American Chemical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8042-1232</orcidid><orcidid>https://orcid.org/0000-0002-1065-0854</orcidid><orcidid>https://orcid.org/0000-0001-6785-6645</orcidid></search><sort><creationdate>20211228</creationdate><title>Macrophage Membrane-Camouflaged Responsive Polymer Nanogels Enable Magnetic Resonance Imaging-Guided Chemotherapy/Chemodynamic Therapy of Orthotopic Glioma</title><author>Xiao, Tingting ; He, Meijuan ; Xu, Fang ; Fan, Yu ; Jia, Bingyang ; Shen, Mingwu ; Wang, Han ; Shi, Xiangyang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a333t-e66eb44d03e4e3df1ba4374e66496e72c518263be5e0abde15eeec14f04582e33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Cell Line, Tumor</topic><topic>Glioma - diagnostic imaging</topic><topic>Glioma - drug therapy</topic><topic>Humans</topic><topic>Macrophages</topic><topic>Magnetic Resonance Imaging</topic><topic>Magnetic Resonance Spectroscopy</topic><topic>Manganese Compounds</topic><topic>Nanogels</topic><topic>Nanoparticles</topic><topic>Oxides</topic><topic>Polymers</topic><topic>Theranostic Nanomedicine</topic><topic>Tumor Microenvironment</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xiao, Tingting</creatorcontrib><creatorcontrib>He, Meijuan</creatorcontrib><creatorcontrib>Xu, Fang</creatorcontrib><creatorcontrib>Fan, Yu</creatorcontrib><creatorcontrib>Jia, Bingyang</creatorcontrib><creatorcontrib>Shen, Mingwu</creatorcontrib><creatorcontrib>Wang, Han</creatorcontrib><creatorcontrib>Shi, Xiangyang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>ACS nano</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xiao, Tingting</au><au>He, Meijuan</au><au>Xu, Fang</au><au>Fan, Yu</au><au>Jia, Bingyang</au><au>Shen, Mingwu</au><au>Wang, Han</au><au>Shi, Xiangyang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Macrophage Membrane-Camouflaged Responsive Polymer Nanogels Enable Magnetic Resonance Imaging-Guided Chemotherapy/Chemodynamic Therapy of Orthotopic Glioma</atitle><jtitle>ACS nano</jtitle><addtitle>ACS Nano</addtitle><date>2021-12-28</date><risdate>2021</risdate><volume>15</volume><issue>12</issue><spage>20377</spage><epage>20390</epage><pages>20377-20390</pages><issn>1936-0851</issn><eissn>1936-086X</eissn><abstract>Development of innovative nanomedicine formulations to traverse the blood–brain barrier (BBB) for effective theranostics of glioma remains a great challenge. 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The thus created Mn(II) enables enhanced CDT through a Fenton-like reaction and T 1-weighted MR imaging, while the loaded cisplatin not only exerts its chemotherapy effect but also promotes the reactive oxygen species generation to enhance the CDT efficacy. Importantly, the macrophage membrane coating rendered the hybrid NGs with prolonged blood circulation time and ability to traverse BBB for specific targeted chemotherapy/CDT of orthotopic glioma. Our study demonstrates a promising self-adaptive and cooperative NG-based nanomedicine platform for highly efficient theranostics of glioma, which may be extended to tackle other difficult cancer types.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>34860014</pmid><doi>10.1021/acsnano.1c08689</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-8042-1232</orcidid><orcidid>https://orcid.org/0000-0002-1065-0854</orcidid><orcidid>https://orcid.org/0000-0001-6785-6645</orcidid></addata></record> |
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subjects | Cell Line, Tumor Glioma - diagnostic imaging Glioma - drug therapy Humans Macrophages Magnetic Resonance Imaging Magnetic Resonance Spectroscopy Manganese Compounds Nanogels Nanoparticles Oxides Polymers Theranostic Nanomedicine Tumor Microenvironment |
title | Macrophage Membrane-Camouflaged Responsive Polymer Nanogels Enable Magnetic Resonance Imaging-Guided Chemotherapy/Chemodynamic Therapy of Orthotopic Glioma |
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