Dual-responsive nanosystem based on TGF-β blockade and immunogenic chemotherapy for effective chemoimmunotherapy
The antitumor immune response induced by chemotherapy has attracted considerable attention. However, the immunosuppressive tumor microenvironment hinders the immune activation effect of cancer chemotherapy. TGF-β plays a key role in driving tumor immunosuppression and can prevent effective antitumor...
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| Published in | Drug delivery Vol. 29; no. 1; pp. 1358 - 1369 |
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| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Taylor & Francis
01.12.2022
Taylor & Francis Ltd Taylor & Francis Group |
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| Abstract | The antitumor immune response induced by chemotherapy has attracted considerable attention. However, the immunosuppressive tumor microenvironment hinders the immune activation effect of cancer chemotherapy. TGF-β plays a key role in driving tumor immunosuppression and can prevent effective antitumor immune response through multiple roles. In this study, a dual-responsive prodrug micelle (PAOL) is designed to co-deliver LY2109761 (a TGF-β receptor I/II inhibitor) and oxaliplatin (OXA, a conventional chemotherapy) to remodel tumor microenvironment and trigger immunogenic cell death (ICD) to induce antitumor immunity response. Under hypoxia tumor environment, the polyethylene glycol shell of the micelle cleavages, along with the release of LY2109761 and OXA prodrug. Cytotoxic effect of OXA is then activated by glutathione-mediated reduction in tumor cells and the activated OXA significantly enhances tumor immunogenicity and promotes intratumoral accumulation of cytotoxic T lymphocytes. Meanwhile, TGF-β blockade through LY2109761 reprograms tumor microenvironment by correcting the immunosuppressive state and regulating tumor extracellular matrix, which further maintaining OXA induced immune response. Therefore, due to the capability of boosting tumor-specific antitumor immunity, the bifunctional micelle presents markedly synergistic antitumor efficacies and provides a potent therapeutic strategy for chemoimmunotherapy of solid tumors. |
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| AbstractList | The antitumor immune response induced by chemotherapy has attracted considerable attention. However, the immunosuppressive tumor microenvironment hinders the immune activation effect of cancer chemotherapy. TGF-β plays a key role in driving tumor immunosuppression and can prevent effective antitumor immune response through multiple roles. In this study, a dual-responsive prodrug micelle (PAOL) is designed to co-deliver LY2109761 (a TGF-β receptor I/II inhibitor) and oxaliplatin (OXA, a conventional chemotherapy) to remodel tumor microenvironment and trigger immunogenic cell death (ICD) to induce antitumor immunity response. Under hypoxia tumor environment, the polyethylene glycol shell of the micelle cleavages, along with the release of LY2109761 and OXA prodrug. Cytotoxic effect of OXA is then activated by glutathione-mediated reduction in tumor cells and the activated OXA significantly enhances tumor immunogenicity and promotes intratumoral accumulation of cytotoxic T lymphocytes. Meanwhile, TGF-β blockade through LY2109761 reprograms tumor microenvironment by correcting the immunosuppressive state and regulating tumor extracellular matrix, which further maintaining OXA induced immune response. Therefore, due to the capability of boosting tumor-specific antitumor immunity, the bifunctional micelle presents markedly synergistic antitumor efficacies and provides a potent therapeutic strategy for chemoimmunotherapy of solid tumors. The antitumor immune response induced by chemotherapy has attracted considerable attention. However, the immunosuppressive tumor microenvironment hinders the immune activation effect of cancer chemotherapy. TGF-β plays a key role in driving tumor immunosuppression and can prevent effective antitumor immune response through multiple roles. In this study, a dual-responsive prodrug micelle (PAOL) is designed to co-deliver LY2109761 (a TGF-β receptor I/II inhibitor) and oxaliplatin (OXA, a conventional chemotherapy) to remodel tumor microenvironment and trigger immunogenic cell death (ICD) to induce antitumor immunity response. Under hypoxia tumor environment, the polyethylene glycol shell of the micelle cleavages, along with the release of LY2109761 and OXA prodrug. Cytotoxic effect of OXA is then activated by glutathione-mediated reduction in tumor cells and the activated OXA significantly enhances tumor immunogenicity and promotes intratumoral accumulation of cytotoxic T lymphocytes. Meanwhile, TGF-β blockade through LY2109761 reprograms tumor microenvironment by correcting the immunosuppressive state and regulating tumor extracellular matrix, which further maintaining OXA induced immune response. Therefore, due to the capability of boosting tumor-specific antitumor immunity, the bifunctional micelle presents markedly synergistic antitumor efficacies and provides a potent therapeutic strategy for chemoimmunotherapy of solid tumors.The antitumor immune response induced by chemotherapy has attracted considerable attention. However, the immunosuppressive tumor microenvironment hinders the immune activation effect of cancer chemotherapy. TGF-β plays a key role in driving tumor immunosuppression and can prevent effective antitumor immune response through multiple roles. In this study, a dual-responsive prodrug micelle (PAOL) is designed to co-deliver LY2109761 (a TGF-β receptor I/II inhibitor) and oxaliplatin (OXA, a conventional chemotherapy) to remodel tumor microenvironment and trigger immunogenic cell death (ICD) to induce antitumor immunity response. Under hypoxia tumor environment, the polyethylene glycol shell of the micelle cleavages, along with the release of LY2109761 and OXA prodrug. Cytotoxic effect of OXA is then activated by glutathione-mediated reduction in tumor cells and the activated OXA significantly enhances tumor immunogenicity and promotes intratumoral accumulation of cytotoxic T lymphocytes. Meanwhile, TGF-β blockade through LY2109761 reprograms tumor microenvironment by correcting the immunosuppressive state and regulating tumor extracellular matrix, which further maintaining OXA induced immune response. Therefore, due to the capability of boosting tumor-specific antitumor immunity, the bifunctional micelle presents markedly synergistic antitumor efficacies and provides a potent therapeutic strategy for chemoimmunotherapy of solid tumors. |
| Author | Huang, Xiaoxian Han, Lingfei Liu, Fulei Zhu, Wanfang Feng, Feng Xue, Jingwei Qu, Wei Wang, Ruyi Zhang, Ning Liu, Wenyuan |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35506467$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_3389_fimmu_2023_1238694 crossref_primary_10_3390_ijms232415827 crossref_primary_10_1016_j_cytogfr_2023_09_005 crossref_primary_10_1016_j_cclet_2023_108928 crossref_primary_10_1038_s41413_023_00246_z crossref_primary_10_1021_acsami_3c16571 crossref_primary_10_1007_s12672_023_00798_w crossref_primary_10_3389_fphar_2024_1350187 |
| Cites_doi | 10.1002/adma.201705054 10.1016/j.cell.2011.02.013 10.1038/nrc3380 10.1016/j.apsb.2020.07.013 10.1016/j.apsb.2021.08.021 10.1016/j.pharmthera.2018.12.002 10.1002/adma.201803001 10.1038/s41571-020-0413-z 10.1016/j.cclet.2020.11.006 10.1002/adma.201901513 10.1111/jcmm.14356 10.1016/j.bioactmat.2020.12.010 10.1016/j.apsb.2020.08.010 10.1002/adfm.201602963 10.1002/adfm.202107791 10.1021/acsami.9b23325 10.1016/j.biomaterials.2021.121010 10.1038/s41571-020-0403-1 10.1126/scitranslmed.aan5488 10.1038/nature25501 10.1039/C9CS00271E 10.1002/anie.202005362 10.1016/j.immuni.2019.03.024 10.1021/acsami.0c06120 10.1021/acsami.9b15116 10.1038/s41467-020-14425-7 10.1073/pnas.0809784106 10.1016/j.ajps.2018.08.009 10.1155/2019/4650695 10.1158/1078-0432.CCR-11-2855 10.1016/j.canlet.2016.01.043 10.1038/nri2808 10.1016/j.canlet.2018.08.028 10.1021/acsnano.0c00764 10.2147/DDDT.S86621 10.1002/advs.201802134 10.1038/s41568-021-00413-6 10.1016/j.biomaterials.2020.120190 10.1016/j.canlet.2015.07.039 10.1158/1078-0432.CCR-07-1157 10.3389/fimmu.2020.563784 10.1038/nrc3726 10.1038/nrc3064 10.1038/s41467-017-01651-9 |
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| SubjectTerms | Apoptosis Cancer Cell culture Cell death Chemoimmunotherapy Chemotherapy Cytokines Cytotoxicity Extracellular matrix Hypoxia immunogenic cell death immunosuppression tumor microenvironment Immunotherapy Kinases Laboratories Metastasis Micelles nanosystem Pharmaceutical sciences Prodrugs - pharmacology TGF-β blockade Transforming Growth Factor beta Tumor Microenvironment Tumors |
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| Title | Dual-responsive nanosystem based on TGF-β blockade and immunogenic chemotherapy for effective chemoimmunotherapy |
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