Polymersome-mediated cytosolic delivery of cyclic dinucleotide STING agonist enhances tumor immunotherapy

Bioactive Materials - Tập 16 - Trang 1-11 - 2022
Huan Zheng1, Beibei Guo1, Xinyun Qiu1, Yifeng Xia1, Yan Qu1, Liang Cheng2, Fenghua Meng1, Zhiyuan Zhong1,2
1Biomedical Polymers Laboratory, College of Chemistry, Chemical Engineering and Materials Science, and State Key Laboratory of Radiation Medicine and Protection, Soochow University, Suzhou, 215123, PR China
2Department of Pharmaceutics, College of Pharmaceutical Sciences, Soochow University, Suzhou, 215123, PR China

Tài liệu tham khảo

Wang, 2020, CAR-NK for tumor immunotherapy: clinical transformation and future prospects, Cancer Lett., 472, 175, 10.1016/j.canlet.2019.11.033 Nam, 2019, Cancer nanomedicine for combination cancer immunotherapy, Nat. Rev. Mater., 4, 398, 10.1038/s41578-019-0108-1 Xu, 2020, A general strategy towards personalized nanovaccines based on fluoropolymers for post-surgical cancer immunotherapy, Nat. Nanotechnol., 15, 1043, 10.1038/s41565-020-00781-4 Hodi, 2010, Improved survival with Ipilimumab in patients with metastatic melanoma, N. Engl. J. Med., 363, 711, 10.1056/NEJMoa1003466 Formenti, 2018, Radiotherapy induces responses of lung cancer to CTLA-4 blockade, Nat. Med., 24, 1845, 10.1038/s41591-018-0232-2 Duruisseaux, 2018, Epigenetic prediction of response to anti-PD-1 treatment in non-small-cell lung cancer: a multicentre, retrospective analysis, Lancet Respir. Med., 6, 771, 10.1016/S2213-2600(18)30284-4 Beaver, 2018, Patients with melanoma treated with an anti-PD-1 antibody beyond recist progression: a US food and drug administration pooled analysis, Lancet Oncol., 19, 229, 10.1016/S1470-2045(17)30846-X Xu, 2019, Anti-PD-1 antibody SHR-1210 combined with Apatinib for advanced hepatocellular carcinoma, gastric, or esophagogastric junction cancer: an open-label, dose escalation and expansion study, Clin. Cancer Res., 25, 515, 10.1158/1078-0432.CCR-18-2484 Kowanetz, 2018, Differential regulation of PD-L1 expression by immune and tumor cells in NSCLC and the response to treatment with atezolizumab (anti–PD-L1), Proc. Natl. Acad. Sci. U. S. A., 115, E10119, 10.1073/pnas.1802166115 Emens, 2019, Long-term clinical outcomes and biomarker analyses of Atezolizumab therapy for patients with metastatic triple-negative breast cancer: a phase 1 study, JAMA Oncol., 5, 74, 10.1001/jamaoncol.2018.4224 Sharma, 2019, Anti-CTLA-4 immunotherapy does not deplete FoxP3(+) regulatory T cells (Tregs) in human cancers, Clin. Cancer Res., 25, 1233, 10.1158/1078-0432.CCR-18-0762 Sabet, 2016, Severe acute pulmonary toxicity associated with brentuximab in a patient with refractory hodgkin’s lymphoma, Case Rep. Pulmonol., 2016 Younes, 2016, Nivolumab for classical Hodgkin's lymphoma after failure of both autologous stem-cell transplantation and brentuximab vedotin: a multicentre, multicohort, single-arm phase 2 trial, Lancet Oncol., 17, 1283, 10.1016/S1470-2045(16)30167-X Collins, 2019, A failure to start: aborted activation of CAR T cells in chronic lymphocytic leukemia, Blood, 134, 10.1182/blood-2019-122063 Mahony, 2007, A pilot study of CTLA-4 blockade after cancer vaccine failure in patients with advanced malignancy, Clin. Cancer Res., 13, 958, 10.1158/1078-0432.CCR-06-1974 Kim, 2017, Combination therapy with anti-PD-1, anti-TIM-3, and focal radiation results in regression of murine gliomas, Clin. Cancer Res., 23, 124, 10.1158/1078-0432.CCR-15-1535 Dewan, 2009, Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti–CTLA-4 antibody, Clin. Cancer Res., 15, 5379, 10.1158/1078-0432.CCR-09-0265 Nie, 2019, Addition of low-dose decitabine to anti–PD-1 antibody camrelizumab in relapsed/refractory classical Hodgkin lymphoma, J. Clin. Oncol., 37, 1479, 10.1200/JCO.18.02151 Wang, 2014, Immunological responses triggered by photothermal therapy with carbon nanotubes in combination with anti-CTLA-4 therapy to inhibit cancer metastasis, Adv. Mater., 26, 8154, 10.1002/adma.201402996 Corrales, 2016, The host STING pathway at the interface of cancer and immunity, J. Clin. Invest., 126, 2404, 10.1172/JCI86892 Su, 2019, STING activation in cancer immunotherapy, Theranostics, 9, 7759, 10.7150/thno.37574 Corrales, 2015, Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity, Cell Rep., 11, 1018, 10.1016/j.celrep.2015.04.031 Foote, 2017, A STING agonist given with OX40 receptor and PD-L1 modulators primes immunity and reduces tumor growth in tolerized mice, Cancer Immunol. Res., 5, 468, 10.1158/2326-6066.CIR-16-0284 Sivick, 2019, Magnitude of therapeutic STING activation determines CD8+ T cell-mediated anti-tumor immunity, Cell Rep., 29, 785, 10.1016/j.celrep.2019.09.089 Junkins, 2018, A robust microparticle platform for a STING-targeted adjuvant that enhances both humoral and cellular immunity during vaccination, J. Contr. Release, 270, 1, 10.1016/j.jconrel.2017.11.030 Amouzegar, 2021, STING agonists as cancer therapeutics, Cancers, 13, 1, 10.3390/cancers13112695 Leach, 2018, STINGel: controlled release of a cyclic dinucleotide for enhanced cancer immunotherapy, Biomaterials, 163, 67, 10.1016/j.biomaterials.2018.01.035 Munoz, 2021, Influence of injection technique, drug formulation and tumor microenvironment on intratumoral immunotherapy delivery and efficacy, J. Immunother. Cancer, 9, 10.1136/jitc-2020-001800 Lu, 2020, Engineered PLGA microparticles for long-term, pulsatile release of STING agonist for cancer immunotherapy, Sci. Transl. Med., 12, 10.1126/scitranslmed.aaz6606 An, 2018, Induction of necrotic cell death and activation of STING in the tumor microenvironment via cationic silica nanoparticles leading to enhanced antitumor immunity, Nanoscale, 10, 9311, 10.1039/C8NR01376D Koshy, 2017, Liposomal delivery enhances immune activation by STING agonists for cancer immunotherapy, Adv. Biosyst, 1, 10.1002/adbi.201600013 Cheng, 2018, A nanoparticle-incorporated STING activator enhances antitumor immunity in PD-L1-insensitive models of triple-negative breast cancer, JCI Insight, 3, 3, 10.1172/jci.insight.120638 Wehbe, 2021, Nanoparticle delivery improves the pharmacokinetic properties of cyclic dinucleotide STING agonists to open a therapeutic window for intravenous administration, J. Contr. Release, 330, 1118, 10.1016/j.jconrel.2020.11.017 Shae, 2019, Endosomolytic polymersomes increase the activity of cyclic dinucleotide STING agonists to enhance cancer immunotherapy, Nat. Nanotechnol., 14, 269, 10.1038/s41565-018-0342-5 Jiang, 2018, Protein toxin chaperoned by LRP-1-targeted virus-mimicking vesicles induces high-efficiency glioblastoma therapy in vivo, Adv. Mater., 30, 10.1002/adma.201800316 Yang, 2018, Granzyme B-loaded, cell-selective penetrating and reduction-responsive polymersomes effectively inhibit progression of orthotopic human lung tumor in vivo, J. Contr. Release, 290, 141, 10.1016/j.jconrel.2018.10.013 Zou, 2017, Virus-mimicking chimaeric polymersomes boost targeted cancer siRNA therapy in vivo, Adv. Mater., 29, 10.1002/adma.201703285 Lhuillier, 2019, Radiation therapy and anti-tumor immunity: exposing immunogenic mutations to the immune system, Genome Med., 11, 2, 10.1186/s13073-019-0653-7 Galluzzi, 2016, Immunogenic cell death in cancer and infectious disease, Nat. Rev. Immunol., 17, 97, 10.1038/nri.2016.107 Uribe-Herranz, 2020, Gut microbiota modulate dendritic cell antigen presentation and radiotherapy-induced antitumor immune response, J. Clin. Invest., 130, 466, 10.1172/JCI124332 Deng, 2016, From DNA damage to nucleic acid sensing: a strategy to enhance radiation therapy, Clin. Cancer Res., 22, 20, 10.1158/1078-0432.CCR-14-3110 Mullard, 2018, Can innate immune system targets turn up the heat on 'cold' tumours?, Nat. Rev. Drug Discov., 17, 3, 10.1038/nrd.2017.264 Vrignaud, 2011, Strategies for the nanoencapsulation of hydrophilic molecules in polymer-based nanoparticles, Biomaterials, 32, 8593, 10.1016/j.biomaterials.2011.07.057 Shi, 2018, Boosting RNAi therapy for orthotopic glioblastoma with nontoxic brain-targeting chimaeric polymersomes, J. Contr. Release, 292, 163, 10.1016/j.jconrel.2018.10.034 Xia, 2021, Systemic administration of polymersomal oncolytic peptide LTX-315 combining with CPG adjuvant and anti-PD-1 antibody boosts immunotherapy of melanoma, J. Contr. Release, 336, 262, 10.1016/j.jconrel.2021.06.032 Lee, 2016, Submicron-sized hydrogels incorporating cyclic dinucleotides for selective delivery and elevated cytokine release in macrophages, Acta Biomater., 29, 271, 10.1016/j.actbio.2015.10.025 Baird, 2016, Radiotherapy combined with novel STING-targeting oligonucleotides results in regression of established tumors, Cancer Res., 76, 50, 10.1158/0008-5472.CAN-14-3619 Wang, 2017, cGAS is essential for the antitumor effect of immune checkpoint blockade, P. Natl. Acad. Sci. USA, 114, 1637, 10.1073/pnas.1621363114 Motwani, 2019, DNA sensing by the cGAS–STING pathway in health and disease, Nat. Rev. Genet., 20, 657, 10.1038/s41576-019-0151-1 Veglia, 2017, Dendritic cells in cancer: the role revisited, Curr. Opin. Immunol., 45, 43, 10.1016/j.coi.2017.01.002 Liu, 2015, Intratumoral dendritic cells in the anti-tumor immune response, Cell. Mol. Immunol., 12, 387, 10.1038/cmi.2014.130 Li, 2018, A facile approach to enhance antigen response for personalized cancer vaccination, Nat. Mater., 17, 528, 10.1038/s41563-018-0028-2 Yang, 2019, Functional T cell activation by smart nanosystems for effective cancer immunotherapy, Nano, Today Off., 27, 28 Flood, 2019, STING pathway agonism as a cancer therapeutic, Immunol. Rev., 290, 24, 10.1111/imr.12765 Li, 2018, The cGAS-cGAMP-STING pathway connects DNA damage to inflammation, senescence, and cancer, J. Exp. Med., 215, 1287, 10.1084/jem.20180139 Shang, 2019, Cryo-em structures of STING reveal its mechanism of activation by cyclic GMP-AMP, Nature, 567, 389, 10.1038/s41586-019-0998-5 Cabral, 2011, Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size, Nat. Nanotechnol., 6, 815, 10.1038/nnano.2011.166 Zhang, 2018, Rational design of nanoparticles with deep tumor penetration for effective treatment of tumor metastasis, Adv. Funct. Mater., 28 Ahn, 2018, Extrinsic phagocyte-dependent STING signaling dictates the immunogenicity of dying cells, Cancer Cell, 33, 862, 10.1016/j.ccell.2018.03.027 Ahmed, 2016, Current insights in radiation combination therapies: influence of omics and novel targeted agents in defining new concepts in radiation biology and clinical radiation oncology, Semin. Radiat. Oncol., 26, 251, 10.1016/j.semradonc.2016.07.002 Liu, 2019, An inhalable nanoparticulate STING agonist synergizes with radiotherapy to confer long-term control of lung metastases, Nat. Commun., 10, 10.1038/s41467-019-13094-5 Deng, 2014, STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors, Immunity, 41, 843, 10.1016/j.immuni.2014.10.019 Schudel, 2019, Material design for lymph node drug delivery, Nat. Rev. Mater., 4, 415, 10.1038/s41578-019-0110-7 Chang, 2018, Irradiation enhances abscopal anti-tumor effects of antigen-specific immunotherapy through regulating tumor microenvironment, Mol. Ther., 26, 404, 10.1016/j.ymthe.2017.11.011 Li, 2019, Activating cGAS-STING pathway for the optimal effect of cancer immunotherapy, J. Hematol. Oncol., 12, 10.1186/s13045-019-0721-x Snell, 2017, Type I interferon in chronic virus infection and cancer, Trends Immunol., 38, 542, 10.1016/j.it.2017.05.005 Mitchell, 2021, Engineering precision nanoparticles for drug delivery, Nat. Rev. Drug Discov., 20, 101, 10.1038/s41573-020-0090-8 Ding, 2019, Engineered nanomedicines with enhanced tumor penetration, Nano Today, 29, 10.1016/j.nantod.2019.100800