Specific surface-modified iron oxide nanoparticles trigger complement-dependent innate and adaptive antileukaemia immunity

Abstract Considerable advances have been achieved in the application of nanomaterials for immunotherapies, yet the precise immune effects induced by protein corona remain elusive. Here, we explore the formation mechanism and immune regulation process of protein corona in acute myeloid leukaemia (AML...

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Main Authors: Yuanyuan Li, Wen Wu, Qihui Liu, Qiong Wu, Ping Ren, Xi Xi, Haiyan Liu, Jiarui Zhao, Wei Zhang, Zizhun Wang, Yuanyuan lv, Bin Tian, Shuang Sun, Jiaqi Cui, Yangyang Zhao, Jingyuan Wu, Mingyuan Gao, Fangfang Chen
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54810-0
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author Yuanyuan Li
Wen Wu
Qihui Liu
Qiong Wu
Ping Ren
Xi Xi
Haiyan Liu
Jiarui Zhao
Wei Zhang
Zizhun Wang
Yuanyuan lv
Bin Tian
Shuang Sun
Jiaqi Cui
Yangyang Zhao
Jingyuan Wu
Mingyuan Gao
Fangfang Chen
author_facet Yuanyuan Li
Wen Wu
Qihui Liu
Qiong Wu
Ping Ren
Xi Xi
Haiyan Liu
Jiarui Zhao
Wei Zhang
Zizhun Wang
Yuanyuan lv
Bin Tian
Shuang Sun
Jiaqi Cui
Yangyang Zhao
Jingyuan Wu
Mingyuan Gao
Fangfang Chen
author_sort Yuanyuan Li
collection DOAJ
description Abstract Considerable advances have been achieved in the application of nanomaterials for immunotherapies, yet the precise immune effects induced by protein corona remain elusive. Here, we explore the formation mechanism and immune regulation process of protein corona in acute myeloid leukaemia (AML) mouse models using commercialized iron oxide nanoparticles (IONPs), with different surface modifications, including an FDA-approved variant. Using macrophages depleted or Complement Component 3 (C3) knockout mice, we demonstrate that carboxymethyl dextran-coated IONP (IONP-COOH) reduces leukaemia burden. Mechanistically, IONP-COOH indirectly binds to C3b after activating the complement alternative pathway, subsequently enhancing phagocytosis of macrophages and activating adaptive immunity mediated by complement corona. While aminated dextran-coated IONPs directly absorb C3b and activate the lectin pathway, leading to immune cell exhaustion. Our findings suggest that IONP-COOH may serve as an immune activator for AML treatment, offering a promising approach to developing therapeutic nanomaterials by leveraging surface chemistry to enhance immunotherapy.
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institution Kabale University
issn 2041-1723
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publishDate 2024-11-01
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spelling doaj-art-ab402e55649542cf88501cce1b46e92d2024-12-01T12:35:32ZengNature PortfolioNature Communications2041-17232024-11-0115111610.1038/s41467-024-54810-0Specific surface-modified iron oxide nanoparticles trigger complement-dependent innate and adaptive antileukaemia immunityYuanyuan Li0Wen Wu1Qihui Liu2Qiong Wu3Ping Ren4Xi Xi5Haiyan Liu6Jiarui Zhao7Wei Zhang8Zizhun Wang9Yuanyuan lv10Bin Tian11Shuang Sun12Jiaqi Cui13Yangyang Zhao14Jingyuan Wu15Mingyuan Gao16Fangfang Chen17Key Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityThe Skaggs School of Pharmacy and Pharmaceutical Sciences, Department of Pharmaceutical Sciences, University of Colorado Anschutz Medical CampusKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityElectron Microscopy Center, Jilin UniversityElectron Microscopy Center, Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityState Key Laboratory of Radiation Medicine and Protection, Collaborative Innovation Center of Radiation Medicine of Jiangsu Higher Education Institutions, School for Radiological and Interdisciplinary Sciences, Soochow UniversityKey Laboratory of Pathobiology, Ministry of Education, Nanomedicine and Translational Research Center, China-Japan Union Hospital of Jilin UniversityAbstract Considerable advances have been achieved in the application of nanomaterials for immunotherapies, yet the precise immune effects induced by protein corona remain elusive. Here, we explore the formation mechanism and immune regulation process of protein corona in acute myeloid leukaemia (AML) mouse models using commercialized iron oxide nanoparticles (IONPs), with different surface modifications, including an FDA-approved variant. Using macrophages depleted or Complement Component 3 (C3) knockout mice, we demonstrate that carboxymethyl dextran-coated IONP (IONP-COOH) reduces leukaemia burden. Mechanistically, IONP-COOH indirectly binds to C3b after activating the complement alternative pathway, subsequently enhancing phagocytosis of macrophages and activating adaptive immunity mediated by complement corona. While aminated dextran-coated IONPs directly absorb C3b and activate the lectin pathway, leading to immune cell exhaustion. Our findings suggest that IONP-COOH may serve as an immune activator for AML treatment, offering a promising approach to developing therapeutic nanomaterials by leveraging surface chemistry to enhance immunotherapy.https://doi.org/10.1038/s41467-024-54810-0
spellingShingle Yuanyuan Li
Wen Wu
Qihui Liu
Qiong Wu
Ping Ren
Xi Xi
Haiyan Liu
Jiarui Zhao
Wei Zhang
Zizhun Wang
Yuanyuan lv
Bin Tian
Shuang Sun
Jiaqi Cui
Yangyang Zhao
Jingyuan Wu
Mingyuan Gao
Fangfang Chen
Specific surface-modified iron oxide nanoparticles trigger complement-dependent innate and adaptive antileukaemia immunity
Nature Communications
title Specific surface-modified iron oxide nanoparticles trigger complement-dependent innate and adaptive antileukaemia immunity
title_full Specific surface-modified iron oxide nanoparticles trigger complement-dependent innate and adaptive antileukaemia immunity
title_fullStr Specific surface-modified iron oxide nanoparticles trigger complement-dependent innate and adaptive antileukaemia immunity
title_full_unstemmed Specific surface-modified iron oxide nanoparticles trigger complement-dependent innate and adaptive antileukaemia immunity
title_short Specific surface-modified iron oxide nanoparticles trigger complement-dependent innate and adaptive antileukaemia immunity
title_sort specific surface modified iron oxide nanoparticles trigger complement dependent innate and adaptive antileukaemia immunity
url https://doi.org/10.1038/s41467-024-54810-0
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