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China","doi-asserted-by":"publisher","award":["22102049"],"award-info":[{"award-number":["22102049"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Molecules"],"abstract":"<jats:p>Sonodynamic therapy (SDT) triggered by ultrasound (US) has attracted increasing attention owing to its ability to overcome critical limitations, including low tissue-penetration depth and phototoxicity in photodynamic therapy (PDT). Biogenic metal oxide nanoparticles (NPs) have been used as anti-cancer drugs due to their biocompatibility properties with most biological systems. Here, sonosensitizer MWO4-PEG NPs (M = Fe Mn Co Ni) were synthesized as inhibitors to activation-induced cytidine deaminase (AID), thus neutralizing the extensive carcinogenesis of AID in diffuse large B-cell lymphoma (DLBCL). The physiological properties of these nanomaterials were examined using transmission electron microscopy (TEM). The inhibition of NPs to AID was primarily identified by the affinity interaction prediction between reactive oxygen species (ROS) and AID through molecular dynamics and molecular docking technology. The cell apoptosis and ROS generation in US-triggered NPs treated DLBCL cells (with high levels of AID) were also detected to indicate the sonosensitivity and toxicity of MWO4-PEG NPs to DLBCL cells. The anti-lymphoma studies using DLBCL and AID-deficient DLBCL cell lines indicated a concentration-dependent profile. The synthesized MWO4-PEG NPs in this study manifested good sonodynamic inhibitory effects to AID and well treatment for AID-positive hematopoietic cancers.<\/jats:p>","DOI":"10.3390\/molecules27217143","type":"journal-article","created":{"date-parts":[[2022,10,24]],"date-time":"2022-10-24T08:19:06Z","timestamp":1666599546000},"page":"7143","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Synthesis and Biological Evaluation of PEGylated MWO4 Nanoparticles as Sonodynamic AID Inhibitors in Treating Diffuse Large B-Cell Lymphoma"],"prefix":"10.3390","volume":"27","author":[{"given":"Junna","family":"Jiao","sequence":"first","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Xinxiang Medical University, Xinxiang 453003, China"},{"name":"Xinxiang Key Laboratory of Tumor Vaccine and Immunotherapy, Xinxiang Medical University, Xinxiang 453003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhuang","family":"Qian","sequence":"additional","affiliation":[{"name":"Institutes of Health Central Plains, Xinxiang Medical University, Xinxiang 453003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yurong","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Xinxiang Medical University, Xinxiang 453003, China"},{"name":"Xinxiang Key Laboratory of Tumor Vaccine and Immunotherapy, Xinxiang Medical University, Xinxiang 453003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mei","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Xinxiang Medical University, Xinxiang 453003, China"},{"name":"Xinxiang Key Laboratory of Tumor Vaccine and Immunotherapy, Xinxiang Medical University, Xinxiang 453003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liye","family":"Fan","sequence":"additional","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Xinxiang Medical University, Xinxiang 453003, China"},{"name":"Xinxiang Key Laboratory of Tumor Vaccine and Immunotherapy, Xinxiang Medical University, Xinxiang 453003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mengqing","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Xinxiang Medical University, Xinxiang 453003, China"},{"name":"Xinxiang Key Laboratory of Tumor Vaccine and Immunotherapy, Xinxiang Medical University, Xinxiang 453003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zichen","family":"Hao","sequence":"additional","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Xinxiang Medical University, Xinxiang 453003, China"},{"name":"Xinxiang Key Laboratory of Tumor Vaccine and Immunotherapy, Xinxiang Medical University, Xinxiang 453003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9252-2409","authenticated-orcid":false,"given":"Junrong","family":"Jiao","sequence":"additional","affiliation":[{"name":"Key Lab for Special Functional Materials of Ministry of Education, National & Local Joint Engineering Research Center for High-Efficiency Display and Lighting Technology, School of Materials Science and Engineering, Collaborative Innovation Center of Nano Functional Materials and Applications, Henan University, Kaifeng 475004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhuangwei","family":"Lv","sequence":"additional","affiliation":[{"name":"Xinxiang Key Laboratory of Tumor Vaccine and Immunotherapy, Xinxiang Medical University, Xinxiang 453003, China"},{"name":"School of Forensic Medicine, Xinxiang Medical University, Xinxiang 453003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,10,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3244","DOI":"10.1039\/C9CS00648F","article-title":"Multifunctional sonosensitizers in sonodynamic cancer therapy","volume":"49","author":"Son","year":"2020","journal-title":"Chem. Soc. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"14212","DOI":"10.1002\/anie.201906823","article-title":"Ultrasound-Activated Sensitizers and Applications","volume":"59","author":"Lin","year":"2020","journal-title":"Angew. Chem. Int. Ed. Engl."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"100949","DOI":"10.1016\/j.nantod.2020.100949","article-title":"Ultrasound mediated therapy: Recent progress and challenges in nanoscience","volume":"35","author":"Ouyang","year":"2020","journal-title":"Nano Today"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"213610","DOI":"10.1016\/j.ccr.2020.213610","article-title":"Sonodynamic and chemodynamic therapy based on organic\/organometallic sensitizers","volume":"429","author":"He","year":"2021","journal-title":"Coord. Chem. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e1800180","DOI":"10.1002\/adma.201800180","article-title":"Metal-Organic-Framework-Derived Carbon Nanostructure Augmented Sonodynamic Cancer Therapy","volume":"30","author":"Pan","year":"2018","journal-title":"Adv. Mater."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"4477","DOI":"10.1021\/ja100192x","article-title":"Efficient Photoinduced Electron Transfer in a Porphyrin Tripod-Fullerene Supramolecular Complex via \u03c0-\u03c0 Interactions in Nonpolar Media","volume":"132","author":"Takai","year":"2010","journal-title":"J. Am. Chem. Soc."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1945","DOI":"10.1039\/D0BM01875A","article-title":"Design and Application of Inorganic Nanoparticles for Sonodynamic Cancer Therapy","volume":"9","author":"Sun","year":"2021","journal-title":"Biomater. 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Lymphoma Myeloma Leuk."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1591","DOI":"10.1007\/s00262-012-1255-z","article-title":"Activation-induced cytidine deaminase (AID) linking immunity, chronic inflammation, and cancer","volume":"61","author":"Mechtcheriakova","year":"2012","journal-title":"Cancer Immunol. Immunother."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1146\/annurev-pathol-020712-164004","article-title":"Chromosome translocation, B cell lymphoma, and activation-induced cytidine deaminase","volume":"8","author":"Robbiani","year":"2013","journal-title":"Annu. Rev. Pathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1775","DOI":"10.1038\/sj.leu.2403488","article-title":"AID is expressed in germinal center B-cell-like and activated B-cell-like diffuse large-cell lymphomas and is not correlated with intraclonal heterogeneity","volume":"18","author":"Lossos","year":"2004","journal-title":"Leukemia"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1182\/blood-2015-02-628164","article-title":"AID-associated DNA repair pathways regulate malignant transformation in a murine model of BCL6-driven diffuse large B-cell lymphoma","volume":"127","author":"Gu","year":"2016","journal-title":"Blood"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1159\/000485089","article-title":"Antioxidants Maintain Cellular Redox Homeostasis by Elimination of Reactive Oxygen Species","volume":"44","author":"He","year":"2017","journal-title":"Cell Physiol. Biochem."},{"key":"ref_22","first-page":"w13659","article-title":"Reactive oxygen species: From health to disease","volume":"142","author":"Brieger","year":"2012","journal-title":"Swiss Med. Wkly."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"491","DOI":"10.3389\/fimmu.2020.00491","article-title":"Estrogen Reverses HDAC Inhibitor-Mediated Repression of Aicda and Class-Switching in Antibody and Autoantibody Responses by Downregulation of miR-26a","volume":"11","author":"Casali","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.neo.2020.01.002","article-title":"AID assists DNMT1 to attenuate BCL6 expression through DNA methylation in diffuse large B-cell lymphoma cell lines","volume":"22","author":"Jiao","year":"2020","journal-title":"Neoplasia"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1111\/cei.13227","article-title":"AID and TET2 co-operation modulates FANCA expression by active demethylation in diffuse large B cell lymphoma","volume":"195","author":"Jiao","year":"2019","journal-title":"Clin. Exp. Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"11012","DOI":"10.1021\/acs.chemrev.5b00140","article-title":"Molecular Interactions in Organic Nanoparticles for Phototheranostic Applications","volume":"115","author":"Ng","year":"2015","journal-title":"Chem. Rev."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e2003214","DOI":"10.1002\/adma.202003214","article-title":"Recent Advances in Nanomaterial-Assisted Combinational Sonodynamic Cancer Therapy","volume":"32","author":"Liang","year":"2020","journal-title":"Adv. Mater."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1039\/C8CS00001H","article-title":"Development of organic semiconducting materials for deep-tissue optical imaging, phototherapy and photoactivation","volume":"48","author":"Li","year":"2019","journal-title":"Chem. Soc. Rev."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"13566","DOI":"10.1021\/acs.chemrev.7b00258","article-title":"Nanotechnology for Multimodal Synergistic Cancer Therapy","volume":"117","author":"Fan","year":"2017","journal-title":"Chem. Rev."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1990","DOI":"10.1021\/cr5004198","article-title":"Nanoparticles in photodynamic therapy","volume":"115","author":"Lucky","year":"2015","journal-title":"Chem. Rev."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"5490","DOI":"10.1002\/adfm.201600676","article-title":"Modulation of hypoxia in solid tumor microenvironment with MnO2 nanoparticles to enhance photodynamic therapy","volume":"26","author":"Zhu","year":"2016","journal-title":"Adv. Funct. Mater."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2365","DOI":"10.1002\/eji.201545462","article-title":"HSP90 inhibitors decrease AID levels and activity in mice and in human cells","volume":"45","author":"Litzler","year":"2015","journal-title":"Eur. J. Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"211","DOI":"10.18632\/oncotarget.1319","article-title":"AID downregulation is a novel function of the DNMT inhibitor 5-aza-deoxycytidine","volume":"5","author":"Tsai","year":"2014","journal-title":"Oncotarget"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/bs.ai.2019.11.007","article-title":"Metalloimmunology: The metal ion-controlled immunity","volume":"145","author":"Wang","year":"2020","journal-title":"Adv. Immunol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"153068","DOI":"10.1016\/j.tox.2021.153068","article-title":"Mitochondria damage and ferroptosis involved in Ni-induced hepatotoxicity in mice","volume":"466","author":"Wei","year":"2022","journal-title":"Toxicology"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1002\/jat.3749","article-title":"The use of cobalt chloride as a chemical hypoxia model","volume":"39","year":"2019","journal-title":"J. Appl. Toxicol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/s40659-019-0221-z","article-title":"CoCl2 simulated hypoxia induce cell proliferation and alter the expression pattern of hypoxia associated genes involved in angiogenesis and apoptosis","volume":"52","author":"Rana","year":"2019","journal-title":"Biol. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e1900730","DOI":"10.1002\/adma.201900730","article-title":"Ultrasmall Oxygen-Deficient Bimetallic Oxide MnWOX Nanoparticles for Depletion of Endogenous GSH and Enhanced Sonodynamic Cancer Therapy","volume":"31","author":"Gong","year":"2019","journal-title":"Adv. Mater."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"11953","DOI":"10.1021\/acsnano.1c03128","article-title":"Catalytically Active CoFe2O4 Nanoflowers for Augmented Sonodynamic and Chemodynamic Combination Therapy with Elicitation of Robust Immune Response","volume":"15","author":"Fu","year":"2021","journal-title":"ACS Nano"}],"container-title":["Molecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1420-3049\/27\/21\/7143\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:00:47Z","timestamp":1760144447000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1420-3049\/27\/21\/7143"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,22]]},"references-count":39,"journal-issue":{"issue":"21","published-online":{"date-parts":[[2022,11]]}},"alternative-id":["molecules27217143"],"URL":"https:\/\/doi.org\/10.3390\/molecules27217143","relation":{},"ISSN":["1420-3049"],"issn-type":[{"value":"1420-3049","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,22]]}}}