USP5 inhibition via bone marrow-targeted engineered exosomes for myeloproliferative neoplasms therapy

Abstract Myeloproliferative neoplasms (MPNs) are challenging to treat due to the complex bone marrow (BM) microenvironment and lack of curative therapies. Current treatments fail to eliminate malignant clones and face issues like drug resistance. This study addressed these challenges by identifying...

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Main Authors: Wenjun Wang, Yufeng Jiang, Donglei Zhang, Xian Zhang, Qian Liang, Jun Shi, Yuan Zhou, Fuling Zhou
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Journal of Nanobiotechnology
Subjects:
Online Access:https://doi.org/10.1186/s12951-025-03588-4
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author Wenjun Wang
Yufeng Jiang
Donglei Zhang
Xian Zhang
Qian Liang
Jun Shi
Yuan Zhou
Fuling Zhou
author_facet Wenjun Wang
Yufeng Jiang
Donglei Zhang
Xian Zhang
Qian Liang
Jun Shi
Yuan Zhou
Fuling Zhou
author_sort Wenjun Wang
collection DOAJ
description Abstract Myeloproliferative neoplasms (MPNs) are challenging to treat due to the complex bone marrow (BM) microenvironment and lack of curative therapies. Current treatments fail to eliminate malignant clones and face issues like drug resistance. This study addressed these challenges by identifying USP5 as a critical regulator in JAK2 V617F-mutated mesenchymal stem cells (MSCs), which promotes proliferation by suppressing Caspase-3-mediated apoptosis. We developed engineered exosomes (USP5@Exosome-CP) co-expressing CXCR4 and a P-selectin-targeting peptide to enhance BM targeting. These exosomes, loaded with the USP5 inhibitor USP5-IN-1, demonstrated efficient BM homing and sustained drug release. In MPN mouse models, USP5@Exosome-CP significantly reduced MSC proliferation, extended survival, and showed minimal systemic toxicity. Transcriptomic analysis revealed that USP5 knockdown activated apoptosis pathways and suppressed oncogenic signaling. Our results establish USP5 as a therapeutic target and validate the engineered exosome platform as a promising strategy for MPN treatment, offering a blueprint for targeting other hematologic malignancies. This approach combines USP5 inhibition with BM-targeted nanotechnology, providing a proof-of-concept for personalized MPN therapy with improved efficacy and reduced off-target effects.
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institution Kabale University
issn 1477-3155
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publishDate 2025-07-01
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series Journal of Nanobiotechnology
spelling doaj-art-1e6c973af8ca42f8b11b0b16b7e5480e2025-08-20T04:03:07ZengBMCJournal of Nanobiotechnology1477-31552025-07-0123111810.1186/s12951-025-03588-4USP5 inhibition via bone marrow-targeted engineered exosomes for myeloproliferative neoplasms therapyWenjun Wang0Yufeng Jiang1Donglei Zhang2Xian Zhang3Qian Liang4Jun Shi5Yuan Zhou6Fuling Zhou7Department of Hematology, Zhongnan Hospital of Wuhan University, Wuhan UniversitySchool of Information and Mathematics, Yangtze UniversityDepartment of Hematology, Zhongnan Hospital of Wuhan University, Wuhan UniversityDepartment of Hematology, Zhongnan Hospital of Wuhan University, Wuhan UniversityState Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Institute of Hematology & Blood Diseases Hospital, National Clinical Research Center for Blood Diseases, Chinese Academy of Medical Sciences & Peking Union Medical CollegeState Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Institute of Hematology & Blood Diseases Hospital, National Clinical Research Center for Blood Diseases, Chinese Academy of Medical Sciences & Peking Union Medical CollegeState Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Institute of Hematology & Blood Diseases Hospital, National Clinical Research Center for Blood Diseases, Chinese Academy of Medical Sciences & Peking Union Medical CollegeDepartment of Hematology, Zhongnan Hospital of Wuhan University, Wuhan UniversityAbstract Myeloproliferative neoplasms (MPNs) are challenging to treat due to the complex bone marrow (BM) microenvironment and lack of curative therapies. Current treatments fail to eliminate malignant clones and face issues like drug resistance. This study addressed these challenges by identifying USP5 as a critical regulator in JAK2 V617F-mutated mesenchymal stem cells (MSCs), which promotes proliferation by suppressing Caspase-3-mediated apoptosis. We developed engineered exosomes (USP5@Exosome-CP) co-expressing CXCR4 and a P-selectin-targeting peptide to enhance BM targeting. These exosomes, loaded with the USP5 inhibitor USP5-IN-1, demonstrated efficient BM homing and sustained drug release. In MPN mouse models, USP5@Exosome-CP significantly reduced MSC proliferation, extended survival, and showed minimal systemic toxicity. Transcriptomic analysis revealed that USP5 knockdown activated apoptosis pathways and suppressed oncogenic signaling. Our results establish USP5 as a therapeutic target and validate the engineered exosome platform as a promising strategy for MPN treatment, offering a blueprint for targeting other hematologic malignancies. This approach combines USP5 inhibition with BM-targeted nanotechnology, providing a proof-of-concept for personalized MPN therapy with improved efficacy and reduced off-target effects.https://doi.org/10.1186/s12951-025-03588-4Myeloproliferative neoplasmsMesenchymal stem cellsDeubiquitinating enzymeBone marrow targeting
spellingShingle Wenjun Wang
Yufeng Jiang
Donglei Zhang
Xian Zhang
Qian Liang
Jun Shi
Yuan Zhou
Fuling Zhou
USP5 inhibition via bone marrow-targeted engineered exosomes for myeloproliferative neoplasms therapy
Journal of Nanobiotechnology
Myeloproliferative neoplasms
Mesenchymal stem cells
Deubiquitinating enzyme
Bone marrow targeting
title USP5 inhibition via bone marrow-targeted engineered exosomes for myeloproliferative neoplasms therapy
title_full USP5 inhibition via bone marrow-targeted engineered exosomes for myeloproliferative neoplasms therapy
title_fullStr USP5 inhibition via bone marrow-targeted engineered exosomes for myeloproliferative neoplasms therapy
title_full_unstemmed USP5 inhibition via bone marrow-targeted engineered exosomes for myeloproliferative neoplasms therapy
title_short USP5 inhibition via bone marrow-targeted engineered exosomes for myeloproliferative neoplasms therapy
title_sort usp5 inhibition via bone marrow targeted engineered exosomes for myeloproliferative neoplasms therapy
topic Myeloproliferative neoplasms
Mesenchymal stem cells
Deubiquitinating enzyme
Bone marrow targeting
url https://doi.org/10.1186/s12951-025-03588-4
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