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

J Nanobiotechnology. 2025 Jul 11;23(1):501. doi: 10.1186/s12951-025-03588-4.

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 JAK2V617F-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.

Keywords: Bone marrow targeting; Deubiquitinating enzyme; Mesenchymal stem cells; Myeloproliferative neoplasms.

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Bone Marrow* / drug effects
  • Bone Marrow* / metabolism
  • Cell Proliferation / drug effects
  • Exosomes* / chemistry
  • Exosomes* / metabolism
  • Humans
  • Mesenchymal Stem Cells / drug effects
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Myeloproliferative Disorders* / drug therapy
  • Myeloproliferative Disorders* / metabolism
  • Receptors, CXCR4 / metabolism
  • Ubiquitin-Specific Proteases* / antagonists & inhibitors
  • Ubiquitin-Specific Proteases* / metabolism

Substances

  • Ubiquitin-Specific Proteases
  • Receptors, CXCR4