USP52 inhibits cell ferroptosis via Hippo-YAP pathway and blocks immunotherapy in colorectal cancer

J Biol Chem. 2025 Nov;301(11):110725. doi: 10.1016/j.jbc.2025.110725. Epub 2025 Sep 15.

Abstract

Colorectal cancer (CRC) is one of the most prevalent malignancies in humans. Understanding its molecular mechanisms to guide clinical management is crucial. Ferroptosis represents a novel form of regulated cell death that is characterized by highly iron-dependent lipid peroxidation. Despite growing interest, the roles and vulnerabilities determining ferroptosis sensitivity in CRC remain unclear. In this study, we identified ubiquitin-specific peptidase 52 (USP52) as a specific deubiquitinating enzyme of Yes-associated protein (YAP) in CRC, which could stabilize YAP by removing the K11-linked ubiquitin chains. USP52 knockdown decreased the expression of YAP protein and its target gene (CTGF, CYR61). Through a series of comprehensive in vivo and in vitro experiments, we proved that USP52 promoted CRC cell proliferation, migration, and invasion and attenuated the sensitivity of CRC cells to ferroptosis. Notably, USP52 inhibition retarded tumor growth and enhanced CD8+ T-cell infiltration, which potentiated tumor response to anti-programmed death-ligand-1 immunotherapy in vivo. In general, our research uncovered that USP52 suppressed ferroptosis through the Hippo-YAP signaling and highlighted targeting USP52 as a potential therapeutic strategy to boost ferroptosis for enhancing cancer immunotherapy.

Keywords: Hippo/YAP pathway; colorectal cancer; ferroptosis; immunotherapy; ubiquitin specific peptidase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing* / metabolism
  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • Colorectal Neoplasms* / immunology
  • Colorectal Neoplasms* / metabolism
  • Colorectal Neoplasms* / pathology
  • Colorectal Neoplasms* / therapy
  • Ferroptosis*
  • Hippo Signaling Pathway
  • Humans
  • Immunotherapy*
  • Mice
  • Mice, Nude
  • Protein Serine-Threonine Kinases* / metabolism
  • Signal Transduction
  • Transcription Factors* / metabolism
  • Ubiquitin-Specific Proteases* / genetics
  • Ubiquitin-Specific Proteases* / metabolism
  • YAP-Signaling Proteins

Substances

  • YAP-Signaling Proteins
  • YAP1 protein, human
  • Protein Serine-Threonine Kinases
  • Ubiquitin-Specific Proteases
  • Adaptor Proteins, Signal Transducing
  • Transcription Factors