Deciphering the role of the MALT1-RC3H1 axis in regulating GPX4 protein stability

Proc Natl Acad Sci U S A. 2025 Jan 7;122(1):e2419625121. doi: 10.1073/pnas.2419625121. Epub 2024 Dec 31.

Abstract

Ferroptosis, a unique form of iron-dependent cell death triggered by lipid peroxidation accumulation, holds great promise for cancer therapy. Despite the crucial role of GPX4 in regulating ferroptosis, our understanding of GPX4 protein regulation remains limited. Through FACS-based genome-wide CRISPR screening, we identified MALT1 as a regulator of GPX4 protein. Inhibition of MALT1 expression enhances GPX4 ubiquitination-mediated degradation by up-regulating the E3 ubiquitin ligase RC3H1. Using both rescue assays and functional genetic screening, we demonstrate that pharmacologically targeting MALT1 triggers ferroptosis in liver cancer cells. Moreover, we show that targeting MALT1 synergizes with sorafenib or regorafenib to induce ferroptosis across multiple cancer types. These findings elucidate the modulatory effects of the MALT1-RC3H1 axis on GPX4 stability, revealing a molecular mechanism that could be exploited to induce ferroptosis for cancer therapy.

Keywords: GPX4; MALT1; ferroptosis; liver cancer.

MeSH terms

  • Cell Line, Tumor
  • Ferroptosis* / genetics
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Liver Neoplasms / drug therapy
  • Liver Neoplasms / genetics
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein* / genetics
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein* / metabolism
  • Phenylurea Compounds / pharmacology
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / genetics
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / metabolism
  • Protein Stability*
  • Pyridines
  • Sorafenib* / pharmacology
  • Ubiquitin-Protein Ligases* / genetics
  • Ubiquitin-Protein Ligases* / metabolism
  • Ubiquitination

Substances

  • Phospholipid Hydroperoxide Glutathione Peroxidase
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein
  • Ubiquitin-Protein Ligases
  • MALT1 protein, human
  • Sorafenib
  • regorafenib
  • Phenylurea Compounds
  • Pyridines