Halofuginone Disrupted Collagen Deposition via mTOR-eIF2α-ATF4 Axis to Enhance Chemosensitivity in Ovarian Cancer

Adv Sci (Weinh). 2025 May;12(19):e2416523. doi: 10.1002/advs.202416523. Epub 2025 Mar 24.

Abstract

The interplay between cancer-associated fibroblasts (CAFs) and extracellular matrix (ECM) mediates progress, metastasis, and therapy resistance. However, strategy of targeting ECM remodeling to enhance chemosensitivity in ovarian cancer remains elusive. Here, a 22-gene matrisome signature predicts chemotherapy response and survival in ovarian cancer. The dense, collagen-rich ECM secreted by CAFs harbors more M2 tumor-associated macrophages (TAMs) than the looser ECM based on single cell RNA-seq (scRNA-seq) of ovarian cancer, suggesting the promising approach of targeting collagen to remodel ECM. An integrated analysis identifies collagen type I alpha 1 chain (COL1A1) as a major component of the ECM that contributes to chemoresistance and poor prognosis, highlighting its potential as a therapeutic target. Halofuginone (HF), a clinically active derivative of febrifugine, is identified as a COL1A1-targeting natural compound by screening the Encyclopedia of Traditional Chinese Medicine (ETCM). Mechanistically, HF inhibits COL1A1 production via the mTOR-eIF2α-ATF4 axis in CAFs. Notably, HF disrupts collagen deposition and promotes CD8+ T cell infiltration, partially via M2-M1 macrophage polarization to enhance chemosensitivity. Overall, the findings suggest that HF combined with chemotherapy is a promising and effective treatment for ovarian cancer.

Keywords: COL1A1; cancer‐associated fibroblasts (CAFs); extracellular matrix; fibrosis; halofuginone; ovarian cancer.

MeSH terms

  • Activating Transcription Factor 4 / metabolism
  • Animals
  • Cancer-Associated Fibroblasts / drug effects
  • Cancer-Associated Fibroblasts / metabolism
  • Cell Line, Tumor
  • Collagen Type I, alpha 1 Chain
  • Collagen* / metabolism
  • Drug Resistance, Neoplasm / drug effects
  • Eukaryotic Initiation Factor-2 / metabolism
  • Extracellular Matrix / drug effects
  • Extracellular Matrix / metabolism
  • Female
  • Humans
  • Mice
  • Ovarian Neoplasms* / drug therapy
  • Ovarian Neoplasms* / genetics
  • Ovarian Neoplasms* / metabolism
  • Ovarian Neoplasms* / pathology
  • Piperidines* / pharmacology
  • Quinazolinones* / pharmacology
  • Quinazolinones* / therapeutic use
  • Signal Transduction / drug effects
  • TOR Serine-Threonine Kinases* / metabolism

Substances

  • halofuginone
  • Quinazolinones
  • TOR Serine-Threonine Kinases
  • Activating Transcription Factor 4
  • Piperidines
  • Eukaryotic Initiation Factor-2
  • Collagen
  • MTOR protein, human
  • ATF4 protein, human
  • Collagen Type I, alpha 1 Chain