IL-1β-mediated suppression of CIITA attenuates IFN-γ-induced MHC-II expression on Fibroblasts

Cell Commun Signal. 2025 Dec 10;24(1):25. doi: 10.1186/s12964-025-02575-4.

Abstract

Background: Cancer-associated fibroblasts (CAFs) are key regulators in tumor microenvironment and tumor immunity, partly through MHC-II expression that modulates T-cell differentiation. However, the upstream cytokine signals controlling MHC-II expression in fibroblasts still remain poorly defined.

Methods: We examined MHC-II expression on fibroblasts under stimulation with interferon-γ (IFN-γ) and interleukin-1β (IL-1β) by using flow cytometry, transcriptomic analysis, and qRT-PCR. To dissect transcriptional regulation, we generated CIITA-overexpressing and CIITA-deficient fibroblast lines by lentiviral transduction and CRISPR/Cas9-mediated editing. Public scRNA-seq, ATAC-seq, and ChIP-seq datasets were further analyzed to validate molecular mechanisms.

Results: IFN-γ robustly up-regulated MHC-II expression on fibroblasts, while IL-1β selectively suppressed this induction without affecting PD-L1. Mechanistically, IL-1β attenuated IFN-γ-induced CIITA expression at the mRNA level but did not alter STAT1 abundance or phosphorylation. Functional assays confirmed that CIITA was indispensable for IFN-γ-driven MHC-II expression in fibroblasts. Integration of transcriptomic and epigenomic data demonstrated that CIITA directly bound MHC-II gene promoters and regulated chromatin accessibility.

Conclusions: Our study identifies an IFN-γ/STAT1/CIITA axis as the central regulator of MHC-II expression in fibroblasts and reveals IL-1β as a potent suppressor of this pathway. These findings highlight a novel cytokine-mediated regulatory mechanism underlying CAF-driven immunosuppression within the tumor microenvironment.

Keywords: CIITA; Fibroblasts; IFN-γ; IL-1β; MHC-II.

MeSH terms

  • Fibroblasts* / drug effects
  • Fibroblasts* / metabolism
  • Histocompatibility Antigens Class II* / genetics
  • Histocompatibility Antigens Class II* / metabolism
  • Humans
  • Interferon-gamma* / metabolism
  • Interferon-gamma* / pharmacology
  • Interleukin-1beta* / metabolism
  • Interleukin-1beta* / pharmacology
  • Nuclear Proteins* / genetics
  • Nuclear Proteins* / metabolism
  • STAT1 Transcription Factor / metabolism
  • Trans-Activators* / genetics
  • Trans-Activators* / metabolism

Substances

  • MHC class II transactivator protein
  • Interferon-gamma
  • Interleukin-1beta
  • Trans-Activators
  • Nuclear Proteins
  • Histocompatibility Antigens Class II
  • STAT1 Transcription Factor