Lnc-H19-derived protein shapes the immunosuppressive microenvironment of glioblastoma

Cell Rep Med. 2024 Nov 19;5(11):101806. doi: 10.1016/j.xcrm.2024.101806. Epub 2024 Oct 30.

Abstract

The immunosuppressive tumor microenvironment (TME) is a prominent feature of glioblastoma (GBM), the most lethal primary brain cancer resistant to current immunotherapies. The mechanisms underlying GBM-TME remain to be explored. We report that long non-coding RNA (LncRNA) H19 encodes an immune-related protein called H19-IRP. Functionally separated from H19 RNA, H19-IRP promotes GBM immunosuppression by binding to the CCL2 and Galectin-9 promoters and activating their transcription, thereby recruiting myeloid-derived suppressor cells (MDSCs) and tumor-associated macrophages (TAMs), leading to T cell exhaustion and an immunosuppressive GBM-TME. H19-IRP, overexpressed in clinical GBM samples, acts as a tumor-associated antigen (TAA) presented by major histocompatibility complex class I (MHC-I). A circular RNA vaccine targeting H19-IRP (circH19-vac) triggers a potent cytotoxic T cell response against GBM and inhibits GBM growth. Our results highlight the unrevealed function of H19-IRP in creating immunosuppressive GBM-TME by recruiting MDSCs and TAMs, supporting the idea of targeting H19-IRP with cancer vaccine for GBM treatment.

Keywords: GBM; H19; H19-IRP; LncRNA; TME; circular RNA vaccine; immunotherapy.

MeSH terms

  • Animals
  • Antigens, Neoplasm / genetics
  • Antigens, Neoplasm / immunology
  • Antigens, Neoplasm / metabolism
  • Brain Neoplasms* / genetics
  • Brain Neoplasms* / immunology
  • Brain Neoplasms* / pathology
  • Cancer Vaccines / immunology
  • Cell Line, Tumor
  • Chemokine CCL2* / genetics
  • Chemokine CCL2* / immunology
  • Chemokine CCL2* / metabolism
  • Galectins* / genetics
  • Galectins* / immunology
  • Galectins* / metabolism
  • Gene Expression Regulation, Neoplastic
  • Glioblastoma* / genetics
  • Glioblastoma* / immunology
  • Glioblastoma* / pathology
  • Humans
  • Macrophages / immunology
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Myeloid-Derived Suppressor Cells* / immunology
  • Myeloid-Derived Suppressor Cells* / metabolism
  • Promoter Regions, Genetic / genetics
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / immunology
  • T-Lymphocytes, Cytotoxic / immunology
  • Tumor Microenvironment* / immunology

Substances

  • RNA, Long Noncoding
  • H19 long non-coding RNA
  • Galectins
  • Chemokine CCL2
  • LGALS9 protein, human
  • Antigens, Neoplasm
  • CCL2 protein, human
  • Cancer Vaccines