Immune landscape of isocitrate dehydrogenase-stratified primary and recurrent human gliomas

Neuro Oncol. 2024 Dec 5;26(12):2239-2255. doi: 10.1093/neuonc/noae139.

Abstract

Background: Human gliomas are classified using isocitrate dehydrogenase (IDH) status as a prognosticator; however, the influence of genetic differences and treatment effects on ensuing immunity remains unclear.

Methods: In this study, we used sequential single-cell transcriptomics on 144 678 and spectral cytometry on over 2 million immune cells encompassing 48 human gliomas to decipher their immune landscape.

Results: We identified 22 distinct immune cell types that contribute to glioma immunity. Specifically, brain-resident microglia (MG) were reduced with a concomitant increase in CD8+ T lymphocytes during glioma recurrence independent of IDH status. In contrast, IDH-wild type-associated patterns, such as an abundance of antigen-presenting cell-like MG and cytotoxic CD8+ T cells, were observed. Beyond elucidating the differences in IDH, relapse, and treatment-associated immunity, we discovered novel inflammatory MG subpopulations expressing granulysin, a cytotoxic peptide that is otherwise expressed in lymphocytes only. Furthermore, we provide a robust genomic framework for defining macrophage polarization beyond M1/M2 paradigm and reference signatures of glioma-specific tumor immune microenvironment (termed GlioTIME-36) for deconvoluting transcriptomic datasets.

Conclusions: This study provides advanced optics of the human pan-glioma immune contexture as a valuable guide for translational and clinical applications.

Keywords: glioma; isocitrate dehydrogenase; microglia; tumor immune microenvironment.

MeSH terms

  • Biomarkers, Tumor / genetics
  • Brain Neoplasms* / genetics
  • Brain Neoplasms* / immunology
  • Brain Neoplasms* / pathology
  • CD8-Positive T-Lymphocytes / immunology
  • Glioma* / genetics
  • Glioma* / immunology
  • Glioma* / pathology
  • Humans
  • Isocitrate Dehydrogenase* / genetics
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Microglia / immunology
  • Microglia / metabolism
  • Microglia / pathology
  • Mutation
  • Neoplasm Recurrence, Local* / genetics
  • Neoplasm Recurrence, Local* / immunology
  • Neoplasm Recurrence, Local* / pathology
  • Prognosis
  • Single-Cell Analysis
  • Transcriptome
  • Tumor Microenvironment* / immunology

Substances

  • Isocitrate Dehydrogenase
  • Biomarkers, Tumor