Transcriptomics-based characterization of the immuno-stromal microenvironment in pediatric low-grade glioma

Oncoimmunology. 2024 Aug 9;13(1):2386789. doi: 10.1080/2162402X.2024.2386789. eCollection 2024.

Abstract

Immunologic treatment options are uncommon in low-grade gliomas, although such therapies might be beneficial for inoperable and aggressive cases. Knowledge of the immune and stromal cells in low-grade gliomas is highly relevant for such approaches but still needs to be improved. Published gene-expression data from 400 low-grade gliomas and 193 high-grade gliomas were gathered to quantify 10 microenvironment cell populations with a deconvolution method designed explicitly for brain tumors. First, we investigated general differences in the microenvironment of low- and high-grade gliomas. Lower-grade and high-grade tumors cluster together, respectively, and show a general similarity within and distinct differences between these groups, the main difference being a higher infiltration of fibroblasts and T cells in high-grade gliomas. Among the analyzed entities, gangliogliomas and pleomorphic xanthoastrocytomas presented the highest overall immune cell infiltration. Further analyses of the low-grade gliomas presented three distinct microenvironmental signatures of immune cell infiltration, which can be divided into T-cell/dendritic/natural killer cell-, neutrophilic/B lineage/natural killer cell-, and monocytic/vascular/stromal-cell-dominated immune clusters. These clusters correlated with tumor location, age, and histological diagnosis but not with sex or progression-free survival. A survival analysis showed that the prognosis can be predicted from gene expression, clinical data, and a combination of both with a support vector machine and revealed the negative prognostic relevance of vascular markers. Overall, our work shows that low- and high-grade gliomas can be characterized and differentiated by their immune cell infiltration. Low-grade gliomas cluster into three distinct immunologic tumor microenvironments, which may be of further interest for upcoming immunotherapeutic research.

Keywords: Astrocytoma; deconvolution; gene expression; low-grade glioma; tumor microenvironment.

MeSH terms

  • Adolescent
  • Brain Neoplasms* / genetics
  • Brain Neoplasms* / immunology
  • Brain Neoplasms* / pathology
  • Child
  • Child, Preschool
  • Female
  • Gene Expression Profiling
  • Glioma* / genetics
  • Glioma* / immunology
  • Glioma* / pathology
  • Humans
  • Male
  • Neoplasm Grading
  • Stromal Cells / immunology
  • Stromal Cells / metabolism
  • Stromal Cells / pathology
  • Transcriptome
  • Tumor Microenvironment* / genetics
  • Tumor Microenvironment* / immunology

Grants and funding

The work was supported by the Fördergemeinschaft Kinderkrebs-Zentrum Hamburg and the Open Access Publication Fund of UKE - Universitätsklinikum Hamburg-Eppendorf.