1p/19q co-deletion status is associated with distinct tumor-associated macrophage infiltration in IDH mutated lower-grade gliomas

Cell Oncol (Dordr). 2021 Feb;44(1):193-204. doi: 10.1007/s13402-020-00561-1. Epub 2020 Sep 11.

Abstract

Background: Tumor-associated macrophages (TAM)s are critical regulators of glioma progression. As yet, however, TAMs in isocitrate dehydrogenase (IDH) mutated lower-grade gliomas (LGGs) have not been thoroughly investigated. The aim of this study was to determine whether 1p/19q co-deletion status affects the TAM phenotype or its prevalence in IDH mutated LGGs.

Methods: TAMs in IDH mutated LGGs were analyzed using transcriptome data from 230 samples in the TCGA database in combination with transcriptome data from single-cell RNA sequencing of IDH-mutated LGGs. Proteins potentially involved in TAM regulation were examined by immuno-staining in primary LGG samples harboring IDH mutations. Essential signaling pathways regulating TAM phenotypes were investigated in a glioma mouse model using small molecule inhibitors.

Results: Most of the TAMs in IDH-mutated LGGs expressed the M1 activation markers CD86 and TNF, whereas a subset of individual TAMs co-expressed both M1 and M2-related markers. Bioinformatics analysis in combination with immuno-staining of IDH-mutated patient samples revealed higher amounts of TAMs expressing M2-related markers in 1p/19q non-codeletion IDH-mutated LGGs compared to 1p/19q codeletion LGGs. The levels of transforming growth factor beta 1 (TGFβ1) and macrophage colony-stimulating factor (M-CSF) were significantly higher in 1p/19q non-codeletion LGGs than in 1p/19q codeletion LGGs. M-CSF and TGFβ1 signal inhibition decreased tumor growth and modulated the TAM phenotype in a glioma mouse model.

Conclusions: Our data indicate that 1p/19q co-deletion status relates to distinct TAM infiltration in gliomas, which is likely mediated by M-CSF and TGFβ1 signaling. M-CSF and TGFβ1 signaling may play a pivotal role in regulating the TAM phenotype in glioma.

Keywords: 1p/19q; Glioma; LGG; Tumor-associated macrophage.

MeSH terms

  • Animals
  • Brain Neoplasms / genetics*
  • Brain Neoplasms / pathology
  • Chromosome Deletion*
  • Chromosomes, Human, Pair 1 / genetics*
  • Chromosomes, Human, Pair 19 / genetics*
  • Disease Progression
  • Female
  • Glioma / genetics*
  • Glioma / pathology
  • Humans
  • Isocitrate Dehydrogenase / genetics*
  • Macrophage Colony-Stimulating Factor / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Monocytes / pathology
  • Mutation / genetics*
  • Neoplasm Grading
  • Phenotype
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • THP-1 Cells
  • Transforming Growth Factor beta1 / metabolism
  • Tumor-Associated Macrophages / metabolism
  • Tumor-Associated Macrophages / pathology*

Substances

  • CSF1R protein, human
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor
  • Transforming Growth Factor beta1
  • Macrophage Colony-Stimulating Factor
  • Isocitrate Dehydrogenase