HOXD12 defines an age-related aggressive subtype of oligodendroglioma

Acta Neuropathol. 2024 Sep 11;148(1):41. doi: 10.1007/s00401-024-02802-1.

Abstract

Oligodendroglioma, IDH-mutant and 1p/19q-codeleted has highly variable outcomes that are strongly influenced by patient age. The distribution of oligodendroglioma age is non-Gaussian and reportedly bimodal, which motivated our investigation of age-associated molecular alterations that may drive poorer outcomes. We found that elevated HOXD12 expression was associated with both older patient age and shorter survival in the TCGA (FDR < 0.01, FDR = 1e-5) and the CGGA (p = 0.03, p < 1e-3). HOXD12 gene body hypermethylation was associated with older age, higher WHO grade, and shorter survival in the TCGA (p < 1e-6, p < 0.001, p < 1e-3) and with older age and higher WHO grade in Capper et al. (p < 0.002, p = 0.014). In the TCGA, HOXD12 gene body hypermethylation and elevated expression were independently prognostic of NOTCH1 and PIK3CA mutations, loss of 15q, MYC activation, and standard histopathological features. Single-nucleus RNA and ATAC sequencing data showed that HOXD12 activity was elevated in neoplastic tissue, particularly within cycling and OPC-like cells, and was associated with a stem-like phenotype. A pan-HOX DNA methylation analysis revealed an age and survival-associated HOX-high signature that was tightly associated with HOXD12 gene body methylation. Overall, HOXD12 expression and gene body hypermethylation were associated with an older, atypically aggressive subtype of oligodendroglioma.

Keywords: ATAC-seq; DNA methylation; HOX; HOXD12; Oligodendroglioma; RNA-Seq.

MeSH terms

  • Adult
  • Age Factors
  • Aged
  • Brain Neoplasms* / genetics
  • Brain Neoplasms* / metabolism
  • Brain Neoplasms* / pathology
  • DNA Methylation
  • Female
  • Homeodomain Proteins* / genetics
  • Homeodomain Proteins* / metabolism
  • Humans
  • Male
  • Middle Aged
  • Mutation
  • Oligodendroglioma* / genetics
  • Oligodendroglioma* / pathology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Homeodomain Proteins
  • Transcription Factors
  • HOXD12 protein, human