Glioblastomas with primitive neuronal component harbor a distinct methylation and copy-number profile with inactivation of TP53, PTEN, and RB1

Acta Neuropathol. 2021 Jul;142(1):179-189. doi: 10.1007/s00401-021-02302-6. Epub 2021 Apr 19.

Abstract

Glioblastoma IDH-wildtype presents with a wide histological spectrum. Some features are so distinctive that they are considered as separate histological variants or patterns for the purpose of classification. However, these usually lack defined (epi-)genetic alterations or profiles correlating with this histology. Here, we describe a molecular subtype with overlap to the unique histological pattern of glioblastoma with primitive neuronal component. Our cohort consists of 63 IDH-wildtype glioblastomas that harbor a characteristic DNA methylation profile. Median age at diagnosis was 59.5 years. Copy-number variations and genetic sequencing revealed frequent alterations in TP53, RB1 and PTEN, with fewer gains of chromosome 7 and homozygous CDKN2A/B deletions than usually described for IDH-wildtype glioblastoma. Gains of chromosome 1 were detected in more than half of the cases. A poorly differentiated phenotype with frequent absence of GFAP expression, high proliferation index and strong staining for p53 and TTF1 often caused misleading histological classification as carcinoma metastasis or primitive neuroectodermal tumor. Clinically, many patients presented with leptomeningeal dissemination and spinal metastasis. Outcome was poor with a median overall survival of only 12 months. Overall, we describe a new molecular subtype of IDH-wildtype glioblastoma with a distinct histological appearance and genetic signature.

Keywords: Classification; DNA methylation; GBM; PNET; Phenotype; Plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain Neoplasms / genetics*
  • Brain Neoplasms / pathology*
  • Chromosomes, Human, Pair 1 / genetics
  • Chromosomes, Human, Pair 7 / genetics
  • Cohort Studies
  • Cyclin-Dependent Kinase Inhibitor p16 / genetics
  • DNA Copy Number Variations
  • DNA Methylation*
  • Female
  • Gene Deletion
  • Glial Fibrillary Acidic Protein / biosynthesis
  • Glial Fibrillary Acidic Protein / genetics
  • Glioblastoma / genetics*
  • Glioblastoma / pathology*
  • Humans
  • Male
  • Middle Aged
  • Neuroectodermal Tumors, Primitive / genetics*
  • Neuroectodermal Tumors, Primitive / pathology*
  • PTEN Phosphohydrolase / genetics*
  • Retinoblastoma Binding Proteins / genetics*
  • Tumor Suppressor Protein p53 / genetics*
  • Ubiquitin-Protein Ligases / genetics*

Substances

  • CDKN2A protein, human
  • Cyclin-Dependent Kinase Inhibitor p16
  • GFAP protein, human
  • Glial Fibrillary Acidic Protein
  • RB1 protein, human
  • Retinoblastoma Binding Proteins
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Ubiquitin-Protein Ligases
  • PTEN Phosphohydrolase
  • PTEN protein, human