Two opposing gene expression patterns within ATRX aberrant neuroblastoma

PLoS One. 2023 Aug 4;18(8):e0289084. doi: 10.1371/journal.pone.0289084. eCollection 2023.

Abstract

Neuroblastoma is the most common extracranial solid tumor in children. A subgroup of high-risk patients is characterized by aberrations in the chromatin remodeller ATRX that is encoded by 35 exons. In contrast to other pediatric cancer where ATRX point mutations are most frequent, multi-exon deletions (MEDs) are the most frequent type of ATRX aberrations in neuroblastoma. 75% of these MEDs are predicted to produce in-frame fusion proteins, suggesting a potential gain-of-function effect compared to nonsense mutations. For neuroblastoma there are only a few patient-derived ATRX aberrant models. Therefore, we created isogenic ATRX aberrant models using CRISPR-Cas9 in several neuroblastoma cell lines and one tumoroid and performed total RNA-sequencing on these and the patient-derived models. Gene set enrichment analysis (GSEA) showed decreased expression of genes related to both ribosome biogenesis and several metabolic processes in our isogenic ATRX exon 2-10 MED model systems, the patient-derived MED models and in tumor data containing two patients with an ATRX exon 2-10 MED. In sharp contrast, these same processes showed an increased expression in our isogenic ATRX knock-out and exon 2-13 MED models. Our validations confirmed a role of ATRX in the regulation of ribosome homeostasis. The two distinct molecular expression patterns within ATRX aberrant neuroblastomas that we identified imply that there might be a need for distinct treatment regimens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Child
  • Chromatin
  • Gene Expression
  • Humans
  • Neuroblastoma* / genetics
  • Neuroblastoma* / pathology
  • X-linked Nuclear Protein / genetics

Substances

  • X-linked Nuclear Protein
  • Chromatin
  • ATRX protein, human

Grants and funding

The research in this paper was supported by funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme under grant agreement numbers 716079 (Predict) and 826121 (iPC project). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.