TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT

EMBO Mol Med. 2022 Oct 10;14(10):e15859. doi: 10.15252/emmm.202215859. Epub 2022 Aug 3.

Abstract

In some types of cancer, telomere length is maintained by the alternative lengthening of telomeres (ALT) mechanism. In many ALT cancers, the α-thalassemia/mental retardation syndrome X-linked (ATRX) gene is mutated leading to the conclusion that the ATRX complex represses ALT. Here, we report that most high-grade pediatric osteosarcomas maintain their telomeres by ALT, and that the majority of these ALT tumors are ATRX wild-type (wt) and instead carry an amplified 17p11.2 chromosomal region containing TOP3A. We found that TOP3A was overexpressed in the ALT-positive ATRX-wt tumors consistent with its amplification. We demonstrated the functional significance of these results by showing that TOP3A overexpression in ALT cancer cells countered ATRX-mediated ALT inhibition and that TOP3A knockdown disrupted the ALT phenotype in ATRX-wt cells. Moreover, we report that TOP3A is required for proper BLM localization and promotes ALT DNA synthesis in ALT cell lines. Collectively, our results identify TOP3A as a major ALT player and potential therapeutic target.

Keywords: ATRX; TOP3A; alternative lengthening of telomeres; osteosarcomas; telomeres.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA
  • DNA Helicases / genetics
  • DNA Topoisomerases, Type I* / genetics
  • Humans
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Osteosarcoma* / genetics
  • Telomere / genetics
  • Telomere / metabolism
  • Telomere Homeostasis
  • X-linked Nuclear Protein* / genetics

Substances

  • Nuclear Proteins
  • DNA
  • DNA Helicases
  • ATRX protein, human
  • X-linked Nuclear Protein
  • TOP3A protein, human
  • DNA Topoisomerases, Type I