Loss of ATRX suppresses ATM dependent DNA damage repair by modulating H3K9me3 to enhance temozolomide sensitivity in glioma

Cancer Lett. 2018 Apr 10:419:280-290. doi: 10.1016/j.canlet.2018.01.056. Epub 2018 Jan 31.

Abstract

Mutations in ATRX constitute the most prevalent genetic abnormalities in gliomas. The presence of ATRX mutations in glioma serves as a marker of better prognosis with longer patient survival although the underlying mechanisms are poorly understood. In the present study, we found that ATRX biological function was significantly involved in DNA replication and repair. CRISPR/Cas9-mediated genetic inactivation of ATRX induced inhibition of cell proliferation, invasion and vasculogenic mimicry. In addition, temozolomide (TMZ) treatment induced greater DNA damage and apoptotic changes in ATRX knockout glioma cells. Moreover, we confirmed that ATRX knockout resulted in a failure to trigger ATM phosphorylation and finally restrained the activation of downstream proteins of the ATM pathway. The ATM-associated DNA repair pathway was extensively compromised in ATRX knockout cells owing to decreased histone H3K9me3 availability. Public databases also showed that patients with low ATRX expression exhibited preferable overall survival and profited more from TMZ treatment. These data suggest that ATRX is involved in DNA damage repair by regulating the ATM pathway and might serve as a prognostic maker in predicting TMZ chemosensitivity.

Keywords: ATM; ATRX; Chemoresistance; DNA damage repair; Glioblastoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents, Alkylating / pharmacology
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / metabolism*
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • DNA Damage*
  • DNA Repair*
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Gene Knockout Techniques
  • Glioma / drug therapy
  • Glioma / genetics
  • Glioma / metabolism
  • Histones / metabolism*
  • Humans
  • Lysine / metabolism
  • Methylation / drug effects
  • Mice, Nude
  • Temozolomide / pharmacology*
  • X-linked Nuclear Protein / genetics
  • X-linked Nuclear Protein / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents, Alkylating
  • Histones
  • Ataxia Telangiectasia Mutated Proteins
  • ATRX protein, human
  • X-linked Nuclear Protein
  • Lysine
  • Temozolomide