ATM couples replication stress and metabolic reprogramming during cellular senescence

Cell Rep. 2015 May 12;11(6):893-901. doi: 10.1016/j.celrep.2015.04.014. Epub 2015 Apr 30.

Abstract

Replication stress induced by nucleotide deficiency plays an important role in cancer initiation. Replication stress in primary cells typically activates the cellular senescence tumor-suppression mechanism. Senescence bypass correlates with development of cancer, a disease characterized by metabolic reprogramming. However, the role of metabolic reprogramming in the cellular response to replication stress has been little explored. Here, we report that ataxia telangiectasia mutated (ATM) plays a central role in regulating the cellular response to replication stress by shifting cellular metabolism. ATM inactivation bypasses senescence induced by replication stress triggered by nucleotide deficiency. This was due to restoration of deoxyribonucleotide triphosphate (dNTP) levels through both upregulation of the pentose phosphate pathway via increased glucose-6-phosphate dehydrogenase (G6PD) activity and enhanced glucose and glutamine consumption. These phenotypes were mediated by a coordinated suppression of p53 and upregulation of c-MYC downstream of ATM inactivation. Our data indicate that ATM status couples replication stress and metabolic reprogramming during senescence.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Ataxia Telangiectasia Mutated Proteins / metabolism*
  • Cell Line
  • Cellular Reprogramming*
  • Cellular Senescence*
  • DNA Damage
  • DNA Replication*
  • Gene Knockdown Techniques
  • Glucose / metabolism
  • Glucosephosphate Dehydrogenase / metabolism
  • Glutamine / metabolism
  • Humans
  • Nucleotides / metabolism
  • Pentose Phosphate Pathway
  • Proto-Oncogene Proteins c-myc / metabolism
  • Stress, Physiological*
  • Substrate Specificity
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Nucleotides
  • Proto-Oncogene Proteins c-myc
  • Tumor Suppressor Protein p53
  • Glutamine
  • Glucosephosphate Dehydrogenase
  • Ataxia Telangiectasia Mutated Proteins
  • Glucose