ATR-CHK1-E2F3 signaling transactivates human ribonucleotide reductase small subunit M2 for DNA repair induced by the chemical carcinogen MNNG

Biochim Biophys Acta. 2016 Apr;1859(4):612-26. doi: 10.1016/j.bbagrm.2016.02.012. Epub 2016 Feb 24.

Abstract

Background: N-methyl-N'-nitro-N-nitrosoguanidine (MNNG), an alkylating agent and an environmental carcinogen, causes DNA lesions and even carcinomas. DNA damage responses induced by MNNG activate various DNA repair genes and related signaling pathways. The present study aimed to investigate the regulatory mechanisms of human RR small subunit M2 (hRRM2) in response to MNNG.

Results: In this study, we demonstrated that the RRM2 gene was transactivated by MNNG exposure more strongly than the other small subunit, p53R2. The upregulated RRM2 translocated to the nucleus for DNA repair. Further study showed that E2F3 transactivated RRM2 expression by directly binding to its promoter after MNNG exposure. The transactivation was enhanced by the upregulation of NFY, which bound to the RRM2 promoter adjacent to the E2F3 binding site and interacted with E2F3. In response to MNNG treatment, E2F3 accumulated mainly through its phosphorylation at S124 and was dependent on ATR-CHK1 signaling. In comparison, p53R2 played a relatively weaker role in the MNNG-induced DNA damage response, and its transcription was regulated by the ATR-CHK2-E2F1/p53 pathway.

Conclusions: We suggest that MNNG-stimulated ATR/CHK1 signaling stabilizes E2F3 by S124 phosphorylation, and then E2F3 together with NFY co-transactivate RRM2 expression for DNA repair.

General significance: We propose a new mechanism for RRM2 regulation to maintain genome stability in response to environmental chemical carcinogens.

Keywords: DNA repair; E2F3; Human ribonucleotide reductase small subunit M2 (RRM2); MNNG; Transcriptional regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ataxia Telangiectasia Mutated Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / metabolism
  • CCAAT-Binding Factor / biosynthesis
  • Carcinogens / toxicity
  • Checkpoint Kinase 1
  • DNA Damage / drug effects*
  • DNA Repair / drug effects
  • DNA-Binding Proteins / genetics
  • E2F3 Transcription Factor / genetics
  • E2F3 Transcription Factor / metabolism*
  • Gene Expression Regulation, Neoplastic / drug effects
  • Genome, Human / drug effects
  • Genomic Instability
  • Humans
  • Methylnitronitrosoguanidine / toxicity
  • Phosphorylation
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Ribonucleoside Diphosphate Reductase / biosynthesis*
  • Ribonucleoside Diphosphate Reductase / genetics
  • Signal Transduction / drug effects
  • Tumor Suppressor Protein p53 / genetics

Substances

  • CCAAT-Binding Factor
  • Carcinogens
  • DNA-Binding Proteins
  • E2F3 Transcription Factor
  • E2F3 protein, human
  • Tumor Suppressor Protein p53
  • nuclear factor Y
  • Methylnitronitrosoguanidine
  • ribonucleotide reductase M2
  • Ribonucleoside Diphosphate Reductase
  • Protein Kinases
  • ATR protein, human
  • Ataxia Telangiectasia Mutated Proteins
  • CHEK1 protein, human
  • Checkpoint Kinase 1