Genome-wide screen of cell-cycle regulators in normal and tumor cells identifies a differential response to nucleosome depletion

Cell Cycle. 2017 Jan 17;16(2):189-199. doi: 10.1080/15384101.2016.1261765. Epub 2016 Dec 8.

Abstract

To identify cell cycle regulators that enable cancer cells to replicate DNA and divide in an unrestricted manner, we performed a parallel genome-wide RNAi screen in normal and cancer cell lines. In addition to many shared regulators, we found that tumor and normal cells are differentially sensitive to loss of the histone genes transcriptional regulator CASP8AP2. In cancer cells, loss of CASP8AP2 leads to a failure to synthesize sufficient amount of histones in the S-phase of the cell cycle, resulting in slowing of individual replication forks. Despite this, DNA replication fails to arrest, and tumor cells progress in an elongated S-phase that lasts several days, finally resulting in death of most of the affected cells. In contrast, depletion of CASP8AP2 in normal cells triggers a response that arrests viable cells in S-phase. The arrest is dependent on p53, and preceded by accumulation of markers of DNA damage, indicating that nucleosome depletion is sensed in normal cells via a DNA-damage -like response that is defective in tumor cells.

Keywords: DNA replication; RNA interference; cancer; cell cycle; chromatin; functional genomics; nucleosome assembly; p53.

MeSH terms

  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Cycle*
  • Cell Line, Tumor
  • DNA / biosynthesis
  • DNA Replication
  • Gene Expression Regulation, Neoplastic
  • Gene Knockdown Techniques
  • Genome*
  • Histones / genetics
  • Histones / metabolism
  • Humans
  • Neoplasm Proteins / metabolism
  • Neoplasms / metabolism*
  • Neoplasms / pathology*
  • Nucleosomes / metabolism*
  • Osteosarcoma / genetics
  • Osteosarcoma / pathology
  • Phosphorylation
  • RNA Interference*
  • RNA, Small Interfering / metabolism
  • S Phase
  • Transcription, Genetic
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Cell Cycle Proteins
  • H2AX protein, human
  • Histones
  • Neoplasm Proteins
  • Nucleosomes
  • RNA, Small Interfering
  • Tumor Suppressor Protein p53
  • DNA