Histone variant H2A.Z is needed for efficient transcription-coupled NER and genome integrity in UV challenged yeast cells

PLoS Genet. 2024 Sep 10;20(9):e1011300. doi: 10.1371/journal.pgen.1011300. eCollection 2024 Sep.

Abstract

The genome of living cells is constantly challenged by DNA lesions that interfere with cellular processes such as transcription and replication. A manifold of mechanisms act in concert to ensure adequate DNA repair, gene expression, and genome stability. Bulky DNA lesions, such as those induced by UV light or the DNA-damaging agent 4-nitroquinoline oxide, act as transcriptional and replicational roadblocks and thus represent a major threat to cell metabolism. When located on the transcribed strand of active genes, these lesions are handled by transcription-coupled nucleotide excision repair (TC-NER), a yet incompletely understood NER sub-pathway. Here, using a genetic screen in the yeast Saccharomyces cerevisiae, we identified histone variant H2A.Z as an important component to safeguard transcription and DNA integrity following UV irradiation. In the absence of H2A.Z, repair by TC-NER is severely impaired and RNA polymerase II clearance reduced, leading to an increase in double-strand breaks. Thus, H2A.Z is needed for proficient TC-NER and plays a major role in the maintenance of genome stability upon UV irradiation.

MeSH terms

  • 4-Nitroquinoline-1-oxide / pharmacology
  • DNA Breaks, Double-Stranded / radiation effects
  • DNA Damage* / genetics
  • DNA Repair* / genetics
  • Gene Expression Regulation, Fungal / radiation effects
  • Genome, Fungal
  • Genomic Instability* / radiation effects
  • Histones* / genetics
  • Histones* / metabolism
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Saccharomyces cerevisiae* / genetics
  • Saccharomyces cerevisiae* / radiation effects
  • Transcription, Genetic*
  • Ultraviolet Rays*

Substances

  • Histones
  • Saccharomyces cerevisiae Proteins
  • Htz1 protein, S cerevisiae
  • RNA Polymerase II
  • 4-Nitroquinoline-1-oxide

Grants and funding

Research was funded by the Spanish Ministry of Science, Innovation and Universities (PID2022-140466NB-I00 to HG and RW), the Junta de Andalucía (P20_01220 to RW), the University of Seville (PP2018-10767 and PP2019-13299 to HG), the Spanish Ministry of Science and Innovation (BFU2016-75058-P to AA), the Spanish Ministry of Economy and Competitiveness (BFU2013-42918-P to AA), and the European Regional Development Fund (FEDER). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.