Genome instability footprint under rapamycin and hydroxyurea treatments

PLoS Genet. 2023 Nov 6;19(11):e1011012. doi: 10.1371/journal.pgen.1011012. eCollection 2023 Nov.

Abstract

The mutational processes dictating the accumulation of mutations in genomes are shaped by genetic background, environment and their interactions. Accurate quantification of mutation rates and spectra under drugs has important implications in disease treatment. Here, we used whole-genome sequencing and time-resolved growth phenotyping of yeast mutation accumulation lines to give a detailed view of the mutagenic effects of rapamycin and hydroxyurea on the genome and cell growth. Mutation rates depended on the genetic backgrounds but were only marginally affected by rapamycin. As a remarkable exception, rapamycin treatment was associated with frequent chromosome XII amplifications, which compensated for rapamycin induced rDNA repeat contraction on this chromosome and served to maintain rDNA content homeostasis and fitness. In hydroxyurea, a wide range of mutation rates were elevated regardless of the genetic backgrounds, with a particularly high occurrence of aneuploidy that associated with dramatic fitness loss. Hydroxyurea also induced a high T-to-G and low C-to-A transversion rate that reversed the common G/C-to-A/T bias in yeast and gave rise to a broad range of structural variants, including mtDNA deletions. The hydroxyurea mutation footprint was consistent with the activation of error-prone DNA polymerase activities and non-homologues end joining repair pathways. Taken together, our study provides an in-depth view of mutation rates and signatures in rapamycin and hydroxyurea and their impact on cell fitness, which brings insights for assessing their chronic effects on genome integrity.

MeSH terms

  • DNA, Ribosomal / genetics
  • Genomic Instability / genetics
  • Humans
  • Hydroxyurea* / pharmacology
  • Mutation
  • Saccharomyces cerevisiae* / genetics
  • Sirolimus / pharmacology

Substances

  • Hydroxyurea
  • Sirolimus
  • DNA, Ribosomal

Grants and funding

This work is supported by the National Natural Science Foundation of China (32000395 to JL and 32070592 to J-X Y), the Natural Science Foundation of Guangdong Province (2022A1515011873 to JL and 2022A1515010717 to J-X Y), the Guangdong Basic and Applied Basic Research Foundation (2019A1515110762 to J-X Y), the Guangdong Pearl River Talents Program (2021QN02Y168 to JL, 2019QN01Y183 to J-XY), Agence Nationale de la Recherche (ANR-15-IDEX-01), Fondation pour la Recherche Médicale (EQU202003010413), Association pour la Recherche sur le Cancer (ARCPJA32020070002320 to GL), and the Swedish Research Council (2018-03638 to JW). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.