Transposon integration enhances expression of stress response genes

Nucleic Acids Res. 2013 Jan;41(2):775-89. doi: 10.1093/nar/gks1185. Epub 2012 Nov 27.

Abstract

Transposable elements possess specific patterns of integration. The biological impact of these integration profiles is not well understood. Tf1, a long-terminal repeat retrotransposon in Schizosaccharomyces pombe, integrates into promoters with a preference for the promoters of stress response genes. To determine the biological significance of Tf1 integration, we took advantage of saturated maps of insertion activity and studied how integration at hot spots affected the expression of the adjacent genes. Our study revealed that Tf1 integration did not reduce gene expression. Importantly, the insertions activated the expression of 6 of 32 genes tested. We found that Tf1 increased gene expression by inserting enhancer activity. Interestingly, the enhancer activity of Tf1 could be limited by Abp1, a host surveillance factor that sequesters transposon sequences into structures containing histone deacetylases. We found the Tf1 promoter was activated by heat treatment and, remarkably, only genes that themselves were induced by heat could be activated by Tf1 integration, suggesting a synergy of Tf1 enhancer sequence with the stress response elements of target promoters. We propose that the integration preference of Tf1 for the promoters of stress response genes and the ability of Tf1 to enhance the expression of these genes co-evolved to promote the survival of cells under stress.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Enhancer Elements, Genetic
  • Gene Expression Regulation, Fungal*
  • Heat-Shock Response / genetics*
  • Oxidative Stress
  • Promoter Regions, Genetic
  • RNA Helicases / metabolism
  • RNA Polymerase II / metabolism
  • Retroelements*
  • Schizosaccharomyces / genetics
  • Schizosaccharomyces pombe Proteins / metabolism
  • Terminal Repeat Sequences
  • Transcription, Genetic

Substances

  • Retroelements
  • Schizosaccharomyces pombe Proteins
  • RNA Polymerase II
  • Upf1 protein, S pombe
  • RNA Helicases