The thioredoxin system protects ribosomes against stress-induced aggregation

Mol Biol Cell. 2006 Jan;17(1):387-401. doi: 10.1091/mbc.e05-06-0520. Epub 2005 Oct 26.

Abstract

We previously showed that thioredoxins are required for dithiothreitol (DTT) tolerance, suggesting they maintain redox homeostasis in response to both oxidative and reductive stress conditions. In this present study, we screened the complete set of viable deletion strains in Saccharomyces cerevisiae for sensitivity to DTT to identify cell functions involved in resistance to reductive stress. We identified 195 mutants, whose gene products are localized throughout the cell. DTT-sensitive mutants were distributed among most major biological processes, but they particularly affected gene expression, metabolism, and the secretory pathway. Strikingly, a mutant lacking TSA1, encoding a peroxiredoxin, showed a similar sensitivity to DTT as a thioredoxin mutant. Epistasis analysis indicated that thioredoxins function upstream of Tsa1 in providing tolerance to DTT. Our data show that the chaperone function of Tsa1, rather than its peroxidase function, is required for this activity. Cells lacking TSA1 were found to accumulate aggregated proteins, and this was exacerbated by exposure to DTT. Analysis of the protein aggregates revealed that they are predominantly composed of ribosomal proteins. Furthermore, aggregation was found to correlate with an inhibition of translation initiation. We propose that Tsa1 normally functions to chaperone misassembled ribosomal proteins, preventing the toxicity that arises from their aggregation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Dithiothreitol / pharmacology
  • Drug Resistance, Fungal
  • Gene Expression Regulation, Fungal / drug effects
  • Mutation / genetics
  • Oxidation-Reduction / drug effects
  • Peroxidases / genetics
  • Peroxidases / metabolism*
  • Protein Folding
  • Reactive Oxygen Species / metabolism
  • Ribosomal Proteins / metabolism
  • Ribosomes / metabolism*
  • Saccharomyces cerevisiae / cytology*
  • Saccharomyces cerevisiae / drug effects
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Thioredoxins / genetics
  • Thioredoxins / metabolism*
  • Transcription Factors / deficiency
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • DNA-Binding Proteins
  • Reactive Oxygen Species
  • Ribosomal Proteins
  • SKN7 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Transcription Factors
  • YAP1 protein, S cerevisiae
  • Thioredoxins
  • Peroxidases
  • Tsa1 protein, S cerevisiae
  • Dithiothreitol