The HOG pathway dictates the short-term translational response after hyperosmotic shock

Mol Biol Cell. 2010 Sep 1;21(17):3080-92. doi: 10.1091/mbc.E10-01-0006. Epub 2010 Jun 29.

Abstract

Cellular responses to environmental changes occur on different levels. We investigated the translational response of yeast cells after mild hyperosmotic shock by isolating mRNA associated with multiple ribosomes (polysomes) followed by array analysis. Globally, recruitment of preexisting mRNAs to ribosomes (translational response) is faster than the transcriptional response. Specific functional groups of mRNAs are recruited to ribosomes without any corresponding increase in total mRNA. Among mRNAs under strong translational up-regulation upon shock, transcripts encoding membrane-bound proteins including hexose transporters were enriched. Similarly, numerous mRNAs encoding cytoplasmic ribosomal proteins run counter to the overall trend of down-regulation and are instead translationally mobilized late in the response. Surprisingly, certain transcriptionally induced mRNAs were excluded from ribosomal association after shock. Importantly, we verify, using constructs with intact 5' and 3' untranslated regions, that the observed changes in polysomal mRNA are reflected in protein levels, including cases with only translational up-regulation. Interestingly, the translational regulation of the most highly osmostress-regulated mRNAs was more strongly dependent on the stress-activated protein kinases Hog1 and Rck2 than the transcriptional regulation. Our results show the importance of translational control for fine tuning of the adaptive responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / drug effects
  • Adaptation, Physiological / genetics
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Down-Regulation / drug effects
  • Gene Expression Regulation, Fungal / drug effects
  • Membrane Proteins / metabolism
  • Mitogen-Activated Protein Kinases / genetics
  • Mitogen-Activated Protein Kinases / metabolism*
  • Osmotic Pressure / drug effects
  • Polyribosomes / drug effects
  • Polyribosomes / metabolism
  • Protein Binding / drug effects
  • Protein Biosynthesis* / drug effects
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Saccharomyces cerevisiae / cytology
  • Saccharomyces cerevisiae / drug effects
  • Saccharomyces cerevisiae / enzymology*
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Signal Transduction* / drug effects
  • Sodium Chloride / pharmacology
  • Stress, Physiological / drug effects
  • Stress, Physiological / genetics
  • Time Factors
  • Transcription, Genetic / drug effects
  • Up-Regulation / drug effects

Substances

  • Membrane Proteins
  • RNA, Messenger
  • Saccharomyces cerevisiae Proteins
  • Sodium Chloride
  • HOG1 protein, S cerevisiae
  • Mitogen-Activated Protein Kinases