The Hog1 stress-activated protein kinase targets nucleoporins to control mRNA export upon stress

J Biol Chem. 2013 Jun 14;288(24):17384-98. doi: 10.1074/jbc.M112.444042. Epub 2013 May 3.

Abstract

The control of mRNA biogenesis is exerted at several steps. In response to extracellular stimuli, stress-activated protein kinases (SAPK) modulate gene expression to maximize cell survival. In yeast, the Hog1 SAPK plays a key role in reprogramming the gene expression pattern required for cell survival upon osmostress by acting during transcriptional initiation and elongation. Here, we genetically show that an intact nuclear pore complex is important for cell survival and maximal expression of stress-responsive genes. The Hog1 SAPK associates with nuclear pore complex components and directly phosphorylates the Nup1, Nup2, and Nup60 components of the inner nuclear basket. Mutation of those factors resulted in a deficient export of stress-responsive genes upon stress. Association of Nup1, Nup2, and Nup60 to stress-responsive promoters occurs upon stress depending on Hog1 activity. Accordingly, STL1 gene territory is maintained at the nuclear periphery upon osmostress in a Hog1-dependent manner. Cells containing non-phosphorylatable mutants in Nup1 or Nup2 display reduced expression of stress-responsive genes. Together, proper mRNA biogenesis of stress-responsive genes requires of the coordinate action of synthesis and export machineries by the Hog1 SAPK.

Keywords: Gene Expression; MAP Kinases (MAPKs); Signal Transduction; Stress Response; Yeast; mRNA Export; p38 MAPK.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Cell Nucleus / metabolism
  • Gene Expression Regulation, Fungal
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism
  • Microbial Viability
  • Mitogen-Activated Protein Kinases / physiology*
  • Molecular Sequence Data
  • Nuclear Pore / metabolism
  • Nuclear Pore Complex Proteins / genetics
  • Nuclear Pore Complex Proteins / metabolism*
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism
  • Phosphorylation
  • Protein Processing, Post-Translational
  • Protein Transport
  • RNA Transport*
  • RNA, Fungal / metabolism
  • Saccharomyces cerevisiae / enzymology*
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Saccharomyces cerevisiae Proteins / physiology*
  • Salt Tolerance
  • Stress, Physiological

Substances

  • Membrane Transport Proteins
  • NUP2 protein, S cerevisiae
  • Nuclear Pore Complex Proteins
  • Nup60 protein, S cerevisiae
  • RNA, Fungal
  • STL1 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Oxidoreductases
  • GRE2 protein, S cerevisiae
  • HOG1 protein, S cerevisiae
  • Mitogen-Activated Protein Kinases