Multiprotein bridging factor 1 is required for robust activation of the integrated stress response on collided ribosomes

Mol Cell. 2024 Dec 5;84(23):4594-4611.e9. doi: 10.1016/j.molcel.2024.10.029. Epub 2024 Nov 19.

Abstract

In yeast, multiprotein bridging factor 1 (Mbf1) has been proposed to function in the integrated stress response (ISR) as a transcriptional coactivator by mediating a direct interaction between general transcription machinery and the process's key effector, Gcn4. However, mounting evidence has demonstrated that Mbf1 (and its human homolog EDF1) is recruited to collided ribosomes, a known activator of the ISR. In this study, we connect these otherwise seemingly disparate functions of Mbf1. Our biochemical and structural analyses reveal that Mbf1 functions as a core ISR factor by interacting with collided ribosomes to mediate Gcn2 activation. We further show that Mbf1 serves no role as a transcriptional coactivator of Gcn4. Instead, Mbf1 is required for optimal stress-induced eukaryotic initiation factor 2α (eIF2α) phosphorylation and downstream de-repression of GCN4 translation. Collectively, our data establish that Mbf1 functions in ISR signaling by acting as a direct sensor of stress-induced ribosome collisions.

Keywords: Gcn2; Gcn4; Mbf1; integrated stress response; ribosome; ribosome collisions; translation.

MeSH terms

  • Basic-Leucine Zipper Transcription Factors* / genetics
  • Basic-Leucine Zipper Transcription Factors* / metabolism
  • Eukaryotic Initiation Factor-2* / genetics
  • Eukaryotic Initiation Factor-2* / metabolism
  • Gene Expression Regulation, Fungal
  • Humans
  • Phosphorylation
  • Protein Binding
  • Protein Biosynthesis
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Ribosomes* / genetics
  • Ribosomes* / metabolism
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Saccharomyces cerevisiae* / genetics
  • Saccharomyces cerevisiae* / metabolism
  • Signal Transduction
  • Stress, Physiological*

Substances

  • Saccharomyces cerevisiae Proteins
  • Basic-Leucine Zipper Transcription Factors
  • GCN4 protein, S cerevisiae
  • Eukaryotic Initiation Factor-2
  • GCN2 protein, S cerevisiae
  • Protein Serine-Threonine Kinases