Dual functions of yeast tRNA ligase in the unfolded protein response: Unconventional cytoplasmic splicing of HAC1 pre-mRNA is not sufficient to release translational attenuation

Takao Mori, Chiharu Ogasawara, Toshifumi Inada, Markus Englert, Hildburg Beier, Mine Takezawa, Toshiya Endo, Tohru Yoshihisa

Research output: Contribution to journalArticlepeer-review

29 Citations (Scopus)

Abstract

The unfolded protein response (UPR) is an essential signal transduction to cope with protein-folding stress in the endoplasmic reticulum. In the yeast UPR, the unconventional splicing of HAC1 mRNA is a key step. Translation of HAC1 pre-mRNA (HAC1u mRNA) is attenuated on polysomes and restarted only after splicing upon the UPR. However, the precise mechanism of this restart remained unclear. Here we show that yeast tRNA ligase (Rlg1p/Trl1p) acting on HAC1 ligation has an unexpected role in HAC1 translation. An RLG1 homologue from Arabidopsis thaliana (AtRLG1) substitutes for yeast RLG1 in tRNA splicing but not in the UPR. Surprisingly, AtRlg1p ligates HAC1 exons, but the spliced mRNA (HAC1i mRNA) is not translated efficiently. In the AtRLG1 cells, the HAC1 intron is circularized after splicing and remains associated on polysomes, impairing relief of the translational repressioC1i mRNA. Furthermore, the HAC1 5′ UTR itself enables yeast Rlg1p to regulate translation of the following ORF. RNA IP revealed that yeast Rlg1p is integrated in HAC1 mRNP, before Ire1p cleaves HAC1u mRNA. These results indicate that the splicing and the release of translational attenuation of HAC1 mRNA are separable steps and that Rlg1p has pivotal roles in both of these steps.

Original languageEnglish
Pages (from-to)3722-3734
Number of pages13
JournalMolecular biology of the cell
Volume21
Issue number21
DOIs
Publication statusPublished - 2010 Nov 1
Externally publishedYes

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

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