Trans-translation-mediated tight regulation of the expression of the alternative ribosome-rescuefactor ArfA in Escherichia coli

Yuhei Chadani, Emi Matsumoto, Hiroaki Aso, Takeo Wada, Kazuhiro Kutsukake, Shizuyo Sutou, Tatsuhiko Abo

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

Ribosomes translating mRNA without an in-frame stop codon (non-stop mRNA) stall at its 3' end. In eubacteria, such ribosomes are rescued by SsrA-mediated trans-translation. Recently, we have shown that Escherichia coli ArfA (formerly YhdL) also rescues stalled ribosomes by a mechanism distinct from that of trans-translation. Synthetic lethality phenotype of ssrA arfA double mutants suggests that accumulation of stalled ribosomes is deleterious to E. coli cells. In this report, we show that the expression of ArfA is tightly regulated by the system involving trans-translation. Both premature transcription termination and specific cleavage by RNase III were programmed at the specific sites within the arfAopen reading frame (ORF) and produced arfA non-stop mRNA. C-terminally truncated ArfA protein synthesized from arfA non-stop mRNA was tagged through SsrA-mediated trans-translation and degraded in wild type cell. In the absence of SsrA, however, C-terminally truncated ArfA escaped from degradation and had a function to rescue stalled ribosomes. Full-length ArfA produced only when arfAmRNA escapes from both premature transcription termination and RNase III cleavage was unstable. From these results, we illustrate a regulatory model in which ArfA is expressed only when it is needed, namely, when the ribosome rescue activity of trans-translation system is insufficient to support cell viability. This sophisticated regulatory mechanism suggests that the ArfA-mediated ribosome rescue is a backup system for trans-translation.

Original languageEnglish
Pages (from-to)151-163
Number of pages13
JournalGenes and Genetic Systems
Volume86
Issue number3
DOIs
Publication statusPublished - 2011

Fingerprint

Ribosomes
Escherichia coli
Ribonuclease III
Messenger RNA
Reading Frames
Terminator Codon
Open Reading Frames
Cell Survival
Bacteria
Phenotype
Proteins

Keywords

  • ArfA
  • Escherichia coli
  • Ribosome
  • SsrA
  • Trans-translation

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology

Cite this

Trans-translation-mediated tight regulation of the expression of the alternative ribosome-rescuefactor ArfA in Escherichia coli. / Chadani, Yuhei; Matsumoto, Emi; Aso, Hiroaki; Wada, Takeo; Kutsukake, Kazuhiro; Sutou, Shizuyo; Abo, Tatsuhiko.

In: Genes and Genetic Systems, Vol. 86, No. 3, 2011, p. 151-163.

Research output: Contribution to journalArticle

Chadani, Yuhei ; Matsumoto, Emi ; Aso, Hiroaki ; Wada, Takeo ; Kutsukake, Kazuhiro ; Sutou, Shizuyo ; Abo, Tatsuhiko. / Trans-translation-mediated tight regulation of the expression of the alternative ribosome-rescuefactor ArfA in Escherichia coli. In: Genes and Genetic Systems. 2011 ; Vol. 86, No. 3. pp. 151-163.
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