Literature DB >> 21944167

Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli.

Oliver Vesper1, Shahar Amitai, Maria Belitsky, Konstantin Byrgazov, Anna Chao Kaberdina, Hanna Engelberg-Kulka, Isabella Moll.   

Abstract

Escherichia coli (E. coli) mazEF is a stress-induced toxin-antitoxin (TA) module. The toxin MazF is an endoribonuclease that cleaves single-stranded mRNAs at ACA sequences. Here, we show that MazF cleaves at ACA sites at or closely upstream of the AUG start codon of some specific mRNAs and thereby generates leaderless mRNAs. Moreover, we provide evidence that MazF also targets 16S rRNA within 30S ribosomal subunits at the decoding center, thereby removing 43 nucleotides from the 3' terminus. As this region comprises the anti-Shine-Dalgarno (aSD) sequence that is required for translation initiation on canonical mRNAs, a subpopulation of ribosomes is formed that selectively translates the described leaderless mRNAs both in vivo and in vitro. Thus, we have discovered a modified translation machinery that is generated in response to MazF induction and that probably serves for stress adaptation in Escherichia coli.
Copyright © 2011 Elsevier Inc. All rights reserved.

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Year:  2011        PMID: 21944167      PMCID: PMC4894548          DOI: 10.1016/j.cell.2011.07.047

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  55 in total

1.  A snapshot of the 30S ribosomal subunit capturing mRNA via the Shine-Dalgarno interaction.

Authors:  Tatsuya Kaminishi; Daniel N Wilson; Chie Takemoto; Joerg M Harms; Masahito Kawazoe; Frank Schluenzen; Kyoko Hanawa-Suetsugu; Mikako Shirouzu; Paola Fucini; Shigeyuki Yokoyama
Journal:  Structure       Date:  2007-03       Impact factor: 5.006

2.  A linear pentapeptide is a quorum-sensing factor required for mazEF-mediated cell death in Escherichia coli.

Authors:  Ilana Kolodkin-Gal; Ronen Hazan; Ariel Gaathon; Shmuel Carmeli; Hanna Engelberg-Kulka
Journal:  Science       Date:  2007-10-26       Impact factor: 47.728

Review 3.  Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest.

Authors:  Finbarr Hayes
Journal:  Science       Date:  2003-09-12       Impact factor: 47.728

4.  Depletion of free 30S ribosomal subunits in Escherichia coli by expression of RNA containing Shine-Dalgarno-like sequences.

Authors:  Mary V Mawn; Maurille J Fournier; David A Tirrell; Thomas L Mason
Journal:  J Bacteriol       Date:  2002-01       Impact factor: 3.490

5.  Significant bias against the ACA triplet in the tmRNA sequence of Escherichia coli K-12.

Authors:  Sarah Baik; Koichi Inoue; Ming Ouyang; Masayori Inouye
Journal:  J Bacteriol       Date:  2009-07-24       Impact factor: 3.490

6.  The complete genome sequence of Escherichia coli K-12.

Authors:  F R Blattner; G Plunkett; C A Bloch; N T Perna; V Burland; M Riley; J Collado-Vides; J D Glasner; C K Rode; G F Mayhew; J Gregor; N W Davis; H A Kirkpatrick; M A Goeden; D J Rose; B Mau; Y Shao
Journal:  Science       Date:  1997-09-05       Impact factor: 47.728

7.  Promotion, termination, and anti-termination in the rpsU-dnaG-rpoD macromolecular synthesis operon of E. coli K-12.

Authors:  J R Lupski; A A Ruiz; G N Godson
Journal:  Mol Gen Genet       Date:  1984

8.  Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA.

Authors:  Susanne K Christensen; Kim Pedersen; Flemming G Hansen; Kenn Gerdes
Journal:  J Mol Biol       Date:  2003-09-26       Impact factor: 5.469

9.  Effects of ribosomal proteins S1, S2 and the DeaD/CsdA DEAD-box helicase on translation of leaderless and canonical mRNAs in Escherichia coli.

Authors:  Isabella Moll; Sonja Grill; Angelika Gründling; Udo Bläsi
Journal:  Mol Microbiol       Date:  2002-06       Impact factor: 3.501

10.  Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes.

Authors:  Deo Prakash Pandey; Kenn Gerdes
Journal:  Nucleic Acids Res       Date:  2005-02-17       Impact factor: 16.971

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  155 in total

1.  Bacterial physiology. Stressed bacteria aren't lost without a leader.

Authors:  Andrew Jermy
Journal:  Nat Rev Microbiol       Date:  2011-11-08       Impact factor: 60.633

Review 2.  One core, two shells: bacterial and eukaryotic ribosomes.

Authors:  Sergey Melnikov; Adam Ben-Shem; Nicolas Garreau de Loubresse; Lasse Jenner; Gulnara Yusupova; Marat Yusupov
Journal:  Nat Struct Mol Biol       Date:  2012-06-05       Impact factor: 15.369

3.  Defining the mRNA recognition signature of a bacterial toxin protein.

Authors:  Marc A Schureck; Jack A Dunkle; Tatsuya Maehigashi; Stacey J Miles; Christine M Dunham
Journal:  Proc Natl Acad Sci U S A       Date:  2015-10-27       Impact factor: 11.205

Review 4.  Cis-regulatory RNA elements that regulate specialized ribosome activity.

Authors:  Shifeng Xue; Maria Barna
Journal:  RNA Biol       Date:  2015-09-01       Impact factor: 4.652

Review 5.  Specialized ribosomes: a new frontier in gene regulation and organismal biology.

Authors:  Shifeng Xue; Maria Barna
Journal:  Nat Rev Mol Cell Biol       Date:  2012-05-23       Impact factor: 94.444

6.  Mapping the RNA-Seq trash bin: unusual transcripts in prokaryotic transcriptome sequencing data.

Authors:  Gero Doose; Maria Alexis; Rebecca Kirsch; Sven Findeiß; David Langenberger; Rainer Machné; Mario Mörl; Steve Hoffmann; Peter F Stadler
Journal:  RNA Biol       Date:  2013-05-13       Impact factor: 4.652

7.  Molecular mechanisms of multiple toxin-antitoxin systems are coordinated to govern the persister phenotype.

Authors:  Rick A Fasani; Michael A Savageau
Journal:  Proc Natl Acad Sci U S A       Date:  2013-06-18       Impact factor: 11.205

8.  Toxins that Trash Translation.

Authors:  Allen R Buskirk
Journal:  Mol Cell       Date:  2018-06-07       Impact factor: 17.970

9.  23S rRNA as an a-Maz-ing new bacterial toxin target.

Authors:  Jason M Schifano; Nancy A Woychik
Journal:  RNA Biol       Date:  2014-02-07       Impact factor: 4.652

10.  Activation of Toxin-Antitoxin System Toxins Suppresses Lethality Caused by the Loss of σE in Escherichia coli.

Authors:  Yasushi Daimon; Shin-ichiro Narita; Yoshinori Akiyama
Journal:  J Bacteriol       Date:  2015-04-27       Impact factor: 3.490

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