Nucleic Acids Research Advance Access originally published online on October 14, 2008
Nucleic Acids Research 2008 36(20):6472-6481; doi:10.1093/nar/gkn667
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Nucleic Acids Research, 2008, Vol. 36, No. 20 6472-6481
© 2008 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Translation affects YoeB and MazF messenger RNA interferase activities by different mechanisms
1Institute for Cell and Molecular Biosciences, Medical School, Newcastle University, Newcastle, NE2 4HH, UK and 2Department of Biochemistry & Molecular Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark
*To whom correspondence should be addressed. Tel: +44 191 222 5318; Fax: +44 191 222 7424; Email: kenn.gerdes{at}ncl.ac.uk
Received May 27, 2008. Revised July 16, 2008. Accepted September 22, 2008.
Prokaryotic toxin–antitoxin loci encode mRNA cleaving enzymes that inhibit translation. Two types are known: those that cleave mRNA codons at the ribosomal A site and those that cleave any RNA site specifically. RelE of Escherichia coli cleaves mRNA at the ribosomal A site in vivo and in vitro but does not cleave pure RNA in vitro. RelE exhibits an incomplete RNase fold that may explain why RelE requires its substrate mRNA to presented by the ribosome. In contrast, RelE homologue YoeB has a complete RNase fold and cleaves RNA independently of ribosomes in vitro. Here, we show that YoeB cleavage of mRNA is strictly dependent on translation of the mRNA in vivo. Non-translated model mRNAs were not cleaved whereas the corresponding wild-type mRNAs were cleaved efficiently. Model mRNAs carrying frameshift mutations exhibited a YoeB-mediated cleavage pattern consistent with the reading frameshift thus giving strong evidence that YoeB cleavage specificity was determined by the translational reading frame. In contrast, site-specific mRNA cleavage by MazF occurred independently of translation. In one case, translation seriously influenced MazF cleavage efficiency, thus solving a previous apparent paradox. We propose that translation enhances MazF-mediated cleavage of mRNA by destabilization of the mRNA secondary structure.
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