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Decline in ribosomal fidelity contributes to the accumulation and stabilization of the master stress response regulator sigma S upon carbon starvation

Journal article
Authors Åsa Fredriksson
Manuel Ballesteros
Celeste N. Peterson
Örjan Persson
Thomas J. Silhavy
Thomas Nyström
Published in Genes & Development
Volume 21
Issue 7
Pages 862-874
Publication year 2007
Published at Department of Cell and Molecular Biology
Pages 862-874
Language en
Links dx.doi.org/10.1101/gad.409407
Keywords Escherichia coli, stationary phase, RpoS, SprE, rpsL, ClpP, protein oxidation
Subject categories Biological Sciences

Abstract

The {sigma}S subunit of RNA polymerase is a master regulator of Escherichia coli that retards cellular senescence and bestows cells with general stress protective functions during growth arrest. We show that mutations and drugs triggering translational errors elevate {sigma}S levels and stability. Furthermore, mutations enhancing translational fidelity attenuate induction of the rpoS regulon and prevent stabilization of {sigma}S upon carbon starvation. Destabilization of {sigma}S by increased proofreading requires the presence of the {sigma}S recognition factor SprE (RssB) and the ClpXP protease. The data further suggest that {sigma}S becomes stabilized upon starvation as a result of ClpP sequestration and this sequestration is enhanced by oxidative modifications of aberrant proteins produced by erroneous translation. ClpP overproduction counteracted starvation-induced stabilization of {sigma}S, whereas overproduction of a ClpXP substrate (ssrA-tagged GFP) stabilized {sigma}S in exponentially growing cells. We present a model for the sequence of events leading to the accumulation and activation of {sigma}S upon carbon starvation, which are linked to alterations in both ribosomal fidelity and efficiency.

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