Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and sigmaE-dependent CyaR-ompX regulatory case

Jesper Johansen, Maiken Eriksen, Birgitte Kallipolitis, Poul Valentin-Hansen

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

The sigma(E) (extracytoplasmic stress response sigma factor in Escherichia coli) signaling system of Gram-negative bacteria plays an essential role in the maintenance of the extracytoplasmic compartment. Upon induction of this system, approximately 100 genes are up-regulated. The majority of these genes encode proteins that participate in the synthesis, assembly, and homeostasis of outer membrane proteins and lipopolysaccharides. A second aspect of the sigma(E) response is a regulatory loop that prevents expression of the major porins. Misfolding or overproduction of most of these porins is sufficient to trigger the envelope stress response. Recent work indicates that small Hfq-binding RNAs play a major role in maintaining envelope homeostasis and, so far, two sigma(E)-dependent small noncoding RNAs (sRNAs), MicA and RybB, have been shown to facilitate rapid removal of multiple omp transcripts in response to elevated activity of the alternative sigma factor. Here we report the identification of the sRNA (CyaR, cyclic AMP-activated RNA) that promotes decay of the ompX mRNA. The transcription of the cyaR gene is stringently controlled by cAMP-cAMP receptor protein and, unexpectedly, cyaR expression is also up-regulated, directly or indirectly, by sigma(E). In addition, this work identified MicA as a factor that cooperates in the negative control of ompX expression. The conservation of CyaR, MicA, RybB, and their targets suggests that the omp mRNA-sRNA regulatory network is an integral part of the envelope stress response in many enterobacteria.
Original languageEnglish
JournalJournal of Molecular Biology
Volume383
Issue number1
Pages (from-to)1-9
Number of pages8
ISSN0022-2836
DOIs
Publication statusPublished - 31. Oct 2008

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Untranslated RNA
Sigma Factor
Membrane Proteins
Down-Regulation
RNA
Homeostasis
Messenger RNA
Maintenance
mica
Proteins

Cite this

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title = "Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and sigmaE-dependent CyaR-ompX regulatory case",
abstract = "The sigma(E) (extracytoplasmic stress response sigma factor in Escherichia coli) signaling system of Gram-negative bacteria plays an essential role in the maintenance of the extracytoplasmic compartment. Upon induction of this system, approximately 100 genes are up-regulated. The majority of these genes encode proteins that participate in the synthesis, assembly, and homeostasis of outer membrane proteins and lipopolysaccharides. A second aspect of the sigma(E) response is a regulatory loop that prevents expression of the major porins. Misfolding or overproduction of most of these porins is sufficient to trigger the envelope stress response. Recent work indicates that small Hfq-binding RNAs play a major role in maintaining envelope homeostasis and, so far, two sigma(E)-dependent small noncoding RNAs (sRNAs), MicA and RybB, have been shown to facilitate rapid removal of multiple omp transcripts in response to elevated activity of the alternative sigma factor. Here we report the identification of the sRNA (CyaR, cyclic AMP-activated RNA) that promotes decay of the ompX mRNA. The transcription of the cyaR gene is stringently controlled by cAMP-cAMP receptor protein and, unexpectedly, cyaR expression is also up-regulated, directly or indirectly, by sigma(E). In addition, this work identified MicA as a factor that cooperates in the negative control of ompX expression. The conservation of CyaR, MicA, RybB, and their targets suggests that the omp mRNA-sRNA regulatory network is an integral part of the envelope stress response in many enterobacteria.",
author = "Jesper Johansen and Maiken Eriksen and Birgitte Kallipolitis and Poul Valentin-Hansen",
year = "2008",
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language = "English",
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Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and sigmaE-dependent CyaR-ompX regulatory case. / Johansen, Jesper; Eriksen, Maiken; Kallipolitis, Birgitte; Valentin-Hansen, Poul.

In: Journal of Molecular Biology, Vol. 383, No. 1, 31.10.2008, p. 1-9.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and sigmaE-dependent CyaR-ompX regulatory case

AU - Johansen, Jesper

AU - Eriksen, Maiken

AU - Kallipolitis, Birgitte

AU - Valentin-Hansen, Poul

PY - 2008/10/31

Y1 - 2008/10/31

N2 - The sigma(E) (extracytoplasmic stress response sigma factor in Escherichia coli) signaling system of Gram-negative bacteria plays an essential role in the maintenance of the extracytoplasmic compartment. Upon induction of this system, approximately 100 genes are up-regulated. The majority of these genes encode proteins that participate in the synthesis, assembly, and homeostasis of outer membrane proteins and lipopolysaccharides. A second aspect of the sigma(E) response is a regulatory loop that prevents expression of the major porins. Misfolding or overproduction of most of these porins is sufficient to trigger the envelope stress response. Recent work indicates that small Hfq-binding RNAs play a major role in maintaining envelope homeostasis and, so far, two sigma(E)-dependent small noncoding RNAs (sRNAs), MicA and RybB, have been shown to facilitate rapid removal of multiple omp transcripts in response to elevated activity of the alternative sigma factor. Here we report the identification of the sRNA (CyaR, cyclic AMP-activated RNA) that promotes decay of the ompX mRNA. The transcription of the cyaR gene is stringently controlled by cAMP-cAMP receptor protein and, unexpectedly, cyaR expression is also up-regulated, directly or indirectly, by sigma(E). In addition, this work identified MicA as a factor that cooperates in the negative control of ompX expression. The conservation of CyaR, MicA, RybB, and their targets suggests that the omp mRNA-sRNA regulatory network is an integral part of the envelope stress response in many enterobacteria.

AB - The sigma(E) (extracytoplasmic stress response sigma factor in Escherichia coli) signaling system of Gram-negative bacteria plays an essential role in the maintenance of the extracytoplasmic compartment. Upon induction of this system, approximately 100 genes are up-regulated. The majority of these genes encode proteins that participate in the synthesis, assembly, and homeostasis of outer membrane proteins and lipopolysaccharides. A second aspect of the sigma(E) response is a regulatory loop that prevents expression of the major porins. Misfolding or overproduction of most of these porins is sufficient to trigger the envelope stress response. Recent work indicates that small Hfq-binding RNAs play a major role in maintaining envelope homeostasis and, so far, two sigma(E)-dependent small noncoding RNAs (sRNAs), MicA and RybB, have been shown to facilitate rapid removal of multiple omp transcripts in response to elevated activity of the alternative sigma factor. Here we report the identification of the sRNA (CyaR, cyclic AMP-activated RNA) that promotes decay of the ompX mRNA. The transcription of the cyaR gene is stringently controlled by cAMP-cAMP receptor protein and, unexpectedly, cyaR expression is also up-regulated, directly or indirectly, by sigma(E). In addition, this work identified MicA as a factor that cooperates in the negative control of ompX expression. The conservation of CyaR, MicA, RybB, and their targets suggests that the omp mRNA-sRNA regulatory network is an integral part of the envelope stress response in many enterobacteria.

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DO - 10.1016/j.jmb.2008.06.058

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SN - 0022-2836

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