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Modulating the Outer Membrane with Small Rnas Downloaded from genesdev.cshlp.org on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press REVIEW Modulating the outer membrane with small RNAs Maude Guillier,1 Susan Gottesman,1,3 and Gisela Storz2,4 1Laboratory of Molecular Biology, National Cancer Institute, Bethesda 20892, Maryland, USA; 2Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, Bethesda 20892, Maryland, USA MicF, one of the first chromosomally encoded regulatory expression they titrate CsrA away from its mRNA target small RNAs (sRNAs) to be discovered, was found to sites. Another mechanism for sRNA action is direct modulate the expression of OmpF, an abundant outer base-pairing with an mRNA target, either with extensive membrane protein. Several recent papers have now complementarity to an mRNA encoded in cis or with shown that this is not an isolated case. At least five other partial complementarity to an mRNA encoded in trans. sRNAs also regulate the synthesis of outer membrane Base-pairing of the sRNA and its target has been found to porins, and additional sRNAs modulate the expression of positively or negatively affect stability and/or the ability other outer membrane proteins. Here we review what is of the mRNA to be translated. For instance, both the known about these sRNAs and discuss the implications DsrA and RprA sRNAs activate rpoS translation because of this regulation. their base-pairing with the rpoS mRNA leader prevents the formation of an inhibitory structure that sequesters the ribosome-binding site (Majdalani et al. 1998, 2002). In contrast, RyhB RNA pairing with the sodB mRNA Escherichia coli small RNAs (sRNAs) blocks translation and leads to degradation of both RNAs Small untranslated regulatory RNAs, usually referred to (Massé et al. 2003). This degradation, which requires the as noncoding RNAs (ncRNAs) in eukaryotes and sRNAs RNase E endonuclease, may be secondary to the trans- in bacteria, have been described in all kingdoms of life. lation block, since reduced SodB protein levels upon Regulatory sRNAs in bacteria were first detected from RyhB expression are still observed in the absence of deg- extrachromosomal genetic elements such as plasmids, radation (Morita et al. 2006). transposons, and bacteriophages (for review, see Wagner All E. coli sRNAs that were shown to act by pairing et al. 2002). Subsequently, several studies showed that with trans-encoded targets bind the RNA chaperone pro- chromosomally encoded sRNAs, most initially found tein Hfq and, where it was examined, were found to re- fortuitously, were induced by and contributed to re- quire this protein for their activity. In addition, all Hfq- sponses to stress conditions such as low temperature and binding sRNAs studied thus far have been found to act oxidative stress (for review, see Gottesman 2004). The by pairing (for review, see Storz and Gottesman 2006). recognition that sRNAs had important regulatory func- Hfq was first described as a host-factor required for rep- ␤ tions led several groups to carry out genome-wide lication of bacteriophage Q , but the pleiotropic effects searches for these regulatory molecules. To date, a vari- displayed by an hfq-null mutant suggested important ety of approaches (for review, see Vogel and Sharma cellular roles for this highly abundant protein (Tsui et al. 2005) have led to the identification of ∼80 sRNAs in E. 1994). The hexameric Hfq ring has been shown to bind coli. The precise role of most of the sRNAs is still un- AU-rich sequences in the sRNAs as well as some target known, though it appears that many are only expressed mRNAs, and to stabilize some of the RNAs, probably by under specific conditions. masking RNase E cleavage sites. In addition, Hfq has Thus far, two main modes of action have been de- been found to facilitate the interaction between sRNAs scribed for regulatory sRNAs in E. coli. Some modify the and mRNAs, though the mechanism by which this oc- activity of a protein, as has been shown for the CsrB and curs remains to be fully elucidated (for review, see Val- CsrC RNAs (Liu et al. 1997; Weilbacher et al. 2003). entin-Hansen et al. 2004). Since at least one third of the These two sRNAs each possess multiple binding sites for known E. coli sRNAs can bind Hfq, base-pairing with the global translational regulatory protein CsrA; upon target mRNAs appears to be a major mechanism for sRNA action. sRNAs that act by pairing with trans-encoded mRNAs [Keywords: Hfq; OmpC; OmpA; ␴E; OmpR] may require the Hfq chaperone because they only have Corresponding authors. partial complementarity with their targets. An advan- 3E-MAIL [email protected]; FAX (301) 496-3875. 4E-MAIL [email protected]; FAX (301) 402-0078. tage of partial complementarity is that trans-encoded Article is online at http://www.genesdev.org/cgi/doi/10.1101/gad.1457506. sRNAs can regulate the expression of several unlinked 2338 GENES & DEVELOPMENT 20:2338–2348 © 2006 by Cold Spring Harbor Laboratory Press ISSN 0890-9369/06; www.genesdev.org Downloaded from genesdev.cshlp.org on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press Modulating the outer membrane with sRNAs genes, as was shown to be the case for RyhB, which nega- molecules while also preventing the entry of deleterious tively regulates the expression of multiple operons en- molecules (for review, see Nikaido 2003). Among the coding iron-binding proteins (Massé and Gottesman most abundant outer membrane proteins are the OmpC 2002; Massé et al. 2005). Conversely, the expression of a and OmpF porins, both trimeric ␤-barrel proteins that given gene can be modulated by distinct trans-encoded span the membrane. OmpA, another abundant ␤-barrel sRNAs. For example, rpoS expression is regulated by at protein, acts as a porin (Sugawara and Nikaido 1992), least three sRNAs (for review, see Repoila et al. 2003). even though its role in the total permeability of the cell It is becoming increasingly clear that base-pairing is likely negligible compared to OmpC and OmpF. sRNAs are widespread regulators of genetic expression OmpA has also been implicated in stabilizing the cell in bacteria. This mode of regulation has several major envelope structure (Sonntag et al. 1978). While OmpF advantages for the cell. Synthesis of sRNA regulators is and OmpC, and probably OmpA, serve as general entry rapid and requires less energy input than the synthesis of portals for small molecules, other related ␤-barrel outer protein regulators. In addition, a given sRNA can act at membrane proteins act as specific channels, often for multiple targets, in response to input signals distinct larger nutrients such as vitamin B12 and iron–sidero- from those regulating transcription of the target; mul- phore complexes (for review, see Nikaido 2003). Trans- tiple sRNAs can also act on a single target and provide port through these channels, sometimes referred to as the integration of different input signals. Degradation of gated channels, is coupled to TonB, which is part of a the mRNA clearly makes the process irreversible; it is complex of proteins found in the inner membrane that less clear whether translational repression or activation, couple the gated channels to the protonmotive force, the in the absence of degradation, is a reversible process. energy source for transport (for review, see Postle and Investigations of the regulation and targets of sRNAs Kadner 2003). Yet other outer membrane proteins serve have recently uncovered a major role for these molecules as anchors for cell surface organelles such as pili. in the modulation of the bacterial cell surface, in par- With their accessibility on the outside of the bacterial ticular, outer membrane proteins of Gram-negative bac- cell, outer membrane proteins also represent attachment teria. Here we introduce the critical characteristics of sites for bacteriophages and colicins. In addition, outer the outer membrane, followed by a consideration of the membrane proteins and structures such as flagella and sRNAs that regulate outer membrane proteins. LPS are the features recognized by the immune system of eukaryotic cells and in some cases are required for host cell interactions. Given the importance of the outer membrane, it is not The E. coli outer membrane surprising that the expression of outer membrane pro- All Gram-negative bacterial cells are surrounded by a teins has been found to be under complex transcriptional cell envelope, which is comprised of an inner membrane, regulation. Two key regulators are the inner membrane a periplasmic space, and an outer membrane (for review, sensor kinase EnvZ and the cognate response regulator see Ruiz et al. 2006). The inner membrane is a lipid bi- OmpR (for review, see Pratt et al. 1996). EnvZ autophos- layer composed mainly of phospholipids and proteins. phorylates in response to stimuli, such as high osmolar- Proteins found in the inner membrane are primarily in- ity, that appear to perturb the outer membrane environ- volved in metabolic processes such as oxidative phos- ment. EnvZ then transfers its phosphate group to OmpR. phorylation, protein translocation, and small-molecule Depending on its phosphorylation state, OmpR has dif- transport and sensing. The interstitial periplasmic space, ferent binding affinities for different promoters. Thus, at an oxidizing environment lacking ATP that can com- low osmolarity OmpR activates ompF transcription, prise as much as 10% of the cell volume, contains a thin whereas at high osmolarity OmpR represses ompF tran- peptidoglycan layer and soluble proteins. Functions of scription and activates ompC transcription. This regula- periplasmic proteins include the transport of small mol- tion is consistent with what might be expected for the ecules and the breakdown of polymers. The outer mem- porins. Under high osmolarity conditions, such as in en- brane is a very asymmetric lipid bilayer with the inner vironments inside a host where nutrient levels are high, leaflet composed of phospholipids and the outer leaflet the small pore porin OmpC will predominate, thus lim- composed of lipopolysaccharides (LPS).
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