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Chapter 25 : Regulatory Mechanisms of Special Significance: Role of Small RNAs in Virulence Regulation

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Abstract:

Pathogenic bacteria express a myriad of systems aimed at subversion and exploitation of a host to promote proliferation and survival. Naturally, host cells have evolved equally complex defensive mechanisms which the bacterial pathogen must overcome in order to successfully establish an infection. Regulatory RNAs can operate at all layers of gene regulation, ranging from transcriptional initiation to protein activity. This chapter selectively details the best-characterized examples of small noncoding regulatory RNAs (sRNAs) and their molecular function in bacterial pathogens of special interest. serovar Typhimurium is a gram-negative pathogen causing gastroenteritis in humans. The two most recent additions to the list of sRNA regulators affecting pathogenicity are TarA and TarB, both of which are controlled by the master virulence regulator ToxT. Virulence of is modulated by quorum sensing (QS) systems that control the production of several virulence factors in a cell density-dependent manner. Posttranscriptional control by the RNA-binding protein RsmA (CsrA) regulates many virulence genes of . There are a few notable exceptions, including RNAIII in , IsrM in , and several sRNAs in , deletion of which leads to clear virulence phenotypes. While many functionally related virulence factors are often clustered in horizontally acquired pathogenicity islands, trans-acting sRNAs located in the ancestral genome can be co-opted into regulation of horizontally acquired genes, thus linking expression of virulence factors with regulation of the core genome.

Citation: Papenfort K, Corcoran C, Gupta S, Miyakoshi M, Heidrich N, Chao Y, Fröhlich K, Ziebuhr W, Böhm A, Vogel J, Sharma C. 2013. Regulatory Mechanisms of Special Significance: Role of Small RNAs in Virulence Regulation, p 493-527. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch25
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Figure 1

Cross talk of core and horizontally acquired genomic elements at the posttranscriptional level. The core genome-encoded SgrS sRNA downregulates expression of the mRNA, encoding a virulence factor secreted by the T3SS, at the posttranscriptional level. InvR, encoded on the horizontally acquired SPI-1, represses the core genome-encoded mRNA. Both sRNAs require the RNA chaperone Hfq for target regulation. IsrM, also acquired by horizontal gene transfer, reduces the expression of the and mRNAs. Thereby, IsrM indirectly induces T3SS secretion, as encodes a global transcriptional regulator inhibiting virulence factor expression. It is currently unclear if IsrM requires Hfq for target regulation. doi:10.1128/9781555818524.ch25f1

Citation: Papenfort K, Corcoran C, Gupta S, Miyakoshi M, Heidrich N, Chao Y, Fröhlich K, Ziebuhr W, Böhm A, Vogel J, Sharma C. 2013. Regulatory Mechanisms of Special Significance: Role of Small RNAs in Virulence Regulation, p 493-527. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch25
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Image of Figure 2
Figure 2

Repertoire of regulatory mechanisms employed by bacterial RNA regulators. (A) AmgR is a -encoded RNA that is expressed convergent to the ORF in . The PhoPQ TCS activates expression of AmgR and , whereas interaction of both RNAs results in degradation of the RNA duplex. (B) CsrA is an RNA-binding protein that modulates expression by antagonizing translational initiation. CsrB-like RNAs (RsmY/Z) carry multiple CsrA binding sites and counteract CsrA activity via a titration mechanism. (C) The mRNA of the PrfA virulence factor of carries an RNA thermometer in its 5′ UTR. This regulatory structure supports translation initiation at high temperatures of (e.g., the mammalian host) but inhibits ribosome binding at lower temperatures. (D) The VR-RNA activates expression in . In the absence of VR-RNA, translation is inhibited by an internal stem-loop structure, blocking ribosome binding. VR-RNA binding to the 5′ UTR of induces an endonucleolytic cleavage which opens the RBS and generates a novel 5′ end which is resistant to RNase activity. doi:10.1128/9781555818524.ch25f2

Citation: Papenfort K, Corcoran C, Gupta S, Miyakoshi M, Heidrich N, Chao Y, Fröhlich K, Ziebuhr W, Böhm A, Vogel J, Sharma C. 2013. Regulatory Mechanisms of Special Significance: Role of Small RNAs in Virulence Regulation, p 493-527. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch25
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Image of Figure 3
Figure 3

QS- and RNAIII-controlled gene expression. produces an autoinducing peptide which is sensed by a histidine kinase (AgrC). Sensing of the autoinducing peptide by AgrC leads to phosphorylation of the response regulator AgrA, which, in turn, is a transcriptional activator of the bifunctional RNAIII. RNAIII encodes the gene (coding for δ-hemolysin) but also acts as a posttranscriptional regulator of several target mRNAs, most of which have profound impact on virulence. Whereas , , , SA1000, and SA2353 mRNAs are inhibited, the mRNA is induced by RNAIII. doi:10.1128/9781555818524.ch25f3

Citation: Papenfort K, Corcoran C, Gupta S, Miyakoshi M, Heidrich N, Chao Y, Fröhlich K, Ziebuhr W, Böhm A, Vogel J, Sharma C. 2013. Regulatory Mechanisms of Special Significance: Role of Small RNAs in Virulence Regulation, p 493-527. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch25
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