Chapter 26 : Negative Regulation during Bacterial Infection

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This chapter highlights some of the many interesting cases of negative regulation at work during different stages of infection for several pathogens, focusing on the diverse molecular mechanisms involved in gene repression and the selective pressures that led to their evolution. Some pathogenic bacteria cycle through multiple hosts; for example, some pathogens use arthropod vectors to invade human populations, an extreme transition that demands a great deal of regulatory flexibility. During infection, pathogenic bacteria must contend with an in vivo environment that is under the surveillance of immune mechanisms capable of rapidly identifying and eliminating foreign microorganisms. Immune recognition presents a significant challenge to pathogenic bacteria. A central mechanism to evade host defenses is to stop producing the structures, such as flagella and pili, that are recognized by host antibodies and toll-like receptors (TLRs). During infection of a new host, flagellar breakage allows the derepression of virulence again. Negative regulation in transcriptional programs in vivo has also been found in , a gram-negative pathogen that is the cause of disease in humans and other mammalian hosts. Virulence genes are frequently encoded in clusters on the genomes of pathogens, and these clusters are termed “pathogenicity islands". The deactivation of CovR has been shown to be mediated through selection of CovS mutants in the presence of innate immune responses, but it also appears to be regulated by as-yet-unknown signals sensed by CovS.

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
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Figure 1

The BvgAS two-component system of controls multiple genes. Under Bvg conditions, the membrane protein BvgS and cytosolic DNA-binding protein BvgA are unphosphorylated. This allows transcription of flagellar genes but not virulence factors such as adhesins and toxins. In response to certain environmental stimuli, the cell switches to a Bvgstate, which is characterized by a phosphorylated BvgS and BvgA. This activated form of BvgA represses flagellar gene expression and activates the expression of adhesins and toxins. The timely repression of flagellar genes in the Bvg state is critical for infection. doi:10.1128/9781555818524.ch26f1

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
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Figure 2

Temperature-dependent repression of flagellar synthesis in . Flagellar genes are repressed by the DNA-binding protein MogR, but under low temperatures, the anti-repressor GmaR binds to and titrates MogR away from the flagellar promoter, allowing expression of flagellar genes. As the temperature increases, a conformational change in GmaR takes place, targeting it for degradation. This allows MogR to bind flagellar promoters and repress transcription. doi:10.1128/9781555818524.ch26f2

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
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Figure 3

Flagellar breakage signals repression of to allow virulence gene expression in . At the high cell densities present in a . inoculum, virulence genes are repressed by the quorum-sensing regulator HapR. As the vibrios penetrate the mucus layer of the host small intestines, the flagella break off, allowing the basal-body-hook complex (BBH) to export the anti-sigma factor FlgM. This frees the sigma factor FliA to repress , which in turn allows virulence gene expression. doi:10.1128/9781555818524.ch26f3

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
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Figure 4

H-NS-mediated repression of transcription of foreign DNA. The nucleoid-associated protein H-NS represses transcription of A+T-rich foreign DNA, a process known as “xenogeneic silencing.” H-NS-mediated gene repression has evolved to become a timing mechanism for the expression of virulence genes, which are commonly inherited horizontally. After acquisition of new A+T-rich DNA, such as might encode virulence genes, the H-NS protein represses transcription of this DNA. Under virulence-inducing conditions, a virulence-activating transcription factor may displace H-NS from the DNA to allow transcription. In an mutant, however, virulence genes may be active under nonvirulent conditions, which can be deleterious to the bacteria. The presence of H-NS or other repressive nucleoid-associated proteins thus ensures timely activation of virulence programs for a wide variety of bacteria. doi:10.1128/9781555818524.ch26f4

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
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Figure 5

Selection of invasive mutants in group A . In the colonizing but noninvasive state, the protease SpeB is expressed, causing degradation or truncation of numerous virulence factors. The expression of SpeB is controlled by the two-component system CovRS. In the presence of neutrophil extracellular traps, there is a selective pressure for expression of the DNase Sda1, which is normally repressed by CovRS. This pressure causes the outgrowth of mutants, which has the effect of coselecting for strains with decreased SpeB expression, leading to increased virulence factor production and an invasive phenotype. doi:10.1128/9781555818524.ch26f5

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
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