Absence of YbeY RNase compromises the growth and enhances the virulence plasmid gene expression of Yersinia enterocolitica O:3

Leskinen, Katarzyna; Varjosalo, Markku; Skurnik, Mikael

doi:10.1099/mic.0.083097-0

Cited by 36 publications

(46 citation statements)

References 56 publications

(56 reference statements)

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“…In V. cholerae , YbeY is involved in pathogenesis, as its depletion leads to reduced colonization of mouse intestines and decreased cholera toxin production (2). Moreover, inactivation of YbeY was recently shown to impair many virulence-related features of Yersinia enterocolitica (10). Yet another striking example for YbeY’s central role in bacterial RNA metabolism is its association with apoptosis-like death (ALD) in E. coli in response to severe DNA damage, which—among other specific characteristics—also shows YbeY-dependent rRNA degradation (11).…”

Section: Introductionmentioning

confidence: 99%

Identification of YbeY-Protein Interactions Involved in 16S rRNA Maturation and Stress Regulation in Escherichia coli

Vercruysse

Köhrer

Shen³

et al. 2016

mBio

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YbeY is part of a core set of RNases in Escherichia coli and other bacteria. This highly conserved endoribonuclease has been implicated in several important processes such as 16S rRNA 3′ end maturation, 70S ribosome quality control, and regulation of mRNAs and small noncoding RNAs, thereby affecting cellular viability, stress tolerance, and pathogenic and symbiotic behavior of bacteria. Thus, YbeY likely interacts with numerous protein or RNA partners that are involved in various aspects of cellular physiology. Using a bacterial two-hybrid system, we identified several proteins that interact with YbeY, including ribosomal protein S11, the ribosome-associated GTPases Era and Der, YbeZ, and SpoT. In particular, the interaction of YbeY with S11 and Era provides insight into YbeY’s involvement in the 16S rRNA maturation process. The three-way association between YbeY, S11, and Era suggests that YbeY is recruited to the ribosome where it could cleave the 17S rRNA precursor endonucleolytically at or near the 3′ end maturation site. Analysis of YbeY missense mutants shows that a highly conserved beta-sheet in YbeY—and not amino acids known to be important for YbeY’s RNase activity—functions as the interface between YbeY and S11. This protein-interacting interface of YbeY is needed for correct rRNA maturation and stress regulation, as missense mutants show significant phenotypic defects. Additionally, structure-based in silico prediction of putative interactions between YbeY and the Era-30S complex through protein docking agrees well with the in vivo results.

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Section: Introductionmentioning

confidence: 99%

Identification of YbeY-Protein Interactions Involved in 16S rRNA Maturation and Stress Regulation in Escherichia coli

Vercruysse

Köhrer

Shen³

et al. 2016

mBio

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“…A transcriptomic study designed to identify genes under the control of the recently recognized YbeY endonuclease demonstrated that deletion of the ybeY gene led to an upregulation of lcrF and the T3SS/yop genes in Y. enterocolitica serotype O:3 under conditions in which these genes are usually repressed (i.e., at 22°C) (76). This derepression was not caused by lower YmoA levels, since the amount of ymoA transcript was increased in the ybeY mutant.…”

Section: Ypstb Ypiii 598 Tcatttcttttctattagtggggtgcgctacccccccaatgccmentioning

confidence: 99%

“…This derepression was not caused by lower YmoA levels, since the amount of ymoA transcript was increased in the ybeY mutant. Instead, the authors suggested that lcrF upregulation in the ybeY mutant was due to increased copy numbers of the virulence plasmid or to altered regulation of global regulators (e.g., Hfq, nucleoid-structuring proteins) affecting the noncoding RNA network and/or DNA supercoiling (76).…”

Section: Ypstb Ypiii 598 Tcatttcttttctattagtggggtgcgctacccccccaatgccmentioning

confidence: 99%

Yersinia Type III Secretion System Master Regulator LcrF

et al. 2016

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c Many Gram-negative pathogens express a type III secretion (T3SS) system to enable growth and survival within a host. The three human-pathogenic Yersinia species, Y. pestis, Y. pseudotuberculosis, and Y. enterocolitica, encode the Ysc T3SS, whose expression is controlled by an AraC-like master regulator called LcrF. In this review, we discuss LcrF structure and function as well as the environmental cues and pathways known to regulate LcrF expression. Similarities and differences in binding motifs and modes of action between LcrF and the Pseudomonas aeruginosa homolog ExsA are summarized. In addition, we present a new bioinformatics analysis that identifies putative LcrF binding sites within Yersinia target gene promoters. There are three Yersinia species pathogenic to humans. Y. pestis is the causative agent of bubonic and pneumonic plague and is transmitted through a flea vector or through airborne transmission from one mammalian host to another (1). In contrast, the enteropathogenic Yersinia species Y. enterocolitica and Y. pseudotuberculosis grow in the environment but can be transmitted to mammalian hosts through ingestion of contaminated food or water (1). Y. enterocolitica and Y. pseudotuberculosis cause typically self-limiting mesenteric lymphadenitis or gastroenteritis in otherwise healthy individuals but can cause a serious blood-borne infection in people with iron overload disorders such as hereditary hemochromatosis (2). In addition, sequelae following enteropathogenic Yersinia infection, such as erythema nodosum and reactive arthritis, have also been reported (3-5).Human-pathogenic Yersinia species share a virulence plasmid, called pCD1 in Y. pestis and pYV in enteropathogenic yersiniae, encoding the Ysc type III secretion system (T3SS) essential for causing disease (6). These 70-kb plasmids carry dozens of T3SS structural genes and encode five or six T3SS effector proteins called Yops and their dedicated chaperones, as well as genes encoding proteins involved in regulating expression and function of the T3SS. One of these regulatory proteins, LcrF, serves as the Yersinia T3SS master regulator, controlling transcription of a large number of plasmid-borne genes. Several environmental cues influence expression of LcrF itself, possibly enabling Yersinia to control T3SS expression during transitions from one niche to another. Recent reviews have highlighted important advances in our understanding of T3SS structure and modulation of the innate immune response by T3SS effector proteins (7). In this review, we focus on factors controlling LcrF expression, the target genes LcrF regulates, and how LcrF activity influences Yersinia pathogenesis. LcrF HISTORY, STRUCTURE, AND FUNCTIONIt has long been appreciated that human-pathogenic Yersinia carrying T3SS genes requires millimolar concentrations of calcium to grow at 37°C, and this phenomenon was termed the low-calcium response, or Lcr (8, 9). The absence of calcium, in combination with a shift to 37°C, triggers secretion of T3SS effector proteins, mimicking t...

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“…Since the levels of Ysc/Yop transcripts and proteins were increased or remained unchanged in the absence of a functional PNPase or RNase E, they seem to influence transcription/mRNA decay and activity of the T3SS by distinct mechanisms [61]. Moreover, the single-strand specific RNase Y (YbeY) that processes the 3'-ends of the 16S rRNA and is responsible for the late-stage 70S ribosome quality control, also affects many virulence-related features, including acid stress resistance, cell adhesion/invasion properties and T3SS [62]. Among the YbeY-regulated ncRNAs are CsrB and CsrC of the global carbon starvation regulator system, which may explain the pleiotropic virulence-associated phenotypic changes of an ybeY mutant.…”

Section: Changing Mrna Half-livesmentioning

confidence: 99%