Transcriptional and post‐transcriptional control of polynucleotide phosphorylase during cold acclimation in <i>Escherichia coli</i>

Zangrossi, Sandro; Briani, Federica; Ghisotti, Daniela; Regonesi, Maria Elena; Tortora, Paolo; Dehò, Gianni

doi:10.1046/j.1365-2958.2000.01971.x

Cited by 84 publications

(104 citation statements)

References 52 publications

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“…For example, in laboratory strains of E. coli one function of PNPase is to degrade cold-shock protein mRNAs, ensuring their transient expression during bacterial cold adaptation (36)(37)(38). Conversely, RNase R* of Shigella flexneri has been reported to be required for the expression of the invasion factors IpaB, IpaC, and IpaD (47).…”

Section: Discussionmentioning

confidence: 99%

“…In this context it is interesting to note that inactivation of PNPase also resulted in increased intracellular replication. The expression of PNPase is autoregulated, as well as responding to environmental changes in E. coli (36)(37)(38). From this finding one may suggest a role for PNPase in degrading mRNAs that adapt the bacteria for host milieu, as does PhoP͞PhoQ and SpvR (6,7), and that a disturbance in such a regulation leads to altered expression of selected virulence functions, which causes altered infection pathogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…PNPase is a defined cold-shock protein in E. coli and Bacillus subtilis, and pnp mutants replicate slower at low temperature (36)(37)(38). When grown in LB at 37°C or 39°C, the doubling times of MC1, MC2, and MC71 were the same (approximately 20 min) (20).…”

Section: The Pnp Mutant Mc2 Shows Increased Invasion and Intracellularmentioning

confidence: 99%

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Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica

Clements

Eriksson

Thompson

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

154

133

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For many pathogens, the ability to regulate their replication in host cells is a key element in establishing persistency. Here, we identified a single point mutation in the gene for polynucleotide phosphorylase (PNPase) as a factor affecting bacterial invasion and intracellular replication, and which determines the alternation between acute or persistent infection in a mouse model for Salmonella enterica infection. In parallel, with microarray analysis, PNPase was found to affect the mRNA levels of a subset of virulence genes, in particular those contained in Salmonella pathogenicity islands 1 and 2. The results demonstrate a connection between PNPase and Salmonella virulence and show that alterations in PNPase activity could represent a strategy for the establishment of persistency.T he species Salmonella enterica is a classic example of the facultative intracellular pathogen that can cause acute and persistent infections (1-4). Typhoid fever is a serious manifestation of systemic salmonellosis in humans and involves an estimated 16.6 million new cases per year (2) with between 2% and 5% of the cases developing into the carrier state (3, 4).Much of the knowledge of salmonellosis pathogenesis comes from work on the murine salmonellosis model (1, 5), and this model has been used to define bacterial virulence factors (1, 6, 7). An important virulence trait of Salmonella is its ability to invade and grow within host cells, and many of the genetic determinants essential for these processes have been well characterized (8-11). Invasion of epithelial cells requires the expression of a type III secretion apparatus, which translocates effector proteins from the bacterium to the host cell, inducing the cell to internalize the bacteria by bacterial-mediated endocytosis (8,11). Proteins involved in this process are encoded by a large cluster of genes collectively termed Salmonella pathogenicity island 1 (SPI 1). The ability to grow intracellularly, once internalized within the host cell, requires the coordinate expression of additional sets of virulence factors (6), such as SPI 2 (1, 10).Although chronic carriage of Salmonella is recognized as a significant complication that facilitates spread of the disease (2) and predisposes victims to additional clinical conditions (12, 13) the mechanism underlying persistency has remained poorly understood. We discovered the link between polynucleotide phosphorylase (PNPase) and chronic infection while characterizing a mutant of Salmonella typhimurium that was defective in its expression of virulence-associated AgfA fimbriae and known to establish persistent infection in BALB͞c mice (14). Materials and Methods Mapping and Sequencing of MC2 Mutation.A random Tn10camd insertion library from S. typhimurium 14028 (22) was transduced into MC1 by P22 transduction selecting for chloramphenicolresistant colonies. Transductants were pooled and used to propagate phage KB1, which was then used to transduce MC2. Chloramphenicol-resistant colonies were screened for agf expression on Congo red pla...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica

Clements

Eriksson

Thompson

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

154

133

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“…These enzymes are primarily involved in RNA metabolism. Both PNPase, 93,94 and RNase R95 are induced by cold shock and are suggested to be the universal degraders of structured RNA in the cell. 96,97 RNase II is not cold shock inducible.…”

Section: Cold-inducible Exoribonucleasesmentioning

confidence: 99%

RNA remodeling and gene regulation by cold shock proteins

2010

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“…It has been proposed that RNase R along with PNPase, encoded by rnr and pnp genes, respectively, are responsible for quality control of rRNA and that rnr pnp double mutants are inviable (12). Interestingly, PNPase was found important for growth at low temperature in E. coli and in the psychrotrophic Yersinia enterocolitica (13,14), although the pnp mutants of P. putida were not cold-sensitive (15). RNase R, on the other hand, was shown to be cold-inducible and involved in tmRNA maturation in E. coli, but the rnr mutant was not cold-sensitive (16).…”

mentioning

confidence: 99%

Exoribonuclease R in Pseudomonas syringae Is Essential for Growth at Low Temperature and Plays a Novel Role in the 3′ End Processing of 16 and 5 S Ribosomal RNA

Rajyaguru

Madhuri

Ray

2007

Journal of Biological Chemistry

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The (3 3 5) exoribonuclease RNase R interacts with the endoribonuclease RNase E in the degradosome of the coldadapted bacterium Pseudomonas syringae Lz4W. We now present evidence that the RNase R is essential for growth of the organism at low temperature (4°C). Mutants of P. syringae with inactivated rnr gene (encoding RNase R) are cold-sensitive and die upon incubation at 4°C, a phenotype that can be complemented by expressing RNase R in trans. Overexpressing polyribonucleotide phosphorylase in the rnr mutant does not rescue the cold sensitivity. This is different from the situation in Escherichia coli, where rnr mutants show normal growth, but pnp (encoding polyribonucleotide phosphorylase) and rnr double mutants are nonviable. Interestingly, RNase R is not cold-inducible in P. syringae. Remarkably, however, rnr mutants of P. syringae at low temperature (4°C) accumulate 16 and 5 S ribosomal RNA (rRNA) that contain untrimmed extra ribonucleotide residues at the 3 ends. This suggests a novel role for RNase R in the rRNA 3 end processing. Unprocessed 16 S rRNA accumulates in the polysome population, which correlates with the inefficient protein synthesis ability of mutant. An additional role of RNase R in the turnover of transfer-messenger RNA was identified from our observation that the rnr mutant accumulates transfer-messenger RNA fragments in the bacterium at 4°C. Taken together our results establish that the processive RNase R is crucial for RNA metabolism at low temperature in the coldadapted Antarctic P. syringae.Regulated degradation of RNA within cells is mostly an outcome of coordinated and combined activities of endoribonucleases, exoribonucleases, and RNA helicases. In bacteria, few of these enzymes interact with each other to form the RNA degradosome complex (1-3). The degradosome has been shown to be involved in both mRNA and rRNA degradation (4, 5). In the Escherichia coli degradosome, RNase E (a 5Ј end-dependent endoribonuclease) associates with polynucleotide phosphorylase (PNPase, 2 a 3Ј 3 5Ј exoribonuclease), RhlB (a DEAD box RNA helicase), and enolase (an enzyme of glycolytic pathway) to constitute the "core" complex. Additionally, DnaK, poly(A) polymerase and polyphosphate kinase have also been reported to be a part of this complex (6). A similar kind of RNA degrading complex has also been reported from Rhodobacter capsulatus (7). On the other hand, we have recently shown that exoribonuclease RNase R interacts with RNase E in the degradosome of the cold-adapted Antarctic bacterium Pseudomonas syringae Lz4W (8). This bacterium does have a pnp gene that is expressed but does not form a part of this complex.3 PNPase and RNase R differ in their mode of action, the former exhibiting phosphorolytic activity and the latter exhibiting hydrolytic activity.RNase R is one of the eight exoribonucleases reported in E. coli and distributed widely in different prokaryotes (9). Although all of these exoribonucleases display 3Ј 3 5Ј activity on RNA substrate, RNase R is the most highly processive enzyme among ...

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Transcriptional and post‐transcriptional control of polynucleotide phosphorylase during cold acclimation in Escherichia coli

Cited by 84 publications

References 52 publications

Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica

Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica

RNA remodeling and gene regulation by cold shock proteins

Exoribonuclease R in Pseudomonas syringae Is Essential for Growth at Low Temperature and Plays a Novel Role in the 3′ End Processing of 16 and 5 S Ribosomal RNA

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