Acquirement of cold sensitivity by quadruple deletion of the <i>cspA</i> family and its suppression by PNPase S1 domain in <i>Escherichia coli</i>

Xia, Bing; Ke, Haiping; Inouye, Masayori

doi:10.1046/j.1365-2958.2001.02372.x

Cited by 205 publications

(226 citation statements)

References 35 publications

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“…In E. coli, the deletion of single csp genes did not result in an obvious phenotype, possibly due to back-up mechanisms based on the presence of closely related CSPs (Xia et al, 2001). In B. bronchiseptica, we investigated the phenotypic effects of mutations in the cspB and cspC genes.…”

Section: Resultsmentioning

confidence: 99%

“…Even the production of knock-out mutants did not contribute much to the understanding of their specific function, possibly because of compensatory effects by related cold-shock proteins. For example, in Bacillus subtilis all three csp genes must be deleted to obtain a lethal phenotype (Graumann et al, 1997), while four out of nine csp genes had to be inactivated before a coldsensitive phenotype was achieved in E. coli Xia et al, 2001). In contrast to these data, the single cspB deletion in B. bronchiseptica led to a growth-impaired phenotype at low (15 u C) and elevated temperature (37 u C).…”

Section: Discussionmentioning

confidence: 99%

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Identification and regulation of cold-inducible factors of Bordetella bronchiseptica

et al. 2005

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The expression of bacterial cold-shock proteins (CSPs) is highly induced in response to cold shock, and some CSPs are essential for cells to resume growth at low temperature. Bordetella bronchiseptica encodes five CSPs (named CspA to CspE) with significant amino acid homology to CspA of Escherichia coli. In contrast to E. coli, the insertional knock-out of a single csp gene (cspB) strongly affected growth of B. bronchiseptica independent of temperature. In the case of three of the csp genes (cspA, cspB, cspC) more than one specific transcript could be detected. The net amount of cspA, cspB and cspC transcripts increased strongly after cold shock, while no such effect could be observed for cspD and cspE. The exposure to other stress conditions, including translation inhibitors, heat shock, osmotic stress and nutrient deprivation in the stationary phase, indicated that the csp genes are also responsive to these conditions. The coding regions of all of the cold-shock genes are preceded by a long non-translated upstream region (59-UTR). In the case of the cspB gene, a deletion of parts of this region led to a significant reduction of translation of the resulting truncated transcript, indicating a role of the 59-UTR in translational control. The cold-shock stimulon was investigated by 2D-PAGE and mass spectrometric characterization, leading to the identification of additional cold-inducible proteins (CIPs). Interestingly, two cold-shock genes (cspC and cspD) were found to be under the negative control of the BvgAS system, the main transcriptional regulator of Bordetella virulence genes. Moreover, a negative effect of slight overexpression of CspB, but not of the other CSPs, on the transcription of the adenylate cyclase toxin CyaA of Bordetella pertussis was observed, suggesting cross-talk between the CSP-mediated stress response stimulon and the Bordetella virulence regulon.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Identification and regulation of cold-inducible factors of Bordetella bronchiseptica

et al. 2005

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“…CSPs, which consist of a 5-stranded anti-parallel ␤-barrel (32), share structural similarity to the S1 domains found in PNPase and the ribosomal protein S1 and have been shown to melt out mRNA secondary structures that form at lower temperatures (33). Xia and Inouye (34) reported that a quadruple deletion of 4 of the 9 CSPs rendered E. coli cold-sensitive, and that overexpressing any 8 of the 9 CSPs or the S1 domain from E. coli PNPase alone enabled the quadruple-deleted strain to grow in the cold. Thus, several proteins with bona fide S1 domains as well as proteins that resemble S1 domains (e.g.…”

Section: Discussionmentioning

confidence: 99%

Modulation of Yersinia Type Three Secretion System by the S1 Domain of Polynucleotide Phosphorylase

Rosenzweig

Weltman

Plano

et al. 2005

Journal of Biological Chemistry

120

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Both low temperatures and encounters with host phagocytes are two stresses that have been relatively well studied in many species of bacteria. Previous work has shown that the exoribonuclease polynucleotide phosphorylase (PNPase) is required for Yersiniae to grow at low temperatures. Here, we show that PNPase also enhances the ability of Yersinia pseudotuberculosis and Yersinia pestis to withstand the killing activities of murine macrophages. PNPase is required for the optimal functioning of the Yersinia type three secretion system (TTSS), an organelle that injects effector proteins directly into host cells. Unexpectedly, the effect of PNPase on the TTSS is independent of its ribonuclease activity and instead requires its S1 RNA binding domain. In contrast, catalytically inactive enzyme does not enhance the low temperature growth effect of PNPase. Surprisingly, wild-type-like TTSS functioning was restored to the pnp mutant strain by expressing just the ϳ70 amino acid S1 domains from either PNPase, RNase R, RNase II, or RpsA. Our findings suggest that PNPase plays multifaceted roles in enhancing Yersinia survival in response to stressful conditions.

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“…E. coli CspA binds to ssDNA/RNA without apparent sequence specificity and has been proposed to function as an RNA chaperone that facilitates efficient translation at low temperature (22). Two internal highly conserved consensus RNA-binding motifs (RNP-1 and RNP-2) are critical for CSD nucleotide binding activity (41). A recent paper reported that the CspA protein family acts as transcription anti-terminators and regulates mRNA levels of cold-induced genes in the metY-rpsO operon (23).…”

Section: Discussionmentioning

confidence: 99%

A Cold-regulated Nucleic Acid-binding Protein of Winter Wheat Shares a Domain with Bacterial Cold Shock Proteins

Karlson

Nakaminami

Toyomasu

et al. 2002

Journal of Biological Chemistry

144

154

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The molecular mechanisms of cold acclimation are still largely unknown; however, it has been established that overwintering plants such as winter wheat increases freeze tolerance during cold treatments. In prokaryotes, cold shock proteins are induced by temperature downshifts and have been proposed to function as RNA chaperones. A wheat cDNA encoding a putative nucleic acid-binding protein, WCSP1, was isolated and found to be homologous to the predominant CspA of Escherichia coli. The putative WCSP1 protein contains a three-domain structure consisting of an N-terminal cold shock domain with two internal conserved consensus RNA binding domains and an internal glycine-rich region, which is interspersed with three C-terminal CX 2 CX 4 HX 4 C (CCHC) zinc fingers. Each domain has been described independently within several nucleotide-binding proteins. Northern and Western blot analyses showed that WCSP1 mRNA and protein levels steadily increased during cold acclimation, respectively. WCSP1 induction was cold-specific because neither abscisic acid treatment, drought, salinity, nor heat stress induced WCSP1 expression. Nucleotide binding assays determined that WCSP1 binds ssDNA, dsDNA, and RNA homopolymers. The capacity to bind dsDNA was nearly eliminated in a mutant protein lacking C-terminal zinc fingers. Structural and expression similarities to E. coli CspA suggest that WCSP1 may be involved in gene regulation during cold acclimation.

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Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli

Cited by 205 publications

References 35 publications

Identification and regulation of cold-inducible factors of Bordetella bronchiseptica

Identification and regulation of cold-inducible factors of Bordetella bronchiseptica

Modulation of Yersinia Type Three Secretion System by the S1 Domain of Polynucleotide Phosphorylase

A Cold-regulated Nucleic Acid-binding Protein of Winter Wheat Shares a Domain with Bacterial Cold Shock Proteins

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