Heat shock protein synthesis during development in Caulobacter crescentus

Gomes, Suely Lopes; Juliani, Maria Helena; Maia, J C C; Silva, A. M.

doi:10.1128/jb.168.2.923-930.1986

Cited by 37 publications

(36 citation statements)

References 41 publications

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“…This correlates well with the large increase in synthesis rates of the proteins DnaK and GroEL upon heat shock (28,49). Additionally, the expression rate of a reporter gene transcriptionally fused to either the hrcA or grpE promoter increased during the initial 10 min of heat shock, although to a much smaller degree.…”

Section: Discussionmentioning

confidence: 59%

“…correlates well with the observed loss of motility of C. crescentus cells at 42ЊC (28). Fusions to the xyl promoter (38) (Fig.…”

Section: Vol 178 1996mentioning

confidence: 60%

“…These two cell types differ both in their ability to replicate DNA and in their programs of gene expression (reviewed in references 8 and 25). It has been demonstrated that under physiological conditions, several heat shock homologs are synthesized at discrete times during the C. crescentus cell cycle (27,28) and that their products are distributed asymmetrically upon cell division (49). The dnaKJ operon was shown to be transcribed from a complex set of promoters that control its response to cell cycle timing cues as well as stress cues (5,27).…”

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confidence: 99%

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Identification of a Caulobacter crescentus operon encoding hrcA, involved in negatively regulating heat-inducible transcription, and the chaperone gene grpE

et al. 1996

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In response to elevated temperature, both prokaryotic and eukaryotic cells increase expression of a small family of chaperones. The regulatory network that functions to control the transcription of the heat shock genes in bacteria includes unique structural motifs in the promoter region of these genes and the expression of alternate sigma factors. One of the conserved structural motifs, the inverted repeat CIRCE element, is found in the 5 region of many heat shock operons, including the Caulobacter crescentus groESL operon. We report the identification of another C. crescentus heat shock operon containing two genes, hrcA (hrc for heat shock regulation at CIRCE elements) and a grpE homolog. Disruption of the hrcA gene, homologs of which are also found upstream of grpE in other bacteria, increased transcription of the groESL operon, and this effect was dependent on the presence of an intact CIRCE element. This suggests a role for HrcA in negative regulation of heat shock gene expression. We identified a major promoter transcribing both hrcA and grpE and a minor promoter located within the hrcA coding sequence just upstream of grpE. Both promoters were heat shock inducible, with maximal expression 10 to 20 min after heat shock. Both promoters were also expressed constitutively throughout the cell cycle under physiological conditions. C. crescentus GrpE, shown to be essential for viability at low and high temperatures, complemented an Escherichia coli ⌬grpE strain in spite of significant differences in the N-and C-terminal regions of these two proteins, demonstrating functional conservation of this important stress protein.

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Section: Discussionmentioning

confidence: 59%

“…correlates well with the observed loss of motility of C. crescentus cells at 42ЊC (28). Fusions to the xyl promoter (38) (Fig.…”

Section: Vol 178 1996mentioning

confidence: 60%

mentioning

confidence: 99%

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Identification of a Caulobacter crescentus operon encoding hrcA, involved in negatively regulating heat-inducible transcription, and the chaperone gene grpE

et al. 1996

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“…The dependence of HfiA levels on DnaK suggests that this molecular chaperone provides the cell with an additional mechanism to control holdfast development and surface adherence. Proteotoxic conditions strongly induce DnaK expression in C. crescentus (34,(45)(46)(47)(48). In a model where HfiA is a client for DnaK, increased levels of DnaK are predicted to stabilize HfiA and reduce the number of newborn cells that develop holdfasts.…”

Section: Discussionmentioning

confidence: 99%

Proper Control of Caulobacter crescentus Cell Surface Adhesion Requires the General Protein Chaperone DnaK

2016

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Growth in a surface-attached bacterial community, or biofilm, confers a number of advantages. However, as a biofilm matures, high-density growth imposes stresses on individual cells, and it can become less advantageous for progeny to remain in the community. Thus, bacteria employ a variety of mechanisms to control attachment to and dispersal from surfaces in response to the state of the environment. The freshwater oligotroph Caulobacter crescentus can elaborate a polysaccharide-rich polar organelle, known as the holdfast, which enables permanent surface attachment. Holdfast development is strongly inhibited by the small protein HfiA; mechanisms that control HfiA levels in the cell are not well understood. We have discovered a connection between the essential general protein chaperone, DnaK, and control of C. crescentus holdfast development. C. crescentus mutants partially or completely lacking the C-terminal substrate binding "lid" domain of DnaK exhibit enhanced bulk surface attachment. Partial or complete truncation of the DnaK lid domain increases the probability that any single cell will develop a holdfast by 3-to 10-fold. These results are consistent with the observation that steady-state levels of an HfiA fusion protein are significantly diminished in strains that lack the entire lid domain of DnaK. While dispensable for growth, the lid domain of C. crescentus DnaK is required for proper chaperone function, as evidenced by observed dysregulation of HfiA and holdfast development in strains expressing lidless DnaK mutants. We conclude that DnaK is an important molecular determinant of HfiA stability and surface adhesion control. IMPORTANCERegulatory control of cell adhesion ensures that bacterial cells can transition between free-living and surface-attached states. We define a role for the essential protein chaperone, DnaK, in the control of Caulobacter crescentus cell adhesion. C. crescentus surface adhesion is mediated by an envelope-attached organelle known as the holdfast. Holdfast development is tightly controlled by HfiA, a small protein inhibitor that directly interacts with a WecG/TagA-family glycosyltransferase required for holdfast biosynthesis. We demonstrate that the C-terminal lid domain of DnaK is not essential for growth but is necessary for proper control of HfiA levels in the cell and for control of holdfast adhesin development. Communities of surface-attached bacteria, called biofilms, account for the majority of cells on the surface of our planet. Biofilms allow bacteria to engage in metabolic cooperation, share genetic information, and afford protection from chemical and physical stresses in the environment. Moreover, organic biopolymers and ions accumulate at surfaces through a process known as conditioning (1-4); thus, the ability of a bacterial cell to adhere can confer a nutritional advantage, particularly in oligotrophic environments where nutrients are extremely scarce (5). Clearly, the capacity to transition from a free-living, unicellular lifestyle into a surface-attached ...

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“…Since some studies (7,14,19) (4), the difference in the moles percent G+C between M. barkeri (41 mol% [5]) and E. coli is not as great. It seems likely that M. voltae does possess homologous and conserved heat shock genes.…”

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Heat shock response of the archaebacterium Methanococcus voltae

1991

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The general properties of the heat shock response of the archaebacterium Methanococcus voltue were characterized. The induction of 11 heat shock proteins, with apparent molecular weights ranging from 18,000 to 90,000, occurred optmaly at 40 to 500C. Some of the heat shock proteins were preferentialy enriched in either the soluble (cytoplssm) or particulate (membrane) fraction. Alternative stresses (ethano, hydrogen peroxide, NaCI) stimulated the synthesis of subsets of the heat shock proteins as well as unique proteins. Western blot (inunuoblot) analysis, in which antisera to Escherichia co/i heat shock proteins (DtaK and GroEL) were used, did not detect any immunologkally cross-reactive proteins. In additin, Southem blot analysis did not reveal any homology between M. voltae and four higly conserved heat shock genes, mopB and dnaK from E. coli and hsp7O genes from Drosophia species and Saceharomyces cerevisiae.Most of the studies of archaebacteria have been concerned with their cytochemistry and physiology (8,10,25). Relatively little is known about the genomic organization, transcription, and regulation of gene expression in these microorganisms (5). Expression of genes easily modulated by environmental manipulations, such as the exposure of cells to rapid shifts in temperature (heat shock), would make ideal systems for studying transcriptional regulation. The heat shock response has been studied in numerous eukaryotes and eubacteria (4,(16)(17)(18)20), as well as in three archaebacteria (an extreme halophile, i.e., Halobacterium halobium [6], and the sulfur-dependent thermophiles Sulfolobus acidocaldarius [9] and Sulfolobus sp. strain B12 [23]). To date, this response has not been examined in any members of the methanogens. A general characteristic of the heat shock response is the rapid and usually transient induction of a limited number of proteins (heat shock proteins [HSPs]). In addition to the universal nature of this response, some of the HSPs exhibit high degrees of conservation across the eubacterial and eukaryotic kingdoms at both the amino acid and nucleotide levels (4). The heat shock phenomenon is very well studied (15,16,18,20) and provides an established framework to study gene expression in Methanococcus voltae.(Portions of this work were presented previously [7a, 7b].) M. voltae cells were grown at 30°C as previously described (11) except that Balch medium III (3) was modified to decrease the content of yeast extract and Trypticase 10-fold (to 0.2 g/liter each) and supplemented with the essential amino acids leucine and isoleucine (26) at 0.5 and 1.0 gfliter, respectively. To study heat shock in M. voltae, cell samples (1.0 ml) were dispensed and temperature equilibrated at 30°C before shifting to 45°C. The cells were radiolabeled for 4 min with 25 ,ul of a 2x-concentrated, uniformly labeled "`Camino acid mixture (50 p.CiIml;

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Heat shock protein synthesis during development in Caulobacter crescentus

Cited by 37 publications

References 41 publications

Identification of a Caulobacter crescentus operon encoding hrcA, involved in negatively regulating heat-inducible transcription, and the chaperone gene grpE

Identification of a Caulobacter crescentus operon encoding hrcA, involved in negatively regulating heat-inducible transcription, and the chaperone gene grpE

Proper Control of Caulobacter crescentus Cell Surface Adhesion Requires the General Protein Chaperone DnaK

Heat shock response of the archaebacterium Methanococcus voltae

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