A transcriptional response to replication status mediated by the conserved bacterial replication protein DnaA

Goranov, Alexi I.; Katz, Luba; Breier, Adam M.; Burge, Christopher B.; Grossman, Alan D.

doi:10.1073/pnas.0506174102

Cited by 97 publications

(267 citation statements)

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“…In the strain with oriC at 257°, replication of one arm of the chromosome takes much less time than replication of the other. In addition, head-on transcription and replication appear to cause induction of the SOS response (see Discussion), which can also cause an increase in DnaAdependent replication initiation at oriC (23,28). We postulate that a significant effect of having oriC at 257°is to cause an increase in DnaA-dependent replication initiation.…”

Section: Inhibition Of Replication Elongation In the Head-onmentioning

confidence: 96%

“…This is probably due to DnaAdependent feedback regulation of replication initiation by replication elongation. Initiation at oriC can be stimulated when elongation is inhibited (23,28). In the strain with oriC at 257°, replication of one arm of the chromosome takes much less time than replication of the other.…”

Section: Inhibition Of Replication Elongation In the Head-onmentioning

confidence: 99%

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Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis

Wang

Berkmen

Grossman

2007

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

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102

119

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In many bacteria, there is a strong bias for genes to be encoded on the leading strand of DNA, resulting in coorientation of replication and transcription. In Bacillus subtilis, transcription of the majority of genes (75%) is cooriented with replication. By using genomewide profiling of replication with DNA microarrays, we found that this coorientation bias reduces adverse effects of transcription on replication. We found that in wild-type cells, transcription did not appear to affect the rate of replication elongation. However, in mutants with reversed transcription bias for an extended region of the chromosome, replication elongation was slower. This reduced replication rate depended on transcription and was limited to the region in which the directions of replication and transcription are opposed. These results support the hypothesis that the strong bias to coorient transcription and replication is due to selective pressure for processive, efficient, and accurate replication.DNA microarrays ͉ elongation of replication ͉ genomic organization ͉ genomic stability ͉ origin of replication M any aspects of the organization of bacterial genomes are conserved and important for cell survival. DNA rearrangements, including large chromosomal inversions, can lead to inviability, decreased fitness, and impaired development (1-4). It has been proposed that genomic organization affects replication, transcription, and segregation of genomes (5).One benefit of proper genomic organization may be the reduction of potential conflicts between replication and transcription (5-7). The same DNA template is used by RNA polymerase (RNAP) for transcription and by the replisome (DNA polymerase and associated proteins) for replication. Transcription complexes that are stalled, initiating, or terminating can slow or block replication (8, 9). RNAP and the replisome can collide when moving toward each other (head-on), or when the replisome, which moves faster than RNAP, catches up with RNAP moving in the same direction (codirectional). Head-on and codirectional collisions can occur when genes are on the lagging and leading strands, respectively.The consequences of head-on and codirectional collisions are different. In Escherichia coli, high levels of transcription can effectively slow or block progression of replication forks if transcription and replication are head-on, but not if they are codirectional (10). In French's landmark study, an inducible plasmid-derived origin of replication was positioned on either side of an rRNA operon, one of the most highly transcribed operons. Replication fork progression, monitored by EM, was much slower when running against, rather than with, the direction of transcription. Plasmid DNA replication in E. coli can also be hindered by head-on transcription from a strong inducible promoter, probably because of collisions between the replisome and RNAP (ref.

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Section: Inhibition Of Replication Elongation In the Head-onmentioning

confidence: 96%

Section: Inhibition Of Replication Elongation In the Head-onmentioning

confidence: 99%

Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis

Wang

Berkmen

Grossman

2007

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

Self Cite

102

119

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“…The activity of KinA is inhibited not only by Sda, which is induced when DNA replication is perturbed (Burkholder et al, 2001;Goranov et al, 2005;Ruvolo et al, 2006;Ishikawa et al, 2007), but also by KipI, which is expressed under specific nutrient conditions (Wang et al, 1997). KipI appears to be poised to inhibit KinA in response to an additional unknown signal, because it is coexpressed with a protein that binds and inhibits KipI, KipA (Wang et al, 1997).…”

Section: Discussionmentioning

confidence: 99%

“…Sda expression is induced in response to perturbations in DNA replication or DNA damage, preventing cells from sporulating until chromosome replication has been resumed or completed (Burkholder et al, 2001;Goranov et al, 2005;Ruvolo et al, 2006;Ishikawa et al, 2007). KipI expression is induced when cells are required to use a non-preferred nitrogen source but still have a preferred carbon source (Wang et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

The histidine kinase inhibitor Sda binds near the site of autophosphorylation and may sterically hinder autophosphorylation and phosphotransfer to Spo0F

Cunningham

Burkholder²

2009

Molecular Microbiology

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SummaryHistidine kinases are widely used by bacteria, fungi and plants to sense and respond to changing environmental conditions. Signals in addition to those directly sensed by the kinase are often integrated by proteins that fine-tune the biological response by modulating the activity of the kinase or its targets. The Bacillus subtilis histidine kinase KinA promotes the initiation of sporulation when nutrients are limiting, but sporulation can be delayed by two inhibitors of KinA, Sda (when DNA replication is perturbed) or KipI (under unknown conditions). We have identified residues in the dimerization/histidinephosphotransfer (DHp) domain of KinA that are functionally important for inhibition by Sda and KipI and overlapping surface-exposed residues that lie close to or comprise the Sda binding site. Sda inhibits the intermolecular transfer of phosphate from the catalytic ATP-binding (CA) domain of KinA to the autophosphorylation site in the DHp domain when the domains are split into separate polypeptides, either by steric hindrance or by altering the conformation of the DHp domain. Sda also slows the rate of phosphotransfer from KinA~P to its target, Spo0F, consistent with our finding that a KinA residue important for Sda function overlaps with the predicted Spo0F binding site on KinA.

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“…Both proteins bind to KinA, thereby blocking autophosphorylation. The synthesis of Sda is induced in response to DNA damage, preventing sporulation if chromosome replication is impaired (6,16,19,33). The production of KipI appears to be linked to the utilization of nitrogen, but the specific signal that results in its inhibition of KinA is not known (39).…”

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confidence: 99%

Phosphorylation of Spo0A by the Histidine Kinase KinD Requires the Lipoprotein Med in Bacillus subtilis

2011

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The response regulatory protein Spo0A of Bacillus subtilis is activated by phosphorylation by multiple histidine kinases via a multicomponent phosphorelay. Here we present evidence that the activity of one of the kinases, KinD, depends on the lipoprotein Med, a mutant of which has been known to cause a cannibalism phenotype. We show that the absence of Med impaired and the overproduction of Med stimulated the transcription of two operons (sdp and skf) involved in cannibalism whose transcription is known to depend on Spo0A in its phosphorylated state (Spo0AϳP). Further, these effects of Med were dependent on KinD but not on kinases KinA, KinB, and KinC. Additionally, we show that deletion or overproduction of Med impaired or enhanced, respectively, biofilm formation and that these effects, too, depended specifically on KinD. Finally, we report that overproduction of Med bypassed the dominant negative effect on transcription of sdp of a truncated KinD retaining the transmembrane segments but lacking the kinase domain. We propose that Med directly or indirectly interacts with KinD in the cytoplasmic membrane and that this interaction is required for KinDdependent phosphorylation of Spo0A.

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A transcriptional response to replication status mediated by the conserved bacterial replication protein DnaA

Cited by 97 publications

References 67 publications

Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis

Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis

The histidine kinase inhibitor Sda binds near the site of autophosphorylation and may sterically hinder autophosphorylation and phosphotransfer to Spo0F

Phosphorylation of Spo0A by the Histidine Kinase KinD Requires the Lipoprotein Med in Bacillus subtilis

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