The Bacillus subtilis DnaD and DnaB Proteins Exhibit Different DNA Remodelling Activities

Zhang, Wenke; Carneiro, Maria J. V. M.; Turner, Ian J.; Allen, Stephanie; Roberts, Clive J.; Soultanas, Panos

doi:10.1016/j.jmb.2005.05.065

Cited by 58 publications

(132 citation statements)

References 32 publications

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“…replication factory and from YabA foci during most of the cell cycle, suggesting that YabA is likely not involved in preventing the untimely firing of distant origins, and other levels of initiation control must be present in B. subtilis, as hinted by the functional interplay between DnaB and DnaD at the cell membrane (16)(17)(18). A possibility is that the YabA oligomers could associate with DnaN at the replisome, and could trap the DnaA protein released from the origin immediately after initiation, thus preventing a refiring of the sister oriC.…”

Section: Discussionmentioning

confidence: 99%

“…It has been proposed that initiation could be controlled through the timely interaction of DnaB and DnaD at the cell membrane (17). Furthermore, DnaB and DnaD could exert their role in initiation control through a remodeling of chromosomal DNA at oriC (18). B. subtilis cells lacking yabA exhibit overinitiation and replication asynchrony, suggesting that YabA acts as a negative regulator of initiation (19,20).…”

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confidence: 99%

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Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis

Noirot‐Gros

Velten

Yoshimura

et al. 2006

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

137

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The regulation of initiation of DNA replication is crucial to ensure that the genome is replicated only once per cell cycle. In the Gram-positive bacterium Bacillus subtilis, the function of the YabA protein in initiation control was assigned based on its interaction with the DnaA initiator and the DnaN sliding clamp in the yeast two-hybrid and on the overinitiation phenotype observed in a yabA null strain. However, YabA is unrelated to known regulators of initiation and interacts with several additional proteins that could also be involved directly or not in initiation control. Here, we investigated the specific role of YabA interactions with DnaA and DnaN in initiation control by identifying single amino acid changes in YabA that disrupted solely the interaction with DnaA or DnaN. These disruptive mutations delineated specific interacting surfaces involving a Zn 2؉ -cluster structure in YabA. In B. subtilis, these YabA interaction mutations abolished both initiation control and the formation of YabA foci at the replication factory. Upon coexpression of deficient YabA mutants, mixed oligomers formed foci at the replisome and restored initiation control, indicating that YabA acts within a heterocomplex with DnaA and DnaN. In agreement, purified YabA oligomerized and formed complexes with DnaA and DnaN. These findings underscore the functional association of YabA with the replication machinery, indicating that YabA regulates initiation through coupling with the elongation of replication.DnaA ͉ DnaN ͉ Gram-positive bacteria ͉ initiation control

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis

Noirot‐Gros

Velten

Yoshimura

et al. 2006

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

137

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“…The N-terminal domain of DnaD forms oligomers in the absence of DNA, while the C-terminal domain harbors DNA binding activity and a DNA-dependent oligomerization activity (48). Atomic force microscopy shows that DnaB forms a tetramer with a central hole (476). DnaB binds and condenses DNA, suggesting a more global role in DNA organization in vivo.…”

Section: Primosome Assemblymentioning

confidence: 99%

DNA Repair and Genome Maintenance in Bacillus subtilis

Lenhart

Schroeder

Walsh

et al. 2012

Microbiol Mol Biol Rev

151

155

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SUMMARY From microbes to multicellular eukaryotic organisms, all cells contain pathways responsible for genome maintenance. DNA replication allows for the faithful duplication of the genome, whereas DNA repair pathways preserve DNA integrity in response to damage originating from endogenous and exogenous sources. The basic pathways important for DNA replication and repair are often conserved throughout biology. In bacteria, high-fidelity repair is balanced with low-fidelity repair and mutagenesis. Such a balance is important for maintaining viability while providing an opportunity for the advantageous selection of mutations when faced with a changing environment. Over the last decade, studies of DNA repair pathways in bacteria have demonstrated considerable differences between Gram-positive and Gram-negative organisms. Here we review and discuss the DNA repair, genome maintenance, and DNA damage checkpoint pathways of the Gram-positive bacterium Bacillus subtilis. We present their molecular mechanisms and compare the functions and regulation of several pathways with known information on other organisms. We also discuss DNA repair during different growth phases and the developmental program of sporulation. In summary, we present a review of the function, regulation, and molecular mechanisms of DNA repair and mutagenesis in Gram-positive bacteria, with a strong emphasis on B. subtilis.

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“…DnaD forms scaffolds and converts supercoiled DNA to an open circular form, whereas DnaB compacts laterally supercoiled and linear DNA (35,40). The biological significance of these activities is not clear at present, but we have proposed a functional model with DnaD and DnaB being the link between global or local nucleoid remodeling and the initiation of DNA replication (35,40). Atomic force microscopy (AFM) revealed that DnaD converts all of the writhe of supercoiled plasmids into twist and suggested that this DNA remodeling might be accompanied by significant untwisting of the duplex (40).…”

mentioning

confidence: 99%

“…The biological significance of these activities is not clear at present, but we have proposed a functional model with DnaD and DnaB being the link between global or local nucleoid remodeling and the initiation of DNA replication (35,40). Atomic force microscopy (AFM) revealed that DnaD converts all of the writhe of supercoiled plasmids into twist and suggested that this DNA remodeling might be accompanied by significant untwisting of the duplex (40). Untwisting of the DNA may compensate for the considerable force required to open up supercoiled plasmids without nicking.…”

mentioning

confidence: 99%

TheBacillus subtilisPrimosomal Protein DnaD Untwists Supercoiled DNA

Zhang¹,

Allen

Roberts

et al. 2006

J Bacteriol

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The essential Bacillus subtilis DnaD and DnaB proteins have been implicated in the initiation of DNA replication. Recently, DNA remodeling activities associated with both proteins were discovered that could provide a link between global or local nucleoid remodeling and initiation of replication. DnaD forms scaffolds and opens up supercoiled plasmids without nicking to form open circular complexes, while DnaB acts as a lateral compaction protein. Here we show that DnaD-mediated opening of supercoiled plasmids is accompanied by significant untwisting of DNA. The net result is the conversion of writhe (Wr) into negative twist (Tw), thus maintaining the linking number (Lk) constant. These changes in supercoiling will reduce the considerable energy required to open up closed circular plectonemic DNA and may be significant in the priming of DNA replication. By comparison, DnaB does not affect significantly the supercoiling of plasmids. Binding of the DnaD C-terminal domain (Cd) to DNA is not sufficient to convert Wr into negative Tw, implying that the formation of scaffolds is essential for duplex untwisting. Overall, our data suggest that the topological effects of the two proteins on supercoiled DNA are different; DnaD opens up, untwists and converts plectonemic DNA to a more paranemic form, whereas DnaB does not affect supercoiling significantly and condenses DNA only via its lateral compaction activity. The significance of these findings in the initiation of DNA replication is discussed.DNA replication is the most fundamental function in all biology. It is divided in three main stages known as initiation, elongation, and termination. Initiation involves remodeling of a replication origin (oriC) through the action of the main initiator protein DnaA and primosomal multiprotein cascades that ultimately load two replicative ring helicases, one on each strand of the DNA duplex. The helicases in turn recruit the DNA primases, thus signaling the switch from initiation to elongation and the two replication forks migrate in opposite directions, one on each strand (11,21). Progression to the elongation stage does not guarantee completion of DNA replication since replication forks could be challenged and arrested anywhere along the DNA. In Escherichia coli, reconstitution of an active replication fork at arrested sites is mediated by PriA and/or PriC primosomal pathways that include the PriA, PriB, PriC, and DnaT proteins (19,25). Homologues of both DnaA and PriA are found in gram-positive bacteria but another primosomal cascade involving the DnaD, DnaB, and DnaI proteins is found only in some low GϩC content grampositive bacteria, including Bacillus subtilis. Although DnaI is the gram-positive functional homologue of the Escherichia coli helicase-loader DnaC (not to be confused with the Bacillus subtilis DnaC helicase), both DnaD and DnaB have no homologues in gram-negative bacteria. They are essential for viability and required for both DnaA and PriA-mediated initiation of DNA replication (3, 27). The molecular events that...

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The Bacillus subtilis DnaD and DnaB Proteins Exhibit Different DNA Remodelling Activities

Cited by 58 publications

References 32 publications

Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis

Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis

DNA Repair and Genome Maintenance in Bacillus subtilis

TheBacillus subtilisPrimosomal Protein DnaD Untwists Supercoiled DNA

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