The DNA‐remodelling activity of DnaD is the sum of oligomerization and DNA‐binding activities on separate domains

Carneiro, Maria J. V. M.; Zhang, Wenke; Ioannou, Charikleia; Scott, David J.; Allen, Stephanie; Roberts, Clive J.; Soultanas, Panos

doi:10.1111/j.1365-2958.2006.05152.x

Cited by 32 publications

(98 citation statements)

References 15 publications

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“…DnaD consists of two domains with distinct activities (5). Its N-terminal domain (Nd) has a DNA-independent oligomerization activity, while its C-terminal domain (Cd) binds to DNA and exhibits a separate DNA-dependent oligomerization activity (5).…”

Section: Resultsmentioning

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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Section: Resultsmentioning

confidence: 99%

TheBacillus subtilisPrimosomal Protein DnaD Untwists Supercoiled DNA

Zhang¹,

Allen

Roberts

et al. 2006

J Bacteriol

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“…As discussed above, DnaD is involved in loading of the replicative DNA helicase at oriC and at sites of replication fork restart (73). In addition, it has been proposed that DnaD provides a general role in nucleoid organization, as it untwists DNA and has DNA remodeling activities (48). Nth has received very little attention in B. subtilis; however, it has been shown to nick substrates with AP sites (73).…”

Section: Processing Of Apurinic/apyrimidinic Sitesmentioning

confidence: 99%

“…DnaD is a scaffold protein that remodels DNA, resulting in untwisting of a plasmid substrate. In contrast, DnaB remodels DNA by compaction, and thus the two proteins have opposing effects (48,361,477). For DnaD, the N-terminal domain forms oligomers, and structural analysis has shown a winged helix domain important for dimer and tetramer formation (361).…”

Section: Primosome Assemblymentioning

confidence: 99%

“…For DnaD, the N-terminal domain forms oligomers, and structural analysis has shown a winged helix domain important for dimer and tetramer formation (361). 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).…”

Section: Primosome Assemblymentioning

confidence: 99%

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DNA Repair and Genome Maintenance in Bacillus subtilis

Lenhart

Schroeder

Walsh

et al. 2012

Microbiol Mol Biol Rev

148

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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“…1B). Binding of DDBH2 to DNA induces the formation of high-order oligomers (11). Interestingly, the cyanobacterial Ftn6 protein, which functions in the recruitment of FtsZ and regulates assembly of the Z ring during cell division, has a 77-amino-acid N-terminal domain structurally homologous to DDBH2 (35).…”

Section: Modular Architecture Of the Dnad And Dnab Proteinsmentioning

confidence: 99%

Chromosomal Replication Initiation Machinery of Low-G+C-Content Firmicutes

2012

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bMuch of our knowledge of the initiation of DNA replication comes from studies in the Gram-negative model organism Escherichia coli. However, the location and structure of the origin of replication within the E. coli genome and the identification and study of the proteins which constitute the E. coli initiation complex suggest that it might not be as universal as once thought. The archetypal low-G؉C-content Gram-positive Firmicutes initiate DNA replication via a unique primosomal machinery, quite distinct from that seen in E. coli, and an examination of oriC in the Firmicutes species Bacillus subtilis indicates that it might provide a better model for the ancestral bacterial origin of replication. Therefore, the study of replication initiation in organisms other than E. coli, such as B. subtilis, will greatly advance our knowledge and understanding of these processes as a whole. In this minireview, we highlight the structure-function relationships of the Firmicutes primosomal proteins, discuss the significance of their oriC architecture, and present a model for replication initiation at oriC. The Firmicutes are Gram-positive bacteria encompassing three major classes, Bacilli, Clostridia, and Mollicutes. They have a relatively low GϩC content in their genomes and are morphologically and physiologically diverse. Rod-shaped bacilli, spherical cocci, and aerobic, anaerobic spore-forming, and non-sporeforming bacteria are found in this group. They likely represent the most ancestral phylum of prokaryotes, with high-GϩC-content Gram-positive and Gram-negative bacteria having diverged from the Firmicutes at a later stage in evolution (13,70). Bacillus subtilis is the best studied of the Firmicutes and is widely considered the Gram-positive model bacterium, but other bacilli, streptococci, staphylococci, and clostridia have been extensively studied because of their medical and industrial importance.In addition to the universally conserved replication initiation protein DnaA (32, 65) and the replication restart protein PriA (17, 39), the low-GϩC-content Firmicutes generally have two unique essential genes, dnaD and dnaB, coding for the replication initiation proteins DnaD and DnaB, respectively ( Table 1) (note that DnaB in B. subtilis is unrelated to DnaB in Escherichia coli). In some cases-for example, in several Mollicutes-there are no distinct dnaD and dnaB genes, but there is, instead, a single gene annotated as dnaD-like which may combine both functions. No homologous proteins are found outside the Firmicutes, suggesting a replication initiation machinery distinctly different from those of other bacteria (31). In addition, there are a number of regulatory proteins which are not found in the Gram-negative model organism Escherichia coli, including YabA, Soj, SirA, and Spo0A, while other regulatory proteins are found in E. coli but not B. subtilis (these regulatory proteins have been subject to a recent review [29]). DnaA, DnaD, and DnaB, together with the helicase loader DnaI (called DnaC in E. coli), the replicativ...

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The DNA‐remodelling activity of DnaD is the sum of oligomerization and DNA‐binding activities on separate domains

Cited by 32 publications

References 15 publications

TheBacillus subtilisPrimosomal Protein DnaD Untwists Supercoiled DNA

TheBacillus subtilisPrimosomal Protein DnaD Untwists Supercoiled DNA

DNA Repair and Genome Maintenance in Bacillus subtilis

Chromosomal Replication Initiation Machinery of Low-G+C-Content Firmicutes

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