Thermotoga maritima oriC involves a DNA unwinding element with distinct modules and a DnaA-oligomerizing region with a novel directional binding mode

Lu, Cheng‐Hsun; Yoshida, Ryusei; Katayama, Tsutomu; Ozaki, Shogo

doi:10.1016/j.jbc.2023.104888

Cited by 2 publications

(3 citation statements)

References 57 publications

(134 reference statements)

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“…Thus, these features support the idea that the ssDUE recruitment mechanism is conserved among diverse bacterial species. Consistently, DnaA-ssDUE interactions have been implicated in other bacterial species including Thermotoga maritima, Bacillus subtilis, and Helicobacter pylori [55][56][57][58]. In B. subtilis, the HU homologue HBsu is essential for in vivo replication initiation from oriC, and E. coli HU stimulates the in vitro DUE unwinding of B. subtilis oriC [59,60].…”

Section: Initiation Complex At Oricmentioning

confidence: 79%

IHF and Fis as Escherichia coli Cell Cycle Regulators: Activation of the Replication Origin oriC and the Regulatory Cycle of the DnaA Initiator

Kasho

Ozaki

Katayama

2023

IJMS

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This review summarizes current knowledge about the mechanisms of timely binding and dissociation of two nucleoid proteins, IHF and Fis, which play fundamental roles in the initiation of chromosomal DNA replication in Escherichia coli. Replication is initiated from a unique replication origin called oriC and is tightly regulated so that it occurs only once per cell cycle. The timing of replication initiation at oriC is rigidly controlled by the timely binding of the initiator protein DnaA and IHF to oriC. The first part of this review presents up-to-date knowledge about the timely stabilization of oriC-IHF binding at oriC during replication initiation. Recent advances in our understanding of the genome-wide profile of cell cycle-coordinated IHF binding have revealed the oriC-specific stabilization of IHF binding by ATP-DnaA oligomers at oriC and by an initiation-specific IHF binding consensus sequence at oriC. The second part of this review summarizes the mechanism of the timely regulation of DnaA activity via the chromosomal loci DARS2 (DnaA-reactivating sequence 2) and datA. The timing of replication initiation at oriC is controlled predominantly by the phosphorylated form of the adenosine nucleotide bound to DnaA, i.e., ATP-DnaA, but not ADP-ADP, is competent for initiation. Before initiation, DARS2 increases the level of ATP-DnaA by stimulating the exchange of ADP for ATP on DnaA. This DARS2 function is activated by the site-specific and timely binding of both IHF and Fis within DARS2. After initiation, another chromosomal locus, datA, which inactivates ATP-DnaA by stimulating ATP hydrolysis, is activated by the timely binding of IHF. A recent study has shown that ATP-DnaA oligomers formed at DARS2-Fis binding sites competitively dissociate Fis via negative feedback, whereas IHF regulation at DARS2 and datA still remains to be investigated. This review summarizes the current knowledge about the specific role of IHF and Fis in the regulation of replication initiation and proposes a mechanism for the regulation of timely IHF binding and dissociation at DARS2 and datA.

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Section: Initiation Complex At Oricmentioning

confidence: 79%

IHF and Fis as Escherichia coli Cell Cycle Regulators: Activation of the Replication Origin oriC and the Regulatory Cycle of the DnaA Initiator

Kasho

Ozaki

Katayama

2023

IJMS

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“…That next can facilitate HU binding between these DnaA-boxes since HU has a higher affinity to bend DNA (Bonnefoy and Rouviere-Yaniv, 1991;Kamashev et al, 2017;Yoshida et al, 2023). The HU binding between two DnaA-boxes occupied by DnaA was also shown for T. maritima origin and the sequence analysis of bacterial origins often revealed the required distance (Koh et al, 2011) between the first and second DnaA-box adjacent to DUE for HU-induced sharp DNA bending (Lu et al, 2023;Yoshida et al, 2023). Although most of the research concerning looping of the DNA as a mechanism of origin opening is based on experiments with DnaA, there are also studies showing that other DNA replication initiators may follow the loop-back mechanism (Chatterjee et al, 2020;Wegrzyn et al, 2023).…”

Section: Loop-back Modelmentioning

confidence: 85%

“…To support the cooperativity of binding, the interaction of domains I might occur (Katayama et al, 2017). Despite differences in motif organization within the origin of T. maritima (see Section 2), a similar model of binding and origin opening is proposed for this bacterium (Lu et al, 2023). Because the "loop-back model" assumes the definite bending of DNA, the assistance of nucleoid-associated proteins (NAPs) is proposed.…”

Section: Loop-back Modelmentioning

confidence: 99%

Toward an understanding of the DNA replication initiation in bacteria

Wegrzyn,

Konieczny

2024

Front. Microbiol.

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Although the mechanism of DNA replication initiation has been investigated for over 50 years, many important discoveries have been made related to this process in recent years. In this mini-review, we discuss the current state of knowledge concerning the structure of the origin region in bacterial chromosomes and plasmids, recently discovered motifs recognized by replication initiator proteins, and proposed in the literature models describing initial origin opening. We review structures of nucleoprotein complexes formed by replication initiators at chromosomal and plasmid replication origins and discuss their functional implications. We also discuss future research challenges in this field.

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Thermotoga maritima oriC involves a DNA unwinding element with distinct modules and a DnaA-oligomerizing region with a novel directional binding mode

Cited by 2 publications

References 57 publications

IHF and Fis as Escherichia coli Cell Cycle Regulators: Activation of the Replication Origin oriC and the Regulatory Cycle of the DnaA Initiator

IHF and Fis as Escherichia coli Cell Cycle Regulators: Activation of the Replication Origin oriC and the Regulatory Cycle of the DnaA Initiator

Toward an understanding of the DNA replication initiation in bacteria

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