MatP regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation

Nolivos, Sophie; Upton, Amy L.; Badrinarayanan, Anjana; Müller, Julius; Zawadzka, Katarzyna; Wiktor, Jakub; Gill, Amber; Arciszewska, Lidia K.; Nicolas, Emilien; Sherratt, David J.

doi:10.1038/ncomms10466

Cited by 128 publications

(255 citation statements)

References 56 publications

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“…6). Such a process is reminiscent with what has been observed for other bacterial SMC proteins, such as MukB and SMC ( B. subtilis or C. crescentus ) that are respectively loaded by MatP45 and ParB46474849. The mechanism by which RecN promotes cohesion is not yet understood.…”

Section: Discussionmentioning

confidence: 84%

Management of E. coli sister chromatid cohesion in response to genotoxic stress

et al. 2017

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Aberrant DNA replication is a major source of the mutations and chromosomal rearrangements associated with pathological disorders. In bacteria, several different DNA lesions are repaired by homologous recombination, a process that involves sister chromatid pairing. Previous work in Escherichia coli has demonstrated that sister chromatid interactions (SCIs) mediated by topological links termed precatenanes, are controlled by topoisomerase IV. In the present work, we demonstrate that during the repair of mitomycin C-induced lesions, topological links are rapidly substituted by an SOS-induced sister chromatid cohesion process involving the RecN protein. The loss of SCIs and viability defects observed in the absence of RecN were compensated by alterations in topoisomerase IV, suggesting that the main role of RecN during DNA repair is to promote contacts between sister chromatids. RecN also modulates whole chromosome organization and RecA dynamics suggesting that SCIs significantly contribute to the repair of DNA double-strand breaks (DSBs).

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Section: Discussionmentioning

confidence: 84%

Management of E. coli sister chromatid cohesion in response to genotoxic stress

et al. 2017

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“…Nevertheless, in B. subtilis, and other studied bacteria that have canonical SMC complexes, the two chromosome arms are colinear along the cell long axis, contrasting with the situation in E. coli, and perhaps other MukBEF-MatPcontaining bacteria (26). The MukBEF interaction with the decatenase, TopoIV, means that the patterns of MukBEF association with chromosomes is mimicked by those of TopoIV, with its action being enriched close to oriC and depleted from ter, with coupling between the activities of both enzymes possible (8). We conclude that chromosome-associated MukBEF complexes are the template and 'machine' for formation of DNA loops in chromosomes, and their characterization adds weight to the hypothesis that lengthwise compaction by intrachromosome loop formation is the mechanism by which all SMC complexes organize and individualize chromosomes.…”

mentioning

confidence: 85%

“…The JM56 strain (mukB-haloTag, ΔmukE) was constructed by removing the kan resistance gene from JM41 using Flp recombinase and replacing the endogenous mukE gene with a kanamycin cassette using λ-red recombination. All genetic modifications were verified by PCR, the Muk +/phenotype was verified by temperature-resistance or lack of it in rich media, and behavior in quantitative imaging, as described (8).…”

Section: Bacterial Strains and Growthmentioning

confidence: 99%

The SMC complex, MukBEF, organizes theEscherichia colichromosome by forming an axial core

Mäkelä

Sherratt

2019

Preprint

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AbstractStructural Maintenance of Chromosomes (SMC) complexes organize and individualize chromosomes ubiquitously, thereby contributing to their faithful segregation. Here we explore how Escherichia coli chromosome organization emerges from the action of the SMC complex MukBEF, using quantitative imaging in cells with increased MukBEF occupancy on the chromosome. We demonstrate that the E. coli chromosome is organized as series of loops around a thin axial MukBEF core whose length is ~1100 times shorter than the chromosomal DNA. The core is linear (1 μm), or circular (1.5 μm) in the absence of MatP, which displaces MukBEF from the 800 kbp replication termination region (ter). Our findings illustrate how MukBEF compacts the chromosome lengthwise and demonstrate how displacement of MukBEF from ter promotes MukBEF enrichment with the replication origin.

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“…3 (Nicolas et al, 2014;Zawadzki et al, 2015), with MatP-matS regulating the distribution and activity of both MukBEF and TopoIV in cells (Nolivos et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…Clusters of wild-type MukBEF complexes are positioned at mid-cell in new born cells and the cell quarter positions thereafter by a 'phase-locked Turing pattern' (Murray and Sourjik, 2017). These clusters position the chromosome replication origin region (ori) (Danilova et al, 2007;Nolivos et al, 2016;Hoffman et al, 2018), thereby facilitating chromosome organisation and segregation. ATP binding and MukB head engagement are essential for the formation of MukBEF clusters, as they are present in wild type and in hydrolysis-deficient mutants (MukB EQ ) cells, but not in cells impaired in nucleotide binding or in head engagement (Badrinarayanan et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Dynamic architecture of the Escherichia coli Structural Maintenance of Chromosomes (SMC) complex, MukBEF

Arciszewska

Rajasekar

Tang

et al. 2019

Preprint

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Structural Maintenance of Chromosomes (SMC) complexes use a proteinaceous ring-shaped architecture to organise chromosomes, thereby facilitating chromosome segregation. They utilise cycles of ATP binding and hydrolysis to transport themselves rapidly with respect to DNA, a process requiring protein conformational changes and multiple DNA contacts. We have analysed changes in the architecture of the Escherichia coli SMC complex, MukBEF, as a function of nucleotide binding to MukB and subsequent ATP hydrolysis. This builds upon previous work showing that MukF kleisin directs formation of a MukBEF tripartite ring as a consequence of functional interactions between the C-and N-terminal domains of MukF with the MukB head and neck, respectively (Zawadzka et al., 2018). Using both model truncated substrates and complexesAlthough the Escherichia coli SMC complex, MukBEF, shares many aspects of the distinctive SMC complex architecture, its kleisin, MukF, is dimeric, which could potentially facilitate the formation and action of higher order complexes (Fennell-Fezzie et al., 2005; Badrinaryananan et al., 2012;Nolivos and Sherratt, 2014). MukBEF homologs are only found in a fraction of γproteobacteria, where they have co-evolved with a group of other proteins, including MatP, Dam and SeqA (Brézellec et al., 2006). MukBEF also coordinates the localization and action of TopoIV

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MatP regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation

Cited by 128 publications

References 56 publications

Management of E. coli sister chromatid cohesion in response to genotoxic stress

Management of E. coli sister chromatid cohesion in response to genotoxic stress

The SMC complex, MukBEF, organizes theEscherichia colichromosome by forming an axial core

Dynamic architecture of the Escherichia coli Structural Maintenance of Chromosomes (SMC) complex, MukBEF

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