Are SMC Complexes Loop Extruding Factors? Linking Theory With Fact

Baxter, Jonathan; Oliver, Antony W.; Schalbetter, Stephanie A.

doi:10.1002/bies.201800182

Cited by 13 publications

(10 citation statements)

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“…As the KITE subunits are stable components of the SMC complexes, we assume that the openings of the kleisin-νSMC interfaces are intrinsically coupled to their ATP cycles. It was proposed for the SMC/ScpAB complex that the opening of the kleisin-νSMC interface might be a part of its ATPase cycle generating loops along DNA strands [52, 53]. The SMC5/6 data are also consistent with the above notions as the ATPase activity of the SMC5/6 complex is needed for its topological binding [36].…”

Section: Discussionsupporting

confidence: 52%

A role of the Nse4 kleisin and Nse1/Nse3 KITE subunits in the ATPase cycle of SMC5/6

Vondrová

Adamus

Nociar

et al. 2019

Preprint

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1 0 1 1 Keywords: SMC5/6 complex; Nse4 klesin linker; Nse1/Nse3 KITE subunits; ATP binding; 1 2 protein-protein interaction, fission yeast 1 3 1 4 2 ABSTRACT 1 5 The SMC (Structural Maintenance of Chromosomes) complexes are composed of 1 6 SMC dimers, kleisin and kleisin-interacting subunits. Mutual interactions of these subunits 1 7 constitute the basal architecture of the SMC complexes. Particularly, terminal domains of the 1 8 kleisin subunit bridge the SMC head domains of the SMC molecules. Binding of ATP 1 9molecules to the heads and their hydrolysis alter the shape of long SMC molecules (from rod-2 0 3 1 upon ATP binding. This mechanism suggests an important role of the KITE subunits in the 3 2 dynamics of the SMC5/6 complexes. 3 3 3 4 AUTHOR SUMMARY 3 5The SMC5/6 complex is member of the Structural maintenance of chromosomes 3 6 (SMC) family, key organizers of both prokaryotic and eukaryotic genomes. Their architecture 3 7 and dynamics (driven by ATP binding and hydrolysis) are essential for cellular processes, like 3 8 3 chromatin segregation, condensation, replication and repair. In this paper, we described 3 9 conserved mode of the Nse4 kleisin subunit binding to the SMC6 (similar to cohesin and 4 0 condensin) and its bridging role. Furthermore, we showed different impact of the binding of 4 1 the Nse1-Nse3 KITE subunits to the Nse4 kleisin bridge. Our study suggested that the KITE 4 2 proteins modulate the stability of the SMC5/6 complex, depending on its binding and 4 3 hydrolysis of ATP. Our findings uncover molecular mechanisms underlying dynamics of the 4 4 SMC5/6 complexes.4 5 4 6 INTRODUCTION 4 7 The SMC (Structural Maintenance of Chromosomes) complexes are key organizers of 4 8 prokaryotic and eukaryotic genomes. They organize chromatin domains (cohesins; [1]), 4 9 condense mitotic chromosomes (condensins; [2]), assist in DNA repair (SMC5/6; [3, 4]) and 5 0 replication (SMC/ScpAB; [5]). These circular complexes use the energy of ATP hydrolysis to 5 1 drive DNA topology changes. In prokaryotes, SMC/ScpAB drives extrusion of loops forming 5 2 behind the replication fork. In eukaryotes, condensins extrude loops laterally and axially to 5 3 shape chromatin to the typical mitotic chromosomes. Cohesins assist in formation of 5 4 topologically associating domains during interphase. Cohesin rings can also hold newly 5 5 replicated sister chromatids together and release them in highly controlled manner. The 5 6 SMC5/6 complexes have been implicated in the repair of DNA damage by homologous 5 7 recombination, stabilization and restart of stressed replication forks. The SMC5/6 instability 5 8 leads to the chromosome breakage syndrome in human [6], however, the molecular 5 9mechanism of the SMC5/6 action is largely unclear. 6 0 All the SMC complexes are composed of three common categories of subunits: SMC, 6 1 kleisin and kleisin-interacting proteins [7, 8]. The SMC proteins are primarily build of long 6 2 anti-parallel coiled-coil arms, a globular hinge (situated in the middle of their peptide chain) 6 3 4...

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Section: Discussionsupporting

confidence: 52%

A role of the Nse4 kleisin and Nse1/Nse3 KITE subunits in the ATPase cycle of SMC5/6

Vondrová

Adamus

Nociar

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…coli chromosome? According to the current view, SMC complexes organize chromosomes by extruding DNA loops [148]. SMC complexes translocate along DNA to extrude loops in a cis-manner (on the same DNA molecule), wherein the size of loops depends on the processivity of the complex.…”

Section: Introductionmentioning

confidence: 99%

“…SMC complexes translocate along DNA to extrude loops in a cis-manner (on the same DNA molecule), wherein the size of loops depends on the processivity of the complex. SMC complexes from different organisms differ in the mechanism of loop extrusion [148]. Single molecule fluorescence microscopy of MukBEF in E .…”

Section: Introductionmentioning

confidence: 99%

Architecture of the Escherichia coli nucleoid

2019

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How genomes are organized within cells and how the 3D architecture of a genome influences cellular functions are significant questions in biology. A bacterial genomic DNA resides inside cells in a highly condensed and functionally organized form called nucleoid (nucleus-like structure without a nuclear membrane). The Escherichia coli chromosome or nucleoid is composed of the genomic DNA, RNA, and protein. The nucleoid forms by condensation and functional arrangement of a single chromosomal DNA with the help of chromosomal architectural proteins and RNA molecules as well as DNA supercoiling. Although a high-resolution structure of a bacterial nucleoid is yet to come, five decades of research has established the following salient features of the E. coli nucleoid elaborated below: 1) The chromosomal DNA is on the average a negatively supercoiled molecule that is folded as plectonemic loops, which are confined into many independent topological domains due to supercoiling diffusion barriers; 2) The loops spatially organize into megabase size regions called macrodomains, which are defined by more frequent physical interactions among DNA sites within the same macrodomain than between different macrodomains; 3) The condensed and spatially organized DNA takes the form of a helical ellipsoid radially confined in the cell; and 4) The DNA in the chromosome appears to have a condition-dependent 3-D structure that is linked to gene expression so that the nucleoid architecture and gene transcription are tightly interdependent, influencing each other reciprocally. Current advents of high-resolution microscopy, single-molecule analysis and molecular structure determination of the components are expected to reveal the total structure and function of the bacterial nucleoid.

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“…Large, rod-shaped, coiled-coil SMC proteins form dimers due to interactions within the hinge region and ATP-binding head domains. ATP hydrolysis and DNA binding induce conformational changes in the dimer that allow DNA loop extrusion, providing the basis for DNA compaction (Nolivos and Sherratt, 2014;Ganji et al, 2018;Baxter et al, 2019;Marko et al, 2019). Since binding and ATP hydrolysis are crucial for condensin activity, the efficiency of chromosome compaction induced by SMC proteins is presumably dependent on ATP levels in the cell.…”

Section: The Additional Roles Of Parab Proteinsmentioning

confidence: 99%

Chromosome Segregation Proteins as Coordinators of Cell Cycle in Response to Environmental Conditions

Pióro

Jakimowicz

2020

Front. Microbiol.

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Chromosome segregation is a crucial stage of the cell cycle. In general, proteins involved in this process are DNA-binding proteins, and in most bacteria, ParA and ParB are the main players; however, some bacteria manage this process by employing other proteins, such as condensins. The dynamic interaction between ParA and ParB drives movement and exerts positioning of the chromosomal origin of replication (oriC) within the cell. In addition, both ParA and ParB were shown to interact with the other proteins, including those involved in cell division or cell elongation. The significance of these interactions for the progression of the cell cycle is currently under investigation. Remarkably, DNA binding by ParA and ParB as well as their interactions with protein partners conceivably may be modulated by intra-and extracellular conditions. This notion provokes the question of whether chromosome segregation can be regarded as a regulatory stage of the cell cycle. To address this question, we discuss how environmental conditions affect chromosome segregation and how segregation proteins influence other cell cycle processes.

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Are SMC Complexes Loop Extruding Factors? Linking Theory With Fact

Cited by 13 publications

References 104 publications

A role of the Nse4 kleisin and Nse1/Nse3 KITE subunits in the ATPase cycle of SMC5/6

A role of the Nse4 kleisin and Nse1/Nse3 KITE subunits in the ATPase cycle of SMC5/6

Architecture of the Escherichia coli nucleoid

Chromosome Segregation Proteins as Coordinators of Cell Cycle in Response to Environmental Conditions

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