Control of Smc Coiled Coil Architecture by the ATPase Heads Facilitates Targeting to Chromosomal ParB/parS and Release onto Flanking DNA
Smc/ScpAB promotes chromosome segregation in prokaryotes, presumably by compacting and resolving nascent sister chromosomes. The underlying mechanisms, however, are poorly understood. Here, we investigate the role of the Smc ATPase activity in the recruitment of Smc/ScpAB to the Bacillus subtilis ch...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2016-03-01
|
Series: | Cell Reports |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124716300596 |
_version_ | 1818291305120268288 |
---|---|
author | Anita Minnen Frank Bürmann Larissa Wilhelm Anna Anchimiuk Marie-Laure Diebold-Durand Stephan Gruber |
author_facet | Anita Minnen Frank Bürmann Larissa Wilhelm Anna Anchimiuk Marie-Laure Diebold-Durand Stephan Gruber |
author_sort | Anita Minnen |
collection | DOAJ |
description | Smc/ScpAB promotes chromosome segregation in prokaryotes, presumably by compacting and resolving nascent sister chromosomes. The underlying mechanisms, however, are poorly understood. Here, we investigate the role of the Smc ATPase activity in the recruitment of Smc/ScpAB to the Bacillus subtilis chromosome. We demonstrate that targeting of Smc/ScpAB to ParB/parS loading sites is strictly dependent on engagement of Smc head domains and relies on an open organization of the Smc coiled coils. We find that dimerization of the Smc hinge domain stabilizes closed Smc rods and hinders head engagement as well as chromosomal targeting. Conversely, the ScpAB sub-complex promotes head engagement and Smc rod opening and thereby facilitates recruitment of Smc to parS sites. Upon ATP hydrolysis, Smc/ScpAB is released from loading sites and relocates within the chromosome—presumably through translocation along DNA double helices. Our findings define an intermediate state in the process of chromosome organization by Smc. |
first_indexed | 2024-12-13T02:41:57Z |
format | Article |
id | doaj.art-9164674b2e7c4c0a9c42f543fe086054 |
institution | Directory Open Access Journal |
issn | 2211-1247 |
language | English |
last_indexed | 2024-12-13T02:41:57Z |
publishDate | 2016-03-01 |
publisher | Elsevier |
record_format | Article |
series | Cell Reports |
spelling | doaj.art-9164674b2e7c4c0a9c42f543fe0860542022-12-22T00:02:17ZengElsevierCell Reports2211-12472016-03-011482003201610.1016/j.celrep.2016.01.066Control of Smc Coiled Coil Architecture by the ATPase Heads Facilitates Targeting to Chromosomal ParB/parS and Release onto Flanking DNAAnita Minnen0Frank Bürmann1Larissa Wilhelm2Anna Anchimiuk3Marie-Laure Diebold-Durand4Stephan Gruber5Research Group ‘Chromosome Organization and Dynamics’, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, GermanyResearch Group ‘Chromosome Organization and Dynamics’, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, GermanyResearch Group ‘Chromosome Organization and Dynamics’, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, GermanyResearch Group ‘Chromosome Organization and Dynamics’, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, GermanyResearch Group ‘Chromosome Organization and Dynamics’, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, GermanyResearch Group ‘Chromosome Organization and Dynamics’, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, GermanySmc/ScpAB promotes chromosome segregation in prokaryotes, presumably by compacting and resolving nascent sister chromosomes. The underlying mechanisms, however, are poorly understood. Here, we investigate the role of the Smc ATPase activity in the recruitment of Smc/ScpAB to the Bacillus subtilis chromosome. We demonstrate that targeting of Smc/ScpAB to ParB/parS loading sites is strictly dependent on engagement of Smc head domains and relies on an open organization of the Smc coiled coils. We find that dimerization of the Smc hinge domain stabilizes closed Smc rods and hinders head engagement as well as chromosomal targeting. Conversely, the ScpAB sub-complex promotes head engagement and Smc rod opening and thereby facilitates recruitment of Smc to parS sites. Upon ATP hydrolysis, Smc/ScpAB is released from loading sites and relocates within the chromosome—presumably through translocation along DNA double helices. Our findings define an intermediate state in the process of chromosome organization by Smc.http://www.sciencedirect.com/science/article/pii/S2211124716300596 |
spellingShingle | Anita Minnen Frank Bürmann Larissa Wilhelm Anna Anchimiuk Marie-Laure Diebold-Durand Stephan Gruber Control of Smc Coiled Coil Architecture by the ATPase Heads Facilitates Targeting to Chromosomal ParB/parS and Release onto Flanking DNA Cell Reports |
title | Control of Smc Coiled Coil Architecture by the ATPase Heads Facilitates Targeting to Chromosomal ParB/parS and Release onto Flanking DNA |
title_full | Control of Smc Coiled Coil Architecture by the ATPase Heads Facilitates Targeting to Chromosomal ParB/parS and Release onto Flanking DNA |
title_fullStr | Control of Smc Coiled Coil Architecture by the ATPase Heads Facilitates Targeting to Chromosomal ParB/parS and Release onto Flanking DNA |
title_full_unstemmed | Control of Smc Coiled Coil Architecture by the ATPase Heads Facilitates Targeting to Chromosomal ParB/parS and Release onto Flanking DNA |
title_short | Control of Smc Coiled Coil Architecture by the ATPase Heads Facilitates Targeting to Chromosomal ParB/parS and Release onto Flanking DNA |
title_sort | control of smc coiled coil architecture by the atpase heads facilitates targeting to chromosomal parb pars and release onto flanking dna |
url | http://www.sciencedirect.com/science/article/pii/S2211124716300596 |
work_keys_str_mv | AT anitaminnen controlofsmccoiledcoilarchitecturebytheatpaseheadsfacilitatestargetingtochromosomalparbparsandreleaseontoflankingdna AT frankburmann controlofsmccoiledcoilarchitecturebytheatpaseheadsfacilitatestargetingtochromosomalparbparsandreleaseontoflankingdna AT larissawilhelm controlofsmccoiledcoilarchitecturebytheatpaseheadsfacilitatestargetingtochromosomalparbparsandreleaseontoflankingdna AT annaanchimiuk controlofsmccoiledcoilarchitecturebytheatpaseheadsfacilitatestargetingtochromosomalparbparsandreleaseontoflankingdna AT marielaurediebolddurand controlofsmccoiledcoilarchitecturebytheatpaseheadsfacilitatestargetingtochromosomalparbparsandreleaseontoflankingdna AT stephangruber controlofsmccoiledcoilarchitecturebytheatpaseheadsfacilitatestargetingtochromosomalparbparsandreleaseontoflankingdna |