Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle
Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome‐...
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| Published in | The EMBO journal Vol. 36; no. 18; pp. 2684 - 2697 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
15.09.2017
EMBO Press John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome‐wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher‐order organization of the
Saccharomyces cerevisiae
genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long‐range intra‐chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin‐dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin‐mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle‐dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division.
Synopsis
Hi‐C analysis at 15 distinct stages provides a comprehensive map of chromosome dynamics throughout the budding yeast cell cycle. This illustrates how SMC complexes control chromosome looping and suggests that condensin contributes to chromosome segregation during anaphase.
Genome‐wide Hi‐C contact maps provide a comprehensive overview of genome reorganization throughout the cell cycle.
Three different chromosome folding states, basic (G1), condensed (metaphase) and extended (anaphase), alternate during the cycle.
Altered contacts upon microtubule destabilization imply microtubule‐induced stretching in anaphase.
Formation of a condensin‐dependent intra‐chromosomal loop during anaphase bridges rDNA with the centromere, possibly through a loop extrusion mechanism.
Graphical Abstract
Hi‐C analysis at 15 distinct synchronization stages provides a comprehensive map of chromosome dynamics throughout the budding yeast cell cycle, and illustrates how SMC complexes control chromosome looping. |
|---|---|
| AbstractList | Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (
SMC
) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome‐wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher‐order organization of the
Saccharomyces cerevisiae
genome throughout the cell cycle and investigate the roles of
SMC
complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long‐range intra‐chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin‐dependent loop bridging the centromere cluster with the
rDNA
loci suggests that condensin‐mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle‐dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division.
image
Hi‐C analysis at 15 distinct stages provides a comprehensive map of chromosome dynamics throughout the budding yeast cell cycle. This illustrates how
SMC
complexes control chromosome looping and suggests that condensin contributes to chromosome segregation during anaphase.
Genome‐wide Hi‐C contact maps provide a comprehensive overview of genome reorganization throughout the cell cycle.
Three different chromosome folding states, basic (G1), condensed (metaphase) and extended (anaphase), alternate during the cycle.
Altered contacts upon microtubule destabilization imply microtubule‐induced stretching in anaphase.
Formation of a condensin‐dependent intra‐chromosomal loop during anaphase bridges rDNA with the centromere, possibly through a loop extrusion mechanism. Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome-wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher-order organization of the Saccharomyces cerevisiae genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long-range intra-chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin-dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin-mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle-dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division. Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome‐wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher‐order organization of the Saccharomyces cerevisiae genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long‐range intra‐chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin‐dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin‐mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle‐dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division. Synopsis Hi‐C analysis at 15 distinct stages provides a comprehensive map of chromosome dynamics throughout the budding yeast cell cycle. This illustrates how SMC complexes control chromosome looping and suggests that condensin contributes to chromosome segregation during anaphase. Genome‐wide Hi‐C contact maps provide a comprehensive overview of genome reorganization throughout the cell cycle. Three different chromosome folding states, basic (G1), condensed (metaphase) and extended (anaphase), alternate during the cycle. Altered contacts upon microtubule destabilization imply microtubule‐induced stretching in anaphase. Formation of a condensin‐dependent intra‐chromosomal loop during anaphase bridges rDNA with the centromere, possibly through a loop extrusion mechanism. Graphical Abstract Hi‐C analysis at 15 distinct synchronization stages provides a comprehensive map of chromosome dynamics throughout the budding yeast cell cycle, and illustrates how SMC complexes control chromosome looping. Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes ( SMC ) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome‐wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher‐order organization of the Saccharomyces cerevisiae genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long‐range intra‐chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin‐dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin‐mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle‐dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division. Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome-wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher-order organization of the Saccharomyces cerevisiae genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long-range intra-chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin-dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin-mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle-dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division.Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome-wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher-order organization of the Saccharomyces cerevisiae genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long-range intra-chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin-dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin-mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle-dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division. Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome‐wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher‐order organization of the Saccharomyces cerevisiae genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long‐range intra‐chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin‐dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin‐mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle‐dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division. Synopsis Hi‐C analysis at 15 distinct stages provides a comprehensive map of chromosome dynamics throughout the budding yeast cell cycle. This illustrates how SMC complexes control chromosome looping and suggests that condensin contributes to chromosome segregation during anaphase. Genome‐wide Hi‐C contact maps provide a comprehensive overview of genome reorganization throughout the cell cycle. Three different chromosome folding states, basic (G1), condensed (metaphase) and extended (anaphase), alternate during the cycle. Altered contacts upon microtubule destabilization imply microtubule‐induced stretching in anaphase. Formation of a condensin‐dependent intra‐chromosomal loop during anaphase bridges rDNA with the centromere, possibly through a loop extrusion mechanism. Hi‐C analysis at 15 distinct synchronization stages provides a comprehensive map of chromosome dynamics throughout the budding yeast cell cycle, and illustrates how SMC complexes control chromosome looping. Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome-wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher-order organization of the genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long-range intra-chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin-dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin-mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle-dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division. |
| Author | Lazar‐Stefanita, Luciana Mercy, Guillaume Mozziconacci, Julien Guérin, Thomas M Thierry, Agnès Muller, Héloise Koszul, Romain Scolari, Vittore F |
| AuthorAffiliation | 3 Institut Pasteur CNRS Center of Bioinformatics, Biostatistics and Integrative Biology (C3BI) USR 3756 Paris France 1 Institut Pasteur Department Genomes and Genetics Unité Régulation Spatiale des Génomes Paris France 6 Sorbonne Universités Theoretical Physics for Condensed Matter Lab UPMC Université Paris 06 Paris France 4 Sorbonne Universités UPMC Université Paris 6 Complexité du Vivant Paris France 2 CNRS UMR 3525 Paris France 5 Laboratoire Télomères et Réparation du Chromosome CEA INSERM UMR 967 IRCM Université Paris‐Saclay Fontenay‐aux‐Roses France 7 CNRS UMR 7600 Paris France |
| AuthorAffiliation_xml | – name: 6 Sorbonne Universités Theoretical Physics for Condensed Matter Lab UPMC Université Paris 06 Paris France – name: 2 CNRS UMR 3525 Paris France – name: 5 Laboratoire Télomères et Réparation du Chromosome CEA INSERM UMR 967 IRCM Université Paris‐Saclay Fontenay‐aux‐Roses France – name: 1 Institut Pasteur Department Genomes and Genetics Unité Régulation Spatiale des Génomes Paris France – name: 3 Institut Pasteur CNRS Center of Bioinformatics, Biostatistics and Integrative Biology (C3BI) USR 3756 Paris France – name: 7 CNRS UMR 7600 Paris France – name: 4 Sorbonne Universités UPMC Université Paris 6 Complexité du Vivant Paris France |
| Author_xml | – sequence: 1 givenname: Luciana surname: Lazar‐Stefanita fullname: Lazar‐Stefanita, Luciana organization: Institut Pasteur, Department Genomes and Genetics, Unité Régulation Spatiale des Génomes, CNRS, UMR 3525, Institut Pasteur, CNRS, Center of Bioinformatics, Biostatistics and Integrative Biology (C3BI), Sorbonne Universités, UPMC Université Paris 6, Complexité du Vivant – sequence: 2 givenname: Vittore F surname: Scolari fullname: Scolari, Vittore F organization: Institut Pasteur, Department Genomes and Genetics, Unité Régulation Spatiale des Génomes, CNRS, UMR 3525, Institut Pasteur, CNRS, Center of Bioinformatics, Biostatistics and Integrative Biology (C3BI) – sequence: 3 givenname: Guillaume surname: Mercy fullname: Mercy, Guillaume organization: Institut Pasteur, Department Genomes and Genetics, Unité Régulation Spatiale des Génomes, CNRS, UMR 3525, Institut Pasteur, CNRS, Center of Bioinformatics, Biostatistics and Integrative Biology (C3BI), Sorbonne Universités, UPMC Université Paris 6, Complexité du Vivant – sequence: 4 givenname: Héloise surname: Muller fullname: Muller, Héloise organization: Institut Pasteur, Department Genomes and Genetics, Unité Régulation Spatiale des Génomes, CNRS, UMR 3525, Institut Pasteur, CNRS, Center of Bioinformatics, Biostatistics and Integrative Biology (C3BI) – sequence: 5 givenname: Thomas M surname: Guérin fullname: Guérin, Thomas M organization: Laboratoire Télomères et Réparation du Chromosome, CEA, INSERM, UMR 967, IRCM, Université Paris‐Saclay – sequence: 6 givenname: Agnès surname: Thierry fullname: Thierry, Agnès organization: Institut Pasteur, Department Genomes and Genetics, Unité Régulation Spatiale des Génomes, CNRS, UMR 3525, Institut Pasteur, CNRS, Center of Bioinformatics, Biostatistics and Integrative Biology (C3BI) – sequence: 7 givenname: Julien orcidid: 0000-0001-5652-0302 surname: Mozziconacci fullname: Mozziconacci, Julien email: mozziconacci@lptmc.jussieu.fr organization: Sorbonne Universités, Theoretical Physics for Condensed Matter Lab, UPMC Université Paris 06, CNRS, UMR 7600 – sequence: 8 givenname: Romain orcidid: 0000-0002-3086-1173 surname: Koszul fullname: Koszul, Romain email: romain.koszul@pasteur.fr organization: Institut Pasteur, Department Genomes and Genetics, Unité Régulation Spatiale des Génomes, CNRS, UMR 3525, Institut Pasteur, CNRS, Center of Bioinformatics, Biostatistics and Integrative Biology (C3BI) |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28729434$$D View this record in MEDLINE/PubMed https://hal.sorbonne-universite.fr/hal-01596511$$DView record in HAL |
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| Issue | 18 |
| Keywords | SMC Hi‐C chromosome segregation replication profile loop extrusion Chromatin Repair & Recombination Hi-C SMC Subject Categories Cell Cycle Epigenetics Genomics & Functional Genomics DNA Replication |
| Language | English |
| License | Attribution 2017 The Authors. Published under the terms of the CC BY 4.0 license. Attribution: http://creativecommons.org/licenses/by This is an open access article under the terms of the Creative Commons Attribution 4.0 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| Title | Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle |
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