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Quantitative imaging of loop extruders rebuilding interphase genome architecture after mitosis

Quantitative imaging of loop extruders rebuilding interphase genome architecture after mitosis
Quantitative imaging of loop extruders rebuilding interphase genome architecture after mitosis

How cells establish the interphase genome organization after mitosis is incompletely understood. Using quantitative and super-resolution microscopy, we show that the transition from a Condensin to a Cohesin-based genome organization occurs dynamically over 2 h. While a significant fraction of Condensins remains chromatin-bound until early G1, Cohesin-STAG1 and its boundary factor CTCF are rapidly imported into daughter nuclei in telophase, immediately bind chromosomes as individual complexes, and are sufficient to build the first interphase TAD structures. By contrast, the more abundant Cohesin-STAG2 accumulates on chromosomes only gradually later in G1, is responsible for compaction inside TAD structures, and forms paired complexes upon completed nuclear import. Our quantitative time-resolved mapping of mitotic and interphase loop extruders in single cells reveals that the nested loop architecture formed by the sequential action of two Condensins in mitosis is seamlessly replaced by a less compact but conceptually similar hierarchically nested loop architecture driven by the sequential action of two Cohesins.

Active Transport, Cell Nucleus, Cohesins/chemistry, DNA-Binding Proteins/chemistry, Genome, HeLa Cells, Humans, Interphase, Mitosis, Nuclear Proteins/metabolism, Polymerization, Single-Cell Analysis
1540-8140
Brunner, Andreas
0d6b87b9-3a36-4198-84bf-e2e4bfc39c03
Morero, Natalia Rosalía
b0efbc0e-75cc-4874-bdf8-a61c895d032e
Zhang, Wanlu
93ba36d4-5605-4f27-9597-c41e60bd7d0b
Hossain, M Julius
bba1b875-7604-462b-a55b-ba0b54f728e8
Lampe, Marko
153782a8-0146-44c2-b9a3-fe5afd331044
Pflaumer, Hannah
092f5e10-ca56-471b-bcd4-0198a689565d
Halavatyi, Aliaksandr
24503a0a-e391-48ac-b0d4-665c3d138a30
Peters, Jan-Michael
1d7ca60e-1ff8-49d7-a08b-edcd62e9ed18
Beckwith, Kai S
fe9ca6b0-3838-46fa-8730-9a9fd7ada80e
Ellenberg, Jan
7b8ab9a9-8076-4db1-b7a2-8445accc9b54
Brunner, Andreas
0d6b87b9-3a36-4198-84bf-e2e4bfc39c03
Morero, Natalia Rosalía
b0efbc0e-75cc-4874-bdf8-a61c895d032e
Zhang, Wanlu
93ba36d4-5605-4f27-9597-c41e60bd7d0b
Hossain, M Julius
bba1b875-7604-462b-a55b-ba0b54f728e8
Lampe, Marko
153782a8-0146-44c2-b9a3-fe5afd331044
Pflaumer, Hannah
092f5e10-ca56-471b-bcd4-0198a689565d
Halavatyi, Aliaksandr
24503a0a-e391-48ac-b0d4-665c3d138a30
Peters, Jan-Michael
1d7ca60e-1ff8-49d7-a08b-edcd62e9ed18
Beckwith, Kai S
fe9ca6b0-3838-46fa-8730-9a9fd7ada80e
Ellenberg, Jan
7b8ab9a9-8076-4db1-b7a2-8445accc9b54

Brunner, Andreas, Morero, Natalia Rosalía, Zhang, Wanlu, Hossain, M Julius, Lampe, Marko, Pflaumer, Hannah, Halavatyi, Aliaksandr, Peters, Jan-Michael, Beckwith, Kai S and Ellenberg, Jan (2025) Quantitative imaging of loop extruders rebuilding interphase genome architecture after mitosis. Journal of Cell Biology, 224 (3). (doi:10.1083/jcb.202405169).

Record type: Article

Abstract

How cells establish the interphase genome organization after mitosis is incompletely understood. Using quantitative and super-resolution microscopy, we show that the transition from a Condensin to a Cohesin-based genome organization occurs dynamically over 2 h. While a significant fraction of Condensins remains chromatin-bound until early G1, Cohesin-STAG1 and its boundary factor CTCF are rapidly imported into daughter nuclei in telophase, immediately bind chromosomes as individual complexes, and are sufficient to build the first interphase TAD structures. By contrast, the more abundant Cohesin-STAG2 accumulates on chromosomes only gradually later in G1, is responsible for compaction inside TAD structures, and forms paired complexes upon completed nuclear import. Our quantitative time-resolved mapping of mitotic and interphase loop extruders in single cells reveals that the nested loop architecture formed by the sequential action of two Condensins in mitosis is seamlessly replaced by a less compact but conceptually similar hierarchically nested loop architecture driven by the sequential action of two Cohesins.

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More information

Published date: 3 March 2025
Keywords: Active Transport, Cell Nucleus, Cohesins/chemistry, DNA-Binding Proteins/chemistry, Genome, HeLa Cells, Humans, Interphase, Mitosis, Nuclear Proteins/metabolism, Polymerization, Single-Cell Analysis

Identifiers

Local EPrints ID: 500171
URI: http://eprints.soton.ac.uk/id/eprint/500171
ISSN: 1540-8140
PURE UUID: 5db9ac76-52c6-44f5-9283-4011e127e916
ORCID for M Julius Hossain: ORCID iD orcid.org/0000-0003-3303-5755

Catalogue record

Date deposited: 22 Apr 2025 16:49
Last modified: 23 Apr 2025 02:05

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Contributors

Author: Andreas Brunner
Author: Natalia Rosalía Morero
Author: Wanlu Zhang
Author: M Julius Hossain ORCID iD
Author: Marko Lampe
Author: Hannah Pflaumer
Author: Aliaksandr Halavatyi
Author: Jan-Michael Peters
Author: Kai S Beckwith
Author: Jan Ellenberg

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