Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria
Double-strand breaks (DSBs) can lead to the loss of genetic information and cell death. Although DSB repair via homologous recombination has been well characterized, the spatial organization of this process inside cells remains poorly understood, and the mechanisms used for chromosome resegregation...
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| Format: | Article |
| Language: | en_US |
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Rockefeller University Press
2016
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| Online Access: | http://hdl.handle.net/1721.1/101424 https://orcid.org/0000-0003-4764-8851 https://orcid.org/0000-0002-8288-7607 https://orcid.org/0000-0002-6807-6576 |
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| author | Badrinarayanan, Anjana Laub, Michael T Le, Tung |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Badrinarayanan, Anjana Laub, Michael T Le, Tung |
| author_sort | Badrinarayanan, Anjana |
| collection | MIT |
| description | Double-strand breaks (DSBs) can lead to the loss of genetic information and cell death. Although DSB repair via homologous recombination has been well characterized, the spatial organization of this process inside cells remains poorly understood, and the mechanisms used for chromosome resegregation after repair are unclear. In this paper, we introduced site-specific DSBs in Caulobacter crescentus and then used time-lapse microscopy to visualize the ensuing chromosome dynamics. Damaged loci rapidly mobilized after a DSB, pairing with their homologous partner to enable repair, before being resegregated to their original cellular locations, independent of DNA replication. Origin-proximal regions were resegregated by the ParABS system with the ParA structure needed for resegregation assembling dynamically in response to the DSB-induced movement of an origin-associated ParB away from one cell pole. Origin-distal regions were resegregated in a ParABS-independent manner and instead likely rely on a physical, spring-like force to segregate repaired loci. Collectively, our results provide a mechanistic basis for the resegregation of chromosomes after a DSB. |
| first_indexed | 2024-09-23T16:45:48Z |
| format | Article |
| id | mit-1721.1/101424 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T16:45:48Z |
| publishDate | 2016 |
| publisher | Rockefeller University Press |
| record_format | dspace |
| spelling | mit-1721.1/1014242022-09-29T21:22:16Z Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria Badrinarayanan, Anjana Laub, Michael T Le, Tung Massachusetts Institute of Technology. Department of Biology Badrinarayanan, Anjana Le, Tung B. K. Laub, Michael T. Double-strand breaks (DSBs) can lead to the loss of genetic information and cell death. Although DSB repair via homologous recombination has been well characterized, the spatial organization of this process inside cells remains poorly understood, and the mechanisms used for chromosome resegregation after repair are unclear. In this paper, we introduced site-specific DSBs in Caulobacter crescentus and then used time-lapse microscopy to visualize the ensuing chromosome dynamics. Damaged loci rapidly mobilized after a DSB, pairing with their homologous partner to enable repair, before being resegregated to their original cellular locations, independent of DNA replication. Origin-proximal regions were resegregated by the ParABS system with the ParA structure needed for resegregation assembling dynamically in response to the DSB-induced movement of an origin-associated ParB away from one cell pole. Origin-distal regions were resegregated in a ParABS-independent manner and instead likely rely on a physical, spring-like force to segregate repaired loci. Collectively, our results provide a mechanistic basis for the resegregation of chromosomes after a DSB. National Institutes of Health (U.S.) (Grant R01GM082899) Gordon and Betty Moore Foundation (Postdoctoral Fellow of the Life Sciences Research Foundation) Human Frontier Science Program (Strasbourg, France) (Postdoctoral Fellowship) 2016-03-03T01:35:02Z 2016-03-03T01:35:02Z 2015-08 2015-05 Article http://purl.org/eprint/type/JournalArticle 0021-9525 1540-8140 http://hdl.handle.net/1721.1/101424 Badrinarayanan, Anjana, Tung B.K. Le, and Michael T. Laub. “Rapid Pairing and Resegregation of Distant Homologous Loci Enables Double-Strand Break Repair in Bacteria.” The Journal of Cell Biology 210, no. 3 (August 3, 2015): 385–400. https://orcid.org/0000-0003-4764-8851 https://orcid.org/0000-0002-8288-7607 https://orcid.org/0000-0002-6807-6576 en_US http://dx.doi.org/10.1083/jcb.201505019 The Journal of Cell Biology Creative Commons Attribution http://creativecommons.org/licenses/by-nc-sa/3.0/ application/pdf Rockefeller University Press Rockefeller University Press |
| spellingShingle | Badrinarayanan, Anjana Laub, Michael T Le, Tung Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria |
| title | Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria |
| title_full | Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria |
| title_fullStr | Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria |
| title_full_unstemmed | Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria |
| title_short | Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria |
| title_sort | rapid pairing and resegregation of distant homologous loci enables double strand break repair in bacteria |
| url | http://hdl.handle.net/1721.1/101424 https://orcid.org/0000-0003-4764-8851 https://orcid.org/0000-0002-8288-7607 https://orcid.org/0000-0002-6807-6576 |
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