Top3-Rmi1 DNA Single-Strand Decatenase Is Integral to the Formation and Resolution of Meiotic Recombination Intermediates
The topoisomerase III (Top3)-Rmi1 heterodimer, which catalyzes DNA single-strand passage, forms a conserved complex with the Bloom’s helicase (BLM, Sgs1 in budding yeast). This complex has been proposed to regulate recombination by disassembling double Holliday junctions in a process called dissolut...
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description | The topoisomerase III (Top3)-Rmi1 heterodimer, which catalyzes DNA single-strand passage, forms a conserved complex with the Bloom’s helicase (BLM, Sgs1 in budding yeast). This complex has been proposed to regulate recombination by disassembling double Holliday junctions in a process called dissolution. Top3-Rmi1 has been suggested to act at the end of this process, resolving hemicatenanes produced by earlier BLM/Sgs1 activity. We show here that, to the contrary, Top3-Rmi1 acts in all meiotic recombination functions previously associated with Sgs1, most notably as an early recombination intermediate chaperone, promoting regulated crossover and noncrossover recombination and preventing aberrant recombination intermediate accumulation. In addition, we show that Top3-Rmi1 has important Sgs1-independent functions that ensure complete recombination intermediate resolution and chromosome segregation. These findings indicate that Top3-Rmi1 activity is important throughout recombination to resolve strand crossings that would otherwise impede progression through both early steps of pathway choice and late steps of intermediate resolution.
[Display omitted]
•The Sgs1-Top3-Rmi1 complex promotes early noncrossover formation during meiosis•The Sgs1-Top3-Rmi1 complex limits aberrant recombination intermediate formation•Top3-Rmi1 are required for complete recombination intermediate resolution•Top3-catalyzed decatenation is critical to successful meiotic recombination
Homologous recombination is critical for genome separation during meiosis. Kaur et al. show that topoisomerase III, Rmi1, and the helicase Sgs1 act together to prevent formation of aberrant recombination intermediates and to ensure that recombination intermediates are completely resolved during meiosis. |
doi_str_mv | 10.1016/j.molcel.2015.01.020 |
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[Display omitted]
•The Sgs1-Top3-Rmi1 complex promotes early noncrossover formation during meiosis•The Sgs1-Top3-Rmi1 complex limits aberrant recombination intermediate formation•Top3-Rmi1 are required for complete recombination intermediate resolution•Top3-catalyzed decatenation is critical to successful meiotic recombination
Homologous recombination is critical for genome separation during meiosis. Kaur et al. show that topoisomerase III, Rmi1, and the helicase Sgs1 act together to prevent formation of aberrant recombination intermediates and to ensure that recombination intermediates are completely resolved during meiosis.</description><identifier>ISSN: 1097-2765</identifier><identifier>EISSN: 1097-4164</identifier><identifier>DOI: 10.1016/j.molcel.2015.01.020</identifier><identifier>PMID: 25699707</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Chromosome Segregation ; DNA Topoisomerases, Type I - physiology ; DNA-Binding Proteins - metabolism ; DNA-Binding Proteins - physiology ; Endonucleases - metabolism ; Endonucleases - physiology ; Flap Endonucleases - metabolism ; Flap Endonucleases - physiology ; Holliday Junction Resolvases - metabolism ; Holliday Junction Resolvases - physiology ; Homologous Recombination - physiology ; Meiosis - genetics ; Models, Genetic ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae Proteins - metabolism ; Saccharomyces cerevisiae Proteins - physiology</subject><ispartof>Molecular cell, 2015-02, Vol.57 (4), p.583-594</ispartof><rights>2015 Elsevier Inc.</rights><rights>Copyright © 2015 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c529t-4d3fab3f3a95027d8829cbde6ea278b4b6f1613b87e7e6f322b2356ef74162a83</citedby><cites>FETCH-LOGICAL-c529t-4d3fab3f3a95027d8829cbde6ea278b4b6f1613b87e7e6f322b2356ef74162a83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.molcel.2015.01.020$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25699707$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kaur, Hardeep</creatorcontrib><creatorcontrib>De Muyt, Arnaud</creatorcontrib><creatorcontrib>Lichten, Michael</creatorcontrib><title>Top3-Rmi1 DNA Single-Strand Decatenase Is Integral to the Formation and Resolution of Meiotic Recombination Intermediates</title><title>Molecular cell</title><addtitle>Mol Cell</addtitle><description>The topoisomerase III (Top3)-Rmi1 heterodimer, which catalyzes DNA single-strand passage, forms a conserved complex with the Bloom’s helicase (BLM, Sgs1 in budding yeast). This complex has been proposed to regulate recombination by disassembling double Holliday junctions in a process called dissolution. Top3-Rmi1 has been suggested to act at the end of this process, resolving hemicatenanes produced by earlier BLM/Sgs1 activity. We show here that, to the contrary, Top3-Rmi1 acts in all meiotic recombination functions previously associated with Sgs1, most notably as an early recombination intermediate chaperone, promoting regulated crossover and noncrossover recombination and preventing aberrant recombination intermediate accumulation. In addition, we show that Top3-Rmi1 has important Sgs1-independent functions that ensure complete recombination intermediate resolution and chromosome segregation. These findings indicate that Top3-Rmi1 activity is important throughout recombination to resolve strand crossings that would otherwise impede progression through both early steps of pathway choice and late steps of intermediate resolution.
[Display omitted]
•The Sgs1-Top3-Rmi1 complex promotes early noncrossover formation during meiosis•The Sgs1-Top3-Rmi1 complex limits aberrant recombination intermediate formation•Top3-Rmi1 are required for complete recombination intermediate resolution•Top3-catalyzed decatenation is critical to successful meiotic recombination
Homologous recombination is critical for genome separation during meiosis. Kaur et al. show that topoisomerase III, Rmi1, and the helicase Sgs1 act together to prevent formation of aberrant recombination intermediates and to ensure that recombination intermediates are completely resolved during meiosis.</description><subject>Chromosome Segregation</subject><subject>DNA Topoisomerases, Type I - physiology</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>DNA-Binding Proteins - physiology</subject><subject>Endonucleases - metabolism</subject><subject>Endonucleases - physiology</subject><subject>Flap Endonucleases - metabolism</subject><subject>Flap Endonucleases - physiology</subject><subject>Holliday Junction Resolvases - metabolism</subject><subject>Holliday Junction Resolvases - physiology</subject><subject>Homologous Recombination - physiology</subject><subject>Meiosis - genetics</subject><subject>Models, Genetic</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Saccharomyces cerevisiae Proteins - physiology</subject><issn>1097-2765</issn><issn>1097-4164</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UctuFDEQtBARecAfIOQjlxn8GNszF6QoD7JSHlISzpbH07PxasZebG-k_D1edglw4eS2u7rKXYXQR0pqSqj8sqrnMFmYakaoqAmtCSNv0BElnaoaKpu3-5opKQ7RcUorQmgj2u4dOmRCdp0i6gi9PIY1r-5nR_H57Sl-cH45QfWQo_EDPgdrMniTAC8SXvgMy2gmnAPOT4AvQ5xNdsHjLfYeUpg2v65hxDfgQna2vNow987vcFuGOMPgCmt6jw5GMyX4sD9P0PfLi8ezq-r67tvi7PS6soJ1uWoGPpqej9x0gjA1tC3rbD-ABMNU2ze9HKmkvG8VKJAjZ6xnXEgYVTGBmZafoK873vWmL9oWfFlu0uvoZhNfdDBO_9vx7kkvw7NuOG8bygvB5z1BDD82kLKeXSrGT8ZD2CRNpVCctVKKAm12UBtDShHGVxlK9DY1vdK71PQ2NU2oLqmVsU9_f_F16HdMf3aAYtSzg6iTdeBtsTKCzXoI7v8KPwGv4KyO</recordid><startdate>20150219</startdate><enddate>20150219</enddate><creator>Kaur, Hardeep</creator><creator>De Muyt, Arnaud</creator><creator>Lichten, Michael</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20150219</creationdate><title>Top3-Rmi1 DNA Single-Strand Decatenase Is Integral to the Formation and Resolution of Meiotic Recombination Intermediates</title><author>Kaur, Hardeep ; De Muyt, Arnaud ; Lichten, Michael</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c529t-4d3fab3f3a95027d8829cbde6ea278b4b6f1613b87e7e6f322b2356ef74162a83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Chromosome Segregation</topic><topic>DNA Topoisomerases, Type I - physiology</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>DNA-Binding Proteins - physiology</topic><topic>Endonucleases - metabolism</topic><topic>Endonucleases - physiology</topic><topic>Flap Endonucleases - metabolism</topic><topic>Flap Endonucleases - physiology</topic><topic>Holliday Junction Resolvases - metabolism</topic><topic>Holliday Junction Resolvases - physiology</topic><topic>Homologous Recombination - physiology</topic><topic>Meiosis - genetics</topic><topic>Models, Genetic</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Saccharomyces cerevisiae Proteins - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kaur, Hardeep</creatorcontrib><creatorcontrib>De Muyt, Arnaud</creatorcontrib><creatorcontrib>Lichten, Michael</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kaur, Hardeep</au><au>De Muyt, Arnaud</au><au>Lichten, Michael</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Top3-Rmi1 DNA Single-Strand Decatenase Is Integral to the Formation and Resolution of Meiotic Recombination Intermediates</atitle><jtitle>Molecular cell</jtitle><addtitle>Mol Cell</addtitle><date>2015-02-19</date><risdate>2015</risdate><volume>57</volume><issue>4</issue><spage>583</spage><epage>594</epage><pages>583-594</pages><issn>1097-2765</issn><eissn>1097-4164</eissn><abstract>The topoisomerase III (Top3)-Rmi1 heterodimer, which catalyzes DNA single-strand passage, forms a conserved complex with the Bloom’s helicase (BLM, Sgs1 in budding yeast). This complex has been proposed to regulate recombination by disassembling double Holliday junctions in a process called dissolution. Top3-Rmi1 has been suggested to act at the end of this process, resolving hemicatenanes produced by earlier BLM/Sgs1 activity. We show here that, to the contrary, Top3-Rmi1 acts in all meiotic recombination functions previously associated with Sgs1, most notably as an early recombination intermediate chaperone, promoting regulated crossover and noncrossover recombination and preventing aberrant recombination intermediate accumulation. In addition, we show that Top3-Rmi1 has important Sgs1-independent functions that ensure complete recombination intermediate resolution and chromosome segregation. These findings indicate that Top3-Rmi1 activity is important throughout recombination to resolve strand crossings that would otherwise impede progression through both early steps of pathway choice and late steps of intermediate resolution.
[Display omitted]
•The Sgs1-Top3-Rmi1 complex promotes early noncrossover formation during meiosis•The Sgs1-Top3-Rmi1 complex limits aberrant recombination intermediate formation•Top3-Rmi1 are required for complete recombination intermediate resolution•Top3-catalyzed decatenation is critical to successful meiotic recombination
Homologous recombination is critical for genome separation during meiosis. Kaur et al. show that topoisomerase III, Rmi1, and the helicase Sgs1 act together to prevent formation of aberrant recombination intermediates and to ensure that recombination intermediates are completely resolved during meiosis.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25699707</pmid><doi>10.1016/j.molcel.2015.01.020</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Chromosome Segregation DNA Topoisomerases, Type I - physiology DNA-Binding Proteins - metabolism DNA-Binding Proteins - physiology Endonucleases - metabolism Endonucleases - physiology Flap Endonucleases - metabolism Flap Endonucleases - physiology Holliday Junction Resolvases - metabolism Holliday Junction Resolvases - physiology Homologous Recombination - physiology Meiosis - genetics Models, Genetic Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae Proteins - metabolism Saccharomyces cerevisiae Proteins - physiology |
title | Top3-Rmi1 DNA Single-Strand Decatenase Is Integral to the Formation and Resolution of Meiotic Recombination Intermediates |
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