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...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Molecular cell 2015-02, Vol.57 (4), p.583-594
Hauptverfasser: Kaur, Hardeep, De Muyt, Arnaud, Lichten, Michael
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 594
container_issue 4
container_start_page 583
container_title Molecular cell
container_volume 57
creator Kaur, Hardeep
De Muyt, Arnaud
Lichten, Michael
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
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4338413</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S1097276515000210</els_id><sourcerecordid>1657328665</sourcerecordid><originalsourceid>FETCH-LOGICAL-c529t-4d3fab3f3a95027d8829cbde6ea278b4b6f1613b87e7e6f322b2356ef74162a83</originalsourceid><addsrcrecordid>eNp9UctuFDEQtBARecAfIOQjlxn8GNszF6QoD7JSHlISzpbH07PxasZebG-k_D1edglw4eS2u7rKXYXQR0pqSqj8sqrnMFmYakaoqAmtCSNv0BElnaoaKpu3-5opKQ7RcUorQmgj2u4dOmRCdp0i6gi9PIY1r-5nR_H57Sl-cH45QfWQo_EDPgdrMniTAC8SXvgMy2gmnAPOT4AvQ5xNdsHjLfYeUpg2v65hxDfgQna2vNow987vcFuGOMPgCmt6jw5GMyX4sD9P0PfLi8ezq-r67tvi7PS6soJ1uWoGPpqej9x0gjA1tC3rbD-ABMNU2ze9HKmkvG8VKJAjZ6xnXEgYVTGBmZafoK873vWmL9oWfFlu0uvoZhNfdDBO_9vx7kkvw7NuOG8bygvB5z1BDD82kLKeXSrGT8ZD2CRNpVCctVKKAm12UBtDShHGVxlK9DY1vdK71PQ2NU2oLqmVsU9_f_F16HdMf3aAYtSzg6iTdeBtsTKCzXoI7v8KPwGv4KyO</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1657328665</pqid></control><display><type>article</type><title>Top3-Rmi1 DNA Single-Strand Decatenase Is Integral to the Formation and Resolution of Meiotic Recombination Intermediates</title><source>MEDLINE</source><source>Elsevier ScienceDirect Journals Complete</source><source>Cell Press Free Archives</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Free Full-Text Journals in Chemistry</source><creator>Kaur, Hardeep ; De Muyt, Arnaud ; Lichten, Michael</creator><creatorcontrib>Kaur, Hardeep ; De Muyt, Arnaud ; Lichten, Michael</creatorcontrib><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><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>
fulltext fulltext
identifier ISSN: 1097-2765
ispartof Molecular cell, 2015-02, Vol.57 (4), p.583-594
issn 1097-2765
1097-4164
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4338413
source MEDLINE; Elsevier ScienceDirect Journals Complete; Cell Press Free Archives; EZB-FREE-00999 freely available EZB journals; Free Full-Text Journals in Chemistry
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
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-27T04%3A17%3A13IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Top3-Rmi1%20DNA%20Single-Strand%20Decatenase%20Is%20Integral%20to%20the%20Formation%20and%20Resolution%20of%20Meiotic%20Recombination%20Intermediates&rft.jtitle=Molecular%20cell&rft.au=Kaur,%20Hardeep&rft.date=2015-02-19&rft.volume=57&rft.issue=4&rft.spage=583&rft.epage=594&rft.pages=583-594&rft.issn=1097-2765&rft.eissn=1097-4164&rft_id=info:doi/10.1016/j.molcel.2015.01.020&rft_dat=%3Cproquest_pubme%3E1657328665%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1657328665&rft_id=info:pmid/25699707&rft_els_id=S1097276515000210&rfr_iscdi=true