{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T02:16:20Z","timestamp":1792635380821,"version":"4.5.0"},"update-to":[{"DOI":"10.1371\/journal.pgen.1011175","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,3,1]],"date-time":"2024-03-01T00:00:00Z","timestamp":1709251200000}}],"reference-count":97,"publisher":"Public Library of Science (PLoS)","issue":"2","license":[{"start":{"date-parts":[[2024,2,20]],"date-time":"2024-02-20T00:00:00Z","timestamp":1708387200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000071","name":"National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["HD097897"],"award-info":[{"award-number":["HD097897"]}],"id":[{"id":"10.13039\/100000071","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000071","name":"National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["HD095296"],"award-info":[{"award-number":["HD095296"]}],"id":[{"id":"10.13039\/100000071","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000071","name":"National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["K99HD112986"],"award-info":[{"award-number":["K99HD112986"]}],"id":[{"id":"10.13039\/100000071","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000052","name":"NIH Office of the Director","doi-asserted-by":"publisher","award":["1S10 OD017992-01"],"award-info":[{"award-number":["1S10 OD017992-01"]}],"id":[{"id":"10.13039\/100000052","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"abstract":"<jats:p>\n                    Meiotic recombination between homologous chromosomes is initiated by the formation of hundreds of programmed double-strand breaks (DSBs). Approximately 10% of these DSBs result in crossovers (COs), sites of physical DNA exchange between homologs that are critical to correct chromosome segregation. Virtually all COs are formed by coordinated efforts of the MSH4\/MSH5 and MLH1\/MLH3 heterodimers, the latter representing the defining marks of CO sites. The regulation of CO number and position is poorly understood, but undoubtedly requires the coordinated action of multiple repair pathways. In a previous report, we found gene-trap disruption of the DNA helicase, FANCJ (BRIP1\/BACH1), elicited elevated numbers of MLH1 foci and chiasmata. In somatic cells, FANCJ interacts with numerous DNA repair proteins including MLH1, and we hypothesized that FANCJ functions with MLH1 to regulate the major CO pathway. To further elucidate the meiotic function of FANCJ, we produced three new\n                    <jats:italic>Fancj<\/jats:italic>\n                    mutant mouse lines via CRISPR\/Cas9 gene editing: a full-gene deletion, truncation of the N-terminal Helicase domain, and a C-terminal dual-tagged allele. We also generated an antibody against the C-terminus of the mouse FANCJ protein. Surprisingly, none of our\n                    <jats:italic>Fancj<\/jats:italic>\n                    mutants show any change in either MLH1 focus counts during pachynema or total CO number at diakinesis of prophase I. We find evidence that FANCJ and MLH1 do not interact in meiosis; further, FANCJ does not co-localize with MSH4, MLH1, or MLH3 in meiosis. Instead, FANCJ co-localizes with BRCA1 and TOPBP1, forming discrete foci along the chromosome cores beginning in early meiotic prophase I and densely localized to unsynapsed chromosome axes in late zygonema and to the XY chromosomes in early pachynema.\n                    <jats:italic>Fancj<\/jats:italic>\n                    mutants also exhibit a subtle persistence of DSBs in pachynema. Collectively, these data indicate a role for FANCJ in early DSB repair, but they rule out a role for FANCJ in MLH1-mediated CO events.\n                  <\/jats:p>","DOI":"10.1371\/journal.pgen.1011175","type":"journal-article","created":{"date-parts":[[2024,2,20]],"date-time":"2024-02-20T13:31:02Z","timestamp":1708435862000},"page":"e1011175","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":14,"title":["The DNA helicase FANCJ (BRIP1) functions in double strand break repair processing, but not crossover formation during prophase I of meiosis in male mice"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5227-6613","authenticated-orcid":true,"given":"Tegan S.","family":"Horan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0882-7390","authenticated-orcid":true,"given":"Carolline F. R.","family":"Ascen\u00e7\u00e3o","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9902-7040","authenticated-orcid":true,"given":"Christopher","family":"Mellor","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meng","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcus B.","family":"Smolka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2050-6979","authenticated-orcid":true,"given":"Paula E.","family":"Cohen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2024,2,20]]},"reference":[{"key":"pgen.1011175.ref001","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/S0092-8674(00)81876-0","article-title":"Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family","volume":"88","author":"S Keeney","year":"1997","journal-title":"Cell"},{"key":"pgen.1011175.ref002","first-page":"81","article-title":"Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis.","author":"S. Keeney","year":"2008"},{"key":"pgen.1011175.ref003","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1038\/s41586-021-03389-3","article-title":"Concerted cutting by Spo11 illuminates meiotic DNA break mechanics","volume":"594","author":"D Johnson","year":"2021","journal-title":"Nature"},{"key":"pgen.1011175.ref004","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1016\/j.cell.2016.09.035","article-title":"The Landscape of Mouse Meiotic Double-Strand Break Formation, Processing, and Repair","volume":"167","author":"J Lange","year":"2016","journal-title":"Cell"},{"key":"pgen.1011175.ref005","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1101\/gad.336032.119","article-title":"Molecular structures and mechanisms of DNA break processing in mouse meiosis","volume":"34","author":"S Yamada","year":"2020","journal-title":"Genes Dev"},{"key":"pgen.1011175.ref006","doi-asserted-by":"crossref","first-page":"1222","DOI":"10.1126\/science.1219379","article-title":"Rad51 Is an Accessory Factor for Dmc1-Mediated Joint Molecule Formation During Meiosis","volume":"337","author":"V Cloud","year":"2012","journal-title":"Science"},{"key":"pgen.1011175.ref007","doi-asserted-by":"crossref","first-page":"11257","DOI":"10.1073\/pnas.1920368117","article-title":"Rad51 facilitates filament assembly of meiosis-specific Dmc1 recombinase","volume":"117","author":"W-H Lan","year":"2020","journal-title":"Proc Natl Acad Sci"},{"key":"pgen.1011175.ref008","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1016\/j.molcel.2020.06.015","article-title":"The Configuration of RPA, RAD51, and DMC1 Binding in Meiosis Reveals the Nature of Critical Recombination Intermediates","volume":"79","author":"AG Hinch","year":"2020","journal-title":"Mol Cell"},{"key":"pgen.1011175.ref009","doi-asserted-by":"crossref","first-page":"e299","DOI":"10.1371\/journal.pbio.0050299","article-title":"Synthesis-Dependent Strand Annealing in Meiosis.","volume":"5","author":"MS McMahill","year":"2007","journal-title":"PLoS Biol"},{"key":"pgen.1011175.ref010","doi-asserted-by":"crossref","first-page":"a016618","DOI":"10.1101\/cshperspect.a016618","article-title":"Meiotic Recombination: The Essence of Heredity.","volume":"7","author":"N. Hunter","year":"2015","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"pgen.1011175.ref011","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1146\/annurev-genet-120215-035111","article-title":"Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation","volume":"50","author":"S Gray","year":"2016","journal-title":"Annu Rev Genet"},{"key":"pgen.1011175.ref012","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1083\/jcb.200506170","article-title":"Localization of MMR proteins on meiotic chromosomes in mice indicates distinct functions during prophase I","volume":"171","author":"NK Kolas","year":"2005","journal-title":"J Cell Biol"},{"key":"pgen.1011175.ref013","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1038\/ng931","article-title":"Meiotic arrest and aneuploidy in MLH3-deficient mice","volume":"31","author":"SM Lipkin","year":"2002","journal-title":"Nat Genet"},{"key":"pgen.1011175.ref014","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1038\/5075","article-title":"Mammalian MutS homologue 5 is required for chromosome pairing in meiosis","volume":"21","author":"W Edelmann","year":"1999","journal-title":"Nat Genet"},{"key":"pgen.1011175.ref015","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1101\/gad.14.9.1085","article-title":"MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice","volume":"14","author":"B Kneitz","year":"2000","journal-title":"Genes Dev"},{"key":"pgen.1011175.ref016","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/j.molcel.2008.07.006","article-title":"RecQ Helicase, Sgs1, and XPF Family Endonuclease, Mus81-Mms4, Resolve Aberrant Joint Molecules during Meiotic Recombination","volume":"31","author":"SD Oh","year":"2008","journal-title":"Mol Cell"},{"key":"pgen.1011175.ref017","doi-asserted-by":"crossref","first-page":"e1000186","DOI":"10.1371\/journal.pgen.1000186","article-title":"MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis.","volume":"4","author":"JK Holloway","year":"2008","journal-title":"PLoS Genet"},{"key":"pgen.1011175.ref018","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1007\/s00412-015-0549-2","article-title":"FancJ (Brip1) loss-of-function allele results in spermatogonial cell depletion during embryogenesis and altered processing of crossover sites during meiotic prophase I in mice.","volume":"125","author":"X Sun","year":"2016","journal-title":"Chromosoma"},{"key":"pgen.1011175.ref019","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1146\/annurev-genet-102108-134222","article-title":"How the Fanconi Anemia pathway guards the genome","volume":"43","author":"G-L Moldovan","year":"2009","journal-title":"Annu Rev Genet"},{"key":"pgen.1011175.ref020","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1038\/nrm.2016.48","article-title":"The Fanconi anaemia pathway: new players and new functions","volume":"17","author":"R Ceccaldi","year":"2016","journal-title":"Nat Rev Mol Cell Biol"},{"key":"pgen.1011175.ref021","doi-asserted-by":"crossref","first-page":"1811","DOI":"10.1007\/s00439-022-02462-9","article-title":"Fanconi anemia: current insights regarding epidemiology, cancer, and DNA repair.","volume":"141","author":"JD Peake","year":"2022","journal-title":"Hum Genet."},{"key":"pgen.1011175.ref022","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/j.tig.2018.12.007","article-title":"The Fanconi Anemia Pathway and Fertility","volume":"35","author":"V Tsui","year":"2019","journal-title":"Trends Genet"},{"key":"pgen.1011175.ref023","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/S0092-8674(01)00304-X","article-title":"BACH1, a Novel Helicase-like Protein, Interacts Directly with BRCA1 and Contributes to Its DNA Repair Function","volume":"105","author":"SB Cantor","year":"2001","journal-title":"Cell"},{"key":"pgen.1011175.ref024","doi-asserted-by":"crossref","first-page":"2390","DOI":"10.1182\/blood-2006-11-057273","article-title":"FANCJ (BACH1) helicase forms DNA damage inducible foci with replication protein A and interacts physically and functionally with the single-stranded DNA-binding protein.","volume":"110","author":"R Gupta","year":"2007","journal-title":"Blood"},{"key":"pgen.1011175.ref025","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1016\/j.molcel.2010.01.002","article-title":"BACH1\/FANCJ Acts with TopBP1 and Participates Early in DNA Replication Checkpoint Control","volume":"37","author":"Z Gong","year":"2010","journal-title":"Mol Cell"},{"key":"pgen.1011175.ref026","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.tig.2011.09.003","article-title":"Fanconi anemia and Bloom\u2019s syndrome crosstalk through FANCJ\u2013BLM helicase interaction","volume":"28","author":"AN Suhasini","year":"2012","journal-title":"Trends Genet"},{"key":"pgen.1011175.ref027","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1038\/emboj.2010.362","article-title":"Interaction between the helicases genetically linked to Fanconi anemia group J and Bloom\u2019s syndrome","volume":"30","author":"AN Suhasini","year":"2011","journal-title":"EMBO J"},{"key":"pgen.1011175.ref028","doi-asserted-by":"crossref","first-page":"3238","DOI":"10.1038\/sj.emboj.7601754","article-title":"The FANCJ\/MutL\u03b1 interaction is required for correction of the cross-link response in FA-J cells","volume":"26","author":"M Peng","year":"2007","journal-title":"EMBO J"},{"key":"pgen.1011175.ref029","doi-asserted-by":"crossref","first-page":"1409","DOI":"10.1158\/1940-6207.CAPR-10-0118","article-title":"An MLH1 Mutation Links BACH1\/FANCJ to Colon Cancer, Signaling, and Insight toward Directed Therapy.","volume":"3","author":"J Xie","year":"2010","journal-title":"Cancer Prev Res (Phila Pa)."},{"key":"pgen.1011175.ref030","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1002\/em.20568","article-title":"Assessing the link between BACH1\/FANCJ and MLH1 in DNA crosslink repair","volume":"51","author":"SB Cantor","year":"2010","journal-title":"Environ Mol Mutagen"},{"key":"pgen.1011175.ref031","doi-asserted-by":"crossref","first-page":"2532","DOI":"10.1101\/gad.272740.115","article-title":"FANCJ suppresses microsatellite instability and lymphomagenesis independent of the Fanconi anemia pathway","volume":"29","author":"K Matsuzaki","year":"2015","journal-title":"Genes Dev"},{"key":"pgen.1011175.ref032","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.mrfmmm.2009.03.010","article-title":"Finding the needle in the hay stack: Hematopoietic stem cells in Fanconi anemia","volume":"668","author":"LUW M\u00fcller","year":"2009","journal-title":"Mutat Res"},{"key":"pgen.1011175.ref033","doi-asserted-by":"crossref","first-page":"265790","DOI":"10.1155\/2012\/265790","article-title":"Disrupted Signaling through the Fanconi Anemia Pathway Leads to Dysfunctional Hematopoietic Stem Cell Biology: Underlying Mechanisms and Potential Therapeutic Strategies.","volume":"2012","author":"A Geiselhart","year":"2012","journal-title":"Anemia"},{"key":"pgen.1011175.ref034","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.molcel.2015.08.020","article-title":"Endogenous Formaldehyde Is a Hematopoietic Stem Cell Genotoxin and Metabolic Carcinogen","volume":"60","author":"LB Pontel","year":"2015","journal-title":"Mol Cell"},{"key":"pgen.1011175.ref035","doi-asserted-by":"crossref","first-page":"2417","DOI":"10.1016\/j.molcel.2023.05.035","article-title":"Genotoxic aldehyde stress prematurely ages hematopoietic stem cells in a p53-driven manner","volume":"83","author":"M Wang","year":"2023","journal-title":"Mol Cell"},{"key":"pgen.1011175.ref036","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1038\/85830","article-title":"Recombinational DNA double-strand breaks in mice precede synapsis","volume":"27","author":"SK Mahadevaiah","year":"2001","journal-title":"Nat Genet"},{"key":"pgen.1011175.ref037","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/S1534-5807(03)00093-5","article-title":"H2AX Is Required for Chromatin Remodeling and Inactivation of Sex Chromosomes in Male Mouse Meiosis","volume":"4","author":"O Fernandez-Capetillo","year":"2003","journal-title":"Dev Cell"},{"key":"pgen.1011175.ref038","doi-asserted-by":"crossref","first-page":"2489","DOI":"10.1093\/nar\/gkv061","article-title":"Multiple facets of histone variant H2AX: a DNA double-strand-break marker with several biological functions","volume":"43","author":"V Turinetto","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011175.ref039","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1016\/j.cub.2019.11.064","article-title":"The Initiation of Meiotic Sex Chromosome Inactivation Sequesters DNA Damage Signaling from Autosomes in Mouse Spermatogenesis","volume":"30","author":"H Abe","year":"2020","journal-title":"Curr Biol"},{"key":"pgen.1011175.ref040","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1242\/jcs.004945","article-title":"Characterization of Spo11-dependent and independent phospho-H2AX foci during meiotic prophase I in the male mouse","volume":"120","author":"A Chicheportiche","year":"2007","journal-title":"J Cell Sci"},{"key":"pgen.1011175.ref041","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1242\/jcs.03394","article-title":"Initiation and resolution of interhomolog connections: crossover and non-crossover sites along mouse synaptonemal complexes","volume":"120","author":"PB Moens","year":"2007","journal-title":"J Cell Sci"},{"key":"pgen.1011175.ref042","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1007\/s00412-012-0364-y","article-title":"Inactivation or non-reactivation: what accounts better for the silence of sex chromosomes during mammalian male meiosis","volume":"121","author":"J Page","year":"2012","journal-title":"Chromosoma"},{"key":"pgen.1011175.ref043","doi-asserted-by":"crossref","first-page":"1698","DOI":"10.15252\/embj.201387530","article-title":"Crosstalk between BRCA-Fanconi anemia and mismatch repair pathways prevents MSH2-dependent aberrant DNA damage responses","volume":"33","author":"M Peng","year":"2014","journal-title":"EMBO J"},{"key":"pgen.1011175.ref044","doi-asserted-by":"crossref","first-page":"1839","DOI":"10.1534\/g3.119.400074","article-title":"Mutation of the ATPase Domain of MutS Homolog-5 (MSH5) Reveals a Requirement for a Functional MutS\u03b3 Complex for All Crossovers in Mammalian Meiosis.","volume":"9","author":"CR Milano","year":"2019","journal-title":"G3 GenesGenomesGenetics."},{"key":"pgen.1011175.ref045","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1002\/em.22401","article-title":"ATR Signaling in Mammalian Meiosis: From Upstream Scaffolds to Downstream Signaling","volume":"61","author":"C Pereira","year":"2020","journal-title":"Environ Mol Mutagen"},{"key":"pgen.1011175.ref046","doi-asserted-by":"crossref","first-page":"e1008740","DOI":"10.1371\/journal.pgen.1008740","article-title":"Cancer-associated mutations in the iron-sulfur domain of FANCJ affect G-quadruplex metabolism","volume":"16","author":"DC Odermatt","year":"2020","journal-title":"PLOS Genet"},{"key":"pgen.1011175.ref047","doi-asserted-by":"crossref","first-page":"2525","DOI":"10.1038\/s41467-021-22830-9","article-title":"Single-molecule imaging reveals replication fork coupled formation of G-quadruplex structures hinders local replication stress signaling.","volume":"12","author":"WTC Lee","year":"2021","journal-title":"Nat Commun"},{"key":"pgen.1011175.ref048","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.molcel.2022.12.005","article-title":"The FANCJ helicase unfolds DNA-protein crosslinks to promote their repair","volume":"83","author":"D Yaneva","year":"2023","journal-title":"Mol Cell"},{"key":"pgen.1011175.ref049","doi-asserted-by":"crossref","first-page":"18545","DOI":"10.1074\/jbc.M115.642884","article-title":"hMSH5 Facilitates the Repair of Camptothecin-induced Double-strand Breaks through an Interaction with FANCJ *","volume":"290","author":"Y Xu","year":"2015","journal-title":"J Biol Chem"},{"key":"pgen.1011175.ref050","doi-asserted-by":"crossref","first-page":"2212","DOI":"10.1128\/MCB.01256-12","article-title":"Fanconi Anemia Group J Helicase and MRE11 Nuclease Interact To Facilitate the DNA Damage Response","volume":"33","author":"AN Suhasini","year":"2013","journal-title":"Mol Cell Biol"},{"key":"pgen.1011175.ref051","doi-asserted-by":"crossref","first-page":"e1008701","DOI":"10.1371\/journal.pgen.1008701","article-title":"FANCJ helicase promotes DNA end resection by facilitating CtIP recruitment to DNA double-strand breaks","volume":"16","author":"S Nath","year":"2020","journal-title":"PLoS Genet"},{"key":"pgen.1011175.ref052","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.1534\/genetics.109.105114","article-title":"Variation in genomic recombination rates among heterogeneous stock mice","volume":"182","author":"BL Dumont","year":"2009","journal-title":"Genetics"},{"key":"pgen.1011175.ref053","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1126\/science.1183439","article-title":"PRDM9 Is a Major Determinant of Meiotic Recombination Hotspots in Humans and Mice","volume":"327","author":"F Baudat","year":"2010","journal-title":"Science"},{"key":"pgen.1011175.ref054","doi-asserted-by":"crossref","first-page":"e1002854","DOI":"10.1371\/journal.pgen.1002854","article-title":"Genetic variants in REC8, RNF212, and PRDM9 influence male recombination in cattle.","volume":"8","author":"C Sandor","year":"2012","journal-title":"PLoS Genet"},{"key":"pgen.1011175.ref055","doi-asserted-by":"crossref","first-page":"e1004125","DOI":"10.1371\/journal.pgen.1004125","article-title":"Variation in Genome-Wide Levels of Meiotic Recombination Is Established at the Onset of Prophase in Mammalian Males.","volume":"10","author":"B Baier","year":"2014","journal-title":"PLoS Genet."},{"key":"pgen.1011175.ref056","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1101\/gad.295501.116","article-title":"Natural variation and dosage of the HEI10 meiotic E3 ligase control Arabidopsis crossover recombination","volume":"31","author":"PA Ziolkowski","year":"2017","journal-title":"Genes Dev"},{"key":"pgen.1011175.ref057","doi-asserted-by":"crossref","first-page":"iyaa019","DOI":"10.1093\/genetics\/iyaa019","article-title":"Sex-specific variation in the genome-wide recombination rate","volume":"217","author":"AL Peterson","year":"2021","journal-title":"Genetics"},{"key":"pgen.1011175.ref058","doi-asserted-by":"crossref","first-page":"1705","DOI":"10.1038\/s12276-020-00519-1","article-title":"DNA end resection and its role in DNA replication and DSB repair choice in mammalian cells","volume":"52","author":"F Zhao","year":"2020","journal-title":"Exp Mol Med"},{"key":"pgen.1011175.ref059","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.molcel.2018.02.032","article-title":"Mechanistic View and Genetic Control of DNA Recombination during Meiosis","volume":"70","author":"M-C Marsolier-Kergoat","year":"2018","journal-title":"Mol Cell"},{"key":"pgen.1011175.ref060","doi-asserted-by":"crossref","first-page":"4258","DOI":"10.1016\/j.molcel.2021.08.003","article-title":"Repeated strand invasion and extensive branch migration are hallmarks of meiotic recombination","volume":"81","author":"JS Ahuja","year":"2021","journal-title":"Mol Cell"},{"key":"pgen.1011175.ref061","doi-asserted-by":"crossref","first-page":"e2109093119","DOI":"10.1073\/pnas.2109093119","article-title":"Mechanism of Bloom syndrome complex assembly required for double Holliday junction dissolution and genome stability","volume":"119","author":"C Hodson","year":"2022","journal-title":"Proc Natl Acad Sci"},{"key":"pgen.1011175.ref062","doi-asserted-by":"crossref","first-page":"a016477","DOI":"10.1101\/cshperspect.a016477","article-title":"The Dissolution of Double Holliday Junctions.","volume":"6","author":"AH Bizard","year":"2014","journal-title":"Cold Spring Harb Perspect Biol."},{"key":"pgen.1011175.ref063","doi-asserted-by":"crossref","first-page":"2087","DOI":"10.1016\/j.bpj.2018.10.029","article-title":"MutS\u03b3-Induced DNA Conformational Changes Provide Insights into Its Role in Meiotic Recombination","volume":"115","author":"S Lahiri","year":"2018","journal-title":"Biophys J"},{"key":"pgen.1011175.ref064","doi-asserted-by":"crossref","first-page":"5622","DOI":"10.1073\/pnas.96.10.5622","article-title":"Bloom\u2019s syndrome protein, BLM, colocalizes with replication protein A in meiotic prophase nuclei of mammalian spermatocytes","volume":"96","author":"D Walpita","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1011175.ref065","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1242\/jcs.113.4.663","article-title":"Expression and nuclear localization of BLM, a chromosome stability protein mutated in Bloom\u2019s syndrome, suggest a role in recombination during meiotic prophase","volume":"113","author":"PB Moens","year":"2000","journal-title":"J Cell Sci"},{"key":"pgen.1011175.ref066","doi-asserted-by":"crossref","first-page":"1611","DOI":"10.1242\/jcs.115.8.1611","article-title":"The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination","volume":"115","author":"PB Moens","year":"2002","journal-title":"J Cell Sci"},{"key":"pgen.1011175.ref067","doi-asserted-by":"crossref","first-page":"25450","DOI":"10.1074\/jbc.M501995200","article-title":"Analysis of the DNA Substrate Specificity of the Human BACH1 HelicaseAssociated with BreastCancer *","volume":"280","author":"R Gupta","year":"2005","journal-title":"J Biol Chem"},{"key":"pgen.1011175.ref068","doi-asserted-by":"crossref","first-page":"7505","DOI":"10.1074\/jbc.M809019200","article-title":"FANCJ Uses Its Motor ATPase to Destabilize Protein-DNA Complexes, Unwind Triplexes, and Inhibit RAD51 Strand Exchange *","volume":"284","author":"JA Sommers","year":"2009","journal-title":"J Biol Chem"},{"key":"pgen.1011175.ref069","doi-asserted-by":"crossref","first-page":"8886","DOI":"10.1093\/nar\/gkx586","article-title":"FANCJ helicase controls the balance between short- and long-tract gene conversions between sister chromatids","volume":"45","author":"S Nath","year":"2017","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011175.ref070","doi-asserted-by":"crossref","first-page":"2404","DOI":"10.1038\/ncomms3404","article-title":"BRCA1 and CtIP suppress long-tract gene conversion between sister chromatids","volume":"4","author":"G Chandramouly","year":"2013","journal-title":"Nat Commun"},{"key":"pgen.1011175.ref071","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.celrep.2014.08.076","article-title":"BRCA1 accelerates CtIP-mediated DNA-end resection","volume":"9","author":"A Cruz-Garc\u00eda","year":"2014","journal-title":"Cell Rep"},{"key":"pgen.1011175.ref072","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1038\/nature24060","article-title":"BRCA1-BARD1 promotes RAD51-mediated homologous DNA pairing","volume":"550","author":"W Zhao","year":"2017","journal-title":"Nature"},{"key":"pgen.1011175.ref073","first-page":"2022","article-title":"BRCA1\/BRC-1 and SMC-5\/6 regulate DNA repair pathway engagement during C","author":"E Toraason","year":"2022","journal-title":"elegans meiosis. bioRxiv"},{"key":"pgen.1011175.ref074","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1111\/febs.13150","article-title":"BRCA1, a \u2018complex\u2019 protein involved in the maintenance of genomic stability.","volume":"282","author":"KI Savage","year":"2015","journal-title":"FEBS J"},{"key":"pgen.1011175.ref075","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1083\/jcb.201311050","article-title":"BRCA1 establishes DNA damage signaling and pericentric heterochromatin of the X chromosome in male meiosis","volume":"205","author":"TJ Broering","year":"2014","journal-title":"J Cell Biol"},{"key":"pgen.1011175.ref076","doi-asserted-by":"crossref","first-page":"12536","DOI":"10.1073\/pnas.1712530114","article-title":"DNA damage response protein TOPBP1 regulates X chromosome silencing in the mammalian germ line","volume":"114","author":"E ElInati","year":"2017","journal-title":"Proc Natl Acad Sci"},{"key":"pgen.1011175.ref077","doi-asserted-by":"crossref","first-page":"36132","DOI":"10.1074\/jbc.M808152200","article-title":"FANCJ Is a Structure-specific DNA Helicase Associated with the Maintenance of Genomic G\/C Tracts *","volume":"283","author":"TBC London","year":"2008","journal-title":"J Biol Chem"},{"key":"pgen.1011175.ref078","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1158\/1541-7786.MCR-20-0828","article-title":"Comprehensive Mutational Analysis of the BRCA1-Associated DNA Helicase and Tumor-Suppressor FANCJ\/BACH1\/BRIP1","volume":"19","author":"JA Calvo","year":"2021","journal-title":"Mol Cancer Res"},{"key":"pgen.1011175.ref079","doi-asserted-by":"crossref","first-page":"e1002094","DOI":"10.1371\/journal.pgen.1002094","article-title":"Mammalian BTBD12 (SLX4) protects against genomic instability during mammalian spermatogenesis.","volume":"7","author":"JK Holloway","year":"2011","journal-title":"PLoS Genet."},{"key":"pgen.1011175.ref080","doi-asserted-by":"crossref","first-page":"1588","DOI":"10.1126\/science.1220381","article-title":"FANCM Limits Meiotic Crossovers.","volume":"336","author":"W Crismani","year":"2012","journal-title":"Science"},{"key":"pgen.1011175.ref081","doi-asserted-by":"crossref","first-page":"2033","DOI":"10.1534\/g3.116.029488","article-title":"Budding Yeast SLX4 Contributes to the Appropriate Distribution of Crossovers and Meiotic Double-Strand Break Formation on Bivalents During Meiosis.","volume":"6","author":"M Higashide","year":"2016","journal-title":"G3 GenesGenomesGenetics."},{"key":"pgen.1011175.ref082","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1105\/tpc.17.00745","article-title":"Arabidopsis thaliana FANCD2 Promotes Meiotic Crossover Formation","volume":"30","author":"M-T Kurzbauer","year":"2018","journal-title":"Plant Cell"},{"key":"pgen.1011175.ref083","doi-asserted-by":"crossref","first-page":"7532","DOI":"10.1093\/nar\/gkz514","article-title":"A Fanci knockout mouse model reveals common and distinct functions for FANCI and FANCD2","volume":"47","author":"EL Dubois","year":"2019","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011175.ref084","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1038\/s41598-019-57096-1","article-title":"In vivo analysis of FANCD2 recruitment at meiotic DNA breaks in Caenorhabditis elegans.","volume":"10","author":"M Germoglio","year":"2020","journal-title":"Sci Rep."},{"key":"pgen.1011175.ref085","doi-asserted-by":"crossref","first-page":"e2107543118","DOI":"10.1073\/pnas.2107543118","article-title":"Regulation of interference-sensitive crossover distribution ensures crossover assurance in Arabidopsis","volume":"118","author":"X Li","year":"2021","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1011175.ref086","doi-asserted-by":"crossref","first-page":"3644","DOI":"10.1038\/s41467-022-31438-6","article-title":"FANCM promotes class I interfering crossovers and suppresses class II non-interfering crossovers in wheat meiosis.","volume":"13","author":"SD Desjardins","year":"2022","journal-title":"Nat Commun"},{"key":"pgen.1011175.ref087","doi-asserted-by":"crossref","first-page":"100349","DOI":"10.1016\/j.xgen.2023.100349","article-title":"Fancm has dual roles in the limiting of meiotic crossovers and germ cell maintenance in mammals","volume":"3","author":"V Tsui","year":"2023","journal-title":"Cell Genomics"},{"key":"pgen.1011175.ref088","doi-asserted-by":"crossref","first-page":"5234","DOI":"10.1093\/hmg\/ddv244","article-title":"FANCB is essential in the male germline and regulates H3K9 methylation on the sex chromosomes during meiosis","volume":"24","author":"Y Kato","year":"2015","journal-title":"Hum Mol Genet"},{"key":"pgen.1011175.ref089","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1016\/j.celrep.2016.09.073","article-title":"Elucidation of the Fanconi Anemia Protein Network in Meiosis and Its Function in the Regulation of Histone Modifications","volume":"17","author":"KG Alavattam","year":"2016","journal-title":"Cell Rep"},{"key":"pgen.1011175.ref090","first-page":"1","article-title":"FANCI plays an essential role in spermatogenesis and regulates meiotic histone methylation","volume":"12","author":"L Xu","year":"2021","journal-title":"Cell Death Dis"},{"key":"pgen.1011175.ref091","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1023\/A:1018445520117","article-title":"A drying-down technique for the spreading of mammalian meiocytes from the male and female germline","volume":"5","author":"AH Peters","year":"1997","journal-title":"Chromosome Res Int J Mol Supramol Evol Asp Chromosome Biol"},{"key":"pgen.1011175.ref092","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1159\/000129818","article-title":"An Air-Drying Method for Meiotic Preparations from Mammalian Testes","volume":"3","author":"EP Evans","year":"1964","journal-title":"Cytogenet Genome Res"},{"key":"pgen.1011175.ref093","doi-asserted-by":"crossref","first-page":"107858","DOI":"10.1016\/j.celrep.2020.107858","article-title":"Cyclin N-Terminal Domain-Containing-1 Coordinates Meiotic Crossover Formation with Cell-Cycle Progression in a Cyclin-Independent Manner","volume":"32","author":"S Gray","year":"2020","journal-title":"Cell Rep"},{"key":"pgen.1011175.ref094","first-page":"2023","article-title":"A TOPBP1 Allele Causing Male Infertility Uncouples XY Silencing Dynamics From Sex Body Formation.","author":"CFR Ascencao","year":"2023","journal-title":"bioRxiv"},{"key":"pgen.1011175.ref095","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1083\/jcb.201607031","article-title":"TOPBP1Dpb11 plays a conserved role in homologous recombination DNA repair through the coordinated recruitment of 53BP1Rad9","volume":"216","author":"Y Liu","year":"2017","journal-title":"J Cell Biol"},{"key":"pgen.1011175.ref096","doi-asserted-by":"crossref","first-page":"e68648","DOI":"10.7554\/eLife.68648","article-title":"Phosphoproteomics of ATR signaling in mouse testes.","volume":"11","author":"JR Sims","year":"2022","journal-title":"eLife"},{"key":"pgen.1011175.ref097","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1002\/pmic.201200439","article-title":"Comet: an open-source MS\/MS sequence database search tool","volume":"13","author":"JK Eng","year":"2013","journal-title":"Proteomics"}],"updated-by":[{"DOI":"10.1371\/journal.pgen.1011175","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,3,1]],"date-time":"2024-03-01T00:00:00Z","timestamp":1709251200000}}],"container-title":["PLOS Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1011175","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,1]],"date-time":"2024-03-01T13:51:05Z","timestamp":1709301065000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1011175"}},"subtitle":[],"editor":[{"given":"Gregory P.","family":"Copenhaver","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2024,2,20]]},"references-count":97,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2024,2,20]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1011175","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.10.06.561296","asserted-by":"object"}]},"ISSN":["1553-7404"],"issn-type":[{"value":"1553-7404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,2,20]]}}}