{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T04:43:58Z","timestamp":1790052238044,"version":"4.0.1"},"reference-count":116,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2018,12,13]],"date-time":"2018-12-13T00:00:00Z","timestamp":1544659200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/K006495\/1"],"award-info":[{"award-number":["BB\/K006495\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/M028909\/1"],"award-info":[{"award-number":["BB\/M028909\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/N016165\/1"],"award-info":[{"award-number":["BB\/N016165\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004440","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["104111"],"award-info":[{"award-number":["104111"]}],"id":[{"id":"10.13039\/100004440","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"DOI":"10.1371\/journal.pgen.1007729","type":"journal-article","created":{"date-parts":[[2018,12,13]],"date-time":"2018-12-13T13:26:28Z","timestamp":1544707588000},"page":"e1007729","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":52,"title":["Ribonuclease H1-targeted R-loops in surface antigen gene expression sites can direct trypanosome immune evasion"],"prefix":"10.1371","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6740-8882","authenticated-orcid":true,"given":"Emma","family":"Briggs","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9310-4762","authenticated-orcid":true,"given":"Kathryn","family":"Crouch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2832-6806","authenticated-orcid":true,"given":"Leandro","family":"Lemgruber","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Craig","family":"Lapsley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5739-976X","authenticated-orcid":true,"given":"Richard","family":"McCulloch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2018,12,13]]},"reference":[{"issue":"6","key":"ref1","article-title":"Programmed Genome Rearrangements in Tetrahymena","volume":"2","author":"MC Yao","year":"2014","journal-title":"Microbiology spectrum"},{"issue":"9","key":"ref2","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1016\/j.pt.2014.07.002","article-title":"Parasexuality and mosaic aneuploidy in Leishmania: alternative genetics","volume":"30","author":"Y Sterkers","year":"2014","journal-title":"Trends in parasitology"},{"issue":"5","key":"ref3","doi-asserted-by":"crossref","first-page":"e1001868","DOI":"10.1371\/journal.pbio.1001868","article-title":"Genome-wide stochastic adaptive DNA amplification at direct and inverted DNA repeats in the parasite Leishmania","volume":"12","author":"JM Ubeda","year":"2014","journal-title":"PLoS biology"},{"issue":"2","key":"ref4","article-title":"Mating-type Gene Switching in Saccharomyces cerevisiae","volume":"3","author":"CS Lee","year":"2015","journal-title":"Microbiology spectrum"},{"issue":"5","key":"ref5","article-title":"A Unique DNA Recombination Mechanism of the Mating\/Cell-type Switching of Fission Yeasts: a Review","volume":"2","author":"AJ Klar","year":"2014","journal-title":"Microbiology spectrum"},{"issue":"6","key":"ref6","article-title":"V(D)J Recombination: Mechanism, Errors, and Fidelity","volume":"2","author":"DB Roth","year":"2014","journal-title":"Microbiology spectrum"},{"issue":"1","key":"ref7","article-title":"Related Mechanisms of Antibody Somatic Hypermutation and Class Switch Recombination","volume":"3","author":"JK Hwang","year":"2015","journal-title":"Microbiology spectrum"},{"issue":"7","key":"ref8","first-page":"493","article-title":"Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens","volume":"7","author":"KW Deitsch","year":"2009","journal-title":"NatRevMicrobiol"},{"issue":"9","key":"ref9","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1016\/j.pt.2007.07.008","article-title":"Gene conversion is a convergent strategy for pathogen antigenic variation","volume":"23","author":"GH Palmer","year":"2007","journal-title":"Trends Parasitol"},{"issue":"5","key":"ref10","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1111\/j.1574-6976.2011.00321.x","article-title":"Microbial antigenic variation mediated by homologous DNA recombination","volume":"36","author":"C Vink","year":"2012","journal-title":"FEMS microbiology reviews"},{"issue":"1","key":"ref11","doi-asserted-by":"crossref","DOI":"10.1128\/microbiolspec.MDNA3-0015-2014","article-title":"Mobile DNA in the Pathogenic Neisseria","volume":"3","author":"KP Obergfell","year":"2015","journal-title":"Microbiology spectrum"},{"issue":"1","key":"ref12","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.gene.2014.09.047","article-title":"Mono-allelic VSG expression by RNA polymerase I in Trypanosoma brucei: expression site control from both ends?","volume":"556","author":"A Gunzl","year":"2015","journal-title":"Gene"},{"issue":"12","key":"ref13","doi-asserted-by":"crossref","first-page":"1984","DOI":"10.1111\/cmi.12215","article-title":"Antigenic variation in African trypanosomes: the importance of chromosomal and nuclear context in VSG expression control","volume":"15","author":"L Glover","year":"2013","journal-title":"Cellular microbiology"},{"issue":"10","key":"ref14","doi-asserted-by":"crossref","first-page":"e3527","DOI":"10.1371\/journal.pone.0003527","article-title":"Telomeric expression sites are highly conserved in Trypanosoma brucei","volume":"3","author":"C Hertz-Fowler","year":"2008","journal-title":"PLoS ONE"},{"issue":"5","key":"ref15","doi-asserted-by":"crossref","first-page":"e1005994","DOI":"10.1371\/journal.pgen.1005994","article-title":"A Conserved DNA Repeat Promotes Selection of a Diverse Repertoire of Trypanosoma brucei Surface Antigens from the Genomic Archive","volume":"12","author":"G Hovel-Miner","year":"2016","journal-title":"PLoS genetics"},{"issue":"1","key":"ref16","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.molbiopara.2014.06.004","article-title":"Capturing the variant surface glycoprotein repertoire (the VSGnome) of Trypanosoma brucei Lister 427","volume":"195","author":"GA Cross","year":"2014","journal-title":"Molecular and biochemical parasitology"},{"issue":"9","key":"ref17","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1101\/gr.6421207","article-title":"Analysis of the VSG gene silent archive in Trypanosoma brucei reveals that mosaic gene expression is prominent in antigenic variation and is favored by archive substructure","volume":"17","author":"L Marcello","year":"2007","journal-title":"Genome Res"},{"issue":"26","key":"ref18","doi-asserted-by":"crossref","first-page":"7225","DOI":"10.1073\/pnas.1600344113","article-title":"VEX1 controls the allelic exclusion required for antigenic variation in trypanosomes","volume":"113","author":"L Glover","year":"2016","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"e02324","DOI":"10.7554\/eLife.02324","article-title":"Expression site attenuation mechanistically links antigenic variation and development in Trypanosoma brucei","volume":"3","author":"C Batram","year":"2014","journal-title":"eLife"},{"issue":"7","key":"ref20","doi-asserted-by":"crossref","first-page":"e161","DOI":"10.1371\/journal.pbio.0060161","article-title":"A histone methyltransferase modulates antigenic variation in African trypanosomes","volume":"6","author":"LM Figueiredo","year":"2008","journal-title":"PLoS Biol"},{"issue":"21","key":"ref21","doi-asserted-by":"crossref","first-page":"E2803","DOI":"10.1073\/pnas.1501206112","article-title":"Inositol phosphate pathway controls transcription of telomeric expression sites in trypanosomes","volume":"112","author":"I Cestari","year":"2015","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"2","key":"ref22","doi-asserted-by":"crossref","DOI":"10.1128\/microbiolspec.MDNA3-0016-2014","article-title":"DNA Recombination Strategies During Antigenic Variation in the African Trypanosome","volume":"3","author":"R McCulloch","year":"2015","journal-title":"Microbiology spectrum"},{"issue":"7244","key":"ref23","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1038\/nature07982","article-title":"A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei","volume":"459","author":"CE Boothroyd","year":"2009","journal-title":"Nature"},{"issue":"3","key":"ref24","doi-asserted-by":"crossref","first-page":"e1003260","DOI":"10.1371\/journal.ppat.1003260","article-title":"DNA break site at fragile subtelomeres determines probability and mechanism of antigenic variation in African trypanosomes","volume":"9","author":"L Glover","year":"2013","journal-title":"PLoS pathogens"},{"issue":"7","key":"ref25","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1038\/cr.2014.60","article-title":"Trypanosoma brucei TIF2 suppresses VSG switching by maintaining subtelomere integrity","volume":"24","author":"SE Jehi","year":"2014","journal-title":"Cell research"},{"key":"ref26","article-title":"Trypanosoma brucei RAP1 maintains telomere and subtelomere integrity by suppressing TERRA and telomeric RNA:DNA hybrids","author":"V Nanavaty","year":"2017","journal-title":"Nucleic Acids Res"},{"issue":"8","key":"ref27","doi-asserted-by":"crossref","first-page":"e1002900","DOI":"10.1371\/journal.ppat.1002900","article-title":"Telomere Length Affects the Frequency and Mechanism of Antigenic Variation in Trypanosoma brucei","volume":"8","author":"GA Hovel-Miner","year":"2012","journal-title":"PLoS Pathog"},{"key":"ref28","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.12765","article-title":"Mapping replication dynamics in Trypanosoma brucei reveals a link with telomere transcription and antigenic variation","volume":"5","author":"R Devlin","year":"2016","journal-title":"eLife"},{"key":"ref29","article-title":"Does DNA replication direct locus-specific recombination during host immune evasion by antigenic variation in the African trypanosome?","author":"R Devlin","year":"2016","journal-title":"Current genetics"},{"issue":"10","key":"ref30","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/nrg3961","article-title":"R loops: new modulators of genome dynamics and function","volume":"16","author":"JM Santos-Pereira","year":"2015","journal-title":"Nature reviews Genetics"},{"issue":"18","key":"ref31","doi-asserted-by":"crossref","first-page":"5779","DOI":"10.1073\/pnas.1501769112","article-title":"Role for RNA:DNA hybrids in origin-independent replication priming in a eukaryotic system","volume":"112","author":"R Stuckey","year":"2015","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"158","DOI":"10.3389\/fgene.2015.00158","article-title":"R-loops and initiation of DNA replication in human cells: a missing link?","volume":"6","author":"R Lombrana","year":"2015","journal-title":"Frontiers in genetics"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"15025","DOI":"10.1038\/ncomms15025","article-title":"PIF1 family DNA helicases suppress R-loop mediated genome instability at tRNA genes","volume":"8","author":"PLT Tran","year":"2017","journal-title":"Nature communications"},{"issue":"11","key":"ref34","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1038\/nsmb.3078","article-title":"TERRA and the state of the telomere","volume":"22","author":"K Rippe","year":"2015","journal-title":"Nature structural & molecular biology"},{"issue":"12","key":"ref35","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1016\/j.tig.2016.10.002","article-title":"Nascent Connections: R-Loops and Chromatin Patterning","volume":"32","author":"F. Chedin","year":"2016","journal-title":"Trends in genetics: TIG"},{"issue":"2","key":"ref36","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1016\/j.molcel.2016.11.030","article-title":"RPA Interacts with HIRA and Regulates H3.3 Deposition at Gene Regulatory Elements in Mammalian Cells","volume":"65","author":"H Zhang","year":"2017","journal-title":"Molecular cell"},{"key":"ref37","article-title":"Canonical DNA Repair Pathways Influence R-Loop-Driven Genome Instability","author":"PC Stirling","year":"2016","journal-title":"Journal of molecular biology"},{"key":"ref38","article-title":"Breaking bad: R-loops and genome integrity","author":"J Sollier","year":"2015","journal-title":"Trends in cell biology"},{"issue":"2","key":"ref39","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.molcel.2012.04.009","article-title":"R loops: from transcription byproducts to threats to genome stability","volume":"46","author":"A Aguilera","year":"2012","journal-title":"Molecular cell"},{"issue":"24","key":"ref40","doi-asserted-by":"crossref","first-page":"5006","DOI":"10.1093\/nar\/23.24.5006","article-title":"RNA:DNA complex formation upon transcription of immunoglobulin switch regions: implications for the mechanism and regulation of class switch recombination","volume":"23","author":"GA Daniels","year":"1995","journal-title":"Nucleic Acids Res"},{"issue":"5","key":"ref41","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1038\/ni919","article-title":"R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells","volume":"4","author":"K Yu","year":"2003","journal-title":"Nat Immunol"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/B978-0-12-800267-4.00001-8","article-title":"Regulation of immunoglobulin class-switch recombination: choreography of noncoding transcription, targeted DNA deamination, and long-range DNA repair","volume":"122","author":"AJ Matthews","year":"2014","journal-title":"Adv Immunol"},{"issue":"9","key":"ref43","doi-asserted-by":"crossref","first-page":"1405","DOI":"10.1101\/gr.237362.118","article-title":"Human proteins that interact with RNA\/DNA hybrids","volume":"28","author":"IX Wang","year":"2018","journal-title":"Genome research"},{"issue":"6","key":"ref44","doi-asserted-by":"crossref","first-page":"1891","DOI":"10.1016\/j.celrep.2018.04.025","article-title":"RNA\/DNA Hybrid Interactome Identifies DXH9 as a Molecular Player in Transcriptional Termination and R-Loop-Associated DNA Damage","volume":"23","author":"A Cristini","year":"2018","journal-title":"Cell reports"},{"issue":"6","key":"ref45","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1111\/j.1742-4658.2009.06908.x","article-title":"Ribonuclease H: the enzymes in eukaryotes","volume":"276","author":"SM Cerritelli","year":"2009","journal-title":"The FEBS journal"},{"issue":"1","key":"ref46","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/S0166-6851(00)00182-1","article-title":"Trypanosoma brucei RNase HI requires its divergent spacer subdomain for enzymatic function and its conserved RNA binding motif for nuclear localization","volume":"107","author":"JH Kobil","year":"2000","journal-title":"Molecular and biochemical parasitology"},{"issue":"3","key":"ref47","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1016\/S1097-2765(03)00088-1","article-title":"Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice","volume":"11","author":"SM Cerritelli","year":"2003","journal-title":"Molecular cell"},{"issue":"10","key":"ref48","doi-asserted-by":"crossref","first-page":"e1004716","DOI":"10.1371\/journal.pgen.1004716","article-title":"Genome-wide distribution of RNA-DNA hybrids identifies RNase H targets in tRNA genes, retrotransposons and mitochondria","volume":"10","author":"A El Hage","year":"2014","journal-title":"PLoS genetics"},{"issue":"1","key":"ref49","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1186\/s12864-016-3154-8","article-title":"High-resolution analysis of multi-copy variant surface glycoprotein gene expression sites in African trypanosomes","volume":"17","author":"S Hutchinson","year":"2016","journal-title":"BMC Genomics"},{"issue":"6","key":"ref50","doi-asserted-by":"crossref","first-page":"1063","DOI":"10.1101\/gr.219394.116","article-title":"RNA-DNA hybrid (R-loop) immunoprecipitation mapping: an analytical workflow to evaluate inherent biases","volume":"27","author":"L Halasz","year":"2017","journal-title":"Genome research"},{"issue":"4","key":"ref51","doi-asserted-by":"crossref","first-page":"e1004288","DOI":"10.1371\/journal.pgen.1004288","article-title":"Genome-wide profiling of yeast DNA:RNA hybrid prone sites with DRIP-chip","volume":"10","author":"YA Chan","year":"2014","journal-title":"PLoS genetics"},{"issue":"2","key":"ref52","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.devcel.2014.05.013","article-title":"Roles for Pbp1 and caloric restriction in genome and lifespan maintenance via suppression of RNA-DNA hybrids","volume":"30","author":"JS Salvi","year":"2014","journal-title":"Dev Cell"},{"key":"ref53","article-title":"Genome-wide mapping reveals conserved and diverged R-loop activities in the unusual genetic landscape of the African trypanosome genome","author":"E Briggs","year":"2018","journal-title":"Nucleic Acids Research"},{"issue":"3","key":"ref54","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1093\/nar\/gkl1100","article-title":"Deletion of a trypanosome telomere leads to loss of silencing and progressive loss of terminal DNA in the absence of cell cycle arrest","volume":"35","author":"L Glover","year":"2007","journal-title":"Nucleic Acids Res"},{"issue":"7","key":"ref55","doi-asserted-by":"crossref","first-page":"3131","DOI":"10.1093\/nar\/gkv1459","article-title":"A transcription-independent epigenetic mechanism is associated with antigenic switching in Trypanosoma brucei","volume":"44","author":"F Aresta-Branco","year":"2016","journal-title":"Nucleic Acids Res"},{"issue":"19","key":"ref56","doi-asserted-by":"crossref","first-page":"2041","DOI":"10.1101\/gad.17010011","article-title":"R-loop-mediated genomic instability is caused by impairment of replication fork progression","volume":"25","author":"W Gan","year":"2011","journal-title":"Genes & development"},{"issue":"6","key":"ref57","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1016\/j.molcel.2011.10.013","article-title":"Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes","volume":"44","author":"A Helmrich","year":"2011","journal-title":"Molecular cell"},{"issue":"11","key":"ref58","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1038\/ncb1984","article-title":"Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription","volume":"11","author":"S Tuduri","year":"2009","journal-title":"Nature cell biology"},{"issue":"15","key":"ref59","doi-asserted-by":"crossref","first-page":"3106","DOI":"10.1038\/emboj.2011.206","article-title":"Genome-wide function of THO\/TREX in active genes prevents R-loop-dependent replication obstacles","volume":"30","author":"B Gomez-Gonzalez","year":"2011","journal-title":"The EMBO journal"},{"issue":"22","key":"ref60","doi-asserted-by":"crossref","first-page":"2445","DOI":"10.1101\/gad.229880.113","article-title":"The Npl3 hnRNP prevents R-loop-mediated transcription-replication conflicts and genome instability","volume":"27","author":"JM Santos-Pereira","year":"2013","journal-title":"Genes & development"},{"key":"ref61","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.17548","article-title":"Co-transcriptional R-loops are the main cause of estrogen-induced DNA damage","volume":"5","author":"CT Stork","year":"2016","journal-title":"eLife"},{"issue":"3","key":"ref62","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1016\/j.molcel.2003.08.010","article-title":"Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination","volume":"12","author":"P Huertas","year":"2003","journal-title":"Molecular cell"},{"issue":"1","key":"ref63","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.molcel.2010.12.007","article-title":"Yeast Sen1 helicase protects the genome from transcription-associated instability","volume":"41","author":"HE Mischo","year":"2011","journal-title":"Molecular cell"},{"issue":"5","key":"ref64","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1038\/nsmb.3395","article-title":"DNA-RNA hybrids: the risks of DNA breakage during transcription","volume":"24","author":"A Aguilera","year":"2017","journal-title":"Nature structural & molecular biology"},{"issue":"1","key":"ref65","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1128\/MCB.00897-09","article-title":"Competition between the RNA transcript and the nontemplate DNA strand during R-loop formation in vitro: a nick can serve as a strong R-loop initiation site","volume":"30","author":"D Roy","year":"2010","journal-title":"Molecular and cellular biology"},{"issue":"8","key":"ref66","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1038\/embor.2009.97","article-title":"Ataxia telangiectasia mutated activation by transcription- and topoisomerase I-induced DNA double-strand breaks","volume":"10","author":"O Sordet","year":"2009","journal-title":"EMBO reports"},{"issue":"5","key":"ref67","doi-asserted-by":"crossref","first-page":"e1004318","DOI":"10.1371\/journal.pgen.1004318","article-title":"R-loops associated with triplet repeat expansions promote gene silencing in Friedreich ataxia and fragile X syndrome","volume":"10","author":"M Groh","year":"2014","journal-title":"PLoS genetics"},{"issue":"14","key":"ref68","doi-asserted-by":"crossref","first-page":"9047","DOI":"10.1093\/nar\/gku601","article-title":"DNA damage triggers SAF-A and RNA biogenesis factors exclusion from chromatin coupled to R-loops removal","volume":"42","author":"S Britton","year":"2014","journal-title":"Nucleic Acids Res"},{"issue":"22","key":"ref69","doi-asserted-by":"crossref","first-page":"2794","DOI":"10.1128\/MCB.00415-16","article-title":"DEAD Box 1 Facilitates Removal of RNA and Homologous Recombination at DNA Double-Strand Breaks","volume":"36","author":"L Li","year":"2016","journal-title":"Molecular and cellular biology"},{"issue":"4","key":"ref70","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1016\/j.cell.2016.10.001","article-title":"Transient RNA-DNA Hybrids Are Required for Efficient Double-Strand Break Repair","volume":"167","author":"C Ohle","year":"2016","journal-title":"Cell"},{"issue":"1","key":"ref71","first-page":"78","article-title":"Trypanosomal histone gammaH2A and the DNA damage response","volume":"183","author":"L Glover","year":"2012","journal-title":"MolBiochemParasitol"},{"issue":"6","key":"ref72","doi-asserted-by":"crossref","first-page":"1054","DOI":"10.1111\/mmi.13441","article-title":"Functional compartmentalization of Rad9 and Hus1 reveals diverse assembly of the 9-1-1 complex components during the DNA damage response in Leishmania","volume":"101","author":"JD Damasceno","year":"2016","journal-title":"Molecular microbiology"},{"issue":"2","key":"ref73","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.molbiopara.2008.04.004","article-title":"Analysis of the Trypanosoma brucei cell cycle by quantitative DAPI imaging","volume":"160","author":"TN Siegel","year":"2008","journal-title":"Molecular and biochemical parasitology"},{"issue":"24","key":"ref74","doi-asserted-by":"crossref","first-page":"8716","DOI":"10.1073\/pnas.0501886102","article-title":"Variant surface glycoprotein RNA interference triggers a precytokinesis cell cycle arrest in African trypanosomes","volume":"102","author":"K Sheader","year":"2005","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"2","key":"ref75","first-page":"163","article-title":"The 5' flanking sequence of a Trypanosoma brucei variable surface glycoprotein gene","volume":"24","author":"JS Shah","year":"1987","journal-title":"MolBiochemParasitol"},{"issue":"28","key":"ref76","first-page":"16784","article-title":"TTA.TAA triplet repeats in plasmids form a non-H bonded structure","volume":"271","author":"K Ohshima","year":"1996","journal-title":"JBiolChem"},{"issue":"12","key":"ref77","doi-asserted-by":"crossref","first-page":"e14271","DOI":"10.1371\/journal.pone.0014271","article-title":"Transcription of AAT*ATT triplet repeats in Escherichia coli is silenced by H-NS and IS1E transposition","volume":"5","author":"X Pan","year":"2010","journal-title":"PLoS One"},{"issue":"6","key":"ref78","first-page":"1608","article-title":"VSG switching in Trypanosoma brucei: antigenic variation analysed using RNAi in the absence of immune selection","volume":"57","author":"N Aitcheson","year":"2005","journal-title":"MolMicrobiol"},{"issue":"21","key":"ref79","doi-asserted-by":"crossref","first-page":"2875","DOI":"10.1101\/gad.13.21.2875","article-title":"A role for RAD51 and homologous recombination in Trypanosoma brucei antigenic variation","volume":"13","author":"R McCulloch","year":"1999","journal-title":"Genes & development"},{"issue":"2","key":"ref80","first-page":"434","article-title":"Interactions among Trypanosoma brucei RAD51 paralogues in DNA repair and antigenic variation","volume":"81","author":"R Dobson","year":"2011","journal-title":"MolMicrobiol"},{"issue":"5","key":"ref81","first-page":"1237","article-title":"Trypanosoma brucei BRCA2 acts in antigenic variation and has undergone a recent expansion in BRC repeat number that is important during homologous recombination","volume":"68","author":"CL Hartley","year":"2008","journal-title":"MolMicrobiol"},{"issue":"14","key":"ref82","first-page":"13363","article-title":"Bloodstream form-specific up-regulation of silent vsg expression sites and procyclin in Trypanosoma brucei after inhibition of DNA synthesis or DNA damage","volume":"279","author":"K Sheader","year":"2004","journal-title":"JBiolChem"},{"issue":"5","key":"ref83","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1038\/ni920","article-title":"Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand","volume":"4","author":"AR Ramiro","year":"2003","journal-title":"Nat Immunol"},{"issue":"6933","key":"ref84","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1038\/nature01574","article-title":"Transcription-targeted DNA deamination by the AID antibody diversification enzyme","volume":"422","author":"J Chaudhuri","year":"2003","journal-title":"Nature"},{"issue":"4","key":"ref85","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1016\/j.cell.2015.03.020","article-title":"Non-coding RNA Generated following Lariat Debranching Mediates Targeting of AID to DNA","volume":"161","author":"S Zheng","year":"2015","journal-title":"Cell"},{"issue":"20","key":"ref86","doi-asserted-by":"crossref","first-page":"7704","DOI":"10.1073\/pnas.85.20.7704","article-title":"Immunoglobulin heavy-chain switching may be directed by prior induction of transcripts from constant-region genes","volume":"85","author":"J Stavnezer","year":"1988","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"2","key":"ref87","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1016\/j.celrep.2014.06.021","article-title":"The strength of an Ig switch region is determined by its ability to drive R loop formation and its number of WGCW sites","volume":"8","author":"ZZ Zhang","year":"2014","journal-title":"Cell reports"},{"issue":"6306","key":"ref88","article-title":"RNA G-quadruplexes are globally unfolded in eukaryotic cells and depleted in bacteria","volume":"353","author":"JU Guo","year":"2016","journal-title":"Science"},{"issue":"5733","key":"ref89","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1126\/science.1112642","article-title":"The genome of the African trypanosome Trypanosoma brucei","volume":"309","author":"M Berriman","year":"2005","journal-title":"Science"},{"issue":"7509","key":"ref90","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1038\/nature13374","article-title":"BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2","volume":"511","author":"V Bhatia","year":"2014","journal-title":"Nature"},{"issue":"7","key":"ref91","doi-asserted-by":"crossref","DOI":"10.3390\/genes8070171","article-title":"The Role of Replication-Associated Repair Factors on R-Loops","volume":"8","author":"V Bhatia","year":"2017","journal-title":"Genes (Basel)"},{"issue":"4","key":"ref92","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.molcel.2013.10.006","article-title":"R loops are linked to histone H3 S10 phosphorylation and chromatin condensation","volume":"52","author":"M Castellano-Pozo","year":"2013","journal-title":"Molecular cell"},{"issue":"5","key":"ref93","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/j.molcel.2017.05.014","article-title":"Histone Mutants Separate R Loop Formation from Genome Instability Induction","volume":"66","author":"D Garcia-Pichardo","year":"2017","journal-title":"Molecular cell"},{"issue":"4","key":"ref94","doi-asserted-by":"crossref","first-page":"650","DOI":"10.1016\/j.molcel.2018.04.001","article-title":"RNA Helicase DDX1 Converts RNA G-Quadruplex Structures into R-Loops to Promote IgH Class Switch Recombination","volume":"70","author":"C Ribeiro de Almeida","year":"2018","journal-title":"Molecular cell"},{"issue":"11","key":"ref95","doi-asserted-by":"crossref","first-page":"2927","DOI":"10.1016\/j.celrep.2016.11.041","article-title":"DNA Replication Origins in Immunoglobulin Switch Regions Regulate Class Switch Recombination in an R-Loop-Dependent Manner","volume":"17","author":"EM Wiedemann","year":"2016","journal-title":"Cell reports"},{"issue":"7","key":"ref96","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1101\/gad.234070.113","article-title":"The yeast and human FACT chromatin-reorganizing complexes solve R-loop-mediated transcription-replication conflicts","volume":"28","author":"E Herrera-Moyano","year":"2014","journal-title":"Genes & development"},{"issue":"4","key":"ref97","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.cell.2017.07.043","article-title":"Transcription-Replication Conflict Orientation Modulates R-Loop Levels and Activates Distinct DNA Damage Responses","volume":"170","author":"S Hamperl","year":"2017","journal-title":"Cell"},{"key":"ref98","doi-asserted-by":"crossref","first-page":"e00505","DOI":"10.7554\/eLife.00505","article-title":"The homologous recombination machinery modulates the formation of RNA-DNA hybrids and associated chromosome instability","volume":"2","author":"L Wahba","year":"2013","journal-title":"eLife"},{"key":"ref99","article-title":"RECQ-like helicases Sgs1 and BLM regulate R-loop-associated genome instability","author":"EY Chang","year":"2017","journal-title":"The Journal of cell biology"},{"key":"ref100","first-page":"5","article-title":"RNase H enables efficient repair of R-loop induced DNA damage","author":"JD Amon","year":"2016","journal-title":"eLife"},{"key":"ref101","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-308X(01)49037-3","article-title":"Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite","volume":"49","author":"JD Barry","year":"2001","journal-title":"Advances in parasitology"},{"issue":"7","key":"ref102","doi-asserted-by":"crossref","first-page":"e1000992","DOI":"10.1371\/journal.ppat.1000992","article-title":"TOPO3alpha influences antigenic variation by monitoring expression-site-associated VSG switching in Trypanosoma brucei","volume":"6","author":"HS Kim","year":"2010","journal-title":"PLoS Pathog"},{"issue":"2","key":"ref103","first-page":"833","article-title":"Gene conversions mediating antigenic variation in Trypanosoma brucei can occur in variant surface glycoprotein expression sites lacking 70- base-pair repeat sequences","volume":"17","author":"R McCulloch","year":"1997","journal-title":"MolCell Biol"},{"issue":"1","key":"ref104","doi-asserted-by":"crossref","first-page":"e1003074","DOI":"10.1371\/journal.ppat.1003074","article-title":"Transcription of a cis-acting, noncoding, small RNA is required for pilin antigenic variation in Neisseria gonorrhoeae","volume":"9","author":"LA Cahoon","year":"2013","journal-title":"PLoS pathogens"},{"issue":"5941","key":"ref105","doi-asserted-by":"crossref","first-page":"764","DOI":"10.1126\/science.1175653","article-title":"An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae","volume":"325","author":"LA Cahoon","year":"2009","journal-title":"Science"},{"issue":"Pt 5","key":"ref106","doi-asserted-by":"crossref","first-page":"1124","DOI":"10.1099\/mic.0.000061","article-title":"pilS loci in Neisseria gonorrhoeae are transcriptionally active","volume":"161","author":"J Wachter","year":"2015","journal-title":"Microbiology"},{"issue":"7518","key":"ref107","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/nature13468","article-title":"Exonuclease-mediated degradation of nascent RNA silences genes linked to severe malaria","volume":"513","author":"Q Zhang","year":"2014","journal-title":"Nature"},{"issue":"9","key":"ref108","doi-asserted-by":"crossref","first-page":"E982","DOI":"10.1073\/pnas.1420855112","article-title":"Antisense long noncoding RNAs regulate var gene activation in the malaria parasite Plasmodium falciparum","volume":"112","author":"I Amit-Avraham","year":"2015","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"20","key":"ref109","first-page":"9710","article-title":"Trans-acting GC-rich non-coding RNA at var expression site modulates gene counting in malaria parasite","volume":"44","author":"J Guizetti","year":"2016","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"ref110","first-page":"76","article-title":"Single-locus targeting constructs for reliable regulated RNAi and transgene expression in Trypanosoma brucei","volume":"161","author":"S Alsford","year":"2008","journal-title":"MolBiochemParasitol"},{"issue":"4","key":"ref111","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"KJ Livak","year":"2001","journal-title":"Methods"},{"issue":"4","key":"ref112","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"B Langmead","year":"2012","journal-title":"Nature methods"},{"issue":"16","key":"ref113","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"H Li","year":"2009","journal-title":"Bioinformatics"},{"issue":"1","key":"ref114","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nbt.1754","article-title":"Integrative genomics viewer","volume":"29","author":"JT Robinson","year":"2011","journal-title":"Nat Biotechnol"},{"key":"ref115","doi-asserted-by":"crossref","first-page":"W187","DOI":"10.1093\/nar\/gku365","article-title":"deepTools: a flexible platform for exploring deep-sequencing data","volume":"42","author":"F Ramirez","year":"2014","journal-title":"Nucleic Acids Res"},{"issue":"9","key":"ref116","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1038\/nprot.2016.095","article-title":"Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown","volume":"11","author":"M Pertea","year":"2016","journal-title":"Nature protocols"}],"container-title":["PLOS Genetics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pgen.1007729","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,8]],"date-time":"2022-09-08T01:14:46Z","timestamp":1662599686000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1007729"}},"subtitle":[],"editor":[{"given":"Nancy","family":"Maizels","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2018,12,13]]},"references-count":116,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2018,12,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1007729","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/361451","asserted-by":"object"}]},"ISSN":["1553-7404"],"issn-type":[{"value":"1553-7404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,12,13]]}}}