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T. brucei regularly switches its major surface antigen, VSG, to evade the host immune response. VSG is expressed exclusively from subtelomeric expression sites, and we have shown that telomere proteins play important roles in the regulation of VSG silencing and switching. In this study, we identify several unique features of TERRA and telomere biology in T. brucei. First, the number of TERRA foci is cell cycle-regulated and influenced by TbTRF, the duplex telomere DNA binding factor in T. brucei. Second, TERRA is transcribed by RNA polymerase I mainly from a single telomere downstream of the active VSG. Third, TbTRF binds TERRA through its C-terminal Myb domain, which also has the duplex DNA binding activity, in a sequence-specific manner and suppresses the TERRA level without affecting its half-life. Finally, levels of the telomeric R-loop and telomere DNA damage were increased upon TbTRF depletion. Overexpression of an ectopic allele of RNase H1 that resolves the R-loop structure in TbTRF RNAi cells can partially suppress these phenotypes, revealing an underlying mechanism of how TbTRF helps maintain telomere integrity.<\/jats:p>","DOI":"10.1093\/nar\/gkab401","type":"journal-article","created":{"date-parts":[[2021,4,29]],"date-time":"2021-04-29T12:57:45Z","timestamp":1619701065000},"page":"5637-5653","source":"Crossref","is-referenced-by-count":28,"title":["<i>Tb<\/i>TRF suppresses the TERRA level and regulates the cell cycle-dependent TERRA foci number with a TERRA binding activity in its C-terminal Myb domain"],"prefix":"10.1093","volume":"49","author":[{"given":"Arpita","family":"Saha","sequence":"first","affiliation":[{"name":"Center for Gene Regulation in Health and Disease, Department of Biological, Geological, and Environmental Sciences, College of Sciences and Health Professions, Cleveland State University, 2121 Euclid Avenue, Cleveland, OH 44115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amit Kumar","family":"Gaurav","sequence":"additional","affiliation":[{"name":"Center for Gene Regulation in Health and Disease, Department of Biological, Geological, and Environmental Sciences, College of Sciences and Health Professions, Cleveland State University, 2121 Euclid Avenue, Cleveland, OH 44115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Unnati M","family":"Pandya","sequence":"additional","affiliation":[{"name":"Center for Gene Regulation in Health and Disease, Department of Biological, Geological, and Environmental Sciences, College of Sciences and Health Professions, Cleveland State University, 2121 Euclid Avenue, Cleveland, OH 44115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marjia","family":"Afrin","sequence":"additional","affiliation":[{"name":"Center for Gene Regulation in Health and Disease, Department of Biological, Geological, and Environmental Sciences, College of Sciences and Health Professions, Cleveland State University, 2121 Euclid Avenue, Cleveland, OH 44115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ranjodh","family":"Sandhu","sequence":"additional","affiliation":[{"name":"Center for Gene Regulation in Health and Disease, Department of Biological, Geological, and Environmental Sciences, College of Sciences and Health Professions, Cleveland State University, 2121 Euclid Avenue, Cleveland, OH 44115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vishal","family":"Nanavaty","sequence":"additional","affiliation":[{"name":"Center for Gene Regulation in Health and Disease, Department of Biological, Geological, and Environmental Sciences, College of Sciences and Health Professions, Cleveland State University, 2121 Euclid Avenue, Cleveland, OH 44115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brittny","family":"Schnur","sequence":"additional","affiliation":[{"name":"Center for Gene Regulation in Health and Disease, Department of Biological, Geological, and Environmental Sciences, College of Sciences and Health Professions, Cleveland State University, 2121 Euclid Avenue, Cleveland, OH 44115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5804-9876","authenticated-orcid":false,"given":"Bibo","family":"Li","sequence":"additional","affiliation":[{"name":"Center for Gene Regulation in Health and Disease, Department of Biological, Geological, and Environmental Sciences, College of Sciences and Health Professions, Cleveland State University, 2121 Euclid Avenue, Cleveland, OH 44115, USA"},{"name":"Case Comprehensive Cancer Center, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44106, USA"},{"name":"Department of Inflammation and Immunity, Lerner Research Institute, Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, USA"},{"name":"Center for RNA Science and Therapeutics, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44106, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,5,28]]},"reference":[{"key":"2021070812113839500_B1","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1146\/annurev-genet-032918-021921","article-title":"Shelterin-mediated telomere protection","volume":"52","author":"de\u00a0Lange","year":"2018","journal-title":"Annu. 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Biol."},{"key":"2021070812113839500_B82","doi-asserted-by":"crossref","first-page":"1635","DOI":"10.1016\/S0960-9822(02)01179-X","article-title":"DNA ligase IV-dependent NHEJ of deprotected mammalian telomeres in G1 and G2","volume":"12","author":"Smogorzewska","year":"2002","journal-title":"Curr. 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