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R-loop-induced replication defects are sensed and suppressed by ATR kinase, whereas it is not known whether R-loop itself is actively involved in ATR activation and, if so, how this is achieved. Here, we report that the nuclear form of RNA-editing enzyme ADAR1 promotes ATR activation and resolves genome-wide R-loops, a process that requires its double-stranded RNA-binding domains. Mechanistically, ADAR1 interacts with TOPBP1 and facilitates its loading on perturbed replication forks by enhancing the association of TOPBP1 with RAD9 of the 9\u20131-1 complex. When replication is inhibited, DNA\u2013RNA hybrid competes with TOPBP1 for ADAR1 binding to promote the translocation of ADAR1 from damaged fork to accumulate at R-loop region. There, ADAR1 recruits RNA helicases DHX9 and DDX21 to unwind R-loops, simultaneously allowing TOPBP1 to stimulate ATR more efficiently. Collectively, we propose that the tempo-spatially regulated assembly of ADAR1-nucleated protein complexes link R-loop clearance and ATR activation, while R-loops crosstalk with blocked replication forks by transposing ADAR1 to finetune ATR activity and safeguard the genome.<\/jats:p>","DOI":"10.1093\/nar\/gkad839","type":"journal-article","created":{"date-parts":[[2023,10,13]],"date-time":"2023-10-13T11:11:11Z","timestamp":1697195471000},"page":"11668-11687","source":"Crossref","is-referenced-by-count":37,"title":["ADAR1 links R-loop homeostasis to ATR activation in replication stress response"],"prefix":"10.1093","volume":"51","author":[{"given":"Biao","family":"Zhang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Key Laboratory of Breast Cancer Prevention and Therapy (Ministry of Education), Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University , Tianjin 300070 , China"},{"name":"Tianjin Institutes of Health Science, National Clinical Research Center for Blood Diseases, Institute of Hematology and Blood Diseases Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College , Tianjin 300020 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Li","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Key Laboratory of Breast Cancer Prevention and Therapy (Ministry of Education), Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University , Tianjin 300070 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jieyou","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Key Laboratory of Breast Cancer Prevention and Therapy (Ministry of Education), Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University , Tianjin 300070 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuejiao","family":"Wang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Key Laboratory of Breast Cancer Prevention and Therapy (Ministry of Education), Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University , Tianjin 300070 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Can","family":"Liang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Key Laboratory of Breast Cancer Prevention and Therapy (Ministry of Education), Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University , Tianjin 300070 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ting","family":"Lu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Key Laboratory of Breast Cancer Prevention and Therapy (Ministry of Education), Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University , Tianjin 300070 , China"},{"name":"Tianjin Institutes of Health Science, National Clinical Research Center for Blood Diseases, Institute of Hematology and Blood Diseases Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College , Tianjin 300020 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunyong","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell Ecosystem, Key Laboratory of Breast Cancer Prevention and Therapy (Ministry of Education), Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University , Tianjin 300070 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ling","family":"Liu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, Haihe Laboratory of Cell 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(Ministry of Education), Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University , Tianjin 300070 , China"},{"name":"Tianjin Institutes of Health Science, National Clinical Research Center for Blood Diseases, Institute of Hematology and Blood Diseases Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College , Tianjin 300020 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3499-5133","authenticated-orcid":false,"given":"Jia","family":"Yu","sequence":"additional","affiliation":[{"name":"Tianjin Institutes of Health Science, National Clinical Research Center for Blood Diseases, Institute of Hematology and Blood Diseases Hospital, 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Cell Biol."},{"key":"2023112805313515100_B2","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1038\/nrc3916","article-title":"Replication stress and cancer","volume":"15","author":"Gaillard","year":"2015","journal-title":"Nat. Rev. Cancer"},{"key":"2023112805313515100_B3","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.mrfmmm.2017.10.001","article-title":"Replication stress in hematopoietic stem cells in mouse and man","volume":"808","author":"Flach","year":"2018","journal-title":"Mutat. Res."},{"key":"2023112805313515100_B4","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1038\/nature13619","article-title":"Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells","volume":"512","author":"Flach","year":"2014","journal-title":"Nature"},{"key":"2023112805313515100_B5","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1016\/j.cell.2013.10.043","article-title":"ATR prohibits replication catastrophe by preventing global exhaustion of RPA","volume":"155","author":"Toledo","year":"2013","journal-title":"Cell"},{"key":"2023112805313515100_B6","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1038\/nrm.2017.67","article-title":"The essential kinase ATR: ensuring faithful duplication of a challenging genome","volume":"18","author":"Saldivar","year":"2017","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023112805313515100_B7","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1016\/j.cell.2005.12.041","article-title":"TopBP1 activates the ATR-ATRIP complex","volume":"124","author":"Kumagai","year":"2006","journal-title":"Cell"},{"key":"2023112805313515100_B8","doi-asserted-by":"crossref","first-page":"1478","DOI":"10.1101\/gad.1666208","article-title":"TopBP1 activates ATR through ATRIP and a PIKK regulatory domain","volume":"22","author":"Mordes","year":"2008","journal-title":"Genes Dev."},{"key":"2023112805313515100_B9","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1093\/nar\/gkq743","article-title":"Structure and function of the Rad9-binding region of the DNA-damage checkpoint adaptor TopBP1","volume":"39","author":"Rappas","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"2023112805313515100_B10","doi-asserted-by":"crossref","first-page":"10780","DOI":"10.1093\/nar\/gks849","article-title":"Distinct roles for DNA-PK, ATM and ATR in RPA phosphorylation and checkpoint activation in response to replication stress","volume":"40","author":"Liu","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"2023112805313515100_B11","doi-asserted-by":"crossref","first-page":"4070","DOI":"10.1242\/jcs.053702","article-title":"Human RPA phosphorylation by ATR stimulates DNA synthesis and prevents ssDNA accumulation during DNA-replication stress","volume":"122","author":"Vassin","year":"2009","journal-title":"J. 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