{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,21]],"date-time":"2026-05-21T06:40:43Z","timestamp":1779345643441,"version":"3.51.4"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"17","license":[{"start":{"date-parts":[[2004,8,5]],"date-time":"2004-08-05T00:00:00Z","timestamp":1091664000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2004,8,5]],"date-time":"2004-08-05T00:00:00Z","timestamp":1091664000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["EMBO J"],"published-print":{"date-parts":[[2004,9,1]]},"DOI":"10.1038\/sj.emboj.7600353","type":"journal-article","created":{"date-parts":[[2004,8,5]],"date-time":"2004-08-05T11:23:22Z","timestamp":1091705002000},"page":"3548-3558","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":51,"title":["Mutation of the mouse Rad17 gene leads to embryonic lethality and reveals a role in DNA damage\u2010dependent recombination"],"prefix":"10.1038","volume":"23","author":[{"given":"Magda","family":"Budzowska","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Iris","family":"Jaspers","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeroen","family":"Essers","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Harm","family":"de Waard","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ellen","family":"van Drunen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katsuhiro","family":"Hanada","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Berna","family":"Beverloo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rudolf W","family":"Hendriks","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Annelies","family":"de Klein","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roland","family":"Kanaar","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jan H","family":"Hoeijmakers","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alex","family":"Maas","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2004,8,5]]},"reference":[{"key":"BFEMBJ7600353_CR1","doi-asserted-by":"crossref","first-page":"6137","DOI":"10.1093\/emboj\/cdg580","volume":"22","author":"J Abraham","year":"2003","unstructured":"Abraham J, Lemmers B, Hande MP, Moynahan ME, Chahwan C, Ciccia A, Essers J, Hanada K, Chahwan R, Khaw AK, McPherson P, Shehabeldin A, Laister R, Arrowsmith C, Kanaar R, West SC, Jasin M, Hakem R (2003) Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J 22: 6137\u20136147","journal-title":"EMBO J"},{"key":"BFEMBJ7600353_CR2","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/S0960-9822(98)70061-2","volume":"8","author":"MI Aladjem","year":"1998","unstructured":"Aladjem MI, Spike BT, Rodewald LW, Hope TJ, Klemm M, Jaenisch R, Wahl GM (1998) ES cells do not activate p53\u2010dependent stress responses and undergo p53\u2010independent apoptosis in response to DNA damage. Curr Biol 8: 145\u2013155","journal-title":"Curr Biol"},{"key":"BFEMBJ7600353_CR3","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1002\/j.1460-2075.1992.tb05179.x","volume":"11","author":"F al\u2010Khodairy","year":"1992","unstructured":"al\u2010Khodairy F, Carr AM (1992) DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe. EMBO J 11: 1343\u20131350","journal-title":"EMBO J"},{"key":"BFEMBJ7600353_CR4","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1101\/gad.1007902","volume":"16","author":"CF Bender","year":"2002","unstructured":"Bender CF, Sikes ML, Sullivan R, Huye LE, Le Beau MM, Roth DB, Mirzoeva OK, Oltz EM, Petrini JH (2002) Cancer predisposition and hematopoietic failure in Rad50(S\/S) mice. Genes Dev 16: 2237\u20132251","journal-title":"Genes Dev"},{"key":"BFEMBJ7600353_CR5","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1006\/geno.1998.5642","volume":"55","author":"HA Bluyssen","year":"1999","unstructured":"Bluyssen HA, Naus NC, van Os RI, Jaspers I, Hoeijmakers JH, de Klein A (1999) Human and mouse homologs of the Schizosaccharomyces pombe rad17+ cell cycle checkpoint control gene. Genomics 55: 219\u2013228","journal-title":"Genomics"},{"key":"BFEMBJ7600353_CR6","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1101\/gad.14.4.397","volume":"14","author":"EJ Brown","year":"2000","unstructured":"Brown EJ, Baltimore D (2000) ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev 14: 397\u2013402","journal-title":"Genes Dev"},{"key":"BFEMBJ7600353_CR7","doi-asserted-by":"crossref","first-page":"26343","DOI":"10.1074\/jbc.M001244200","volume":"275","author":"MA Burtelow","year":"2000","unstructured":"Burtelow MA, Kaufmann SH, Karnitz LM (2000) Retention of the human Rad9 checkpoint complex in extraction\u2010resistant nuclear complexes after DNA damage. J Biol Chem 275: 26343\u201326348","journal-title":"J Biol Chem"},{"key":"BFEMBJ7600353_CR8","doi-asserted-by":"crossref","first-page":"1713","DOI":"10.1126\/science.1065521","volume":"294","author":"D Cortez","year":"2001","unstructured":"Cortez D, Guntuku S, Qin J, Elledge SJ (2001) ATR and ATRIP: partners in checkpoint signaling. Science 294: 1713\u20131716","journal-title":"Science"},{"key":"BFEMBJ7600353_CR9","doi-asserted-by":"crossref","first-page":"2173","DOI":"10.1101\/gad.1025402","volume":"16","author":"M de Jager","year":"2002","unstructured":"de Jager M, Kanaar R (2002) Genome instability and Rad50(S): subtle yet severe. Genes Dev 16: 2173\u20132178","journal-title":"Genes Dev"},{"key":"BFEMBJ7600353_CR10","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1016\/S0960-9822(00)00447-4","volume":"10","author":"A de Klein","year":"2000","unstructured":"de Klein A, Muijtjens M, van Os R, Verhoeven Y, Smit B, Carr AM, Lehmann AR, Hoeijmakers JH (2000) Targeted disruption of the cell\u2010cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr Biol 10: 479\u2013482","journal-title":"Curr Biol"},{"key":"BFEMBJ7600353_CR11","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1038\/15623","volume":"1","author":"RJ Edwards","year":"1999","unstructured":"Edwards RJ, Bentley NJ, Carr AM (1999) A Rad3\u2013Rad26 complex responds to DNA damage independently of other checkpoint proteins. Nat Cell Biol 1: 393\u2013398","journal-title":"Nat Cell Biol"},{"key":"BFEMBJ7600353_CR12","doi-asserted-by":"crossref","first-page":"E33","DOI":"10.1371\/journal.pbio.0000033","volume":"1","author":"V Ellison","year":"2003","unstructured":"Ellison V, Stillman B (2003) Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5\u2032 recessed DNA. PLoS Biol 1: E33","journal-title":"PLoS Biol"},{"key":"BFEMBJ7600353_CR13","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/S0092-8674(00)80199-3","volume":"89","author":"J Essers","year":"1997","unstructured":"Essers J, Hendriks RW, Swagemakers SM, Troelstra C, de Wit J, Bootsma D, Hoeijmakers JH, Kanaar R (1997) Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89: 195\u2013204","journal-title":"Cell"},{"key":"BFEMBJ7600353_CR14","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/ng845","volume":"30","author":"J Falck","year":"2002","unstructured":"Falck J, Petrini JH, Williams BR, Lukas J, Bartek J (2002) The DNA damage\u2010dependent intra\u2010S phase checkpoint is regulated by parallel pathways. Nat Genet 30: 290\u2013294","journal-title":"Nat Genet"},{"key":"BFEMBJ7600353_CR15","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/S0960-9822(99)00263-8","volume":"10","author":"CM Green","year":"2000","unstructured":"Green CM, Erdjument\u2010Bromage H, Tempst P, Lowndes NF (2000) A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr Biol 10: 39\u201342","journal-title":"Curr Biol"},{"key":"BFEMBJ7600353_CR16","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1126\/science.2683079","volume":"246","author":"LH Hartwell","year":"1989","unstructured":"Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246: 629\u2013634","journal-title":"Science"},{"key":"BFEMBJ7600353_CR17","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1146\/annurev.biochem.71.090501.150041","volume":"71","author":"U Hubscher","year":"2002","unstructured":"Hubscher U, Maga G, Spadari S (2002) Eukaryotic DNA polymerases. Annu Rev Biochem 71: 133\u2013163","journal-title":"Annu Rev Biochem"},{"key":"BFEMBJ7600353_CR18","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1016\/S1568-7864(02)00166-0","volume":"1","author":"NG Jaspers","year":"2002","unstructured":"Jaspers NG, Raams A, Kelner MJ, Ng JM, Yamashita YM, Takeda S, McMorris TC, Hoeijmakers JH (2002) Anti\u2010tumour compounds illudin S and Irofulven induce DNA lesions ignored by global repair and exclusively processed by transcription\u2010 and replication\u2010coupled repair pathways. DNA Repair (Amst) 1: 1027\u20131038","journal-title":"DNA Repair (Amst)"},{"key":"BFEMBJ7600353_CR19","doi-asserted-by":"crossref","first-page":"2055","DOI":"10.1093\/emboj\/17.7.2055","volume":"17","author":"CF Kostrub","year":"1998","unstructured":"Kostrub CF, Knudsen K, Subramani S, Enoch T (1998) Hus1p, a conserved fission yeast checkpoint protein, interacts with Rad1p and is phosphorylated in response to DNA damage. EMBO J 17: 2055\u20132066","journal-title":"EMBO J"},{"key":"BFEMBJ7600353_CR20","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1016\/S0021-9258(18)52476-5","volume":"266","author":"SH Lee","year":"1991","unstructured":"Lee SH, Kwong AD, Pan ZQ, Hurwitz J (1991) Studies on the activator 1 protein complex, an accessory factor for proliferating cell nuclear antigen\u2010dependent DNA polymerase delta. J Biol Chem 266: 594\u2013602","journal-title":"J Biol Chem"},{"key":"BFEMBJ7600353_CR21","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1007\/s004380050612","volume":"256","author":"D Lydall","year":"1997","unstructured":"Lydall D, Weinert T (1997) G2\/M checkpoint genes of Saccharomyces cerevisiae: further evidence for roles in DNA replication and\/or repair. Mol Gen Genet 256: 638\u2013651","journal-title":"Mol Gen Genet"},{"key":"BFEMBJ7600353_CR22","doi-asserted-by":"crossref","first-page":"6540","DOI":"10.1093\/emboj\/20.22.6540","volume":"20","author":"LJ Niedernhofer","year":"2001","unstructured":"Niedernhofer LJ, Essers J, Weeda G, Beverloo B, de Wit J, Muijtjens M, Odijk H, Hoeijmakers JH, Kanaar R (2001) The structure\u2010specific endonuclease Ercc1\u2010Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J 20: 6540\u20136549","journal-title":"EMBO J"},{"key":"BFEMBJ7600353_CR23","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1016\/0092-8674(95)90481-6","volume":"82","author":"AG Paulovich","year":"1995","unstructured":"Paulovich AG, Hartwell LH (1995) A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82: 841\u2013847","journal-title":"Cell"},{"key":"BFEMBJ7600353_CR24","doi-asserted-by":"crossref","first-page":"29767","DOI":"10.1074\/jbc.M005782200","volume":"275","author":"M Rauen","year":"2000","unstructured":"Rauen M, Burtelow MA, Dufault VM, Karnitz LM (2000) The human checkpoint protein hRad17 interacts with the PCNA\u2010like proteins hRad1, hHus1, and hRad9. J Biol Chem 275: 29767\u201329771","journal-title":"J Biol Chem"},{"key":"BFEMBJ7600353_CR25","doi-asserted-by":"crossref","first-page":"1749","DOI":"10.1126\/science.7792600","volume":"268","author":"K Savitsky","year":"1995","unstructured":"Savitsky K, Bar\u2010Shira A, Gilad S, Rotman G, Ziv Y, Vanagaite L, Tagle DA, Smith S, Uziel T, Sfez S, Ashkenazi M, Pecker I, Frydman M, Harnik R, Patanjali S, Simmons A, Clines G, Sartiel A, Gatti R, Chessa L, Sanal O, Lavin M, Jaspers N, Taylor A, Arlett C, Miki T, Weissman S, Lovett M, Collins F, Shiloh Y (1995) A single ataxia telangiectasia gene with a product similar to PI\u20103 kinase. Science 268: 1749\u20131753","journal-title":"Science"},{"key":"BFEMBJ7600353_CR26","doi-asserted-by":"crossref","first-page":"3003","DOI":"10.1038\/sj.onc.1201835","volume":"16","author":"PK Schmidt\u2010Kastner","year":"1998","unstructured":"Schmidt\u2010Kastner PK, Jardine K, Cormier M, McBurney MW (1998) Absence of p53\u2010dependent cell cycle regulation in pluripotent mouse cell lines. Oncogene 16: 3003\u20133011","journal-title":"Oncogene"},{"key":"BFEMBJ7600353_CR27","doi-asserted-by":"crossref","first-page":"7985","DOI":"10.1073\/pnas.90.17.7985","volume":"90","author":"W Siede","year":"1993","unstructured":"Siede W, Friedberg AS, Friedberg EC (1993) RAD9\u2010dependent G1 arrest defines a second checkpoint for damaged DNA in the cell cycle of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 90: 7985\u20137989","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFEMBJ7600353_CR28","doi-asserted-by":"crossref","first-page":"2481","DOI":"10.1093\/nar\/28.13.2481","volume":"28","author":"C Venclovas","year":"2000","unstructured":"Venclovas C, Thelen MP (2000) Structure\u2010based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp\u2010loading complexes. Nucleic Acids Res 28: 2481\u20132493","journal-title":"Nucleic Acids Res"},{"key":"BFEMBJ7600353_CR29","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s004399900067","volume":"105","author":"F von Deimling","year":"1999","unstructured":"von Deimling F, Scharf JM, Liehr T, Rothe M, Kelter AR, Albers P, Dietrich WF, Kunkel LM, Wernert N, Wirth B (1999) Human and mouse RAD17 genes: identification, localization, genomic structure and histological expression pattern in normal testis and seminoma. Hum Genet 105: 17\u201327","journal-title":"Hum Genet"},{"key":"BFEMBJ7600353_CR30","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1101\/gad.1065103","volume":"17","author":"X Wang","year":"2003","unstructured":"Wang X, Zou L, Zheng H, Wei Q, Elledge SJ, Li L (2003) Genomic instability and endoreduplication triggered by RAD17 deletion. Genes Dev 17: 965\u2013970","journal-title":"Genes Dev"},{"key":"BFEMBJ7600353_CR31","doi-asserted-by":"crossref","first-page":"14590","DOI":"10.1073\/pnas.94.26.14590","volume":"94","author":"YA Wang","year":"1997","unstructured":"Wang YA, Elson A, Leder P (1997) Loss of p21 increases sensitivity to ionizing radiation and delays the onset of lymphoma in atm\u2010deficient mice. Proc Natl Acad Sci USA 94: 14590\u201314595","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFEMBJ7600353_CR32","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1101\/gad.8.6.652","volume":"8","author":"TA Weinert","year":"1994","unstructured":"Weinert TA, Kiser GL, Hartwell LH (1994) Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev 8: 652\u2013665","journal-title":"Genes Dev"},{"key":"BFEMBJ7600353_CR33","doi-asserted-by":"crossref","first-page":"1886","DOI":"10.1101\/gad.14.15.1886","volume":"14","author":"RS Weiss","year":"2000","unstructured":"Weiss RS, Enoch T, Leder P (2000) Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev 14: 1886\u20131898","journal-title":"Genes Dev"},{"key":"BFEMBJ7600353_CR34","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1128\/MCB.22.4.1049-1059.2002","volume":"22","author":"B Xu","year":"2002","unstructured":"Xu B, Kim ST, Lim DS, Kastan MB (2002) Two molecularly distinct G(2)\/M checkpoints are induced by ionizing irradiation. Mol Cell Biol 22: 1049\u20131059","journal-title":"Mol Cell Biol"},{"key":"BFEMBJ7600353_CR35","doi-asserted-by":"crossref","first-page":"4385","DOI":"10.1128\/MCB.18.7.4385","volume":"18","author":"Y Xu","year":"1998","unstructured":"Xu Y, Yang EM, Brugarolas J, Jacks T, Baltimore D (1998) Involvement of p53 and p21 in cellular defects and tumorigenesis in Atm\u2212\/\u2212 mice. Mol Cell Biol 18: 4385\u20134390","journal-title":"Mol Cell Biol"},{"key":"BFEMBJ7600353_CR36","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1038\/35044005","volume":"408","author":"BB Zhou","year":"2000","unstructured":"Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408: 433\u2013439","journal-title":"Nature"},{"key":"BFEMBJ7600353_CR37","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1101\/gad.950302","volume":"16","author":"L Zou","year":"2002","unstructured":"Zou L, Cortez D, Elledge SJ (2002) Regulation of ATR substrate selection by Rad17\u2010dependent loading of Rad9 complexes onto chromatin. Genes Dev 16: 198\u2013208","journal-title":"Genes Dev"}],"container-title":["The EMBO Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1038%2Fsj.emboj.7600353","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1038\/sj.emboj.7600353.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1038\/sj.emboj.7600353","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full\/10.1038\/sj.emboj.7600353","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1038\/sj.emboj.7600353.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,19]],"date-time":"2026-05-19T23:15:42Z","timestamp":1779232542000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1038\/sj.emboj.7600353"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2004,8,5]]},"references-count":37,"journal-issue":{"issue":"17","published-print":{"date-parts":[[2004,9,1]]}},"alternative-id":["BFEMBJ7600353"],"URL":"https:\/\/doi.org\/10.1038\/sj.emboj.7600353","relation":{},"ISSN":["0261-4189","1460-2075"],"issn-type":[{"value":"0261-4189","type":"print"},{"value":"1460-2075","type":"electronic"}],"subject":[],"published":{"date-parts":[[2004,8,5]]},"assertion":[{"value":"19 August 2003","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 July 2004","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 August 2004","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"This content has been made available to all.","name":"free","label":"Free to read"}]}}