{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T15:40:49Z","timestamp":1787499649913,"version":"build-2736575974"},"reference-count":59,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2003,12,1]],"date-time":"2003-12-01T00:00:00Z","timestamp":1070236800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2003,12,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>DNA Ligase IV has a crucial role in double-strand break (DSB) repair through nonhomologous end joining (NHEJ). Most notably, its inactivation leads to embryonic lethality in mammals. To elucidate the role of DNA Ligase IV (Lig4) in DSB repair in a multicellular lower eukaryote, we generated viable Lig4-deficient Drosophila strains by P-element-mediated mutagenesis. Embryos and larvae of mutant lines are hypersensitive to ionizing radiation but hardly so to methyl methanesulfonate (MMS) or the crosslinking agent cis-diamminedichloroplatinum (cisDDP). To determine the relative contribution of NHEJ and homologous recombination (HR) in Drosophila, Lig4; Rad54 double-mutant flies were generated. Survival studies demonstrated that both HR and NHEJ have a major role in DSB repair. The synergistic increase in sensitivity seen in the double mutant, in comparison with both single mutants, indicates that both pathways partially overlap. However, during the very first hours after fertilization NHEJ has a minor role in DSB repair after exposure to ionizing radiation. Throughout the first stages of embryogenesis of the fly, HR is the predominant pathway in DSB repair. At late stages of development NHEJ also becomes less important. The residual survival of double mutants after irradiation strongly suggests the existence of a third pathway for the repair of DSBs in Drosophila.<\/jats:p>","DOI":"10.1093\/genetics\/165.4.1929","type":"journal-article","created":{"date-parts":[[2021,4,27]],"date-time":"2021-04-27T12:27:19Z","timestamp":1619526439000},"page":"1929-1941","source":"Crossref","is-referenced-by-count":39,"title":["The\n                    <i>Drosophila melanogaster<\/i>\n                    DNA\n                    <i>Ligase IV<\/i>\n                    Gene Plays a Crucial Role in the Repair of Radiation-Induced DNA Double-Strand Breaks and Acts Synergistically With\n                    <i>Rad54<\/i>"],"prefix":"10.1093","volume":"165","author":[{"given":"Marcin M","family":"Gorski","sequence":"first","affiliation":[{"name":"Department of Toxicogenetics, Leiden University Medical Center, 2333 AL, Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan C J","family":"Eeken","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anja W M","family":"de Jong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ilse","family":"Klink","sequence":"additional","affiliation":[{"name":"Department of Toxicogenetics, Leiden University Medical Center, 2333 AL, Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marjan","family":"Loos","sequence":"additional","affiliation":[{"name":"Department of Toxicogenetics, Leiden University Medical Center, 2333 AL, Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ron J","family":"Romeijn","sequence":"additional","affiliation":[{"name":"Department of Toxicogenetics, Leiden University Medical Center, 2333 AL, Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bert L","family":"van Veen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leon H","family":"Mullenders","sequence":"additional","affiliation":[{"name":"Department of Toxicogenetics, Leiden University Medical Center, 2333 AL, Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wouter","family":"Ferro","sequence":"additional","affiliation":[{"name":"Department of Toxicogenetics, Leiden University Medical Center, 2333 AL, Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Albert","family":"Pastink","sequence":"additional","affiliation":[{"name":"Department of Toxicogenetics, Leiden University Medical Center, 2333 AL, Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2003,12,1]]},"reference":[{"key":"2022010522443541200_R1","doi-asserted-by":"crossref","first-page":"14899","DOI":"10.1073\/pnas.96.26.14899","article-title":"DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes","volume":"96","author":"Bailey","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2022010522443541200_R2","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1016\/S0960-9822(98)00021-9","article-title":"Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice","volume":"8","author":"Barnes","year":"1998","journal-title":"Curr. Biol."},{"key":"2022010522443541200_R3","doi-asserted-by":"crossref","first-page":"4639","DOI":"10.1093\/nar\/24.23.4639","article-title":"Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance","volume":"24","author":"Boulton","year":"1996","journal-title":"Nucleic Acids Res."},{"key":"2022010522443541200_R4","doi-asserted-by":"crossref","first-page":"5093","DOI":"10.1002\/j.1460-2075.1996.tb00890.x","article-title":"Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways","volume":"15","author":"Boulton","year":"1996","journal-title":"EMBO J."},{"key":"2022010522443541200_R5","doi-asserted-by":"crossref","first-page":"1819","DOI":"10.1093\/emboj\/17.6.1819","article-title":"Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing","volume":"17","author":"Boulton","year":"1998","journal-title":"EMBO J."},{"key":"2022010522443541200_R6","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1093\/nar\/15.4.1353","article-title":"Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates","volume":"15","author":"Cavener","year":"1987","journal-title":"Nucleic Acids Res."},{"key":"2022010522443541200_R7","doi-asserted-by":"crossref","first-page":"47242","DOI":"10.1074\/jbc.M208542200","article-title":"Human Ku70\/80 associates physically with telomerase through interaction with hTERT","volume":"277","author":"Chai","year":"2002","journal-title":"J. Biol. Chem."},{"key":"2022010522443541200_R8","doi-asserted-by":"crossref","first-page":"5789","DOI":"10.1073\/pnas.89.13.5789","article-title":"Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun","volume":"89","author":"Chevray","year":"1992","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2022010522443541200_R9","doi-asserted-by":"crossref","first-page":"2535","DOI":"10.1093\/emboj\/16.9.2535","article-title":"Recombinational repair in yeast: functional interactions between Rad51 and Rad54 proteins","volume":"16","author":"Clever","year":"1997","journal-title":"EMBO J."},{"key":"2022010522443541200_R10","doi-asserted-by":"crossref","first-page":"10881","DOI":"10.1093\/nar\/16.22.10881","article-title":"Multiple sequence alignment with hierarchical clustering","volume":"16","author":"Corpet","year":"1988","journal-title":"Nucleic Acids Res."},{"key":"2022010522443541200_R11","doi-asserted-by":"crossref","first-page":"588","DOI":"10.1016\/S0960-9822(06)00258-2","article-title":"Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV","volume":"7","author":"Critchlow","year":"1997","journal-title":"Curr. Biol."},{"key":"2022010522443541200_R12","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1016\/S0960-9822(01)00555-3","article-title":"DNA repair: how Ku makes ends meet","volume":"11","author":"Doherty","year":"2001","journal-title":"Curr. Biol."},{"key":"2022010522443541200_R13","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/S0092-8674(00)80199-3","article-title":"Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination","volume":"89","author":"Essers","year":"1997","journal-title":"Cell"},{"key":"2022010522443541200_R14","doi-asserted-by":"crossref","first-page":"1703","DOI":"10.1093\/emboj\/19.7.1703","article-title":"Homologous and non-homologous recombination differentially affect DNA damage repair in mice","volume":"19","author":"Essers","year":"2000","journal-title":"EMBO J."},{"key":"2022010522443541200_R15","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0921-8777(99)00006-3","article-title":"Ku, a DNA repair protein with multiple cellular functions?","volume":"434","author":"Featherstone","year":"1999","journal-title":"Mutat. Res."},{"key":"2022010522443541200_R16","doi-asserted-by":"crossref","first-page":"222","DOI":"10.4049\/jimmunol.149.1.222","article-title":"Predominance of VH-D-JH junctions occurring at sites of short sequence homology results in limited junctional diversity in neonatal antibodies","volume":"149","author":"Feeney","year":"1992","journal-title":"J. Immunol."},{"key":"2022010522443541200_R17","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1038\/24172","article-title":"Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV","volume":"396","author":"Frank","year":"1998","journal-title":"Nature"},{"key":"2022010522443541200_R18","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1016\/S1097-2765(00)80264-6","article-title":"DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway","volume":"5","author":"Frank","year":"2000","journal-title":"Mol. Cell"},{"key":"2022010522443541200_R19","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/S1074-7613(00)80619-6","article-title":"A targeted DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination","volume":"9","author":"Gao","year":"1998","journal-title":"Immunity"},{"key":"2022010522443541200_R20","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1016\/S0092-8674(00)81714-6","article-title":"A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis","volume":"95","author":"Gao","year":"1998","journal-title":"Cell"},{"key":"2022010522443541200_R21","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1038\/363625a0","article-title":"Extent to which homology can constrain coding exon junctional diversity in V(D)J recombination","volume":"363","author":"Gerstein","year":"1993","journal-title":"Nature"},{"key":"2022010522443541200_R22","doi-asserted-by":"crossref","first-page":"2711","DOI":"10.1101\/gad.12.17.2711","article-title":"okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis","volume":"12","author":"Ghabrial","year":"1998","journal-title":"Genes Dev."},{"key":"2022010522443541200_R23","doi-asserted-by":"crossref","first-page":"4106","DOI":"10.1093\/nar\/25.20.4106","article-title":"Interaction of human recombination proteins Rad51 and Rad54","volume":"25","author":"Golub","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"2022010522443541200_R24","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1046\/j.1432-1327.1998.2580387.x","article-title":"Rejoining of DNA double-strand breaks in vitro by single-strand annealing","volume":"258","author":"Gottlich","year":"1998","journal-title":"Eur. J. Biochem."},{"key":"2022010522443541200_R25","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1126\/science.280.5364.741","article-title":"Yeast Ku as a regulator of chromosomal DNA end structure","volume":"280","author":"Gravel","year":"1998","journal-title":"Science"},{"key":"2022010522443541200_R26","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1038\/41358","article-title":"Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells","volume":"388","author":"Grawunder","year":"1997","journal-title":"Nature"},{"key":"2022010522443541200_R27","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/S1097-2765(00)80147-1","article-title":"DNA ligase IV is essential for V(D)J recombination and DNA double-strand break repair in human precursor lymphocytes","volume":"2","author":"Grawunder","year":"1998","journal-title":"Mol. Cell"},{"key":"2022010522443541200_R28","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1016\/S0960-9822(07)00349-1","article-title":"DNA ligase IV binds to XRCC4 via a motif located between rather than within its BRCT domains","volume":"8","author":"Grawunder","year":"1998","journal-title":"Curr. Biol."},{"key":"2022010522443541200_R29","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/S1074-7613(00)80386-6","article-title":"Growth retardation and leaky SCID phenotype of Ku70-deficient mice","volume":"7","author":"Gu","year":"1997","journal-title":"Immunity"},{"key":"2022010522443541200_R30","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1016\/0092-8674(93)90499-G","article-title":"The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases","volume":"75","author":"Harper","year":"1993","journal-title":"Cell"},{"key":"2022010522443541200_R31","doi-asserted-by":"crossref","first-page":"4188","DOI":"10.1093\/emboj\/17.14.4188","article-title":"Saccharomyces cerevisiae LIF1: a function involved in DNA double-strand break repair related to mammalian XRCC4","volume":"17","author":"Herrmann","year":"1998","journal-title":"EMBO J."},{"key":"2022010522443541200_R32","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/S0960-9822(99)80278-4","article-title":"DNA repair: Rad52\u2014the means to an end","volume":"9","author":"Hiom","year":"1999","journal-title":"Curr. Biol."},{"key":"2022010522443541200_R33","doi-asserted-by":"crossref","first-page":"12454","DOI":"10.1073\/pnas.96.22.12454","article-title":"Ku is associated with the telomere in mammals","volume":"96","author":"Hsu","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2022010522443541200_R34","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/S1011-1344(01)00243-3","article-title":"Immune diversity and genomic stability: opposite goals but similar paths","volume":"65","author":"Jeggo","year":"2001","journal-title":"J. Photochem. Photobiol. B."},{"key":"2022010522443541200_R35","doi-asserted-by":"crossref","first-page":"5333","DOI":"10.1093\/nar\/26.23.5333","article-title":"Double-strand break repair in Ku86- and XRCC4-deficient cells","volume":"26","author":"Kabotyanski","year":"1998","journal-title":"Nucleic Acids Res."},{"key":"2022010522443541200_R36","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1016\/S1568-7864(02)00151-9","article-title":"The embryonic lethality in DNA ligase IV-deficient mice is rescued by deletion of Ku: implications for unifying the heterogeneous phenotypes of NHEJ mutants","volume":"1","author":"Karanjawala","year":"2002","journal-title":"DNA Repair"},{"key":"2022010522443541200_R37","doi-asserted-by":"crossref","first-page":"6097","DOI":"10.1128\/MCB.17.10.6097","article-title":"The Drosophila melanogaster RAD54 homolog, DmRAD54, is involved in the repair of radiation damage and recombination","volume":"17","author":"Kooistra","year":"1997","journal-title":"Mol. Cell. Biol."},{"key":"2022010522443541200_R38","doi-asserted-by":"crossref","first-page":"6269","DOI":"10.1128\/MCB.19.9.6269","article-title":"The Drosophila melanogaster DmRAD54 gene plays a crucial role in double-strand break repair after P-element excision and acts synergistically with Ku70 in the repair of X-ray damage","volume":"19","author":"Kooistra","year":"1999","journal-title":"Mol. Cell. Biol."},{"key":"2022010522443541200_R39","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1016\/S0092-8674(02)00671-2","article-title":"Hairpin opening and overhang processing by an Artemis\/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination","volume":"108","author":"Ma","year":"2002","journal-title":"Cell"},{"key":"2022010522443541200_R40","doi-asserted-by":"crossref","first-page":"REVIEWS3005","DOI":"10.1186\/gb-2002-3-4-reviews3005","article-title":"ATP-dependent DNA ligases","volume":"3","author":"Martin","year":"2002","journal-title":"Genome Biol."},{"key":"2022010522443541200_R41","doi-asserted-by":"crossref","first-page":"2996","DOI":"10.1128\/MCB.20.9.2996-3003.2000","article-title":"Ku recruits the XRCC4-ligase IV complex to DNA ends","volume":"20","author":"McElhinny","year":"2000","journal-title":"Mol. Cell. Biol."},{"key":"2022010522443541200_R42","doi-asserted-by":"crossref","first-page":"4189","DOI":"10.1128\/MCB.16.8.4189","article-title":"Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae","volume":"16","author":"Milne","year":"1996","journal-title":"Mol. Cell. Biol."},{"key":"2022010522443541200_R43","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/S0092-8674(01)00309-9","article-title":"Artemis, a novel DNA double-strand break repair\/V(D)J recombination protein, is mutated in human severe combined immune deficiency","volume":"105","author":"Moshous","year":"2001","journal-title":"Cell"},{"key":"2022010522443541200_R44","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1038\/382551a0","article-title":"Requirement for Ku80 in growth and immunoglobulin V(D)J recombination","volume":"382","author":"Nussenzweig","year":"1996","journal-title":"Nature"},{"key":"2022010522443541200_R45","doi-asserted-by":"crossref","first-page":"13588","DOI":"10.1073\/pnas.94.25.13588","article-title":"Hypersensitivity of Ku80-deficient cell lines and mice to DNA damage: the effects of ionizing radiation on growth, survival, and development","volume":"94","author":"Nussenzweig","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2022010522443541200_R46","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/S0027-5107(01)00167-1","article-title":"Genomic integrity and the repair of double-strand DNA breaks","volume":"480\u2013481","author":"Pastink","year":"2001","journal-title":"Mutat. Res"},{"key":"2022010522443541200_R47","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1093\/genetics\/161.2.711","article-title":"Efficient repair of DNA breaks in Drosophila: evidence for single-strand annealing and competition with other repair pathways","volume":"161","author":"Preston","year":"2002","journal-title":"Genetics"},{"key":"2022010522443541200_R48","doi-asserted-by":"crossref","first-page":"9068","DOI":"10.1128\/MCB.20.23.9068-9075.2000","article-title":"Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells","volume":"20","author":"Richardson","year":"2000","journal-title":"Mol. Cell. Biol."},{"key":"2022010522443541200_R49","doi-asserted-by":"crossref","first-page":"2013","DOI":"10.1126\/science.288.5473.2013","article-title":"Gene targeting by homologous recombination in Drosophila","volume":"288","author":"Rong","year":"2000","journal-title":"Science"},{"key":"2022010522443541200_R50","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1038\/nsb725","article-title":"Crystal structure of an Xrcc4-DNA ligase IV complex","volume":"8","author":"Sibanda","year":"2001","journal-title":"Nat. Struct. Biol"},{"key":"2022010522443541200_R51","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1093\/genetics\/142.1.91","article-title":"The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination","volume":"142","author":"Siede","year":"1996","journal-title":"Genetics"},{"key":"2022010522443541200_R52","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/S1074-7613(00)80618-4","article-title":"Targeted disruption of the catalytic subunit of the DNA-PK gene in mice confers severe combined immunodeficiency and radiosensitivity","volume":"9","author":"Taccioli","year":"1998","journal-title":"Immunity"},{"key":"2022010522443541200_R53","doi-asserted-by":"crossref","first-page":"5497","DOI":"10.1093\/emboj\/17.18.5497","article-title":"Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells","volume":"17","author":"Takata","year":"1998","journal-title":"EMBO J."},{"key":"2022010522443541200_R54","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0921-8777(97)00050-5","article-title":"Structure and function of mammalian DNA ligases","volume":"407","author":"Tomkinson","year":"1998","journal-title":"Mutat. Res."},{"key":"2022010522443541200_R55","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1038\/19560","article-title":"Binding of double-strand breaks in DNA by human Rad52 protein","volume":"398","author":"Van Dyck","year":"1999","journal-title":"Nature"},{"key":"2022010522443541200_R56","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1038\/35056049","article-title":"Chromosomal stability and the DNA double-stranded break connection","volume":"2","author":"van Gent","year":"2001","journal-title":"Nat. Rev. Genet."},{"key":"2022010522443541200_R57","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1002\/1521-4141(200203)32:3<701::AID-IMMU701>3.0.CO;2-T","article-title":"Different types of V(D)J recombination and end-joining defects in DNA double-strand break repair mutant mammalian cells","volume":"32","author":"Verkaik","year":"2002","journal-title":"Eur. J. Immunol."},{"key":"2022010522443541200_R58","doi-asserted-by":"crossref","first-page":"3206","DOI":"10.1128\/MCB.15.6.3206","article-title":"Molecular cloning and expression of human cDNAs encoding a novel DNA ligase IV and DNA ligase III, an enzyme active in DNA repair and recombination","volume":"15","author":"Wei","year":"1995","journal-title":"Mol. Cell. Biol."},{"key":"2022010522443541200_R59","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/S0092-8674(00)80111-7","article-title":"Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates","volume":"86","author":"Zhu","year":"1996","journal-title":"Cell"}],"container-title":["Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/165\/4\/1929\/42054080\/genetics1929.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/165\/4\/1929\/42054080\/genetics1929.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,2]],"date-time":"2023-11-02T16:55:59Z","timestamp":1698944159000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/genetics\/article\/165\/4\/1929\/6050559"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,12,1]]},"references-count":59,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2003,12,1]]},"published-print":{"date-parts":[[2003,12,1]]}},"URL":"https:\/\/doi.org\/10.1093\/genetics\/165.4.1929","relation":{},"ISSN":["1943-2631"],"issn-type":[{"value":"1943-2631","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2003,12,1]]},"published":{"date-parts":[[2003,12,1]]}}}