DOI: 10.1101/gad.11.15.1912. A newly identified DNA ligase of <i>Saccharomyces cerevisiae</i>involved in <i>RAD52</i>-independent repair of DNA double-strand breaks

A newly identified DNA ligase of Saccharomyces cerevisiaeinvolved in RAD52-independent repair of DNA double-strand breaks

10.1101/gad.11.15.1912

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

Eukaryotic DNA ligases are ATP-dependent DNA strand-joining enzymes that participate in DNA replication, repair, and recombination. Whereas mammalian cells contain several different DNA ligases, encoded by at least three distinct genes, only one DNA ligase has been detected previously in either budding yeast or fission yeast. Here, we describe a newly identified nonessential Saccharomyces cerevisiae gene that encodes a DNA ligase distinct from the CDC9 gene product. This DNA ligase shares significant amino acid sequence homology with human DNA ligase IV; accordingly, we designate the yeast gene LIG4.Recombinant LIG4 protein forms a covalent enzyme-AMP complex and can join a DNA single-strand break in a DNA/RNA hybrid duplex, the preferred substrate in vitro. Disruption of theLIG4 gene causes only marginally increased cellular sensitivity to several DNA damaging agents, and does not further sensitizecdc9 or rad52 mutant cells. In contrast, lig4mutant cells have a 1000-fold reduced capacity for correct recircularization of linearized plasmids by illegitimate end-joining after transformation. Moreover, homozygous lig4 mutant diploids sporulate less efficiently than isogenic wild-type cells, and show retarded progression through meiotic prophase I. Spore viability is normal, but lig4 mutants appear to produce a higher proportion of tetrads with only three viable spores. The mutant phenotypes are consistent with functions of LIG4 in an illegitimate DNA end-joining pathway and ensuring efficient meiosis.

Bibliography

SchÃ¤r, P., Herrmann, G., Daly, G., & Lindahl, T. (1997). A newly identified DNA ligase of Saccharomyces cerevisiaeinvolved in RAD52-independent repair of DNA double-strandâbreaks. Genes & Development, 11(15), 1912â1924.

Authors 4

Primo Schär (first)
Gernot Herrmann (additional)
Graham Daly (additional)
Tomas Lindahl (additional)

References 55 Referenced 144

10.1002/(SICI)1097-0061(199607)12:9<893::AID-YEA973>3.0.CO;2-I
10.1007/BF00352322 / Chromosoma / Saccharomyces cerevisiae cells lacking the homologous pairing protein p175SEP1 arrest at pachytene during meiotic prophase. by Bähler (1994)
10.1093/nar/13.23.8323
10.1111/j.1432-1033.1987.tb10688.x / Eur. J. Biochem. / Molecular characterisation of the DNA ligase gene, CDC17, from the fission yeast Schizosaccharomyces pombe. (1987)
10.1073/pnas.87.17.6679
10.1016/0092-8674(92)90450-Q
10.1073/pnas.94.3.867
10.1093/nar/24.23.4639
10.1002/j.1460-2075.1996.tb00890.x / EMBO J. / Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. (1996)
10.1016/S0014-5793(96)01312-9
10.1128/MCB.15.10.5412 / Mol. Cell. Biol. / Mammalian DNA ligase III: Molecular cloning, chromosomal localization, and expression in spermatocytes undergoing meiotic recombination. by Chen (1995)
10.1016/0092-8674(91)90187-4
{'key': '2021111418462429000_11.15.1912.13', 'first-page': '7025', 'article-title': 'A comprehensive set of sequence analysis programs for the VAX.', 'volume': '16', 'author': 'Devereux', 'year': '1984', 'journal-title': 'Nucleic Acids Res.'} / Nucleic Acids Res. / A comprehensive set of sequence analysis programs for the VAX. by Devereux (1984)
10.1016/S0021-9258(18)31470-4 / J. Biol. Chem. / A putative homologue of the human autoantigen Ku from Saccharomyces cerevisiae. by Feldmann (1993)
Friedberg E.C. Walker G.C. Siede W. (1995) DNA repair and mutagenesis. (American Society for Microbiology, Washington, D.C.) pp 662–669.
10.1002/yea.320070307
10.1016/0955-0674(92)90005-W
10.1016/0168-9525(92)90329-3 / Trends Genet. / Mating-type gene switching in Saccharomyces cerevisiae. (1992)
10.1007/BF00352100
10.1038/274891a0
{'key': '2021111418462429000_11.15.1912.21', 'first-page': '1293', 'article-title': 'Two different types of double strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52 independent, nonhomologous recombination events.', 'volume': '14', 'author': 'Kramer', 'year': '1994', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Two different types of double strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52 independent, nonhomologous recombination events. by Kramer (1994)
10.1002/j.1460-2075.1996.tb01056.x / EMBO J. / Reconstitution of DNA base excision-repair with purified human proteins: Interaction between DNA polymerase β and the XRCC1 protein. by Kubota (1996)
10.1146/annurev.bi.61.070192.001343
10.1074/jbc.272.17.11550
10.1074/jbc.271.14.7910
{'key': '2021111418462429000_11.15.1912.26', 'first-page': '1278', 'article-title': 'Homologous, homeologous, and illegitimate repair of double-strand breaks during transformation of a wild-type strain and a rad52 mutant strain of Saccharomyces cerevisiae.', 'volume': '14', 'author': 'Mezard', 'year': '1994', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Homologous, homeologous, and illegitimate repair of double-strand breaks during transformation of a wild-type strain and a rad52 mutant strain of Saccharomyces cerevisiae. by Mezard (1994)
10.1128/MCB.16.8.4189 / Mol. Cell. Biol. / Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. by Milne (1996)
10.1128/MCB.16.5.2164 / Mol. Cell. Biol. / Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. by Moore (1996)
10.1021/bi962281m
10.1007/BF01924007
10.1016/0092-8674(91)90046-2
{'key': '2021111418462429000_11.15.1912.32', 'first-page': '407', 'article-title': 'Recombination in yeast.', 'volume': '1', 'author': 'Petes', 'year': '1991', 'journal-title': 'The molecular and cellular biology of the yeast Saccharomyces: Genome dynamics, protein synthesis and energetics'} / The molecular and cellular biology of the yeast Saccharomyces: Genome dynamics, protein synthesis and energetics / Recombination in yeast. by Petes (1991)
10.1128/MCB.15.8.4303 / Mol. Cell. Biol. / DNA ligase I mediates essential functions in mammalian cells. by Petrini (1995)
{'key': '2021111418462429000_11.15.1912.34', 'first-page': '310', 'article-title': 'Aberrant DNA repair and DNA replication due to an inherited enzymatic defect in human DNA ligase I.', 'volume': '14', 'author': 'Prigent', 'year': '1994', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Aberrant DNA repair and DNA replication due to an inherited enzymatic defect in human DNA ligase I. by Prigent (1994)
10.1093/nar/25.8.1485
10.1016/S0021-9258(17)41929-6 / J. Biol. Chem. / Different active sites of mammalian DNA ligases I and II. by Roberts (1994)
10.1074/jbc.271.39.24257
10.1073/pnas.92.23.10450
10.1073/pnas.88.17.7585
{'key': '2021111418462429000_11.15.1912.40', 'first-page': '4493', 'article-title': 'Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae.', 'volume': '14', 'author': 'Schiestl', 'year': '1994', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae. by Schiestl (1994)
Sherman F. Fink G.K. Hicks J.B. (1982) Methods in yeast genetics. (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY).
10.1111/j.1365-2958.1995.mmi_17030405.x
10.1093/genetics/142.1.91 / Genetics / The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. by Siede (1996)
10.1093/genetics/76.4.745 / Genetics / Are mitotic functions required in meiosis? by Simchen (1974)
10.1007/BF00260499 / Mol. & Gen. Genet. / Recombination and mating-type switching in a ligase-deficient mutant of Schizosaccharomyces pombe. by Sipiczki (1990)
10.1002/(SICI)1097-0061(199609)12:10B<1091::AID-YEA22>3.0.CO;2-I
10.1016/S0092-8674(00)81260-X
Teo, S.-H. and S.P. Jackson. 1997. Identification of Saccharomyces cerevisiae DNA ligase IV: Involvement in DNA double-strand-break repair. EMBO J. (in press).. (10.1093/emboj/16.15.4788)
{'key': '2021111418462429000_11.15.1912.49', 'first-page': '6160', 'article-title': 'Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange.', 'volume': '10', 'author': 'Thompson', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. by Thompson (1990)
10.1073/pnas.88.2.400
10.1021/bi00162a013
10.1093/nar/24.11.2067
10.1002/yea.320101310
10.1016/S0021-9258(17)34146-7 / J. Biol. Chem. / Reconstitution of complete SV40 DNA replication with purified replication factors. by Waga (1994)
10.1128/MCB.15.6.3206 / Mol. Cell. Biol. / 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. by Wei (1995)

Dates

Type	When
Created	17 years, 6 months ago (Feb. 20, 2008, 5:15 p.m.)
Deposited	3 years, 9 months ago (Nov. 14, 2021, 10:04 p.m.)
Indexed	1 week, 6 days ago (Aug. 19, 2025, 6:01 a.m.)
Issued	28 years, 1 month ago (Aug. 1, 1997)
Published	28 years, 1 month ago (Aug. 1, 1997)
Published Online	28 years, 1 month ago (Aug. 1, 1997)
Published Print	28 years, 1 month ago (Aug. 1, 1997)

Funders 0

None

BibTeX

@article{Sch_r_1997, title={A newly identified DNA ligase of Saccharomyces cerevisiaeinvolved in RAD52-independent repair of DNA double-strand breaks}, volume={11}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.11.15.1912}, DOI={10.1101/gad.11.15.1912}, number={15}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Schär, Primo and Herrmann, Gernot and Daly, Graham and Lindahl, Tomas}, year={1997}, month=aug, pages={1912–1924} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        19
      ]
    ],
    "date-time": "2025-08-19T10:01:49Z",
    "timestamp": 1755597709323
  },
  "reference-count": 55,
  "publisher": "Cold Spring Harbor Laboratory",
  "issue": "15",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1997,
        8,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Eukaryotic DNA ligases are ATP-dependent DNA strand-joining enzymes that participate in DNA replication, repair, and recombination. Whereas mammalian cells contain several different DNA ligases, encoded by at least three distinct genes, only one DNA ligase has been detected previously in either budding yeast or fission yeast. Here, we describe a newly identified nonessential <jats:italic>Saccharomyces cerevisiae</jats:italic> gene that encodes a DNA ligase distinct from the CDC9 gene product. This DNA ligase shares significant amino acid sequence homology with human DNA ligase IV; accordingly, we designate the yeast gene <jats:italic>LIG4.</jats:italic>Recombinant LIG4 protein forms a covalent enzyme-AMP complex and can join a DNA single-strand break in a DNA/RNA hybrid duplex, the preferred substrate in vitro. Disruption of the<jats:italic>LIG4</jats:italic> gene causes only marginally increased cellular sensitivity to several DNA damaging agents, and does not further sensitize<jats:italic>cdc9</jats:italic> or <jats:italic>rad52</jats:italic> mutant cells. In contrast, <jats:italic>lig4</jats:italic>mutant cells have a 1000-fold reduced capacity for correct recircularization of linearized plasmids by illegitimate end-joining after transformation. Moreover, homozygous <jats:italic>lig4</jats:italic> mutant diploids sporulate less efficiently than isogenic wild-type cells, and show retarded progression through meiotic prophase I. Spore viability is normal, but <jats:italic>lig4</jats:italic> mutants appear to produce a higher proportion of tetrads with only three viable spores. The mutant phenotypes are consistent with functions of LIG4 in an illegitimate DNA end-joining pathway and ensuring efficient meiosis.</jats:p>",
  "DOI": "10.1101/gad.11.15.1912",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2008,
        2,
        20
      ]
    ],
    "date-time": "2008-02-20T22:15:26Z",
    "timestamp": 1203545726000
  },
  "page": "1912-1924",
  "source": "Crossref",
  "is-referenced-by-count": 144,
  "title": "A newly identified DNA ligase of <i>Saccharomyces cerevisiae</i>involved in <i>RAD52</i>-independent repair of DNA double-strand\u2009breaks",
  "prefix": "10.1101",
  "volume": "11",
  "author": [
    {
      "given": "Primo",
      "family": "Sch\u00e4r",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Gernot",
      "family": "Herrmann",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Graham",
      "family": "Daly",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Tomas",
      "family": "Lindahl",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "246",
  "published-online": {
    "date-parts": [
      [
        1997,
        8,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2021111418462429000_11.15.1912.1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0061(199607)12:9<893::AID-YEA973>3.0.CO;2-I"
    },
    {
      "key": "2021111418462429000_11.15.1912.2",
      "doi-asserted-by": "crossref",
      "first-page": "129",
      "DOI": "10.1007/BF00352322",
      "article-title": "Saccharomyces cerevisiae cells lacking the homologous pairing protein p175SEP1 arrest at pachytene during meiotic prophase.",
      "volume": "103",
      "author": "B\u00e4hler",
      "year": "1994",
      "journal-title": "Chromosoma"
    },
    {
      "key": "2021111418462429000_11.15.1912.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/13.23.8323"
    },
    {
      "key": "2021111418462429000_11.15.1912.4",
      "doi-asserted-by": "crossref",
      "first-page": "659",
      "DOI": "10.1111/j.1432-1033.1987.tb10688.x",
      "article-title": "Molecular characterisation of the DNA ligase gene, CDC17, from the fission yeast Schizosaccharomyces pombe.",
      "volume": "162",
      "year": "1987",
      "journal-title": "Eur. J. Biochem."
    },
    {
      "key": "2021111418462429000_11.15.1912.5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.87.17.6679"
    },
    {
      "key": "2021111418462429000_11.15.1912.6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90450-Q"
    },
    {
      "key": "2021111418462429000_11.15.1912.7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.94.3.867"
    },
    {
      "key": "2021111418462429000_11.15.1912.8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/24.23.4639"
    },
    {
      "key": "2021111418462429000_11.15.1912.9",
      "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",
      "year": "1996",
      "journal-title": "EMBO J."
    },
    {
      "key": "2021111418462429000_11.15.1912.10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0014-5793(96)01312-9"
    },
    {
      "key": "2021111418462429000_11.15.1912.11",
      "doi-asserted-by": "crossref",
      "first-page": "5412",
      "DOI": "10.1128/MCB.15.10.5412",
      "article-title": "Mammalian DNA ligase III: Molecular cloning, chromosomal localization, and expression in spermatocytes undergoing meiotic recombination.",
      "volume": "15",
      "author": "Chen",
      "year": "1995",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111418462429000_11.15.1912.12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90187-4"
    },
    {
      "key": "2021111418462429000_11.15.1912.13",
      "first-page": "7025",
      "article-title": "A comprehensive set of sequence analysis programs for the VAX.",
      "volume": "16",
      "author": "Devereux",
      "year": "1984",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2021111418462429000_11.15.1912.14",
      "doi-asserted-by": "crossref",
      "first-page": "12895",
      "DOI": "10.1016/S0021-9258(18)31470-4",
      "article-title": "A putative homologue of the human autoantigen Ku from Saccharomyces cerevisiae.",
      "volume": "268",
      "author": "Feldmann",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2021111418462429000_11.15.1912.15",
      "unstructured": "Friedberg E.C. Walker G.C. Siede W. (1995) DNA repair and mutagenesis. (American Society for Microbiology, Washington, D.C.) pp 662\u2013669."
    },
    {
      "key": "2021111418462429000_11.15.1912.16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/yea.320070307"
    },
    {
      "key": "2021111418462429000_11.15.1912.17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0955-0674(92)90005-W"
    },
    {
      "key": "2021111418462429000_11.15.1912.18",
      "doi-asserted-by": "crossref",
      "first-page": "446",
      "DOI": "10.1016/0168-9525(92)90329-3",
      "article-title": "Mating-type gene switching in Saccharomyces cerevisiae.",
      "volume": "8",
      "year": "1992",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2021111418462429000_11.15.1912.19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00352100"
    },
    {
      "key": "2021111418462429000_11.15.1912.20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/274891a0"
    },
    {
      "key": "2021111418462429000_11.15.1912.21",
      "first-page": "1293",
      "article-title": "Two different types of double strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52 independent, nonhomologous recombination events.",
      "volume": "14",
      "author": "Kramer",
      "year": "1994",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111418462429000_11.15.1912.22",
      "doi-asserted-by": "crossref",
      "first-page": "6662",
      "DOI": "10.1002/j.1460-2075.1996.tb01056.x",
      "article-title": "Reconstitution of DNA base excision-repair with purified human proteins: Interaction between DNA polymerase \u03b2 and the XRCC1 protein.",
      "volume": "15",
      "author": "Kubota",
      "year": "1996",
      "journal-title": "EMBO J."
    },
    {
      "key": "2021111418462429000_11.15.1912.23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.bi.61.070192.001343"
    },
    {
      "key": "2021111418462429000_11.15.1912.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.17.11550"
    },
    {
      "key": "2021111418462429000_11.15.1912.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.14.7910"
    },
    {
      "key": "2021111418462429000_11.15.1912.26",
      "first-page": "1278",
      "article-title": "Homologous, homeologous, and illegitimate repair of double-strand breaks during transformation of a wild-type strain and a rad52 mutant strain of Saccharomyces cerevisiae.",
      "volume": "14",
      "author": "Mezard",
      "year": "1994",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111418462429000_11.15.1912.27",
      "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": "2021111418462429000_11.15.1912.28",
      "doi-asserted-by": "crossref",
      "first-page": "2164",
      "DOI": "10.1128/MCB.16.5.2164",
      "article-title": "Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae.",
      "volume": "16",
      "author": "Moore",
      "year": "1996",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111418462429000_11.15.1912.29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi962281m"
    },
    {
      "key": "2021111418462429000_11.15.1912.30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01924007"
    },
    {
      "key": "2021111418462429000_11.15.1912.31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90046-2"
    },
    {
      "key": "2021111418462429000_11.15.1912.32",
      "first-page": "407",
      "article-title": "Recombination in yeast.",
      "volume": "1",
      "author": "Petes",
      "year": "1991",
      "journal-title": "The molecular and cellular biology of the yeast  Saccharomyces:  Genome dynamics, protein synthesis and energetics"
    },
    {
      "key": "2021111418462429000_11.15.1912.33",
      "doi-asserted-by": "crossref",
      "first-page": "4303",
      "DOI": "10.1128/MCB.15.8.4303",
      "article-title": "DNA ligase I mediates essential functions in mammalian cells.",
      "volume": "15",
      "author": "Petrini",
      "year": "1995",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111418462429000_11.15.1912.34",
      "first-page": "310",
      "article-title": "Aberrant DNA repair and DNA replication due to an inherited enzymatic defect in human DNA ligase I.",
      "volume": "14",
      "author": "Prigent",
      "year": "1994",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111418462429000_11.15.1912.35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/25.8.1485"
    },
    {
      "key": "2021111418462429000_11.15.1912.36",
      "doi-asserted-by": "crossref",
      "first-page": "3789",
      "DOI": "10.1016/S0021-9258(17)41929-6",
      "article-title": "Different active sites of mammalian DNA ligases I and II.",
      "volume": "269",
      "author": "Roberts",
      "year": "1994",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2021111418462429000_11.15.1912.37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.39.24257"
    },
    {
      "key": "2021111418462429000_11.15.1912.38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.92.23.10450"
    },
    {
      "key": "2021111418462429000_11.15.1912.39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.17.7585"
    },
    {
      "key": "2021111418462429000_11.15.1912.40",
      "first-page": "4493",
      "article-title": "Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae.",
      "volume": "14",
      "author": "Schiestl",
      "year": "1994",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111418462429000_11.15.1912.41",
      "unstructured": "Sherman F. Fink G.K. Hicks J.B. (1982) Methods in yeast genetics. (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY)."
    },
    {
      "key": "2021111418462429000_11.15.1912.42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1995.mmi_17030405.x"
    },
    {
      "key": "2021111418462429000_11.15.1912.43",
      "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": "2021111418462429000_11.15.1912.44",
      "doi-asserted-by": "crossref",
      "first-page": "745",
      "DOI": "10.1093/genetics/76.4.745",
      "article-title": "Are mitotic functions required in meiosis?",
      "volume": "76",
      "author": "Simchen",
      "year": "1974",
      "journal-title": "Genetics"
    },
    {
      "key": "2021111418462429000_11.15.1912.45",
      "doi-asserted-by": "crossref",
      "first-page": "307",
      "DOI": "10.1007/BF00260499",
      "article-title": "Recombination and mating-type switching in a ligase-deficient mutant of Schizosaccharomyces pombe.",
      "volume": "220",
      "author": "Sipiczki",
      "year": "1990",
      "journal-title": "Mol. & Gen. Genet."
    },
    {
      "key": "2021111418462429000_11.15.1912.46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0061(199609)12:10B<1091::AID-YEA22>3.0.CO;2-I"
    },
    {
      "key": "2021111418462429000_11.15.1912.47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81260-X"
    },
    {
      "key": "2021111418462429000_11.15.1912.48",
      "doi-asserted-by": "crossref",
      "unstructured": "Teo, S.-H. and S.P. Jackson. 1997. Identification of Saccharomyces cerevisiae DNA ligase IV: Involvement in DNA double-strand-break repair. EMBO J. (in press)..",
      "DOI": "10.1093/emboj/16.15.4788"
    },
    {
      "key": "2021111418462429000_11.15.1912.49",
      "first-page": "6160",
      "article-title": "Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange.",
      "volume": "10",
      "author": "Thompson",
      "year": "1990",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111418462429000_11.15.1912.50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.2.400"
    },
    {
      "key": "2021111418462429000_11.15.1912.51",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00162a013"
    },
    {
      "key": "2021111418462429000_11.15.1912.52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/24.11.2067"
    },
    {
      "key": "2021111418462429000_11.15.1912.53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/yea.320101310"
    },
    {
      "key": "2021111418462429000_11.15.1912.54",
      "doi-asserted-by": "crossref",
      "first-page": "10923",
      "DOI": "10.1016/S0021-9258(17)34146-7",
      "article-title": "Reconstitution of complete SV40 DNA replication with purified replication factors.",
      "volume": "269",
      "author": "Waga",
      "year": "1994",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2021111418462429000_11.15.1912.55",
      "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."
    }
  ],
  "container-title": "Genes &amp; Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1101/gad.11.15.1912",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        11,
        15
      ]
    ],
    "date-time": "2021-11-15T03:04:59Z",
    "timestamp": 1636945499000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "http://genesdev.cshlp.org/lookup/doi/10.1101/gad.11.15.1912"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1997,
        8,
        1
      ]
    ]
  },
  "references-count": 55,
  "journal-issue": {
    "issue": "15",
    "published-print": {
      "date-parts": [
        [
          1997,
          8,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1101/gad.11.15.1912"
  ],
  "URL": "http://dx.doi.org/10.1101/gad.11.15.1912",
  "relation": {},
  "ISSN": [
    "0890-9369",
    "1549-5477"
  ],
  "subject": [],
  "container-title-short": "Genes Dev.",
  "published": {
    "date-parts": [
      [
        1997,
        8,
        1
      ]
    ]
  }
}