DOI: 10.1101/gad.5.6.958. A group of interacting yeast DNA replication genes.

A group of interacting yeast DNA replication genes.

10.1101/gad.5.6.958

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

Mutations in the cell-division-cycle genes CDC46 and CDC47 were originally isolated as suppressors of mutations in two other cell-division-cycle genes (CDC45 and CDC54). We found several combinations of mutations in these genes that result in allele-specific suppression and synthetic lethality, confirming that this set of genes forms a group of genetically interacting components. Here, we show that the other genes, like CDC46, are all involved in an early step of DNA replication, possibly initiation of DNA synthesis. Mutants defective in each of the four genes exhibit high rates of mitotic chromosome loss and recombination. The mutants appear also to accumulate chromosome damage that can be detected by a novel chromosome electrophoresis assay. Conditional mutants in this group, under fully nonpermissive conditions, show cell-cycle arrest at the beginning of DNA synthesis; under less stringent conditions, some arrest later, in S-phase. The DNA sequence of the CDC46 gene indicates that the protein is a member of a new family of genes apparently required for DNA initiation, with family members now identified in Saccharomyces cerevisiae, Schizosaccharomyces pombe, and mouse cells.

Bibliography

Hennessy, K. M., Lee, A., Chen, E., & Botstein, D. (1991). A group of interacting yeast DNA replication genes. Genes & Development, 5(6), 958â969.

Authors 4

K M Hennessy (first)
A Lee (additional)
E Chen (additional)
D Botstein (additional)

References 49 Referenced 222

10.1126/science.2643162
10.1016/S0021-9258(17)39688-6 / J. Biol. Chem. / Yeast LEU2: Repression of mRNA levels by leucine and primary structure of the gene product. (1984)
10.1038/300706a0
10.1038/332546a0
10.1016/0076-6879(87)54076-9
10.1126/science.3287619
10.1002/j.1460-2075.1988.tb02948.x / EMBO J. / Primary structure and develpmental expression pattern of Hox 3.1, a member of the murine Hox 3 homeobox gene cluster. (1988)
{'key': '2021111320181452000_5.6.958.8', 'first-page': '365', 'article-title': 'DNA polymerase I is required for premeiotic DNA replication and sporulation but not for X-ray repair in Saccharomyces cerevisiae.', 'volume': '9', 'year': '1989', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / DNA polymerase I is required for premeiotic DNA replication and sporulation but not for X-ray repair in Saccharomyces cerevisiae. (1989)
Carson, M.J. 1987. CDC17, the structural gene for DNA polymerase I of yeast: Mitotic hyperrecombination and effects on telomere metabolism, Ph.D. thesis. University of Washington, Seattle.
{'key': '2021111320181452000_5.6.958.10', 'first-page': '4675', 'article-title': 'DAF1, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae.', 'volume': '8', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / DAF1, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae. (1988)
Davis, R., D. Botstein, and J. Roth. 1980. Advanced bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
10.1093/nar/10.8.2625
{'key': '2021111320181452000_5.6.958.13', 'first-page': '3081', 'article-title': 'A single essential gene, PRI2, encodes the large subunit of DNA primase in Saccharomyces cerevisiae.', 'volume': '9', 'year': '1989', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / A single essential gene, PRI2, encodes the large subunit of DNA primase in Saccharomyces cerevisiae. (1989)
{'key': '2021111320181452000_5.6.958.14', 'first-page': '5707', 'article-title': 'The phenotype of the minichromosome maintenance mutant mcm3 is characteristic of mutants defective in DNA replication.', 'volume': '10', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / The phenotype of the minichromosome maintenance mutant mcm3 is characteristic of mutants defective in DNA replication. (1990)
10.1073/pnas.86.16.6255
10.1016/0022-2836(76)90183-2
10.1073/pnas.66.2.352
10.1093/genetics/110.3.381 / Genetics / Altered fidelity of mitotic chromosome transmission in cell cycle mutants of S. cerevisiae. (1985)
10.1126/science.2683079
10.1101/gad.4.12b.2252
{'key': '2021111320181452000_5.6.958.21', 'first-page': '159', 'article-title': 'DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage.', 'volume': '9', 'year': '1989', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. (1989)
10.1083/jcb.106.6.1997
10.1007/BF00394305
10.1002/yea.320030405
10.1038/274891a0
10.1093/nar/15.13.5017
10.1016/0092-8674(84)90344-1
10.1038/327031a0
10.1093/genetics/106.3.365 / Genetics / Mutants of S. cerevisiae defective in the maintenance of minichromosomes. (1984)
Maniatis, T., E.F. Fritsch, and J. Sambrook. 1982. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
10.1016/S0021-9258(17)43493-4 / J. Biol. Chem. / Gene amplification in a single cell cycle in chinese hamster ovary cells. (1984)
10.1093/genetics/100.4.565 / Genetics / Determination of the order of gene function in the yeast nuclear division pathway using cs and ts mutants. (1982)
10.1093/genetics/100.4.547 / Genetics / Cold-sensitive cell-division-cycle mutants of yeast: Properties and pseudoreversion studies. (1982)
10.1002/yea.320050503
10.1128/mr.52.4.568-601.1988 / Microbiol. Rev. / Yeast chromosome replication and segregation. (1988)
10.1038/344503a0
Pringle, J.R. and L.H. Hartwell. 1981. The Saccharomyces cerevisiae cell cycle. In The molecular biology of the yeast Saccharomyces: Life cycle and inheritance (ed. J.N. Strathern, E.W. Jones, and J.R. Broach), pp. 97–142. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
{'key': '2021111320181452000_5.6.958.38', 'first-page': '135', 'article-title': 'Regulation of enzyme levels by proteolysis: The role of PEST regions.', 'volume': '627', 'year': '1988', 'journal-title': 'Adv. Enz. Reg.'} / Adv. Enz. Reg. / Regulation of enzyme levels by proteolysis: The role of PEST regions. (1988)
{'key': '2021111320181452000_5.6.958.39', 'first-page': '761', 'article-title': 'Superkiller mutations in Saccharomyces cerevisiae suppress exclusion of M2 double-stranded RNA by L-A-HN and confer cold sensitivity in the presence of M and L-A-HN.', 'volume': '4', 'year': '1984', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Superkiller mutations in Saccharomyces cerevisiae suppress exclusion of M2 double-stranded RNA by L-A-HN and confer cold sensitivity in the presence of M and L-A-HN. (1984)
10.1126/science.2876518
Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
10.1073/pnas.74.12.5463
{'key': '2021111320181452000_5.6.958.43', 'first-page': '3711', 'article-title': 'Two functional α-tubulin genes of the yeast Saccharomyces cerevisiae encode divergent proteins.', 'volume': '6', 'year': '1986', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Two functional α-tubulin genes of the yeast Saccharomyces cerevisiae encode divergent proteins. (1986)
Sherman, F., G. Fink, and C. Lawrence. 1974. Methods in yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
10.1016/0092-8674(89)90582-5
10.1128/jb.113.1.263-270.1973 / J. Bacteriol. / Effect of reversible inhibition of deoxyribonucleic acid synthesis on the yeast cell cycle. (1973)
10.1093/genetics/119.2.249 / Genetics / Unlinked noncomplementation: Isolation of new conditional-lethal mutations in each of the tubulin genes of Saccharomyces cerevisiae. (1988)
10.1021/bi00406a024
10.1016/S0022-2836(83)80017-5

Dates

Type	When
Created	18 years, 2 months ago (June 5, 2007, 5:15 p.m.)
Deposited	3 years, 9 months ago (Nov. 13, 2021, 11:18 p.m.)
Indexed	4 months, 4 weeks ago (March 31, 2025, 2:05 a.m.)
Issued	34 years, 2 months ago (June 1, 1991)
Published	34 years, 2 months ago (June 1, 1991)
Published Online	34 years, 2 months ago (June 1, 1991)
Published Print	34 years, 2 months ago (June 1, 1991)

Funders 0

None

BibTeX

@article{Hennessy_1991, title={A group of interacting yeast DNA replication genes.}, volume={5}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.5.6.958}, DOI={10.1101/gad.5.6.958}, number={6}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Hennessy, K M and Lee, A and Chen, E and Botstein, D}, year={1991}, month=jun, pages={958–969} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        3,
        31
      ]
    ],
    "date-time": "2025-03-31T06:05:12Z",
    "timestamp": 1743401112122
  },
  "reference-count": 49,
  "publisher": "Cold Spring Harbor Laboratory",
  "issue": "6",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1991,
        6
      ]
    ]
  },
  "abstract": "<jats:p>Mutations in the cell-division-cycle genes CDC46 and CDC47 were originally isolated as suppressors of mutations in two other cell-division-cycle genes (CDC45 and CDC54). We found several combinations of mutations in these genes that result in allele-specific suppression and synthetic lethality, confirming that this set of genes forms a group of genetically interacting components. Here, we show that the other genes, like CDC46, are all involved in an early step of DNA replication, possibly initiation of DNA synthesis. Mutants defective in each of the four genes exhibit high rates of mitotic chromosome loss and recombination. The mutants appear also to accumulate chromosome damage that can be detected by a novel chromosome electrophoresis assay. Conditional mutants in this group, under fully nonpermissive conditions, show cell-cycle arrest at the beginning of DNA synthesis; under less stringent conditions, some arrest later, in S-phase. The DNA sequence of the CDC46 gene indicates that the protein is a member of a new family of genes apparently required for DNA initiation, with family members now identified in Saccharomyces cerevisiae, Schizosaccharomyces pombe, and mouse cells.</jats:p>",
  "DOI": "10.1101/gad.5.6.958",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        6,
        5
      ]
    ],
    "date-time": "2007-06-05T21:15:46Z",
    "timestamp": 1181078146000
  },
  "page": "958-969",
  "source": "Crossref",
  "is-referenced-by-count": 222,
  "title": "A group of interacting yeast DNA replication genes.",
  "prefix": "10.1101",
  "volume": "5",
  "author": [
    {
      "given": "K M",
      "family": "Hennessy",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "A",
      "family": "Lee",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "E",
      "family": "Chen",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "D",
      "family": "Botstein",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "246",
  "published-online": {
    "date-parts": [
      [
        1991,
        6,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2021111320181452000_5.6.958.1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2643162"
    },
    {
      "key": "2021111320181452000_5.6.958.2",
      "doi-asserted-by": "crossref",
      "first-page": "8059",
      "DOI": "10.1016/S0021-9258(17)39688-6",
      "article-title": "Yeast LEU2: Repression of mRNA levels by leucine and primary structure of the gene product.",
      "volume": "259",
      "year": "1984",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2021111320181452000_5.6.958.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/300706a0"
    },
    {
      "key": "2021111320181452000_5.6.958.4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/332546a0"
    },
    {
      "key": "2021111320181452000_5.6.958.5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0076-6879(87)54076-9"
    },
    {
      "key": "2021111320181452000_5.6.958.6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3287619"
    },
    {
      "key": "2021111320181452000_5.6.958.7",
      "doi-asserted-by": "crossref",
      "first-page": "1329",
      "DOI": "10.1002/j.1460-2075.1988.tb02948.x",
      "article-title": "Primary structure and develpmental expression pattern of Hox 3.1, a member of the murine Hox 3 homeobox gene cluster.",
      "volume": "7",
      "year": "1988",
      "journal-title": "EMBO J."
    },
    {
      "key": "2021111320181452000_5.6.958.8",
      "first-page": "365",
      "article-title": "DNA polymerase I is required for premeiotic DNA replication and sporulation but not for X-ray repair in Saccharomyces cerevisiae.",
      "volume": "9",
      "year": "1989",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320181452000_5.6.958.9",
      "unstructured": "Carson, M.J. 1987. CDC17, the structural gene for DNA polymerase I of yeast: Mitotic hyperrecombination and effects on telomere metabolism, Ph.D. thesis. University of Washington, Seattle."
    },
    {
      "key": "2021111320181452000_5.6.958.10",
      "first-page": "4675",
      "article-title": "DAF1, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae.",
      "volume": "8",
      "year": "1988",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320181452000_5.6.958.11",
      "unstructured": "Davis, R., D. Botstein, and J. Roth. 1980. Advanced bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York."
    },
    {
      "key": "2021111320181452000_5.6.958.12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/10.8.2625"
    },
    {
      "key": "2021111320181452000_5.6.958.13",
      "first-page": "3081",
      "article-title": "A single essential gene, PRI2, encodes the large subunit of DNA primase in Saccharomyces cerevisiae.",
      "volume": "9",
      "year": "1989",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320181452000_5.6.958.14",
      "first-page": "5707",
      "article-title": "The phenotype of the minichromosome maintenance mutant mcm3 is characteristic of mutants defective in DNA replication.",
      "volume": "10",
      "year": "1990",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320181452000_5.6.958.15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.16.6255"
    },
    {
      "key": "2021111320181452000_5.6.958.16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(76)90183-2"
    },
    {
      "key": "2021111320181452000_5.6.958.17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.66.2.352"
    },
    {
      "key": "2021111320181452000_5.6.958.18",
      "doi-asserted-by": "crossref",
      "first-page": "381",
      "DOI": "10.1093/genetics/110.3.381",
      "article-title": "Altered fidelity of mitotic chromosome transmission in cell cycle mutants of S. cerevisiae.",
      "volume": "110",
      "year": "1985",
      "journal-title": "Genetics"
    },
    {
      "key": "2021111320181452000_5.6.958.19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2683079"
    },
    {
      "key": "2021111320181452000_5.6.958.20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.4.12b.2252"
    },
    {
      "key": "2021111320181452000_5.6.958.21",
      "first-page": "159",
      "article-title": "DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage.",
      "volume": "9",
      "year": "1989",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320181452000_5.6.958.22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.106.6.1997"
    },
    {
      "key": "2021111320181452000_5.6.958.23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00394305"
    },
    {
      "key": "2021111320181452000_5.6.958.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/yea.320030405"
    },
    {
      "key": "2021111320181452000_5.6.958.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/274891a0"
    },
    {
      "key": "2021111320181452000_5.6.958.26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/15.13.5017"
    },
    {
      "key": "2021111320181452000_5.6.958.27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(84)90344-1"
    },
    {
      "key": "2021111320181452000_5.6.958.28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/327031a0"
    },
    {
      "key": "2021111320181452000_5.6.958.29",
      "doi-asserted-by": "crossref",
      "first-page": "365",
      "DOI": "10.1093/genetics/106.3.365",
      "article-title": "Mutants of S. cerevisiae defective in the maintenance of minichromosomes.",
      "volume": "106",
      "year": "1984",
      "journal-title": "Genetics"
    },
    {
      "key": "2021111320181452000_5.6.958.30",
      "unstructured": "Maniatis, T., E.F. Fritsch, and J. Sambrook. 1982. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York."
    },
    {
      "key": "2021111320181452000_5.6.958.31",
      "doi-asserted-by": "crossref",
      "first-page": "1901",
      "DOI": "10.1016/S0021-9258(17)43493-4",
      "article-title": "Gene amplification in a single cell cycle in chinese hamster ovary cells.",
      "volume": "259",
      "year": "1984",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2021111320181452000_5.6.958.32",
      "doi-asserted-by": "crossref",
      "first-page": "565",
      "DOI": "10.1093/genetics/100.4.565",
      "article-title": "Determination of the order of gene function in the yeast nuclear division pathway using cs and ts mutants.",
      "volume": "100",
      "year": "1982",
      "journal-title": "Genetics"
    },
    {
      "key": "2021111320181452000_5.6.958.33",
      "doi-asserted-by": "crossref",
      "first-page": "547",
      "DOI": "10.1093/genetics/100.4.547",
      "article-title": "Cold-sensitive cell-division-cycle mutants of yeast: Properties and pseudoreversion studies.",
      "volume": "100",
      "year": "1982",
      "journal-title": "Genetics"
    },
    {
      "key": "2021111320181452000_5.6.958.34",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/yea.320050503"
    },
    {
      "key": "2021111320181452000_5.6.958.35",
      "doi-asserted-by": "crossref",
      "first-page": "568",
      "DOI": "10.1128/mr.52.4.568-601.1988",
      "article-title": "Yeast chromosome replication and segregation.",
      "volume": "52",
      "year": "1988",
      "journal-title": "Microbiol. Rev."
    },
    {
      "key": "2021111320181452000_5.6.958.36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/344503a0"
    },
    {
      "key": "2021111320181452000_5.6.958.37",
      "unstructured": "Pringle, J.R. and L.H. Hartwell. 1981. The Saccharomyces cerevisiae cell cycle. In The molecular biology of the yeast Saccharomyces: Life cycle and inheritance (ed. J.N. Strathern, E.W. Jones, and J.R. Broach), pp. 97\u2013142. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York."
    },
    {
      "key": "2021111320181452000_5.6.958.38",
      "first-page": "135",
      "article-title": "Regulation of enzyme levels by proteolysis: The role of PEST regions.",
      "volume": "627",
      "year": "1988",
      "journal-title": "Adv. Enz. Reg."
    },
    {
      "key": "2021111320181452000_5.6.958.39",
      "first-page": "761",
      "article-title": "Superkiller mutations in Saccharomyces cerevisiae suppress exclusion of M2 double-stranded RNA by L-A-HN and confer cold sensitivity in the presence of M and L-A-HN.",
      "volume": "4",
      "year": "1984",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320181452000_5.6.958.40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2876518"
    },
    {
      "key": "2021111320181452000_5.6.958.41",
      "unstructured": "Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York."
    },
    {
      "key": "2021111320181452000_5.6.958.42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.74.12.5463"
    },
    {
      "key": "2021111320181452000_5.6.958.43",
      "first-page": "3711",
      "article-title": "Two functional \u03b1-tubulin genes of the yeast Saccharomyces cerevisiae encode divergent proteins.",
      "volume": "6",
      "year": "1986",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320181452000_5.6.958.44",
      "unstructured": "Sherman, F., G. Fink, and C. Lawrence. 1974. Methods in yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York."
    },
    {
      "key": "2021111320181452000_5.6.958.45",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90582-5"
    },
    {
      "key": "2021111320181452000_5.6.958.46",
      "doi-asserted-by": "crossref",
      "first-page": "263",
      "DOI": "10.1128/jb.113.1.263-270.1973",
      "article-title": "Effect of reversible inhibition of deoxyribonucleic acid synthesis on the yeast cell cycle.",
      "volume": "113",
      "year": "1973",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2021111320181452000_5.6.958.47",
      "doi-asserted-by": "crossref",
      "first-page": "249",
      "DOI": "10.1093/genetics/119.2.249",
      "article-title": "Unlinked noncomplementation: Isolation of new conditional-lethal mutations in each of the tubulin genes of Saccharomyces cerevisiae.",
      "volume": "119",
      "year": "1988",
      "journal-title": "Genetics"
    },
    {
      "key": "2021111320181452000_5.6.958.48",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00406a024"
    },
    {
      "key": "2021111320181452000_5.6.958.49",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0022-2836(83)80017-5"
    }
  ],
  "container-title": "Genes &amp; Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1101/gad.5.6.958",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        11,
        14
      ]
    ],
    "date-time": "2021-11-14T04:18:54Z",
    "timestamp": 1636863534000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "http://genesdev.cshlp.org/lookup/doi/10.1101/gad.5.6.958"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1991,
        6
      ]
    ]
  },
  "references-count": 49,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          1991,
          6
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1101/gad.5.6.958"
  ],
  "URL": "http://dx.doi.org/10.1101/gad.5.6.958",
  "relation": {},
  "ISSN": [
    "0890-9369",
    "1549-5477"
  ],
  "subject": [],
  "container-title-short": "Genes Dev.",
  "published": {
    "date-parts": [
      [
        1991,
        6
      ]
    ]
  }
}