DOI: 10.1101/gad.1683308. Cdc7–Drf1 kinase links chromosome cohesion to the initiation of DNA replication in <i>Xenopus</i> egg extracts

Cdc7–Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts

10.1101/gad.1683308

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

To establish functional cohesion between replicated sister chromatids, cohesin is recruited to chromatin before S phase. Cohesin is loaded onto chromosomes in the G1 phase by the Scc2–Scc4 complex, but little is known about how Scc2–Scc4 itself is recruited to chromatin. Using Xenopus egg extracts as a vertebrate model system, we showed previously that the chromatin association of Scc2 and cohesin is dependent on the prior establishment of prereplication complexes (pre-RCs) at origins of replication. Here, we report that Scc2–Scc4 exists in a stable complex with the Cdc7–Drf1 protein kinase (DDK), which is known to bind pre-RCs and activate them for DNA replication. Immunodepletion of DDK from Xenopus egg extracts impairs chromatin association of Scc2–Scc4, a defect that is reversed by wild-type, but not catalytically inactive DDK. A complex of Scc4 and the N terminus of Scc2 is sufficient for chromatin loading of Scc2–Scc4, but not for cohesin recruitment. These results show that DDK is required to tether Scc2–Scc4 to pre-RCs, and they underscore the intimate link between early steps in DNA replication and cohesion.

Bibliography

Takahashi, T. S., Basu, A., Bermudez, V., Hurwitz, J., & Walter, J. C. (2008). Cdc7âDrf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts. Genes & Development, 22(14), 1894â1905.

Authors 5

Tatsuro S. Takahashi (first)
Abhijit Basu (additional)
Vladimir Bermudez (additional)
Jerard Hurwitz (additional)
Johannes C. Walter (additional)

References 79 Referenced 108

10.1038/ncb1069
10.1146/annurev.biochem.71.110601.135425
10.1073/pnas.1434308100
10.1016/j.cub.2006.03.037
10.1083/jcb.122.5.993
10.1016/0092-8674(86)90622-7
10.1038/375418a0
10.1016/S1097-2765(00)80420-7
10.1016/S0378-1119(99)00160-2
10.1101/gad.12.21.3408
10.1038/ncb1382
10.1016/j.cub.2004.07.053
10.1128/MCB.21.9.3144-3158.2001
10.1073/pnas.94.7.3151
10.1371/journal.pbio.0030069
10.1038/nrm1909
10.1098/rstb.2004.1609
10.1002/j.1460-2075.1993.tb06140.x / EMBO J. / Chromosomal replication initiates and terminates at random sequences but at regular intervals in the ribosomal DNA of Xenopus early embryos by Hyrien, (1993)
10.1016/j.cell.2005.07.018
10.1016/j.molcel.2007.07.002
{'key': '2021111608064236000_22.14.1894.21', 'first-page': '2899', 'article-title': 'Cell cycle regulation of the yeast Cdc7 protein kinase by association with the Dbf4 protein', 'volume': '13', 'author': 'Jackson,', 'year': '1993', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Cell cycle regulation of the yeast Cdc7 protein kinase by association with the Dbf4 protein by Jackson, (1993)
10.1101/gad.14.12.1528 / Genes & Dev. / Xenopus cdc7 function is dependent on licensing but not on XORC, XCdc6, or CDK activity and is required for XCdc45 loading by Jares, (2000)
10.1186/1471-2199-5-5
10.1093/emboj/18.20.5703
10.1128/MCB.23.8.2999-3007.2003
10.1038/ng1364
10.1016/0092-8674(95)90081-0
10.1101/gad.1070003
10.1128/MCB.19.7.5083 / Mol. Cell. Biol. / A novel growth- and cell cycle-regulated protein, ASK, activates human Cdc7-related kinase and is essential for G1/S transition in mammalian cells by Kumagai, (1999)
10.1038/nature02742
10.1016/j.molcel.2006.08.018
10.1007/s00412-007-0104-x
10.1101/gad.12.13.1986
10.1101/gad.249202
10.1101/gad.1246404
10.1002/jcp.10070
10.1074/jbc.M002713200
10.1074/jbc.M608935200
10.1016/S1097-2765(01)00254-4
10.1128/MCB.20.22.8602-8612.2000
{'key': '2021111608064236000_22.14.1894.41', 'first-page': '5724', 'article-title': 'Evidence that POB1, a Saccharomyces cerevisiae protein that binds to DNA polymerase α, acts in DNA metabolism in vivo', 'volume': '12', 'author': 'Miles,', 'year': '1992', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Evidence that POB1, a Saccharomyces cerevisiae protein that binds to DNA polymerase α, acts in DNA metabolism in vivo by Miles, (1992)
10.1371/journal.pgen.0030012
10.1038/nature03024
10.1007/s00412-007-0129-1
10.1016/j.molcel.2006.07.007
10.1093/emboj/21.12.3171
10.1074/jbc.M512921200
10.1073/pnas.0602400103
10.1146/annurev.biochem.74.082803.133219
10.1101/gr.147400
10.1038/sj.emboj.7600369
10.1016/j.molcel.2006.01.030
10.1126/science.1097639
10.1128/MCB.24.8.3100-3111.2004
10.1242/jcs.113.12.2111 / J. Cell Sci. / Cdc7p–Dbf4p becomes famous in the cell cycle by Sclafani, (2000)
10.1371/journal.pbio.0040242
10.1016/j.molcel.2006.07.033
10.1074/jbc.M510278200
10.1101/gad.13.3.307
10.1083/jcb.151.4.749
10.1101/gad.1339805
10.1038/ncb1177
10.1101/gad.1065903
10.1091/mbc.12.5.1257
10.1038/nature05465
10.1038/ng1363
10.1101/gad.13.3.320
10.1016/S0960-9822(98)70463-4
10.1016/S0092-8674(00)00130-6
10.1016/S0092-8674(00)00132-X
10.1074/jbc.M008107200
10.1126/science.275.5302.993
10.1016/S1097-2765(00)80241-5
10.1016/S1097-2765(00)80052-0
10.1016/j.cub.2006.03.049
10.1074/jbc.M307144200
10.1074/jbc.M411653200
10.1038/nature05432
10.1128/MCB.20.9.3086-3096.2000

Dates

Type	When
Created	17 years, 1 month ago (July 15, 2008, 1:34 p.m.)
Deposited	3 years, 9 months ago (Nov. 16, 2021, 12:16 p.m.)
Indexed	4 days, 4 hours ago (Sept. 3, 2025, 6:25 a.m.)
Issued	17 years, 1 month ago (July 15, 2008)
Published	17 years, 1 month ago (July 15, 2008)
Published Online	17 years, 1 month ago (July 15, 2008)
Published Print	17 years, 1 month ago (July 15, 2008)

Funders 0

None

BibTeX

@article{Takahashi_2008, title={Cdc7–Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts}, volume={22}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.1683308}, DOI={10.1101/gad.1683308}, number={14}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Takahashi, Tatsuro S. and Basu, Abhijit and Bermudez, Vladimir and Hurwitz, Jerard and Walter, Johannes C.}, year={2008}, month=jul, pages={1894–1905} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        9,
        3
      ]
    ],
    "date-time": "2025-09-03T10:25:57Z",
    "timestamp": 1756895157522
  },
  "reference-count": 79,
  "publisher": "Cold Spring Harbor Laboratory",
  "issue": "14",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2008,
        7,
        15
      ]
    ]
  },
  "abstract": "<jats:p>To establish functional cohesion between replicated sister chromatids, cohesin is recruited to chromatin before S phase. Cohesin is loaded onto chromosomes in the G1 phase by the Scc2\u2013Scc4 complex, but little is known about how Scc2\u2013Scc4 itself is recruited to chromatin. Using <jats:italic>Xenopus</jats:italic> egg extracts as a vertebrate model system, we showed previously that the chromatin association of Scc2 and cohesin is dependent on the prior establishment of prereplication complexes (pre-RCs) at origins of replication. Here, we report that Scc2\u2013Scc4 exists in a stable complex with the Cdc7\u2013Drf1 protein kinase (DDK), which is known to bind pre-RCs and activate them for DNA replication. Immunodepletion of DDK from <jats:italic>Xenopus</jats:italic> egg extracts impairs chromatin association of Scc2\u2013Scc4, a defect that is reversed by wild-type, but not catalytically inactive DDK. A complex of Scc4 and the N terminus of Scc2 is sufficient for chromatin loading of Scc2\u2013Scc4, but not for cohesin recruitment. These results show that DDK is required to tether Scc2\u2013Scc4 to pre-RCs, and they underscore the intimate link between early steps in DNA replication and cohesion.</jats:p>",
  "DOI": "10.1101/gad.1683308",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2008,
        7,
        15
      ]
    ],
    "date-time": "2008-07-15T17:34:38Z",
    "timestamp": 1216143278000
  },
  "page": "1894-1905",
  "source": "Crossref",
  "is-referenced-by-count": 108,
  "title": "Cdc7\u2013Drf1 kinase links chromosome cohesion to the initiation of DNA replication in <i>Xenopus</i> egg extracts",
  "prefix": "10.1101",
  "volume": "22",
  "author": [
    {
      "given": "Tatsuro S.",
      "family": "Takahashi",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Abhijit",
      "family": "Basu",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Vladimir",
      "family": "Bermudez",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Jerard",
      "family": "Hurwitz",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Johannes C.",
      "family": "Walter",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "246",
  "published-online": {
    "date-parts": [
      [
        2008,
        7,
        15
      ]
    ]
  },
  "reference": [
    {
      "key": "2021111608064236000_22.14.1894.1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ncb1069"
    },
    {
      "key": "2021111608064236000_22.14.1894.2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.biochem.71.110601.135425"
    },
    {
      "key": "2021111608064236000_22.14.1894.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.1434308100"
    },
    {
      "key": "2021111608064236000_22.14.1894.4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.cub.2006.03.037"
    },
    {
      "key": "2021111608064236000_22.14.1894.5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.122.5.993"
    },
    {
      "key": "2021111608064236000_22.14.1894.6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(86)90622-7"
    },
    {
      "key": "2021111608064236000_22.14.1894.7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/375418a0"
    },
    {
      "key": "2021111608064236000_22.14.1894.8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1097-2765(00)80420-7"
    },
    {
      "key": "2021111608064236000_22.14.1894.9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0378-1119(99)00160-2"
    },
    {
      "key": "2021111608064236000_22.14.1894.10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.12.21.3408"
    },
    {
      "key": "2021111608064236000_22.14.1894.11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ncb1382"
    },
    {
      "key": "2021111608064236000_22.14.1894.12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.cub.2004.07.053"
    },
    {
      "key": "2021111608064236000_22.14.1894.13",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.21.9.3144-3158.2001"
    },
    {
      "key": "2021111608064236000_22.14.1894.14",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.94.7.3151"
    },
    {
      "key": "2021111608064236000_22.14.1894.15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.pbio.0030069"
    },
    {
      "key": "2021111608064236000_22.14.1894.16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nrm1909"
    },
    {
      "key": "2021111608064236000_22.14.1894.17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1098/rstb.2004.1609"
    },
    {
      "key": "2021111608064236000_22.14.1894.18",
      "doi-asserted-by": "crossref",
      "first-page": "4511",
      "DOI": "10.1002/j.1460-2075.1993.tb06140.x",
      "article-title": "Chromosomal replication initiates and terminates at random sequences but at regular intervals in the ribosomal DNA of Xenopus early embryos",
      "volume": "12",
      "author": "Hyrien,",
      "year": "1993",
      "journal-title": "EMBO J."
    },
    {
      "key": "2021111608064236000_22.14.1894.19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.cell.2005.07.018"
    },
    {
      "key": "2021111608064236000_22.14.1894.20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.molcel.2007.07.002"
    },
    {
      "key": "2021111608064236000_22.14.1894.21",
      "first-page": "2899",
      "article-title": "Cell cycle regulation of the yeast Cdc7 protein kinase by association with the Dbf4 protein",
      "volume": "13",
      "author": "Jackson,",
      "year": "1993",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111608064236000_22.14.1894.22",
      "doi-asserted-by": "crossref",
      "first-page": "1528",
      "DOI": "10.1101/gad.14.12.1528",
      "article-title": "Xenopus cdc7 function is dependent on licensing but not on XORC, XCdc6, or CDK activity and is required for XCdc45 loading",
      "volume": "14",
      "author": "Jares,",
      "year": "2000",
      "journal-title": "Genes & Dev."
    },
    {
      "key": "2021111608064236000_22.14.1894.23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1186/1471-2199-5-5"
    },
    {
      "key": "2021111608064236000_22.14.1894.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/18.20.5703"
    },
    {
      "key": "2021111608064236000_22.14.1894.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.23.8.2999-3007.2003"
    },
    {
      "key": "2021111608064236000_22.14.1894.26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ng1364"
    },
    {
      "key": "2021111608064236000_22.14.1894.27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(95)90081-0"
    },
    {
      "key": "2021111608064236000_22.14.1894.28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1070003"
    },
    {
      "key": "2021111608064236000_22.14.1894.29",
      "doi-asserted-by": "crossref",
      "first-page": "5083",
      "DOI": "10.1128/MCB.19.7.5083",
      "article-title": "A novel growth- and cell cycle-regulated protein, ASK, activates human Cdc7-related kinase and is essential for G1/S transition in mammalian cells",
      "volume": "19",
      "author": "Kumagai,",
      "year": "1999",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111608064236000_22.14.1894.30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature02742"
    },
    {
      "key": "2021111608064236000_22.14.1894.31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.molcel.2006.08.018"
    },
    {
      "key": "2021111608064236000_22.14.1894.32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s00412-007-0104-x"
    },
    {
      "key": "2021111608064236000_22.14.1894.33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.12.13.1986"
    },
    {
      "key": "2021111608064236000_22.14.1894.34",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.249202"
    },
    {
      "key": "2021111608064236000_22.14.1894.35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1246404"
    },
    {
      "key": "2021111608064236000_22.14.1894.36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jcp.10070"
    },
    {
      "key": "2021111608064236000_22.14.1894.37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M002713200"
    },
    {
      "key": "2021111608064236000_22.14.1894.38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M608935200"
    },
    {
      "key": "2021111608064236000_22.14.1894.39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1097-2765(01)00254-4"
    },
    {
      "key": "2021111608064236000_22.14.1894.40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.20.22.8602-8612.2000"
    },
    {
      "key": "2021111608064236000_22.14.1894.41",
      "first-page": "5724",
      "article-title": "Evidence that POB1, a Saccharomyces cerevisiae protein that binds to DNA polymerase \u03b1, acts in DNA metabolism in vivo",
      "volume": "12",
      "author": "Miles,",
      "year": "1992",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111608064236000_22.14.1894.42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.pgen.0030012"
    },
    {
      "key": "2021111608064236000_22.14.1894.43",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature03024"
    },
    {
      "key": "2021111608064236000_22.14.1894.44",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s00412-007-0129-1"
    },
    {
      "key": "2021111608064236000_22.14.1894.45",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.molcel.2006.07.007"
    },
    {
      "key": "2021111608064236000_22.14.1894.46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/21.12.3171"
    },
    {
      "key": "2021111608064236000_22.14.1894.47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M512921200"
    },
    {
      "key": "2021111608064236000_22.14.1894.48",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0602400103"
    },
    {
      "key": "2021111608064236000_22.14.1894.49",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.biochem.74.082803.133219"
    },
    {
      "key": "2021111608064236000_22.14.1894.50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gr.147400"
    },
    {
      "key": "2021111608064236000_22.14.1894.51",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/sj.emboj.7600369"
    },
    {
      "key": "2021111608064236000_22.14.1894.52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.molcel.2006.01.030"
    },
    {
      "key": "2021111608064236000_22.14.1894.53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1097639"
    },
    {
      "key": "2021111608064236000_22.14.1894.54",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.24.8.3100-3111.2004"
    },
    {
      "key": "2021111608064236000_22.14.1894.55",
      "doi-asserted-by": "crossref",
      "first-page": "2111",
      "DOI": "10.1242/jcs.113.12.2111",
      "article-title": "Cdc7p\u2013Dbf4p becomes famous in the cell cycle",
      "volume": "113",
      "author": "Sclafani,",
      "year": "2000",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2021111608064236000_22.14.1894.56",
      "doi-asserted-by": "publisher",
      "DOI": "10.1371/journal.pbio.0040242"
    },
    {
      "key": "2021111608064236000_22.14.1894.57",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.molcel.2006.07.033"
    },
    {
      "key": "2021111608064236000_22.14.1894.58",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M510278200"
    },
    {
      "key": "2021111608064236000_22.14.1894.59",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.13.3.307"
    },
    {
      "key": "2021111608064236000_22.14.1894.60",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.151.4.749"
    },
    {
      "key": "2021111608064236000_22.14.1894.61",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1339805"
    },
    {
      "key": "2021111608064236000_22.14.1894.62",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ncb1177"
    },
    {
      "key": "2021111608064236000_22.14.1894.63",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1065903"
    },
    {
      "key": "2021111608064236000_22.14.1894.64",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.12.5.1257"
    },
    {
      "key": "2021111608064236000_22.14.1894.65",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature05465"
    },
    {
      "key": "2021111608064236000_22.14.1894.66",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ng1363"
    },
    {
      "key": "2021111608064236000_22.14.1894.67",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.13.3.320"
    },
    {
      "key": "2021111608064236000_22.14.1894.68",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-9822(98)70463-4"
    },
    {
      "key": "2021111608064236000_22.14.1894.69",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)00130-6"
    },
    {
      "key": "2021111608064236000_22.14.1894.70",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)00132-X"
    },
    {
      "key": "2021111608064236000_22.14.1894.71",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M008107200"
    },
    {
      "key": "2021111608064236000_22.14.1894.72",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.275.5302.993"
    },
    {
      "key": "2021111608064236000_22.14.1894.73",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1097-2765(00)80241-5"
    },
    {
      "key": "2021111608064236000_22.14.1894.74",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1097-2765(00)80052-0"
    },
    {
      "key": "2021111608064236000_22.14.1894.75",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.cub.2006.03.049"
    },
    {
      "key": "2021111608064236000_22.14.1894.76",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M307144200"
    },
    {
      "key": "2021111608064236000_22.14.1894.77",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M411653200"
    },
    {
      "key": "2021111608064236000_22.14.1894.78",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature05432"
    },
    {
      "key": "2021111608064236000_22.14.1894.79",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.20.9.3086-3096.2000"
    }
  ],
  "container-title": "Genes &amp; Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1101/gad.1683308",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        11,
        16
      ]
    ],
    "date-time": "2021-11-16T17:16:28Z",
    "timestamp": 1637082988000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "http://genesdev.cshlp.org/lookup/doi/10.1101/gad.1683308"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2008,
        7,
        15
      ]
    ]
  },
  "references-count": 79,
  "journal-issue": {
    "issue": "14",
    "published-print": {
      "date-parts": [
        [
          2008,
          7,
          15
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1101/gad.1683308"
  ],
  "URL": "http://dx.doi.org/10.1101/gad.1683308",
  "relation": {
    "has-review": [
      {
        "id-type": "doi",
        "id": "10.3410/f.1119463.575662",
        "asserted-by": "object"
      }
    ]
  },
  "ISSN": [
    "0890-9369",
    "1549-5477"
  ],
  "subject": [],
  "container-title-short": "Genes Dev.",
  "published": {
    "date-parts": [
      [
        2008,
        7,
        15
      ]
    ]
  }
}