DOI: 10.1091/mbc.e07-02-0123. Nucleoporins Prevent DNA Damage Accumulation by Modulating Ulp1-dependent Sumoylation Processes

Nucleoporins Prevent DNA Damage Accumulation by Modulating Ulp1-dependent Sumoylation Processes

10.1091/mbc.e07-02-0123

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Increasing evidences suggest that nuclear pore complexes (NPCs) control different aspects of nuclear metabolism, including transcription, nuclear organization, and DNA repair. We previously established that the Nup84 complex, a major NPC building block, is part of a genetic network involved in DNA repair. Here, we show that double-strand break (DSB) appearance is linked to a shared function of the Nup84 and the Nup60/Mlp1–2 complexes. Mutants within these complexes exhibit similar genetic interactions and alteration in DNA repair processes as mutants of the SUMO-protease Ulp1. Consistently, these nucleoporins are required for maintenance of proper Ulp1 levels at NPCs and for the establishment of the appropriate sumoylation of several cellular proteins, including the DNA repair factor Yku70. Moreover, restoration of nuclear envelope-associated Ulp1 in nucleoporin mutants reestablishes proper sumoylation patterns and suppresses DSB accumulation and genetic interactions with DNA repair genes. Our results thus provide a molecular mechanism that underlies the connection between NPC and genome stability.

Bibliography

Palancade, B., Liu, X., Garcia-Rubio, M., Aguilera, A., Zhao, X., & Doye, V. (2007). Nucleoporins Prevent DNA Damage Accumulation by Modulating Ulp1-dependent Sumoylation Processes. Molecular Biology of the Cell, 18(8), 2912â2923.

Authors 6

Benoit Palancade (first)
Xianpeng Liu (additional)
Maria Garcia-Rubio (additional)
Andrès Aguilera (additional)
Xiaolan Zhao (additional)
Valérie Doye (additional)

References 51 Referenced 129

10.1128/MCB.22.23.8292-8301.2002 / Mol. Cell Biol by Andrulis E. D. (2002)
10.1091/mbc.9.12.3475
10.1371/journal.pbio.0020342 / PLoS Biol by Brickner J. H. (2004)
10.1038/nature04752 / Nature by Cabal G. G. (2006)
10.1101/gad.1307205 / Genes Dev by Casolari J. M. (2005)
10.1074/jbc.271.31.18477 / J. Biol. Chem by Corbett A. H. (1996)
10.1074/mcp.M400154-MCP200 / Mol. Cell Proteomics by Denison C. (2005)
10.1534/genetics.106.063438 / Genetics by De Souza C. P. (2006)
10.1128/MCB.00870-06 / Mol. Cell. Biol by Dieppois G. (2006)
10.1038/ncb756 / Nat. Cell Biol by Feuerbach F. (2002)
10.1093/emboj/cdf590 / EMBO J by Fischer T. (2002)
10.1016/S0092-8674(03)01026-2 / Cell by Galy V. (2004)
10.1038/47528 / Nature by Galy V. (2000)
10.1074/jbc.M413209200 / J. Biol. Chem by Hannich J. T. (2005)
10.1016/S1047-8477(02)00533-6 / J. Struct. Biol by Hediger F. (2002)
10.1093/nar/28.14.2779 / Nucleic Acids Res by Hegde V. (2000)
10.1074/jbc.M500947200 / J. Biol. Chem by Jacquiau H. R. (2005)
10.1093/genetics/161.3.1015 / Genetics by Karathanasis E. (2002)
10.1128/MCB.22.8.2544-2555.2002 / Mol. Cell Biol by Leslie D. M. (2002)
10.1083/jcb.200212052 / J. Cell Biol by Li S. J. (2003)
10.1016/j.biochi.2004.10.023 / Biochimie by Lisby M. (2005)
10.1016/j.dnarep.2004.11.010 / DNA Rep by Loeillet S. (2005)
10.1074/jbc.M608741200 / J. Biol. Chem by Luthra R. (2006)
10.1093/emboj/21.3.387 / EMBO J by Lutzmann M. (2002)
10.1083/jcb.200608066 / J. Cell Biol by Makhnevych T. (2007)
10.1016/j.molcel.2006.02.007 / Mol. Cell by Mendjan S. (2006)
10.1073/pnas.0501768102 / Proc. Natl. Acad. Sci. USA by Menon B. B. (2005)
10.1128/MCB.26.4.1424-1433.2006 / Mol. Cell Biol by Motegi A. (2006)
10.1093/genetics/157.1.103 / Genetics by Mullen J. R. (2001)
10.1091/mbc.e05-06-0527
10.1074/jbc.M407950200 / J. Biol. Chem by Panse V. G. (2004)
10.1038/ncb893 / Nat. Cell Biol by Panse V. G. (2003)
10.1038/nature03665 / Nature by Pfander B. (2005)
10.1093/genetics/143.4.1533 / Genetics by Piruat J. I. (1996)
10.1038/ncb1488 / Nat. Cell Biol by Sacher M. (2006)
10.1016/j.molcel.2005.12.012 / Mol. Cell by Schmid M. (2006)
10.1091/mbc.e05-01-0011
10.1128/MCB.25.10.3934-3944.2005 / Mol. Cell Biol by Shim E. Y. (2005)
10.1128/MCB.24.12.5130-5143.2004 / Mol. Cell Biol by Soustelle C. (2004)
10.1016/S1534-5807(03)00162-X / Dev. Cell by Suntharalingam M. (2003)
10.1038/sj.emboj.7600144 / EMBO J by Taddei A. (2004)
10.1038/nature04845 / Nature by Taddei A. (2006)
10.1083/jcb.200505159 / J. Cell Biol by Therizols P. (2006)
10.1083/jcb.200608141 / J. Cell Biol by Timney B. L. (2006)
10.1002/j.1460-2075.1991.tb07984.x / EMBO J by Tollervey D. (1991)
10.1534/genetics.105.052811 / Genetics by Wang Z. (2006)
10.1074/jbc.M409203200 / J. Biol. Chem by Wohlschlegel J. A. (2004)
10.1074/mcp.M400166-MCP200 / Mol. Cell Proteomics by Wykoff D. D. (2005)
10.1093/nar/gkl685 / Nucleic Acids Res by Yang L. (2006)
10.1073/pnas.0500537102 / Proc. Natl. Acad. Sci. USA by Zhao X. (2005)
10.1083/jcb.200405168 / J. Cell Biol by Zhao X. (2004)

Dates

Type	When
Created	18 years, 2 months ago (May 30, 2007, 9:10 p.m.)
Deposited	4 years ago (Aug. 14, 2021, 6:58 a.m.)
Indexed	3 weeks ago (Aug. 7, 2025, 4:23 p.m.)
Issued	18 years ago (Aug. 1, 2007)
Published	18 years ago (Aug. 1, 2007)
Published Print	18 years ago (Aug. 1, 2007)

Funders 0

None

BibTeX

@article{Palancade_2007, title={Nucleoporins Prevent DNA Damage Accumulation by Modulating Ulp1-dependent Sumoylation Processes}, volume={18}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e07-02-0123}, DOI={10.1091/mbc.e07-02-0123}, number={8}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Palancade, Benoit and Liu, Xianpeng and Garcia-Rubio, Maria and Aguilera, Andrès and Zhao, Xiaolan and Doye, Valérie}, editor={Weis, Karsten}, year={2007}, month=aug, pages={2912–2923} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        7
      ]
    ],
    "date-time": "2025-08-07T20:23:57Z",
    "timestamp": 1754598237290
  },
  "reference-count": 51,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "8",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2007,
        8
      ]
    ]
  },
  "abstract": "<jats:p>Increasing evidences suggest that nuclear pore complexes (NPCs) control different aspects of nuclear metabolism, including transcription, nuclear organization, and DNA repair. We previously established that the Nup84 complex, a major NPC building block, is part of a genetic network involved in DNA repair. Here, we show that double-strand break (DSB) appearance is linked to a shared function of the Nup84 and the Nup60/Mlp1\u20132 complexes. Mutants within these complexes exhibit similar genetic interactions and alteration in DNA repair processes as mutants of the SUMO-protease Ulp1. Consistently, these nucleoporins are required for maintenance of proper Ulp1 levels at NPCs and for the establishment of the appropriate sumoylation of several cellular proteins, including the DNA repair factor Yku70. Moreover, restoration of nuclear envelope-associated Ulp1 in nucleoporin mutants reestablishes proper sumoylation patterns and suppresses DSB accumulation and genetic interactions with DNA repair genes. Our results thus provide a molecular mechanism that underlies the connection between NPC and genome stability.</jats:p>",
  "DOI": "10.1091/mbc.e07-02-0123",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        5,
        31
      ]
    ],
    "date-time": "2007-05-31T01:10:44Z",
    "timestamp": 1180573844000
  },
  "page": "2912-2923",
  "source": "Crossref",
  "is-referenced-by-count": 129,
  "title": "Nucleoporins Prevent DNA Damage Accumulation by Modulating Ulp1-dependent Sumoylation Processes",
  "prefix": "10.1091",
  "volume": "18",
  "author": [
    {
      "given": "Benoit",
      "family": "Palancade",
      "sequence": "first",
      "affiliation": [
        {
          "name": "*Institut Curie, Centre de Recherche, and"
        },
        {
          "name": "Unit\u00e9 Mixte de Recherche 144 Centre National de la Recherche Scientifique, F-75248 Paris, France;"
        }
      ]
    },
    {
      "given": "Xianpeng",
      "family": "Liu",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10021; and"
        }
      ]
    },
    {
      "given": "Maria",
      "family": "Garcia-Rubio",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Molecular Biology, Centro Andaluz de Biologia Molecular y Medicina Regenerativa (CABIMER), Consejo Superior de Investigaciones Cientificas-Universidad de Sevilla, 41092 Sevilla, Spain"
        }
      ]
    },
    {
      "given": "Andr\u00e8s",
      "family": "Aguilera",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Molecular Biology, Centro Andaluz de Biologia Molecular y Medicina Regenerativa (CABIMER), Consejo Superior de Investigaciones Cientificas-Universidad de Sevilla, 41092 Sevilla, Spain"
        }
      ]
    },
    {
      "given": "Xiaolan",
      "family": "Zhao",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10021; and"
        }
      ]
    },
    {
      "given": "Val\u00e9rie",
      "family": "Doye",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "*Institut Curie, Centre de Recherche, and"
        },
        {
          "name": "Unit\u00e9 Mixte de Recherche 144 Centre National de la Recherche Scientifique, F-75248 Paris, France;"
        }
      ]
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "B1",
      "doi-asserted-by": "crossref",
      "first-page": "8292",
      "DOI": "10.1128/MCB.22.23.8292-8301.2002",
      "volume": "22",
      "author": "Andrulis E. D.",
      "year": "2002",
      "journal-title": "Mol. Cell Biol"
    },
    {
      "key": "B2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.9.12.3475"
    },
    {
      "key": "B3",
      "doi-asserted-by": "crossref",
      "first-page": "e342",
      "DOI": "10.1371/journal.pbio.0020342",
      "volume": "2",
      "author": "Brickner J. H.",
      "year": "2004",
      "journal-title": "PLoS Biol"
    },
    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "770",
      "DOI": "10.1038/nature04752",
      "volume": "441",
      "author": "Cabal G. G.",
      "year": "2006",
      "journal-title": "Nature"
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "1188",
      "DOI": "10.1101/gad.1307205",
      "volume": "19",
      "author": "Casolari J. M.",
      "year": "2005",
      "journal-title": "Genes Dev"
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "18477",
      "DOI": "10.1074/jbc.271.31.18477",
      "volume": "271",
      "author": "Corbett A. H.",
      "year": "1996",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "246",
      "DOI": "10.1074/mcp.M400154-MCP200",
      "volume": "4",
      "author": "Denison C.",
      "year": "2005",
      "journal-title": "Mol. Cell Proteomics"
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "1881",
      "DOI": "10.1534/genetics.106.063438",
      "volume": "174",
      "author": "De Souza C. P.",
      "year": "2006",
      "journal-title": "Genetics"
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "7858",
      "DOI": "10.1128/MCB.00870-06",
      "volume": "26",
      "author": "Dieppois G.",
      "year": "2006",
      "journal-title": "Mol. Cell. Biol"
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "214",
      "DOI": "10.1038/ncb756",
      "volume": "4",
      "author": "Feuerbach F.",
      "year": "2002",
      "journal-title": "Nat. Cell Biol"
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "5843",
      "DOI": "10.1093/emboj/cdf590",
      "volume": "21",
      "author": "Fischer T.",
      "year": "2002",
      "journal-title": "EMBO J"
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "63",
      "DOI": "10.1016/S0092-8674(03)01026-2",
      "volume": "116",
      "author": "Galy V.",
      "year": "2004",
      "journal-title": "Cell"
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "108",
      "DOI": "10.1038/47528",
      "volume": "403",
      "author": "Galy V.",
      "year": "2000",
      "journal-title": "Nature"
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "4102",
      "DOI": "10.1074/jbc.M413209200",
      "volume": "280",
      "author": "Hannich J. T.",
      "year": "2005",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "79",
      "DOI": "10.1016/S1047-8477(02)00533-6",
      "volume": "140",
      "author": "Hediger F.",
      "year": "2002",
      "journal-title": "J. Struct. Biol"
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "2779",
      "DOI": "10.1093/nar/28.14.2779",
      "volume": "28",
      "author": "Hegde V.",
      "year": "2000",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "23566",
      "DOI": "10.1074/jbc.M500947200",
      "volume": "280",
      "author": "Jacquiau H. R.",
      "year": "2005",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "1015",
      "DOI": "10.1093/genetics/161.3.1015",
      "volume": "161",
      "author": "Karathanasis E.",
      "year": "2002",
      "journal-title": "Genetics"
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "2544",
      "DOI": "10.1128/MCB.22.8.2544-2555.2002",
      "volume": "22",
      "author": "Leslie D. M.",
      "year": "2002",
      "journal-title": "Mol. Cell Biol"
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "1069",
      "DOI": "10.1083/jcb.200212052",
      "volume": "160",
      "author": "Li S. J.",
      "year": "2003",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "579",
      "DOI": "10.1016/j.biochi.2004.10.023",
      "volume": "87",
      "author": "Lisby M.",
      "year": "2005",
      "journal-title": "Biochimie"
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "459",
      "DOI": "10.1016/j.dnarep.2004.11.010",
      "volume": "4",
      "author": "Loeillet S.",
      "year": "2005",
      "journal-title": "DNA Rep"
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "3042",
      "DOI": "10.1074/jbc.M608741200",
      "volume": "282",
      "author": "Luthra R.",
      "year": "2006",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "387",
      "DOI": "10.1093/emboj/21.3.387",
      "volume": "21",
      "author": "Lutzmann M.",
      "year": "2002",
      "journal-title": "EMBO J"
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "39",
      "DOI": "10.1083/jcb.200608066",
      "volume": "177",
      "author": "Makhnevych T.",
      "year": "2007",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "811",
      "DOI": "10.1016/j.molcel.2006.02.007",
      "volume": "21",
      "author": "Mendjan S.",
      "year": "2006",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "5749",
      "DOI": "10.1073/pnas.0501768102",
      "volume": "102",
      "author": "Menon B. B.",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B28",
      "doi-asserted-by": "crossref",
      "first-page": "1424",
      "DOI": "10.1128/MCB.26.4.1424-1433.2006",
      "volume": "26",
      "author": "Motegi A.",
      "year": "2006",
      "journal-title": "Mol. Cell Biol"
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "103",
      "DOI": "10.1093/genetics/157.1.103",
      "volume": "157",
      "author": "Mullen J. R.",
      "year": "2001",
      "journal-title": "Genetics"
    },
    {
      "key": "B30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.e05-06-0527"
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "41346",
      "DOI": "10.1074/jbc.M407950200",
      "volume": "279",
      "author": "Panse V. G.",
      "year": "2004",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "21",
      "DOI": "10.1038/ncb893",
      "volume": "5",
      "author": "Panse V. G.",
      "year": "2003",
      "journal-title": "Nat. Cell Biol"
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "428",
      "DOI": "10.1038/nature03665",
      "volume": "436",
      "author": "Pfander B.",
      "year": "2005",
      "journal-title": "Nature"
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "1533",
      "DOI": "10.1093/genetics/143.4.1533",
      "volume": "143",
      "author": "Piruat J. I.",
      "year": "1996",
      "journal-title": "Genetics"
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "1284",
      "DOI": "10.1038/ncb1488",
      "volume": "8",
      "author": "Sacher M.",
      "year": "2006",
      "journal-title": "Nat. Cell Biol"
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "379",
      "DOI": "10.1016/j.molcel.2005.12.012",
      "volume": "21",
      "author": "Schmid M.",
      "year": "2006",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "B37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.e05-01-0011"
    },
    {
      "key": "B38",
      "doi-asserted-by": "crossref",
      "first-page": "3934",
      "DOI": "10.1128/MCB.25.10.3934-3944.2005",
      "volume": "25",
      "author": "Shim E. Y.",
      "year": "2005",
      "journal-title": "Mol. Cell Biol"
    },
    {
      "key": "B39",
      "doi-asserted-by": "crossref",
      "first-page": "5130",
      "DOI": "10.1128/MCB.24.12.5130-5143.2004",
      "volume": "24",
      "author": "Soustelle C.",
      "year": "2004",
      "journal-title": "Mol. Cell Biol"
    },
    {
      "key": "B40",
      "doi-asserted-by": "crossref",
      "first-page": "775",
      "DOI": "10.1016/S1534-5807(03)00162-X",
      "volume": "4",
      "author": "Suntharalingam M.",
      "year": "2003",
      "journal-title": "Dev. Cell"
    },
    {
      "key": "B41",
      "doi-asserted-by": "crossref",
      "first-page": "1301",
      "DOI": "10.1038/sj.emboj.7600144",
      "volume": "23",
      "author": "Taddei A.",
      "year": "2004",
      "journal-title": "EMBO J"
    },
    {
      "key": "B42",
      "doi-asserted-by": "crossref",
      "first-page": "774",
      "DOI": "10.1038/nature04845",
      "volume": "441",
      "author": "Taddei A.",
      "year": "2006",
      "journal-title": "Nature"
    },
    {
      "key": "B43",
      "doi-asserted-by": "crossref",
      "first-page": "189",
      "DOI": "10.1083/jcb.200505159",
      "volume": "172",
      "author": "Therizols P.",
      "year": "2006",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B44",
      "doi-asserted-by": "crossref",
      "first-page": "579",
      "DOI": "10.1083/jcb.200608141",
      "volume": "175",
      "author": "Timney B. L.",
      "year": "2006",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B45",
      "doi-asserted-by": "crossref",
      "first-page": "573",
      "DOI": "10.1002/j.1460-2075.1991.tb07984.x",
      "volume": "10",
      "author": "Tollervey D.",
      "year": "1991",
      "journal-title": "EMBO J"
    },
    {
      "key": "B46",
      "doi-asserted-by": "crossref",
      "first-page": "1499",
      "DOI": "10.1534/genetics.105.052811",
      "volume": "172",
      "author": "Wang Z.",
      "year": "2006",
      "journal-title": "Genetics"
    },
    {
      "key": "B47",
      "doi-asserted-by": "crossref",
      "first-page": "45662",
      "DOI": "10.1074/jbc.M409203200",
      "volume": "279",
      "author": "Wohlschlegel J. A.",
      "year": "2004",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B48",
      "doi-asserted-by": "crossref",
      "first-page": "73",
      "DOI": "10.1074/mcp.M400166-MCP200",
      "volume": "4",
      "author": "Wykoff D. D.",
      "year": "2005",
      "journal-title": "Mol. Cell Proteomics"
    },
    {
      "key": "B49",
      "doi-asserted-by": "crossref",
      "first-page": "5541",
      "DOI": "10.1093/nar/gkl685",
      "volume": "34",
      "author": "Yang L.",
      "year": "2006",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "B50",
      "doi-asserted-by": "crossref",
      "first-page": "4777",
      "DOI": "10.1073/pnas.0500537102",
      "volume": "102",
      "author": "Zhao X.",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B51",
      "doi-asserted-by": "crossref",
      "first-page": "605",
      "DOI": "10.1083/jcb.200405168",
      "volume": "167",
      "author": "Zhao X.",
      "year": "2004",
      "journal-title": "J. Cell Biol"
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2021,
        8,
        14
      ]
    ],
    "date-time": "2021-08-14T10:58:38Z",
    "timestamp": 1628938718000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.e07-02-0123"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "Karsten",
      "family": "Weis",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2007,
        8
      ]
    ]
  },
  "references-count": 51,
  "journal-issue": {
    "issue": "8",
    "published-print": {
      "date-parts": [
        [
          2007,
          8
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.e07-02-0123"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.E07-02-0123",
  "relation": {
    "has-review": [
      {
        "id-type": "doi",
        "id": "10.3410/f.1089259.542463",
        "asserted-by": "object"
      }
    ]
  },
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        2007,
        8
      ]
    ]
  }
}