DOI: 10.1083/jcb.200101081. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells

An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells

10.1083/jcb.200101081

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

The nuclear pore complexes (NPCs) are evolutionarily conserved assemblies that allow traffic between the cytoplasm and the nucleus. In this study, we have identified and characterized a novel human nuclear pore protein, hNup133, through its homology with the Saccharomyces cerevisiae nucleoporin scNup133. Two-hybrid screens and immunoprecipitation experiments revealed a direct and evolutionarily conserved interaction between Nup133 and Nup84/Nup107 and indicated that hNup133 and hNup107 are part of a NPC subcomplex that contains two other nucleoporins (the previously characterized hNup96 and a novel nucleoporin designated as hNup120) homologous to constituents of the scNup84 subcomplex. We further demonstrate that hNup133 and hNup107 are localized on both sides of the NPC to which they are stably associated at interphase, remain associated as part of a NPC subcomplex during mitosis, and are targeted at early stages to the reforming nuclear envelope. Throughout mitosis, a fraction of hNup133 and hNup107 localizes to the kinetochores, thus revealing an unexpected connection between structural NPCs constituents and kinetochores. Photobleaching experiments further showed that the mitotic cytoplasm contains kinetochore-binding competent hNup133 molecules and that in contrast to its stable association with the NPCs the interaction of this nucleoporin with kinetochores is dynamic.

Bibliography

Belgareh, N., Rabut, G., BaiÌ, S. W., van Overbeek, M., Beaudouin, J., Daigle, N., Zatsepina, O. V., Pasteau, F., Labas, V., Fromont-Racine, M., Ellenberg, J., & Doye, V. (2001). An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. The Journal of Cell Biology, 154(6), 1147â1160.

Authors 12

Naïma Belgareh (first)
Gwénaël Rabut (additional)
Siau Wei Baï (additional)
Megan van Overbeek (additional)
Joël Beaudouin (additional)
Nathalie Daigle (additional)
Olga V. Zatsepina (additional)
Fabien Pasteau (additional)
Valérie Labas (additional)
Micheline Fromont-Racine (additional)
Jan Ellenberg (additional)
Valérie Doye (additional)

References 40 Referenced 276

10.1083/jcb.111.3.807 / J. Cell Biol. (1990)
10.1016/S0962-8924(00)01880-8 / Trends Cell Biol (2001)
10.1016/S0955-0674(00)00093-4 / Curr. Opin. Cell Biol. (2000)
10.1007/BF01453442 / Protoplasma (1999)
10.1242/jcs.112.13.2253 / J. Cell Sci. (1999)
10.1016/S0960-9822(98)70208-8 / Curr. Biol (1998)
10.1242/jcs.114.5.953 / J. Cell Sci (2001)
10.1083/jcb.143.1.49 / J. Cell Biol (1998)
{'key': '2023072211542613300_BIB9', 'first-page': '31', 'volume': '55', 'year': '1991', 'journal-title': 'Eur. J. Cell Biol.'} / Eur. J. Cell Biol. (1991)
10.1083/jcb.200102130 / J. Cell Biol. (2001)
10.1016/S0955-0674(97)80014-2 / Curr. Opin. Cell Biol. (1997)
10.1002/j.1460-2075.1994.tb06953.x / EMBO J. (1994)
10.1083/jcb.132.4.617 / J. Cell Biol. (1996)
10.1083/jcb.144.6.1097 / J. Cell Biol. (1999)
10.1038/ng0797-277 / Nat. Genet. (1997)
{'key': '2023072211542613300_BIB16', 'first-page': '95', 'volume': '17', 'year': '2000', 'journal-title': 'Yeast'} / Yeast (2000)
10.1242/jcs.110.4.409 / J. Cell Sci. (1997)
10.1091/mbc.8.10.2017 / Mol. Biol. Cell (1997)
{'key': '2023072211542613300_BIB19', 'first-page': '266', 'volume': '43', 'year': '1987', 'journal-title': 'Eur. J. Cell Biol.'} / Eur. J. Cell Biol. (1987)
10.1083/jcb.150.6.1233 / J. Cell Biol (2000)
10.1074/jbc.270.38.22473 / J. Biol. Chem. (1995)
10.1093/genetics/157.4.1543 / Genetics (2001)
10.1006/geno.1996.0177 / Genomics (1996)
10.1083/jcb.135.6.1457 / J. Cell Biol. (1996)
10.1016/S0021-9258(17)32483-3 / J. Biol. Chem. (1994)
{'key': '2023072211542613300_BIB26'}
10.1083/jcb.148.4.635 / J. Cell Biol. (2000)
10.1016/S0092-8674(00)00202-6 / Cell (2000)
10.1021/ac950914h / Anal. Chem. (1996)
10.1016/S0092-8674(00)80981-2 / Cell. (1996)
10.1083/jcb.149.1.41 / J. Cell Biol. (2000)
10.1242/jcs.112.21.3649 / J. Cell Sci. (1999)
10.1016/S0955-0674(99)80055-6 / Curr. Opin. Cell Biol. (1999)
10.1093/emboj/16.16.5086 / EMBO J (1997)
10.1242/jcs.112.18.3049 / J. Cell Sci. (1999)
10.1083/jcb.153.2.397 / J. Cell Biol. (2001)
10.1073/pnas.96.14.7950 / Proc. Natl. Acad. Sci. USA. (1999)
10.1016/S0955-0674(00)00221-0 / Curr. Opin. Cell Biol. (2001)
10.1074/jbc.M101083200 / J. Biol. Chem. (2001)
10.1016/S0092-8674(00)81548-2 / Cell (1999)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:46 p.m.)
Deposited	2 years, 1 month ago (July 22, 2023, 7:56 a.m.)
Indexed	1 month, 3 weeks ago (July 12, 2025, 6:49 p.m.)
Issued	23 years, 11 months ago (Sept. 17, 2001)
Published	23 years, 11 months ago (Sept. 17, 2001)
Published Online	23 years, 11 months ago (Sept. 17, 2001)
Published Print	23 years, 11 months ago (Sept. 17, 2001)

Funders 0

None

BibTeX

@article{Belgareh_2001, title={An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells}, volume={154}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.200101081}, DOI={10.1083/jcb.200101081}, number={6}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Belgareh, Naïma and Rabut, Gwénaël and Baï, Siau Wei and van Overbeek, Megan and Beaudouin, Joël and Daigle, Nathalie and Zatsepina, Olga V. and Pasteau, Fabien and Labas, Valérie and Fromont-Racine, Micheline and Ellenberg, Jan and Doye, Valérie}, year={2001}, month=sep, pages={1147–1160} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        12
      ]
    ],
    "date-time": "2025-07-12T22:49:54Z",
    "timestamp": 1752360594702
  },
  "reference-count": 40,
  "publisher": "Rockefeller University Press",
  "issue": "6",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        9,
        17
      ]
    ]
  },
  "abstract": "<jats:p>The nuclear pore complexes (NPCs) are evolutionarily conserved assemblies that allow traffic between the cytoplasm and the nucleus. In this study, we have identified and characterized a novel human nuclear pore protein, hNup133, through its homology with the Saccharomyces cerevisiae nucleoporin scNup133. Two-hybrid screens and immunoprecipitation experiments revealed a direct and evolutionarily conserved interaction between Nup133 and Nup84/Nup107 and indicated that hNup133 and hNup107 are part of a NPC subcomplex that contains two other nucleoporins (the previously characterized hNup96 and a novel nucleoporin designated as hNup120) homologous to constituents of the scNup84 subcomplex. We further demonstrate that hNup133 and hNup107 are localized on both sides of the NPC to which they are stably associated at interphase, remain associated as part of a NPC subcomplex during mitosis, and are targeted at early stages to the reforming nuclear envelope. Throughout mitosis, a fraction of hNup133 and hNup107 localizes to the kinetochores, thus revealing an unexpected connection between structural NPCs constituents and kinetochores. Photobleaching experiments further showed that the mitotic cytoplasm contains kinetochore-binding competent hNup133 molecules and that in contrast to its stable association with the NPCs the interaction of this nucleoporin with kinetochores is dynamic.</jats:p>",
  "DOI": "10.1083/jcb.200101081",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:46:23Z",
    "timestamp": 1027701983000
  },
  "page": "1147-1160",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 276,
  "title": "An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells",
  "prefix": "10.1083",
  "volume": "154",
  "author": [
    {
      "given": "Nai\u0308ma",
      "family": "Belgareh",
      "sequence": "first",
      "affiliation": [
        {
          "name": "1UMR 144 Centre National de la Recherche Scientifique-Institut Curie, 75005 Paris, France"
        }
      ]
    },
    {
      "given": "Gwe\u0301nae\u0308l",
      "family": "Rabut",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "2Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory, 69117 Heidelberg, Germany"
        }
      ]
    },
    {
      "given": "Siau Wei",
      "family": "Bai\u0308",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1UMR 144 Centre National de la Recherche Scientifique-Institut Curie, 75005 Paris, France"
        }
      ]
    },
    {
      "given": "Megan",
      "family": "van Overbeek",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1UMR 144 Centre National de la Recherche Scientifique-Institut Curie, 75005 Paris, France"
        }
      ]
    },
    {
      "given": "Joe\u0308l",
      "family": "Beaudouin",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "2Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory, 69117 Heidelberg, Germany"
        }
      ]
    },
    {
      "given": "Nathalie",
      "family": "Daigle",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "2Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory, 69117 Heidelberg, Germany"
        }
      ]
    },
    {
      "given": "Olga V.",
      "family": "Zatsepina",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "3UMR 218 Centre National de la Recherche Scientifique-Institut Curie, 75005 Paris, France"
        }
      ]
    },
    {
      "given": "Fabien",
      "family": "Pasteau",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1UMR 144 Centre National de la Recherche Scientifique-Institut Curie, 75005 Paris, France"
        }
      ]
    },
    {
      "given": "Vale\u0301rie",
      "family": "Labas",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "4E\u0301cole Supe\u0301rieure de Physique et de Chimie Industrielles-Centre National de la Recherche Scientifique, UMR 7637, 75005 Paris, France"
        }
      ]
    },
    {
      "given": "Micheline",
      "family": "Fromont-Racine",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "5De\u0301partement des Biotechnologies, Institut Pasteur, 75015 Paris, France"
        }
      ]
    },
    {
      "given": "Jan",
      "family": "Ellenberg",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "2Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory, 69117 Heidelberg, Germany"
        }
      ]
    },
    {
      "given": "Vale\u0301rie",
      "family": "Doye",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1UMR 144 Centre National de la Recherche Scientifique-Institut Curie, 75005 Paris, France"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2001,
        9,
        17
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072211542613300_BIB1",
      "doi-asserted-by": "crossref",
      "first-page": "807",
      "DOI": "10.1083/jcb.111.3.807",
      "volume": "111",
      "year": "1990",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB2",
      "doi-asserted-by": "crossref",
      "first-page": "49",
      "DOI": "10.1016/S0962-8924(00)01880-8",
      "volume": "11",
      "year": "2001",
      "journal-title": "Trends Cell Biol"
    },
    {
      "key": "2023072211542613300_BIB3",
      "doi-asserted-by": "crossref",
      "first-page": "302",
      "DOI": "10.1016/S0955-0674(00)00093-4",
      "volume": "12",
      "year": "2000",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB4",
      "doi-asserted-by": "crossref",
      "first-page": "133",
      "DOI": "10.1007/BF01453442",
      "volume": "209",
      "year": "1999",
      "journal-title": "Protoplasma"
    },
    {
      "key": "2023072211542613300_BIB5",
      "doi-asserted-by": "crossref",
      "first-page": "2253",
      "DOI": "10.1242/jcs.112.13.2253",
      "volume": "112",
      "year": "1999",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072211542613300_BIB6",
      "doi-asserted-by": "crossref",
      "first-page": "541",
      "DOI": "10.1016/S0960-9822(98)70208-8",
      "volume": "8",
      "year": "1998",
      "journal-title": "Curr. Biol"
    },
    {
      "key": "2023072211542613300_BIB7",
      "doi-asserted-by": "crossref",
      "first-page": "953",
      "DOI": "10.1242/jcs.114.5.953",
      "volume": "114",
      "year": "2001",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "2023072211542613300_BIB8",
      "doi-asserted-by": "crossref",
      "first-page": "49",
      "DOI": "10.1083/jcb.143.1.49",
      "volume": "143",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211542613300_BIB9",
      "first-page": "31",
      "volume": "55",
      "year": "1991",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB10",
      "doi-asserted-by": "crossref",
      "first-page": "763",
      "DOI": "10.1083/jcb.200102130",
      "volume": "154",
      "year": "2001",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB11",
      "doi-asserted-by": "crossref",
      "first-page": "401",
      "DOI": "10.1016/S0955-0674(97)80014-2",
      "volume": "9",
      "year": "1997",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB12",
      "doi-asserted-by": "crossref",
      "first-page": "6062",
      "DOI": "10.1002/j.1460-2075.1994.tb06953.x",
      "volume": "13",
      "year": "1994",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072211542613300_BIB13",
      "doi-asserted-by": "crossref",
      "first-page": "617",
      "DOI": "10.1083/jcb.132.4.617",
      "volume": "132",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB14",
      "doi-asserted-by": "crossref",
      "first-page": "1097",
      "DOI": "10.1083/jcb.144.6.1097",
      "volume": "144",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB15",
      "doi-asserted-by": "crossref",
      "first-page": "277",
      "DOI": "10.1038/ng0797-277",
      "volume": "16",
      "year": "1997",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "2023072211542613300_BIB16",
      "first-page": "95",
      "volume": "17",
      "year": "2000",
      "journal-title": "Yeast"
    },
    {
      "key": "2023072211542613300_BIB17",
      "doi-asserted-by": "crossref",
      "first-page": "409",
      "DOI": "10.1242/jcs.110.4.409",
      "volume": "110",
      "year": "1997",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072211542613300_BIB18",
      "doi-asserted-by": "crossref",
      "first-page": "2017",
      "DOI": "10.1091/mbc.8.10.2017",
      "volume": "8",
      "year": "1997",
      "journal-title": "Mol. Biol. Cell"
    },
    {
      "key": "2023072211542613300_BIB19",
      "first-page": "266",
      "volume": "43",
      "year": "1987",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB20",
      "doi-asserted-by": "crossref",
      "first-page": "1233",
      "DOI": "10.1083/jcb.150.6.1233",
      "volume": "150",
      "year": "2000",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211542613300_BIB21",
      "doi-asserted-by": "crossref",
      "first-page": "22473",
      "DOI": "10.1074/jbc.270.38.22473",
      "volume": "270",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072211542613300_BIB22",
      "doi-asserted-by": "crossref",
      "first-page": "1543",
      "DOI": "10.1093/genetics/157.4.1543",
      "volume": "157",
      "year": "2001",
      "journal-title": "Genetics"
    },
    {
      "key": "2023072211542613300_BIB23",
      "doi-asserted-by": "crossref",
      "first-page": "151",
      "DOI": "10.1006/geno.1996.0177",
      "volume": "33",
      "year": "1996",
      "journal-title": "Genomics"
    },
    {
      "key": "2023072211542613300_BIB24",
      "doi-asserted-by": "crossref",
      "first-page": "1457",
      "DOI": "10.1083/jcb.135.6.1457",
      "volume": "135",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB25",
      "doi-asserted-by": "crossref",
      "first-page": "17600",
      "DOI": "10.1016/S0021-9258(17)32483-3",
      "volume": "269",
      "year": "1994",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072211542613300_BIB26"
    },
    {
      "key": "2023072211542613300_BIB27",
      "doi-asserted-by": "crossref",
      "first-page": "635",
      "DOI": "10.1083/jcb.148.4.635",
      "volume": "148",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB28",
      "doi-asserted-by": "crossref",
      "first-page": "997",
      "DOI": "10.1016/S0092-8674(00)00202-6",
      "volume": "103",
      "year": "2000",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211542613300_BIB29",
      "doi-asserted-by": "crossref",
      "first-page": "850",
      "DOI": "10.1021/ac950914h",
      "volume": "68",
      "year": "1996",
      "journal-title": "Anal. Chem."
    },
    {
      "key": "2023072211542613300_BIB30",
      "doi-asserted-by": "crossref",
      "first-page": "265",
      "DOI": "10.1016/S0092-8674(00)80981-2",
      "volume": "84",
      "year": "1996",
      "journal-title": "Cell."
    },
    {
      "key": "2023072211542613300_BIB31",
      "doi-asserted-by": "crossref",
      "first-page": "41",
      "DOI": "10.1083/jcb.149.1.41",
      "volume": "149",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB32",
      "doi-asserted-by": "crossref",
      "first-page": "3649",
      "DOI": "10.1242/jcs.112.21.3649",
      "volume": "112",
      "year": "1999",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072211542613300_BIB33",
      "doi-asserted-by": "crossref",
      "first-page": "391",
      "DOI": "10.1016/S0955-0674(99)80055-6",
      "volume": "11",
      "year": "1999",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB34",
      "doi-asserted-by": "crossref",
      "first-page": "5086",
      "DOI": "10.1093/emboj/16.16.5086",
      "volume": "16",
      "year": "1997",
      "journal-title": "EMBO J"
    },
    {
      "key": "2023072211542613300_BIB35",
      "doi-asserted-by": "crossref",
      "first-page": "3049",
      "DOI": "10.1242/jcs.112.18.3049",
      "volume": "112",
      "year": "1999",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072211542613300_BIB36",
      "doi-asserted-by": "crossref",
      "first-page": "397",
      "DOI": "10.1083/jcb.153.2.397",
      "volume": "153",
      "year": "2001",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB37",
      "doi-asserted-by": "crossref",
      "first-page": "7950",
      "DOI": "10.1073/pnas.96.14.7950",
      "volume": "96",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072211542613300_BIB38",
      "doi-asserted-by": "crossref",
      "first-page": "363",
      "DOI": "10.1016/S0955-0674(00)00221-0",
      "volume": "13",
      "year": "2001",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072211542613300_BIB39",
      "doi-asserted-by": "crossref",
      "first-page": "26559",
      "DOI": "10.1074/jbc.M101083200",
      "volume": "276",
      "year": "2001",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072211542613300_BIB40",
      "doi-asserted-by": "crossref",
      "first-page": "589",
      "DOI": "10.1016/S0092-8674(00)81548-2",
      "volume": "99",
      "year": "1999",
      "journal-title": "Cell"
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/154/6/1147/1513878/jcb15461147.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/154/6/1147/1513878/jcb15461147.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        22
      ]
    ],
    "date-time": "2023-07-22T11:56:39Z",
    "timestamp": 1690026999000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/154/6/1147/32202/An-evolutionarily-conserved-NPC-subcomplex-which"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        9,
        17
      ]
    ]
  },
  "references-count": 40,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2001,
          9,
          17
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.200101081",
  "relation": {
    "has-review": [
      {
        "id-type": "doi",
        "id": "10.3410/f.1001893.17509",
        "asserted-by": "object"
      }
    ]
  },
  "ISSN": [
    "1540-8140",
    "0021-9525"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2001,
        9,
        17
      ]
    ]
  }
}