DOI: 10.1091/mbc.11.6.2103. Mitochondria-to-Nuclear Signaling Is Regulated by the Subcellular Localization of the Transcription Factors Rtg1p and Rtg3p

Mitochondria-to-Nuclear Signaling Is Regulated by the Subcellular Localization of the Transcription Factors Rtg1p and Rtg3p

10.1091/mbc.11.6.2103

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Cells modulate the expression of nuclear genes in response to changes in the functional state of mitochondria, an interorganelle communication pathway called retrograde regulation. In yeast, expression of the CIT2 gene shows a typical retrograde response in that its expression is dramatically increased in cells with dysfunctional mitochondria, such as in ρopetites. Three genes control this signaling pathway: RTG1 andRTG3, which encode basic helix-loop-helix leucine zipper transcription factors that bind as heterodimer to theCIT2 upstream activation site, and RTG2, which encodes a protein of unknown function. We show that in respiratory-competent (ρ+) cells in whichCIT2 expression is low, Rtg1p and Rtg3p exist as a complex largely in the cytoplasm, and in ρopetites in which CIT2 expression is high, they exist as a complex predominantly localized in the nucleus. Cytoplasmic Rtg3p is multiply phosphorylated and becomes partially dephosphorylated when localized in the nucleus. Rtg2p, which is cytoplasmic in both ρ+and ρocells, is required for the dephosphorylation and nuclear localization of Rtg3p. Interaction of Rtg3p with Rtg1p is required to retain Rtg3p in the cytoplasm of ρ+cells; in the absence of such interaction, nuclear localization and dephosphorylation of Rtg3p is independent of Rtg2p. Our data show that Rtg1p acts as both a positive and negative regulator of the retrograde response and that Rtg2p acts to transduce mitochondrial signals affecting the phosphorylation state and subcellular localization of Rtg3p.

Bibliography

Sekito, T., Thornton, J., & Butow, R. A. (2000). Mitochondria-to-Nuclear Signaling Is Regulated by the Subcellular Localization of the Transcription Factors Rtg1p and Rtg3p. Molecular Biology of the Cell, 11(6), 2103â2115.

Authors 3

Takayuki Sekito (first)
Janet Thornton (additional)
Ronald A. Butow (additional)

References 47 Referenced 198

10.1073/pnas.90.17.8063 / Proc. Natl. Acad. Sci. USA by Aronheim A. (1993)
10.1126/science.3140380 / Science by Baeuerle P.A. (1988)
10.1093/emboj/18.3.522 / EMBO J. by Biswas G. (1999)
10.1073/pnas.89.16.7290 / Proc. Natl. Acad. Sci. USA by Bork P. (1992)
10.1126/science.7878466 / Science by Brown K. (1995)
10.1074/jbc.270.30.18141 / J. Biol. Chem. by Chelstowska A. (1995)
10.1002/(SICI)1097-0061(19990930)15:13<1377::AID-YEA473>3.0.CO;2-0 / Yeast by Chelstowska A. (1999)
10.1016/S0960-9822(99)80503-X / Curr. Biol. by De Vit M.J. (1999)
10.1091/mbc.8.8.1603
10.1016/S0959-440X(94)90054-X / Curr. Opin. Struct. Biol. by Ellenberger T. (1994)
10.1101/gad.8.8.970 / Genes Dev. by Ellenberger T. (1994)
10.1038/363038a0 / Nature by Ferré-D'Amaré A.R. (1993)
10.1016/S0092-8674(00)80371-2 / Cell by Fornerod M. (1997)
10.1016/0092-8674(92)90595-4 / Cell by Geisler R. (1992)
10.1083/jcb.138.1.65 / J. Cell Biol. by Gorlich D. (1997)
10.1101/gad.11.13.1640 / Genes Dev. by Grant P.A. (1997)
10.1016/S0962-8924(98)01263-X / Trends Cell Biol. by Grant P.A. (1998)
10.1016/S0960-9822(99)80494-1 / Curr. Biol. by Hopper A.K. (1999)
10.1152/physrev.1996.76.3.651 / Physiol. Rev. by Jans D.A. (1996)
10.1128/MCB.17.3.1110 / Mol. Cell. Biol. by Jia Y. (1997)
10.1126/science.8108735 / Science by Kaffman A. (1994)
10.1038/24898 / Nature by Kaffman A. (1998)
10.1101/gad.12.17.2673 / Genes Dev. by Kaffman A. (1998)
10.1101/gad.13.10.1211 / Genes Dev. by Kaufman R.J. (1999)
10.1016/0092-8674(92)90596-5 / Cell by Kidd S. (1992)
10.1126/science.284.5416.977 / Science by Komeili A. (1999)
10.1016/0968-0004(94)90275-5 / Trends Biochem. Sci. by Koonin E.V. (1994)
{'key': 'B28', 'first-page': '79', 'volume': '1264', 'author': 'Kos W.', 'year': '1995', 'journal-title': 'Biochem. Biophys. Acta'} / Biochem. Biophys. Acta by Kos W. (1995)
10.1016/0092-8674(93)90050-Z / Cell by Liao X. (1993)
10.1128/MCB.11.1.38 / Mol. Cell. Biol. by Liao X. (1991)
10.1128/MCB.19.10.6720 / Mol. Cell. Biol. by Liu Z. (1999)
10.1016/S1097-2765(00)80188-4 / Mol. Cell by Massari M.E. (1999)
10.1128/MCB.16.1.121 / Mol. Cell. Biol. by Massari M.E. (1996)
10.1038/386779a0 / Nature by Nigg E.A. (1997)
10.1083/jcb.142.3.613 / J. Cell Biol. by Okamoto K. (1998)
10.1266/ggs.72.323 / Genes Genet. Syst. by Oshima Y. (1997)
10.1126/science.3027892 / Science by Parikh V.S. (1987)
10.1146/annurev.bi.65.070196.003023 / Annu. Rev. Biochem. by Poyton R.O. (1996)
10.1128/MCB.13.2.792 / Mol. Cell. Biol. by Quong M.W. (1993)
10.1006/dbio.1996.0308 / Dev. Biol. by Reach M. (1996)
10.1242/dev.112.2.371 / Development by Roth S. (1991)
10.1074/jbc.272.32.19801 / J. Biol. Chem. by Rothermel B. (1997)
10.1074/jbc.270.49.29476 / J. Biol. Chem. by Rothermel B.A. (1995)
10.1093/nar/18.10.3091 / Nucleic Acids Res. by Schmitt M.E. (1990)
10.1016/0092-8674(86)90807-X / Cell by Sen R. (1986)
10.1016/0960-9822(93)90212-7 / Curr. Biol. by Shyjan A.W. (1993)
10.1021/bi00016a031 / Biochemistry by Small W.C. (1995)

Dates

Type	When
Created	12 years, 1 month ago (July 2, 2013, 7:53 p.m.)
Deposited	3 years, 6 months ago (Feb. 26, 2022, 9:42 p.m.)
Indexed	6 days, 22 hours ago (Aug. 20, 2025, 8:29 a.m.)
Issued	25 years, 2 months ago (June 1, 2000)
Published	25 years, 2 months ago (June 1, 2000)
Published Print	25 years, 2 months ago (June 1, 2000)

Funders 0

None

BibTeX

@article{Sekito_2000, title={Mitochondria-to-Nuclear Signaling Is Regulated by the Subcellular Localization of the Transcription Factors Rtg1p and Rtg3p}, volume={11}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.11.6.2103}, DOI={10.1091/mbc.11.6.2103}, number={6}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Sekito, Takayuki and Thornton, Janet and Butow, Ronald A.}, editor={Fox, Thomas D.}, year={2000}, month=jun, pages={2103–2115} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        20
      ]
    ],
    "date-time": "2025-08-20T12:29:50Z",
    "timestamp": 1755692990804
  },
  "reference-count": 47,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "6",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        6
      ]
    ]
  },
  "abstract": "<jats:p>Cells modulate the expression of nuclear genes in response to changes in the functional state of mitochondria, an interorganelle communication pathway called retrograde regulation. In yeast, expression of the CIT2 gene shows a typical retrograde response in that its expression is dramatically increased in cells with dysfunctional mitochondria, such as in \u03c1<jats:sup>o</jats:sup>petites. Three genes control this signaling pathway: RTG1 andRTG3, which encode basic helix-loop-helix leucine zipper transcription factors that bind as heterodimer to theCIT2 upstream activation site, and RTG2, which encodes a protein of unknown function. We show that in respiratory-competent (\u03c1<jats:sup>+</jats:sup>) cells in whichCIT2 expression is low, Rtg1p and Rtg3p exist as a complex largely in the cytoplasm, and in \u03c1<jats:sup>o</jats:sup>petites in which CIT2 expression is high, they exist as a complex predominantly localized in the nucleus. Cytoplasmic Rtg3p is multiply phosphorylated and becomes partially dephosphorylated when localized in the nucleus. Rtg2p, which is cytoplasmic in both \u03c1<jats:sup>+</jats:sup>and \u03c1<jats:sup>o</jats:sup>cells, is required for the dephosphorylation and nuclear localization of Rtg3p. Interaction of Rtg3p with Rtg1p is required to retain Rtg3p in the cytoplasm of \u03c1<jats:sup>+</jats:sup>cells; in the absence of such interaction, nuclear localization and dephosphorylation of Rtg3p is independent of Rtg2p. Our data show that Rtg1p acts as both a positive and negative regulator of the retrograde response and that Rtg2p acts to transduce mitochondrial signals affecting the phosphorylation state and subcellular localization of Rtg3p.</jats:p>",
  "DOI": "10.1091/mbc.11.6.2103",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2013,
        7,
        2
      ]
    ],
    "date-time": "2013-07-02T23:53:47Z",
    "timestamp": 1372809227000
  },
  "page": "2103-2115",
  "source": "Crossref",
  "is-referenced-by-count": 198,
  "title": "Mitochondria-to-Nuclear Signaling Is Regulated by the Subcellular Localization of the Transcription Factors Rtg1p and Rtg3p",
  "prefix": "10.1091",
  "volume": "11",
  "author": [
    {
      "given": "Takayuki",
      "family": "Sekito",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9148"
        }
      ]
    },
    {
      "given": "Janet",
      "family": "Thornton",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9148"
        }
      ]
    },
    {
      "given": "Ronald A.",
      "family": "Butow",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9148"
        }
      ]
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "B1",
      "doi-asserted-by": "crossref",
      "first-page": "8063",
      "DOI": "10.1073/pnas.90.17.8063",
      "volume": "90",
      "author": "Aronheim A.",
      "year": "1993",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B2",
      "doi-asserted-by": "crossref",
      "first-page": "540",
      "DOI": "10.1126/science.3140380",
      "volume": "242",
      "author": "Baeuerle P.A.",
      "year": "1988",
      "journal-title": "Science"
    },
    {
      "key": "B3",
      "doi-asserted-by": "crossref",
      "first-page": "522",
      "DOI": "10.1093/emboj/18.3.522",
      "volume": "18",
      "author": "Biswas G.",
      "year": "1999",
      "journal-title": "EMBO J."
    },
    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "7290",
      "DOI": "10.1073/pnas.89.16.7290",
      "volume": "89",
      "author": "Bork P.",
      "year": "1992",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "1485",
      "DOI": "10.1126/science.7878466",
      "volume": "267",
      "author": "Brown K.",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "18141",
      "DOI": "10.1074/jbc.270.30.18141",
      "volume": "270",
      "author": "Chelstowska A.",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "1377",
      "DOI": "10.1002/(SICI)1097-0061(19990930)15:13<1377::AID-YEA473>3.0.CO;2-0",
      "volume": "15",
      "author": "Chelstowska A.",
      "year": "1999",
      "journal-title": "Yeast"
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "1231",
      "DOI": "10.1016/S0960-9822(99)80503-X",
      "volume": "9",
      "author": "De Vit M.J.",
      "year": "1999",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "B9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.8.8.1603"
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "12",
      "DOI": "10.1016/S0959-440X(94)90054-X",
      "volume": "4",
      "author": "Ellenberger T.",
      "year": "1994",
      "journal-title": "Curr. Opin. Struct. Biol."
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "970",
      "DOI": "10.1101/gad.8.8.970",
      "volume": "8",
      "author": "Ellenberger T.",
      "year": "1994",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "38",
      "DOI": "10.1038/363038a0",
      "volume": "363",
      "author": "Ferr\u00e9-D'Amar\u00e9 A.R.",
      "year": "1993",
      "journal-title": "Nature"
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "1051",
      "DOI": "10.1016/S0092-8674(00)80371-2",
      "volume": "90",
      "author": "Fornerod M.",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "613",
      "DOI": "10.1016/0092-8674(92)90595-4",
      "volume": "71",
      "author": "Geisler R.",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "65",
      "DOI": "10.1083/jcb.138.1.65",
      "volume": "138",
      "author": "Gorlich D.",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "1640",
      "DOI": "10.1101/gad.11.13.1640",
      "volume": "11",
      "author": "Grant P.A.",
      "year": "1997",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "193",
      "DOI": "10.1016/S0962-8924(98)01263-X",
      "volume": "8",
      "author": "Grant P.A.",
      "year": "1998",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "R803",
      "DOI": "10.1016/S0960-9822(99)80494-1",
      "volume": "9",
      "author": "Hopper A.K.",
      "year": "1999",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "651",
      "DOI": "10.1152/physrev.1996.76.3.651",
      "volume": "76",
      "author": "Jans D.A.",
      "year": "1996",
      "journal-title": "Physiol. Rev."
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "1110",
      "DOI": "10.1128/MCB.17.3.1110",
      "volume": "17",
      "author": "Jia Y.",
      "year": "1997",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "1153",
      "DOI": "10.1126/science.8108735",
      "volume": "263",
      "author": "Kaffman A.",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "482",
      "DOI": "10.1038/24898",
      "volume": "396",
      "author": "Kaffman A.",
      "year": "1998",
      "journal-title": "Nature"
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "2673",
      "DOI": "10.1101/gad.12.17.2673",
      "volume": "12",
      "author": "Kaffman A.",
      "year": "1998",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "1211",
      "DOI": "10.1101/gad.13.10.1211",
      "volume": "13",
      "author": "Kaufman R.J.",
      "year": "1999",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "623",
      "DOI": "10.1016/0092-8674(92)90596-5",
      "volume": "71",
      "author": "Kidd S.",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "977",
      "DOI": "10.1126/science.284.5416.977",
      "volume": "284",
      "author": "Komeili A.",
      "year": "1999",
      "journal-title": "Science"
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "156",
      "DOI": "10.1016/0968-0004(94)90275-5",
      "volume": "19",
      "author": "Koonin E.V.",
      "year": "1994",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "B28",
      "first-page": "79",
      "volume": "1264",
      "author": "Kos W.",
      "year": "1995",
      "journal-title": "Biochem. Biophys. Acta"
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "61",
      "DOI": "10.1016/0092-8674(93)90050-Z",
      "volume": "72",
      "author": "Liao X.",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "38",
      "DOI": "10.1128/MCB.11.1.38",
      "volume": "11",
      "author": "Liao X.",
      "year": "1991",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "6720",
      "DOI": "10.1128/MCB.19.10.6720",
      "volume": "19",
      "author": "Liu Z.",
      "year": "1999",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "63",
      "DOI": "10.1016/S1097-2765(00)80188-4",
      "volume": "4",
      "author": "Massari M.E.",
      "year": "1999",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "121",
      "DOI": "10.1128/MCB.16.1.121",
      "volume": "16",
      "author": "Massari M.E.",
      "year": "1996",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "779",
      "DOI": "10.1038/386779a0",
      "volume": "386",
      "author": "Nigg E.A.",
      "year": "1997",
      "journal-title": "Nature"
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "613",
      "DOI": "10.1083/jcb.142.3.613",
      "volume": "142",
      "author": "Okamoto K.",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "323",
      "DOI": "10.1266/ggs.72.323",
      "volume": "72",
      "author": "Oshima Y.",
      "year": "1997",
      "journal-title": "Genes Genet. Syst."
    },
    {
      "key": "B37",
      "doi-asserted-by": "crossref",
      "first-page": "576",
      "DOI": "10.1126/science.3027892",
      "volume": "235",
      "author": "Parikh V.S.",
      "year": "1987",
      "journal-title": "Science"
    },
    {
      "key": "B38",
      "doi-asserted-by": "crossref",
      "first-page": "563",
      "DOI": "10.1146/annurev.bi.65.070196.003023",
      "volume": "65",
      "author": "Poyton R.O.",
      "year": "1996",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "B39",
      "doi-asserted-by": "crossref",
      "first-page": "792",
      "DOI": "10.1128/MCB.13.2.792",
      "volume": "13",
      "author": "Quong M.W.",
      "year": "1993",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "B40",
      "doi-asserted-by": "crossref",
      "first-page": "353",
      "DOI": "10.1006/dbio.1996.0308",
      "volume": "180",
      "author": "Reach M.",
      "year": "1996",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "B41",
      "doi-asserted-by": "crossref",
      "first-page": "371",
      "DOI": "10.1242/dev.112.2.371",
      "volume": "112",
      "author": "Roth S.",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "B42",
      "doi-asserted-by": "crossref",
      "first-page": "19801",
      "DOI": "10.1074/jbc.272.32.19801",
      "volume": "272",
      "author": "Rothermel B.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B43",
      "doi-asserted-by": "crossref",
      "first-page": "29476",
      "DOI": "10.1074/jbc.270.49.29476",
      "volume": "49",
      "author": "Rothermel B.A.",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B44",
      "doi-asserted-by": "crossref",
      "first-page": "3091",
      "DOI": "10.1093/nar/18.10.3091",
      "volume": "18",
      "author": "Schmitt M.E.",
      "year": "1990",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "B45",
      "doi-asserted-by": "crossref",
      "first-page": "921",
      "DOI": "10.1016/0092-8674(86)90807-X",
      "volume": "47",
      "author": "Sen R.",
      "year": "1986",
      "journal-title": "Cell"
    },
    {
      "key": "B46",
      "doi-asserted-by": "crossref",
      "first-page": "398",
      "DOI": "10.1016/0960-9822(93)90212-7",
      "volume": "3",
      "author": "Shyjan A.W.",
      "year": "1993",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "B47",
      "doi-asserted-by": "crossref",
      "first-page": "5569",
      "DOI": "10.1021/bi00016a031",
      "volume": "16",
      "author": "Small W.C.",
      "year": "1995",
      "journal-title": "Biochemistry"
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2022,
        2,
        27
      ]
    ],
    "date-time": "2022-02-27T02:42:05Z",
    "timestamp": 1645929725000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.11.6.2103"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "Thomas D.",
      "family": "Fox",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        6
      ]
    ]
  },
  "references-count": 47,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2000,
          6
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.11.6.2103"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.11.6.2103",
  "relation": {},
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        2000,
        6
      ]
    ]
  }
}