DOI: 10.1083/jcb.200611128. Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6

Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6

10.1083/jcb.200611128

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Sequestration of misfolded proteins into pericentriolar inclusions called aggresomes is a means that cells use to minimize misfolded protein-induced cytotoxicity. However, the molecular mechanism by which misfolded proteins are recruited to aggresomes remains unclear. Mutations in the E3 ligase parkin cause autosomal recessive Parkinson's disease that is devoid of Lewy bodies, which are similar to aggresomes. Here, we report that parkin cooperates with heterodimeric E2 enzyme UbcH13/Uev1a to mediate K63-linked polyubiquitination of misfolded DJ-1. K63-linked polyubiquitination of misfolded DJ-1 serves as a signal for interaction with histone deacetylase 6, an adaptor protein that binds the dynein–dynactin complex. Through this interaction, misfolded DJ-1 is linked to the dynein motor and transported to aggresomes. Furthermore, fibroblasts lacking parkin display deficits in targeting misfolded DJ-1 to aggresomes. Our findings reveal a signaling role for K63-linked polyubiquitination in dynein-mediated transport, identify parkin as a key regulator in the recruitment of misfolded DJ-1 to aggresomes, and have important implications regarding the biogenesis of Lewy bodies.

Bibliography

Olzmann, J. A., Li, L., Chudaev, M. V., Chen, J., Perez, F. A., Palmiter, R. D., & Chin, L.-S. (2007). Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. The Journal of Cell Biology, 178(6), 1025â1038.

Authors 7

James A. Olzmann (first)
Lian Li (additional)
Maksim V. Chudaev (additional)
Jue Chen (additional)
Francisco A. Perez (additional)
Richard D. Palmiter (additional)
Lih-Shen Chin (additional)

References 78 Referenced 280

10.1002/ana.10675 / Ann. Neurol. (2003)
10.1091/mbc.e03-02-0078 / Mol. Biol. Cell. (2003)
10.1016/j.mcn.2004.06.014 / Mol. Cell. Neurosci. (2004)
10.1126/science.292.5521.1552 / Science. (2001)
10.1016/j.molcel.2004.12.021 / Mol. Cell. (2005)
10.1042/bj20031677 / Biochem. J. (2004)
{'key': '2023072219295873900_BIB7', 'first-page': '3', 'volume': '66', 'year': '1995', 'journal-title': 'Eur. J. Cell Biol.'} / Eur. J. Cell Biol. (1995)
10.1126/science.1077209 / Science. (2003)
10.1146/annurev.neuro.26.010302.081142 / Annu. Rev. Neurosci. (2003)
10.1074/jbc.275.2.1191 / J. Biol. Chem. (2000)
10.1074/jbc.M203300200 / J. Biol. Chem. (2002)
10.1111/j.1582-4934.2006.tb00407.x / J. Cell. Mol. Med. (2006)
10.1016/S0092-8674(00)00126-4 / Cell. (2000)
10.1074/jbc.M413591200 / J. Biol. Chem. (2005)
10.1038/ncb1441 / Nat. Cell Biol. (2006)
10.1083/jcb.146.6.1239 / J. Cell Biol. (1999)
10.1034/j.1600-0854.2002.30602.x / Traffic. (2002)
10.1038/nature02263 / Nature. (2003)
10.1074/jbc.M308947200 / J. Biol. Chem. (2003)
10.1074/jbc.M309204200 / J. Biol. Chem. (2004)
10.1146/annurev.genom.7.080505.115737 / Annu. Rev. Genomics Hum. Genet. (2006)
10.1038/sj.emboj.7600808 / EMBO J. (2005)
10.1093/hmg/ddl131 / Hum. Mol. Genet. (2006)
10.1016/S0140-6736(04)16901-8 / Lancet. (2004)
10.1002/1531-8257(200009)15:5<884::AID-MDS1019>3.0.CO;2-8 / Mov. Disord. (2000)
10.1073/pnas.0503221102 / Proc. Natl. Acad. Sci. USA. (2005)
10.1038/sj.emboj.7600426 / EMBO J. (2004)
10.1073/pnas.172511699 / Proc. Natl. Acad. Sci. USA. (2002)
10.1016/S1097-2765(02)00583-X / Mol. Cell. (2002)
10.1074/jbc.M508786200 / J. Biol. Chem. (2005)
10.1371/journal.pbio.0030156 / PLoS Biol. (2005)
10.1083/jcb.143.7.1883 / J. Cell Biol. (1998)
10.1002/cm.10057 / Cell Motil. Cytoskeleton. (2002)
10.1074/jbc.M203159200 / J. Biol. Chem. (2002)
10.1038/sj.embor.7400188 / EMBO Rep. (2004)
10.1016/S0092-8674(03)00939-5 / Cell. (2003)
10.1091/mbc.e06-09-0787 / Mol. Biol. Cell. (2007)
10.1038/33416 / Nature. (1998)
10.1523/JNEUROSCI.2172-05.2005 / J. Neurosci. (2005)
10.1074/jbc.C600041200 / J. Biol. Chem. (2006)
10.1016/S0962-8924(00)01852-3 / Trends Cell Biol. (2000)
10.1016/j.molcel.2007.04.001 / Mol. Cell. (2007)
10.1080/10715760500260348 / Free Radic. Res. (2005)
10.1523/JNEUROSCI.4474-04.2005 / J. Neurosci. (2005)
{'key': '2023072219295873900_BIB45', 'first-page': '524', 'volume': '27', 'year': '2005', 'journal-title': 'Neurobiol. Aging.'} / Neurobiol. Aging. (2005)
10.1056/NEJM200005253422103 / N. Engl. J. Med. (2000)
10.1042/bj20031123 / Biochem. J. (2004)
10.1074/jbc.M510393200 / J. Biol. Chem. (2006)
10.1074/jbc.M304272200 / J. Biol. Chem. (2003)
10.1111/j.1471-4159.2003.02265.x / J. Neurochem. (2003)
10.1093/hmg/ddi007 / Hum. Mol. Genet. (2005)
10.1212/WNL.51.3.890 / Neurology. (1998)
{'key': '2023072219295873900_BIB53', 'first-page': '117', 'volume': '13', 'year': '2004', 'journal-title': 'Hum. Mol. Genet.'} / Hum. Mol. Genet. (2004)
10.1016/S1474-4422(04)00827-0 / Lancet Neurol. (2004)
10.1074/jbc.M311017200 / J. Biol. Chem. (2004)
{'key': '2023072219295873900_BIB56', 'year': '2005'} (2005)
10.1002/cne.21191 / J. Comp. Neurol. (2007)
10.1074/jbc.M306889200 / J. Biol. Chem. (2003)
10.1073/pnas.0409598102 / Proc. Natl. Acad. Sci. USA. (2005)
10.1186/1471-2202-6-71 / BMC Neurosci. (2005)
10.1111/j.1471-4159.2005.03442.x / J. Neurochem. (2005)
10.1016/j.cbpa.2004.09.009 / Curr. Opin. Chem. Biol. (2004)
10.1251/bpo66 / Biol. Proced. Online. (2003)
10.1016/j.cell.2004.11.013 / Cell. (2005)
10.1016/S0002-9440(10)61113-3 / Am. J. Pathol. (2002)
10.1371/journal.pbio.0020362 / PLoS Biol. (2004)
10.1038/77060 / Nat. Genet. (2000)
10.1126/science.1060627 / Science. (2001)
10.1016/j.tins.2007.03.009 / Trends Neurosci. (2007)
10.1212/WNL.44.3_Part_1.437 / Neurology. (1994)
10.1093/hmg/ddg074 / Hum. Mol. Genet. (2003)
10.1016/S1097-2765(04)00151-0 / Mol. Cell. (2004)
10.1038/35085597 / Nature. (2001)
10.1073/pnas.0502352102 / Proc. Natl. Acad. Sci. USA. (2005)
10.1038/35056563 / Nat. Rev. Mol. Cell Biol. (2001)
10.1074/jbc.M107857200 / J. Biol. Chem. (2002)
10.1073/pnas.240347797 / Proc. Natl. Acad. Sci. USA. (2000)
10.1242/jcs.00700 / J. Cell Sci. (2003)

Dates

Type	When
Created	17 years, 11 months ago (Sept. 10, 2007, 2:38 p.m.)
Deposited	2 years, 1 month ago (July 22, 2023, 3:31 p.m.)
Indexed	1 week, 2 days ago (Aug. 27, 2025, 12:29 p.m.)
Issued	17 years, 11 months ago (Sept. 10, 2007)
Published	17 years, 11 months ago (Sept. 10, 2007)
Published Online	17 years, 11 months ago (Sept. 10, 2007)
Published Print	17 years, 11 months ago (Sept. 10, 2007)

Funders 0

None

BibTeX

@article{Olzmann_2007, title={Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6}, volume={178}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.200611128}, DOI={10.1083/jcb.200611128}, number={6}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Olzmann, James A. and Li, Lian and Chudaev, Maksim V. and Chen, Jue and Perez, Francisco A. and Palmiter, Richard D. and Chin, Lih-Shen}, year={2007}, month=sep, pages={1025–1038} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        27
      ]
    ],
    "date-time": "2025-08-27T16:29:11Z",
    "timestamp": 1756312151319
  },
  "reference-count": 78,
  "publisher": "Rockefeller University Press",
  "issue": "6",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2007,
        9,
        10
      ]
    ]
  },
  "abstract": "<jats:p>Sequestration of misfolded proteins into pericentriolar inclusions called aggresomes is a means that cells use to minimize misfolded protein-induced cytotoxicity. However, the molecular mechanism by which misfolded proteins are recruited to aggresomes remains unclear. Mutations in the E3 ligase parkin cause autosomal recessive Parkinson's disease that is devoid of Lewy bodies, which are similar to aggresomes. Here, we report that parkin cooperates with heterodimeric E2 enzyme UbcH13/Uev1a to mediate K63-linked polyubiquitination of misfolded DJ-1. K63-linked polyubiquitination of misfolded DJ-1 serves as a signal for interaction with histone deacetylase 6, an adaptor protein that binds the dynein\u2013dynactin complex. Through this interaction, misfolded DJ-1 is linked to the dynein motor and transported to aggresomes. Furthermore, fibroblasts lacking parkin display deficits in targeting misfolded DJ-1 to aggresomes. Our findings reveal a signaling role for K63-linked polyubiquitination in dynein-mediated transport, identify parkin as a key regulator in the recruitment of misfolded DJ-1 to aggresomes, and have important implications regarding the biogenesis of Lewy bodies.</jats:p>",
  "DOI": "10.1083/jcb.200611128",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        9,
        10
      ]
    ],
    "date-time": "2007-09-10T18:38:15Z",
    "timestamp": 1189449495000
  },
  "page": "1025-1038",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 280,
  "title": "Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6",
  "prefix": "10.1083",
  "volume": "178",
  "author": [
    {
      "given": "James A.",
      "family": "Olzmann",
      "sequence": "first",
      "affiliation": [
        {
          "name": "1Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322"
        }
      ]
    },
    {
      "given": "Lian",
      "family": "Li",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322"
        }
      ]
    },
    {
      "given": "Maksim V.",
      "family": "Chudaev",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322"
        }
      ]
    },
    {
      "given": "Jue",
      "family": "Chen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322"
        }
      ]
    },
    {
      "given": "Francisco A.",
      "family": "Perez",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "2Department of Biochemistry and Howard Hughes Medical Institute, University of Washington, Seattle, WA 98195"
        }
      ]
    },
    {
      "given": "Richard D.",
      "family": "Palmiter",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "2Department of Biochemistry and Howard Hughes Medical Institute, University of Washington, Seattle, WA 98195"
        }
      ]
    },
    {
      "given": "Lih-Shen",
      "family": "Chin",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2007,
        9,
        10
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072219295873900_BIB1",
      "doi-asserted-by": "crossref",
      "first-page": "283",
      "DOI": "10.1002/ana.10675",
      "volume": "54",
      "year": "2003",
      "journal-title": "Ann. Neurol."
    },
    {
      "key": "2023072219295873900_BIB2",
      "doi-asserted-by": "crossref",
      "first-page": "4541",
      "DOI": "10.1091/mbc.e03-02-0078",
      "volume": "14",
      "year": "2003",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072219295873900_BIB3",
      "doi-asserted-by": "crossref",
      "first-page": "236",
      "DOI": "10.1016/j.mcn.2004.06.014",
      "volume": "27",
      "year": "2004",
      "journal-title": "Mol. Cell. Neurosci."
    },
    {
      "key": "2023072219295873900_BIB4",
      "doi-asserted-by": "crossref",
      "first-page": "1552",
      "DOI": "10.1126/science.292.5521.1552",
      "volume": "292",
      "year": "2001",
      "journal-title": "Science."
    },
    {
      "key": "2023072219295873900_BIB5",
      "doi-asserted-by": "crossref",
      "first-page": "351",
      "DOI": "10.1016/j.molcel.2004.12.021",
      "volume": "17",
      "year": "2005",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072219295873900_BIB6",
      "doi-asserted-by": "crossref",
      "first-page": "695",
      "DOI": "10.1042/bj20031677",
      "volume": "380",
      "year": "2004",
      "journal-title": "Biochem. J."
    },
    {
      "key": "2023072219295873900_BIB7",
      "first-page": "3",
      "volume": "66",
      "year": "1995",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "2023072219295873900_BIB8",
      "doi-asserted-by": "crossref",
      "first-page": "256",
      "DOI": "10.1126/science.1077209",
      "volume": "299",
      "year": "2003",
      "journal-title": "Science."
    },
    {
      "key": "2023072219295873900_BIB9",
      "doi-asserted-by": "crossref",
      "first-page": "267",
      "DOI": "10.1146/annurev.neuro.26.010302.081142",
      "volume": "26",
      "year": "2003",
      "journal-title": "Annu. Rev. Neurosci."
    },
    {
      "key": "2023072219295873900_BIB10",
      "doi-asserted-by": "crossref",
      "first-page": "1191",
      "DOI": "10.1074/jbc.275.2.1191",
      "volume": "275",
      "year": "2000",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB11",
      "doi-asserted-by": "crossref",
      "first-page": "35071",
      "DOI": "10.1074/jbc.M203300200",
      "volume": "277",
      "year": "2002",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB12",
      "doi-asserted-by": "crossref",
      "first-page": "389",
      "DOI": "10.1111/j.1582-4934.2006.tb00407.x",
      "volume": "10",
      "year": "2006",
      "journal-title": "J. Cell. Mol. Med."
    },
    {
      "key": "2023072219295873900_BIB13",
      "doi-asserted-by": "crossref",
      "first-page": "351",
      "DOI": "10.1016/S0092-8674(00)00126-4",
      "volume": "103",
      "year": "2000",
      "journal-title": "Cell."
    },
    {
      "key": "2023072219295873900_BIB14",
      "doi-asserted-by": "crossref",
      "first-page": "16619",
      "DOI": "10.1074/jbc.M413591200",
      "volume": "280",
      "year": "2005",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB15",
      "doi-asserted-by": "crossref",
      "first-page": "834",
      "DOI": "10.1038/ncb1441",
      "volume": "8",
      "year": "2006",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "2023072219295873900_BIB16",
      "doi-asserted-by": "crossref",
      "first-page": "1239",
      "DOI": "10.1083/jcb.146.6.1239",
      "volume": "146",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072219295873900_BIB17",
      "doi-asserted-by": "crossref",
      "first-page": "388",
      "DOI": "10.1034/j.1600-0854.2002.30602.x",
      "volume": "3",
      "year": "2002",
      "journal-title": "Traffic."
    },
    {
      "key": "2023072219295873900_BIB18",
      "doi-asserted-by": "crossref",
      "first-page": "895",
      "DOI": "10.1038/nature02263",
      "volume": "426",
      "year": "2003",
      "journal-title": "Nature."
    },
    {
      "key": "2023072219295873900_BIB19",
      "doi-asserted-by": "crossref",
      "first-page": "43628",
      "DOI": "10.1074/jbc.M308947200",
      "volume": "278",
      "year": "2003",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB20",
      "doi-asserted-by": "crossref",
      "first-page": "6943",
      "DOI": "10.1074/jbc.M309204200",
      "volume": "279",
      "year": "2004",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB21",
      "doi-asserted-by": "crossref",
      "first-page": "103",
      "DOI": "10.1146/annurev.genom.7.080505.115737",
      "volume": "7",
      "year": "2006",
      "journal-title": "Annu. Rev. Genomics Hum. Genet."
    },
    {
      "key": "2023072219295873900_BIB22",
      "doi-asserted-by": "crossref",
      "first-page": "3353",
      "DOI": "10.1038/sj.emboj.7600808",
      "volume": "24",
      "year": "2005",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072219295873900_BIB23",
      "doi-asserted-by": "crossref",
      "first-page": "2059",
      "DOI": "10.1093/hmg/ddl131",
      "volume": "15",
      "year": "2006",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072219295873900_BIB24",
      "doi-asserted-by": "crossref",
      "first-page": "722",
      "DOI": "10.1016/S0140-6736(04)16901-8",
      "volume": "364",
      "year": "2004",
      "journal-title": "Lancet."
    },
    {
      "key": "2023072219295873900_BIB25",
      "doi-asserted-by": "crossref",
      "first-page": "884",
      "DOI": "10.1002/1531-8257(200009)15:5<884::AID-MDS1019>3.0.CO;2-8",
      "volume": "15",
      "year": "2000",
      "journal-title": "Mov. Disord."
    },
    {
      "key": "2023072219295873900_BIB26",
      "doi-asserted-by": "crossref",
      "first-page": "8567",
      "DOI": "10.1073/pnas.0503221102",
      "volume": "102",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072219295873900_BIB27",
      "doi-asserted-by": "crossref",
      "first-page": "4307",
      "DOI": "10.1038/sj.emboj.7600426",
      "volume": "23",
      "year": "2004",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072219295873900_BIB28",
      "doi-asserted-by": "crossref",
      "first-page": "13425",
      "DOI": "10.1073/pnas.172511699",
      "volume": "99",
      "year": "2002",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072219295873900_BIB29",
      "doi-asserted-by": "crossref",
      "first-page": "55",
      "DOI": "10.1016/S1097-2765(02)00583-X",
      "volume": "10",
      "year": "2002",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072219295873900_BIB30",
      "doi-asserted-by": "crossref",
      "first-page": "40282",
      "DOI": "10.1074/jbc.M508786200",
      "volume": "280",
      "year": "2005",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB31",
      "doi-asserted-by": "crossref",
      "first-page": "e156",
      "DOI": "10.1371/journal.pbio.0030156",
      "volume": "3",
      "year": "2005",
      "journal-title": "PLoS Biol."
    },
    {
      "key": "2023072219295873900_BIB32",
      "doi-asserted-by": "crossref",
      "first-page": "1883",
      "DOI": "10.1083/jcb.143.7.1883",
      "volume": "143",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072219295873900_BIB33",
      "doi-asserted-by": "crossref",
      "first-page": "26",
      "DOI": "10.1002/cm.10057",
      "volume": "53",
      "year": "2002",
      "journal-title": "Cell Motil. Cytoskeleton."
    },
    {
      "key": "2023072219295873900_BIB34",
      "doi-asserted-by": "crossref",
      "first-page": "47870",
      "DOI": "10.1074/jbc.M203159200",
      "volume": "277",
      "year": "2002",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB35",
      "doi-asserted-by": "crossref",
      "first-page": "681",
      "DOI": "10.1038/sj.embor.7400188",
      "volume": "5",
      "year": "2004",
      "journal-title": "EMBO Rep."
    },
    {
      "key": "2023072219295873900_BIB36",
      "doi-asserted-by": "crossref",
      "first-page": "727",
      "DOI": "10.1016/S0092-8674(03)00939-5",
      "volume": "115",
      "year": "2003",
      "journal-title": "Cell."
    },
    {
      "key": "2023072219295873900_BIB37",
      "doi-asserted-by": "crossref",
      "first-page": "1129",
      "DOI": "10.1091/mbc.e06-09-0787",
      "volume": "18",
      "year": "2007",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072219295873900_BIB38",
      "doi-asserted-by": "crossref",
      "first-page": "605",
      "DOI": "10.1038/33416",
      "volume": "392",
      "year": "1998",
      "journal-title": "Nature."
    },
    {
      "key": "2023072219295873900_BIB39",
      "doi-asserted-by": "crossref",
      "first-page": "7968",
      "DOI": "10.1523/JNEUROSCI.2172-05.2005",
      "volume": "25",
      "year": "2005",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "2023072219295873900_BIB40",
      "doi-asserted-by": "crossref",
      "first-page": "16193",
      "DOI": "10.1074/jbc.C600041200",
      "volume": "281",
      "year": "2006",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB41",
      "doi-asserted-by": "crossref",
      "first-page": "524",
      "DOI": "10.1016/S0962-8924(00)01852-3",
      "volume": "10",
      "year": "2000",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "2023072219295873900_BIB42",
      "doi-asserted-by": "crossref",
      "first-page": "175",
      "DOI": "10.1016/j.molcel.2007.04.001",
      "volume": "26",
      "year": "2007",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072219295873900_BIB43",
      "doi-asserted-by": "crossref",
      "first-page": "1091",
      "DOI": "10.1080/10715760500260348",
      "volume": "39",
      "year": "2005",
      "journal-title": "Free Radic. Res."
    },
    {
      "key": "2023072219295873900_BIB44",
      "doi-asserted-by": "crossref",
      "first-page": "2002",
      "DOI": "10.1523/JNEUROSCI.4474-04.2005",
      "volume": "25",
      "year": "2005",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "2023072219295873900_BIB45",
      "first-page": "524",
      "volume": "27",
      "year": "2005",
      "journal-title": "Neurobiol. Aging."
    },
    {
      "key": "2023072219295873900_BIB46",
      "doi-asserted-by": "crossref",
      "first-page": "1560",
      "DOI": "10.1056/NEJM200005253422103",
      "volume": "342",
      "year": "2000",
      "journal-title": "N. Engl. J. Med."
    },
    {
      "key": "2023072219295873900_BIB47",
      "doi-asserted-by": "crossref",
      "first-page": "205",
      "DOI": "10.1042/bj20031123",
      "volume": "377",
      "year": "2004",
      "journal-title": "Biochem. J."
    },
    {
      "key": "2023072219295873900_BIB48",
      "doi-asserted-by": "crossref",
      "first-page": "3204",
      "DOI": "10.1074/jbc.M510393200",
      "volume": "281",
      "year": "2006",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB49",
      "doi-asserted-by": "crossref",
      "first-page": "36588",
      "DOI": "10.1074/jbc.M304272200",
      "volume": "278",
      "year": "2003",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB50",
      "doi-asserted-by": "crossref",
      "first-page": "1558",
      "DOI": "10.1111/j.1471-4159.2003.02265.x",
      "volume": "87",
      "year": "2003",
      "journal-title": "J. Neurochem."
    },
    {
      "key": "2023072219295873900_BIB51",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1093/hmg/ddi007",
      "volume": "14",
      "year": "2005",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072219295873900_BIB52",
      "doi-asserted-by": "crossref",
      "first-page": "890",
      "DOI": "10.1212/WNL.51.3.890",
      "volume": "51",
      "year": "1998",
      "journal-title": "Neurology."
    },
    {
      "key": "2023072219295873900_BIB53",
      "first-page": "117",
      "volume": "13",
      "year": "2004",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072219295873900_BIB54",
      "doi-asserted-by": "crossref",
      "first-page": "496",
      "DOI": "10.1016/S1474-4422(04)00827-0",
      "volume": "3",
      "year": "2004",
      "journal-title": "Lancet Neurol."
    },
    {
      "key": "2023072219295873900_BIB55",
      "doi-asserted-by": "crossref",
      "first-page": "8506",
      "DOI": "10.1074/jbc.M311017200",
      "volume": "279",
      "year": "2004",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB56",
      "year": "2005"
    },
    {
      "key": "2023072219295873900_BIB57",
      "doi-asserted-by": "crossref",
      "first-page": "585",
      "DOI": "10.1002/cne.21191",
      "volume": "500",
      "year": "2007",
      "journal-title": "J. Comp. Neurol."
    },
    {
      "key": "2023072219295873900_BIB58",
      "doi-asserted-by": "crossref",
      "first-page": "48120",
      "DOI": "10.1074/jbc.M306889200",
      "volume": "278",
      "year": "2003",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB59",
      "doi-asserted-by": "crossref",
      "first-page": "2174",
      "DOI": "10.1073/pnas.0409598102",
      "volume": "102",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072219295873900_BIB60",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1186/1471-2202-6-71",
      "volume": "6",
      "year": "2005",
      "journal-title": "BMC Neurosci."
    },
    {
      "key": "2023072219295873900_BIB61",
      "doi-asserted-by": "crossref",
      "first-page": "1259",
      "DOI": "10.1111/j.1471-4159.2005.03442.x",
      "volume": "95",
      "year": "2005",
      "journal-title": "J. Neurochem."
    },
    {
      "key": "2023072219295873900_BIB62",
      "doi-asserted-by": "crossref",
      "first-page": "610",
      "DOI": "10.1016/j.cbpa.2004.09.009",
      "volume": "8",
      "year": "2004",
      "journal-title": "Curr. Opin. Chem. Biol."
    },
    {
      "key": "2023072219295873900_BIB63",
      "doi-asserted-by": "crossref",
      "first-page": "228",
      "DOI": "10.1251/bpo66",
      "volume": "5",
      "year": "2003",
      "journal-title": "Biol. Proced. Online."
    },
    {
      "key": "2023072219295873900_BIB64",
      "doi-asserted-by": "crossref",
      "first-page": "73",
      "DOI": "10.1016/j.cell.2004.11.013",
      "volume": "120",
      "year": "2005",
      "journal-title": "Cell."
    },
    {
      "key": "2023072219295873900_BIB65",
      "doi-asserted-by": "crossref",
      "first-page": "1655",
      "DOI": "10.1016/S0002-9440(10)61113-3",
      "volume": "160",
      "year": "2002",
      "journal-title": "Am. J. Pathol."
    },
    {
      "key": "2023072219295873900_BIB67",
      "doi-asserted-by": "crossref",
      "first-page": "e362",
      "DOI": "10.1371/journal.pbio.0020362",
      "volume": "2",
      "year": "2004",
      "journal-title": "PLoS Biol."
    },
    {
      "key": "2023072219295873900_BIB68",
      "doi-asserted-by": "crossref",
      "first-page": "302",
      "DOI": "10.1038/77060",
      "volume": "25",
      "year": "2000",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "2023072219295873900_BIB69",
      "doi-asserted-by": "crossref",
      "first-page": "263",
      "DOI": "10.1126/science.1060627",
      "volume": "293",
      "year": "2001",
      "journal-title": "Science."
    },
    {
      "key": "2023072219295873900_BIB70",
      "doi-asserted-by": "crossref",
      "first-page": "244",
      "DOI": "10.1016/j.tins.2007.03.009",
      "volume": "30",
      "year": "2007",
      "journal-title": "Trends Neurosci."
    },
    {
      "key": "2023072219295873900_BIB71",
      "doi-asserted-by": "crossref",
      "first-page": "437",
      "DOI": "10.1212/WNL.44.3_Part_1.437",
      "volume": "44",
      "year": "1994",
      "journal-title": "Neurology."
    },
    {
      "key": "2023072219295873900_BIB72",
      "doi-asserted-by": "crossref",
      "first-page": "749",
      "DOI": "10.1093/hmg/ddg074",
      "volume": "12",
      "year": "2003",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072219295873900_BIB73",
      "doi-asserted-by": "crossref",
      "first-page": "95",
      "DOI": "10.1016/S1097-2765(04)00151-0",
      "volume": "14",
      "year": "2004",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072219295873900_BIB74",
      "doi-asserted-by": "crossref",
      "first-page": "346",
      "DOI": "10.1038/35085597",
      "volume": "412",
      "year": "2001",
      "journal-title": "Nature."
    },
    {
      "key": "2023072219295873900_BIB75",
      "doi-asserted-by": "crossref",
      "first-page": "9394",
      "DOI": "10.1073/pnas.0502352102",
      "volume": "102",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072219295873900_BIB76",
      "doi-asserted-by": "crossref",
      "first-page": "169",
      "DOI": "10.1038/35056563",
      "volume": "2",
      "year": "2001",
      "journal-title": "Nat. Rev. Mol. Cell Biol."
    },
    {
      "key": "2023072219295873900_BIB77",
      "doi-asserted-by": "crossref",
      "first-page": "10273",
      "DOI": "10.1074/jbc.M107857200",
      "volume": "277",
      "year": "2002",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072219295873900_BIB78",
      "doi-asserted-by": "crossref",
      "first-page": "13354",
      "DOI": "10.1073/pnas.240347797",
      "volume": "97",
      "year": "2000",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072219295873900_BIB79",
      "doi-asserted-by": "crossref",
      "first-page": "4011",
      "DOI": "10.1242/jcs.00700",
      "volume": "116",
      "year": "2003",
      "journal-title": "J. Cell Sci."
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/178/6/1025/1547725/jcb_200611128.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/178/6/1025/1547725/jcb_200611128.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        22
      ]
    ],
    "date-time": "2023-07-22T19:31:23Z",
    "timestamp": 1690054283000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/178/6/1025/44862/Parkin-mediated-K63-linked-polyubiquitination"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2007,
        9,
        10
      ]
    ]
  },
  "references-count": 78,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2007,
          9,
          10
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.200611128",
  "relation": {},
  "ISSN": [
    "1540-8140",
    "0021-9525"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2007,
        9,
        10
      ]
    ]
  }
}