DOI: 10.1091/mbc.e04-02-0101. Organellar Proteomics Reveals Golgi Arginine Dimethylation

Organellar Proteomics Reveals Golgi Arginine Dimethylation

10.1091/mbc.e04-02-0101

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

The Golgi complex functions to posttranslationally modify newly synthesized proteins and lipids and to sort them to their sites of function. In this study, a stacked Golgi fraction was isolated by classical cell fractionation, and the protein complement (the Golgi proteome) was characterized using multidimensional protein identification technology. Many of the proteins identified are known residents of the Golgi, and 64% of these are predicted transmembrane proteins. Proteins localized to other organelles also were identified, strengthening reports of functional interfacing between the Golgi and the endoplasmic reticulum and cytoskeleton. Importantly, 41 proteins of unknown function were identified. Two were selected for further analysis, and Golgi localization was confirmed. One of these, a putative methyltransferase, was shown to be arginine dimethylated, and upon further proteomic analysis, arginine dimethylation was identified on 18 total proteins in the Golgi proteome. This survey illustrates the utility of proteomics in the discovery of novel organellar functions and resulted in 1) a protein profile of an enriched Golgi fraction; 2) identification of 41 previously uncharacterized proteins, two with confirmed Golgi localization; 3) the identification of arginine dimethylated residues in Golgi proteins; and 4) a confirmation of methyltransferase activity within the Golgi fraction.

Bibliography

Wu, C. C., MacCoss, M. J., Mardones, G., Finnigan, C., Mogelsvang, S., Yates, J. R., & Howell, K. E. (2004). Organellar Proteomics Reveals Golgi Arginine Dimethylation. Molecular Biology of the Cell, 15(6), 2907â2919.

Authors 7

Christine C. Wu (first)
Michael J. MacCoss (additional)
Gonzalo Mardones (additional)
Claire Finnigan (additional)
Soren Mogelsvang (additional)
John R. Yates (additional)
Kathryn E. Howell (additional)

References 49 Referenced 116

Dates

Type	When
Created	21 years, 4 months ago (March 29, 2004, 8:53 p.m.)
Deposited	6 years, 1 month ago (July 14, 2019, 12:37 p.m.)
Indexed	11 months, 1 week ago (Sept. 17, 2024, 6:48 a.m.)
Issued	21 years, 2 months ago (June 1, 2004)
Published	21 years, 2 months ago (June 1, 2004)
Published Print	21 years, 2 months ago (June 1, 2004)

Funders 0

None

BibTeX

@article{Wu_2004, title={Organellar Proteomics Reveals Golgi Arginine Dimethylation}, volume={15}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e04-02-0101}, DOI={10.1091/mbc.e04-02-0101}, number={6}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Wu, Christine C. and MacCoss, Michael J. and Mardones, Gonzalo and Finnigan, Claire and Mogelsvang, Soren and Yates, John R. and Howell, Kathryn E.}, year={2004}, month=jun, pages={2907–2919} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        9,
        17
      ]
    ],
    "date-time": "2024-09-17T10:48:22Z",
    "timestamp": 1726570102441
  },
  "reference-count": 49,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "6",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2004,
        6
      ]
    ]
  },
  "abstract": "<jats:p> The Golgi complex functions to posttranslationally modify newly synthesized proteins and lipids and to sort them to their sites of function. In this study, a stacked Golgi fraction was isolated by classical cell fractionation, and the protein complement (the Golgi proteome) was characterized using multidimensional protein identification technology. Many of the proteins identified are known residents of the Golgi, and 64% of these are predicted transmembrane proteins. Proteins localized to other organelles also were identified, strengthening reports of functional interfacing between the Golgi and the endoplasmic reticulum and cytoskeleton. Importantly, 41 proteins of unknown function were identified. Two were selected for further analysis, and Golgi localization was confirmed. One of these, a putative methyltransferase, was shown to be arginine dimethylated, and upon further proteomic analysis, arginine dimethylation was identified on 18 total proteins in the Golgi proteome. This survey illustrates the utility of proteomics in the discovery of novel organellar functions and resulted in 1) a protein profile of an enriched Golgi fraction; 2) identification of 41 previously uncharacterized proteins, two with confirmed Golgi localization; 3) the identification of arginine dimethylated residues in Golgi proteins; and 4) a confirmation of methyltransferase activity within the Golgi fraction. </jats:p>",
  "DOI": "10.1091/mbc.e04-02-0101",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2004,
        3,
        30
      ]
    ],
    "date-time": "2004-03-30T01:53:25Z",
    "timestamp": 1080611605000
  },
  "page": "2907-2919",
  "source": "Crossref",
  "is-referenced-by-count": 116,
  "title": "Organellar Proteomics Reveals Golgi Arginine Dimethylation",
  "prefix": "10.1091",
  "volume": "15",
  "author": [
    {
      "given": "Christine C.",
      "family": "Wu",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Cell Biology, The Scripps Research Institute, La Jolla, California 92037"
        }
      ]
    },
    {
      "given": "Michael J.",
      "family": "MacCoss",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Cell Biology, The Scripps Research Institute, La Jolla, California 92037"
        }
      ]
    },
    {
      "given": "Gonzalo",
      "family": "Mardones",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Cell and Developmental Biology, University of Colorado Health Sciences Center, Denver, Colorado 80262"
        }
      ]
    },
    {
      "given": "Claire",
      "family": "Finnigan",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Cell and Developmental Biology, University of Colorado Health Sciences Center, Denver, Colorado 80262"
        }
      ]
    },
    {
      "given": "Soren",
      "family": "Mogelsvang",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Cell and Developmental Biology, University of Colorado Health Sciences Center, Denver, Colorado 80262"
        }
      ]
    },
    {
      "suffix": "III",
      "given": "John R.",
      "family": "Yates",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Cell Biology, The Scripps Research Institute, La Jolla, California 92037"
        }
      ]
    },
    {
      "given": "Kathryn E.",
      "family": "Howell",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Cell and Developmental Biology, University of Colorado Health Sciences Center, Denver, Colorado 80262"
        }
      ]
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "REF1",
      "doi-asserted-by": "crossref",
      "unstructured": "Allan, V.J., Thompson, H.M., and McNiven, M.A. (2002). Motoring around the Golgi. Nat. Cell Biol. 10, 236-242.",
      "DOI": "10.1038/ncb1002-e236"
    },
    {
      "key": "REF2",
      "doi-asserted-by": "crossref",
      "unstructured": "Andersen, J.S., Wilkinson, C.J., Mayor, T., Mortensen, P., Nigg, E.A., and Mann, M. (2003). Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570-574.",
      "DOI": "10.1038/nature02166"
    },
    {
      "key": "REF3",
      "doi-asserted-by": "crossref",
      "unstructured": "Bannister, A.J., Schneider, R., and Kouzarides, T. (2002). Histone methylation: dynamic or static? Cell 109, 801-806.",
      "DOI": "10.1016/S0092-8674(02)00798-5"
    },
    {
      "key": "REF4",
      "doi-asserted-by": "crossref",
      "unstructured": "Bell, A.W. et al. (2001). Proteomics characterization of abundant Golgi membrane proteins. J. Biol. Chem. 276, 5152-565.",
      "DOI": "10.1074/jbc.M006143200"
    },
    {
      "key": "REF5",
      "doi-asserted-by": "crossref",
      "unstructured": "Casaubon, R.L., and Snapper, M.L. (2001). S-adenosylmethionine reverses ilimaquinone's vesiculation of the Golgi apparatus: a fluorescence study on the cellular interactions of ilimaquinone. Bioorg. Med. Chem. Lett. 11, 133-136.",
      "DOI": "10.1016/S0960-894X(00)00617-X"
    },
    {
      "key": "REF6",
      "doi-asserted-by": "crossref",
      "unstructured": "Colanzi, A., Suetterlin, C., and Malhotra, V. (2003). Cell-cycle-specific Golgi fragmentation: how and why? Curr. Opin. Cell Biol. 15, 462-467.",
      "DOI": "10.1016/S0955-0674(03)00067-X"
    },
    {
      "key": "REF7",
      "doi-asserted-by": "crossref",
      "unstructured": "Donaldson, J.G., and Lippincott-Schwartz, J. (2000). Sorting and signaling at the Golgi complex. Cell 101, 693-696.",
      "DOI": "10.1016/S0092-8674(00)80881-8"
    },
    {
      "key": "REF8",
      "doi-asserted-by": "crossref",
      "unstructured": "Doyle, H.A., and Mamula, M.J. (2002). Posttranslational protein modifications: new flavors in the menu of autoantigens. Curr. Opin. Rheumatol. 1, 244-249.",
      "DOI": "10.1097/00002281-200205000-00009"
    },
    {
      "key": "REF9",
      "doi-asserted-by": "crossref",
      "unstructured": "Eng, J.K., McCormack, A.L., and Yates III, J.R. (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass. Spectrom. 5, 967-989.",
      "DOI": "10.1016/1044-0305(94)80016-2"
    },
    {
      "key": "REF10",
      "doi-asserted-by": "crossref",
      "unstructured": "Fischle, W., Wang, Y., and Allis, C.D. (2003). Binary switches and modification cassettes in histone biology and beyond. Nature 425, 475-479.",
      "DOI": "10.1038/nature02017"
    },
    {
      "key": "REF11",
      "doi-asserted-by": "crossref",
      "unstructured": "Florens, L. et al. (2002). A proteomic view of the Plasmodium falciparum life cycle. Nature 419, 520-526.",
      "DOI": "10.1038/nature01107"
    },
    {
      "key": "REF12",
      "doi-asserted-by": "crossref",
      "unstructured": "Friesen, W.J., Massenet, S., Paushkin, S., Wyce, A., and Dreyfuss, G. (2001a). SMN, the product of the spinal muscular atrophy gene, binds preferentially to dimethylarginine-containing protein targets. Mol. Cell. 7, 1111-1117.",
      "DOI": "10.1016/S1097-2765(01)00244-1"
    },
    {
      "key": "REF13",
      "doi-asserted-by": "crossref",
      "unstructured": "Friesen, W.J., Paushkin, S., Wyce, A., Massenet, S., Pesiridis, G.S., Van Duyne, G., Rappsilber, J., Mann, M., and Dreyfuss, G. (2001b). The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol. Cell. Biol. 21, 8289-8300.",
      "DOI": "10.1128/MCB.21.24.8289-8300.2001"
    },
    {
      "key": "REF14",
      "doi-asserted-by": "crossref",
      "unstructured": "Gao, J., Opiteck, G.J., Friedrichs, M.S., Dongre, A.R., and Hefta, S.A. (2003). Changes in the protein expression of yeast as a function of carbon source. J. Proteome Res. 2, 643-649.",
      "DOI": "10.1021/pr034038x"
    },
    {
      "key": "REF15",
      "doi-asserted-by": "crossref",
      "unstructured": "Hanada, K., Kumagai, K., Yasuda, S., Miura, Y., Kawano, M., Fukasawa, M., and Nishijima, M. (2003). Molecular machinery for non-vesicular trafficking of ceramide. Nature 426, 803-809.",
      "DOI": "10.1038/nature02188"
    },
    {
      "key": "REF16",
      "doi-asserted-by": "crossref",
      "unstructured": "Huber, L.A., Pfaller, K., and Vietor, I. (2003). Organelle proteomics: implications for subcellular fractionation in proteomics. Circ. Res. 92, 962-968.",
      "DOI": "10.1161/01.RES.0000071748.48338.25"
    },
    {
      "key": "REF17",
      "doi-asserted-by": "crossref",
      "unstructured": "Kim, J.K., Mastronardi, F.G, Wood, D.D., Lubman, D.M., and Moscarello, M.A. (2003). Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Mol. Cell Proteomics 2, 453-462.",
      "DOI": "10.1074/mcp.M200050-MCP200"
    },
    {
      "key": "REF18",
      "doi-asserted-by": "crossref",
      "unstructured": "Ladinsky, M.S., Mastronarde, D.N., McIntosh, J.R., Howell, K.E., and Staehelin. L.A. (1999). Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144, 1135-1149.",
      "DOI": "10.1083/jcb.144.6.1135"
    },
    {
      "key": "REF19",
      "doi-asserted-by": "crossref",
      "unstructured": "Laird, P.W. (2003). The power and the promise of DNA methylation markers. Nat. Rev. Cancer 4, 253-266.",
      "DOI": "10.1038/nrc1045"
    },
    {
      "key": "REF20",
      "doi-asserted-by": "crossref",
      "unstructured": "Lin, C.H., Hsieh, M., Li, Y.C., Li, S.Y., Pearson, D.L., Pollard, K.M., and Li, C. (2000). Protein N-arginine methylation in subcellular fractions of lymphoblastoid cells. J. Biochem. 128, 493-498.",
      "DOI": "10.1093/oxfordjournals.jbchem.a022779"
    },
    {
      "key": "REF21",
      "doi-asserted-by": "crossref",
      "unstructured": "Link A.J., Eng, J., Schieltz, D.M., Carmack, E., Mize, G.J., Morris, R.D., Garvik, B.M., and Yates III, J.R. (1999). Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17, 676-682.",
      "DOI": "10.1038/10890"
    },
    {
      "key": "REF22",
      "doi-asserted-by": "crossref",
      "unstructured": "Lowe, M., Nakamura, N., and Warren, G. (1998). Golgi division and membrane traffic. Trends Cell Biol. 8, 40-44.",
      "DOI": "10.1016/S0962-8924(97)01189-6"
    },
    {
      "key": "REF23",
      "doi-asserted-by": "crossref",
      "unstructured": "MacCoss, M.J. et al. (2002a). Shotgun identification of protein modifications from protein complexes and lens tissue. Proc. Natl. Acad. Sci. USA 99, 7900-7905.",
      "DOI": "10.1073/pnas.122231399"
    },
    {
      "key": "REF24",
      "doi-asserted-by": "crossref",
      "unstructured": "MacCoss, M.J., Wu, C.C., and Yates III, J.R. (2002b). Probability-based validation of protein identifications using a modified SEQUEST algorithm. Anal. Chem. 74, 5593-5599.",
      "DOI": "10.1021/ac025826t"
    },
    {
      "key": "REF25",
      "doi-asserted-by": "crossref",
      "unstructured": "Marsh, B.J., Mastronarde, D.N., Buttle, K.F., Howell, K.E., and McIntosh, J.R. (2001). Organellar relationships in the Golgi region of pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc. Nat. Acad. Sci. USA 98, 2399-2406.",
      "DOI": "10.1073/pnas.051631998"
    },
    {
      "key": "REF26",
      "doi-asserted-by": "crossref",
      "unstructured": "Martin, S.E., Shabanowitz, J., Hunt, D.F., and Marto, J.A. (2000). Subfemtomole MS and MS/MS peptide sequence analysis using nano-HPLC micro-ESI Fourier transform ion cyclotron resonance mass spectrometry. Anal. Chem. 72, 4266-4274.",
      "DOI": "10.1021/ac000497v"
    },
    {
      "key": "REF27",
      "doi-asserted-by": "crossref",
      "unstructured": "McBride, A.E., and Silver, P.A. (2001). State of the Arg: protein methylation at arginine comes of age. Cell 106, 5-8.",
      "DOI": "10.1016/S0092-8674(01)00423-8"
    },
    {
      "key": "REF28",
      "doi-asserted-by": "crossref",
      "unstructured": "Mootha, V.K. et al. (2003). Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115, 629-640.",
      "DOI": "10.1016/S0092-8674(03)00926-7"
    },
    {
      "key": "REF29",
      "doi-asserted-by": "crossref",
      "unstructured": "Munro, S. (2003). Cell biology: earthworms and lipid couriers. Nature 42, 775-776.",
      "DOI": "10.1038/426775a"
    },
    {
      "key": "REF30",
      "doi-asserted-by": "crossref",
      "unstructured": "Nozawa, K., Casiano, C.A., Hamel, J.C., Molinaro, C., Fritzler, M.J., and Chan. C. (2002). Fragmentation of Golgi complex and Golgi autoantigens during apoptosis and necrosis. Arthritis Res. 4, 1-9.",
      "DOI": "10.1186/ar422"
    },
    {
      "key": "REF31",
      "unstructured": "Novikoff, A.B. (1964). GERL, its form and function in neurons of rat spinal ganglia. Biol. Bull. 127, 358"
    },
    {
      "key": "REF32",
      "doi-asserted-by": "crossref",
      "unstructured": "Palade, G.E. (1975). Intracellular aspects of the process of protein secretion. Science 189, 347-358.",
      "DOI": "10.1126/science.1096303"
    },
    {
      "key": "REF33",
      "doi-asserted-by": "crossref",
      "unstructured": "Radeke, H.S., Digits, C.A., Casaubon, R.L., and Snapper, M.L. (1999). Interactions of (-)-ilimaquinone with methylation enzymes: implications for vesicular-mediated secretion. Chem. Biol. 9, 639-647.",
      "DOI": "10.1016/S1074-5521(99)80115-X"
    },
    {
      "key": "REF34",
      "doi-asserted-by": "crossref",
      "unstructured": "Roepstorff, P. and Fohlman J. (1984). Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed. Mass. Spectrom. 11, 601.",
      "DOI": "10.1002/bms.1200111109"
    },
    {
      "key": "REF35",
      "doi-asserted-by": "crossref",
      "unstructured": "Schirmer, E.C., Florens, L., Guan, T., Yates III, J.R., and Gerace, L. (2003). Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 301, 1380-1382.",
      "DOI": "10.1126/science.1088176"
    },
    {
      "key": "REF36",
      "doi-asserted-by": "crossref",
      "unstructured": "Schubert, H.L., Blumenthal, R.M., and Cheng, X. (2003). Many paths to methyltransfer: a chronicle of convergence. Trends Biochem. Sci. 28, 329-335.",
      "DOI": "10.1016/S0968-0004(03)00090-2"
    },
    {
      "key": "REF37",
      "doi-asserted-by": "crossref",
      "unstructured": "Shields, D., and Arvan, P. (1999). Disease models provide insights into post-Golgi protein trafficking, localization and processing. Curr. Opin. Cell Biol. 11, 489-494.",
      "DOI": "10.1016/S0955-0674(99)80070-2"
    },
    {
      "key": "REF38",
      "doi-asserted-by": "crossref",
      "unstructured": "Tabb, D.L., McDonald, H.D., and Yates, III, J.R. (2002). DTASelect and Contrast: tools for assembling and comparting protein identification form Shotgun proteomics. J. Proteome Res. 1, 21-26.",
      "DOI": "10.1021/pr015504q"
    },
    {
      "key": "REF39",
      "doi-asserted-by": "crossref",
      "unstructured": "Takizawa, P.A., Yucel, J.K. Veit B., Faulkner, D.J. Deerinck, T., Soto, G., Ellisman, M., and V. Malhotra, V. (1993). Complete vesiculation of Golgi membranes and inhibition of protein transport by a novel sea sponge metabolite, ilimaquinone. Cell 73, 1079-1090.",
      "DOI": "10.1016/0092-8674(93)90638-7"
    },
    {
      "key": "REF40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.8.10.1911"
    },
    {
      "key": "REF41",
      "doi-asserted-by": "crossref",
      "unstructured": "Taylor, R.S., Wu, C.C., Hays, L.G., Eng, J.K., Yates, J.R. 3rd, and Howell, K.E. (2000). Proteomics of rat liver Golgi complex: minor proteins are identified through sequential fractionation. Electrophoresis. 16, 3441-3459.",
      "DOI": "10.1002/1522-2683(20001001)21:16<3441::AID-ELPS3441>3.0.CO;2-G"
    },
    {
      "key": "REF42",
      "doi-asserted-by": "crossref",
      "unstructured": "Van Lint, J., Rykx, A., Maeda, Y., Vantus, T., Sturany, S., Malhotra, V., Vandenheede, J.R., and Seufferlein, T. (2002). Protein kinase D: an intracellular traffic regulator on the move. Trends Cell Biol. 12, 193-200.",
      "DOI": "10.1016/S0962-8924(02)02262-6"
    },
    {
      "key": "REF43",
      "doi-asserted-by": "crossref",
      "unstructured": "van Meer, G., and Lisma, Q. (2002). Sphingolipid transport: rafts and translocators. J. Biol. Chem. 277, 25855-25858.",
      "DOI": "10.1074/jbc.R200010200"
    },
    {
      "key": "REF44",
      "doi-asserted-by": "crossref",
      "unstructured": "Ward, T.H., Polishchuk, R.S., Caplan, S., Hirschberg. K., and Lippincott-Schwartz, J. (2001). Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557-570.",
      "DOI": "10.1083/jcb.200107045"
    },
    {
      "key": "REF45",
      "doi-asserted-by": "crossref",
      "unstructured": "Washburn, M.P., Wolters, D. and Yates III, J.R. (2001). Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247.",
      "DOI": "10.1038/85686"
    },
    {
      "key": "REF46",
      "doi-asserted-by": "crossref",
      "unstructured": "Westermann, S., Cheeseman, I.M., Anderson, S., Yates III, J.R., Drubin, D.G., and Barnes, G. (2003). Architecture of the budding yeast kinetochore reveals a conserved molecular core. J. Cell Biol. 163, 215-222.",
      "DOI": "10.1083/jcb.200305100"
    },
    {
      "key": "REF47",
      "doi-asserted-by": "crossref",
      "unstructured": "Wu, C.C., MacCoss, M.J., Howell, K.E., and Yates III, J.R. (2003). A method for the comprehensive proteomic analysis of membrane proteins. Nat. Biotechnol. 21, 532-538.",
      "DOI": "10.1038/nbt819"
    },
    {
      "key": "REF48",
      "doi-asserted-by": "crossref",
      "unstructured": "Wu, C.C., and Yates III, J.R. (2003). The application of mass spectrometry to membrane proteomics. Nat. Biotechnol. 21, 262-267.",
      "DOI": "10.1038/nbt0303-262"
    },
    {
      "key": "REF49",
      "doi-asserted-by": "crossref",
      "unstructured": "Wu, C.C., Yates III, J.R., Neville, M.C., and Howell, K.E. (2000). Proteomic analysis of two functional states of the Golgi complex in mammary epithelial cells. Traffic 1, 769-782.",
      "DOI": "10.1034/j.1600-0854.2000.011004.x"
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2019,
        7,
        14
      ]
    ],
    "date-time": "2019-07-14T16:37:07Z",
    "timestamp": 1563122227000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.e04-02-0101"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2004,
        6
      ]
    ]
  },
  "references-count": 49,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2004,
          6
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.e04-02-0101"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.e04-02-0101",
  "relation": {},
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        2004,
        6
      ]
    ]
  }
}