DOI: 10.1091/mbc.12.6.1819. Sphingomyelin-enriched Microdomains at the Golgi Complex

Sphingomyelin-enriched Microdomains at the Golgi Complex

10.1091/mbc.12.6.1819

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Sphingomyelin- and cholesterol-enriched microdomains can be isolated as detergent-resistant membranes from total cell extracts (total-DRM). It is generally believed that this total-DRM represents microdomains of the plasma membrane. Here we describe the purification and detailed characterization of microdomains from Golgi membranes. These Golgi-derived detergent-insoluble complexes (GICs) have a low buoyant density and are highly enriched in lipids, containing 25% of total Golgi phospholipids including 67% of Golgi-derived sphingomyelin, and 43% of Golgi-derived cholesterol. In contrast to total-DRM, GICs contain only 10 major proteins, present in nearly stoichiometric amounts, including the α- and β-subunits of heterotrimeric G proteins, flotillin-1, caveolin, and subunits of the vacuolar ATPase. Morphological data show a brefeldin A-sensitive and temperature-sensitive localization to the Golgi complex. Strikingly, the stability of GICs does not depend on its membrane environment, because, after addition of brefeldin A to cells, GICs can be isolated from a fused Golgi-endoplasmic reticulum organelle. This indicates that GIC microdomains are not in a dynamic equilibrium with neighboring membrane proteins and lipids. After disruption of the microdomains by cholesterol extraction with cyclodextrin, a subcomplex of several GIC proteins including the B-subunit of the vacuolar ATPase, flotillin-1, caveolin, and p17 could still be isolated by immunoprecipitation. This indicates that several of the identified GIC proteins localize to the same microdomains and that the microdomain scaffold is not required for protein interactions between these GIC proteins but instead might modulate their affinity.

Bibliography

Gkantiragas, I., BrÃ¼gger, B., StÃ¼ven, E., Kaloyanova, D., Li, X.-Y., LÃ¶hr, K., Lottspeich, F., Wieland, F. T., & Helms, J. B. (2001). Sphingomyelin-enriched Microdomains at the Golgi Complex. Molecular Biology of the Cell, 12(6), 1819â1833.

Authors 9

Ioannis Gkantiragas (first)
Britta Brügger (additional)
Ernstpeter Stüven (additional)
Dora Kaloyanova (additional)
Xue-Yi Li (additional)
Kristina Löhr (additional)
Friedrich Lottspeich (additional)
Felix T. Wieland (additional)
J. Bernd Helms (additional)

References 76 Referenced 129

10.1146/annurev.biochem.67.1.199 / Annu. Rev. Biochem. by Anderson R.G.W. (1998)
10.1073/pnas.97.7.3254 / Proc. Natl. Acad. Sci USA by Bagnat M. (2000)
10.1016/0092-8674(84)90019-9 / Cell. by Balch W.E. (1984)
10.1074/jbc.272.21.13793 / J. Biol. Chem. by Bickel P.E. (1997)
10.1139/y59-099 / Can. J. Biochem. Physiol. by Bligh E.G. (1959)
10.1091/mbc.3.12.1317
10.1126/science.8362242 / Science by Bretscher M.S. (1993)
10.1007/s002329900397 / J. Membr. Biol. by Brown D.A. (1998)
10.1016/0092-8674(92)90189-J / Cell. by Brown D.A. (1992)
10.1073/pnas.94.6.2339 / Proc. Natl. Acad. Sci. USA. by Brügger B. (1997)
10.1083/jcb.151.3.507 / J. Cell Biol. by Brügger B. (2000)
10.1083/jcb.126.1.127 / J. Cell Biol. by Chang W.J. (1994)
10.1083/jcb.133.5.1027 / J. Cell Biol. by Denker S.P. (1996)
10.1016/0962-8924(91)90064-G / Trends Cell Biol. by Duden R. (1991)
10.1002/j.1460-2075.1993.tb05804.x / EMBO J. by Dupree P. (1993)
10.1007/BF02290390 / Chromatographia by Eckerskorn C. (1989)
10.1073/pnas.96.4.1327 / Proc. Natl. Acad. Sci. USA by Exner T. (1999)
10.1021/bi00076a009 / Biochemistry by Fiedler K. (1993)
10.1042/bj3240697 / Biochem. J. by Finbow M.E. (1997)
10.1146/annurev.cellbio.13.1.779 / Annu. Rev. Cell Dev. Biol. by Forgac M. (1997)
10.1016/S0021-9258(18)47340-1 / J. Biol. Chem. by Fra A.M. (1994)
10.1038/29570 / Nature by Friedrichson T. (1998)
10.1016/S0378-1119(98)00064-X / Gene by Galbiati F. (1998)
10.1083/jcb.152.1.165 / J. Cell Biol. by Garin J. (2001)
10.1038/15658 / Nat. Cell Biol. by Girod A. (1999)
10.1083/jcb.129.3.619 / J. Cell Biol. by Gorodinsky A. (1995)
10.1016/0003-2697(89)90089-4 / Anal. Biochem. by Grassel S. (1989)
10.1083/jcb.141.4.929 / J. Cell Biol. by Harder T. (1998)
10.1242/jcs.113.4.587 / J. Cell Sci. by Hauri H.P. (2000)
10.1073/pnas.140218797 / Proc. Natl. Acad. Sci. USA by Heino S. (2000)
10.1016/0014-5793(95)00620-O / FEBS Lett. by Helms J.B. (1995)
10.1074/jbc.273.24.15203 / J. Biol. Chem. by Helms J.B. (1998)
10.1016/S0962-8924(98)01495-0 / Trends Cell Biol. by Jacobson K. (1999)
10.1016/S0092-8674(00)80449-3 / Cell. by Jamora C. (1997)
10.1083/jcb.142.1.69 / J. Cell Biol. by Kenworthy A.K. (1998)
10.1091/mbc.11.5.1645
10.1083/jcb.116.5.1071 / J. Cell Biol. by Klausner R.D. (1992)
{'key': 'B38', 'first-page': '187', 'volume': '5', 'author': 'Kurzchalia T.V.', 'year': '1995', 'journal-title': 'Trends Cell Biol.'} / Trends Cell Biol. by Kurzchalia T.V. (1995)
10.1002/(SICI)1097-4695(199812)37:4<502::AID-NEU2>3.0.CO;2-S / J. Neurobiol. by Lang D.M. (1998)
10.1016/0092-8674(89)90685-5 / Cell by Lippincott-Schwartz J. (1989)
10.1016/S0021-9258(19)52451-6 / J. Biol. Chem. by Lowry O.H. (1951)
10.1083/jcb.145.7.1443 / J. Cell Biol. by Luetterforst R. (1999)
10.1083/jcb.148.1.17 / J. Cell Biol. by Machleidt T. (2000)
10.1093/emboj/18.24.6917 / EMBO J. by Madore N. (1999)
10.1016/0092-8674(89)90847-7 / Cell by Malhotra V. (1989)
10.1006/excr.1996.0133 / Exp. Cell Res. by Mineo C. (1996)
10.1091/mbc.6.7.911
10.1074/jbc.274.36.25708 / J. Biol. Chem. by Mora R. (1999)
10.1016/S0962-8924(97)01197-5 / Trends Cell Biol. by Munro S. (1998)
10.1074/jbc.273.10.5419 / J. Biol. Chem. by Okamoto T. (1998)
10.1074/jbc.274.36.25718 / J. Biol. Chem. by Parolini I. (1999)
10.1038/35054500 / Nature by Peters C. (2001)
10.1083/jcb.148.5.997 / J. Cell Biol. by Pralle A. (2000)
10.1007/BF02531316 / Lipids by Rouser G. (1970)
10.1016/S0022-2275(20)33347-2 / J. Lipid Res. by Sandhoff R. (1999)
10.1083/jcb.122.4.789 / J. Cell Biol. by Sargiacomo M. (1993)
10.1093/emboj/16.18.5501 / EMBO J. by Scheiffele P. (1997)
10.1126/science.7660128 / Science. by Schnitzer J.E. (1995)
10.1242/dev.124.2.577 / Development by Schulte T. (1997)
10.1083/jcb.107.5.1643 / J. Cell Biol. by Schweizer A. (1988)
10.1038/349215a0 / Nature by Serafini T. (1991)
10.1042/bj3430627 / Biochem. J. by Sevlever D. (1999)
10.1038/42408 / Nature by Simons K. (1997)
10.1021/bi00417a001 / Biochemistry by Simons K. (1988)
10.1083/jcb.127.5.1185 / J. Cell Biol. by Smart E.J. (1994)
10.1083/jcb.135.5.1239 / J. Cell Biol. by Sohn K. (1996)
10.1083/jcb.114.6.1113 / J. Cell Biol. by Stow J.L. (1991)
10.1016/S0968-0004(99)01467-X / Trends Biochem. Sci. by Tavernarakis N. (1999)
10.1016/0092-8674(90)90097-X / Cell. by Tooze S.A. (1990)
10.1016/0955-0674(93)90137-F / Curr. Opin. Cell Biol. by van Meer G. (1993)
10.1016/S0962-8924(97)01196-3 / Trends Cell Biol. by van Meer G. (1998)
10.1038/29563 / Nature by Varma R. (1998)
10.1083/jcb.147.4.743 / J. Cell Biol. by White J. (1999)
10.1210/endo.134.1.8275939 / Endocrinology by Wilson B.S. (1994)
10.1083/jcb.149.5.1131 / J. Cell Biol. by Wilson B.S. (2000)
10.1074/jbc.272.40.25260 / J. Biol. Chem. by Yamaguchi T. (1997)

Dates

Type	When
Created	12 years, 1 month ago (July 2, 2013, 8:15 p.m.)
Deposited	3 years, 6 months ago (Feb. 26, 2022, 9:45 p.m.)
Indexed	9 months, 1 week ago (Nov. 19, 2024, 11:42 a.m.)
Issued	24 years, 2 months ago (June 1, 2001)
Published	24 years, 2 months ago (June 1, 2001)
Published Print	24 years, 2 months ago (June 1, 2001)

Funders 0

None

BibTeX

@article{Gkantiragas_2001, title={Sphingomyelin-enriched Microdomains at the Golgi Complex}, volume={12}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.12.6.1819}, DOI={10.1091/mbc.12.6.1819}, number={6}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Gkantiragas, Ioannis and Brügger, Britta and Stüven, Ernstpeter and Kaloyanova, Dora and Li, Xue-Yi and Löhr, Kristina and Lottspeich, Friedrich and Wieland, Felix T. and Helms, J. Bernd}, editor={Malhotra, Vivek}, year={2001}, month=jun, pages={1819–1833} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        11,
        19
      ]
    ],
    "date-time": "2024-11-19T16:42:55Z",
    "timestamp": 1732034575052
  },
  "reference-count": 76,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "6",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        6
      ]
    ]
  },
  "abstract": "<jats:p>Sphingomyelin- and cholesterol-enriched microdomains can be isolated as detergent-resistant membranes from total cell extracts (total-DRM). It is generally believed that this total-DRM represents microdomains of the plasma membrane. Here we describe the purification and detailed characterization of microdomains from Golgi membranes. These Golgi-derived detergent-insoluble complexes (GICs) have a low buoyant density and are highly enriched in lipids, containing 25% of total Golgi phospholipids including 67% of Golgi-derived sphingomyelin, and 43% of Golgi-derived cholesterol. In contrast to total-DRM, GICs contain only 10 major proteins, present in nearly stoichiometric amounts, including the \u03b1- and \u03b2-subunits of heterotrimeric G proteins, flotillin-1, caveolin, and subunits of the vacuolar ATPase. Morphological data show a brefeldin A-sensitive and temperature-sensitive localization to the Golgi complex. Strikingly, the stability of GICs does not depend on its membrane environment, because, after addition of brefeldin A to cells, GICs can be isolated from a fused Golgi-endoplasmic reticulum organelle. This indicates that GIC microdomains are not in a dynamic equilibrium with neighboring membrane proteins and lipids. After disruption of the microdomains by cholesterol extraction with cyclodextrin, a subcomplex of several GIC proteins including the B-subunit of the vacuolar ATPase, flotillin-1, caveolin, and p17 could still be isolated by immunoprecipitation. This indicates that several of the identified GIC proteins localize to the same microdomains and that the microdomain scaffold is not required for protein interactions between these GIC proteins but instead might modulate their affinity.</jats:p>",
  "DOI": "10.1091/mbc.12.6.1819",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2013,
        7,
        3
      ]
    ],
    "date-time": "2013-07-03T00:15:20Z",
    "timestamp": 1372810520000
  },
  "page": "1819-1833",
  "source": "Crossref",
  "is-referenced-by-count": 129,
  "title": "Sphingomyelin-enriched Microdomains at the Golgi Complex",
  "prefix": "10.1091",
  "volume": "12",
  "author": [
    {
      "given": "Ioannis",
      "family": "Gkantiragas",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Biochemie-Zentrum Heidelberg (BZH), University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany; and"
        }
      ]
    },
    {
      "given": "Britta",
      "family": "Br\u00fcgger",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Biochemie-Zentrum Heidelberg (BZH), University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany; and"
        }
      ]
    },
    {
      "given": "Ernstpeter",
      "family": "St\u00fcven",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Biochemie-Zentrum Heidelberg (BZH), University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany; and"
        }
      ]
    },
    {
      "given": "Dora",
      "family": "Kaloyanova",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Biochemie-Zentrum Heidelberg (BZH), University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany; and"
        }
      ]
    },
    {
      "given": "Xue-Yi",
      "family": "Li",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Biochemie-Zentrum Heidelberg (BZH), University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany; and"
        }
      ]
    },
    {
      "given": "Kristina",
      "family": "L\u00f6hr",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Biochemie-Zentrum Heidelberg (BZH), University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany; and"
        }
      ]
    },
    {
      "given": "Friedrich",
      "family": "Lottspeich",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Max-Planck Institut f\u00fcr Biochemie, Martinsried, Germany"
        }
      ]
    },
    {
      "given": "Felix T.",
      "family": "Wieland",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Biochemie-Zentrum Heidelberg (BZH), University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany; and"
        }
      ]
    },
    {
      "given": "J. Bernd",
      "family": "Helms",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Biochemie-Zentrum Heidelberg (BZH), University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany; and"
        }
      ]
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "B1",
      "doi-asserted-by": "crossref",
      "first-page": "199",
      "DOI": "10.1146/annurev.biochem.67.1.199",
      "volume": "67",
      "author": "Anderson R.G.W.",
      "year": "1998",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "B2",
      "doi-asserted-by": "crossref",
      "first-page": "3254",
      "DOI": "10.1073/pnas.97.7.3254",
      "volume": "97",
      "author": "Bagnat M.",
      "year": "2000",
      "journal-title": "Proc. Natl. Acad. Sci USA"
    },
    {
      "key": "B3",
      "doi-asserted-by": "crossref",
      "first-page": "405",
      "DOI": "10.1016/0092-8674(84)90019-9",
      "volume": "39",
      "author": "Balch W.E.",
      "year": "1984",
      "journal-title": "Cell."
    },
    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "13793",
      "DOI": "10.1074/jbc.272.21.13793",
      "volume": "272",
      "author": "Bickel P.E.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "911",
      "DOI": "10.1139/y59-099",
      "volume": "37",
      "author": "Bligh E.G.",
      "year": "1959",
      "journal-title": "Can. J. Biochem. Physiol."
    },
    {
      "key": "B6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.3.12.1317"
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "1280",
      "DOI": "10.1126/science.8362242",
      "volume": "261",
      "author": "Bretscher M.S.",
      "year": "1993",
      "journal-title": "Science"
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "103",
      "DOI": "10.1007/s002329900397",
      "volume": "164",
      "author": "Brown D.A.",
      "year": "1998",
      "journal-title": "J. Membr. Biol."
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "533",
      "DOI": "10.1016/0092-8674(92)90189-J",
      "volume": "68",
      "author": "Brown D.A.",
      "year": "1992",
      "journal-title": "Cell."
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "2339",
      "DOI": "10.1073/pnas.94.6.2339",
      "volume": "94",
      "author": "Br\u00fcgger B.",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1083/jcb.151.3.507",
      "volume": "151",
      "author": "Br\u00fcgger B.",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.1083/jcb.126.1.127",
      "volume": "126",
      "author": "Chang W.J.",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "1027",
      "DOI": "10.1083/jcb.133.5.1027",
      "volume": "133",
      "author": "Denker S.P.",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "14",
      "DOI": "10.1016/0962-8924(91)90064-G",
      "volume": "1",
      "author": "Duden R.",
      "year": "1991",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "1597",
      "DOI": "10.1002/j.1460-2075.1993.tb05804.x",
      "volume": "12",
      "author": "Dupree P.",
      "year": "1993",
      "journal-title": "EMBO J."
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "92",
      "DOI": "10.1007/BF02290390",
      "volume": "28",
      "author": "Eckerskorn C.",
      "year": "1989",
      "journal-title": "Chromatographia"
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "1327",
      "DOI": "10.1073/pnas.96.4.1327",
      "volume": "96",
      "author": "Exner T.",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "6365",
      "DOI": "10.1021/bi00076a009",
      "volume": "32",
      "author": "Fiedler K.",
      "year": "1993",
      "journal-title": "Biochemistry"
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "697",
      "DOI": "10.1042/bj3240697",
      "volume": "324",
      "author": "Finbow M.E.",
      "year": "1997",
      "journal-title": "Biochem. J."
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "779",
      "DOI": "10.1146/annurev.cellbio.13.1.779",
      "volume": "13",
      "author": "Forgac M.",
      "year": "1997",
      "journal-title": "Annu. Rev. Cell Dev. Biol."
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "30745",
      "DOI": "10.1016/S0021-9258(18)47340-1",
      "volume": "269",
      "author": "Fra A.M.",
      "year": "1994",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "802",
      "DOI": "10.1038/29570",
      "volume": "394",
      "author": "Friedrichson T.",
      "year": "1998",
      "journal-title": "Nature"
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "229",
      "DOI": "10.1016/S0378-1119(98)00064-X",
      "volume": "210",
      "author": "Galbiati F.",
      "year": "1998",
      "journal-title": "Gene"
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "165",
      "DOI": "10.1083/jcb.152.1.165",
      "volume": "152",
      "author": "Garin J.",
      "year": "2001",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "423",
      "DOI": "10.1038/15658",
      "volume": "1",
      "author": "Girod A.",
      "year": "1999",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "619",
      "DOI": "10.1083/jcb.129.3.619",
      "volume": "129",
      "author": "Gorodinsky A.",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "72",
      "DOI": "10.1016/0003-2697(89)90089-4",
      "volume": "180",
      "author": "Grassel S.",
      "year": "1989",
      "journal-title": "Anal. Biochem."
    },
    {
      "key": "B28",
      "doi-asserted-by": "crossref",
      "first-page": "929",
      "DOI": "10.1083/jcb.141.4.929",
      "volume": "141",
      "author": "Harder T.",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "587",
      "DOI": "10.1242/jcs.113.4.587",
      "volume": "113",
      "author": "Hauri H.P.",
      "year": "2000",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "8375",
      "DOI": "10.1073/pnas.140218797",
      "volume": "97",
      "author": "Heino S.",
      "year": "2000",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "84",
      "DOI": "10.1016/0014-5793(95)00620-O",
      "volume": "369",
      "author": "Helms J.B.",
      "year": "1995",
      "journal-title": "FEBS Lett."
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "15203",
      "DOI": "10.1074/jbc.273.24.15203",
      "volume": "273",
      "author": "Helms J.B.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "87",
      "DOI": "10.1016/S0962-8924(98)01495-0",
      "volume": "9",
      "author": "Jacobson K.",
      "year": "1999",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "617",
      "DOI": "10.1016/S0092-8674(00)80449-3",
      "volume": "91",
      "author": "Jamora C.",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "69",
      "DOI": "10.1083/jcb.142.1.69",
      "volume": "142",
      "author": "Kenworthy A.K.",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.11.5.1645"
    },
    {
      "key": "B37",
      "doi-asserted-by": "crossref",
      "first-page": "1071",
      "DOI": "10.1083/jcb.116.5.1071",
      "volume": "116",
      "author": "Klausner R.D.",
      "year": "1992",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B38",
      "first-page": "187",
      "volume": "5",
      "author": "Kurzchalia T.V.",
      "year": "1995",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B39",
      "doi-asserted-by": "crossref",
      "first-page": "502",
      "DOI": "10.1002/(SICI)1097-4695(199812)37:4<502::AID-NEU2>3.0.CO;2-S",
      "volume": "37",
      "author": "Lang D.M.",
      "year": "1998",
      "journal-title": "J. Neurobiol."
    },
    {
      "key": "B40",
      "doi-asserted-by": "crossref",
      "first-page": "801",
      "DOI": "10.1016/0092-8674(89)90685-5",
      "volume": "56",
      "author": "Lippincott-Schwartz J.",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "B41",
      "doi-asserted-by": "crossref",
      "first-page": "265",
      "DOI": "10.1016/S0021-9258(19)52451-6",
      "volume": "193",
      "author": "Lowry O.H.",
      "year": "1951",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B42",
      "doi-asserted-by": "crossref",
      "first-page": "1443",
      "DOI": "10.1083/jcb.145.7.1443",
      "volume": "145",
      "author": "Luetterforst R.",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B43",
      "doi-asserted-by": "crossref",
      "first-page": "17",
      "DOI": "10.1083/jcb.148.1.17",
      "volume": "148",
      "author": "Machleidt T.",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B44",
      "doi-asserted-by": "crossref",
      "first-page": "6917",
      "DOI": "10.1093/emboj/18.24.6917",
      "volume": "18",
      "author": "Madore N.",
      "year": "1999",
      "journal-title": "EMBO J."
    },
    {
      "key": "B45",
      "doi-asserted-by": "crossref",
      "first-page": "329",
      "DOI": "10.1016/0092-8674(89)90847-7",
      "volume": "58",
      "author": "Malhotra V.",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "B46",
      "doi-asserted-by": "crossref",
      "first-page": "237",
      "DOI": "10.1006/excr.1996.0133",
      "volume": "224",
      "author": "Mineo C.",
      "year": "1996",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "B47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.6.7.911"
    },
    {
      "key": "B48",
      "doi-asserted-by": "crossref",
      "first-page": "25708",
      "DOI": "10.1074/jbc.274.36.25708",
      "volume": "274",
      "author": "Mora R.",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B49",
      "doi-asserted-by": "crossref",
      "first-page": "11",
      "DOI": "10.1016/S0962-8924(97)01197-5",
      "volume": "8",
      "author": "Munro S.",
      "year": "1998",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B50",
      "doi-asserted-by": "crossref",
      "first-page": "5419",
      "DOI": "10.1074/jbc.273.10.5419",
      "volume": "273",
      "author": "Okamoto T.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B51",
      "doi-asserted-by": "crossref",
      "first-page": "25718",
      "DOI": "10.1074/jbc.274.36.25718",
      "volume": "274",
      "author": "Parolini I.",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B52",
      "doi-asserted-by": "crossref",
      "first-page": "581",
      "DOI": "10.1038/35054500",
      "volume": "409",
      "author": "Peters C.",
      "year": "2001",
      "journal-title": "Nature"
    },
    {
      "key": "B53",
      "doi-asserted-by": "crossref",
      "first-page": "997",
      "DOI": "10.1083/jcb.148.5.997",
      "volume": "148",
      "author": "Pralle A.",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B54",
      "doi-asserted-by": "crossref",
      "first-page": "494",
      "DOI": "10.1007/BF02531316",
      "volume": "5",
      "author": "Rouser G.",
      "year": "1970",
      "journal-title": "Lipids"
    },
    {
      "key": "B55",
      "doi-asserted-by": "crossref",
      "first-page": "126",
      "DOI": "10.1016/S0022-2275(20)33347-2",
      "volume": "40",
      "author": "Sandhoff R.",
      "year": "1999",
      "journal-title": "J. Lipid Res."
    },
    {
      "key": "B56",
      "doi-asserted-by": "crossref",
      "first-page": "789",
      "DOI": "10.1083/jcb.122.4.789",
      "volume": "122",
      "author": "Sargiacomo M.",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B57",
      "doi-asserted-by": "crossref",
      "first-page": "5501",
      "DOI": "10.1093/emboj/16.18.5501",
      "volume": "16",
      "author": "Scheiffele P.",
      "year": "1997",
      "journal-title": "EMBO J."
    },
    {
      "key": "B58",
      "doi-asserted-by": "crossref",
      "first-page": "1435",
      "DOI": "10.1126/science.7660128",
      "volume": "269",
      "author": "Schnitzer J.E.",
      "year": "1995",
      "journal-title": "Science."
    },
    {
      "key": "B59",
      "doi-asserted-by": "crossref",
      "first-page": "577",
      "DOI": "10.1242/dev.124.2.577",
      "volume": "124",
      "author": "Schulte T.",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "B60",
      "doi-asserted-by": "crossref",
      "first-page": "1643",
      "DOI": "10.1083/jcb.107.5.1643",
      "volume": "107",
      "author": "Schweizer A.",
      "year": "1988",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B61",
      "doi-asserted-by": "crossref",
      "first-page": "215",
      "DOI": "10.1038/349215a0",
      "volume": "349",
      "author": "Serafini T.",
      "year": "1991",
      "journal-title": "Nature"
    },
    {
      "issue": "3",
      "key": "B62",
      "doi-asserted-by": "crossref",
      "first-page": "627",
      "DOI": "10.1042/bj3430627",
      "volume": "343",
      "author": "Sevlever D.",
      "year": "1999",
      "journal-title": "Biochem. J."
    },
    {
      "key": "B63",
      "doi-asserted-by": "crossref",
      "first-page": "569",
      "DOI": "10.1038/42408",
      "volume": "387",
      "author": "Simons K.",
      "year": "1997",
      "journal-title": "Nature"
    },
    {
      "key": "B64",
      "doi-asserted-by": "crossref",
      "first-page": "6197",
      "DOI": "10.1021/bi00417a001",
      "volume": "27",
      "author": "Simons K.",
      "year": "1988",
      "journal-title": "Biochemistry"
    },
    {
      "key": "B65",
      "doi-asserted-by": "crossref",
      "first-page": "1185",
      "DOI": "10.1083/jcb.127.5.1185",
      "volume": "127",
      "author": "Smart E.J.",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B66",
      "doi-asserted-by": "crossref",
      "first-page": "1239",
      "DOI": "10.1083/jcb.135.5.1239",
      "volume": "135",
      "author": "Sohn K.",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B67",
      "doi-asserted-by": "crossref",
      "first-page": "1113",
      "DOI": "10.1083/jcb.114.6.1113",
      "volume": "114",
      "author": "Stow J.L.",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B68",
      "doi-asserted-by": "crossref",
      "first-page": "425",
      "DOI": "10.1016/S0968-0004(99)01467-X",
      "volume": "24",
      "author": "Tavernarakis N.",
      "year": "1999",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "B69",
      "doi-asserted-by": "crossref",
      "first-page": "837",
      "DOI": "10.1016/0092-8674(90)90097-X",
      "volume": "60",
      "author": "Tooze S.A.",
      "year": "1990",
      "journal-title": "Cell."
    },
    {
      "key": "B70",
      "doi-asserted-by": "crossref",
      "first-page": "661",
      "DOI": "10.1016/0955-0674(93)90137-F",
      "volume": "5",
      "author": "van Meer G.",
      "year": "1993",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B71",
      "doi-asserted-by": "crossref",
      "first-page": "29",
      "DOI": "10.1016/S0962-8924(97)01196-3",
      "volume": "8",
      "author": "van Meer G.",
      "year": "1998",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B72",
      "doi-asserted-by": "crossref",
      "first-page": "798",
      "DOI": "10.1038/29563",
      "volume": "394",
      "author": "Varma R.",
      "year": "1998",
      "journal-title": "Nature"
    },
    {
      "key": "B73",
      "doi-asserted-by": "crossref",
      "first-page": "743",
      "DOI": "10.1083/jcb.147.4.743",
      "volume": "147",
      "author": "White J.",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B74",
      "doi-asserted-by": "crossref",
      "first-page": "233",
      "DOI": "10.1210/endo.134.1.8275939",
      "volume": "134",
      "author": "Wilson B.S.",
      "year": "1994",
      "journal-title": "Endocrinology"
    },
    {
      "key": "B75",
      "doi-asserted-by": "crossref",
      "first-page": "1131",
      "DOI": "10.1083/jcb.149.5.1131",
      "volume": "149",
      "author": "Wilson B.S.",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B76",
      "doi-asserted-by": "crossref",
      "first-page": "25260",
      "DOI": "10.1074/jbc.272.40.25260",
      "volume": "272",
      "author": "Yamaguchi T.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2022,
        2,
        27
      ]
    ],
    "date-time": "2022-02-27T02:45:27Z",
    "timestamp": 1645929927000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.12.6.1819"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "Vivek",
      "family": "Malhotra",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        6
      ]
    ]
  },
  "references-count": 76,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2001,
          6
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.12.6.1819"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.12.6.1819",
  "relation": {},
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        2001,
        6
      ]
    ]
  }
}