DOI: 10.1091/mbc.11.1.325. Identification of Filamin as a Novel Ligand for Caveolin-1: Evidence for the Organization of Caveolin-1–associated Membrane Domains by the Actin Cytoskeleton

Identification of Filamin as a Novel Ligand for Caveolin-1: Evidence for the Organization of Caveolin-1–associated Membrane Domains by the Actin Cytoskeleton

10.1091/mbc.11.1.325

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Reports on the ultrastructure of cells as well as biochemical data have, for several years, been indicating a connection between caveolae and the actin cytoskeleton. Here, using a yeast two-hybrid approach, we have identified the F-actin cross-linking protein filamin as a ligand for the caveolae-associated protein caveolin-1. Binding of caveolin-1 to filamin involved the N-terminal region of caveolin-1 and the C terminus of filamin close to the filamin-dimerization domain. In in vitro binding assays, recombinant caveolin-1 bound to both nonmuscle and muscle filamin, indicating that the interaction might not be cell type specific. With the use of confocal microscopy, colocalization of caveolin-1 and filamin was observed in elongated patches at the plasma membrane. Remarkably, when stress fiber formation was induced with Rho-stimulating Escherichia coli cytotoxic necrotizing factor 1, the caveolin-1–positive structures became coaligned with stress fibers, indicating that there was a physical link connecting them. Immunogold double-labeling electron microscopy confirmed that caveolin-1–labeled racemose caveolae clusters were positive for filamin. The actin network, therefore, seems to be directly involved in the spatial organization of caveolin-1–associated membrane domains.

Bibliography

Stahlhut, M., & van Deurs, B. (2000). Identification of Filamin as a Novel Ligand for Caveolin-1: Evidence for the Organization of Caveolin-1âassociated Membrane Domains by the Actin Cytoskeleton. Molecular Biology of the Cell, 11(1), 325â337.

Authors 2

Martin Stahlhut (first)
Bo van Deurs (additional)

References 56 Referenced 242

10.1016/S0966-842X(97)01067-6 / Trends Microbiol. by Aktories K. (1997)
10.1146/annurev.biochem.67.1.199 / Annu. Rev. Biochem. by Anderson R.G. (1998)
10.1083/jcb.126.1.127 / J. Cell Biol. by Chang W.J. (1994)
10.1074/jbc.272.10.6525 / J. Biol. Chem. by Couet J. (1997)
10.1126/science.1549777 / Science by Cunningham C.C. (1992)
10.1002/j.1460-2075.1993.tb05804.x / EMBO J. by Dupree P. (1993)
10.1074/jbc.272.26.16374 / J. Biol. Chem. by Engelman J.A. (1997)
10.1016/0041-0101(88)90203-6 / Toxicon by Fiorentini C. (1988)
10.1006/abio.1993.1170 / Anal. Biochem. by Frangioni J.V. (1993)
10.1242/jcs.108.1.7 / J. Cell Sci. by Fujimoto T. (1995)
10.1074/jbc.271.44.27237 / J. Biol. Chem. by Garcia-Cardena G. (1996)
{'key': 'B12', 'first-page': '255', 'volume': '5', 'author': 'Gietz R.D.', 'year': '1995', 'journal-title': 'Methods Mol. Cell. Biol.'} / Methods Mol. Cell. Biol. by Gietz R.D. (1995)
10.1016/S0021-9258(19)47038-5 / J. Biol. Chem. by Glenney J.R. (1989)
10.1073/pnas.89.21.10517 / Proc. Natl. Acad. Sci. USA by Glenney J.R. (1992)
10.1074/jbc.273.3.1689 / J. Biol. Chem. by Glogauer M. (1998)
10.1083/jcb.111.3.1089 / J. Cell Biol. by Gorlin J.B. (1990)
10.1242/jcs.108.10.3243 / J. Cell Sci. by Horiguchi Y. (1995)
10.1002/ar.1092200302 / Anat. Rec. by Izumi T. (1988)
10.1073/pnas.92.5.1381 / Proc. Natl. Acad. Sci. USA by Koleske A.J. (1995)
10.1083/jcb.118.5.1003 / J. Cell Biol. by Kurzchalia T.V. (1992)
10.1074/jbc.271.46.29182 / J. Biol. Chem. by Li S. (1996)
10.1074/jbc.270.26.15693 / J. Biol. Chem. by Li S. (1995)
10.1083/jcb.139.7.1719 / J. Cell Biol. by Liu G. (1997)
10.1074/jbc.274.22.15781 / J. Biol. Chem. by Liu J. (1999)
10.1074/jbc.273.36.23304 / J. Biol. Chem. by Loo D.T. (1998)
10.1074/jbc.272.5.2914 / J. Biol. Chem. by Meyer S.C. (1997)
10.1091/mbc.6.7.911
10.1016/S0006-3495(98)77632-5 / Biophys. J. by Mukherjee S. (1998)
10.1074/jbc.274.33.23144 / J. Biol. Chem. by Oh P. (1999)
10.1074/jbc.272.52.33416 / J. Biol. Chem. by Oka N. (1997)
10.1074/jbc.273.10.5419 / J. Biol. Chem. by Okamoto T. (1998)
10.1016/S0955-0674(96)80033-0 / Curr. Opin. Cell Biol. by Parton R.G. (1996)
10.1083/jcb.127.5.1199 / J. Cell Biol. by Parton R.G. (1994)
{'key': 'B34', 'first-page': '500', 'volume': '50', 'author': 'Petersen O.W.', 'year': '1989', 'journal-title': 'Eur. J. Cell Biol.'} / Eur. J. Cell Biol. by Petersen O.W. (1989)
10.1074/jbc.273.11.6104 / J. Biol. Chem. by Pfaff M. (1998)
10.1242/jcs.106.2.565 / J. Cell Sci. by Provance D.W. (1993)
10.1016/0092-8674(92)90163-7 / Cell by Ridley A.J. (1992)
10.1016/S0022-5320(76)80059-7 / J. Ultrastruct Res. by Rohlich P. (1976)
10.1016/0092-8674(92)90143-Z / Cell by Rothberg K.G. (1992)
10.1073/pnas.92.20.9407 / Proc. Natl. Acad. Sci. USA by Sargiacomo M. (1995)
10.1083/jcb.122.4.789 / J. Cell Biol. by Sargiacomo M. (1993)
10.1083/jcb.140.4.795 / J. Cell Biol. by Scheiffele P. (1998)
10.1074/jbc.272.46.29337 / J. Biol. Chem. by Scherer P.E. (1997)
10.1073/pnas.93.1.131 / Proc. Natl. Acad. Sci. USA by Scherer P.E. (1996)
10.1074/jbc.270.27.16395 / J. Biol. Chem. by Scherer P.E. (1995)
10.1073/pnas.92.5.1759 / Proc. Natl. Acad. Sci. USA by Schnitzer J.E. (1995)
10.3181/00379727-196-43185 / Proc. Soc. Exp. Biol. Med. by Schroeder F. (1991)
10.1006/excr.1996.3414 / Exp. Cell Res. by Senda T. (1997)
10.1083/jcb.113.1.123 / J. Cell Biol. by Slot J.W. (1991)
10.1083/jcb.127.5.1185 / J. Cell Biol. by Smart E.J. (1994)
10.1073/pnas.92.22.10104 / Proc. Natl. Acad. Sci. USA by Smart E.J. (1995)
10.1091/mbc.8.4.595
10.1074/jbc.273.28.17531 / J. Biol. Chem. by Takafuta T. (1998)
10.1016/0962-8924(93)90045-3 / Trends Cell Biol. by van Deurs B. (1993)
{'key': 'B55', 'first-page': '270', 'volume': '27', 'author': 'van Deurs B.', 'year': '1982', 'journal-title': 'Eur. J. Cell Biol.'} / Eur. J. Cell Biol. by van Deurs B. (1982)
10.1242/jcs.111.6.825 / J. Cell Sci. by Vogel U. (1998)

Dates

Type	When
Created	12 years, 1 month ago (July 2, 2013, 7:39 p.m.)
Deposited	3 years, 5 months ago (Feb. 26, 2022, 9:39 p.m.)
Indexed	1 month, 3 weeks ago (July 2, 2025, 3:10 p.m.)
Issued	25 years, 7 months ago (Jan. 1, 2000)
Published	25 years, 7 months ago (Jan. 1, 2000)
Published Print	25 years, 7 months ago (Jan. 1, 2000)

Funders 0

None

BibTeX

@article{Stahlhut_2000, title={Identification of Filamin as a Novel Ligand for Caveolin-1: Evidence for the Organization of Caveolin-1–associated Membrane Domains by the Actin Cytoskeleton}, volume={11}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.11.1.325}, DOI={10.1091/mbc.11.1.325}, number={1}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Stahlhut, Martin and van Deurs, Bo}, editor={Guidotti, Guido}, year={2000}, month=jan, pages={325–337} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        2
      ]
    ],
    "date-time": "2025-07-02T19:10:07Z",
    "timestamp": 1751483407885
  },
  "reference-count": 56,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "1",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Reports on the ultrastructure of cells as well as biochemical data have, for several years, been indicating a connection between caveolae and the actin cytoskeleton. Here, using a yeast two-hybrid approach, we have identified the F-actin cross-linking protein filamin as a ligand for the caveolae-associated protein caveolin-1. Binding of caveolin-1 to filamin involved the N-terminal region of caveolin-1 and the C terminus of filamin close to the filamin-dimerization domain. In in vitro binding assays, recombinant caveolin-1 bound to both nonmuscle and muscle filamin, indicating that the interaction might not be cell type specific. With the use of confocal microscopy, colocalization of caveolin-1 and filamin was observed in elongated patches at the plasma membrane. Remarkably, when stress fiber formation was induced with Rho-stimulating Escherichia coli cytotoxic necrotizing factor 1, the caveolin-1\u2013positive structures became coaligned with stress fibers, indicating that there was a physical link connecting them. Immunogold double-labeling electron microscopy confirmed that caveolin-1\u2013labeled racemose caveolae clusters were positive for filamin. The actin network, therefore, seems to be directly involved in the spatial organization of caveolin-1\u2013associated membrane domains.</jats:p>",
  "DOI": "10.1091/mbc.11.1.325",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2013,
        7,
        2
      ]
    ],
    "date-time": "2013-07-02T23:39:26Z",
    "timestamp": 1372808366000
  },
  "page": "325-337",
  "source": "Crossref",
  "is-referenced-by-count": 242,
  "title": "Identification of Filamin as a Novel Ligand for Caveolin-1: Evidence for the Organization of Caveolin-1\u2013associated Membrane Domains by the Actin Cytoskeleton",
  "prefix": "10.1091",
  "volume": "11",
  "author": [
    {
      "given": "Martin",
      "family": "Stahlhut",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Structural Cell Biology Unit, Department of Medical Anatomy, The Panum Institute, University of Copenhagen, DK-2200 Copenhagen N, Denmark"
        }
      ]
    },
    {
      "given": "Bo",
      "family": "van Deurs",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Structural Cell Biology Unit, Department of Medical Anatomy, The Panum Institute, University of Copenhagen, DK-2200 Copenhagen N, Denmark"
        }
      ]
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "B1",
      "doi-asserted-by": "crossref",
      "first-page": "282",
      "DOI": "10.1016/S0966-842X(97)01067-6",
      "volume": "5",
      "author": "Aktories K.",
      "year": "1997",
      "journal-title": "Trends Microbiol."
    },
    {
      "key": "B2",
      "doi-asserted-by": "crossref",
      "first-page": "199",
      "DOI": "10.1146/annurev.biochem.67.1.199",
      "volume": "67",
      "author": "Anderson R.G.",
      "year": "1998",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "B3",
      "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": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "6525",
      "DOI": "10.1074/jbc.272.10.6525",
      "volume": "272",
      "author": "Couet J.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "325",
      "DOI": "10.1126/science.1549777",
      "volume": "255",
      "author": "Cunningham C.C.",
      "year": "1992",
      "journal-title": "Science"
    },
    {
      "key": "B6",
      "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": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "16374",
      "DOI": "10.1074/jbc.272.26.16374",
      "volume": "272",
      "author": "Engelman J.A.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "1047",
      "DOI": "10.1016/0041-0101(88)90203-6",
      "volume": "26",
      "author": "Fiorentini C.",
      "year": "1988",
      "journal-title": "Toxicon"
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "179",
      "DOI": "10.1006/abio.1993.1170",
      "volume": "210",
      "author": "Frangioni J.V.",
      "year": "1993",
      "journal-title": "Anal. Biochem."
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "7",
      "DOI": "10.1242/jcs.108.1.7",
      "volume": "108",
      "author": "Fujimoto T.",
      "year": "1995",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "27237",
      "DOI": "10.1074/jbc.271.44.27237",
      "volume": "271",
      "author": "Garcia-Cardena G.",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B12",
      "first-page": "255",
      "volume": "5",
      "author": "Gietz R.D.",
      "year": "1995",
      "journal-title": "Methods Mol. Cell. Biol."
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "20163",
      "DOI": "10.1016/S0021-9258(19)47038-5",
      "volume": "264",
      "author": "Glenney J.R.",
      "year": "1989",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "10517",
      "DOI": "10.1073/pnas.89.21.10517",
      "volume": "89",
      "author": "Glenney J.R.",
      "year": "1992",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "1689",
      "DOI": "10.1074/jbc.273.3.1689",
      "volume": "273",
      "author": "Glogauer M.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "1089",
      "DOI": "10.1083/jcb.111.3.1089",
      "volume": "111",
      "author": "Gorlin J.B.",
      "year": "1990",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "3243",
      "DOI": "10.1242/jcs.108.10.3243",
      "volume": "108",
      "author": "Horiguchi Y.",
      "year": "1995",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "225",
      "DOI": "10.1002/ar.1092200302",
      "volume": "220",
      "author": "Izumi T.",
      "year": "1988",
      "journal-title": "Anat. Rec."
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "1381",
      "DOI": "10.1073/pnas.92.5.1381",
      "volume": "92",
      "author": "Koleske A.J.",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "1003",
      "DOI": "10.1083/jcb.118.5.1003",
      "volume": "118",
      "author": "Kurzchalia T.V.",
      "year": "1992",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "29182",
      "DOI": "10.1074/jbc.271.46.29182",
      "volume": "271",
      "author": "Li S.",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "15693",
      "DOI": "10.1074/jbc.270.26.15693",
      "volume": "270",
      "author": "Li S.",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "1719",
      "DOI": "10.1083/jcb.139.7.1719",
      "volume": "139",
      "author": "Liu G.",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "15781",
      "DOI": "10.1074/jbc.274.22.15781",
      "volume": "274",
      "author": "Liu J.",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "23304",
      "DOI": "10.1074/jbc.273.36.23304",
      "volume": "273",
      "author": "Loo D.T.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "2914",
      "DOI": "10.1074/jbc.272.5.2914",
      "volume": "272",
      "author": "Meyer S.C.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.6.7.911"
    },
    {
      "key": "B28",
      "doi-asserted-by": "crossref",
      "first-page": "1915",
      "DOI": "10.1016/S0006-3495(98)77632-5",
      "volume": "75",
      "author": "Mukherjee S.",
      "year": "1998",
      "journal-title": "Biophys. J."
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "23144",
      "DOI": "10.1074/jbc.274.33.23144",
      "volume": "274",
      "author": "Oh P.",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "33416",
      "DOI": "10.1074/jbc.272.52.33416",
      "volume": "272",
      "author": "Oka N.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B31",
      "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": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "542",
      "DOI": "10.1016/S0955-0674(96)80033-0",
      "volume": "8",
      "author": "Parton R.G.",
      "year": "1996",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "1199",
      "DOI": "10.1083/jcb.127.5.1199",
      "volume": "127",
      "author": "Parton R.G.",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B34",
      "first-page": "500",
      "volume": "50",
      "author": "Petersen O.W.",
      "year": "1989",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "6104",
      "DOI": "10.1074/jbc.273.11.6104",
      "volume": "273",
      "author": "Pfaff M.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "565",
      "DOI": "10.1242/jcs.106.2.565",
      "volume": "106",
      "author": "Provance D.W.",
      "year": "1993",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B37",
      "doi-asserted-by": "crossref",
      "first-page": "389",
      "DOI": "10.1016/0092-8674(92)90163-7",
      "volume": "70",
      "author": "Ridley A.J.",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "B38",
      "doi-asserted-by": "crossref",
      "first-page": "94",
      "DOI": "10.1016/S0022-5320(76)80059-7",
      "volume": "57",
      "author": "Rohlich P.",
      "year": "1976",
      "journal-title": "J. Ultrastruct Res."
    },
    {
      "key": "B39",
      "doi-asserted-by": "crossref",
      "first-page": "673",
      "DOI": "10.1016/0092-8674(92)90143-Z",
      "volume": "68",
      "author": "Rothberg K.G.",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "B40",
      "doi-asserted-by": "crossref",
      "first-page": "9407",
      "DOI": "10.1073/pnas.92.20.9407",
      "volume": "92",
      "author": "Sargiacomo M.",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B41",
      "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": "B42",
      "doi-asserted-by": "crossref",
      "first-page": "795",
      "DOI": "10.1083/jcb.140.4.795",
      "volume": "140",
      "author": "Scheiffele P.",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B43",
      "doi-asserted-by": "crossref",
      "first-page": "29337",
      "DOI": "10.1074/jbc.272.46.29337",
      "volume": "272",
      "author": "Scherer P.E.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B44",
      "doi-asserted-by": "crossref",
      "first-page": "131",
      "DOI": "10.1073/pnas.93.1.131",
      "volume": "93",
      "author": "Scherer P.E.",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B45",
      "doi-asserted-by": "crossref",
      "first-page": "16395",
      "DOI": "10.1074/jbc.270.27.16395",
      "volume": "270",
      "author": "Scherer P.E.",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B46",
      "doi-asserted-by": "crossref",
      "first-page": "1759",
      "DOI": "10.1073/pnas.92.5.1759",
      "volume": "92",
      "author": "Schnitzer J.E.",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B47",
      "doi-asserted-by": "crossref",
      "first-page": "235",
      "DOI": "10.3181/00379727-196-43185",
      "volume": "196",
      "author": "Schroeder F.",
      "year": "1991",
      "journal-title": "Proc. Soc. Exp. Biol. Med."
    },
    {
      "key": "B48",
      "doi-asserted-by": "crossref",
      "first-page": "163",
      "DOI": "10.1006/excr.1996.3414",
      "volume": "230",
      "author": "Senda T.",
      "year": "1997",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "B49",
      "doi-asserted-by": "crossref",
      "first-page": "123",
      "DOI": "10.1083/jcb.113.1.123",
      "volume": "113",
      "author": "Slot J.W.",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B50",
      "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": "B51",
      "doi-asserted-by": "crossref",
      "first-page": "10104",
      "DOI": "10.1073/pnas.92.22.10104",
      "volume": "92",
      "author": "Smart E.J.",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.8.4.595"
    },
    {
      "key": "B53",
      "doi-asserted-by": "crossref",
      "first-page": "17531",
      "DOI": "10.1074/jbc.273.28.17531",
      "volume": "273",
      "author": "Takafuta T.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B54",
      "doi-asserted-by": "crossref",
      "first-page": "249",
      "DOI": "10.1016/0962-8924(93)90045-3",
      "volume": "3",
      "author": "van Deurs B.",
      "year": "1993",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B55",
      "first-page": "270",
      "volume": "27",
      "author": "van Deurs B.",
      "year": "1982",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "B56",
      "doi-asserted-by": "crossref",
      "first-page": "825",
      "DOI": "10.1242/jcs.111.6.825",
      "volume": "111",
      "author": "Vogel U.",
      "year": "1998",
      "journal-title": "J. Cell Sci."
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2022,
        2,
        27
      ]
    ],
    "date-time": "2022-02-27T02:39:54Z",
    "timestamp": 1645929594000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.11.1.325"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "Guido",
      "family": "Guidotti",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        1
      ]
    ]
  },
  "references-count": 56,
  "journal-issue": {
    "issue": "1",
    "published-print": {
      "date-parts": [
        [
          2000,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.11.1.325"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.11.1.325",
  "relation": {},
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        2000,
        1
      ]
    ]
  }
}