DOI: 10.1242/jcs.1993.supplement_17.2. Polarity signals in epithelial cells

10.1242/jcs.1993.supplement_17.2

Crossref journal-article

The Company of Biologists

Journal of Cell Science (237)

Abstract

ABSTRACT In simple epithelia, specialized vectorial functions such as transport and secretion are made possible by the segregation of proteins and lipids into opposite surface domains. This polarized distribution results from selective delivery to and retention at the appropriate domain. In the case of direct delivery, the sorting site for apical and basolateral proteins is the tram-Golgi network (TGN) where they are incorporated into distinct apical and basolateral vesicles that are targeted to the respective surfaces. The machinery that controls this simple process is in fact rather complicated. It involves many different steps from the recognition event (between ‘sorting signal(s)’ and ‘sorting receptor(s)’) to the formation of the vesicles, their budding, and the docking to the specialized plasma membrane domain. Here we summarize the latest developments in the sorting of apical and basolateral proteins, focusing in particular on the signals that are involved in this process and the current hypotheses about the mechanisms responsible for it, in both epithelia and in non-polarized cells.

Bibliography

Rodriguez-Boulan, E., & Zurzolot, C. (1993). Polarity signals in epithelial cells. Journal of Cell Science, 1993(Supplement_17), 9â12.

Authors 2

Enrique Rodriguez-Boulan (first)
Chiara Zurzolot (additional)

References 43 Referenced 32

10.1042/bj2710193 / Biochem. J / Priority targeting of GPI-anchored proteins to the bile-conalicular (apical) plasma membrane of hepatocytes. by Ali (1990)
10.1016/S0021-9258(19)81619-8 / Biol. Chem / COOH-terminal requirements for the correct processing of a phosphatidyl-inositol-glycan anchored membrane protein. J. by Berger (1988)
10.1083/jcb.114.3.413 / J. CellBiol / A single amino acid change in the cytoplasmic domain alters the polarized delivery of Influenza Viral Hemagglutin. by Brewer (1991)
10.1016/0962-8924(92)90183-N / Trends CellBiol / Interactions between GPI-anchored proteins and membrane lipids. by Brown (1992)
10.1126/science.2571189 / Science / Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. by Brown (1989)
10.1083/jcb.108.4.1387 / J. Cell Biol / Analysis of the signal for attachment of a glycosylphospholipid membrane anchor. by Caras (1989)
10.1016/0092-8674(91)90139-P / Cell / An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. by Casanova (1991)
10.1007/BF01871169 / J. Membr. Biol / Occluding junctions in a cultured transporting epithelium: Structural and functional heterogeneity. by Cerejido (1980)
{'key': '2024071020052973800_JOCES_1993_S17_0009C9', 'first-page': '1', 'article-title': 'Glycolipid anchoring of plasma membrane proteins. Ann".', 'volume': '6', 'author': 'Cross', 'year': '1990', 'journal-title': 'Rev. CellBiol'} / Rev. CellBiol / Glycolipid anchoring of plasma membrane proteins. Ann". by Cross (1990)
10.1002/j.1460-2075.1993.tb05816.x / EMBO J / The internalization signal and the phosphorylation site of transferrin receptor are distinct from the main basolateral sorting information. by Dagermont (1993)
10.1016/0014-4827(88)90190-5 / Exp. Cell Res / Isolation of a fraction enriched in the trans-Golgi network from baby hamster kidney cells. by de Curtis (1988)
10.1016/S0021-9258(19)37000-0 / J. Biol. Chem / Glycan components in the glycoinositol phospholipid anchor of human erythrocyte acetylcholinesterase. by Deeg (1992)
10.1146/annurev.bi.57.070188.001441 / Annu. Rev. Biochem / Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. by Ferguson (1988)
10.1016/S0021-9258(19)49819-0 / J. Biol. Chem / Phosphatidylinositol glycan (PI-G) anchored membrane proteins. by Gerber (1992)
10.1016/S0092-8674(88)80026-6 / Cell / The mannose 6-phosphate receptor and the biogenesis of lysosomes. by Griffiths (1988)
10.1126/science.2945253 / Science / The trans Golgi network: sorting at the exit site of the Golgi complex. by Griffiths (1986)
10.1016/0955-0674(90)90087-U / Curr. Opin. Cell Biol / Generation and maintenance of epithelial cell polarity. by Gumbiner (1990)
10.1083/jcb.120.2.353 / CellBiol / Correctly sorted molecules of a GPI-anchored protein are clustered and immobile when they arrive at the apical surface of MDCK cells. J. by Hannan (1993)
10.1016/0014-4827(85)90278-2 / Exp. Cell Res / Association of specific cellsurface glycoproteins with a Triton X-I00 resistant complex of plasma membrane proteins isolated from T-lymphoma cells (P1798). by Hoessli (1985)
10.1042/bj2500865 / Biochem. J / Ectoenzymes of the kidney microvillar membrane. by Hooper (1988)
10.1016/0092-8674(91)90437-4 / Cell / Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. by Hunziker (1991)
10.1083/jcb.118.5.1003 / J. Cell Biol / VIP21, a 21 kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles by Kurzchalia (1992)
10.1083/jcb.115.3.607 / J. CellBiol / An internal deletion in the cytoplasmic tail reverses the apical localization of human NGF receptor in transfected MDCK cells. by Le Bivic (1991)
10.1083/jcb.109.5.2145 / J. Cell Biol / A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. by Lisanti (1989)
10.1073/pnas.85.24.9557 / Proc. Nat. Acad. Sci. USA / Polarized apical distribution of glycosyl phosphatidylinositol anchored proteins in a renal epithelial line. by Lisanti (1988)
10.1007/BF01872889 / J. Membr. Biol / Preferred apical distribution of glycosyl-phosphatidylinositol (GPI) anchored proteins: a highly conserved feature of the polarized epithelial cell phenotype. by Lisanti (1990)
10.1126/science.3276003 / Science / Structural and fuctional roles of glycosyl-phosphatidylinositol in membranes. by Low (1988)
10.1016/0092-8674(92)90551-M / Cell / Basolateral sorting of LDL receptor in MDCK cells: The cytoplasmic domain contains two Tyrosine-dependent targeting determinants. by Matter (1992)
{'key': '2024071020052973800_JOCES_1993_S17_0009C29', 'first-page': '375', 'article-title': 'Cytoskeleton functions in membrane traffic in polarized epithelial cells.', 'volume': '2', 'author': 'Nelson', 'year': '1991', 'journal-title': 'Semin. Cell Biol'} / Semin. Cell Biol / Cytoskeleton functions in membrane traffic in polarized epithelial cells. by Nelson (1991)
{'key': '2024071020052973800_JOCES_1993_S17_0009C30', 'first-page': '151', 'article-title': 'Clathrin, adaptors and sorting. Ann".', 'volume': '6', 'author': 'Pearse', 'year': '1990', 'journal-title': 'Rev. CellBiol'} / Rev. CellBiol / Clathrin, adaptors and sorting. Ann". by Pearse (1990)
10.1038/353076a0 / Nature / Transmembrane and GPI anchored forms of NCAM are targeted to opposite domains of a polarized epithelial cell. by Powell (1991)
10.1002/j.1460-2075.1993.tb05866.x / EMBO J / The cytoplasmic tail of lysosomal acid phosphatase contains overlapping but distinct signals for basolateral sorting and rapid internalization in polarized MDCK cells. by Prill (1993)
10.1016/0962-8924(92)90118-7 / Trends Cell Biol / Adaptins. by Robinson (1992)
10.1146/annurev.cb.08.110192.002143 / Annu. Rev. Cell Biol / Polarity of epithelial and neuronal cells. by Rodriguez-Boulan (1992)
10.1016/0092-8674(92)90143-Z / Cell / Caveolin, a protein component of caveolae membrane coats. by Rothberg (1992)
10.1016/0092-8674(90)90357-K / Cell / Polarized sorting in epithelia. by Simons (1990)
10.1016/0092-8674(90)90097-X / Cell / Cell-free protein sorting to the regulated and constitutive secretory pathways. by Tooze (1990)
10.1016/0962-8924(92)90182-M / Trends Cell Biol / Sphingolipid trafficking-sorted out?. by van Meer (1992)
10.1002/jcb.240360106 / J. Cell. Biochem / Lipid polarity and sorting in epithelial cells. by van Meer (1988)
10.1083/jcb.111.3.987 / J. Cell Biol / Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of MDCK cells. by Wandinger-Ness (1990)
10.1083/jcb.117.1.39 / J. Cell Biol / Cytoplasmic sequence required for basolateral targeting of LDL receptor in livers of transgenic mice. by Yokode (1992)
10.1083/jcb.121.5.1031 / CellBiol / Glycosylphosphatidilinositol-anchored proteins are preferentially targeted to the basolateral surface in Fischer Rat Thyroid epithelial cells. J. by Zurzolo (1993)
{'key': '2024071020052973800_JOCES_1993_S17_0009C43', 'article-title': 'VIP21/caveolin, glysphingolipid clusters, and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells.', 'volume': '13', 'author': 'Zurzolo', 'year': '1993', 'journal-title': 'EMBO J'} / EMBO J / VIP21/caveolin, glysphingolipid clusters, and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. by Zurzolo (1993)

Dates

Type	When
Created	12 years, 3 months ago (May 23, 2013, 8:48 a.m.)
Deposited	1 year, 1 month ago (July 10, 2024, 4:05 p.m.)
Indexed	1 year, 1 month ago (July 10, 2024, 8:02 p.m.)
Issued	31 years, 8 months ago (Dec. 1, 1993)
Published	31 years, 8 months ago (Dec. 1, 1993)
Published Online	31 years, 8 months ago (Dec. 1, 1993)
Published Print	31 years, 8 months ago (Dec. 1, 1993)

Funders 0

None

BibTeX

@article{Rodriguez_Boulan_1993, title={Polarity signals in epithelial cells}, volume={1993}, ISSN={1477-9137}, url={http://dx.doi.org/10.1242/jcs.1993.supplement_17.2}, DOI={10.1242/jcs.1993.supplement_17.2}, number={Supplement_17}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Rodriguez-Boulan, Enrique and Zurzolot, Chiara}, year={1993}, month=dec, pages={9–12} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        7,
        11
      ]
    ],
    "date-time": "2024-07-11T00:02:23Z",
    "timestamp": 1720656143185
  },
  "reference-count": 43,
  "publisher": "The Company of Biologists",
  "issue": "Supplement_17",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1993,
            12,
            1
          ]
        ],
        "date-time": "1993-12-01T00:00:00Z",
        "timestamp": 754704000000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://www.biologists.com/user-licence-1-1/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1993,
        12,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>In simple epithelia, specialized vectorial functions such as transport and secretion are made possible by the segregation of proteins and lipids into opposite surface domains. This polarized distribution results from selective delivery to and retention at the appropriate domain. In the case of direct delivery, the sorting site for apical and basolateral proteins is the tram-Golgi network (TGN) where they are incorporated into distinct apical and basolateral vesicles that are targeted to the respective surfaces. The machinery that controls this simple process is in fact rather complicated. It involves many different steps from the recognition event (between \u2018sorting signal(s)\u2019 and \u2018sorting receptor(s)\u2019) to the formation of the vesicles, their budding, and the docking to the specialized plasma membrane domain. Here we summarize the latest developments in the sorting of apical and basolateral proteins, focusing in particular on the signals that are involved in this process and the current hypotheses about the mechanisms responsible for it, in both epithelia and in non-polarized cells.</jats:p>",
  "DOI": "10.1242/jcs.1993.supplement_17.2",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2013,
        5,
        23
      ]
    ],
    "date-time": "2013-05-23T12:48:12Z",
    "timestamp": 1369313292000
  },
  "page": "9-12",
  "source": "Crossref",
  "is-referenced-by-count": 32,
  "title": "Polarity signals in epithelial cells",
  "prefix": "10.1242",
  "volume": "1993",
  "author": [
    {
      "given": "Enrique",
      "family": "Rodriguez-Boulan",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Chiara",
      "family": "Zurzolot",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Cell Biology, Cornell University Medical College, 1300 York Ave, New York, NY 10021, USA"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1993,
        12,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C1",
      "doi-asserted-by": "publisher",
      "first-page": "193",
      "DOI": "10.1042/bj2710193",
      "article-title": "Priority targeting of GPI-anchored proteins to the bile-conalicular (apical) plasma membrane of hepatocytes.",
      "volume": "271",
      "author": "Ali",
      "year": "1990",
      "journal-title": "Biochem. J"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C2",
      "doi-asserted-by": "publisher",
      "first-page": "10016",
      "DOI": "10.1016/S0021-9258(19)81619-8",
      "article-title": "COOH-terminal requirements for the correct processing of a phosphatidyl-inositol-glycan anchored membrane protein. J.",
      "volume": "263",
      "author": "Berger",
      "year": "1988",
      "journal-title": "Biol. Chem"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C3",
      "doi-asserted-by": "publisher",
      "first-page": "413",
      "DOI": "10.1083/jcb.114.3.413",
      "article-title": "A single amino acid change in the cytoplasmic domain alters the polarized delivery of Influenza Viral Hemagglutin.",
      "volume": "114",
      "author": "Brewer",
      "year": "1991",
      "journal-title": "J. CellBiol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C4",
      "doi-asserted-by": "publisher",
      "first-page": "338",
      "DOI": "10.1016/0962-8924(92)90183-N",
      "article-title": "Interactions between GPI-anchored proteins and membrane lipids.",
      "volume": "2",
      "author": "Brown",
      "year": "1992",
      "journal-title": "Trends CellBiol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C5",
      "doi-asserted-by": "publisher",
      "first-page": "1499",
      "DOI": "10.1126/science.2571189",
      "article-title": "Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells.",
      "volume": "245",
      "author": "Brown",
      "year": "1989",
      "journal-title": "Science"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C6",
      "doi-asserted-by": "publisher",
      "first-page": "1387",
      "DOI": "10.1083/jcb.108.4.1387",
      "article-title": "Analysis of the signal for attachment of a glycosylphospholipid membrane anchor.",
      "volume": "108",
      "author": "Caras",
      "year": "1989",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C7",
      "doi-asserted-by": "publisher",
      "first-page": "65",
      "DOI": "10.1016/0092-8674(91)90139-P",
      "article-title": "An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor.",
      "volume": "66",
      "author": "Casanova",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C8",
      "doi-asserted-by": "publisher",
      "first-page": "19",
      "DOI": "10.1007/BF01871169",
      "article-title": "Occluding junctions in a cultured transporting epithelium: Structural and functional heterogeneity.",
      "volume": "53",
      "author": "Cerejido",
      "year": "1980",
      "journal-title": "J. Membr. Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C9",
      "first-page": "1",
      "article-title": "Glycolipid anchoring of plasma membrane proteins. Ann\".",
      "volume": "6",
      "author": "Cross",
      "year": "1990",
      "journal-title": "Rev. CellBiol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C10",
      "doi-asserted-by": "publisher",
      "first-page": "1713",
      "DOI": "10.1002/j.1460-2075.1993.tb05816.x",
      "article-title": "The internalization signal and the phosphorylation site of transferrin receptor are distinct from the main basolateral sorting information.",
      "volume": "12",
      "author": "Dagermont",
      "year": "1993",
      "journal-title": "EMBO J"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C11",
      "doi-asserted-by": "publisher",
      "first-page": "248",
      "DOI": "10.1016/0014-4827(88)90190-5",
      "article-title": "Isolation of a fraction enriched in the trans-Golgi network from baby hamster kidney cells.",
      "volume": "175",
      "author": "de Curtis",
      "year": "1988",
      "journal-title": "Exp. Cell Res"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C12",
      "doi-asserted-by": "publisher",
      "first-page": "18573",
      "DOI": "10.1016/S0021-9258(19)37000-0",
      "article-title": "Glycan components in the glycoinositol phospholipid anchor of human erythrocyte acetylcholinesterase.",
      "volume": "267",
      "author": "Deeg",
      "year": "1992",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C13",
      "doi-asserted-by": "publisher",
      "first-page": "285",
      "DOI": "10.1146/annurev.bi.57.070188.001441",
      "article-title": "Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures.",
      "volume": "57",
      "author": "Ferguson",
      "year": "1988",
      "journal-title": "Annu. Rev. Biochem"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C14",
      "doi-asserted-by": "publisher",
      "first-page": "12168",
      "DOI": "10.1016/S0021-9258(19)49819-0",
      "article-title": "Phosphatidylinositol glycan (PI-G) anchored membrane proteins.",
      "volume": "267",
      "author": "Gerber",
      "year": "1992",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C15",
      "doi-asserted-by": "publisher",
      "first-page": "329",
      "DOI": "10.1016/S0092-8674(88)80026-6",
      "article-title": "The mannose 6-phosphate receptor and the biogenesis of lysosomes.",
      "volume": "52",
      "author": "Griffiths",
      "year": "1988",
      "journal-title": "Cell"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C16",
      "doi-asserted-by": "publisher",
      "first-page": "438",
      "DOI": "10.1126/science.2945253",
      "article-title": "The trans Golgi network: sorting at the exit site of the Golgi complex.",
      "volume": "234",
      "author": "Griffiths",
      "year": "1986",
      "journal-title": "Science"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C17",
      "doi-asserted-by": "publisher",
      "first-page": "881",
      "DOI": "10.1016/0955-0674(90)90087-U",
      "article-title": "Generation and maintenance of epithelial cell polarity.",
      "volume": "2",
      "author": "Gumbiner",
      "year": "1990",
      "journal-title": "Curr. Opin. Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C18",
      "doi-asserted-by": "publisher",
      "first-page": "353",
      "DOI": "10.1083/jcb.120.2.353",
      "article-title": "Correctly sorted molecules of a GPI-anchored protein are clustered and immobile when they arrive at the apical surface of MDCK cells. J.",
      "volume": "120",
      "author": "Hannan",
      "year": "1993",
      "journal-title": "CellBiol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C19",
      "doi-asserted-by": "publisher",
      "first-page": "239",
      "DOI": "10.1016/0014-4827(85)90278-2",
      "article-title": "Association of specific cellsurface glycoproteins with a Triton X-I00 resistant complex of plasma membrane proteins isolated from T-lymphoma cells (P1798).",
      "volume": "156",
      "author": "Hoessli",
      "year": "1985",
      "journal-title": "Exp. Cell Res"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C20",
      "doi-asserted-by": "publisher",
      "first-page": "865",
      "DOI": "10.1042/bj2500865",
      "article-title": "Ectoenzymes of the kidney microvillar membrane.",
      "volume": "250",
      "author": "Hooper",
      "year": "1988",
      "journal-title": "Biochem. J"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C21",
      "doi-asserted-by": "publisher",
      "first-page": "907",
      "DOI": "10.1016/0092-8674(91)90437-4",
      "article-title": "Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant.",
      "volume": "66",
      "author": "Hunziker",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C22",
      "doi-asserted-by": "publisher",
      "first-page": "1003",
      "DOI": "10.1083/jcb.118.5.1003",
      "article-title": "VIP21, a 21 kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles",
      "volume": "118",
      "author": "Kurzchalia",
      "year": "1992",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C23",
      "doi-asserted-by": "publisher",
      "first-page": "607",
      "DOI": "10.1083/jcb.115.3.607",
      "article-title": "An internal deletion in the cytoplasmic tail reverses the apical localization of human NGF receptor in transfected MDCK cells.",
      "volume": "115",
      "author": "Le Bivic",
      "year": "1991",
      "journal-title": "J. CellBiol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C24",
      "doi-asserted-by": "publisher",
      "first-page": "2145",
      "DOI": "10.1083/jcb.109.5.2145",
      "article-title": "A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells.",
      "volume": "109",
      "author": "Lisanti",
      "year": "1989",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C25",
      "doi-asserted-by": "publisher",
      "first-page": "9557",
      "DOI": "10.1073/pnas.85.24.9557",
      "article-title": "Polarized apical distribution of glycosyl phosphatidylinositol anchored proteins in a renal epithelial line.",
      "volume": "85",
      "author": "Lisanti",
      "year": "1988",
      "journal-title": "Proc. Nat. Acad. Sci. USA"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C26",
      "doi-asserted-by": "publisher",
      "first-page": "155",
      "DOI": "10.1007/BF01872889",
      "article-title": "Preferred apical distribution of glycosyl-phosphatidylinositol (GPI) anchored proteins: a highly conserved feature of the polarized epithelial cell phenotype.",
      "volume": "113",
      "author": "Lisanti",
      "year": "1990",
      "journal-title": "J. Membr. Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C27",
      "doi-asserted-by": "publisher",
      "first-page": "268",
      "DOI": "10.1126/science.3276003",
      "article-title": "Structural and fuctional roles of glycosyl-phosphatidylinositol in membranes.",
      "volume": "239",
      "author": "Low",
      "year": "1988",
      "journal-title": "Science"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C28",
      "doi-asserted-by": "publisher",
      "first-page": "741",
      "DOI": "10.1016/0092-8674(92)90551-M",
      "article-title": "Basolateral sorting of LDL receptor in MDCK cells: The cytoplasmic domain contains two Tyrosine-dependent targeting determinants.",
      "volume": "71",
      "author": "Matter",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C29",
      "first-page": "375",
      "article-title": "Cytoskeleton functions in membrane traffic in polarized epithelial cells.",
      "volume": "2",
      "author": "Nelson",
      "year": "1991",
      "journal-title": "Semin. Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C30",
      "first-page": "151",
      "article-title": "Clathrin, adaptors and sorting. Ann\".",
      "volume": "6",
      "author": "Pearse",
      "year": "1990",
      "journal-title": "Rev. CellBiol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C31",
      "doi-asserted-by": "publisher",
      "first-page": "76",
      "DOI": "10.1038/353076a0",
      "article-title": "Transmembrane and GPI anchored forms of NCAM are targeted to opposite domains of a polarized epithelial cell.",
      "volume": "353",
      "author": "Powell",
      "year": "1991",
      "journal-title": "Nature"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C32",
      "doi-asserted-by": "publisher",
      "first-page": "2181",
      "DOI": "10.1002/j.1460-2075.1993.tb05866.x",
      "article-title": "The cytoplasmic tail of lysosomal acid phosphatase contains overlapping but distinct signals for basolateral sorting and rapid internalization in polarized MDCK cells.",
      "volume": "12",
      "author": "Prill",
      "year": "1993",
      "journal-title": "EMBO J"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C33",
      "doi-asserted-by": "publisher",
      "first-page": "293",
      "DOI": "10.1016/0962-8924(92)90118-7",
      "article-title": "Adaptins.",
      "volume": "2",
      "author": "Robinson",
      "year": "1992",
      "journal-title": "Trends Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C34",
      "doi-asserted-by": "publisher",
      "first-page": "395",
      "DOI": "10.1146/annurev.cb.08.110192.002143",
      "article-title": "Polarity of epithelial and neuronal cells.",
      "volume": "8",
      "author": "Rodriguez-Boulan",
      "year": "1992",
      "journal-title": "Annu. Rev. Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C35",
      "doi-asserted-by": "publisher",
      "first-page": "673",
      "DOI": "10.1016/0092-8674(92)90143-Z",
      "article-title": "Caveolin, a protein component of caveolae membrane coats.",
      "volume": "68",
      "author": "Rothberg",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C36",
      "doi-asserted-by": "publisher",
      "first-page": "207",
      "DOI": "10.1016/0092-8674(90)90357-K",
      "article-title": "Polarized sorting in epithelia.",
      "volume": "62",
      "author": "Simons",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C37",
      "doi-asserted-by": "publisher",
      "first-page": "837847",
      "DOI": "10.1016/0092-8674(90)90097-X",
      "article-title": "Cell-free protein sorting to the regulated and constitutive secretory pathways.",
      "volume": "60",
      "author": "Tooze",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C38",
      "doi-asserted-by": "publisher",
      "first-page": "332",
      "DOI": "10.1016/0962-8924(92)90182-M",
      "article-title": "Sphingolipid trafficking-sorted out?.",
      "volume": "2",
      "author": "van Meer",
      "year": "1992",
      "journal-title": "Trends Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C39",
      "doi-asserted-by": "publisher",
      "first-page": "51",
      "DOI": "10.1002/jcb.240360106",
      "article-title": "Lipid polarity and sorting in epithelial cells.",
      "volume": "36",
      "author": "van Meer",
      "year": "1988",
      "journal-title": "J. Cell. Biochem"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C40",
      "doi-asserted-by": "publisher",
      "first-page": "987",
      "DOI": "10.1083/jcb.111.3.987",
      "article-title": "Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of MDCK cells.",
      "volume": "Ill",
      "author": "Wandinger-Ness",
      "year": "1990",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C41",
      "doi-asserted-by": "publisher",
      "first-page": "39",
      "DOI": "10.1083/jcb.117.1.39",
      "article-title": "Cytoplasmic sequence required for basolateral targeting of LDL receptor in livers of transgenic mice.",
      "volume": "117",
      "author": "Yokode",
      "year": "1992",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C42",
      "doi-asserted-by": "publisher",
      "first-page": "1031",
      "DOI": "10.1083/jcb.121.5.1031",
      "article-title": "Glycosylphosphatidilinositol-anchored proteins are preferentially targeted to the basolateral surface in Fischer Rat Thyroid epithelial cells. J.",
      "volume": "121",
      "author": "Zurzolo",
      "year": "1993",
      "journal-title": "CellBiol"
    },
    {
      "key": "2024071020052973800_JOCES_1993_S17_0009C43",
      "article-title": "VIP21/caveolin, glysphingolipid clusters, and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells.",
      "volume": "13",
      "author": "Zurzolo",
      "year": "1993",
      "journal-title": "EMBO J"
    }
  ],
  "container-title": "Journal of Cell Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/jcs/article-pdf/1993/Supplement_17/9/3552385/joces_1993_supplement_17_2.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/jcs/article-pdf/1993/Supplement_17/9/3552385/joces_1993_supplement_17_2.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        7,
        10
      ]
    ],
    "date-time": "2024-07-10T20:05:42Z",
    "timestamp": 1720641942000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/jcs/article/1993/Supplement_17/9/58261/Polarity-signals-in-epithelial-cells"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1993,
        12,
        1
      ]
    ]
  },
  "references-count": 43,
  "journal-issue": {
    "issue": "Supplement_17",
    "published-print": {
      "date-parts": [
        [
          1993,
          12,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/jcs.1993.Supplement_17.2",
  "relation": {},
  "ISSN": [
    "0021-9533",
    "1477-9137"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1993,
        12,
        1
      ]
    ]
  }
}