DOI: 10.1083/jcb.137.6.1255. Structural Requirements for Basolateral Sorting of the Human Transferrin Receptor in the Biosynthetic and Endocytic Pathways of Madin-Darby Canine Kidney Cells

Structural Requirements for Basolateral Sorting of the Human Transferrin Receptor in the Biosynthetic and Endocytic Pathways of Madin-Darby Canine Kidney Cells

10.1083/jcb.137.6.1255

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

In polarized Madin-Darby canine kidney (MDCK) cells, the transferrin receptor (TR) is selectively delivered to the basolateral surface, where it internalizes transferrin via clathrin-coated pits and recycles back to the basolateral border. Mutant tailless receptors are sorted randomly in both the biosynthetic and endocytic pathways, indicating that the basolateral sorting of TR is dependent upon a signal located within the 61–amino acid cytoplasmic domain. To identify the basolateral sorting signal of TR, we have analyzed a series of mutant human TR expressed in MDCK cells. We find that residues 19–41 are sufficient for basolateral sorting from both the biosynthetic and endocytic pathways and that this is the only region of the TR cytoplasmic tail containing basolateral sorting information. The basolateral sorting signal is distinct from the YTRF internalization signal contained within this region and is not tyrosine based. Detailed functional analyses of the mutant TR indicate that residues 29–35 are the most important for basolateral sorting from the biosynthetic pathway. The structural requirements for basolateral sorting of internalized receptors from the endocytic pathway are not identical. The most striking difference is that alteration of G31DNS34 to YTRF impairs basolateral sorting of newly synthesized receptors from the biosynthetic pathway but not internalized receptors from the endocytic pathway. Also, mutations have been identified that selectively impair basolateral sorting of internalized TRs from the endocytic pathway without affecting basolateral sorting of newly synthesized receptors. These results imply that there are subtle differences in the recognition of the TR basolateral sorting signal by separate sorting machinery located within the biosynthetic and endocytic pathways.

Bibliography

Odorizzi, G., & Trowbridge, I. S. (1997). Structural Requirements for Basolateral Sorting of the Human Transferrin Receptor in the Biosynthetic and Endocytic Pathways of Madin-Darby Canine Kidney Cells. The Journal of Cell Biology, 137(6), 1255â1264.

Authors 2

Greg Odorizzi (first)
Ian S. Trowbridge (additional)

References 41 Referenced 106

10.1002/j.1460-2075.1994.tb06513.x / EMBO (Eur Mol Biol Organ) J / Polarized sorting of the polymeric immunoglobulin receptor in the exocytic and endocytic pathways is controlled by the same amino acids by Aroeti (1994)
10.1083/jcb.123.5.1149 / J Cell Biol / Mutational and secondary structural analysis of the basolateral sorting signal of the polymeric immunoglobulin receptor by Aroeti (1993)
10.1016/0092-8674(93)90726-7 / Cell / A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor by Bates (1993)
10.1083/jcb.114.3.413 / J Cell Biol / A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin by Brewer (1991)
10.1126/science.2571189 / Science (Wash DC) / Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells by Brown (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)
10.1016/0092-8674(90)90509-D / Cell / Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis by Collawn (1990)
10.1016/S0021-9258(20)80596-1 / J Biol Chem / YTRF is the conserved internalization signal of the transferrin receptor, and a second YTRF signal at position 31-34 enhances endocytosis by Collawn (1993)
10.1002/j.1460-2075.1993.tb05816.x / EMBO (Eur Mol Biol Organ) J / The internalization signal and the phosphorylation site of transferrin receptor are distinct from the main basolateral sorting information by Dargemont (1993)
10.1083/jcb.109.6.3303 / J Cell Biol / Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome by Dunn (1989)
10.1016/0092-8674(91)90296-B / Cell / The essential tyrosine of the internalization signals in lysosomal acid phosphatase is part of a β turn by Eberle (1991)
10.1074/jbc.270.18.10999 / J Biol Chem / Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface by Futter (1995)
10.1016/S0021-9258(19)36850-4 / J Biol Chem / Related signals for endocytosis and basolateral sorting of the asialoglycoprotein receptor by Geffen (1993)
10.1083/jcb.128.3.321 / J Cell Biol / Cytoplasmic determinants involved in direct lysosomal sorting, endocytosis, and basolateral targeting of rat lgp120 (lamp-I) in MDCK cells by Höning (1995)
10.1083/jcb.97.2.508 / J Cell Biol / Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells by Hopkins (1983)
{'key': '2023072206592332200_B16'}
10.1002/j.1460-2075.1994.tb06594.x / EMBO (Eur Mol Biol Organ) J / A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells by Hunziker (1994)
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.110.2.283 / J Cell Biol / Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization by Jing (1990)
10.1073/pnas.82.2.488 / Proc Natl Acad Sci USA / Rapid and efficient site-specific mutagenesis without phenotypic selection by Kunkel (1985)
10.1073/pnas.92.22.10109 / Proc Natl Acad Sci USA / Biosynthetic transport of the asialoglycoprotein receptor H1 to the cell surface occurs via endosomes by Leitinger (1995)
10.1016/0955-0674(94)90075-2 / Curr Opin Cell Biol / Mechanisms of cell polarity: sorting and transport in epithelial cells by Matter (1994)
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)
10.1083/jcb.126.4.991 / J Cell Biol / Structural requirements and sequence motifs for polarized sorting and endocytosis of LDL and Fc receptors in MDCK cells by Matter (1994)
10.1016/0092-8674(93)90727-8 / Cell / Common signals control low density lipoprotein receptor sorting in endosomes and the Golgi complex of MDCK cells by Matter (1993)
10.1074/jbc.270.20.12219 / J Biol Chem / A cytoplasmic tyrosine is essential for the basolateral localization of mutants of the human nerve growth factor receptor in Madin-Darby canine kidney cells by Monlauzeur (1995)
10.1126/science.1439806 / Science (Wash DC) / Regulation of cell surface polarity from bacteria to mammals by Nelson (1992)
10.1016/S0091-679X(08)60599-3 / Methods Cell Biol / Recombinant Rous sarcoma virus vectors for avian cells by Odorizzi (1994)
10.1074/jbc.272.18.11757 / J Biol Chem / Structural requirements for MHC class II invariant chain trafficking in polarized MDCK cells by Odorizzi (1997)
10.1083/jcb.126.2.317 / J Cell Biol / Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment by Odorizzi (1994)
10.1083/jcb.135.1.139 / J Cell Biol / Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism by Odorizzi (1996)
10.1016/S0021-9258(19)50181-8 / J Biol Chem / The cytoplasmic domain of the polymeric immunoglobulin receptor contains two internalization signals that are distinct from its basolateral sorting signal by Okamoto (1992)
10.1016/S0021-9258(18)42979-1 / J Biol Chem / Biosynthesis of the human transferrin receptor in cultured cells by Omary (1981)
10.1002/j.1460-2075.1993.tb05866.x / EMBO (Eur Mol Biol Organ) 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)
10.1074/jbc.270.16.9067 / J Biol Chem / An internalization motif is created in the cytoplasmic domain of the transferrin receptor by substitution of a tyrosine at the first position of a predicted tight turn by Pytowski (1995)
10.1073/pnas.74.12.5463 / Proc Natl Acad Sci USA / DNA sequencing with chainterminating inhibitors by Sanger (1977)
10.1146/annurev.cb.01.110185.001331 / Annu Rev Cell Biol / Cell surface polarity in epithelia by Simons (1985)
10.1016/0092-8674(90)90357-K / Cell / Polarized sorting in epithelia by Simons (1990)
10.1073/pnas.84.14.4767 / Proc Natl Acad Sci USA / DNA sequence analysis with a modified bacteriophage T7 DNA polymerase by Tabor (1987)
10.1016/S0021-9258(18)53695-4 / J Biol Chem / Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine by Thomas (1993)
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)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited	2 years, 1 month ago (July 22, 2023, 3 a.m.)
Indexed	11 months, 2 weeks ago (Sept. 14, 2024, 7:31 p.m.)
Issued	28 years, 2 months ago (June 16, 1997)
Published	28 years, 2 months ago (June 16, 1997)
Published Online	28 years, 2 months ago (June 16, 1997)
Published Print	28 years, 2 months ago (June 16, 1997)

Funders 0

None

BibTeX

@article{Odorizzi_1997, title={Structural Requirements for Basolateral Sorting of the Human Transferrin Receptor in the Biosynthetic and Endocytic Pathways of Madin-Darby Canine Kidney Cells}, volume={137}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.137.6.1255}, DOI={10.1083/jcb.137.6.1255}, number={6}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Odorizzi, Greg and Trowbridge, Ian S.}, year={1997}, month=jun, pages={1255–1264} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        9,
        14
      ]
    ],
    "date-time": "2024-09-14T23:31:06Z",
    "timestamp": 1726356666905
  },
  "reference-count": 41,
  "publisher": "Rockefeller University Press",
  "issue": "6",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1997,
        6,
        16
      ]
    ]
  },
  "abstract": "<jats:p>In polarized Madin-Darby canine kidney (MDCK) cells, the transferrin receptor (TR) is selectively delivered to the basolateral surface, where it internalizes transferrin via clathrin-coated pits and recycles back to the basolateral border. Mutant tailless receptors are sorted randomly in both the biosynthetic and endocytic pathways, indicating that the basolateral sorting of TR is dependent upon a signal located within the 61\u2013amino acid cytoplasmic domain. To identify the basolateral sorting signal of TR, we have analyzed a series of mutant human TR expressed in MDCK cells. We find that residues 19\u201341 are sufficient for basolateral sorting from both the biosynthetic and endocytic pathways and that this is the only region of the TR cytoplasmic tail containing basolateral sorting information. The basolateral sorting signal is distinct from the YTRF internalization signal contained within this region and is not tyrosine based. Detailed functional analyses of the mutant TR indicate that residues 29\u201335 are the most important for basolateral sorting from the biosynthetic pathway. The structural requirements for basolateral sorting of internalized receptors from the endocytic pathway are not identical. The most striking difference is that alteration of G31DNS34 to YTRF impairs basolateral sorting of newly synthesized receptors from the biosynthetic pathway but not internalized receptors from the endocytic pathway. Also, mutations have been identified that selectively impair basolateral sorting of internalized TRs from the endocytic pathway without affecting basolateral sorting of newly synthesized receptors. These results imply that there are subtle differences in the recognition of the TR basolateral sorting signal by separate sorting machinery located within the biosynthetic and endocytic pathways.</jats:p>",
  "DOI": "10.1083/jcb.137.6.1255",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:47:50Z",
    "timestamp": 1027702070000
  },
  "page": "1255-1264",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 106,
  "title": "Structural Requirements for Basolateral Sorting of the Human Transferrin Receptor in the Biosynthetic and Endocytic Pathways of Madin-Darby Canine Kidney Cells",
  "prefix": "10.1083",
  "volume": "137",
  "author": [
    {
      "given": "Greg",
      "family": "Odorizzi",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Cancer Biology, The Salk Institute for Biological Studies, San Diego, California 92186-5800"
        }
      ]
    },
    {
      "given": "Ian S.",
      "family": "Trowbridge",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Cancer Biology, The Salk Institute for Biological Studies, San Diego, California 92186-5800"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        1997,
        6,
        16
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072206592332200_B1",
      "doi-asserted-by": "crossref",
      "first-page": "2297",
      "DOI": "10.1002/j.1460-2075.1994.tb06513.x",
      "article-title": "Polarized sorting of the polymeric immunoglobulin receptor in the exocytic and endocytic pathways is controlled by the same amino acids",
      "volume": "13",
      "author": "Aroeti",
      "year": "1994",
      "journal-title": "EMBO (Eur Mol Biol Organ) J"
    },
    {
      "key": "2023072206592332200_B2",
      "doi-asserted-by": "crossref",
      "first-page": "1149",
      "DOI": "10.1083/jcb.123.5.1149",
      "article-title": "Mutational and secondary structural analysis of the basolateral sorting signal of the polymeric immunoglobulin receptor",
      "volume": "123",
      "author": "Aroeti",
      "year": "1993",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B3",
      "doi-asserted-by": "crossref",
      "first-page": "1043",
      "DOI": "10.1016/0092-8674(93)90726-7",
      "article-title": "A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor",
      "volume": "74",
      "author": "Bates",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2023072206592332200_B4",
      "doi-asserted-by": "crossref",
      "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 virus hemagglutinin",
      "volume": "114",
      "author": "Brewer",
      "year": "1991",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B5",
      "doi-asserted-by": "crossref",
      "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 (Wash DC)"
    },
    {
      "key": "2023072206592332200_B6",
      "doi-asserted-by": "crossref",
      "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": "2023072206592332200_B7",
      "doi-asserted-by": "crossref",
      "first-page": "1061",
      "DOI": "10.1016/0092-8674(90)90509-D",
      "article-title": "Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis",
      "volume": "63",
      "author": "Collawn",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2023072206592332200_B8",
      "doi-asserted-by": "crossref",
      "first-page": "21686",
      "DOI": "10.1016/S0021-9258(20)80596-1",
      "article-title": "YTRF is the conserved internalization signal of the transferrin receptor, and a second YTRF signal at position 31-34 enhances endocytosis",
      "volume": "268",
      "author": "Collawn",
      "year": "1993",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B9",
      "doi-asserted-by": "crossref",
      "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": "Dargemont",
      "year": "1993",
      "journal-title": "EMBO (Eur Mol Biol Organ) J"
    },
    {
      "key": "2023072206592332200_B10",
      "doi-asserted-by": "crossref",
      "first-page": "3303",
      "DOI": "10.1083/jcb.109.6.3303",
      "article-title": "Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome",
      "volume": "109",
      "author": "Dunn",
      "year": "1989",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B11",
      "doi-asserted-by": "crossref",
      "first-page": "1203",
      "DOI": "10.1016/0092-8674(91)90296-B",
      "article-title": "The essential tyrosine of the internalization signals in lysosomal acid phosphatase is part of a \u03b2 turn",
      "volume": "67",
      "author": "Eberle",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2023072206592332200_B12",
      "doi-asserted-by": "crossref",
      "first-page": "10999",
      "DOI": "10.1074/jbc.270.18.10999",
      "article-title": "Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface",
      "volume": "270",
      "author": "Futter",
      "year": "1995",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B13",
      "doi-asserted-by": "crossref",
      "first-page": "20772",
      "DOI": "10.1016/S0021-9258(19)36850-4",
      "article-title": "Related signals for endocytosis and basolateral sorting of the asialoglycoprotein receptor",
      "volume": "268",
      "author": "Geffen",
      "year": "1993",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B14",
      "doi-asserted-by": "crossref",
      "first-page": "321",
      "DOI": "10.1083/jcb.128.3.321",
      "article-title": "Cytoplasmic determinants involved in direct lysosomal sorting, endocytosis, and basolateral targeting of rat lgp120 (lamp-I) in MDCK cells",
      "volume": "128",
      "author": "H\u00f6ning",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B15",
      "doi-asserted-by": "crossref",
      "first-page": "508",
      "DOI": "10.1083/jcb.97.2.508",
      "article-title": "Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells",
      "volume": "97",
      "author": "Hopkins",
      "year": "1983",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B16"
    },
    {
      "key": "2023072206592332200_B17",
      "doi-asserted-by": "crossref",
      "first-page": "2963",
      "DOI": "10.1002/j.1460-2075.1994.tb06594.x",
      "article-title": "A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells",
      "volume": "13",
      "author": "Hunziker",
      "year": "1994",
      "journal-title": "EMBO (Eur Mol Biol Organ) J"
    },
    {
      "key": "2023072206592332200_B18",
      "doi-asserted-by": "crossref",
      "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": "2023072206592332200_B19",
      "doi-asserted-by": "crossref",
      "first-page": "283",
      "DOI": "10.1083/jcb.110.2.283",
      "article-title": "Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization",
      "volume": "110",
      "author": "Jing",
      "year": "1990",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B20",
      "doi-asserted-by": "crossref",
      "first-page": "488",
      "DOI": "10.1073/pnas.82.2.488",
      "article-title": "Rapid and efficient site-specific mutagenesis without phenotypic selection",
      "volume": "82",
      "author": "Kunkel",
      "year": "1985",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072206592332200_B21",
      "doi-asserted-by": "crossref",
      "first-page": "10109",
      "DOI": "10.1073/pnas.92.22.10109",
      "article-title": "Biosynthetic transport of the asialoglycoprotein receptor H1 to the cell surface occurs via endosomes",
      "volume": "92",
      "author": "Leitinger",
      "year": "1995",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072206592332200_B22",
      "doi-asserted-by": "crossref",
      "first-page": "545",
      "DOI": "10.1016/0955-0674(94)90075-2",
      "article-title": "Mechanisms of cell polarity: sorting and transport in epithelial cells",
      "volume": "6",
      "author": "Matter",
      "year": "1994",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
      "key": "2023072206592332200_B23",
      "doi-asserted-by": "crossref",
      "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": "2023072206592332200_B24",
      "doi-asserted-by": "crossref",
      "first-page": "991",
      "DOI": "10.1083/jcb.126.4.991",
      "article-title": "Structural requirements and sequence motifs for polarized sorting and endocytosis of LDL and Fc receptors in MDCK cells",
      "volume": "126",
      "author": "Matter",
      "year": "1994",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B25",
      "doi-asserted-by": "crossref",
      "first-page": "1053",
      "DOI": "10.1016/0092-8674(93)90727-8",
      "article-title": "Common signals control low density lipoprotein receptor sorting in endosomes and the Golgi complex of MDCK cells",
      "volume": "74",
      "author": "Matter",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2023072206592332200_B26",
      "doi-asserted-by": "crossref",
      "first-page": "12219",
      "DOI": "10.1074/jbc.270.20.12219",
      "article-title": "A cytoplasmic tyrosine is essential for the basolateral localization of mutants of the human nerve growth factor receptor in Madin-Darby canine kidney cells",
      "volume": "270",
      "author": "Monlauzeur",
      "year": "1995",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B27",
      "doi-asserted-by": "crossref",
      "first-page": "948",
      "DOI": "10.1126/science.1439806",
      "article-title": "Regulation of cell surface polarity from bacteria to mammals",
      "volume": "258",
      "author": "Nelson",
      "year": "1992",
      "journal-title": "Science (Wash DC)"
    },
    {
      "key": "2023072206592332200_B28",
      "doi-asserted-by": "crossref",
      "first-page": "79",
      "DOI": "10.1016/S0091-679X(08)60599-3",
      "article-title": "Recombinant Rous sarcoma virus vectors for avian cells",
      "volume": "43",
      "author": "Odorizzi",
      "year": "1994",
      "journal-title": "Methods Cell Biol"
    },
    {
      "key": "2023072206592332200_B29",
      "doi-asserted-by": "crossref",
      "first-page": "11757",
      "DOI": "10.1074/jbc.272.18.11757",
      "article-title": "Structural requirements for MHC class II invariant chain trafficking in polarized MDCK cells",
      "volume": "272",
      "author": "Odorizzi",
      "year": "1997",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B30",
      "doi-asserted-by": "crossref",
      "first-page": "317",
      "DOI": "10.1083/jcb.126.2.317",
      "article-title": "Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment",
      "volume": "126",
      "author": "Odorizzi",
      "year": "1994",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B31",
      "doi-asserted-by": "crossref",
      "first-page": "139",
      "DOI": "10.1083/jcb.135.1.139",
      "article-title": "Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism",
      "volume": "135",
      "author": "Odorizzi",
      "year": "1996",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072206592332200_B32",
      "doi-asserted-by": "crossref",
      "first-page": "9925",
      "DOI": "10.1016/S0021-9258(19)50181-8",
      "article-title": "The cytoplasmic domain of the polymeric immunoglobulin receptor contains two internalization signals that are distinct from its basolateral sorting signal",
      "volume": "267",
      "author": "Okamoto",
      "year": "1992",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B33",
      "doi-asserted-by": "crossref",
      "first-page": "12888",
      "DOI": "10.1016/S0021-9258(18)42979-1",
      "article-title": "Biosynthesis of the human transferrin receptor in cultured cells",
      "volume": "256",
      "author": "Omary",
      "year": "1981",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B34",
      "doi-asserted-by": "crossref",
      "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 (Eur Mol Biol Organ) J"
    },
    {
      "key": "2023072206592332200_B35",
      "doi-asserted-by": "crossref",
      "first-page": "9067",
      "DOI": "10.1074/jbc.270.16.9067",
      "article-title": "An internalization motif is created in the cytoplasmic domain of the transferrin receptor by substitution of a tyrosine at the first position of a predicted tight turn",
      "volume": "270",
      "author": "Pytowski",
      "year": "1995",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B36",
      "doi-asserted-by": "crossref",
      "first-page": "5463",
      "DOI": "10.1073/pnas.74.12.5463",
      "article-title": "DNA sequencing with chainterminating inhibitors",
      "volume": "74",
      "author": "Sanger",
      "year": "1977",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072206592332200_B37",
      "doi-asserted-by": "crossref",
      "first-page": "243",
      "DOI": "10.1146/annurev.cb.01.110185.001331",
      "article-title": "Cell surface polarity in epithelia",
      "volume": "1",
      "author": "Simons",
      "year": "1985",
      "journal-title": "Annu Rev Cell Biol"
    },
    {
      "key": "2023072206592332200_B38",
      "doi-asserted-by": "crossref",
      "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": "2023072206592332200_B39",
      "doi-asserted-by": "crossref",
      "first-page": "4767",
      "DOI": "10.1073/pnas.84.14.4767",
      "article-title": "DNA sequence analysis with a modified bacteriophage T7 DNA polymerase",
      "volume": "84",
      "author": "Tabor",
      "year": "1987",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072206592332200_B40",
      "doi-asserted-by": "crossref",
      "first-page": "3313",
      "DOI": "10.1016/S0021-9258(18)53695-4",
      "article-title": "Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine",
      "volume": "5",
      "author": "Thomas",
      "year": "1993",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072206592332200_B41",
      "doi-asserted-by": "crossref",
      "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": "111",
      "author": "Wandinger-Ness",
      "year": "1990",
      "journal-title": "J Cell Biol"
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/137/6/1255/1485399/14479.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/137/6/1255/1485399/14479.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        22
      ]
    ],
    "date-time": "2023-07-22T07:00:26Z",
    "timestamp": 1690009226000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/137/6/1255/619/Structural-Requirements-for-Basolateral-Sorting-of"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1997,
        6,
        16
      ]
    ]
  },
  "references-count": 41,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          1997,
          6,
          16
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.137.6.1255",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1997,
        6,
        16
      ]
    ]
  }
}