DOI: 10.1126/science.2110383. Phosphorylation of the Polymeric Immunoglobulin Receptor Required for Its Efficient Transcytosis

Phosphorylation of the Polymeric Immunoglobulin Receptor Required for Its Efficient Transcytosis

10.1126/science.2110383

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The endosomal compartment of polarized epithelial cells is a major crossroads for membrane traffic. Proteins entering this compartment from the cell surface are sorted for transport to one of several destinations: recycling to the original cell surface, targeting to lysosomes for degradation, or transcytosis to the opposite surface. The polymeric immunoglobulin receptor (pIgR), which is normally transcytosed from the basolateral to the apical surface, was used as a model to dissect the signals that mediate this sorting event. When exogenous receptor was expressed in Madin-Darby Canine Kidney (MDCK) cells, it was shown that phosphorylation of pIgR at the serine residue at position 664 is required for efficient transcytosis. Replacement of this serine with alanine generated a receptor that is transcytosed only slowly, and appears to be recycled. Conversely, substitution with aspartic acid (which mimics the negative charge of the phosphate group) results in rapid transcytosis. It was concluded that phosphorylation is the signal that directs the pIgR from the endosome into the transcytotic pathway.

Bibliography

Casanova, J. E., Breitfeld, P. P., Ross, S. A., & Mostov, K. E. (1990). Phosphorylation of the Polymeric Immunoglobulin Receptor Required for Its Efficient Transcytosis. Science, 248(4956), 742â745.

Authors 4

James E. Casanova (first)
Philip P. Breitfeld (additional)
Stuart A. Ross (additional)
Keith E. Mostov (additional)

References 37 Referenced 198

BARTLES, J.R., BIOGENESIS OF THE RAT HEPATOCYTE PLASMA-MEMBRANE INVIVO - COMPARISON OF THE PATHWAYS TAKEN BY APICAL AND BASOLATERAL PROTEINS USING SUBCELLULAR FRACTIONATION, JOURNAL OF CELL BIOLOGY 105: 1241 (1987). (10.1083/jcb.105.3.1241) / JOURNAL OF CELL BIOLOGY (1987)
BREITFELD, P.P., POSTENDOCYTOTIC SORTING OF THE LIGAND FOR THE POLYMERIC IMMUNOGLOBULIN RECEPTOR IN MADIN-DARBY CANINE KIDNEY-CELLS, JOURNAL OF CELL BIOLOGY 109: 475 (1989). (10.1083/jcb.109.2.475) / JOURNAL OF CELL BIOLOGY (1989)
BREITFELD, P.P., EXPRESSION AND ANALYSIS OF THE POLYMERIC IMMUNOGLOBULIN RECEPTOR IN MADIN-DARBY CANINE KIDNEY-CELLS USING RETROVIRAL VECTORS, METHODS IN CELL BIOLOGY 32: 329 (1989). (10.1016/S0091-679X(08)61178-4) / METHODS IN CELL BIOLOGY (1989)
BROWN, M.S., RECYCLING RECEPTORS - THE ROUND-TRIP ITINERARY OF MIGRANT MEMBRANE-PROTEINS, CELL 32: 663 (1983). (10.1016/0092-8674(83)90052-1) / CELL (1983)
CASANOVA J unpublished data.
COLOMA, J, CHARACTERIZATION AND SEQUENCE OF A CDNA CLONE OF GAMMA-GLUTAMYL-TRANSPEPTIDASE, NUCLEIC ACIDS RESEARCH 14: 1393 (1986). (10.1093/nar/14.3.1393) / NUCLEIC ACIDS RESEARCH (1986)
EDELMAN, A.M., PROTEIN SERINE THREONINE KINASES, ANNUAL REVIEW OF BIOCHEMISTRY 56: 567 (1987). (10.1146/annurev.bi.56.070187.003031) / ANNUAL REVIEW OF BIOCHEMISTRY (1987)
FULLER, S.D., TRANSFERRIN RECEPTOR POLARITY AND RECYCLING ACCURACY IN TIGHT AND LEAKY STRAINS OF MADIN-DARBY CANINE KIDNEY-CELLS, JOURNAL OF CELL BIOLOGY 103: 1767 (1986). (10.1083/jcb.103.5.1767) / JOURNAL OF CELL BIOLOGY (1986)
GEUZE, H.J., INTRACELLULAR RECEPTOR SORTING DURING ENDOCYTOSIS - COMPARATIVE IMMUNOELECTRON MICROSCOPY OF MULTIPLE RECEPTORS IN RAT-LIVER, CELL 37: 195 (1984). (10.1016/0092-8674(84)90315-5) / CELL (1984)
Heuser, J. E., Journal of Cell Biology 108: 389 (1989). (10.1083/jcb.108.2.389) / Journal of Cell Biology (1989)
Heuser, J. E., Journal of Cell Biology 108: 401 (1989). (10.1083/jcb.108.2.401) / Journal of Cell Biology (1989)
HOUMARD, J, STAPHYLOCOCCAL PROTEASE - A PROTEOLYTIC-ENZYME SPECIFIC FOR GLUTAMOYL BONDS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 69: 3506 (1972). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1972)
HUNZIKER, W, THE SUCRASE-ISOMALTASE COMPLEX - PRIMARY STRUCTURE, MEMBRANE-ORIENTATION, AND EVOLUTION OF A STALKED, INTRINSIC BRUSH-BORDER PROTEIN, CELL 46: 227 (1986). (10.1016/0092-8674(86)90739-7) / CELL (1986)
HUNZIKER, W, EXPRESSION OF MACROPHAGE LYMPHOCYTE FC-RECEPTORS IN MADIN-DARBY CANINE KIDNEY-CELLS - POLARITY AND TRANSCYTOSIS DIFFER FOR ISOFORMS WITH OR WITHOUT COATED PIT LOCALIZATION DOMAINS, JOURNAL OF CELL BIOLOGY 109: 3291 (1989). (10.1083/jcb.109.6.3291) / JOURNAL OF CELL BIOLOGY (1989)
KUNKEL, T.A., RAPID AND EFFICIENT SITE-SPECIFIC MUTAGENESIS WITHOUT PHENOTYPIC SELECTION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 82: 488 (1985). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1985)
LARKIN, J.M., PHOSPHORYLATION OF THE RAT HEPATIC POLYMERIC IGA RECEPTOR, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 4759 (1986). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1986)
LISANTI, M.P., POLARIZED APICAL DISTRIBUTION OF GLYCOSYL-PHOSPHATIDYLINOSITOL-ANCHORED PROTEINS IN A RENAL EPITHELIAL-CELL LINE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 9557 (1988). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1988)
MARATOSFLIER, E, RECEPTOR-MEDIATED VECTORIAL TRANSCYTOSIS OF EPIDERMAL GROWTH-FACTOR BY MADIN-DARBY CANINE KIDNEY-CELLS, JOURNAL OF CELL BIOLOGY 105: 1595 (1987). (10.1083/jcb.105.4.1595) / JOURNAL OF CELL BIOLOGY (1987)
MASSEY, D, EVIDENCE FOR THE TRANSIT OF AMINOPEPTIDASE-N THROUGH THE BASOLATERAL MEMBRANE BEFORE IT REACHES THE BRUSH-BORDER OF ENTEROCYTES, JOURNAL OF MEMBRANE BIOLOGY 96: 19 (1987). (10.1007/BF01869331) / JOURNAL OF MEMBRANE BIOLOGY (1987)
MATLIN, K.S., SORTING OF AN APICAL PLASMA-MEMBRANE GLYCOPROTEIN OCCURS BEFORE IT REACHES THE CELL-SURFACE IN CULTURED EPITHELIAL-CELLS, JOURNAL OF CELL BIOLOGY 99: 2131 (1984). (10.1083/jcb.99.6.2131) / JOURNAL OF CELL BIOLOGY (1984)
MATTER, K, SORTING OF ENDOGENOUS PLASMA-MEMBRANE PROTEINS OCCURS FROM 2 SITES IN CULTURED HUMAN INTESTINAL EPITHELIAL-CELLS (CACO-2), CELL 60: 429 (1990). (10.1016/0092-8674(90)90594-5) / CELL (1990)
MOKTARI, S, SUBCELLULAR FRACTIONATION AND SUBCELLULAR-LOCALIZATION OF AMINOPEPTIDASE-N IN THE RABBIT ENTEROCYTES, JOURNAL OF MEMBRANE BIOLOGY 89: 53 (1986). (10.1007/BF01870895) / JOURNAL OF MEMBRANE BIOLOGY (1986)
MOSTOV, K.E., TRANSCYTOSIS, CELL 43: 389 (1985). (10.1016/0092-8674(85)90166-7) / CELL (1985)
MOSTOV, K.E., POLYMERIC IMMUNOGLOBULIN RECEPTOR EXPRESSED IN MDCK CELLS TRANSCYTOSES IGA, CELL 46: 613 (1986). (10.1016/0092-8674(86)90887-1) / CELL (1986)
MOSTOV, K.E., DELETION OF THE CYTOPLASMIC DOMAIN OF THE POLYMERIC IMMUNOGLOBULIN RECEPTOR PREVENTS BASOLATERAL LOCALIZATION AND ENDOCYTOSIS, CELL 47: 359 (1986). (10.1016/0092-8674(86)90592-1) / CELL (1986)
MOSTOV, K.E., THE RECEPTOR FOR TRANS-EPITHELIAL TRANSPORT OF IGA AND IGM CONTAINS MULTIPLE IMMUNOGLOBULIN-LIKE DOMAINS, NATURE 308: 37 (1984). (10.1038/308037a0) / NATURE (1984)
PARTON, R.G., MEETING OF THE APICAL AND BASOLATERAL ENDOCYTIC PATHWAYS OF THE MADIN-DARBY CANINE KIDNEY-CELL IN LATE ENDOSOMES, JOURNAL OF CELL BIOLOGY 109: 3259 (1989). (10.1083/jcb.109.6.3259) / JOURNAL OF CELL BIOLOGY (1989)
PFEIFFER, S.E., EMBO J 3: 2687 (1984). (10.1002/j.1460-2075.1984.tb02194.x) / EMBO J (1984)
RAPHAEL, G.D., PATHO-PHYSIOLOGY OF RHINITIS .1. ASSESSMENT OF THE SOURCES OF PROTEIN IN METHACHOLINE-INDUCED NASAL SECRETIONS, AMERICAN REVIEW OF RESPIRATORY DISEASE 138: 413 (1988). (10.1164/ajrccm/138.2.413) / AMERICAN REVIEW OF RESPIRATORY DISEASE (1988)
RODEWALD, R, RECEPTOR-MEDIATED TRANSPORT OF IGG, JOURNAL OF CELL BIOLOGY 99: S159 (1984). (10.1083/jcb.99.1.159s) / JOURNAL OF CELL BIOLOGY (1984)
SCHLESSINGER, J, REGULATION OF CELL-PROLIFERATION BY EPIDERMAL GROWTH-FACTOR, CRC CRITICAL REVIEWS IN BIOCHEMISTRY 14: 93 (1983). (10.3109/10409238309102791) / CRC CRITICAL REVIEWS IN BIOCHEMISTRY (1983)
SIMISTER, N.E., AN FC RECEPTOR STRUCTURALLY RELATED TO MHC CLASS-I ANTIGENS, NATURE 337: 184 (1989). (10.1038/337184a0) / NATURE (1989)
SIMONS, K, LIPID SORTING IN EPITHELIAL-CELLS, BIOCHEMISTRY 27: 6197 (1988). (10.1021/bi00417a001) / BIOCHEMISTRY (1988)
SZTUL, E.S., BIOGENESIS OF THE POLYMERIC IGA RECEPTOR IN RAT HEPATOCYTES .2. LOCALIZATION OF ITS INTRACELLULAR FORMS BY CELL FRACTIONATION STUDIES, JOURNAL OF CELL BIOLOGY 100: 1255 (1985). (10.1083/jcb.100.4.1255) / JOURNAL OF CELL BIOLOGY (1985)
THORSNESS, P.E., INACTIVATION OF ISOCITRATE DEHYDROGENASE BY PHOSPHORYLATION IS MEDIATED BY THE NEGATIVE CHARGE OF THE PHOSPHATE, JOURNAL OF BIOLOGICAL CHEMISTRY 262: 10422 (1987). (10.1016/S0021-9258(18)60975-5) / JOURNAL OF BIOLOGICAL CHEMISTRY (1987)
URBAN, J, CONSTITUTIVE APICAL SECRETION OF AN 80-KD SULFATED GLYCOPROTEIN COMPLEX IN THE POLARIZED EPITHELIAL MADIN-DARBY CANINE KIDNEY-CELL LINE, JOURNAL OF CELL BIOLOGY 105: 2735 (1987). (10.1083/jcb.105.6.2735) / JOURNAL OF CELL BIOLOGY (1987)
VONBONSDORFF, C.H., APICAL AND BASOLATERAL ENDOCYTOSIS IN MADIN-DARBY CANINE KIDNEY (MDCK) CELLS GROWN ON NITROCELLULOSE FILTERS, EMBO JOURNAL 4: 2781 (1985). (10.1002/j.1460-2075.1985.tb04004.x) / EMBO JOURNAL (1985)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 6:10 p.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 4:17 a.m.)
Indexed	1 week, 1 day ago (Aug. 23, 2025, 1:02 a.m.)
Issued	35 years, 3 months ago (May 11, 1990)
Published	35 years, 3 months ago (May 11, 1990)
Published Print	35 years, 3 months ago (May 11, 1990)

Funders 0

None

BibTeX

@article{Casanova_1990, title={Phosphorylation of the Polymeric Immunoglobulin Receptor Required for Its Efficient Transcytosis}, volume={248}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.2110383}, DOI={10.1126/science.2110383}, number={4956}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Casanova, James E. and Breitfeld, Philip P. and Ross, Stuart A. and Mostov, Keith E.}, year={1990}, month=may, pages={742–745} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        23
      ]
    ],
    "date-time": "2025-08-23T05:02:40Z",
    "timestamp": 1755925360029
  },
  "reference-count": 37,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "4956",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1990,
        5,
        11
      ]
    ]
  },
  "abstract": "<jats:p>The endosomal compartment of polarized epithelial cells is a major crossroads for membrane traffic. Proteins entering this compartment from the cell surface are sorted for transport to one of several destinations: recycling to the original cell surface, targeting to lysosomes for degradation, or transcytosis to the opposite surface. The polymeric immunoglobulin receptor (pIgR), which is normally transcytosed from the basolateral to the apical surface, was used as a model to dissect the signals that mediate this sorting event. When exogenous receptor was expressed in Madin-Darby Canine Kidney (MDCK) cells, it was shown that phosphorylation of pIgR at the serine residue at position 664 is required for efficient transcytosis. Replacement of this serine with alanine generated a receptor that is transcytosed only slowly, and appears to be recycled. Conversely, substitution with aspartic acid (which mimics the negative charge of the phosphate group) results in rapid transcytosis. It was concluded that phosphorylation is the signal that directs the pIgR from the endosome into the transcytotic pathway.</jats:p>",
  "DOI": "10.1126/science.2110383",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ],
    "date-time": "2006-10-05T22:10:14Z",
    "timestamp": 1160086214000
  },
  "page": "742-745",
  "source": "Crossref",
  "is-referenced-by-count": 198,
  "title": "Phosphorylation of the Polymeric Immunoglobulin Receptor Required for Its Efficient Transcytosis",
  "prefix": "10.1126",
  "volume": "248",
  "author": [
    {
      "given": "James E.",
      "family": "Casanova",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Anatomy, Program in Cell Biology, and Cardiovascular Research Institute, University of California, San Francisco, CA 94143."
        }
      ]
    },
    {
      "given": "Philip P.",
      "family": "Breitfeld",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pediatrics (Hematology), University of Massachusetts Medical School, Worcester, MA 01655."
        }
      ]
    },
    {
      "given": "Stuart A.",
      "family": "Ross",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy, Program in Cell Biology, and Cardiovascular Research Institute, University of California, San Francisco, CA 94143."
        }
      ]
    },
    {
      "given": "Keith E.",
      "family": "Mostov",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy, Program in Cell Biology, and Cardiovascular Research Institute, University of California, San Francisco, CA 94143."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "crossref",
      "first-page": "1241",
      "DOI": "10.1083/jcb.105.3.1241",
      "volume": "105",
      "year": "1987",
      "unstructured": "BARTLES, J.R., BIOGENESIS OF THE RAT HEPATOCYTE PLASMA-MEMBRANE INVIVO - COMPARISON OF THE PATHWAYS TAKEN BY APICAL AND BASOLATERAL PROTEINS USING SUBCELLULAR FRACTIONATION, JOURNAL OF CELL BIOLOGY 105: 1241 (1987).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "crossref",
      "first-page": "475",
      "DOI": "10.1083/jcb.109.2.475",
      "volume": "109",
      "year": "1989",
      "unstructured": "BREITFELD, P.P., POSTENDOCYTOTIC SORTING OF THE LIGAND FOR THE POLYMERIC IMMUNOGLOBULIN RECEPTOR IN MADIN-DARBY CANINE KIDNEY-CELLS, JOURNAL OF CELL BIOLOGY 109: 475 (1989).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "crossref",
      "first-page": "329",
      "DOI": "10.1016/S0091-679X(08)61178-4",
      "volume": "32",
      "year": "1989",
      "unstructured": "BREITFELD, P.P., EXPRESSION AND ANALYSIS OF THE POLYMERIC IMMUNOGLOBULIN RECEPTOR IN MADIN-DARBY CANINE KIDNEY-CELLS USING RETROVIRAL VECTORS, METHODS IN CELL BIOLOGY 32: 329 (1989).",
      "journal-title": "METHODS IN CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "663",
      "DOI": "10.1016/0092-8674(83)90052-1",
      "volume": "32",
      "year": "1983",
      "unstructured": "BROWN, M.S., RECYCLING RECEPTORS - THE ROUND-TRIP ITINERARY OF MIGRANT MEMBRANE-PROTEINS, CELL 32: 663 (1983).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_5_1",
      "unstructured": "CASANOVA J unpublished data."
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "crossref",
      "first-page": "1393",
      "DOI": "10.1093/nar/14.3.1393",
      "volume": "14",
      "year": "1986",
      "unstructured": "COLOMA, J, CHARACTERIZATION AND SEQUENCE OF A CDNA CLONE OF GAMMA-GLUTAMYL-TRANSPEPTIDASE, NUCLEIC ACIDS RESEARCH 14: 1393 (1986).",
      "journal-title": "NUCLEIC ACIDS RESEARCH"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "567",
      "DOI": "10.1146/annurev.bi.56.070187.003031",
      "volume": "56",
      "year": "1987",
      "unstructured": "EDELMAN, A.M., PROTEIN SERINE THREONINE KINASES, ANNUAL REVIEW OF BIOCHEMISTRY 56: 567 (1987).",
      "journal-title": "ANNUAL REVIEW OF BIOCHEMISTRY"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "1767",
      "DOI": "10.1083/jcb.103.5.1767",
      "volume": "103",
      "year": "1986",
      "unstructured": "FULLER, S.D., TRANSFERRIN RECEPTOR POLARITY AND RECYCLING ACCURACY IN TIGHT AND LEAKY STRAINS OF MADIN-DARBY CANINE KIDNEY-CELLS, JOURNAL OF CELL BIOLOGY 103: 1767 (1986).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "crossref",
      "first-page": "195",
      "DOI": "10.1016/0092-8674(84)90315-5",
      "volume": "37",
      "year": "1984",
      "unstructured": "GEUZE, H.J., INTRACELLULAR RECEPTOR SORTING DURING ENDOCYTOSIS - COMPARATIVE IMMUNOELECTRON MICROSCOPY OF MULTIPLE RECEPTORS IN RAT-LIVER, CELL 37: 195 (1984).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "389",
      "DOI": "10.1083/jcb.108.2.389",
      "volume": "108",
      "year": "1989",
      "unstructured": "Heuser, J. E., Journal of Cell Biology 108: 389 (1989).",
      "journal-title": "Journal of Cell Biology"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "crossref",
      "first-page": "401",
      "DOI": "10.1083/jcb.108.2.401",
      "volume": "108",
      "year": "1989",
      "unstructured": "Heuser, J. E., Journal of Cell Biology 108: 401 (1989).",
      "journal-title": "Journal of Cell Biology"
    },
    {
      "key": "e_1_2_1_12_1",
      "first-page": "3506",
      "volume": "69",
      "year": "1972",
      "unstructured": "HOUMARD, J, STAPHYLOCOCCAL PROTEASE - A PROTEOLYTIC-ENZYME SPECIFIC FOR GLUTAMOYL BONDS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 69: 3506 (1972).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "227",
      "DOI": "10.1016/0092-8674(86)90739-7",
      "volume": "46",
      "year": "1986",
      "unstructured": "HUNZIKER, W, THE SUCRASE-ISOMALTASE COMPLEX - PRIMARY STRUCTURE, MEMBRANE-ORIENTATION, AND EVOLUTION OF A STALKED, INTRINSIC BRUSH-BORDER PROTEIN, CELL 46: 227 (1986).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "3291",
      "DOI": "10.1083/jcb.109.6.3291",
      "volume": "109",
      "year": "1989",
      "unstructured": "HUNZIKER, W, EXPRESSION OF MACROPHAGE LYMPHOCYTE FC-RECEPTORS IN MADIN-DARBY CANINE KIDNEY-CELLS - POLARITY AND TRANSCYTOSIS DIFFER FOR ISOFORMS WITH OR WITHOUT COATED PIT LOCALIZATION DOMAINS, JOURNAL OF CELL BIOLOGY 109: 3291 (1989).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_15_1",
      "first-page": "488",
      "volume": "82",
      "year": "1985",
      "unstructured": "KUNKEL, T.A., RAPID AND EFFICIENT SITE-SPECIFIC MUTAGENESIS WITHOUT PHENOTYPIC SELECTION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 82: 488 (1985).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_16_1",
      "first-page": "4759",
      "volume": "83",
      "year": "1986",
      "unstructured": "LARKIN, J.M., PHOSPHORYLATION OF THE RAT HEPATIC POLYMERIC IGA RECEPTOR, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 4759 (1986).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_17_1",
      "first-page": "9557",
      "volume": "85",
      "year": "1988",
      "unstructured": "LISANTI, M.P., POLARIZED APICAL DISTRIBUTION OF GLYCOSYL-PHOSPHATIDYLINOSITOL-ANCHORED PROTEINS IN A RENAL EPITHELIAL-CELL LINE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 9557 (1988).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "crossref",
      "first-page": "1595",
      "DOI": "10.1083/jcb.105.4.1595",
      "volume": "105",
      "year": "1987",
      "unstructured": "MARATOSFLIER, E, RECEPTOR-MEDIATED VECTORIAL TRANSCYTOSIS OF EPIDERMAL GROWTH-FACTOR BY MADIN-DARBY CANINE KIDNEY-CELLS, JOURNAL OF CELL BIOLOGY 105: 1595 (1987).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_19_1",
      "doi-asserted-by": "crossref",
      "first-page": "19",
      "DOI": "10.1007/BF01869331",
      "volume": "96",
      "year": "1987",
      "unstructured": "MASSEY, D, EVIDENCE FOR THE TRANSIT OF AMINOPEPTIDASE-N THROUGH THE BASOLATERAL MEMBRANE BEFORE IT REACHES THE BRUSH-BORDER OF ENTEROCYTES, JOURNAL OF MEMBRANE BIOLOGY 96: 19 (1987).",
      "journal-title": "JOURNAL OF MEMBRANE BIOLOGY"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "crossref",
      "first-page": "2131",
      "DOI": "10.1083/jcb.99.6.2131",
      "volume": "99",
      "year": "1984",
      "unstructured": "MATLIN, K.S., SORTING OF AN APICAL PLASMA-MEMBRANE GLYCOPROTEIN OCCURS BEFORE IT REACHES THE CELL-SURFACE IN CULTURED EPITHELIAL-CELLS, JOURNAL OF CELL BIOLOGY 99: 2131 (1984).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "429",
      "DOI": "10.1016/0092-8674(90)90594-5",
      "volume": "60",
      "year": "1990",
      "unstructured": "MATTER, K, SORTING OF ENDOGENOUS PLASMA-MEMBRANE PROTEINS OCCURS FROM 2 SITES IN CULTURED HUMAN INTESTINAL EPITHELIAL-CELLS (CACO-2), CELL 60: 429 (1990).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "crossref",
      "first-page": "53",
      "DOI": "10.1007/BF01870895",
      "volume": "89",
      "year": "1986",
      "unstructured": "MOKTARI, S, SUBCELLULAR FRACTIONATION AND SUBCELLULAR-LOCALIZATION OF AMINOPEPTIDASE-N IN THE RABBIT ENTEROCYTES, JOURNAL OF MEMBRANE BIOLOGY 89: 53 (1986).",
      "journal-title": "JOURNAL OF MEMBRANE BIOLOGY"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "389",
      "DOI": "10.1016/0092-8674(85)90166-7",
      "volume": "43",
      "year": "1985",
      "unstructured": "MOSTOV, K.E., TRANSCYTOSIS, CELL 43: 389 (1985).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "crossref",
      "first-page": "613",
      "DOI": "10.1016/0092-8674(86)90887-1",
      "volume": "46",
      "year": "1986",
      "unstructured": "MOSTOV, K.E., POLYMERIC IMMUNOGLOBULIN RECEPTOR EXPRESSED IN MDCK CELLS TRANSCYTOSES IGA, CELL 46: 613 (1986).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "crossref",
      "first-page": "359",
      "DOI": "10.1016/0092-8674(86)90592-1",
      "volume": "47",
      "year": "1986",
      "unstructured": "MOSTOV, K.E., DELETION OF THE CYTOPLASMIC DOMAIN OF THE POLYMERIC IMMUNOGLOBULIN RECEPTOR PREVENTS BASOLATERAL LOCALIZATION AND ENDOCYTOSIS, CELL 47: 359 (1986).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "37",
      "DOI": "10.1038/308037a0",
      "volume": "308",
      "year": "1984",
      "unstructured": "MOSTOV, K.E., THE RECEPTOR FOR TRANS-EPITHELIAL TRANSPORT OF IGA AND IGM CONTAINS MULTIPLE IMMUNOGLOBULIN-LIKE DOMAINS, NATURE 308: 37 (1984).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "3259",
      "DOI": "10.1083/jcb.109.6.3259",
      "volume": "109",
      "year": "1989",
      "unstructured": "PARTON, R.G., MEETING OF THE APICAL AND BASOLATERAL ENDOCYTIC PATHWAYS OF THE MADIN-DARBY CANINE KIDNEY-CELL IN LATE ENDOSOMES, JOURNAL OF CELL BIOLOGY 109: 3259 (1989).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "crossref",
      "first-page": "2687",
      "DOI": "10.1002/j.1460-2075.1984.tb02194.x",
      "volume": "3",
      "year": "1984",
      "unstructured": "PFEIFFER, S.E., EMBO J 3: 2687 (1984).",
      "journal-title": "EMBO J"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "crossref",
      "first-page": "413",
      "DOI": "10.1164/ajrccm/138.2.413",
      "volume": "138",
      "year": "1988",
      "unstructured": "RAPHAEL, G.D., PATHO-PHYSIOLOGY OF RHINITIS .1. ASSESSMENT OF THE SOURCES OF PROTEIN IN METHACHOLINE-INDUCED NASAL SECRETIONS, AMERICAN REVIEW OF RESPIRATORY DISEASE 138: 413 (1988).",
      "journal-title": "AMERICAN REVIEW OF RESPIRATORY DISEASE"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "crossref",
      "first-page": "S159",
      "DOI": "10.1083/jcb.99.1.159s",
      "volume": "99",
      "year": "1984",
      "unstructured": "RODEWALD, R, RECEPTOR-MEDIATED TRANSPORT OF IGG, JOURNAL OF CELL BIOLOGY 99: S159 (1984).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "crossref",
      "first-page": "93",
      "DOI": "10.3109/10409238309102791",
      "volume": "14",
      "year": "1983",
      "unstructured": "SCHLESSINGER, J, REGULATION OF CELL-PROLIFERATION BY EPIDERMAL GROWTH-FACTOR, CRC CRITICAL REVIEWS IN BIOCHEMISTRY 14: 93 (1983).",
      "journal-title": "CRC CRITICAL REVIEWS IN BIOCHEMISTRY"
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "crossref",
      "first-page": "184",
      "DOI": "10.1038/337184a0",
      "volume": "337",
      "year": "1989",
      "unstructured": "SIMISTER, N.E., AN FC RECEPTOR STRUCTURALLY RELATED TO MHC CLASS-I ANTIGENS, NATURE 337: 184 (1989).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_33_1",
      "doi-asserted-by": "crossref",
      "first-page": "6197",
      "DOI": "10.1021/bi00417a001",
      "volume": "27",
      "year": "1988",
      "unstructured": "SIMONS, K, LIPID SORTING IN EPITHELIAL-CELLS, BIOCHEMISTRY 27: 6197 (1988).",
      "journal-title": "BIOCHEMISTRY"
    },
    {
      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "crossref",
      "first-page": "1255",
      "DOI": "10.1083/jcb.100.4.1255",
      "volume": "100",
      "year": "1985",
      "unstructured": "SZTUL, E.S., BIOGENESIS OF THE POLYMERIC IGA RECEPTOR IN RAT HEPATOCYTES .2. LOCALIZATION OF ITS INTRACELLULAR FORMS BY CELL FRACTIONATION STUDIES, JOURNAL OF CELL BIOLOGY 100: 1255 (1985).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "crossref",
      "first-page": "10422",
      "DOI": "10.1016/S0021-9258(18)60975-5",
      "volume": "262",
      "year": "1987",
      "unstructured": "THORSNESS, P.E., INACTIVATION OF ISOCITRATE DEHYDROGENASE BY PHOSPHORYLATION IS MEDIATED BY THE NEGATIVE CHARGE OF THE PHOSPHATE, JOURNAL OF BIOLOGICAL CHEMISTRY 262: 10422 (1987).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_36_1",
      "doi-asserted-by": "crossref",
      "first-page": "2735",
      "DOI": "10.1083/jcb.105.6.2735",
      "volume": "105",
      "year": "1987",
      "unstructured": "URBAN, J, CONSTITUTIVE APICAL SECRETION OF AN 80-KD SULFATED GLYCOPROTEIN COMPLEX IN THE POLARIZED EPITHELIAL MADIN-DARBY CANINE KIDNEY-CELL LINE, JOURNAL OF CELL BIOLOGY 105: 2735 (1987).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_37_1",
      "doi-asserted-by": "crossref",
      "first-page": "2781",
      "DOI": "10.1002/j.1460-2075.1985.tb04004.x",
      "volume": "4",
      "year": "1985",
      "unstructured": "VONBONSDORFF, C.H., APICAL AND BASOLATERAL ENDOCYTOSIS IN MADIN-DARBY CANINE KIDNEY (MDCK) CELLS GROWN ON NITROCELLULOSE FILTERS, EMBO JOURNAL 4: 2781 (1985).",
      "journal-title": "EMBO JOURNAL"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.2110383",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        12
      ]
    ],
    "date-time": "2024-01-12T09:17:54Z",
    "timestamp": 1705051074000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.2110383"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1990,
        5,
        11
      ]
    ]
  },
  "references-count": 37,
  "journal-issue": {
    "issue": "4956",
    "published-print": {
      "date-parts": [
        [
          1990,
          5,
          11
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.2110383"
  ],
  "URL": "http://dx.doi.org/10.1126/science.2110383",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1990,
        5,
        11
      ]
    ]
  }
}