DOI: 10.1083/jcb.139.5.1209. Role for a Glycan Phosphoinositol Anchor in Fcγ Receptor Synergy [Penn]

Role for a Glycan Phosphoinositol Anchor in Fcγ Receptor Synergy

10.1083/jcb.139.5.1209

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

While many cell types express receptors for the Fc domain of IgG (FcγR), only primate polymorphonuclear neutrophils (PMN) express an FcγR linked to the membrane via a glycan phosphoinositol (GPI) anchor. Previous studies have demonstrated that this GPI-linked FcγR (FcγRIIIB) cooperates with the transmembrane FcγR (FcγRIIA) to mediate many of the functional effects of immune complex binding. To determine the role of the GPI anchor in Fcγ receptor synergy, we have developed a model system in Jurkat T cells, which lack endogenously expressed Fcγ receptors. Jurkat T cells were stably transfected with cDNA encoding FcγRIIA and/or FcγRIIIB. Cocrosslinking the two receptors produced a synergistic rise in intracytoplasmic calcium ([Ca2+]i) to levels not reached by stimulation of either FcγRIIA or FcγRIIIB alone. Synergy was achieved by prolonged entry of extracellular Ca2+. Cocrosslinking FcγRIIA with CD59 or CD48, two other GPI-linked proteins on Jurkat T cells also led to a synergistic [Ca2+]i rise, as did crosslinking CD59 with FcγRIIA on PMN, suggesting that interactions between the extracellular domains of the two Fcγ receptors are not required for synergy. Replacement of the GPI anchor of FcγRIIIB with a transmembrane anchor abolished synergy. In addition, tyrosine to phenylalanine substitutions in the immunoreceptor tyrosine-based activation motif (ITAM) of the FcγRIIA cytoplasmic tail abolished synergy. While the ITAM of FcγRIIA was required for the increase in [Ca2+]i, tyrosine phosphorylation of crosslinked FcγRIIA was diminished when cocrosslinked with FcγRIIIB. These data demonstrate that FcγRIIA association with GPI-linked proteins facilitates FcγR signal transduction and suggest that this may be a physiologically significant role for the unusual GPI-anchored FcγR of human PMN.

Bibliography

Green, J. M., Schreiber, A. D., & Brown, E. J. (1997). Role for a Glycan Phosphoinositol Anchor in FcÎ³ Receptor Synergy. The Journal of Cell Biology, 139(5), 1209â1217.

Authors 3

Jennifer M. Green (first)
Alan D. Schreiber (additional)
Eric J. Brown (additional)

References 49 Referenced 43

10.1084/jem.171.4.1333 / J Exp Med / Phagocytosis mediated by three distinct Fc γ receptor classes on human leukocytes by Anderson (1990)
{'key': '2023072207263265100_B2', 'first-page': '49', 'article-title': 'Actin dynamics in human neutrophils during adhesion and phagocytosis is controlled by changes in intracellular free calcium', 'volume': '62', 'author': 'Bengtsson', 'year': '1993', 'journal-title': 'Eur J Cell Biol'} / Eur J Cell Biol / Actin dynamics in human neutrophils during adhesion and phagocytosis is controlled by changes in intracellular free calcium by Bengtsson (1993)
10.4049/jimmunol.135.2.1342 / J Immunol / Calcium requirements for increased complement receptor expression during neutrophil activation by Berger (1985)
10.1016/0952-7915(93)90052-T / Curr Opin Immunol / The tyrosine kinase connection: how GPI anchored proteins activate T cells by Brown (1993)
10.1016/S0091-679X(08)61850-6 / Methods Cell Biol / In vitro assays of phagocytic function of human peripheral blood leukocytes: receptor modulation and signal transduction by Brown (1994)
10.1038/380634a0 / Nature / Calcium mobilization via sphingosine kinase in signaling by the FcεRI antigen receptor by Choi (1996)
10.1002/eji.1830210820 / Eur J Immunol / A single amino acid distinguishes the high-responder from the low-responder form of Fc receptor II on human monocytes by Clark (1991)
10.4049/jimmunol.149.9.2906 / J Immunol / Mapping of epitopes, glycosylation sites, and complement regulatory domains in human decay accelerating factor by Coyne (1992)
10.1073/pnas.79.10.3275 / Proc Natl Acad Sci USA / Human neutrophil Fc γ receptor distribution and structure by Fleit (1982)
10.1083/jcb.120.5.1147 / J Cell Biol / Calcium pump of the plasma membrane is localized in caveolae by Fujimoto (1993)
10.1016/S0021-9258(18)42789-5 / J Biol Chem / Activation of FcγRII induces tyrosine phosphorylation of multiple proteins including FcγRII by Huang (1992)
{'key': '2023072207263265100_B12'}
10.4049/jimmunol.142.7.2365 / J Immunol / The 40-kDa Fc γ receptor (FcγRII) on human neutrophils is essential for the IgG-induced respiratory burst and IgG-induced phagocytosis by Huizinga (1989)
10.1002/eji.1830220327 / Eur J Immunol / The glycosylphosphatidylinositol-linked Fcγ receptor III represents the dominant receptor structure for immune complex activation of neutrophils by Hundt (1992)
10.1073/pnas.91.21.10232 / Proc Natl Acad Sci USA / Transfection of an Fcγ receptor cDNA induces T cells to become phagocytic by Hunter (1994)
10.1182/blood.V86.12.4389.bloodjournal86124389 / Blood / The molecular dissection of Fcγ receptor mediated phagocytosis by Indik (1995)
10.1083/jcb.110.5.1555 / J Cell Biol / Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils by Jaconi (1990)
10.1007/BF02072084 / Eur J Pediatr / Cytosolic free Ca2+signals in single adherent human neutrophils: generation and functional role by Jaconi (1993)
10.1084/jem.171.4.1239 / J Exp Med / The glycosyl phosphatidylinositol-linked FcγRIII on PMN mediates transmembrane signaling events distinct from FcγRII by Kimberly (1990)
10.1016/0092-8674(93)90304-9 / Cell / T cell activation by clustered tyrosine kinases by Kolanus (1993)
10.4049/jimmunol.153.4.1769 / J Immunol / Reconstitution of antibody-dependent phagocytosis in fibroblasts expressing FcγRIIIB and the complement receptor type 3 by Krauss (1994)
10.1016/0167-5699(96)80585-8 / Immunol Today / Inhibitory MHC class I receptors on NK cells and T cells by Lanier (1996)
10.1083/jcb.102.6.2197 / J Cell Biol / Quantitative analysis of the cytosolic free calcium dependency of exocytosis from three subcellular compartments in intact human neutrophils by Lew (1986)
10.1083/jcb.123.2.485 / J Cell Biol / Molecular cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane spanning domains implicated in αvβ3-dependent ligand binding by Lindberg (1993)
10.1016/0092-8674(94)90148-1 / Cell / Lipid second messengers by Liscovitch (1994)
10.1084/jem.163.4.826 / J Exp Med / Identification of a second class of IgG Fc receptors on human neutrophils. A 40-kilodalton molecule also found on eosinophils by Looney (1986)
10.1182/blood.V84.6.1753.1753 / Blood / Substitutions and deletions in the cytoplasmic domain of the phagocytic receptor FcγRIIA: effect on receptor tyrosine phosphorylation and phagocytosis by Mitchell (1994)
10.1126/science.1837175 / Science / Regulation of phagocytosis and [Ca2+]iflux by distinct regions of an Fc receptor by Odin (1991)
10.1126/science.7660120 / Science / Digging into caveolae by Parton (1995)
10.1016/0167-5699(96)30013-3 / Immunol Today / Integrins as promiscuous signal transduction devices by Petty (1996)
10.1126/science.7716542 / Science / Superantigen-dependent, cell-mediated cytotoxicty inhibited by MHC class I receptors on T lymphocytes by Phillips (1995)
10.1084/jem.170.2.481 / J Exp Med / Alternative membrane forms of FcγRIII (CD16) on human natural killer cells and neutrophils: cell type-specific expression of two genes that differ in single nucleotide substitutions by Ravetch (1989)
10.1146/annurev.iy.09.040191.002325 / Annu Rev Immunol / Fc receptors by Ravetch (1991)
10.1083/jcb.135.6.1515 / J Cell Biol / Exclusion of CD45 inhibits activity of p56 associated with glycolipid-enriched membrane domains by Rodgers (1996)
10.4049/jimmunol.146.11.3937 / J Immunol / Two mechanisms for IgG Fc-receptor-mediated phagocytosis by human neutrophils by Rosales (1991)
10.1016/S0021-9258(18)42761-5 / J Biol Chem / Signal transduction by neutrophil immunoglobulin G Fc receptors. Dissociation of [Ca2+] rise from IP3 by Rosales (1992)
10.1016/S0021-9258(18)45965-0 / J Biol Chem / Calcium channel blockers nifedipine and diltiazem inhibit Ca2+release from intracellular stores in neutrophils by Rosales (1992)
{'key': '2023072207263265100_B38'}
10.4049/jimmunol.146.3.997 / J Immunol / Fcγ receptor III induces actin polymerization in human neutrophils and primes phagocytosis mediated by Fcγ receptor II by Salmon (1991)
10.4049/jimmunol.150.10.4571 / J Immunol / Lectin-like inhibition of immune-complex receptor-mediated stimulation of neutrophils: effects on cytosolic calcium release and superoxide production by Sehgal (1993)
10.1006/excr.1995.1028 / Exp Cell Res / Distinct mechanisms for Ca2+ entry induced by OKT3 and Ca2+depletion in Jurkat T cells by Sei (1995)
10.4049/jimmunol.152.6.3017 / J Immunol / Correlations among tyrosine phosphorylation of Shc, p72syk, PLC-γ1, and [Ca2+]iflux in FcγRIIA signaling by Shen (1994)
10.1126/science.1719635 / Science / GPI-anchored cell-surface molecules complexed to protein tyrosine kinases by Stefanova (1991)
10.1074/jbc.270.18.10671 / J Biol Chem / Heterotypic FcγR clusters evoke a synergistic Ca2+response in human neutrophils by Vossebeld (1995)
10.1084/jem.170.2.431 / J Exp Med / Leukocyte function- associated antigen 1 is an activation molecule for human T cells by Wacholtz (1989)
10.1126/science.273.5281.1551 / Science / Regulation of integrin function by the urokinase receptor by Wei (1996)
10.1083/jcb.125.6.1407 / J Cell Biol / CR3 (Mac-1, aMb2, CD11b/CD18) and FcγRIII cooperate in generation of a neutrophil respiratory burst: requirement for FcγRII and tyrosine phosphorylation by Zhou (1994)
10.4049/jimmunol.150.7.3030 / J Immunol / Cocapping of the leukoadhesin molecules complement receptor type 3 and lymphocyte function-associated antigen-1 with Fcγ receptor III on human neutrophils: possible role of lectin-like interactions by Zhou (1993)
10.1074/jbc.270.22.13553 / J Biol Chem / Distinct tyrosine kinase activation and Triton X-100 insolubility upon FcγRII or FcγRIIIB ligation in human polymorphonuclear leukocytes: implications for immune complex activation of the respiratory burst by Zhou (1995)

Dates

Type	When
Created	23 years ago (July 26, 2002, 12:47 p.m.)
Deposited	2 years, 1 month ago (July 22, 2023, 3:27 a.m.)
Indexed	1 month, 2 weeks ago (July 6, 2025, 1:25 p.m.)
Issued	27 years, 8 months ago (Dec. 1, 1997)
Published	27 years, 8 months ago (Dec. 1, 1997)
Published Online	27 years, 8 months ago (Dec. 1, 1997)
Published Print	27 years, 8 months ago (Dec. 1, 1997)

Funders 0

None

BibTeX

@article{Green_1997, title={Role for a Glycan Phosphoinositol Anchor in Fcγ Receptor Synergy}, volume={139}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.139.5.1209}, DOI={10.1083/jcb.139.5.1209}, number={5}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Green, Jennifer M. and Schreiber, Alan D. and Brown, Eric J.}, year={1997}, month=dec, pages={1209–1217} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        6
      ]
    ],
    "date-time": "2025-07-06T17:25:51Z",
    "timestamp": 1751822751995
  },
  "reference-count": 49,
  "publisher": "Rockefeller University Press",
  "issue": "5",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1997,
        12,
        1
      ]
    ]
  },
  "abstract": "<jats:p>While many cell types express receptors for the Fc domain of IgG (Fc\u03b3R), only primate polymorphonuclear neutrophils (PMN) express an Fc\u03b3R linked to the membrane via a glycan phosphoinositol (GPI) anchor. Previous studies have demonstrated that this GPI-linked Fc\u03b3R (Fc\u03b3RIIIB) cooperates with the transmembrane Fc\u03b3R (Fc\u03b3RIIA) to mediate many of the functional effects of immune complex binding. To determine the role of the GPI anchor in Fc\u03b3 receptor synergy, we have developed a model system in Jurkat T cells, which lack endogenously expressed Fc\u03b3 receptors. Jurkat T cells were stably transfected with cDNA encoding Fc\u03b3RIIA and/or Fc\u03b3RIIIB. Cocrosslinking the two receptors produced a synergistic rise in intracytoplasmic calcium ([Ca2+]i) to levels not reached by stimulation of either Fc\u03b3RIIA or Fc\u03b3RIIIB alone. Synergy was achieved by prolonged entry of extracellular Ca2+. Cocrosslinking Fc\u03b3RIIA with CD59 or CD48, two other GPI-linked proteins on Jurkat T cells also led to a synergistic [Ca2+]i rise, as did crosslinking CD59 with Fc\u03b3RIIA on PMN, suggesting that interactions between the extracellular domains of the two Fc\u03b3 receptors are not required for synergy. Replacement of the GPI anchor of Fc\u03b3RIIIB with a transmembrane anchor abolished synergy. In addition, tyrosine to phenylalanine substitutions in the immunoreceptor tyrosine-based activation motif (ITAM) of the Fc\u03b3RIIA cytoplasmic tail abolished synergy. While the ITAM of Fc\u03b3RIIA was required for the increase in [Ca2+]i, tyrosine phosphorylation of crosslinked Fc\u03b3RIIA was diminished when cocrosslinked with Fc\u03b3RIIIB. These data demonstrate that Fc\u03b3RIIA association with GPI-linked proteins facilitates Fc\u03b3R signal transduction and suggest that this may be a physiologically significant role for the unusual GPI-anchored Fc\u03b3R of human PMN.</jats:p>",
  "DOI": "10.1083/jcb.139.5.1209",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:47:50Z",
    "timestamp": 1027702070000
  },
  "page": "1209-1217",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 43,
  "title": "Role for a Glycan Phosphoinositol Anchor in Fc\u03b3 Receptor Synergy",
  "prefix": "10.1083",
  "volume": "139",
  "author": [
    {
      "given": "Jennifer M.",
      "family": "Green",
      "sequence": "first",
      "affiliation": [
        {
          "name": "*Division of Infectious Diseases, Washington University, School of Medicine, St. Louis, Missouri 63110; and \u2021Department of Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104"
        }
      ]
    },
    {
      "given": "Alan D.",
      "family": "Schreiber",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "*Division of Infectious Diseases, Washington University, School of Medicine, St. Louis, Missouri 63110; and \u2021Department of Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104"
        }
      ]
    },
    {
      "given": "Eric J.",
      "family": "Brown",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "*Division of Infectious Diseases, Washington University, School of Medicine, St. Louis, Missouri 63110; and \u2021Department of Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        1997,
        12,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072207263265100_B1",
      "doi-asserted-by": "crossref",
      "first-page": "1333",
      "DOI": "10.1084/jem.171.4.1333",
      "article-title": "Phagocytosis mediated by three distinct Fc \u03b3 receptor classes on human leukocytes",
      "volume": "171",
      "author": "Anderson",
      "year": "1990",
      "journal-title": "J Exp Med"
    },
    {
      "key": "2023072207263265100_B2",
      "first-page": "49",
      "article-title": "Actin dynamics in human neutrophils during adhesion and phagocytosis is controlled by changes in intracellular free calcium",
      "volume": "62",
      "author": "Bengtsson",
      "year": "1993",
      "journal-title": "Eur J Cell Biol"
    },
    {
      "key": "2023072207263265100_B3",
      "doi-asserted-by": "crossref",
      "first-page": "1342",
      "DOI": "10.4049/jimmunol.135.2.1342",
      "article-title": "Calcium requirements for increased complement receptor expression during neutrophil activation",
      "volume": "135",
      "author": "Berger",
      "year": "1985",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B4",
      "doi-asserted-by": "crossref",
      "first-page": "349",
      "DOI": "10.1016/0952-7915(93)90052-T",
      "article-title": "The tyrosine kinase connection: how GPI anchored proteins activate T cells",
      "volume": "5",
      "author": "Brown",
      "year": "1993",
      "journal-title": "Curr Opin Immunol"
    },
    {
      "key": "2023072207263265100_B5",
      "doi-asserted-by": "crossref",
      "first-page": "147",
      "DOI": "10.1016/S0091-679X(08)61850-6",
      "article-title": "In vitro assays of phagocytic function of human peripheral blood leukocytes: receptor modulation and signal transduction",
      "volume": "45",
      "author": "Brown",
      "year": "1994",
      "journal-title": "Methods Cell Biol"
    },
    {
      "key": "2023072207263265100_B6",
      "doi-asserted-by": "crossref",
      "first-page": "634",
      "DOI": "10.1038/380634a0",
      "article-title": "Calcium mobilization via sphingosine kinase in signaling by the Fc\u03b5RI antigen receptor",
      "volume": "380",
      "author": "Choi",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2023072207263265100_B7",
      "doi-asserted-by": "crossref",
      "first-page": "1911",
      "DOI": "10.1002/eji.1830210820",
      "article-title": "A single amino acid distinguishes the high-responder from the low-responder form of Fc receptor II on human monocytes",
      "volume": "21",
      "author": "Clark",
      "year": "1991",
      "journal-title": "Eur J Immunol"
    },
    {
      "key": "2023072207263265100_B8",
      "doi-asserted-by": "crossref",
      "first-page": "2906",
      "DOI": "10.4049/jimmunol.149.9.2906",
      "article-title": "Mapping of epitopes, glycosylation sites, and complement regulatory domains in human decay accelerating factor",
      "volume": "149",
      "author": "Coyne",
      "year": "1992",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B9",
      "doi-asserted-by": "crossref",
      "first-page": "3275",
      "DOI": "10.1073/pnas.79.10.3275",
      "article-title": "Human neutrophil Fc \u03b3 receptor distribution and structure",
      "volume": "79",
      "author": "Fleit",
      "year": "1982",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072207263265100_B10",
      "doi-asserted-by": "crossref",
      "first-page": "1147",
      "DOI": "10.1083/jcb.120.5.1147",
      "article-title": "Calcium pump of the plasma membrane is localized in caveolae",
      "volume": "120",
      "author": "Fujimoto",
      "year": "1993",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072207263265100_B11",
      "doi-asserted-by": "crossref",
      "first-page": "5467",
      "DOI": "10.1016/S0021-9258(18)42789-5",
      "article-title": "Activation of Fc\u03b3RII induces tyrosine phosphorylation of multiple proteins including Fc\u03b3RII",
      "volume": "267",
      "author": "Huang",
      "year": "1992",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072207263265100_B12"
    },
    {
      "key": "2023072207263265100_B13",
      "doi-asserted-by": "crossref",
      "first-page": "2365",
      "DOI": "10.4049/jimmunol.142.7.2365",
      "article-title": "The 40-kDa Fc \u03b3 receptor (Fc\u03b3RII) on human neutrophils is essential for the IgG-induced respiratory burst and IgG-induced phagocytosis",
      "volume": "142",
      "author": "Huizinga",
      "year": "1989",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B14",
      "doi-asserted-by": "crossref",
      "first-page": "811",
      "DOI": "10.1002/eji.1830220327",
      "article-title": "The glycosylphosphatidylinositol-linked Fc\u03b3 receptor III represents the dominant receptor structure for immune complex activation of neutrophils",
      "volume": "22",
      "author": "Hundt",
      "year": "1992",
      "journal-title": "Eur J Immunol"
    },
    {
      "key": "2023072207263265100_B15",
      "doi-asserted-by": "crossref",
      "first-page": "10232",
      "DOI": "10.1073/pnas.91.21.10232",
      "article-title": "Transfection of an Fc\u03b3 receptor cDNA induces T cells to become phagocytic",
      "volume": "91",
      "author": "Hunter",
      "year": "1994",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072207263265100_B16",
      "doi-asserted-by": "crossref",
      "first-page": "4389",
      "DOI": "10.1182/blood.V86.12.4389.bloodjournal86124389",
      "article-title": "The molecular dissection of Fc\u03b3 receptor mediated phagocytosis",
      "volume": "86",
      "author": "Indik",
      "year": "1995",
      "journal-title": "Blood"
    },
    {
      "key": "2023072207263265100_B17",
      "doi-asserted-by": "crossref",
      "first-page": "1555",
      "DOI": "10.1083/jcb.110.5.1555",
      "article-title": "Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils",
      "volume": "110",
      "author": "Jaconi",
      "year": "1990",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072207263265100_B18",
      "doi-asserted-by": "crossref",
      "first-page": "S26",
      "DOI": "10.1007/BF02072084",
      "article-title": "Cytosolic free Ca2+signals in single adherent human neutrophils: generation and functional role",
      "volume": "152",
      "author": "Jaconi",
      "year": "1993",
      "journal-title": "Eur J Pediatr"
    },
    {
      "key": "2023072207263265100_B19",
      "doi-asserted-by": "crossref",
      "first-page": "1239",
      "DOI": "10.1084/jem.171.4.1239",
      "article-title": "The glycosyl phosphatidylinositol-linked Fc\u03b3RIII on PMN mediates transmembrane signaling events distinct from Fc\u03b3RII",
      "volume": "171",
      "author": "Kimberly",
      "year": "1990",
      "journal-title": "J Exp Med"
    },
    {
      "key": "2023072207263265100_B20",
      "doi-asserted-by": "crossref",
      "first-page": "171",
      "DOI": "10.1016/0092-8674(93)90304-9",
      "article-title": "T cell activation by clustered tyrosine kinases",
      "volume": "74",
      "author": "Kolanus",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2023072207263265100_B21",
      "doi-asserted-by": "crossref",
      "first-page": "1769",
      "DOI": "10.4049/jimmunol.153.4.1769",
      "article-title": "Reconstitution of antibody-dependent phagocytosis in fibroblasts expressing Fc\u03b3RIIIB and the complement receptor type 3",
      "volume": "153",
      "author": "Krauss",
      "year": "1994",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B22",
      "doi-asserted-by": "crossref",
      "first-page": "86",
      "DOI": "10.1016/0167-5699(96)80585-8",
      "article-title": "Inhibitory MHC class I receptors on NK cells and T cells",
      "volume": "17",
      "author": "Lanier",
      "year": "1996",
      "journal-title": "Immunol Today"
    },
    {
      "key": "2023072207263265100_B23",
      "doi-asserted-by": "crossref",
      "first-page": "2197",
      "DOI": "10.1083/jcb.102.6.2197",
      "article-title": "Quantitative analysis of the cytosolic free calcium dependency of exocytosis from three subcellular compartments in intact human neutrophils",
      "volume": "102",
      "author": "Lew",
      "year": "1986",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072207263265100_B24",
      "doi-asserted-by": "crossref",
      "first-page": "485",
      "DOI": "10.1083/jcb.123.2.485",
      "article-title": "Molecular cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane spanning domains implicated in \u03b1v\u03b23-dependent ligand binding",
      "volume": "123",
      "author": "Lindberg",
      "year": "1993",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072207263265100_B25",
      "doi-asserted-by": "crossref",
      "first-page": "329",
      "DOI": "10.1016/0092-8674(94)90148-1",
      "article-title": "Lipid second messengers",
      "volume": "77",
      "author": "Liscovitch",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "2023072207263265100_B26",
      "doi-asserted-by": "crossref",
      "first-page": "826",
      "DOI": "10.1084/jem.163.4.826",
      "article-title": "Identification of a second class of IgG Fc receptors on human neutrophils. A 40-kilodalton molecule also found on eosinophils",
      "volume": "163",
      "author": "Looney",
      "year": "1986",
      "journal-title": "J Exp Med"
    },
    {
      "key": "2023072207263265100_B27",
      "doi-asserted-by": "crossref",
      "first-page": "1753",
      "DOI": "10.1182/blood.V84.6.1753.1753",
      "article-title": "Substitutions and deletions in the cytoplasmic domain of the phagocytic receptor Fc\u03b3RIIA: effect on receptor tyrosine phosphorylation and phagocytosis",
      "volume": "84",
      "author": "Mitchell",
      "year": "1994",
      "journal-title": "Blood"
    },
    {
      "key": "2023072207263265100_B28",
      "doi-asserted-by": "crossref",
      "first-page": "1785",
      "DOI": "10.1126/science.1837175",
      "article-title": "Regulation of phagocytosis and [Ca2+]iflux by distinct regions of an Fc receptor",
      "volume": "254",
      "author": "Odin",
      "year": "1991",
      "journal-title": "Science"
    },
    {
      "key": "2023072207263265100_B29",
      "doi-asserted-by": "crossref",
      "first-page": "1398",
      "DOI": "10.1126/science.7660120",
      "article-title": "Digging into caveolae",
      "volume": "269",
      "author": "Parton",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "2023072207263265100_B30",
      "doi-asserted-by": "crossref",
      "first-page": "209",
      "DOI": "10.1016/0167-5699(96)30013-3",
      "article-title": "Integrins as promiscuous signal transduction devices",
      "volume": "17",
      "author": "Petty",
      "year": "1996",
      "journal-title": "Immunol Today"
    },
    {
      "key": "2023072207263265100_B31",
      "doi-asserted-by": "crossref",
      "first-page": "403",
      "DOI": "10.1126/science.7716542",
      "article-title": "Superantigen-dependent, cell-mediated cytotoxicty inhibited by MHC class I receptors on T lymphocytes",
      "volume": "268",
      "author": "Phillips",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "2023072207263265100_B32",
      "doi-asserted-by": "crossref",
      "first-page": "481",
      "DOI": "10.1084/jem.170.2.481",
      "article-title": "Alternative membrane forms of Fc\u03b3RIII (CD16) on human natural killer cells and neutrophils: cell type-specific expression of two genes that differ in single nucleotide substitutions",
      "volume": "170",
      "author": "Ravetch",
      "year": "1989",
      "journal-title": "J Exp Med"
    },
    {
      "key": "2023072207263265100_B33",
      "doi-asserted-by": "crossref",
      "first-page": "457",
      "DOI": "10.1146/annurev.iy.09.040191.002325",
      "article-title": "Fc receptors",
      "volume": "9",
      "author": "Ravetch",
      "year": "1991",
      "journal-title": "Annu Rev Immunol"
    },
    {
      "key": "2023072207263265100_B34",
      "doi-asserted-by": "crossref",
      "first-page": "1515",
      "DOI": "10.1083/jcb.135.6.1515",
      "article-title": "Exclusion of CD45 inhibits activity of p56 associated with glycolipid-enriched membrane domains",
      "volume": "135",
      "author": "Rodgers",
      "year": "1996",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072207263265100_B35",
      "doi-asserted-by": "crossref",
      "first-page": "3937",
      "DOI": "10.4049/jimmunol.146.11.3937",
      "article-title": "Two mechanisms for IgG Fc-receptor-mediated phagocytosis by human neutrophils",
      "volume": "146",
      "author": "Rosales",
      "year": "1991",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B36",
      "doi-asserted-by": "crossref",
      "first-page": "5265",
      "DOI": "10.1016/S0021-9258(18)42761-5",
      "article-title": "Signal transduction by neutrophil immunoglobulin G Fc receptors. Dissociation of [Ca2+] rise from IP3",
      "volume": "267",
      "author": "Rosales",
      "year": "1992",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072207263265100_B37",
      "doi-asserted-by": "crossref",
      "first-page": "1443",
      "DOI": "10.1016/S0021-9258(18)45965-0",
      "article-title": "Calcium channel blockers nifedipine and diltiazem inhibit Ca2+release from intracellular stores in neutrophils",
      "volume": "267",
      "author": "Rosales",
      "year": "1992",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072207263265100_B38"
    },
    {
      "key": "2023072207263265100_B39",
      "doi-asserted-by": "crossref",
      "first-page": "997",
      "DOI": "10.4049/jimmunol.146.3.997",
      "article-title": "Fc\u03b3 receptor III induces actin polymerization in human neutrophils and primes phagocytosis mediated by Fc\u03b3 receptor II",
      "volume": "146",
      "author": "Salmon",
      "year": "1991",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B40",
      "doi-asserted-by": "crossref",
      "first-page": "4571",
      "DOI": "10.4049/jimmunol.150.10.4571",
      "article-title": "Lectin-like inhibition of immune-complex receptor-mediated stimulation of neutrophils: effects on cytosolic calcium release and superoxide production",
      "volume": "150",
      "author": "Sehgal",
      "year": "1993",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B41",
      "doi-asserted-by": "crossref",
      "first-page": "222",
      "DOI": "10.1006/excr.1995.1028",
      "article-title": "Distinct mechanisms for Ca2+ entry induced by OKT3 and Ca2+depletion in Jurkat T cells",
      "volume": "216",
      "author": "Sei",
      "year": "1995",
      "journal-title": "Exp Cell Res"
    },
    {
      "key": "2023072207263265100_B42",
      "doi-asserted-by": "crossref",
      "first-page": "3017",
      "DOI": "10.4049/jimmunol.152.6.3017",
      "article-title": "Correlations among tyrosine phosphorylation of Shc, p72syk, PLC-\u03b31, and [Ca2+]iflux in Fc\u03b3RIIA signaling",
      "volume": "152",
      "author": "Shen",
      "year": "1994",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B43",
      "doi-asserted-by": "crossref",
      "first-page": "1016",
      "DOI": "10.1126/science.1719635",
      "article-title": "GPI-anchored cell-surface molecules complexed to protein tyrosine kinases",
      "volume": "254",
      "author": "Stefanova",
      "year": "1991",
      "journal-title": "Science"
    },
    {
      "key": "2023072207263265100_B44",
      "doi-asserted-by": "crossref",
      "first-page": "10671",
      "DOI": "10.1074/jbc.270.18.10671",
      "article-title": "Heterotypic Fc\u03b3R clusters evoke a synergistic Ca2+response in human neutrophils",
      "volume": "270",
      "author": "Vossebeld",
      "year": "1995",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072207263265100_B45",
      "doi-asserted-by": "crossref",
      "first-page": "431",
      "DOI": "10.1084/jem.170.2.431",
      "article-title": "Leukocyte function- associated antigen 1 is an activation molecule for human T cells",
      "volume": "170",
      "author": "Wacholtz",
      "year": "1989",
      "journal-title": "J Exp Med"
    },
    {
      "key": "2023072207263265100_B46",
      "doi-asserted-by": "crossref",
      "first-page": "1551",
      "DOI": "10.1126/science.273.5281.1551",
      "article-title": "Regulation of integrin function by the urokinase receptor",
      "volume": "273",
      "author": "Wei",
      "year": "1996",
      "journal-title": "Science"
    },
    {
      "key": "2023072207263265100_B47",
      "doi-asserted-by": "crossref",
      "first-page": "1407",
      "DOI": "10.1083/jcb.125.6.1407",
      "article-title": "CR3 (Mac-1, aMb2, CD11b/CD18) and Fc\u03b3RIII cooperate in generation of a neutrophil respiratory burst: requirement for Fc\u03b3RII and tyrosine phosphorylation",
      "volume": "125",
      "author": "Zhou",
      "year": "1994",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072207263265100_B48",
      "doi-asserted-by": "crossref",
      "first-page": "3030",
      "DOI": "10.4049/jimmunol.150.7.3030",
      "article-title": "Cocapping of the leukoadhesin molecules complement receptor type 3 and lymphocyte function-associated antigen-1 with Fc\u03b3 receptor III on human neutrophils: possible role of lectin-like interactions",
      "volume": "150",
      "author": "Zhou",
      "year": "1993",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072207263265100_B49",
      "doi-asserted-by": "crossref",
      "first-page": "13553",
      "DOI": "10.1074/jbc.270.22.13553",
      "article-title": "Distinct tyrosine kinase activation and Triton X-100 insolubility upon Fc\u03b3RII or Fc\u03b3RIIIB ligation in human polymorphonuclear leukocytes: implications for immune complex activation of the respiratory burst",
      "volume": "270",
      "author": "Zhou",
      "year": "1995",
      "journal-title": "J Biol Chem"
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/139/5/1209/1489246/12436.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/139/5/1209/1489246/12436.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        22
      ]
    ],
    "date-time": "2023-07-22T07:27:12Z",
    "timestamp": 1690010832000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/139/5/1209/756/Role-for-a-Glycan-Phosphoinositol-Anchor-in-Fc"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1997,
        12,
        1
      ]
    ]
  },
  "references-count": 49,
  "journal-issue": {
    "issue": "5",
    "published-print": {
      "date-parts": [
        [
          1997,
          12,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.139.5.1209",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1997,
        12,
        1
      ]
    ]
  }
}