DOI: 10.1189/jlb.0308171. CSF-1 receptor structure/function in MacCsf1r–/– macrophages: regulation of proliferation, differentiation, and morphology

CSF-1 receptor structure/function in MacCsf1r–/– macrophages: regulation of proliferation, differentiation, and morphology

10.1189/jlb.0308171

Crossref journal-article

Oxford University Press (OUP)

Journal of Leukocyte Biology (286)

Abstract

AbstractCSF-1 is the major regulator of tissue macrophage development and function. A GM-CSF-dependent, CSF-1 receptor (CSF-1R)-deficient F4/80hiMac-1+Gr1–CD11c+ bone marrow macrophage (BMM) line (MacCsf1r−/−) was developed to study the roles of the eight intracellular CSF-1R tyrosines phosphorylated upon receptor activation. Retroviral expression of the wild-type CSF-1R rescued the CSF-1-induced survival, proliferation, differentiation, and morphological characteristics of primary BMM. Mutation of all eight tyrosines failed to rescue, whereas the individual Y → F mutants (544, 559, 697, 706, 721, 807, 921, 974) rescued these CSF-1-inducible phenotypes to varying degrees. The juxtamembrane domain Y559F and activation loop Y807F mutations severely compromised proliferation and differentiation, whereas Y706, Y721F, and Y974F mutations altered morphological responses, and Y706F increased differentiation. Despite their retention of significant in vitro tyrosine kinase activity, Y559F and Y807F mutants exhibited severely impaired in vivo receptor tyrosine phosphorylation, consistent with the existence of cellular mechanisms inhibiting CSF-1R tyrosine phosphorylation that are relieved by phosphorylation of these two sites. The MacCsf1r−/− macrophage line will facilitate genetic and proteomic approaches to CSF-1R structure/function studies in the major disease-related CSF-1R-expressing cell type.

Bibliography

Yu, W., Chen, J., Xiong, Y., Pixley, F. J., Dai, X.-M., Yeung, Y.-G., & Stanley, E. R. (2008). CSF-1 receptor structure/function in MacCsf1râ/â macrophages: regulation of proliferation, differentiation, and morphology. Journal of Leukocyte Biology, 84(3), 852â863.

Authors 7

Wenfeng Yu (first)
Jian Chen (additional)
Ying Xiong (additional)
Fiona J Pixley (additional)
Xu-Ming Dai (additional)
Yee-Guide Yeung (additional)
E Richard Stanley (additional)

References 43 Referenced 81

10.1016/j.tcb.2004.09.016 / Trends Cell Biol. / CSF-1 regulation of the wandering macrophage: complexity in action by Pixley (2004)
10.1111/j.0105-2896.2005.00331.x / Immunol. Rev. / αvβ3 and macrophage colony-stimulating factor: partners in osteoclast biology by Ross (2005)
10.1016/j.coi.2005.11.006 / Curr. Opin. Immunol. / Colony-stimulating factor-1 in immunity and inflammation by Chitu (2006)
10.1016/S1064-2722(08)60060-2 / Adv. Dev. Biochem. (Amsterdam, Netherlands) / Pleiotropic roles for CSF-1 in development defined by the mouse mutation osteopetrotic by Pollard (1996)
10.1242/dev.120.6.1357 / Development / Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse by Cecchini (1994)
10.1182/blood.V99.1.111 / Blood / Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects by Dai (2002)
10.1016/S0092-8674(85)80047-7 / Cell / The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1 by Sherr (1985)
10.1002/j.1460-2075.1991.tb07948.x / EMBO J. / Role of dimerization and modification of the CSF-1 receptor in its activation and internalization during the CSF-1 response by Li (1991)
10.1093/emboj/18.13.3616 / EMBO J. / The Cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation by Lee (1999)
10.1002/jlb.62.2.145 / J. Leukoc. Biol. / CSF-1 signal transduction by Hamilton (1997)
{'key': '2023032712484969800_', 'first-page': '689', 'article-title': 'The biochemistry of colony stimulating factor-1 action', 'author': 'Hamilton', 'year': '1999', 'edition': '3rd ed'} / The biochemistry of colony stimulating factor-1 action by Hamilton (1999)
10.3109/08977190009001065 / Growth Factors / Early events in M-CSF receptor signaling by Bourette (2000)
10.1074/jbc.M610938200 / J. Biol. Chem. / c-Fms tyrosine 559 is a major mediator of M-CSF-induced proliferation of primary macrophages by Takeshita (2007)
10.1038/sj.onc.1205166 / Oncogene / C-Cbl binds the CSF-1 receptor at tyrosine 973, a novel phosphorylation site in the receptor’s carboxy-terminus by Wilhelmsen (2002)
10.1074/jbc.271.40.24476 / J. Biol. Chem. / Tyrosine phosphorylation of the juxtamembrane domain of the v-Fms oncogene product is required for its association with a 55-kDa protein by Joos (1996)
10.1038/sj.onc.1201518 / Oncogene / Identification of a second Grb2 binding site in the v-Fms tyrosine kinase by Mancini (1997)
10.1074/jbc.M314170200 / J. Biol. Chem. / A juxtamembrane tyrosine in the colony stimulating factor-1 receptor regulates ligand-induced Src association, receptor kinase function, and down-regulation by Rohde (2004)
10.1182/blood.V93.2.488 / Blood / Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis by Persons (1999)
{'key': '2023032712484969800_', 'first-page': '1785', 'article-title': 'BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias', 'volume': '11', 'author': 'Muller', 'year': '1991', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias by Muller (1991)
10.1128/jvi.59.3.746-750.1986 / J. Virol. / Large T antigens of simian virus 40 and polyomavirus efficiently establish primary fibroblasts by Jat (1986)
{'key': '2023032712484969800_', 'first-page': '301', 'article-title': 'Murine bone marrow-derived macrophages', 'author': 'Stanley', 'year': '1998'} / Murine bone marrow-derived macrophages by Stanley (1998)
{'key': '2023032712484969800_', 'first-page': '1672', 'article-title': 'Cell lines established by a temperature-sensitive simian virus 40 large-T-antigen gene are growth restricted at the nonpermissive temperature', 'volume': '9', 'author': 'Jat', 'year': '1989', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Cell lines established by a temperature-sensitive simian virus 40 large-T-antigen gene are growth restricted at the nonpermissive temperature by Jat (1989)
{'key': '2023032712484969800_', 'first-page': '2469', 'article-title': 'Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M', 'volume': '11', 'author': 'Sudo', 'year': '1995', 'journal-title': 'Oncogene'} / Oncogene / Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M by Sudo (1995)
10.1016/0092-8674(82)90376-2 / Cell / Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy by Tushinski (1982)
10.1002/(SICI)1097-4644(19990101)72:1<119::AID-JCB13>3.0.CO;2-R / J. Cell. Biochem. / CSF-1 stimulated multiubiquitination of the CSF-1 receptor and of Cbl follows their tyrosine phosphorylation and association with other signaling proteins by Wang (1999)
10.1074/jbc.273.27.17128 / J. Biol. Chem. / Colony-stimulating factor-1 stimulates the formation of multimeric cytosolic complexes of signaling proteins and cytoskeletal components in macrophages by Yeung (1998)
10.1074/jbc.274.50.35855 / J. Biol. Chem. / SHP-1 regulation of p62dok tyrosine phosphorylation in macrophages by Berg (1999)
10.1002/jcp.1041300316 / J. Cell. Physiol. / Isolation and characterization of a cloned growth factor dependent macrophage cell line, BAC12F5 by Morgan (1987)
10.1038/360258a0 / Nature / GM-CSF and TNF-α cooperate in the generation of dendritic Langerhans cells by Caux (1992)
10.1046/j.1365-2567.1997.00295.x / Immunology / Generation of dendritic cells from bone marrow progenitors using GM-CSF, TNF-α, and additional cytokines: antagonistic effects of IL-4 and IFN-γ and selective involvement of TNF-α receptor-1 by Lardon (1997)
10.1002/eji.1830111013 / Eur. J. Immunol. / F4/80, a monoclonal antibody directed specifically against the mouse macrophage by Austyn (1981)
10.1084/jem.157.5.1704 / J. Exp. Med. / The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: identification of resident macrophages in renal medullary and cortical interstitium and the juxtaglomerular complex by Hume (1983)
10.1242/jcs.66.1.189 / J. Cell Sci. / The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: macrophages of bone and associated connective tissue by Hume (1984)
10.1182/blood-2003-08-2739 / Blood / Incomplete restoration of colony-stimulating factor 1 (CSF-1) function in CSF-1-deficient Csf1op/Csf1op mice by transgenic expression of cell surface CSF-1 by Dai (2004)
10.1073/pnas.84.5.1268 / Proc. Natl. Acad. Sci. USA / Purification of the colony-stimulating factor 1 receptor and demonstration of its tyrosine kinase activity by Yeung (1987)
10.1242/jcs.93.3.447 / J. Cell Sci. / Colony-stimulating factor-1 induces rapid behavioral responses in the mouse macrophage cell line, BAC1.2F5 by Boocock (1989)
10.1128/MCB.21.5.1795-1809.2001 / Mol. Cell. Biol. / Protein tyrosine phosphatase ϕ regulates paxillin tyrosine phosphorylation and mediates colony-stimulating factor 1-induced morphological changes in macrophages by Pixley (2001)
10.1128/MCB.23.9.3067-3078.2003 / Mol. Cell. Biol. / Autoinhibition of the kit receptor tyrosine kinase by the cytosolic juxtamembrane region by Chan (2003)
10.1073/pnas.87.17.6738 / Proc. Natl. Acad. Sci. USA / A point mutation at tyrosine-809 in the human colony-stimulating factor 1 receptor impairs mitogenesis without abrogating tyrosine kinase activity, association with phosphatidylinositol 3-kinase, or induction of c-fos and junB genes by Roussel (1990)
{'key': '2023032712484969800_', 'first-page': '4698', 'article-title': 'Tyrosine 706 and 807 phosphorylation site mutants in the murine colony-stimulating factor-1 receptor are unaffected in their ability to bind or phosphorylate phosphatidylinositol-3 kinase but show differential defects in their ability to induce early response gene transcription', 'volume': '11', 'author': 'Van der Geer', 'year': '1991', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Tyrosine 706 and 807 phosphorylation site mutants in the murine colony-stimulating factor-1 receptor are unaffected in their ability to bind or phosphorylate phosphatidylinositol-3 kinase but show differential defects in their ability to induce early response gene transcription by Van der Geer (1991)
10.2741/A778 / Front. Biosci. / Autoinhibitory mechanisms in receptor tyrosine kinases by Hubbard (2002)
10.1126/science.1154370 / Science / Discovery of a cytokine and its receptor by functional screening of the extracellular proteome by Lin (2008)
10.1158/0008-5472.CAN-06-1823 / Cancer Res. / Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors by Wyckoff (2007)

Dates

Type	When
Created	17 years, 3 months ago (June 2, 2008, 8:58 p.m.)
Deposited	2 years, 3 months ago (May 18, 2023, 12:41 p.m.)
Indexed	4 days, 23 hours ago (Aug. 31, 2025, 7:11 p.m.)
Issued	17 years, 3 months ago (June 2, 2008)
Published	17 years, 3 months ago (June 2, 2008)
Published Online	17 years, 3 months ago (June 2, 2008)
Published Print	17 years ago (Sept. 1, 2008)

Funders 2

National Institutes of Health 10.13039/100000002
Region: Americas
gov (National government)
Labels3
1. Institutos Nacionales de la Salud
2. US National Institutes of Health
3. NIH
Awards3
1. PO1 CA 100324
2. CA26504
3. KO8 CA097348
Albert Einstein College of Medicine Cancer Center
Awards1
1. 5P30-CA13330

BibTeX

@article{Yu_2008, title={CSF-1 receptor structure/function in MacCsf1r–/– macrophages: regulation of proliferation, differentiation, and morphology}, volume={84}, ISSN={1938-3673}, url={http://dx.doi.org/10.1189/jlb.0308171}, DOI={10.1189/jlb.0308171}, number={3}, journal={Journal of Leukocyte Biology}, publisher={Oxford University Press (OUP)}, author={Yu, Wenfeng and Chen, Jian and Xiong, Ying and Pixley, Fiona J and Dai, Xu-Ming and Yeung, Yee-Guide and Stanley, E Richard}, year={2008}, month=jun, pages={852–863} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        31
      ]
    ],
    "date-time": "2025-08-31T23:11:48Z",
    "timestamp": 1756681908781,
    "version": "3.37.3"
  },
  "reference-count": 43,
  "publisher": "Oxford University Press (OUP)",
  "issue": "3",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2008,
            6,
            2
          ]
        ],
        "date-time": "2008-06-02T00:00:00Z",
        "timestamp": 1212364800000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "https://academic.oup.com/pages/standard-publication-reuse-rights"
    }
  ],
  "funder": [
    {
      "DOI": "10.13039/100000002",
      "name": "National Institutes of Health",
      "doi-asserted-by": "publisher",
      "award": [
        "CA26504",
        "PO1 CA 100324",
        "KO8 CA097348"
      ],
      "id": [
        {
          "id": "10.13039/100000002",
          "id-type": "DOI",
          "asserted-by": "publisher"
        }
      ]
    },
    {
      "name": "Albert Einstein College of Medicine Cancer Center",
      "award": [
        "5P30-CA13330"
      ]
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2008,
        9,
        1
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>CSF-1 is the major regulator of tissue macrophage development and function. A GM-CSF-dependent, CSF-1 receptor (CSF-1R)-deficient F4/80hiMac-1+Gr1\u2013CD11c+ bone marrow macrophage (BMM) line (MacCsf1r\u2212/\u2212) was developed to study the roles of the eight intracellular CSF-1R tyrosines phosphorylated upon receptor activation. Retroviral expression of the wild-type CSF-1R rescued the CSF-1-induced survival, proliferation, differentiation, and morphological characteristics of primary BMM. Mutation of all eight tyrosines failed to rescue, whereas the individual Y \u2192 F mutants (544, 559, 697, 706, 721, 807, 921, 974) rescued these CSF-1-inducible phenotypes to varying degrees. The juxtamembrane domain Y559F and activation loop Y807F mutations severely compromised proliferation and differentiation, whereas Y706, Y721F, and Y974F mutations altered morphological responses, and Y706F increased differentiation. Despite their retention of significant in vitro tyrosine kinase activity, Y559F and Y807F mutants exhibited severely impaired in vivo receptor tyrosine phosphorylation, consistent with the existence of cellular mechanisms inhibiting CSF-1R tyrosine phosphorylation that are relieved by phosphorylation of these two sites. The MacCsf1r\u2212/\u2212 macrophage line will facilitate genetic and proteomic approaches to CSF-1R structure/function studies in the major disease-related CSF-1R-expressing cell type.</jats:p>",
  "DOI": "10.1189/jlb.0308171",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2008,
        6,
        3
      ]
    ],
    "date-time": "2008-06-03T00:58:29Z",
    "timestamp": 1212454709000
  },
  "page": "852-863",
  "source": "Crossref",
  "is-referenced-by-count": 81,
  "title": "CSF-1 receptor structure/function in MacCsf1r\u2013/\u2013 macrophages: regulation of proliferation, differentiation, and morphology",
  "prefix": "10.1093",
  "volume": "84",
  "author": [
    {
      "given": "Wenfeng",
      "family": "Yu",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Developmental and Molecular Biology, Albert Einstein College of Medicine , Bronx, New York , USA"
        }
      ]
    },
    {
      "given": "Jian",
      "family": "Chen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Developmental and Molecular Biology, Albert Einstein College of Medicine , Bronx, New York , USA"
        }
      ]
    },
    {
      "given": "Ying",
      "family": "Xiong",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Developmental and Molecular Biology, Albert Einstein College of Medicine , Bronx, New York , USA"
        }
      ]
    },
    {
      "given": "Fiona J",
      "family": "Pixley",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Developmental and Molecular Biology, Albert Einstein College of Medicine , Bronx, New York , USA"
        }
      ]
    },
    {
      "given": "Xu-Ming",
      "family": "Dai",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Developmental and Molecular Biology, Albert Einstein College of Medicine , Bronx, New York , USA"
        }
      ]
    },
    {
      "given": "Yee-Guide",
      "family": "Yeung",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Developmental and Molecular Biology, Albert Einstein College of Medicine , Bronx, New York , USA"
        }
      ]
    },
    {
      "given": "E Richard",
      "family": "Stanley",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Developmental and Molecular Biology, Albert Einstein College of Medicine , Bronx, New York , USA"
        }
      ]
    }
  ],
  "member": "286",
  "published-online": {
    "date-parts": [
      [
        2008,
        6,
        2
      ]
    ]
  },
  "reference": [
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "628",
      "DOI": "10.1016/j.tcb.2004.09.016",
      "article-title": "CSF-1 regulation of the wandering macrophage: complexity in action",
      "volume": "14",
      "author": "Pixley",
      "year": "2004",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "88",
      "DOI": "10.1111/j.0105-2896.2005.00331.x",
      "article-title": "\u03b1v\u03b23 and macrophage colony-stimulating factor: partners in osteoclast biology",
      "volume": "208",
      "author": "Ross",
      "year": "2005",
      "journal-title": "Immunol. Rev."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "39",
      "DOI": "10.1016/j.coi.2005.11.006",
      "article-title": "Colony-stimulating factor-1 in immunity and inflammation",
      "volume": "18",
      "author": "Chitu",
      "year": "2006",
      "journal-title": "Curr. Opin. Immunol."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "153",
      "DOI": "10.1016/S1064-2722(08)60060-2",
      "article-title": "Pleiotropic roles for CSF-1 in development defined by the mouse mutation osteopetrotic",
      "volume": "4",
      "author": "Pollard",
      "year": "1996",
      "journal-title": "Adv. Dev. Biochem. (Amsterdam, Netherlands)"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "1357",
      "DOI": "10.1242/dev.120.6.1357",
      "article-title": "Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse",
      "volume": "120",
      "author": "Cecchini",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "111",
      "DOI": "10.1182/blood.V99.1.111",
      "article-title": "Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects",
      "volume": "99",
      "author": "Dai",
      "year": "2002",
      "journal-title": "Blood"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "665",
      "DOI": "10.1016/S0092-8674(85)80047-7",
      "article-title": "The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1",
      "volume": "41",
      "author": "Sherr",
      "year": "1985",
      "journal-title": "Cell"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "277",
      "DOI": "10.1002/j.1460-2075.1991.tb07948.x",
      "article-title": "Role of dimerization and modification of the CSF-1 receptor in its activation and internalization during the CSF-1 response",
      "volume": "10",
      "author": "Li",
      "year": "1991",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "3616",
      "DOI": "10.1093/emboj/18.13.3616",
      "article-title": "The Cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation",
      "volume": "18",
      "author": "Lee",
      "year": "1999",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "145",
      "DOI": "10.1002/jlb.62.2.145",
      "article-title": "CSF-1 signal transduction",
      "volume": "62",
      "author": "Hamilton",
      "year": "1997",
      "journal-title": "J. Leukoc. Biol."
    },
    {
      "key": "2023032712484969800_",
      "first-page": "689",
      "article-title": "The biochemistry of colony stimulating factor-1 action",
      "author": "Hamilton",
      "year": "1999",
      "edition": "3rd ed"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "155",
      "DOI": "10.3109/08977190009001065",
      "article-title": "Early events in M-CSF receptor signaling",
      "volume": "17",
      "author": "Bourette",
      "year": "2000",
      "journal-title": "Growth Factors"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "18980",
      "DOI": "10.1074/jbc.M610938200",
      "article-title": "c-Fms tyrosine 559 is a major mediator of M-CSF-induced proliferation of primary macrophages",
      "volume": "282",
      "author": "Takeshita",
      "year": "2007",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "1079",
      "DOI": "10.1038/sj.onc.1205166",
      "article-title": "C-Cbl binds the CSF-1 receptor at tyrosine 973, a novel phosphorylation site in the receptor\u2019s carboxy-terminus",
      "volume": "21",
      "author": "Wilhelmsen",
      "year": "2002",
      "journal-title": "Oncogene"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "24476",
      "DOI": "10.1074/jbc.271.40.24476",
      "article-title": "Tyrosine phosphorylation of the juxtamembrane domain of the v-Fms oncogene product is required for its association with a 55-kDa protein",
      "volume": "271",
      "author": "Joos",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "1565",
      "DOI": "10.1038/sj.onc.1201518",
      "article-title": "Identification of a second Grb2 binding site in the v-Fms tyrosine kinase",
      "volume": "15",
      "author": "Mancini",
      "year": "1997",
      "journal-title": "Oncogene"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "43448",
      "DOI": "10.1074/jbc.M314170200",
      "article-title": "A juxtamembrane tyrosine in the colony stimulating factor-1 receptor regulates ligand-induced Src association, receptor kinase function, and down-regulation",
      "volume": "279",
      "author": "Rohde",
      "year": "2004",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "488",
      "DOI": "10.1182/blood.V93.2.488",
      "article-title": "Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis",
      "volume": "93",
      "author": "Persons",
      "year": "1999",
      "journal-title": "Blood"
    },
    {
      "key": "2023032712484969800_",
      "first-page": "1785",
      "article-title": "BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias",
      "volume": "11",
      "author": "Muller",
      "year": "1991",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "746",
      "DOI": "10.1128/jvi.59.3.746-750.1986",
      "article-title": "Large T antigens of simian virus 40 and polyomavirus efficiently establish primary fibroblasts",
      "volume": "59",
      "author": "Jat",
      "year": "1986",
      "journal-title": "J. Virol."
    },
    {
      "key": "2023032712484969800_",
      "first-page": "301",
      "article-title": "Murine bone marrow-derived macrophages",
      "author": "Stanley",
      "year": "1998"
    },
    {
      "key": "2023032712484969800_",
      "first-page": "1672",
      "article-title": "Cell lines established by a temperature-sensitive simian virus 40 large-T-antigen gene are growth restricted at the nonpermissive temperature",
      "volume": "9",
      "author": "Jat",
      "year": "1989",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023032712484969800_",
      "first-page": "2469",
      "article-title": "Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M",
      "volume": "11",
      "author": "Sudo",
      "year": "1995",
      "journal-title": "Oncogene"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1016/0092-8674(82)90376-2",
      "article-title": "Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy",
      "volume": "28",
      "author": "Tushinski",
      "year": "1982",
      "journal-title": "Cell"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "119",
      "DOI": "10.1002/(SICI)1097-4644(19990101)72:1<119::AID-JCB13>3.0.CO;2-R",
      "article-title": "CSF-1 stimulated multiubiquitination of the CSF-1 receptor and of Cbl follows their tyrosine phosphorylation and association with other signaling proteins",
      "volume": "72",
      "author": "Wang",
      "year": "1999",
      "journal-title": "J. Cell. Biochem."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "17128",
      "DOI": "10.1074/jbc.273.27.17128",
      "article-title": "Colony-stimulating factor-1 stimulates the formation of multimeric cytosolic complexes of signaling proteins and cytoskeletal components in macrophages",
      "volume": "273",
      "author": "Yeung",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "35855",
      "DOI": "10.1074/jbc.274.50.35855",
      "article-title": "SHP-1 regulation of p62dok tyrosine phosphorylation in macrophages",
      "volume": "274",
      "author": "Berg",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "420",
      "DOI": "10.1002/jcp.1041300316",
      "article-title": "Isolation and characterization of a cloned growth factor dependent macrophage cell line, BAC12F5",
      "volume": "130",
      "author": "Morgan",
      "year": "1987",
      "journal-title": "J. Cell. Physiol."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "258",
      "DOI": "10.1038/360258a0",
      "article-title": "GM-CSF and TNF-\u03b1 cooperate in the generation of dendritic Langerhans cells",
      "volume": "360",
      "author": "Caux",
      "year": "1992",
      "journal-title": "Nature"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "553",
      "DOI": "10.1046/j.1365-2567.1997.00295.x",
      "article-title": "Generation of dendritic cells from bone marrow progenitors using GM-CSF, TNF-\u03b1, and additional cytokines: antagonistic effects of IL-4 and IFN-\u03b3 and selective involvement of TNF-\u03b1 receptor-1",
      "volume": "91",
      "author": "Lardon",
      "year": "1997",
      "journal-title": "Immunology"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "805",
      "DOI": "10.1002/eji.1830111013",
      "article-title": "F4/80, a monoclonal antibody directed specifically against the mouse macrophage",
      "volume": "11",
      "author": "Austyn",
      "year": "1981",
      "journal-title": "Eur. J. Immunol."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "1704",
      "DOI": "10.1084/jem.157.5.1704",
      "article-title": "The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: identification of resident macrophages in renal medullary and cortical interstitium and the juxtaglomerular complex",
      "volume": "157",
      "author": "Hume",
      "year": "1983",
      "journal-title": "J. Exp. Med."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "189",
      "DOI": "10.1242/jcs.66.1.189",
      "article-title": "The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: macrophages of bone and associated connective tissue",
      "volume": "66",
      "author": "Hume",
      "year": "1984",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "1114",
      "DOI": "10.1182/blood-2003-08-2739",
      "article-title": "Incomplete restoration of colony-stimulating factor 1 (CSF-1) function in CSF-1-deficient Csf1op/Csf1op mice by transgenic expression of cell surface CSF-1",
      "volume": "103",
      "author": "Dai",
      "year": "2004",
      "journal-title": "Blood"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "1268",
      "DOI": "10.1073/pnas.84.5.1268",
      "article-title": "Purification of the colony-stimulating factor 1 receptor and demonstration of its tyrosine kinase activity",
      "volume": "84",
      "author": "Yeung",
      "year": "1987",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "447",
      "DOI": "10.1242/jcs.93.3.447",
      "article-title": "Colony-stimulating factor-1 induces rapid behavioral responses in the mouse macrophage cell line, BAC1.2F5",
      "volume": "93",
      "author": "Boocock",
      "year": "1989",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "1795",
      "DOI": "10.1128/MCB.21.5.1795-1809.2001",
      "article-title": "Protein tyrosine phosphatase \u03d5 regulates paxillin tyrosine phosphorylation and mediates colony-stimulating factor 1-induced morphological changes in macrophages",
      "volume": "21",
      "author": "Pixley",
      "year": "2001",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "3067",
      "DOI": "10.1128/MCB.23.9.3067-3078.2003",
      "article-title": "Autoinhibition of the kit receptor tyrosine kinase by the cytosolic juxtamembrane region",
      "volume": "23",
      "author": "Chan",
      "year": "2003",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "6738",
      "DOI": "10.1073/pnas.87.17.6738",
      "article-title": "A point mutation at tyrosine-809 in the human colony-stimulating factor 1 receptor impairs mitogenesis without abrogating tyrosine kinase activity, association with phosphatidylinositol 3-kinase, or induction of c-fos and junB genes",
      "volume": "87",
      "author": "Roussel",
      "year": "1990",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2023032712484969800_",
      "first-page": "4698",
      "article-title": "Tyrosine 706 and 807 phosphorylation site mutants in the murine colony-stimulating factor-1 receptor are unaffected in their ability to bind or phosphorylate phosphatidylinositol-3 kinase but show differential defects in their ability to induce early response gene transcription",
      "volume": "11",
      "author": "Van der Geer",
      "year": "1991",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "d330",
      "DOI": "10.2741/A778",
      "article-title": "Autoinhibitory mechanisms in receptor tyrosine kinases",
      "volume": "7",
      "author": "Hubbard",
      "year": "2002",
      "journal-title": "Front. Biosci."
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "807",
      "DOI": "10.1126/science.1154370",
      "article-title": "Discovery of a cytokine and its receptor by functional screening of the extracellular proteome",
      "volume": "320",
      "author": "Lin",
      "year": "2008",
      "journal-title": "Science"
    },
    {
      "key": "2023032712484969800_",
      "doi-asserted-by": "crossref",
      "first-page": "2649",
      "DOI": "10.1158/0008-5472.CAN-06-1823",
      "article-title": "Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors",
      "volume": "67",
      "author": "Wyckoff",
      "year": "2007",
      "journal-title": "Cancer Res."
    }
  ],
  "container-title": "Journal of Leukocyte Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1189%2Fjlb.0308171",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://academic.oup.com/jleukbio/article-pdf/84/3/852/49608501/jlb0852.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://academic.oup.com/jleukbio/article-pdf/84/3/852/49608501/jlb0852.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        5,
        18
      ]
    ],
    "date-time": "2023-05-18T16:41:18Z",
    "timestamp": 1684428078000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://academic.oup.com/jleukbio/article/84/3/852/6975265"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2008,
        6,
        2
      ]
    ]
  },
  "references-count": 43,
  "journal-issue": {
    "issue": "3",
    "published-online": {
      "date-parts": [
        [
          2008,
          6,
          2
        ]
      ]
    },
    "published-print": {
      "date-parts": [
        [
          2008,
          9,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1189/jlb.0308171",
  "relation": {},
  "ISSN": [
    "0741-5400",
    "1938-3673"
  ],
  "subject": [],
  "published-other": {
    "date-parts": [
      [
        2008,
        9
      ]
    ]
  },
  "published": {
    "date-parts": [
      [
        2008,
        6,
        2
      ]
    ]
  }
}