DOI: 10.1083/jcb.200606017. Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane

Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane

10.1083/jcb.200606017

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Wnt11 is a key signal, determining cell polarization and migration during vertebrate gastrulation. It is known that Wnt11 functionally interacts with several signaling components, the homologues of which control planar cell polarity in Drosophila melanogaster. Although in D. melanogaster these components are thought to polarize cells by asymmetrically localizing at the plasma membrane, it is not yet clear whether their subcellular localization plays a similarly important role in vertebrates. We show that in zebrafish embryonic cells, Wnt11 locally functions at the plasma membrane by accumulating its receptor, Frizzled 7, on adjacent sites of cell contacts. Wnt11-induced Frizzled 7 accumulations recruit the intracellular Wnt signaling mediator Dishevelled, as well as Wnt11 itself, and locally increase cell contact persistence. This increase in cell contact persistence is mediated by the local interaction of Wnt11, Frizzled 7, and the atypical cadherin Flamingo at the plasma membrane, and it does not require the activity of further downstream effectors of Wnt11 signaling, such as RhoA and Rok2. We propose that Wnt11, by interacting with Frizzled 7 and Flamingo, modulates local cell contact persistence to coordinate cell movements during gastrulation.

Bibliography

Witzel, S., Zimyanin, V., Carreira-Barbosa, F., Tada, M., & Heisenberg, C.-P. (2006). Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane. The Journal of Cell Biology, 175(5), 791â802.

Authors 5

Sabine Witzel (first)
Vitaly Zimyanin (additional)
Filipa Carreira-Barbosa (additional)
Masazumi Tada (additional)
Carl-Philipp Heisenberg (additional)

References 43 Referenced 119

10.1016/S1534-5807(02)00176-4 / Dev. Cell. (2002)
10.1523/JNEUROSCI.14-06-03475.1994 / J. Neurosci. (1994)
10.1101/gad.890501 / Genes Dev. (2001)
10.1016/j.devcel.2005.10.016 / Dev. Cell. (2005)
10.1242/dev.127.14.3091 / Development. (2000)
10.1016/S0925-4773(01)00291-X / Mech. Dev. (2001)
10.1016/j.ydbio.2005.03.026 / Dev. Biol. (2005)
10.1038/35011068 / Nature. (2000)
10.1101/gr.209601 / Genome Res. (2001)
10.1016/S0925-4773(98)00013-6 / Mech. Dev. (1998)
10.1242/dev.128.18.3635 / Development. (2001)
10.1038/sj.emboj.7600329 / EMBO J. (2004)
10.1016/S0960-9822(03)00505-0 / Curr. Biol. (2003)
10.1242/dev.01667 / Development. (2005)
10.1038/ncb1399 / Nat. Cell Biol. (2006)
10.1016/j.cub.2005.04.062 / Curr. Biol. (2005)
10.1242/jcs.02547 / J. Cell Sci. (2005)
10.1038/nbt945 / Nat. Biotechnol. (2004)
10.1093/emboj/19.5.1010 / EMBO J. (2000)
10.1016/j.ygeno.2005.03.010 / Genomics. (2005)
10.1242/dev.120.4.1009 / Development. (1994)
10.1242/jcs.02646 / J. Cell Sci. (2005)
10.1016/j.devcel.2004.07.007 / Dev. Cell. (2004)
10.1016/S0960-9822(01)00233-0 / Curr. Biol. (2001)
10.1242/dev.00695 / Development. (2003)
10.1016/S1097-2765(01)00184-8 / Mol. Cell. (2001)
10.1002/gene.1044 / Genesis. (2001)
10.1242/dev.127.9.1981 / Development. (2000)
10.1006/dbio.1994.1212 / Dev. Biol. (1994)
10.1083/jcb.133.5.1123 / J. Cell Biol. (1996)
10.1242/dev.00758 / Development. (2003)
10.1016/j.devcel.2005.08.011 / Dev. Cell. (2005)
10.1016/S0925-4773(02)00221-6 / Mech. Dev. (2002)
10.1038/sj.emboj.7600332 / EMBO J. (2004)
10.1016/S0092-8674(00)80046-X / Cell. (1999)
10.1016/S1534-5807(03)00266-1 / Dev. Cell. (2003)
10.1242/dev.108.4.569 / Development. (1990)
{'key': '2023072908100101700_BIB38', 'year': '2000'} (2000)
10.1242/jcs.115.3.531 / J. Cell Sci. (2002)
10.1038/35101621 / Nature. (2001)
10.1016/S1097-2765(03)00427-1 / Mol. Cell. (2003)
10.1016/S0960-9822(02)70716-1 / Curr. Biol. (1996)
10.1016/j.cellsig.2005.05.019 / Cell. Signal. (2006)

Dates

Type	When
Created	18 years, 9 months ago (Nov. 27, 2006, 10:38 p.m.)
Deposited	2 years, 1 month ago (July 29, 2023, 4:12 a.m.)
Indexed	2 months ago (July 2, 2025, 9:09 a.m.)
Issued	18 years, 9 months ago (Nov. 27, 2006)
Published	18 years, 9 months ago (Nov. 27, 2006)
Published Online	18 years, 9 months ago (Nov. 27, 2006)
Published Print	18 years, 9 months ago (Dec. 4, 2006)

Funders 0

None

BibTeX

@article{Witzel_2006, title={Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane}, volume={175}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.200606017}, DOI={10.1083/jcb.200606017}, number={5}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Witzel, Sabine and Zimyanin, Vitaly and Carreira-Barbosa, Filipa and Tada, Masazumi and Heisenberg, Carl-Philipp}, year={2006}, month=nov, pages={791–802} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        2
      ]
    ],
    "date-time": "2025-07-02T13:09:22Z",
    "timestamp": 1751461762026
  },
  "reference-count": 43,
  "publisher": "Rockefeller University Press",
  "issue": "5",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2006,
        12,
        4
      ]
    ]
  },
  "abstract": "<jats:p>Wnt11 is a key signal, determining cell polarization and migration during vertebrate gastrulation. It is known that Wnt11 functionally interacts with several signaling components, the homologues of which control planar cell polarity in Drosophila melanogaster. Although in D. melanogaster these components are thought to polarize cells by asymmetrically localizing at the plasma membrane, it is not yet clear whether their subcellular localization plays a similarly important role in vertebrates. We show that in zebrafish embryonic cells, Wnt11 locally functions at the plasma membrane by accumulating its receptor, Frizzled 7, on adjacent sites of cell contacts. Wnt11-induced Frizzled 7 accumulations recruit the intracellular Wnt signaling mediator Dishevelled, as well as Wnt11 itself, and locally increase cell contact persistence. This increase in cell contact persistence is mediated by the local interaction of Wnt11, Frizzled 7, and the atypical cadherin Flamingo at the plasma membrane, and it does not require the activity of further downstream effectors of Wnt11 signaling, such as RhoA and Rok2. We propose that Wnt11, by interacting with Frizzled 7 and Flamingo, modulates local cell contact persistence to coordinate cell movements during gastrulation.</jats:p>",
  "DOI": "10.1083/jcb.200606017",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        11,
        28
      ]
    ],
    "date-time": "2006-11-28T03:38:48Z",
    "timestamp": 1164685128000
  },
  "page": "791-802",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 119,
  "title": "Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane",
  "prefix": "10.1083",
  "volume": "175",
  "author": [
    {
      "given": "Sabine",
      "family": "Witzel",
      "sequence": "first",
      "affiliation": [
        {
          "name": "1Max-Planck-Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany"
        }
      ]
    },
    {
      "given": "Vitaly",
      "family": "Zimyanin",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1Max-Planck-Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany"
        }
      ]
    },
    {
      "given": "Filipa",
      "family": "Carreira-Barbosa",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "2Department of Anatomy and Developmental Biology, University College London, London WC1E 6BT, England, UK"
        }
      ]
    },
    {
      "given": "Masazumi",
      "family": "Tada",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "2Department of Anatomy and Developmental Biology, University College London, London WC1E 6BT, England, UK"
        }
      ]
    },
    {
      "given": "Carl-Philipp",
      "family": "Heisenberg",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1Max-Planck-Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2006,
        11,
        27
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072908100101700_BIB1",
      "doi-asserted-by": "crossref",
      "first-page": "525",
      "DOI": "10.1016/S1534-5807(02)00176-4",
      "volume": "2",
      "year": "2002",
      "journal-title": "Dev. Cell."
    },
    {
      "key": "2023072908100101700_BIB2",
      "doi-asserted-by": "crossref",
      "first-page": "3475",
      "DOI": "10.1523/JNEUROSCI.14-06-03475.1994",
      "volume": "14",
      "year": "1994",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "2023072908100101700_BIB3",
      "doi-asserted-by": "crossref",
      "first-page": "1182",
      "DOI": "10.1101/gad.890501",
      "volume": "15",
      "year": "2001",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072908100101700_BIB4",
      "doi-asserted-by": "crossref",
      "first-page": "805",
      "DOI": "10.1016/j.devcel.2005.10.016",
      "volume": "9",
      "year": "2005",
      "journal-title": "Dev. Cell."
    },
    {
      "key": "2023072908100101700_BIB5",
      "doi-asserted-by": "crossref",
      "first-page": "3091",
      "DOI": "10.1242/dev.127.14.3091",
      "volume": "127",
      "year": "2000",
      "journal-title": "Development."
    },
    {
      "key": "2023072908100101700_BIB6",
      "doi-asserted-by": "crossref",
      "first-page": "231",
      "DOI": "10.1016/S0925-4773(01)00291-X",
      "volume": "102",
      "year": "2001",
      "journal-title": "Mech. Dev."
    },
    {
      "key": "2023072908100101700_BIB7",
      "doi-asserted-by": "crossref",
      "first-page": "320",
      "DOI": "10.1016/j.ydbio.2005.03.026",
      "volume": "282",
      "year": "2005",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "2023072908100101700_BIB8",
      "doi-asserted-by": "crossref",
      "first-page": "76",
      "DOI": "10.1038/35011068",
      "volume": "405",
      "year": "2000",
      "journal-title": "Nature."
    },
    {
      "key": "2023072908100101700_BIB9",
      "doi-asserted-by": "crossref",
      "first-page": "1979",
      "DOI": "10.1101/gr.209601",
      "volume": "11",
      "year": "2001",
      "journal-title": "Genome Res."
    },
    {
      "key": "2023072908100101700_BIB10",
      "doi-asserted-by": "crossref",
      "first-page": "165",
      "DOI": "10.1016/S0925-4773(98)00013-6",
      "volume": "71",
      "year": "1998",
      "journal-title": "Mech. Dev."
    },
    {
      "key": "2023072908100101700_BIB11",
      "doi-asserted-by": "crossref",
      "first-page": "3635",
      "DOI": "10.1242/dev.128.18.3635",
      "volume": "128",
      "year": "2001",
      "journal-title": "Development."
    },
    {
      "key": "2023072908100101700_BIB12",
      "doi-asserted-by": "crossref",
      "first-page": "3249",
      "DOI": "10.1038/sj.emboj.7600329",
      "volume": "23",
      "year": "2004",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072908100101700_BIB13",
      "doi-asserted-by": "crossref",
      "first-page": "1279",
      "DOI": "10.1016/S0960-9822(03)00505-0",
      "volume": "13",
      "year": "2003",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072908100101700_BIB14",
      "doi-asserted-by": "crossref",
      "first-page": "1187",
      "DOI": "10.1242/dev.01667",
      "volume": "132",
      "year": "2005",
      "journal-title": "Development."
    },
    {
      "key": "2023072908100101700_BIB15",
      "doi-asserted-by": "crossref",
      "first-page": "492",
      "DOI": "10.1038/ncb1399",
      "volume": "8",
      "year": "2006",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "2023072908100101700_BIB16",
      "doi-asserted-by": "crossref",
      "first-page": "1039",
      "DOI": "10.1016/j.cub.2005.04.062",
      "volume": "15",
      "year": "2005",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072908100101700_BIB17",
      "doi-asserted-by": "crossref",
      "first-page": "4199",
      "DOI": "10.1242/jcs.02547",
      "volume": "118",
      "year": "2005",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072908100101700_BIB18",
      "doi-asserted-by": "crossref",
      "first-page": "445",
      "DOI": "10.1038/nbt945",
      "volume": "22",
      "year": "2004",
      "journal-title": "Nat. Biotechnol."
    },
    {
      "key": "2023072908100101700_BIB19",
      "doi-asserted-by": "crossref",
      "first-page": "1010",
      "DOI": "10.1093/emboj/19.5.1010",
      "volume": "19",
      "year": "2000",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072908100101700_BIB20",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1016/j.ygeno.2005.03.010",
      "volume": "86",
      "year": "2005",
      "journal-title": "Genomics."
    },
    {
      "key": "2023072908100101700_BIB21",
      "doi-asserted-by": "crossref",
      "first-page": "1009",
      "DOI": "10.1242/dev.120.4.1009",
      "volume": "120",
      "year": "1994",
      "journal-title": "Development."
    },
    {
      "key": "2023072908100101700_BIB22",
      "doi-asserted-by": "crossref",
      "first-page": "5269",
      "DOI": "10.1242/jcs.02646",
      "volume": "118",
      "year": "2005",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072908100101700_BIB23",
      "doi-asserted-by": "crossref",
      "first-page": "205",
      "DOI": "10.1016/j.devcel.2004.07.007",
      "volume": "7",
      "year": "2004",
      "journal-title": "Dev. Cell."
    },
    {
      "key": "2023072908100101700_BIB24",
      "doi-asserted-by": "crossref",
      "first-page": "859",
      "DOI": "10.1016/S0960-9822(01)00233-0",
      "volume": "11",
      "year": "2001",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072908100101700_BIB25",
      "doi-asserted-by": "crossref",
      "first-page": "4501",
      "DOI": "10.1242/dev.00695",
      "volume": "130",
      "year": "2003",
      "journal-title": "Development."
    },
    {
      "key": "2023072908100101700_BIB26",
      "doi-asserted-by": "crossref",
      "first-page": "367",
      "DOI": "10.1016/S1097-2765(01)00184-8",
      "volume": "7",
      "year": "2001",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072908100101700_BIB27",
      "doi-asserted-by": "crossref",
      "first-page": "119",
      "DOI": "10.1002/gene.1044",
      "volume": "30",
      "year": "2001",
      "journal-title": "Genesis."
    },
    {
      "key": "2023072908100101700_BIB28",
      "doi-asserted-by": "crossref",
      "first-page": "1981",
      "DOI": "10.1242/dev.127.9.1981",
      "volume": "127",
      "year": "2000",
      "journal-title": "Development."
    },
    {
      "key": "2023072908100101700_BIB29",
      "doi-asserted-by": "crossref",
      "first-page": "420",
      "DOI": "10.1006/dbio.1994.1212",
      "volume": "164",
      "year": "1994",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "2023072908100101700_BIB30",
      "doi-asserted-by": "crossref",
      "first-page": "1123",
      "DOI": "10.1083/jcb.133.5.1123",
      "volume": "133",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072908100101700_BIB31",
      "doi-asserted-by": "crossref",
      "first-page": "5375",
      "DOI": "10.1242/dev.00758",
      "volume": "130",
      "year": "2003",
      "journal-title": "Development."
    },
    {
      "key": "2023072908100101700_BIB32",
      "doi-asserted-by": "crossref",
      "first-page": "555",
      "DOI": "10.1016/j.devcel.2005.08.011",
      "volume": "9",
      "year": "2005",
      "journal-title": "Dev. Cell."
    },
    {
      "key": "2023072908100101700_BIB33",
      "doi-asserted-by": "crossref",
      "first-page": "165",
      "DOI": "10.1016/S0925-4773(02)00221-6",
      "volume": "118",
      "year": "2002",
      "journal-title": "Mech. Dev."
    },
    {
      "key": "2023072908100101700_BIB34",
      "doi-asserted-by": "crossref",
      "first-page": "3259",
      "DOI": "10.1038/sj.emboj.7600332",
      "volume": "23",
      "year": "2004",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072908100101700_BIB35",
      "doi-asserted-by": "crossref",
      "first-page": "585",
      "DOI": "10.1016/S0092-8674(00)80046-X",
      "volume": "98",
      "year": "1999",
      "journal-title": "Cell."
    },
    {
      "key": "2023072908100101700_BIB36",
      "doi-asserted-by": "crossref",
      "first-page": "367",
      "DOI": "10.1016/S1534-5807(03)00266-1",
      "volume": "5",
      "year": "2003",
      "journal-title": "Dev. Cell."
    },
    {
      "key": "2023072908100101700_BIB37",
      "doi-asserted-by": "crossref",
      "first-page": "569",
      "DOI": "10.1242/dev.108.4.569",
      "volume": "108",
      "year": "1990",
      "journal-title": "Development."
    },
    {
      "key": "2023072908100101700_BIB38",
      "year": "2000"
    },
    {
      "key": "2023072908100101700_BIB39",
      "doi-asserted-by": "crossref",
      "first-page": "531",
      "DOI": "10.1242/jcs.115.3.531",
      "volume": "115",
      "year": "2002",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072908100101700_BIB40",
      "doi-asserted-by": "crossref",
      "first-page": "856",
      "DOI": "10.1038/35101621",
      "volume": "413",
      "year": "2001",
      "journal-title": "Nature."
    },
    {
      "key": "2023072908100101700_BIB41",
      "doi-asserted-by": "crossref",
      "first-page": "1251",
      "DOI": "10.1016/S1097-2765(03)00427-1",
      "volume": "12",
      "year": "2003",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072908100101700_BIB42",
      "doi-asserted-by": "crossref",
      "first-page": "1302",
      "DOI": "10.1016/S0960-9822(02)70716-1",
      "volume": "6",
      "year": "1996",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072908100101700_BIB43",
      "doi-asserted-by": "crossref",
      "first-page": "359",
      "DOI": "10.1016/j.cellsig.2005.05.019",
      "volume": "18",
      "year": "2006",
      "journal-title": "Cell. Signal."
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/175/5/791/1877596/jcb_200606017.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/175/5/791/1877596/jcb_200606017.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        29
      ]
    ],
    "date-time": "2023-07-29T08:12:11Z",
    "timestamp": 1690618331000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/175/5/791/44623/Wnt11-controls-cell-contact-persistence-by-local"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2006,
        11,
        27
      ]
    ]
  },
  "references-count": 43,
  "journal-issue": {
    "issue": "5",
    "published-print": {
      "date-parts": [
        [
          2006,
          12,
          4
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.200606017",
  "relation": {},
  "ISSN": [
    "1540-8140",
    "0021-9525"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2006,
        11,
        27
      ]
    ]
  }
}