DOI: 10.1242/dev.120.2.369. <i>wingless</i> signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo

wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo

10.1242/dev.120.2.369

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT wingless/wnt-1 signaling directs cell fate during development. Genetic analysis in Drosophila identified genes that may encode components of the wingless signal transduction system. Drosophila Armadillo, homolog of vertebrate β-catenin, is required for wingless signaling. Unlike armadillo RNA, Armadillo protein accumulates non-uniformly in different cells of each embryonic segment. We found that cells alter their intracellular distribution of Armadillo in response to Wingless signal, accumulating increased levels of cytoplasmic Armadillo relative to those of membrane-associated protein. Levels of cytoplasmic Armadillo are also regulated by Zeste-White 3 kinase. Analysis of double mutants demonstrates that Armadillo’s role in wingless signaling is direct, and that Armadillo functions down-stream of both wingless and zeste-white 3. We present a model for the role of Armadillo stripes in transduction of wingless signal.

Bibliography

Peifer, M., Sweeton, D., Casey, M., & Wieschaus, E. (1994). wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development, 120(2), 369â380.

Authors 4

Mark Peifer (first)
Dari Sweeton (additional)
Michael Casey (additional)
Eric Wieschaus (additional)

References 37 Referenced 356

{'key': '2023072009321734900_DEVELOP_120_2_369C1', 'article-title': 'Segment polarity gene interactions modulate the wg signaling pathway in Drosophila embryos', 'author': 'Bejsovec', 'year': '1993', 'journal-title': 'Development, in press'} / Development, in press / Segment polarity gene interactions modulate the wg signaling pathway in Drosophila embryos by Bejsovec (1993)
10.1016/S0092-8674(05)80056-X / Cell / Receptor-to-effector signaling through G-proteins: Roles for βγ dimers as well as α subunits by Birnbaumer (1992)
10.1002/j.1460-2075.1990.tb07477.x / EMBO J / An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2+ subfamily by Bourouis (1990)
10.1083/jcb.123.6.1857 / J. Cell Biol. (in press) / Expression on Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion by Bradley (1993)
10.1093/genetics/131.3.643 / Genetics / Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila by Chou (1992)
10.1126/science.8372355 / Science / Neuroblast specification and formation regulated by wingless in the Drosophila CNS by Chu-LaGraff (1993)
{'key': '2023072009321734900_DEVELOP_120_2_369C7', 'first-page': '841', 'article-title': 'Negative regulation of Jun/AP-1: conserved function of glycogen synthase kinase 3 and the Drosophila kinase shaggy', 'volume': '8', 'author': 'de Groot', 'year': '1993', 'journal-title': 'Oncogene'} / Oncogene / Negative regulation of Jun/AP-1: conserved function of glycogen synthase kinase 3 and the Drosophila kinase shaggy by de Groot (1993)
10.1016/0925-4773(91)90040-D / Mech. Dev / Secretion and movement of the wingless protein in the Drosophila embryo by Gonzalez (1991)
10.1016/0092-8674(91)90263-X / Cell / The choice of cell fate in the epidermis of Drosophila by Heitzler (1991)
10.1016/0092-8674(90)90364-K / Cell / Induction across germlayers in Drosophila mediated by a genetic cascade by Immerglück (1990)
10.1016/0012-1606(89)90084-5 / Dev. Biol / The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death by Klingensmith (1989)
10.1126/science.1962194 / Science / A homolog of Drosophila armadillo (plakoglobin) associated with the cytoplasmic tail of E-cadherin by McCrea (1991)
10.1083/jcb.123.2.477 / J. Cell Biol / Induction of a secondary body axis in Xenopus by antibodies to β-catenin by McCrea (1993)
10.1016/0168-9525(92)90393-I / Trends Genet / The Wnt family of developmental regulators by McMahon (1992)
10.1016/0092-8674(89)90506-0 / Cell / Ectopic expression of the protooncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis by McMahon (1989)
10.1083/jcb.109.6.2963 / J. Cell Biol / Actin-binding proteins from Drosophila embryos: a complex network of interacting proteins detected by F-actin affinity chromatagraphy by Miller (1989)
10.1242/dev.116.3.711 / Development / The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo by Noordermeer (1992)
10.1038/287795a0 / Nature / Mutations affecting segment number and polarity in Drosophila by Nüsslein-Volhard (1980)
10.1007/BF00848156 / Roux’s Arch. Dev. Biol / Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster : I. Zygotic loci on the second chromosome by Nüsslein-Volhard (1984)
10.1083/jcb.121.5.1133 / J. Cell Biol / Identification of a Drosophila homologue of alpha-catenin and its association with armadillo protein by Oda (1993)
10.1242/jcs.105.4.993 / J. Cell Sci / The product of the Drosophila segment polarity gene armadillo is part of a multi-protein complex similar to the vertebrate adherens junction by Peifer (1993)
10.1016/0168-9525(92)90394-J / Trends Genet / Knowing your neighbors; cell interactions determine intrasegmental pattern in Drosophila by Peifer (1992)
10.1016/0092-8674(90)90413-9 / Cell / The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin by Peifer (1990)
10.1242/dev.111.4.1029 / Development / The segment polarity gene armadillo affects the wingless signaling pathway in both embryonic and adult pattern formation by Peifer (1991)
10.1242/dev.118.4.1191 / Development / A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis by Peifer (1993)
10.1016/0012-1606(89)90180-2 / Dev. Biol / Multiple functions of a Drosophila homeotic gene, zeste-white 3, during segmentation and neurogenesis by Perrimon (1989)
10.1101/gad.3.1.96 / Genes Dev / Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene by Riggleman (1989)
10.1016/0092-8674(90)90451-J / Cell / Spatial expression of the Drosophila segment polarity gene armadillo is post-transcriptionally regulated by wingless by Riggleman (1990)
10.1038/345825a0 / Nature / Putative protein kinase product of the Drosophila segment polarity gene zeste-white 3 by Siegfried (1990)
10.1016/S0092-8674(05)80065-0 / Cell / wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase- 3, to regulate engrailed and establish cell fate by Siegfried (1992)
{'key': '2023072009321734900_DEVELOP_120_2_369C31', 'article-title': 'Components of Wingless signaling in Drosophila', 'author': 'Siegfried', 'year': '1993', 'journal-title': 'Nature (in press)'} / Nature (in press) / Components of Wingless signaling in Drosophila by Siegfried (1993)
10.1016/0092-8674(91)90365-6 / Cell / The role of the Bicaudal-D protein and its phosphorylation in Drosophila oocyte differentiation by Suter (1991)
10.1083/jcb.113.4.867 / J. Cell Biol / Specific proto-oncogenic tyrosine kinases of src family are enriched in cell-to-cell adhrens junctions where the level of tyrosine phosphorylation is elevated by Tsukita (1991)
10.1016/0092-8674(89)90020-2 / Cell / Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication by van den Heuvel (1989)
10.1007/BF00444042 / Roux’s Arch Dev. Biol / Specificity of embryonic lethal mutations in Drosophila analyzed in germ line clones by Wieschaus (1986)
{'key': '2023072009321734900_DEVELOP_120_2_369C36', 'volume-title': 'Looking at embryos. In Drosophila, A Practical Approach', 'author': 'Wieschaus', 'year': '1986'} / Looking at embryos. In Drosophila, A Practical Approach by Wieschaus (1986)
10.1016/0092-8674(87)90558-7 / Cell / Autonomous requirements for the segment polarity gene armadillo during Drosophila embryogenesis by Wieschaus (1987)

Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 2:43 p.m.)
Deposited	2 years, 1 month ago (July 20, 2023, 5:44 a.m.)
Indexed	2 days, 21 hours ago (Sept. 3, 2025, 5:52 a.m.)
Issued	31 years, 7 months ago (Feb. 1, 1994)
Published	31 years, 7 months ago (Feb. 1, 1994)
Published Online	31 years, 7 months ago (Feb. 1, 1994)
Published Print	31 years, 7 months ago (Feb. 1, 1994)

Funders 0

None

BibTeX

@article{Peifer_1994, title={wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo}, volume={120}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.120.2.369}, DOI={10.1242/dev.120.2.369}, number={2}, journal={Development}, publisher={The Company of Biologists}, author={Peifer, Mark and Sweeton, Dari and Casey, Michael and Wieschaus, Eric}, year={1994}, month=feb, pages={369–380} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        9,
        3
      ]
    ],
    "date-time": "2025-09-03T09:52:25Z",
    "timestamp": 1756893145636
  },
  "reference-count": 37,
  "publisher": "The Company of Biologists",
  "issue": "2",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1994,
            2,
            1
          ]
        ],
        "date-time": "1994-02-01T00:00:00Z",
        "timestamp": 760060800000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://www.biologists.com/user-licence-1-1/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1994,
        2,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>wingless/wnt-1 signaling directs cell fate during development. Genetic analysis in Drosophila identified genes that may encode components of the wingless signal transduction system. Drosophila Armadillo, homolog of vertebrate \u03b2-catenin, is required for wingless signaling. Unlike armadillo RNA, Armadillo protein accumulates non-uniformly in different cells of each embryonic segment. We found that cells alter their intracellular distribution of Armadillo in response to Wingless signal, accumulating increased levels of cytoplasmic Armadillo relative to those of membrane-associated protein. Levels of cytoplasmic Armadillo are also regulated by Zeste-White 3 kinase. Analysis of double mutants demonstrates that Armadillo\u2019s role in wingless signaling is direct, and that Armadillo functions down-stream of both wingless and zeste-white 3. We present a model for the role of Armadillo stripes in transduction of wingless signal.</jats:p>",
  "DOI": "10.1242/dev.120.2.369",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        23
      ]
    ],
    "date-time": "2021-04-23T18:43:37Z",
    "timestamp": 1619203417000
  },
  "page": "369-380",
  "source": "Crossref",
  "is-referenced-by-count": 356,
  "title": "<i>wingless</i> signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo",
  "prefix": "10.1242",
  "volume": "120",
  "author": [
    {
      "given": "Mark",
      "family": "Peifer",
      "sequence": "first",
      "affiliation": [
        {
          "name": "University of North Carolina 1 Department of Biology , , Chapel Hill, NC 27599-3280, USA"
        }
      ]
    },
    {
      "given": "Dari",
      "family": "Sweeton",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Princeton University 2 Department of Molecular Biology , , Princeton, NJ 08544-1014, USA"
        }
      ]
    },
    {
      "given": "Michael",
      "family": "Casey",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "University of North Carolina 1 Department of Biology , , Chapel Hill, NC 27599-3280, USA"
        }
      ]
    },
    {
      "given": "Eric",
      "family": "Wieschaus",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Princeton University 2 Department of Molecular Biology , , Princeton, NJ 08544-1014, USA"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1994,
        2,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C1",
      "article-title": "Segment polarity gene interactions modulate the wg signaling pathway in Drosophila embryos",
      "author": "Bejsovec",
      "year": "1993",
      "journal-title": "Development, in press"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C2",
      "doi-asserted-by": "publisher",
      "first-page": "1069",
      "DOI": "10.1016/S0092-8674(05)80056-X",
      "article-title": "Receptor-to-effector signaling through G-proteins: Roles for \u03b2\u03b3 dimers as well as \u03b1 subunits",
      "volume": "71",
      "author": "Birnbaumer",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C3",
      "doi-asserted-by": "publisher",
      "first-page": "2877",
      "DOI": "10.1002/j.1460-2075.1990.tb07477.x",
      "article-title": "An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2+ subfamily",
      "volume": "9",
      "author": "Bourouis",
      "year": "1990",
      "journal-title": "EMBO J"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C4",
      "doi-asserted-by": "crossref",
      "DOI": "10.1083/jcb.123.6.1857",
      "article-title": "Expression on Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion",
      "author": "Bradley",
      "year": "1993",
      "journal-title": "J. Cell Biol. (in press)"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C5",
      "doi-asserted-by": "publisher",
      "first-page": "643",
      "DOI": "10.1093/genetics/131.3.643",
      "article-title": "Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila",
      "volume": "131",
      "author": "Chou",
      "year": "1992",
      "journal-title": "Genetics"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C6",
      "doi-asserted-by": "publisher",
      "first-page": "1594",
      "DOI": "10.1126/science.8372355",
      "article-title": "Neuroblast specification and formation regulated by wingless in the Drosophila CNS",
      "volume": "261",
      "author": "Chu-LaGraff",
      "year": "1993",
      "journal-title": "Science"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C7",
      "first-page": "841",
      "article-title": "Negative regulation of Jun/AP-1: conserved function of glycogen synthase kinase 3 and the Drosophila kinase shaggy",
      "volume": "8",
      "author": "de Groot",
      "year": "1993",
      "journal-title": "Oncogene"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C8",
      "doi-asserted-by": "publisher",
      "first-page": "43",
      "DOI": "10.1016/0925-4773(91)90040-D",
      "article-title": "Secretion and movement of the wingless protein in the Drosophila embryo",
      "volume": "35",
      "author": "Gonzalez",
      "year": "1991",
      "journal-title": "Mech. Dev"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C9",
      "doi-asserted-by": "publisher",
      "first-page": "1083",
      "DOI": "10.1016/0092-8674(91)90263-X",
      "article-title": "The choice of cell fate in the epidermis of Drosophila",
      "volume": "64",
      "author": "Heitzler",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C10",
      "doi-asserted-by": "publisher",
      "first-page": "261",
      "DOI": "10.1016/0092-8674(90)90364-K",
      "article-title": "Induction across germlayers in Drosophila mediated by a genetic cascade",
      "volume": "62",
      "author": "Immergl\u00fcck",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C11",
      "doi-asserted-by": "publisher",
      "first-page": "130",
      "DOI": "10.1016/0012-1606(89)90084-5",
      "article-title": "The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death",
      "volume": "134",
      "author": "Klingensmith",
      "year": "1989",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C12",
      "doi-asserted-by": "publisher",
      "first-page": "1359",
      "DOI": "10.1126/science.1962194",
      "article-title": "A homolog of Drosophila armadillo (plakoglobin) associated with the cytoplasmic tail of E-cadherin",
      "volume": "25",
      "author": "McCrea",
      "year": "1991",
      "journal-title": "Science"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C13",
      "doi-asserted-by": "publisher",
      "first-page": "477",
      "DOI": "10.1083/jcb.123.2.477",
      "article-title": "Induction of a secondary body axis in Xenopus by antibodies to \u03b2-catenin",
      "volume": "123",
      "author": "McCrea",
      "year": "1993",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C14",
      "doi-asserted-by": "publisher",
      "first-page": "236",
      "DOI": "10.1016/0168-9525(92)90393-I",
      "article-title": "The Wnt family of developmental regulators",
      "volume": "8",
      "author": "McMahon",
      "year": "1992",
      "journal-title": "Trends Genet"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C15",
      "doi-asserted-by": "publisher",
      "first-page": "1075",
      "DOI": "10.1016/0092-8674(89)90506-0",
      "article-title": "Ectopic expression of the protooncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis",
      "volume": "58",
      "author": "McMahon",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C16",
      "doi-asserted-by": "publisher",
      "first-page": "2963",
      "DOI": "10.1083/jcb.109.6.2963",
      "article-title": "Actin-binding proteins from Drosophila embryos: a complex network of interacting proteins detected by F-actin affinity chromatagraphy",
      "volume": "109",
      "author": "Miller",
      "year": "1989",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C17",
      "doi-asserted-by": "publisher",
      "first-page": "711",
      "DOI": "10.1242/dev.116.3.711",
      "article-title": "The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo",
      "volume": "116",
      "author": "Noordermeer",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C18",
      "doi-asserted-by": "publisher",
      "first-page": "795",
      "DOI": "10.1038/287795a0",
      "article-title": "Mutations affecting segment number and polarity in Drosophila",
      "volume": "287",
      "author": "N\u00fcsslein-Volhard",
      "year": "1980",
      "journal-title": "Nature"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C19",
      "doi-asserted-by": "publisher",
      "first-page": "267",
      "DOI": "10.1007/BF00848156",
      "article-title": "Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster : I. Zygotic loci on the second chromosome",
      "volume": "193",
      "author": "N\u00fcsslein-Volhard",
      "year": "1984",
      "journal-title": "Roux\u2019s Arch. Dev. Biol"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C20",
      "doi-asserted-by": "publisher",
      "first-page": "1133",
      "DOI": "10.1083/jcb.121.5.1133",
      "article-title": "Identification of a Drosophila homologue of alpha-catenin and its association with armadillo protein",
      "volume": "121",
      "author": "Oda",
      "year": "1993",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C21",
      "doi-asserted-by": "publisher",
      "first-page": "993",
      "DOI": "10.1242/jcs.105.4.993",
      "article-title": "The product of the Drosophila segment polarity gene armadillo is part of a multi-protein complex similar to the vertebrate adherens junction",
      "volume": "105",
      "author": "Peifer",
      "year": "1993",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C22",
      "doi-asserted-by": "publisher",
      "first-page": "243",
      "DOI": "10.1016/0168-9525(92)90394-J",
      "article-title": "Knowing your neighbors; cell interactions determine intrasegmental pattern in Drosophila",
      "volume": "8",
      "author": "Peifer",
      "year": "1992",
      "journal-title": "Trends Genet"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C23",
      "doi-asserted-by": "publisher",
      "first-page": "1167",
      "DOI": "10.1016/0092-8674(90)90413-9",
      "article-title": "The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin",
      "volume": "63",
      "author": "Peifer",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C24",
      "doi-asserted-by": "publisher",
      "first-page": "1028",
      "DOI": "10.1242/dev.111.4.1029",
      "article-title": "The segment polarity gene armadillo affects the wingless signaling pathway in both embryonic and adult pattern formation",
      "volume": "111",
      "author": "Peifer",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C25",
      "doi-asserted-by": "publisher",
      "first-page": "1191",
      "DOI": "10.1242/dev.118.4.1191",
      "article-title": "A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis",
      "volume": "118",
      "author": "Peifer",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C26",
      "doi-asserted-by": "publisher",
      "first-page": "287",
      "DOI": "10.1016/0012-1606(89)90180-2",
      "article-title": "Multiple functions of a Drosophila homeotic gene, zeste-white 3, during segmentation and neurogenesis",
      "volume": "135",
      "author": "Perrimon",
      "year": "1989",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C27",
      "doi-asserted-by": "publisher",
      "first-page": "96",
      "DOI": "10.1101/gad.3.1.96",
      "article-title": "Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene",
      "volume": "3",
      "author": "Riggleman",
      "year": "1989",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C28",
      "doi-asserted-by": "publisher",
      "first-page": "549",
      "DOI": "10.1016/0092-8674(90)90451-J",
      "article-title": "Spatial expression of the Drosophila segment polarity gene armadillo is post-transcriptionally regulated by wingless",
      "volume": "63",
      "author": "Riggleman",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C29",
      "doi-asserted-by": "publisher",
      "first-page": "825",
      "DOI": "10.1038/345825a0",
      "article-title": "Putative protein kinase product of the Drosophila segment polarity gene zeste-white 3",
      "volume": "345",
      "author": "Siegfried",
      "year": "1990",
      "journal-title": "Nature"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C30",
      "doi-asserted-by": "publisher",
      "first-page": "1167",
      "DOI": "10.1016/S0092-8674(05)80065-0",
      "article-title": "wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase- 3, to regulate engrailed and establish cell fate",
      "volume": "71",
      "author": "Siegfried",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C31",
      "article-title": "Components of Wingless signaling in Drosophila",
      "author": "Siegfried",
      "year": "1993",
      "journal-title": "Nature (in press)"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C32",
      "doi-asserted-by": "publisher",
      "first-page": "917",
      "DOI": "10.1016/0092-8674(91)90365-6",
      "article-title": "The role of the Bicaudal-D protein and its phosphorylation in Drosophila oocyte differentiation",
      "volume": "67",
      "author": "Suter",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C33",
      "doi-asserted-by": "publisher",
      "first-page": "867",
      "DOI": "10.1083/jcb.113.4.867",
      "article-title": "Specific proto-oncogenic tyrosine kinases of src family are enriched in cell-to-cell adhrens junctions where the level of tyrosine phosphorylation is elevated",
      "volume": "113",
      "author": "Tsukita",
      "year": "1991",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C34",
      "doi-asserted-by": "publisher",
      "first-page": "739",
      "DOI": "10.1016/0092-8674(89)90020-2",
      "article-title": "Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication",
      "volume": "59",
      "author": "van den Heuvel",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C35",
      "doi-asserted-by": "publisher",
      "first-page": "63",
      "DOI": "10.1007/BF00444042",
      "article-title": "Specificity of embryonic lethal mutations in Drosophila analyzed in germ line clones",
      "volume": "195",
      "author": "Wieschaus",
      "year": "1986",
      "journal-title": "Roux\u2019s Arch Dev. Biol"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C36",
      "volume-title": "Looking at embryos. In Drosophila, A Practical Approach",
      "author": "Wieschaus",
      "year": "1986"
    },
    {
      "key": "2023072009321734900_DEVELOP_120_2_369C37",
      "doi-asserted-by": "publisher",
      "first-page": "177",
      "DOI": "10.1016/0092-8674(87)90558-7",
      "article-title": "Autonomous requirements for the segment polarity gene armadillo during Drosophila embryogenesis",
      "volume": "49",
      "author": "Wieschaus",
      "year": "1987",
      "journal-title": "Cell"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/120/2/369/3053060/develop_120_2_369.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/120/2/369/3053060/develop_120_2_369.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        20
      ]
    ],
    "date-time": "2023-07-20T09:44:04Z",
    "timestamp": 1689846244000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/120/2/369/38270/wingless-signal-and-Zeste-white-3-kinase-trigger"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1994,
        2,
        1
      ]
    ]
  },
  "references-count": 37,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          1994,
          2,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.120.2.369",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1994,
        2,
        1
      ]
    ]
  }
}