DOI: 10.1101/gad.12.15.2345. A novel homeobox gene, <i>dharma,</i> can induce the organizer in a non-cell-autonomous manner

A novel homeobox gene, dharma, can induce the organizer in a non-cell-autonomous manner

10.1101/gad.12.15.2345

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

The formation of Spemann organizer is one of the most important steps in dorsoventral axis determination in vertebrate development. However, whether the organizer forms autonomously or is induced non-cell-autonomously is controversial. In this report we have isolated a novel zebrafish homeobox gene, dharma, capable of inducing the organizer ectopically. The expression of dharma was first detected in several blastomeres at one side of the margin soon after the mid-blastula transition and continued in the dorsal side of the yolk syncytial layer (YSL) under the embryonic shield, the zebrafish organizer, until the onset of gastrulation. Furthermore, dharmaexpressed in the YSL induced the organizer in a non-cell-autonomous manner. These results provided the first identification of a zygotic gene to be implicated in the formation of an organizer-inducing center.

Bibliography

Yamanaka, Y., Mizuno, T., Sasai, Y., Kishi, M., Takeda, H., Kim, C.-H., Hibi, M., & Hirano, T. (1998). A novel homeobox gene, dharma, can induce the organizer in a non-cell-autonomousâmanner. Genes & Development, 12(15), 2345â2353.

Authors 8

Yojiro Yamanaka (first)
Toshiro Mizuno (additional)
Yoshiki Sasai (additional)
Masashi Kishi (additional)
Hiroyuki Takeda (additional)
Cheol-Hee Kim (additional)
Masahiko Hibi (additional)
Toshio Hirano (additional)

References 43 Referenced 113

10.1242/dev.120.5.1179 / Development / The cleavage stage origin of Spemann’s Organizer: Analysis of the movements of blastomere clones before and during gastrulation in Xenopus. by Bauer (1994)
10.1038/382638a0
10.1007/BF00575837
10.1101/gad.11.24.3286
10.1016/0092-8674(91)90288-A
10.1006/dbio.1996.0294
10.1139/bcb-75-5-563
10.1242/dev.124.21.4275 / Development / Animal and vegetal pole cells of early Xenopus embryos respond differently to maternal dorsal determinants: Implications for the patterning of the organiser. by Darras (1997)
10.1016/0959-437X(95)80030-1
10.1242/dev.112.4.1103 / Development / Autonomous differentiation of dorsal axial structures from an animal cap cleavage stage blastomere in Xenopus. by Gallagher (1991)
10.1016/0012-1606(86)90254-X
10.1016/0012-1606(84)90042-3
10.1101/gad.10.19.2452
10.1242/dev.124.21.4179 / Development / Patterning the Xenopus blastula. by Heasman (1997)
10.1242/dev.101.3.557 / Development / The development of animal cap cells in Xenopus: A measure of the start of animal cap competence to form mesoderm. by Jones (1987)
10.1016/0168-9525(94)90220-8
10.1016/0012-1606(90)90365-P
10.1073/pnas.93.16.8455
10.1083/jcb.136.5.1123
10.1242/dev.124.23.4905 / Development / The Xenopus homeobox gene Twin mediates Wnt induction of Goosecoid in establishment of Spemann’s organizer. by Laurent (1997)
10.1242/dev.120.5.1191 / Development / A role for cytoplasmic determinants in mesoderm patterning: Cell-autonomous activation of the goosecoid and Xwnt-8 genes along the dorsoventral axis of early Xenopus embryos. by Lemaire (1994)
10.1016/S0168-9525(97)81401-1
10.1016/0092-8674(95)90373-9
10.1038/383131a0
10.1016/S0092-8674(00)81915-7
10.1016/S0168-9525(97)01093-7
10.1016/S0092-8674(00)80112-9
10.1242/dev.123.1.81 / Development / Genes establishing dorsoventral pattern formation in the zebrafish embryo: The ventral specifying genes. by Mullins (1995)
10.1007/BF00578701
10.1242/dev.122.6.1873 / Development / Anteroposterior patterning in the zebrafish, Danio rerio: An explant assay reveals inductive and suppressive cell interactions. by Sagerstrom (1996)
10.1242/dev.122.7.2207 / Development / The vegetal determinants required for the Spemann organizer move equatorially during the first cell cycle. by Sakai (1996)
10.1006/dbio.1996.8445
10.1016/0925-4773(96)00546-1
10.1242/dev.116.4.1021 / Development / The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. by Schulte-Merker (1992)
10.1242/dev.120.4.843 / Development / Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. by Schulte-Merker (1994)
10.1016/S0960-9822(94)00027-8
10.1016/0092-8674(91)90070-F
10.1016/0092-8674(92)90316-5
10.1242/dev.117.4.1261 / Development / Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. by Stachel (1993)
10.1101/gad.6.3.356
10.1111/j.1440-169X.1987.00141.x / Dev. Growth Differ. / Tates and roles of the presumptive organizer region in the 32-cell embryo in normal development of Xenopus laevis. by Takasaki (1987)
Westerfield M. (1995) The zebrafish book (University of Oregon Press, Eugene, OR), 3rd ed..
10.1242/dev.122.10.2987 / Development / Maternal β-catenin establishes a dorsal signal in early Xenopus embryos. by Wylie (1996)

Dates

Type	When
Created	17 years, 6 months ago (Feb. 20, 2008, 5:52 p.m.)
Deposited	3 years, 9 months ago (Nov. 14, 2021, 10:22 p.m.)
Indexed	1 month, 1 week ago (July 24, 2025, 7:17 a.m.)
Issued	27 years, 1 month ago (Aug. 1, 1998)
Published	27 years, 1 month ago (Aug. 1, 1998)
Published Online	27 years, 1 month ago (Aug. 1, 1998)
Published Print	27 years, 1 month ago (Aug. 1, 1998)

Funders 0

None

BibTeX

@article{Yamanaka_1998, title={A novel homeobox gene, dharma, can induce the organizer in a non-cell-autonomous manner}, volume={12}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.12.15.2345}, DOI={10.1101/gad.12.15.2345}, number={15}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Yamanaka, Yojiro and Mizuno, Toshiro and Sasai, Yoshiki and Kishi, Masashi and Takeda, Hiroyuki and Kim, Cheol-Hee and Hibi, Masahiko and Hirano, Toshio}, year={1998}, month=aug, pages={2345–2353} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        24
      ]
    ],
    "date-time": "2025-07-24T11:17:28Z",
    "timestamp": 1753355848912
  },
  "reference-count": 43,
  "publisher": "Cold Spring Harbor Laboratory",
  "issue": "15",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1998,
        8,
        1
      ]
    ]
  },
  "abstract": "<jats:p>The formation of Spemann organizer is one of the most important steps in dorsoventral axis determination in vertebrate development. However, whether the organizer forms autonomously or is induced non-cell-autonomously is controversial. In this report we have isolated a novel zebrafish homeobox gene, <jats:italic>dharma,</jats:italic> capable of inducing the organizer ectopically. The expression of <jats:italic>dharma</jats:italic> was first detected in several blastomeres at one side of the margin soon after the mid-blastula transition and continued in the dorsal side of the yolk syncytial layer (YSL) under the embryonic shield, the zebrafish organizer, until the onset of gastrulation. Furthermore, <jats:italic>dharma</jats:italic>expressed in the YSL induced the organizer in a non-cell-autonomous manner. These results provided the first identification of a zygotic gene to be implicated in the formation of an organizer-inducing center.</jats:p>",
  "DOI": "10.1101/gad.12.15.2345",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2008,
        2,
        20
      ]
    ],
    "date-time": "2008-02-20T22:52:17Z",
    "timestamp": 1203547937000
  },
  "page": "2345-2353",
  "source": "Crossref",
  "is-referenced-by-count": 113,
  "title": "A novel homeobox gene, <i>dharma,</i> can induce the organizer in a non-cell-autonomous\u2009manner",
  "prefix": "10.1101",
  "volume": "12",
  "author": [
    {
      "given": "Yojiro",
      "family": "Yamanaka",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Toshiro",
      "family": "Mizuno",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Yoshiki",
      "family": "Sasai",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Masashi",
      "family": "Kishi",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Hiroyuki",
      "family": "Takeda",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Cheol-Hee",
      "family": "Kim",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Masahiko",
      "family": "Hibi",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Toshio",
      "family": "Hirano",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "246",
  "published-online": {
    "date-parts": [
      [
        1998,
        8,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2021111418553116000_12.15.2345.1",
      "doi-asserted-by": "crossref",
      "first-page": "1179",
      "DOI": "10.1242/dev.120.5.1179",
      "article-title": "The cleavage stage origin of Spemann\u2019s Organizer: Analysis of the movements of blastomere clones before and during gastrulation in Xenopus.",
      "volume": "120",
      "author": "Bauer",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/382638a0"
    },
    {
      "key": "2021111418553116000_12.15.2345.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00575837"
    },
    {
      "key": "2021111418553116000_12.15.2345.4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.11.24.3286"
    },
    {
      "key": "2021111418553116000_12.15.2345.5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90288-A"
    },
    {
      "key": "2021111418553116000_12.15.2345.6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1996.0294"
    },
    {
      "key": "2021111418553116000_12.15.2345.7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1139/bcb-75-5-563"
    },
    {
      "key": "2021111418553116000_12.15.2345.8",
      "doi-asserted-by": "crossref",
      "first-page": "4275",
      "DOI": "10.1242/dev.124.21.4275",
      "article-title": "Animal and vegetal pole cells of early Xenopus embryos respond differently to maternal dorsal determinants: Implications for the patterning of the organiser.",
      "volume": "124",
      "author": "Darras",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0959-437X(95)80030-1"
    },
    {
      "key": "2021111418553116000_12.15.2345.10",
      "doi-asserted-by": "crossref",
      "first-page": "1103",
      "DOI": "10.1242/dev.112.4.1103",
      "article-title": "Autonomous differentiation of dorsal axial structures from an animal cap cleavage stage blastomere in Xenopus.",
      "volume": "112",
      "author": "Gallagher",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(86)90254-X"
    },
    {
      "key": "2021111418553116000_12.15.2345.12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(84)90042-3"
    },
    {
      "key": "2021111418553116000_12.15.2345.13",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.10.19.2452"
    },
    {
      "key": "2021111418553116000_12.15.2345.14",
      "doi-asserted-by": "crossref",
      "first-page": "4179",
      "DOI": "10.1242/dev.124.21.4179",
      "article-title": "Patterning the Xenopus blastula.",
      "volume": "124",
      "author": "Heasman",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.15",
      "doi-asserted-by": "crossref",
      "first-page": "557",
      "DOI": "10.1242/dev.101.3.557",
      "article-title": "The development of animal cap cells in Xenopus: A measure of the start of animal cap competence to form mesoderm.",
      "volume": "101",
      "author": "Jones",
      "year": "1987",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-9525(94)90220-8"
    },
    {
      "key": "2021111418553116000_12.15.2345.17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(90)90365-P"
    },
    {
      "key": "2021111418553116000_12.15.2345.18",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.93.16.8455"
    },
    {
      "key": "2021111418553116000_12.15.2345.19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.136.5.1123"
    },
    {
      "key": "2021111418553116000_12.15.2345.20",
      "doi-asserted-by": "crossref",
      "first-page": "4905",
      "DOI": "10.1242/dev.124.23.4905",
      "article-title": "The Xenopus homeobox gene Twin mediates Wnt induction of Goosecoid in establishment of Spemann\u2019s organizer.",
      "volume": "124",
      "author": "Laurent",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.21",
      "doi-asserted-by": "crossref",
      "first-page": "1191",
      "DOI": "10.1242/dev.120.5.1191",
      "article-title": "A role for cytoplasmic determinants in mesoderm patterning: Cell-autonomous activation of the goosecoid and Xwnt-8 genes along the dorsoventral axis of early Xenopus embryos.",
      "volume": "120",
      "author": "Lemaire",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0168-9525(97)81401-1"
    },
    {
      "key": "2021111418553116000_12.15.2345.23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(95)90373-9"
    },
    {
      "key": "2021111418553116000_12.15.2345.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/383131a0"
    },
    {
      "key": "2021111418553116000_12.15.2345.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81915-7"
    },
    {
      "key": "2021111418553116000_12.15.2345.26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0168-9525(97)01093-7"
    },
    {
      "key": "2021111418553116000_12.15.2345.27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)80112-9"
    },
    {
      "key": "2021111418553116000_12.15.2345.28",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1242/dev.123.1.81",
      "article-title": "Genes establishing dorsoventral pattern formation in the zebrafish embryo: The ventral specifying genes.",
      "volume": "123",
      "author": "Mullins",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00578701"
    },
    {
      "key": "2021111418553116000_12.15.2345.30",
      "doi-asserted-by": "crossref",
      "first-page": "1873",
      "DOI": "10.1242/dev.122.6.1873",
      "article-title": "Anteroposterior patterning in the zebrafish, Danio rerio: An explant assay reveals inductive and suppressive cell interactions.",
      "volume": "122",
      "author": "Sagerstrom",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.31",
      "doi-asserted-by": "crossref",
      "first-page": "2207",
      "DOI": "10.1242/dev.122.7.2207",
      "article-title": "The vegetal determinants required for the Spemann organizer move equatorially during the first cell cycle.",
      "volume": "122",
      "author": "Sakai",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1996.8445"
    },
    {
      "key": "2021111418553116000_12.15.2345.33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0925-4773(96)00546-1"
    },
    {
      "key": "2021111418553116000_12.15.2345.34",
      "doi-asserted-by": "crossref",
      "first-page": "1021",
      "DOI": "10.1242/dev.116.4.1021",
      "article-title": "The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo.",
      "volume": "116",
      "author": "Schulte-Merker",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.35",
      "doi-asserted-by": "crossref",
      "first-page": "843",
      "DOI": "10.1242/dev.120.4.843",
      "article-title": "Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos.",
      "volume": "120",
      "author": "Schulte-Merker",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-9822(94)00027-8"
    },
    {
      "key": "2021111418553116000_12.15.2345.37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90070-F"
    },
    {
      "key": "2021111418553116000_12.15.2345.38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90316-5"
    },
    {
      "key": "2021111418553116000_12.15.2345.39",
      "doi-asserted-by": "crossref",
      "first-page": "1261",
      "DOI": "10.1242/dev.117.4.1261",
      "article-title": "Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish.",
      "volume": "117",
      "author": "Stachel",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2021111418553116000_12.15.2345.40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.6.3.356"
    },
    {
      "key": "2021111418553116000_12.15.2345.41",
      "doi-asserted-by": "crossref",
      "first-page": "141",
      "DOI": "10.1111/j.1440-169X.1987.00141.x",
      "article-title": "Tates and roles of the presumptive organizer region in the 32-cell embryo in normal development of Xenopus laevis.",
      "volume": "29",
      "author": "Takasaki",
      "year": "1987",
      "journal-title": "Dev. Growth Differ."
    },
    {
      "key": "2021111418553116000_12.15.2345.42",
      "unstructured": "Westerfield M. (1995) The zebrafish book (University of Oregon Press, Eugene, OR), 3rd ed.."
    },
    {
      "key": "2021111418553116000_12.15.2345.43",
      "doi-asserted-by": "crossref",
      "first-page": "2987",
      "DOI": "10.1242/dev.122.10.2987",
      "article-title": "Maternal \u03b2-catenin establishes a dorsal signal in early Xenopus embryos.",
      "volume": "122",
      "author": "Wylie",
      "year": "1996",
      "journal-title": "Development"
    }
  ],
  "container-title": "Genes &amp; Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1101/gad.12.15.2345",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        11,
        15
      ]
    ],
    "date-time": "2021-11-15T03:22:58Z",
    "timestamp": 1636946578000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "http://genesdev.cshlp.org/lookup/doi/10.1101/gad.12.15.2345"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1998,
        8,
        1
      ]
    ]
  },
  "references-count": 43,
  "journal-issue": {
    "issue": "15",
    "published-print": {
      "date-parts": [
        [
          1998,
          8,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1101/gad.12.15.2345"
  ],
  "URL": "http://dx.doi.org/10.1101/gad.12.15.2345",
  "relation": {},
  "ISSN": [
    "0890-9369",
    "1549-5477"
  ],
  "subject": [],
  "container-title-short": "Genes Dev.",
  "published": {
    "date-parts": [
      [
        1998,
        8,
        1
      ]
    ]
  }
}