DOI: 10.1242/dev.119.3.649. A role for <i>Pax-1</i> as a mediator of notochordal signals during the dorsoventral specification of vertebrae

A role for Pax-1 as a mediator of notochordal signals during the dorsoventral specification of vertebrae

10.1242/dev.119.3.649

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT The notochord plays an important role in the differentiation of the paraxial mesoderm and the neural tube. We have analyzed the role of the notochord in somite differentiation and subsequent formation of the vertebral column using a mouse mutant, Danforth’s short-tail (Sd). In this mutant, the skeletal phenotype is most probably a result of degeneration and subsequent loss of the notochord. The Sd gene is known to interact with undulated (un), a sclerotome mutant. Double mutants between Sd and un alleles show an increase in the severity of the defects, mainly in the ventral parts of the vertebrae. We also show that part of the Sd phenotype is strikingly similar to that of the un alleles. As un is known to be caused by a mutation in the Pax-1 gene, we analyzed Pax-1 expression in Sd embryos. In Sd embryos, Pax-1 expression is reduced, providing a potential molecular basis for the genetic interaction observed. A complete loss of Pax-1 expression in morphologically intact mesenchyme was found in the lower thoracic-lumbar region, which is phenotypically very similar to the corresponding region in a Pax-1 null mutant, Undulated short-tail. The sclerotome developmental abnormalities in Sd coincide closely, both in time and space, with notochordal changes, as determined by whole-mount T antibody staining. These findings indicate that an intact notochord is necessary for normal Pax-1 expression in sclerotome cells, which is in turn required for the formation of the ventral parts of the vertebrae. The observed correlation among structural changes of the notochord, Pax-1 expression levels and skeletal phenotypes, suggests that Pax-1 might be an intrinsic mediator of notochordal signals during the dorsoventral specification of vertebrae.

Bibliography

Koseki, H., Wallin, J., Wilting, J., Mizutani, Y., Kispert, A., Ebensperger, C., Herrmann, B. G., Christ, B., & Balling, R. (1993). A role for Pax-1 as a mediator of notochordal signals during the dorsoventral specification of vertebrae. Development, 119(3), 649â660.

Authors 9

Haruhiko Koseki (first)
Johan Wallin (additional)
Jörg Wilting (additional)
Yoko Mizutani (additional)
Andreas Kispert (additional)
Cecilia Ebensperger (additional)
Bernhard G. Herrmann (additional)
Bodo Christ (additional)
Rudi Balling (additional)

References 51 Referenced 149

10.1002/jez.1401320303 / J. Exp. Zool / An experimental analysis of the development of the spinal column, V. Reactivity of chick somites by Avery (1956)
10.1016/0092-8674(88)90039-6 / Cell / undulated, a mutation affecting the development of the mouse skeleton, has a point mutation in the paired box of Pax-1 by Balling (1988)
{'key': '2024121723201103500_DEVELOP_119_3_649C3', 'first-page': '132', 'article-title': 'Development of the skeletal system', 'volume': '165', 'author': 'Balling', 'year': '1991', 'journal-title': 'Ciba Found. Symp'} / Ciba Found. Symp / Development of the skeletal system by Balling (1991)
{'key': '2024121723201103500_DEVELOP_119_3_649C4', 'first-page': '43', 'article-title': 'Sut allelic with un', 'volume': '52', 'author': 'Blandova', 'year': '1975', 'journal-title': 'Mouse News Lett'} / Mouse News Lett / Sut allelic with un by Blandova (1975)
10.1016/0092-8674(86)90818-4 / Cell / Conservation of a large protein domain in the segmentation gene Paired and in functionally related genes of Drosophila by Bopp (1986)
10.1242/dev.113.2.625 / Development / Perturbation of neuronal differentiation and axon guidance in the spinal cord of mouse embryos lacking a floor plate: analysis of Danforth’s short-tail mutation by Bovolenta (1991)
{'key': '2024121723201103500_DEVELOP_119_3_649C7', 'article-title': 'The ventralizing effect of the notochord on somite differentiation', 'volume-title': 'Anat. Embryol. (in press)', 'author': 'Brand-Saberi', 'year': '1993'} / Anat. Embryol. (in press) / The ventralizing effect of the notochord on somite differentiation by Brand-Saberi (1993)
10.1093/oxfordjournals.jhered.a109648 / J. Hered / Perichordal sheath of heterozygous and homozygous Danforth’s short-tail mice by Center (1982)
10.1016/0092-8674(91)90434-Z / Cell / The molecular basis of the undulated/Pax-1 mutation by Chalepakis (1991)
10.1016/S0940-9602(11)80337-7 / Ann. Anat / From somites to vertebral column by Christ (1992)
10.1016/0012-1606(65)90027-8 / Dev. Biol / Induction of somite chondrogenesis by cartilage and notochord: A correlation between inductive activity and specific stages of cytodifferentiation by Cooper (1965)
10.1002/jez.1401320207 / J. Exp. Zool / The developmental dependence of the vertebral column upon the spinal cord in the urodele by Detwiler (1956)
10.1016/0092-8674(88)90577-6 / Cell / Pax-1, a member of a paired box homologous murine gene family, is expressed in segmented structures during development by Deutsch (1988)
10.1093/genetics/131.2.423 / Genetics / A genetic map of the mouse suitable for typing intraspecific crosses by Dietrich (1992)
10.1093/oxfordjournals.jhered.a104924 / J. Hered / A new mutation in the mouse affecting spinal column and urogenital system by Dunn (1940)
10.1016/0092-8674(91)90071-6 / Cell / splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3 by Epstein (1991)
10.1007/BF00171747 / Anat. Embryol / The splotch mutation interferes with muscle development in the limbs by Franz (1993)
10.1021/bi00709a025 / Biochemistry / Ribonucleic acid isolated by cesium chloride centrifugation by Glisin (1974)
10.1093/genetics/30.1.29 / Genetics / The embryonic development of mutants of the Sd-strain in mice by Gluecksohn-Schoenheimer (1945)
10.1002/j.1460-2075.1991.tb08054.x / EMBO J / Pax-3, a novel murine DNA binding protein expressed during early neurogenesis by Goulding (1991)
10.1242/dev.117.3.1001 / Development / Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord by Goulding (1993)
10.1002/jez.1401280205 / J. Exp. Zool / In vitro studies of cartilage induction in mouse somite mesoderm by Grobstein (1955)
10.1007/BF03023300 / J. Genet / Genetical studies on the skeleton of the mouse. VI. Danforth’s short-tail by Grüneberg (1953)
10.1007/BF02981536 / J. Genet / Genetical studies on the skeleton of the mouse. XII. The development of undulated by Grüneberg (1954)
{'key': '2024121723201103500_DEVELOP_119_3_649C25', 'first-page': '124', 'article-title': 'Genetical studies on the skeleton of the mouse. XXII. The development of Danforth’s short-tail', 'volume': '6', 'author': 'Grüneberg', 'year': '1958', 'journal-title': 'J. Embryol. exp. Morph'} / J. Embryol. exp. Morph / Genetical studies on the skeleton of the mouse. XXII. The development of Danforth’s short-tail by Grüneberg (1958)
10.1016/0092-8674(92)90281-G / Cell / Pax in development by Gruss (1992)
10.1038/350339a0 / Nature / The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system by Hatta (1991)
10.1016/0092-8674(90)90810-2 / Cell / Variations of cervical vertebrae after expression of a Hox-1.1 transgene in mice by Kessel (1990)
10.1016/0092-8674(91)90574-I / Cell / Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid by Kessel (1991)
10.1002/j.1460-2075.1993.tb05990.x / EMBO J / The Brachyury gene encodes a novel DNA binding protein by Kispert (1993)
10.1007/BF00357091 / Mammalian Genome / Fine genetic mapping of the proximal part of mouse Chromosome 2 excludes Pax-8 as a candidate gene for Danforth’s short tail (Sd) by Koseki (1993)
{'key': '2024121723201103500_DEVELOP_119_3_649C32', 'first-page': '255', 'article-title': 'Polarity and patterning of the neural tube : the origin and function of the floor plate', 'volume': '144', 'author': 'Jessell', 'year': '1989', 'journal-title': 'Ciba Found. Symp'} / Ciba Found. Symp / Polarity and patterning of the neural tube : the origin and function of the floor plate by Jessell (1989)
10.1093/nar/12.18.7035 / Nucl. Acids Res / Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promotor by Melton (1984)
{'key': '2024121723201103500_DEVELOP_119_3_649C34', 'first-page': '227', 'article-title': 'Histochemistry of the developing notochord, perichordal sheath and vertebrae in Danforthś short-tail (Sd) and normal C57BL/6 mice', 'volume': '55', 'author': 'Paavola', 'year': '1980', 'journal-title': 'J. Embryol. exp. Morph'} / J. Embryol. exp. Morph / Histochemistry of the developing notochord, perichordal sheath and vertebrae in Danforthś short-tail (Sd) and normal C57BL/6 mice by Paavola (1980)
10.1126/science.2237443 / Science / Mesodermal control of neural cell identity: floor plate induction by the notochord by Placzek (1990)
10.1073/pnas.90.11.5242 / Proc. Natl. Acad. Sci. USA / Control of dorsoventral patterning of somitic derivatives by notochord and floor plate by Pourquie (1993)
10.1016/0168-9525(93)90162-B / Trends Genet / Whole-mount in situ hybridization in the mouse embryo: gene expression in three dimensions by Rosen (1993)
10.1017/S0016672300009496 / Genet. Res., Camb / Curtailed, a new dominant T-allele in the house mouse by Searle (1966)
10.1073/pnas.89.21.10237 / Proc. Natl. Acad. Sci. USA / A role for Quox-8 in the establishment of the dorsoventral pattern during vertebra development by Takahashi (1992)
10.1007/BF01744261 / Anat. Embryol / Development of floor plate, neurons and axonal outgrowth pattern in the early spinal cord of the notochord-deficient chick embryo by van Straaten (1991)
10.1093/oxfordjournals.jhered.a110091 / J. Hered / An inherited agent of mutation with chromosome damage in wild mice by Wallace (1985)
10.1007/BF00128096 / Genetica / A modifier mapped in the mouse by Wallace (1985)
10.1007/BF00360584 / Mammalian Genome / A new Pax gene, Pax-9, maps to mouse chromosome 12 by Wallin (1993)
10.1083/jcb.103.5.1903 / J. Cell Biol / The mammalian β-tubulin repertoire: hematopoietic expression of a novel, heterologous β-tubulin isotype by Wang (1986)
10.1002/aja.1000950302 / Am. J. Anat / The role of the neural tube and notochord in development of the axial skeleton of the chick by Watterson (1954)
10.1038/343657a0 / Nature / Expression pattern of the mouse T gene and its role in mesoderm formation by Wilkinson (1990)
10.1016/0012-1606(91)90086-I / Dev. Biol / The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and Drosophila twist genes by Wolf (1992)
10.1038/hdy.1947.10 / Hered / undulated: a new genetic factor in Mus musculus affecting the spine and tail by Wright (1947)
10.1016/0092-8674(91)90247-V / Cell / Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord by Yamada (1991)
10.1016/0092-8674(93)90248-O / Cell / Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from the notochord and floor plate by Yamada (1993)
10.1016/0012-1606(81)90479-6 / Dev. Biol / Axial structure development in ultraviolet-irradiated (notochord-defective) amphibian embryos by Youn (1980)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 9:24 p.m.)
Deposited	8 months, 1 week ago (Dec. 17, 2024, 6:20 p.m.)
Indexed	8 months, 1 week ago (Dec. 18, 2024, 12:40 a.m.)
Issued	31 years, 9 months ago (Nov. 1, 1993)
Published	31 years, 9 months ago (Nov. 1, 1993)
Published Online	31 years, 9 months ago (Nov. 1, 1993)
Published Print	31 years, 9 months ago (Nov. 1, 1993)

Funders 0

None

BibTeX

@article{Koseki_1993, title={A role for Pax-1 as a mediator of notochordal signals during the dorsoventral specification of vertebrae}, volume={119}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.119.3.649}, DOI={10.1242/dev.119.3.649}, number={3}, journal={Development}, publisher={The Company of Biologists}, author={Koseki, Haruhiko and Wallin, Johan and Wilting, Jörg and Mizutani, Yoko and Kispert, Andreas and Ebensperger, Cecilia and Herrmann, Bernhard G. and Christ, Bodo and Balling, Rudi}, year={1993}, month=nov, pages={649–660} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        12,
        18
      ]
    ],
    "date-time": "2024-12-18T05:40:35Z",
    "timestamp": 1734500435966,
    "version": "3.30.2"
  },
  "reference-count": 51,
  "publisher": "The Company of Biologists",
  "issue": "3",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1993,
            11,
            1
          ]
        ],
        "date-time": "1993-11-01T00:00:00Z",
        "timestamp": 752112000000
      },
      "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": [
      [
        1993,
        11,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>The notochord plays an important role in the differentiation of the paraxial mesoderm and the neural tube. We have analyzed the role of the notochord in somite differentiation and subsequent formation of the vertebral column using a mouse mutant, Danforth\u2019s short-tail (Sd). In this mutant, the skeletal phenotype is most probably a result of degeneration and subsequent loss of the notochord. The Sd gene is known to interact with undulated (un), a sclerotome mutant. Double mutants between Sd and un alleles show an increase in the severity of the defects, mainly in the ventral parts of the vertebrae. We also show that part of the Sd phenotype is strikingly similar to that of the un alleles. As un is known to be caused by a mutation in the Pax-1 gene, we analyzed Pax-1 expression in Sd embryos. In Sd embryos, Pax-1 expression is reduced, providing a potential molecular basis for the genetic interaction observed. A complete loss of Pax-1 expression in morphologically intact mesenchyme was found in the lower thoracic-lumbar region, which is phenotypically very similar to the corresponding region in a Pax-1 null mutant, Undulated short-tail. The sclerotome developmental abnormalities in Sd coincide closely, both in time and space, with notochordal changes, as determined by whole-mount T antibody staining. These findings indicate that an intact notochord is necessary for normal Pax-1 expression in sclerotome cells, which is in turn required for the formation of the ventral parts of the vertebrae. The observed correlation among structural changes of the notochord, Pax-1 expression levels and skeletal phenotypes, suggests that Pax-1 might be an intrinsic mediator of notochordal signals during the dorsoventral specification of vertebrae.</jats:p>",
  "DOI": "10.1242/dev.119.3.649",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T01:24:42Z",
    "timestamp": 1619400282000
  },
  "page": "649-660",
  "source": "Crossref",
  "is-referenced-by-count": 149,
  "title": "A role for <i>Pax-1</i> as a mediator of notochordal signals during the dorsoventral specification of vertebrae",
  "prefix": "10.1242",
  "volume": "119",
  "author": [
    {
      "given": "Haruhiko",
      "family": "Koseki",
      "sequence": "first",
      "affiliation": [
        {
          "name": "1 Department of Developmental Biology, Max-Planck-Institute of Immunobiology, St\u00fcbeweg 51, W-79108 Freiburg, Germany"
        }
      ]
    },
    {
      "given": "Johan",
      "family": "Wallin",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1 Department of Developmental Biology, Max-Planck-Institute of Immunobiology, St\u00fcbeweg 51, W-79108 Freiburg, Germany"
        }
      ]
    },
    {
      "given": "J\u00f6rg",
      "family": "Wilting",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Freiburg University 2 Department of Anatomy , , Albertstrasse 17, W-79104 Freiburg, Germany"
        }
      ]
    },
    {
      "given": "Yoko",
      "family": "Mizutani",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1 Department of Developmental Biology, Max-Planck-Institute of Immunobiology, St\u00fcbeweg 51, W-79108 Freiburg, Germany"
        }
      ]
    },
    {
      "given": "Andreas",
      "family": "Kispert",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "3 Department of Biochemistry, Max-Planck-Institute of Developmental Biology, Spemannstrasse 35, W-72076 T\u00fcbingen, Germany"
        }
      ]
    },
    {
      "given": "Cecilia",
      "family": "Ebensperger",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Freiburg University 2 Department of Anatomy , , Albertstrasse 17, W-79104 Freiburg, Germany"
        }
      ]
    },
    {
      "given": "Bernhard G.",
      "family": "Herrmann",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "3 Department of Biochemistry, Max-Planck-Institute of Developmental Biology, Spemannstrasse 35, W-72076 T\u00fcbingen, Germany"
        }
      ]
    },
    {
      "given": "Bodo",
      "family": "Christ",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Freiburg University 2 Department of Anatomy , , Albertstrasse 17, W-79104 Freiburg, Germany"
        }
      ]
    },
    {
      "given": "Rudi",
      "family": "Balling",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "1 Department of Developmental Biology, Max-Planck-Institute of Immunobiology, St\u00fcbeweg 51, W-79108 Freiburg, Germany"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1993,
        11,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C1",
      "doi-asserted-by": "publisher",
      "first-page": "409",
      "DOI": "10.1002/jez.1401320303",
      "article-title": "An experimental analysis of the development of the spinal column, V. Reactivity of chick somites",
      "volume": "132",
      "author": "Avery",
      "year": "1956",
      "journal-title": "J. Exp. Zool"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C2",
      "doi-asserted-by": "publisher",
      "first-page": "531",
      "DOI": "10.1016/0092-8674(88)90039-6",
      "article-title": "undulated, a mutation affecting the development of the mouse skeleton, has a point mutation in the paired box of Pax-1",
      "volume": "55",
      "author": "Balling",
      "year": "1988",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C3",
      "first-page": "132",
      "article-title": "Development of the skeletal system",
      "volume": "165",
      "author": "Balling",
      "year": "1991",
      "journal-title": "Ciba Found. Symp"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C4",
      "first-page": "43",
      "article-title": "Sut allelic with un",
      "volume": "52",
      "author": "Blandova",
      "year": "1975",
      "journal-title": "Mouse News Lett"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C5",
      "doi-asserted-by": "publisher",
      "first-page": "1033",
      "DOI": "10.1016/0092-8674(86)90818-4",
      "article-title": "Conservation of a large protein domain in the segmentation gene Paired and in functionally related genes of Drosophila",
      "volume": "47",
      "author": "Bopp",
      "year": "1986",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C6",
      "doi-asserted-by": "publisher",
      "first-page": "625",
      "DOI": "10.1242/dev.113.2.625",
      "article-title": "Perturbation of neuronal differentiation and axon guidance in the spinal cord of mouse embryos lacking a floor plate: analysis of Danforth\u2019s short-tail mutation",
      "volume": "113",
      "author": "Bovolenta",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C7",
      "article-title": "The ventralizing effect of the notochord on somite differentiation",
      "volume-title": "Anat. Embryol. (in press)",
      "author": "Brand-Saberi",
      "year": "1993"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C8",
      "doi-asserted-by": "publisher",
      "first-page": "299",
      "DOI": "10.1093/oxfordjournals.jhered.a109648",
      "article-title": "Perichordal sheath of heterozygous and homozygous Danforth\u2019s short-tail mice",
      "volume": "73",
      "author": "Center",
      "year": "1982",
      "journal-title": "J. Hered"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C9",
      "doi-asserted-by": "publisher",
      "first-page": "873",
      "DOI": "10.1016/0092-8674(91)90434-Z",
      "article-title": "The molecular basis of the undulated/Pax-1 mutation",
      "volume": "66",
      "author": "Chalepakis",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C10",
      "doi-asserted-by": "publisher",
      "first-page": "23",
      "DOI": "10.1016/S0940-9602(11)80337-7",
      "article-title": "From somites to vertebral column",
      "volume": "174",
      "author": "Christ",
      "year": "1992",
      "journal-title": "Ann. Anat"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C11",
      "doi-asserted-by": "publisher",
      "first-page": "185",
      "DOI": "10.1016/0012-1606(65)90027-8",
      "article-title": "Induction of somite chondrogenesis by cartilage and notochord: A correlation between inductive activity and specific stages of cytodifferentiation",
      "volume": "12",
      "author": "Cooper",
      "year": "1965",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C12",
      "doi-asserted-by": "publisher",
      "first-page": "299",
      "DOI": "10.1002/jez.1401320207",
      "article-title": "The developmental dependence of the vertebral column upon the spinal cord in the urodele",
      "volume": "132",
      "author": "Detwiler",
      "year": "1956",
      "journal-title": "J. Exp. Zool"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C13",
      "doi-asserted-by": "publisher",
      "first-page": "617",
      "DOI": "10.1016/0092-8674(88)90577-6",
      "article-title": "Pax-1, a member of a paired box homologous murine gene family, is expressed in segmented structures during development",
      "volume": "53",
      "author": "Deutsch",
      "year": "1988",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C14",
      "doi-asserted-by": "publisher",
      "first-page": "423",
      "DOI": "10.1093/genetics/131.2.423",
      "article-title": "A genetic map of the mouse suitable for typing intraspecific crosses",
      "volume": "131",
      "author": "Dietrich",
      "year": "1992",
      "journal-title": "Genetics"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C15",
      "doi-asserted-by": "publisher",
      "first-page": "343",
      "DOI": "10.1093/oxfordjournals.jhered.a104924",
      "article-title": "A new mutation in the mouse affecting spinal column and urogenital system",
      "volume": "31",
      "author": "Dunn",
      "year": "1940",
      "journal-title": "J. Hered"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C16",
      "doi-asserted-by": "publisher",
      "first-page": "767",
      "DOI": "10.1016/0092-8674(91)90071-6",
      "article-title": "splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3",
      "volume": "67",
      "author": "Epstein",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C17",
      "doi-asserted-by": "crossref",
      "first-page": "153",
      "DOI": "10.1007/BF00171747",
      "article-title": "The splotch mutation interferes with muscle development in the limbs",
      "volume": "187",
      "author": "Franz",
      "year": "1993",
      "journal-title": "Anat. Embryol"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C18",
      "doi-asserted-by": "publisher",
      "first-page": "2633",
      "DOI": "10.1021/bi00709a025",
      "article-title": "Ribonucleic acid isolated by cesium chloride centrifugation",
      "volume": "13",
      "author": "Glisin",
      "year": "1974",
      "journal-title": "Biochemistry"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C19",
      "doi-asserted-by": "publisher",
      "first-page": "29",
      "DOI": "10.1093/genetics/30.1.29",
      "article-title": "The embryonic development of mutants of the Sd-strain in mice",
      "volume": "30",
      "author": "Gluecksohn-Schoenheimer",
      "year": "1945",
      "journal-title": "Genetics"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C20",
      "doi-asserted-by": "publisher",
      "first-page": "1135",
      "DOI": "10.1002/j.1460-2075.1991.tb08054.x",
      "article-title": "Pax-3, a novel murine DNA binding protein expressed during early neurogenesis",
      "volume": "10",
      "author": "Goulding",
      "year": "1991",
      "journal-title": "EMBO J"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C21",
      "doi-asserted-by": "publisher",
      "first-page": "1001",
      "DOI": "10.1242/dev.117.3.1001",
      "article-title": "Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord",
      "volume": "117",
      "author": "Goulding",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C22",
      "doi-asserted-by": "publisher",
      "first-page": "333",
      "DOI": "10.1002/jez.1401280205",
      "article-title": "In vitro studies of cartilage induction in mouse somite mesoderm",
      "volume": "128",
      "author": "Grobstein",
      "year": "1955",
      "journal-title": "J. Exp. Zool"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C23",
      "doi-asserted-by": "publisher",
      "first-page": "317",
      "DOI": "10.1007/BF03023300",
      "article-title": "Genetical studies on the skeleton of the mouse. VI. Danforth\u2019s short-tail",
      "volume": "51",
      "author": "Gr\u00fcneberg",
      "year": "1953",
      "journal-title": "J. Genet"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C24",
      "doi-asserted-by": "publisher",
      "first-page": "441",
      "DOI": "10.1007/BF02981536",
      "article-title": "Genetical studies on the skeleton of the mouse. XII. The development of undulated",
      "volume": "52",
      "author": "Gr\u00fcneberg",
      "year": "1954",
      "journal-title": "J. Genet"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C25",
      "first-page": "124",
      "article-title": "Genetical studies on the skeleton of the mouse. XXII. The development of Danforth\u2019s short-tail",
      "volume": "6",
      "author": "Gr\u00fcneberg",
      "year": "1958",
      "journal-title": "J. Embryol. exp. Morph"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C26",
      "doi-asserted-by": "publisher",
      "first-page": "719",
      "DOI": "10.1016/0092-8674(92)90281-G",
      "article-title": "Pax in development",
      "volume": "69",
      "author": "Gruss",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C27",
      "doi-asserted-by": "publisher",
      "first-page": "339",
      "DOI": "10.1038/350339a0",
      "article-title": "The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system",
      "volume": "350",
      "author": "Hatta",
      "year": "1991",
      "journal-title": "Nature"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C28",
      "doi-asserted-by": "publisher",
      "first-page": "301",
      "DOI": "10.1016/0092-8674(90)90810-2",
      "article-title": "Variations of cervical vertebrae after expression of a Hox-1.1 transgene in mice",
      "volume": "61",
      "author": "Kessel",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C29",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1016/0092-8674(91)90574-I",
      "article-title": "Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid",
      "volume": "67",
      "author": "Kessel",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C30",
      "doi-asserted-by": "publisher",
      "first-page": "3211",
      "DOI": "10.1002/j.1460-2075.1993.tb05990.x",
      "article-title": "The Brachyury gene encodes a novel DNA binding protein",
      "volume": "12",
      "author": "Kispert",
      "year": "1993",
      "journal-title": "EMBO J"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C31",
      "doi-asserted-by": "publisher",
      "first-page": "324",
      "DOI": "10.1007/BF00357091",
      "article-title": "Fine genetic mapping of the proximal part of mouse Chromosome 2 excludes Pax-8 as a candidate gene for Danforth\u2019s short tail (Sd)",
      "volume": "4",
      "author": "Koseki",
      "year": "1993",
      "journal-title": "Mammalian Genome"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C32",
      "first-page": "255",
      "article-title": "Polarity and patterning of the neural tube : the origin and function of the floor plate",
      "volume": "144",
      "author": "Jessell",
      "year": "1989",
      "journal-title": "Ciba Found. Symp"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C33",
      "doi-asserted-by": "publisher",
      "first-page": "7035",
      "DOI": "10.1093/nar/12.18.7035",
      "article-title": "Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promotor",
      "volume": "12",
      "author": "Melton",
      "year": "1984",
      "journal-title": "Nucl. Acids Res"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C34",
      "first-page": "227",
      "article-title": "Histochemistry of the developing notochord, perichordal sheath and vertebrae in Danforth\u015b short-tail (Sd) and normal C57BL/6 mice",
      "volume": "55",
      "author": "Paavola",
      "year": "1980",
      "journal-title": "J. Embryol. exp. Morph"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C35",
      "doi-asserted-by": "publisher",
      "first-page": "985",
      "DOI": "10.1126/science.2237443",
      "article-title": "Mesodermal control of neural cell identity: floor plate induction by the notochord",
      "volume": "250",
      "author": "Placzek",
      "year": "1990",
      "journal-title": "Science"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C36",
      "doi-asserted-by": "publisher",
      "first-page": "5242",
      "DOI": "10.1073/pnas.90.11.5242",
      "article-title": "Control of dorsoventral patterning of somitic derivatives by notochord and floor plate",
      "volume": "90",
      "author": "Pourquie",
      "year": "1993",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C37",
      "doi-asserted-by": "publisher",
      "first-page": "162",
      "DOI": "10.1016/0168-9525(93)90162-B",
      "article-title": "Whole-mount in situ hybridization in the mouse embryo: gene expression in three dimensions",
      "volume": "9",
      "author": "Rosen",
      "year": "1993",
      "journal-title": "Trends Genet"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C38",
      "doi-asserted-by": "publisher",
      "first-page": "86",
      "DOI": "10.1017/S0016672300009496",
      "article-title": "Curtailed, a new dominant T-allele in the house mouse",
      "volume": "7",
      "author": "Searle",
      "year": "1966",
      "journal-title": "Genet. Res., Camb"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C39",
      "doi-asserted-by": "publisher",
      "first-page": "10237",
      "DOI": "10.1073/pnas.89.21.10237",
      "article-title": "A role for Quox-8 in the establishment of the dorsoventral pattern during vertebra development",
      "volume": "89",
      "author": "Takahashi",
      "year": "1992",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C40",
      "doi-asserted-by": "publisher",
      "first-page": "55",
      "DOI": "10.1007/BF01744261",
      "article-title": "Development of floor plate, neurons and axonal outgrowth pattern in the early spinal cord of the notochord-deficient chick embryo",
      "volume": "184",
      "author": "van Straaten",
      "year": "1991",
      "journal-title": "Anat. Embryol"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C41",
      "doi-asserted-by": "publisher",
      "first-page": "271",
      "DOI": "10.1093/oxfordjournals.jhered.a110091",
      "article-title": "An inherited agent of mutation with chromosome damage in wild mice",
      "volume": "76",
      "author": "Wallace",
      "year": "1985",
      "journal-title": "J. Hered"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C42",
      "doi-asserted-by": "publisher",
      "first-page": "529",
      "DOI": "10.1007/BF00128096",
      "article-title": "A modifier mapped in the mouse",
      "volume": "46",
      "author": "Wallace",
      "year": "1985",
      "journal-title": "Genetica"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C43",
      "doi-asserted-by": "publisher",
      "first-page": "354",
      "DOI": "10.1007/BF00360584",
      "article-title": "A new Pax gene, Pax-9, maps to mouse chromosome 12",
      "volume": "4",
      "author": "Wallin",
      "year": "1993",
      "journal-title": "Mammalian Genome"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C44",
      "doi-asserted-by": "publisher",
      "first-page": "1903",
      "DOI": "10.1083/jcb.103.5.1903",
      "article-title": "The mammalian \u03b2-tubulin repertoire: hematopoietic expression of a novel, heterologous \u03b2-tubulin isotype",
      "volume": "103",
      "author": "Wang",
      "year": "1986",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C45",
      "doi-asserted-by": "publisher",
      "first-page": "337",
      "DOI": "10.1002/aja.1000950302",
      "article-title": "The role of the neural tube and notochord in development of the axial skeleton of the chick",
      "volume": "95",
      "author": "Watterson",
      "year": "1954",
      "journal-title": "Am. J. Anat"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C46",
      "doi-asserted-by": "publisher",
      "first-page": "657",
      "DOI": "10.1038/343657a0",
      "article-title": "Expression pattern of the mouse T gene and its role in mesoderm formation",
      "volume": "343",
      "author": "Wilkinson",
      "year": "1990",
      "journal-title": "Nature"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C47",
      "doi-asserted-by": "publisher",
      "first-page": "363",
      "DOI": "10.1016/0012-1606(91)90086-I",
      "article-title": "The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and Drosophila twist genes",
      "volume": "143",
      "author": "Wolf",
      "year": "1992",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C48",
      "doi-asserted-by": "publisher",
      "first-page": "137",
      "DOI": "10.1038/hdy.1947.10",
      "article-title": "undulated: a new genetic factor in Mus musculus affecting the spine and tail",
      "volume": "1",
      "author": "Wright",
      "year": "1947",
      "journal-title": "Hered"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C49",
      "doi-asserted-by": "publisher",
      "first-page": "635",
      "DOI": "10.1016/0092-8674(91)90247-V",
      "article-title": "Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord",
      "volume": "64",
      "author": "Yamada",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C50",
      "doi-asserted-by": "publisher",
      "first-page": "673",
      "DOI": "10.1016/0092-8674(93)90248-O",
      "article-title": "Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from the notochord and floor plate",
      "volume": "73",
      "author": "Yamada",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2024121723201103500_DEVELOP_119_3_649C51",
      "doi-asserted-by": "publisher",
      "first-page": "339",
      "DOI": "10.1016/0012-1606(81)90479-6",
      "article-title": "Axial structure development in ultraviolet-irradiated (notochord-defective) amphibian embryos",
      "volume": "83",
      "author": "Youn",
      "year": "1980",
      "journal-title": "Dev. Biol"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/119/3/649/3593146/develop_119_3_649.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/119/3/649/3593146/develop_119_3_649.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        12,
        17
      ]
    ],
    "date-time": "2024-12-17T23:20:29Z",
    "timestamp": 1734477629000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/119/3/649/37972/A-role-for-Pax-1-as-a-mediator-of-notochordal"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1993,
        11,
        1
      ]
    ]
  },
  "references-count": 51,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          1993,
          11,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.119.3.649",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1993,
        11,
        1
      ]
    ]
  }
}