DOI: 10.1101/gad.189801. <i>Krox-20</i> patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms

Krox-20 patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms

10.1101/gad.189801

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

The Krox-20 gene encodes a zinc finger transcription factor, which has been shown previously, by targeted inactivation in the mouse, to be required for the development of rhombomeres (r) 3 and 5 in the segmented embryonic hindbrain. In the present work, Krox-20 was expressed ectopically in the developing chick hindbrain by use of electroporation. We demonstrate that Krox-20 expression is sufficient to confer odd-numbered rhombomere characteristics to r2, r4, and r6 cells, presumably in a cell-autonomous manner. Therefore, Krox-20, appears as the major determinant of odd-numbered identity within the hindbrain. In addition, we provide evidence for the existence of a non cell-autonomous autoactivation mechanism allowing recruitment of Krox-20-positive cells from even-numbered territories by neighboring Krox-20-expressing cells. On the basis of these observations, we propose that Krox-20 regulates multiple, intertwined steps in segmental patterning: Initial activation of Krox-20 in a few cells leads to the segregation, homogenization, and possibly expansion of territories to which Krox-20 in addition confers an odd-numbered identity.

Bibliography

Giudicelli, F., Taillebourg, E., Charnay, P., & Gilardi-Hebenstreit, P. (2001). Krox-20 patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms. Genes & Development, 15(5), 567â580.

Authors 4

François Giudicelli (first)
Emmanuel Taillebourg (additional)
Patrick Charnay (additional)
Pascale Gilardi-Hebenstreit (additional)

References 53 Referenced 100

10.1177/29.6.7252134
10.1242/dev.127.5.933 / Development / Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse. by Barrow (2000)
10.1016/0014-5793(95)00652-P
10.1242/dev.120.6.1347 / Development / Violation of cell lineage restriction compartments in the chick hindbrain. by Birgbauer (1994)
{'key': '2021111507331945000_15.5.567.5', 'first-page': '53', 'article-title': 'Patterning of the vertebrate neural crest.', 'volume': '3', 'author': 'Bronner-Fraser', 'year': '1995', 'journal-title': 'Perspect. Dev. Neurobiol.'} / Perspect. Dev. Neurobiol. / Patterning of the vertebrate neural crest. by Bronner-Fraser (1995)
10.1002/j.1460-2075.1988.tb02780.x / EMBO J. / A gene encoding a protein with zinc fingers is activated during G0/G1 transition in cultured cells. by Chavrier (1988)
{'key': '2021111507331945000_15.5.567.7', 'first-page': '787', 'article-title': 'Structure, chromosome location, and expression of the mouse zinc finger gene Krox-20: Multiple gene products and coregulation with the proto-oncogene c-fos.', 'volume': '9', 'author': 'Chavrier', 'year': '1989', 'journal-title': 'Mol. Cell. Biol .'} / Mol. Cell. Biol . / Structure, chromosome location, and expression of the mouse zinc finger gene Krox-20: Multiple gene products and coregulation with the proto-oncogene c-fos. by Chavrier (1989)
10.1007/s003350010068
10.1016/S0925-4773(97)00063-4
10.1038/344431a0
{'key': '2021111507331945000_15.5.567.11', 'first-page': '5848', 'article-title': 'The encephalomyocarditis virus internal ribosome entry site allows efficient coexpression of two genes from a recombinant provirus in cultured cells and in embryos.', 'volume': '11', 'author': 'Ghattas', 'year': '1991', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / The encephalomyocarditis virus internal ribosome entry site allows efficient coexpression of two genes from a recombinant provirus in cultured cells and in embryos. by Ghattas (1991)
{'key': '2021111507331945000_15.5.567.12', 'first-page': '2499', 'article-title': 'An Eph-related receptor protein tyrosine kinase gene segmentally expressed in the developing mouse hindbrain.', 'volume': '7', 'author': 'Gilardi-Hebenstreit', 'year': '1992', 'journal-title': 'Oncogene'} / Oncogene / An Eph-related receptor protein tyrosine kinase gene segmentally expressed in the developing mouse hindbrain. by Gilardi-Hebenstreit (1992)
10.1242/dev.122.2.473 / Development / Interactions between rhombomeres modulate Krox-20 and follistatin expression in the chick embryo hindbrain. by Graham (1996)
10.1242/dev.121.9.2707 / Development / Plasticity of transposed rhombomeres: Hox gene induction is correlated with phenotypic modifications. by Grapin-Botton (1995)
10.1242/dev.112.1.221 / Development / Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. by Guthrie (1991)
10.1038/356157a0
10.1242/dev.118.2.527 / Development / Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts. by Guthrie (1993)
10.1002/jmor.1050880104
10.1242/dev.125.23.4739 / Development / Hoxa1 and krox-20 synergize to control the development of rhombomere 3. by Helmbacher (1998)
10.1007/s004290050130
10.1006/dbio.1996.0004
10.1038/70231
10.1242/dev.122.10.3229 / Development / Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. by Kontges (1996)
10.1126/science.8382374
10.1016/0166-2236(90)90144-Y
10.1038/337424a0
10.1126/science.274.5290.1109
10.1006/dbio.1999.9318
10.1242/dev.127.22.4925 / Development / Hindbrain patterning: FGFs regulate krox20 and mafB/kr expression in the otic/preotic region. by Marin (2000)
10.1242/dev.127.1.119 / Development / Nab proteins mediate a negative feedback loop controlling Krox-20 activity in the developing hindbrain. by Mechta-Grigoriou (2000)
10.1038/21907
10.1016/S0959-4388(00)00095-7
10.1006/mthe.2000.0050
10.1242/dev.111.1.61 / Development / Expression of the mouse labial-like homeobox-containing genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain. by Murphy (1991)
Nieto, M.A., Bradley, L.C., and Wilkinson, D.G. 1991. Conserved segmental expression of Krox-20 in the vertebrate hindbrain and its relationship to lineage restriction. Development (Suppl.) 59–62.. (10.1242/dev.113.Supplement_2.59)
10.1242/dev.122.2.543 / Development / Segmental expression of Hoxa-2 in the hindbrain is directly regulated by Krox-20. by Nonchev (1996)
10.1242/dev.120.4.911 / Development / Hoxa-2 expression in normal and transposed rhombomeres: Independent regulation in the neural tube and neural crest. by Prince (1994)
{'key': '2021111507331945000_15.5.567.38', 'first-page': '1807', 'article-title': 'Five novel avian Eph-related tyrosine kinases are differentially expressed.', 'volume': '8', 'author': 'Sajjadi', 'year': '1993', 'journal-title': 'Oncogene'} / Oncogene / Five novel avian Eph-related tyrosine kinases are differentially expressed. by Sajjadi (1993)
10.1016/0092-8674(93)90329-O
10.1016/S0764-4469(99)80022-5 / C.R. Acad. Sci. Iii / How to build a vertebrate hindbrain. Lessons from genetics. by Schneider-Maunoury (1998)
10.1016/S0925-4773(97)00051-8
10.1016/0092-8674(93)90659-E
10.1038/384630a0
10.1101/gad.4.8.1267
10.1242/dev.125.3.443 / Development / Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20. by Theil (1998)
10.1038/371796a0
{'key': '2021111507331945000_15.5.567.47', 'first-page': '3', 'article-title': 'The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological, histochemical and autoradiographical investigation.', 'volume': '41', 'author': 'Vaage', 'year': '1969', 'journal-title': 'Ergeb Anat. Entwicklungsgesch'} / Ergeb Anat. Entwicklungsgesch / The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological, histochemical and autoradiographical investigation. by Vaage (1969)
10.1093/nar/20.10.2485
10.1038/ng0498-382
10.1093/hmg/8.7.1245
10.1016/0076-6879(93)25025-W
10.1038/337461a0
10.1038/20452

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 8 p.m.)
Deposited	3 years, 9 months ago (Nov. 15, 2021, 10:34 a.m.)
Indexed	1 week, 1 day ago (Aug. 29, 2025, 6:41 a.m.)
Issued	24 years, 6 months ago (March 1, 2001)
Published	24 years, 6 months ago (March 1, 2001)
Published Online	24 years, 6 months ago (March 1, 2001)
Published Print	24 years, 6 months ago (March 1, 2001)

Funders 0

None

BibTeX

@article{Giudicelli_2001, title={Krox-20 patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms}, volume={15}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.189801}, DOI={10.1101/gad.189801}, number={5}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Giudicelli, François and Taillebourg, Emmanuel and Charnay, Patrick and Gilardi-Hebenstreit, Pascale}, year={2001}, month=mar, pages={567–580} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        29
      ]
    ],
    "date-time": "2025-08-29T10:41:16Z",
    "timestamp": 1756464076957
  },
  "reference-count": 53,
  "publisher": "Cold Spring Harbor Laboratory",
  "issue": "5",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        3,
        1
      ]
    ]
  },
  "abstract": "<jats:p>The <jats:italic>Krox-20</jats:italic> gene encodes a zinc finger transcription factor, which has been shown previously, by targeted inactivation in the mouse, to be required for the development of rhombomeres (r) 3 and 5 in the segmented embryonic hindbrain. In the present work, <jats:italic>Krox-20</jats:italic> was expressed ectopically in the developing chick hindbrain by use of electroporation. We demonstrate that <jats:italic>Krox-20</jats:italic> expression is sufficient to confer odd-numbered rhombomere characteristics to r2, r4, and r6 cells, presumably in a cell-autonomous manner. Therefore, Krox-20, appears as the major determinant of odd-numbered identity within the hindbrain. In addition, we provide evidence for the existence of a non cell-autonomous autoactivation mechanism allowing recruitment of <jats:italic>Krox-20</jats:italic>-positive cells from even-numbered territories by neighboring <jats:italic>Krox-20</jats:italic>-expressing cells. On the basis of these observations, we propose that <jats:italic>Krox-20</jats:italic> regulates multiple, intertwined steps in segmental patterning: Initial activation of <jats:italic>Krox-20</jats:italic> in a few cells leads to the segregation, homogenization, and possibly expansion of territories to which Krox-20 in addition confers an odd-numbered identity.</jats:p>",
  "DOI": "10.1101/gad.189801",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        27
      ]
    ],
    "date-time": "2002-07-27T00:00:34Z",
    "timestamp": 1027728034000
  },
  "page": "567-580",
  "source": "Crossref",
  "is-referenced-by-count": 100,
  "title": "<i>Krox-20</i> patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms",
  "prefix": "10.1101",
  "volume": "15",
  "author": [
    {
      "given": "Fran\u00e7ois",
      "family": "Giudicelli",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Emmanuel",
      "family": "Taillebourg",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Patrick",
      "family": "Charnay",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Pascale",
      "family": "Gilardi-Hebenstreit",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "246",
  "published-online": {
    "date-parts": [
      [
        2001,
        3,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2021111507331945000_15.5.567.1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1177/29.6.7252134"
    },
    {
      "key": "2021111507331945000_15.5.567.2",
      "doi-asserted-by": "crossref",
      "first-page": "933",
      "DOI": "10.1242/dev.127.5.933",
      "article-title": "Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse.",
      "volume": "127",
      "author": "Barrow",
      "year": "2000",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(95)00652-P"
    },
    {
      "key": "2021111507331945000_15.5.567.4",
      "doi-asserted-by": "crossref",
      "first-page": "1347",
      "DOI": "10.1242/dev.120.6.1347",
      "article-title": "Violation of cell lineage restriction compartments in the chick hindbrain.",
      "volume": "120",
      "author": "Birgbauer",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.5",
      "first-page": "53",
      "article-title": "Patterning of the vertebrate neural crest.",
      "volume": "3",
      "author": "Bronner-Fraser",
      "year": "1995",
      "journal-title": "Perspect. Dev. Neurobiol."
    },
    {
      "key": "2021111507331945000_15.5.567.6",
      "doi-asserted-by": "crossref",
      "first-page": "29",
      "DOI": "10.1002/j.1460-2075.1988.tb02780.x",
      "article-title": "A gene encoding a protein with zinc fingers is activated during G0/G1 transition in cultured cells.",
      "volume": "7",
      "author": "Chavrier",
      "year": "1988",
      "journal-title": "EMBO J."
    },
    {
      "key": "2021111507331945000_15.5.567.7",
      "first-page": "787",
      "article-title": "Structure, chromosome location, and expression of the mouse zinc finger gene Krox-20: Multiple gene products and coregulation with the proto-oncogene c-fos.",
      "volume": "9",
      "author": "Chavrier",
      "year": "1989",
      "journal-title": "Mol. Cell. Biol ."
    },
    {
      "key": "2021111507331945000_15.5.567.8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s003350010068"
    },
    {
      "key": "2021111507331945000_15.5.567.9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0925-4773(97)00063-4"
    },
    {
      "key": "2021111507331945000_15.5.567.10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/344431a0"
    },
    {
      "key": "2021111507331945000_15.5.567.11",
      "first-page": "5848",
      "article-title": "The encephalomyocarditis virus internal ribosome entry site allows efficient coexpression of two genes from a recombinant provirus in cultured cells and in embryos.",
      "volume": "11",
      "author": "Ghattas",
      "year": "1991",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111507331945000_15.5.567.12",
      "first-page": "2499",
      "article-title": "An Eph-related receptor protein tyrosine kinase gene segmentally expressed in the developing mouse hindbrain.",
      "volume": "7",
      "author": "Gilardi-Hebenstreit",
      "year": "1992",
      "journal-title": "Oncogene"
    },
    {
      "key": "2021111507331945000_15.5.567.13",
      "doi-asserted-by": "crossref",
      "first-page": "473",
      "DOI": "10.1242/dev.122.2.473",
      "article-title": "Interactions between rhombomeres modulate Krox-20 and follistatin expression in the chick embryo hindbrain.",
      "volume": "122",
      "author": "Graham",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.14",
      "doi-asserted-by": "crossref",
      "first-page": "2707",
      "DOI": "10.1242/dev.121.9.2707",
      "article-title": "Plasticity of transposed rhombomeres: Hox gene induction is correlated with phenotypic modifications.",
      "volume": "121",
      "author": "Grapin-Botton",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.15",
      "doi-asserted-by": "crossref",
      "first-page": "221",
      "DOI": "10.1242/dev.112.1.221",
      "article-title": "Formation and regeneration of rhombomere boundaries in the developing chick hindbrain.",
      "volume": "112",
      "author": "Guthrie",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/356157a0"
    },
    {
      "key": "2021111507331945000_15.5.567.17",
      "doi-asserted-by": "crossref",
      "first-page": "527",
      "DOI": "10.1242/dev.118.2.527",
      "article-title": "Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts.",
      "volume": "118",
      "author": "Guthrie",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.18",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jmor.1050880104"
    },
    {
      "key": "2021111507331945000_15.5.567.19",
      "doi-asserted-by": "crossref",
      "first-page": "4739",
      "DOI": "10.1242/dev.125.23.4739",
      "article-title": "Hoxa1 and krox-20 synergize to control the development of rhombomere 3.",
      "volume": "125",
      "author": "Helmbacher",
      "year": "1998",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s004290050130"
    },
    {
      "key": "2021111507331945000_15.5.567.21",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1996.0004"
    },
    {
      "key": "2021111507331945000_15.5.567.22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/70231"
    },
    {
      "key": "2021111507331945000_15.5.567.23",
      "doi-asserted-by": "crossref",
      "first-page": "3229",
      "DOI": "10.1242/dev.122.10.3229",
      "article-title": "Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny.",
      "volume": "122",
      "author": "Kontges",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8382374"
    },
    {
      "key": "2021111507331945000_15.5.567.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0166-2236(90)90144-Y"
    },
    {
      "key": "2021111507331945000_15.5.567.26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/337424a0"
    },
    {
      "key": "2021111507331945000_15.5.567.27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.274.5290.1109"
    },
    {
      "key": "2021111507331945000_15.5.567.28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1999.9318"
    },
    {
      "key": "2021111507331945000_15.5.567.29",
      "doi-asserted-by": "crossref",
      "first-page": "4925",
      "DOI": "10.1242/dev.127.22.4925",
      "article-title": "Hindbrain patterning: FGFs regulate krox20 and mafB/kr expression in the otic/preotic region.",
      "volume": "127",
      "author": "Marin",
      "year": "2000",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.30",
      "doi-asserted-by": "crossref",
      "first-page": "119",
      "DOI": "10.1242/dev.127.1.119",
      "article-title": "Nab proteins mediate a negative feedback loop controlling Krox-20 activity in the developing hindbrain.",
      "volume": "127",
      "author": "Mechta-Grigoriou",
      "year": "2000",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/21907"
    },
    {
      "key": "2021111507331945000_15.5.567.32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0959-4388(00)00095-7"
    },
    {
      "key": "2021111507331945000_15.5.567.33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/mthe.2000.0050"
    },
    {
      "key": "2021111507331945000_15.5.567.34",
      "doi-asserted-by": "crossref",
      "first-page": "61",
      "DOI": "10.1242/dev.111.1.61",
      "article-title": "Expression of the mouse labial-like homeobox-containing genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain.",
      "volume": "111",
      "author": "Murphy",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.35",
      "doi-asserted-by": "crossref",
      "unstructured": "Nieto, M.A., Bradley, L.C., and Wilkinson, D.G. 1991. Conserved segmental expression of Krox-20 in the vertebrate hindbrain and its relationship to lineage restriction. Development (Suppl.) 59\u201362..",
      "DOI": "10.1242/dev.113.Supplement_2.59"
    },
    {
      "key": "2021111507331945000_15.5.567.36",
      "doi-asserted-by": "crossref",
      "first-page": "543",
      "DOI": "10.1242/dev.122.2.543",
      "article-title": "Segmental expression of Hoxa-2 in the hindbrain is directly regulated by Krox-20.",
      "volume": "122",
      "author": "Nonchev",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.37",
      "doi-asserted-by": "crossref",
      "first-page": "911",
      "DOI": "10.1242/dev.120.4.911",
      "article-title": "Hoxa-2 expression in normal and transposed rhombomeres: Independent regulation in the neural tube and neural crest.",
      "volume": "120",
      "author": "Prince",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.38",
      "first-page": "1807",
      "article-title": "Five novel avian Eph-related tyrosine kinases are differentially expressed.",
      "volume": "8",
      "author": "Sajjadi",
      "year": "1993",
      "journal-title": "Oncogene"
    },
    {
      "key": "2021111507331945000_15.5.567.39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90329-O"
    },
    {
      "key": "2021111507331945000_15.5.567.40",
      "doi-asserted-by": "crossref",
      "first-page": "819",
      "DOI": "10.1016/S0764-4469(99)80022-5",
      "article-title": "How to build a vertebrate hindbrain. Lessons from genetics.",
      "volume": "321",
      "author": "Schneider-Maunoury",
      "year": "1998",
      "journal-title": "C.R. Acad. Sci. Iii"
    },
    {
      "key": "2021111507331945000_15.5.567.41",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0925-4773(97)00051-8"
    },
    {
      "key": "2021111507331945000_15.5.567.42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90659-E"
    },
    {
      "key": "2021111507331945000_15.5.567.43",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/384630a0"
    },
    {
      "key": "2021111507331945000_15.5.567.44",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.4.8.1267"
    },
    {
      "key": "2021111507331945000_15.5.567.45",
      "doi-asserted-by": "crossref",
      "first-page": "443",
      "DOI": "10.1242/dev.125.3.443",
      "article-title": "Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20.",
      "volume": "125",
      "author": "Theil",
      "year": "1998",
      "journal-title": "Development"
    },
    {
      "key": "2021111507331945000_15.5.567.46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/371796a0"
    },
    {
      "key": "2021111507331945000_15.5.567.47",
      "first-page": "3",
      "article-title": "The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological, histochemical and autoradiographical investigation.",
      "volume": "41",
      "author": "Vaage",
      "year": "1969",
      "journal-title": "Ergeb Anat. Entwicklungsgesch"
    },
    {
      "key": "2021111507331945000_15.5.567.48",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/20.10.2485"
    },
    {
      "key": "2021111507331945000_15.5.567.49",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ng0498-382"
    },
    {
      "key": "2021111507331945000_15.5.567.50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/hmg/8.7.1245"
    },
    {
      "key": "2021111507331945000_15.5.567.51",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0076-6879(93)25025-W"
    },
    {
      "key": "2021111507331945000_15.5.567.52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/337461a0"
    },
    {
      "key": "2021111507331945000_15.5.567.53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/20452"
    }
  ],
  "container-title": "Genes &amp; Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1101/gad.189801",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        11,
        15
      ]
    ],
    "date-time": "2021-11-15T15:34:57Z",
    "timestamp": 1636990497000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "http://genesdev.cshlp.org/lookup/doi/10.1101/gad.189801"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        3,
        1
      ]
    ]
  },
  "references-count": 53,
  "journal-issue": {
    "issue": "5",
    "published-print": {
      "date-parts": [
        [
          2001,
          3,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1101/gad.189801"
  ],
  "URL": "http://dx.doi.org/10.1101/gad.189801",
  "relation": {},
  "ISSN": [
    "0890-9369",
    "1549-5477"
  ],
  "subject": [],
  "container-title-short": "Genes Dev.",
  "published": {
    "date-parts": [
      [
        2001,
        3,
        1
      ]
    ]
  }
}