DOI: 10.1242/dev.121.12.4077. Lineage restriction of the myogenic conversion factor <i>myf-5</i> in the brain

Lineage restriction of the myogenic conversion factor myf-5 in the brain

10.1242/dev.121.12.4077

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT myf-5 is one of four transcription factors belonging to the MyoD family that play key roles in skeletal muscle determination and differentiation. We have shown earlier by gene targeting nlacZ into the murine myf-5 locus that myf-5 expression in the developing mouse embryo is closely associated with the restriction of precursor muscle cells to the myogenic lineage. We now identify unexpected expression of this myogenic factor in subdomains of the brain. myf-5 expression begins to be detected at embryonic day 8 (E8) in the mesencephalon and coincides with the appearance of the first differentiated neurons; expression in the secondary prosencephalon initiates at E10 and is confined to the ventral domain of prosomere p4, later becoming restricted to the posterior hypothalamus. This expression is observed throughout embryogenesis. No other member of the MyoD family is detected in these regions, consistent with the lack of myogenic conversion. Furthermore, embryonic stem cells expressing the myf-5/nlacZ allele yield both skeletal muscle and neuronal cells when differentiated in vitro. These observations raise questions about the role of myf-5 in neurogenesis as well as myogenesis, and introduce a new lineage marker for the developing brain.

Bibliography

Tajbakhsh, S., & Buckingham, M. E. (1995). Lineage restriction of the myogenic conversion factor myf-5 in the brain. Development, 121(12), 4077â4083.

Authors 2

Shahragim Tajbakhsh (first)
Margaret E. Buckingham (additional)

References 51 Referenced 52

10.1016/0896-6273(90)90348-J / Neuron / Specificity of expression of the muscle and brain dystrophin gene promoters in muscle and brain cells by Barnea (1990)
10.1002/j.1460-2075.1990.tb08179.x / EMBO J / Myf-6 a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12 by Braun (1990)
10.1002/j.1460-2075.1989.tb03429.x / EMBO J / A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts by Braun (1989)
10.1016/0092-8674(92)90507-9 / Cell / Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death by Braun (1992)
10.1016/0168-9525(92)90081-E / Trends Genet / Making muscle in mammals by Buckingham (1992)
{'key': '2025011515212993800_DEVELOP_121_12_4077C6', 'first-page': '1040', 'article-title': 'Expression of myogenic factors in the mouse: myf-5, the first member of the MyoD gene family to be transcribed during skeletal myogenesis', 'volume': '316', 'author': 'Buckingham', 'year': '1993', 'journal-title': 'C. R. Acad. Sci. Paris'} / C. R. Acad. Sci. Paris / Expression of myogenic factors in the mouse: myf-5, the first member of the MyoD gene family to be transcribed during skeletal myogenesis by Buckingham (1993)
10.1523/JNEUROSCI.13-07-03155.1993 / J. Neurosci / Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries by Bulfone (1993)
10.1073/pnas.92.6.2254 / Proc. Natl. Acad. Sci. USA / Myoblast differentiation during mammalian somitogenesis is dependent upon a community effect by Cossu (1995)
10.1016/0092-8674(87)90585-X / Cell / Expression of a single transfected cDNA converts fibroblasts to myoblasts by Davis (1987)
10.1523/JNEUROSCI.13-01-00285.1993 / J. Neurosci / Initial tract formation in the mouse brain by Easter (1993)
10.1242/dev.120.5.1251 / Development / Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis by Edmondson (1994)
10.1101/gad.3.5.628 / Genes Dev / A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program by Edmondson (1989)
10.1038/363630a0 / Nature / Segmental organization of embryonic diencephalon by Figdor (1993)
10.1016/0960-9822(93)90033-K / Curr. Biol / Segmentation moves to the fore by Fraser (1993)
10.1016/0168-9525(89)90097-8 / Trends Genet / Genesis of the Drosophila peripheral nervous system by Ghysen (1989)
10.1016/0092-8674(93)90381-Y / Cell / Mammalian Achaete-Scute homolog-1 is required for the early development of olfactory and autonomic neurons by Guillemot (1993)
{'key': '2025011515212993800_DEVELOP_121_12_4077C17', 'first-page': '255', 'article-title': 'Myogenesis in Xenopus development', 'volume': '3', 'author': 'Gurdon', 'year': '1992', 'journal-title': 'Seminars in Dev. Biol'} / Seminars in Dev. Biol / Myogenesis in Xenopus development by Gurdon (1992)
10.1038/364501a0 / Nature / Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene by Hasty (1993)
10.1083/jcb.119.4.811 / J. Cell Biol / Localization of dystrophin gene transcripts during mouse embryogenesis by Houzelstein (1992)
10.1007/978-1-4757-4951-9 / Developmental Neurobiology by Jacobson (1978)
10.1126/science.7973707 / Science / Activation of the myogenic lineage by MEF-2A, a factor that induces and cooperates with MyoD by Kaushal (1994)
10.1242/jcs.1992.Supplement_16.13 / J. Cell Sci. Suppl / Functional conservation of nematode and vertebrate myogenic regulatory factors by Krause (1992)
10.1016/0092-8674(94)90290-9 / Cell / Hox genes in vertebrate development by Krumlauf (1994)
10.1038/281586a0 / Nature / Neurectoderm markers retained in phenotypical skeletal muscle cells arising from a glial cell line by Lennon (1979)
10.1242/dev.117.3.905 / Development / Two enhancer regions in the mouse En-2 locus direct expression to the mid/hindbrain region and mandibular myoblasts by Logan (1993)
10.1002/aja.1001940203 / Dev. Dynamics / Expression of NCAM isoforms during skeletal myogenesis in the mouse embryo by Lyons (1992)
10.1038/299165a0 / Nature / Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line by McBurney (1982)
10.1016/S0021-9258(19)74594-3 / J. Biol. Chem / In vitro chamber specification during embryonic stem cell cardiogenesis by Miller-Hance (1993)
10.1242/dev.114.4.853 / Development / Skeletal muscle phenotypes initiated by ectopic MyoD in transgenic mouse heart by Miner (1992)
10.1073/pnas.87.3.1089 / Proc. Natl. Acad. Sci. USA / Herculin a fourth member of the MyoD family of myogenic regulatory genes by Miner (1990)
10.1002/cne.902790406 / J. Comp. Neurol / Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti- beta-tubulin monoclonal antibody by Moody (1987)
10.1038/364532a0 / Nature / Myogenin gene disruption results in perinatal lethality because of severe muscle defect [see comments] by Nabeshima (1993)
10.1159/000143177 / Acta anat / The occurrence of striated muscle within the cerebellum of the albino rat by Ohanian (1968)
10.1101/gad.8.1.1 / Genes Dev / bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out by Olson (1994)
10.1242/dev.111.4.1097 / Development / Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo by Ott (1991)
10.1016/0166-2236(93)90080-6 / Trends Neurosci / Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization by Puelles (1993)
10.1101/gad.3.12b.2050 / Genes Dev / Identification of MRF4: a new member of the muscle regulatory factor gene family by Rhodes (1989)
{'key': '2025011515212993800_DEVELOP_121_12_4077C38', 'first-page': '71', 'article-title': 'Embryo-derived stem cell lines', 'volume-title': 'Teratocarcinomas and Embryonic Stem Cells: a Practical Approach', 'author': 'Robertson', 'year': '1987'} / Teratocarcinomas and Embryonic Stem Cells: a Practical Approach / Embryo-derived stem cell lines by Robertson (1987)
10.1016/0092-8674(93)90621-V / Cell / MyoD or myf-5 is required for the formation of skeletal muscle by Rudnicki (1993)
{'key': '2025011515212993800_DEVELOP_121_12_4077C40', 'first-page': '6044', 'article-title': 'Expression of bovine myf-5 induces ectopic skeletal muscle fromation in transgenic mice', 'volume': '13', 'author': 'Santerre', 'year': '1993', 'journal-title': 'Mol. Cell Biol'} / Mol. Cell Biol / Expression of bovine myf-5 induces ectopic skeletal muscle fromation in transgenic mice by Santerre (1993)
10.1038/341303a0 / Nature / Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis by Sassoon (1989)
10.1016/0076-6879(93)25027-Y / Guide to Techniques in Mouse Development / Detection of messenger RNA by in situ hybridization. In Methods in Enzymology by Sassoon (1993)
10.1083/jcb.61.2.398 / J. Cell Biol / Characterization of a unique muscle cell line by Schubert (1974)
10.1073/pnas.91.2.747 / Proc. Natl. Acad. Sci. USA / Mouse limb muscle is determined in the absence of the earliest myogenic factor myf-5 by Tajbakhsh (1994)
10.1016/0896-6273(94)90248-8 / Neuron / A population of myogenic cells derived from the mouse neural tube by Tajbakhsh (1994)
{'key': '2025011515212993800_DEVELOP_121_12_4077C46', 'first-page': '364', 'article-title': 'An embryonic origin for medulloblastoma', 'volume': '3', 'author': 'Valtz', 'year': '1991', 'journal-title': 'New Biologist'} / New Biologist / An embryonic origin for medulloblastoma by Valtz (1991)
10.1111/j.1471-4159.1990.tb04563.x / J. Neurochem / N-cadherin gene maps to human chromosome 18 and is not linked to the E-cadherin gene by Walsh (1990)
10.1016/0955-0674(93)90015-I / Curr. Opin. Cell Biol / POU-domain proteins: structure and function of developmental regulators by Wegner (1993)
10.1126/science.1846704 / Science / The MyoD gene family: nodal point during specification of the muscle cell lineage by Weintraub (1991)
10.1016/0092-8674(89)90583-7 / Cell / Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD by Wright (1989)
10.1016/0896-6273(94)90148-1 / Neuron / Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors by Zimmerman (1994)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 10:14 p.m.)
Deposited	7 months, 2 weeks ago (Jan. 15, 2025, 10:22 a.m.)
Indexed	1 month, 3 weeks ago (July 8, 2025, 7:33 a.m.)
Issued	29 years, 9 months ago (Dec. 1, 1995)
Published	29 years, 9 months ago (Dec. 1, 1995)
Published Online	29 years, 9 months ago (Dec. 1, 1995)
Published Print	29 years, 9 months ago (Dec. 1, 1995)

Funders 0

None

BibTeX

@article{Tajbakhsh_1995, title={Lineage restriction of the myogenic conversion factor myf-5 in the brain}, volume={121}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.121.12.4077}, DOI={10.1242/dev.121.12.4077}, number={12}, journal={Development}, publisher={The Company of Biologists}, author={Tajbakhsh, Shahragim and Buckingham, Margaret E.}, year={1995}, month=dec, pages={4077–4083} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        8
      ]
    ],
    "date-time": "2025-07-08T11:33:03Z",
    "timestamp": 1751974383705,
    "version": "3.33.0"
  },
  "reference-count": 51,
  "publisher": "The Company of Biologists",
  "issue": "12",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1995,
            12,
            1
          ]
        ],
        "date-time": "1995-12-01T00:00:00Z",
        "timestamp": 817776000000
      },
      "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": [
      [
        1995,
        12,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>myf-5 is one of four transcription factors belonging to the MyoD family that play key roles in skeletal muscle determination and differentiation. We have shown earlier by gene targeting nlacZ into the murine myf-5 locus that myf-5 expression in the developing mouse embryo is closely associated with the restriction of precursor muscle cells to the myogenic lineage. We now identify unexpected expression of this myogenic factor in subdomains of the brain. myf-5 expression begins to be detected at embryonic day 8 (E8) in the mesencephalon and coincides with the appearance of the first differentiated neurons; expression in the secondary prosencephalon initiates at E10 and is confined to the ventral domain of prosomere p4, later becoming restricted to the posterior hypothalamus. This expression is observed throughout embryogenesis. No other member of the MyoD family is detected in these regions, consistent with the lack of myogenic conversion. Furthermore, embryonic stem cells expressing the myf-5/nlacZ allele yield both skeletal muscle and neuronal cells when differentiated in vitro. These observations raise questions about the role of myf-5 in neurogenesis as well as myogenesis, and introduce a new lineage marker for the developing brain.</jats:p>",
  "DOI": "10.1242/dev.121.12.4077",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T02:14:52Z",
    "timestamp": 1619403292000
  },
  "page": "4077-4083",
  "source": "Crossref",
  "is-referenced-by-count": 52,
  "title": "Lineage restriction of the myogenic conversion factor <i>myf-5</i> in the brain",
  "prefix": "10.1242",
  "volume": "121",
  "author": [
    {
      "given": "Shahragim",
      "family": "Tajbakhsh",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Molecular Biology, CNRS URA1947, Pasteur Institute, 25 rue du Dr. Roux, 75724 Paris Cedex 15, France"
        }
      ]
    },
    {
      "given": "Margaret E.",
      "family": "Buckingham",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Molecular Biology, CNRS URA1947, Pasteur Institute, 25 rue du Dr. Roux, 75724 Paris Cedex 15, France"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1995,
        12,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C1",
      "doi-asserted-by": "publisher",
      "first-page": "881",
      "DOI": "10.1016/0896-6273(90)90348-J",
      "article-title": "Specificity of expression of the muscle and brain dystrophin gene promoters in muscle and brain cells",
      "volume": "5",
      "author": "Barnea",
      "year": "1990",
      "journal-title": "Neuron"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C2",
      "doi-asserted-by": "publisher",
      "first-page": "821",
      "DOI": "10.1002/j.1460-2075.1990.tb08179.x",
      "article-title": "Myf-6 a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12",
      "volume": "9",
      "author": "Braun",
      "year": "1990",
      "journal-title": "EMBO J"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C3",
      "doi-asserted-by": "publisher",
      "first-page": "701",
      "DOI": "10.1002/j.1460-2075.1989.tb03429.x",
      "article-title": "A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts",
      "volume": "8",
      "author": "Braun",
      "year": "1989",
      "journal-title": "EMBO J"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C4",
      "doi-asserted-by": "publisher",
      "first-page": "369",
      "DOI": "10.1016/0092-8674(92)90507-9",
      "article-title": "Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death",
      "volume": "71",
      "author": "Braun",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C5",
      "doi-asserted-by": "publisher",
      "first-page": "144",
      "DOI": "10.1016/0168-9525(92)90081-E",
      "article-title": "Making muscle in mammals",
      "volume": "8",
      "author": "Buckingham",
      "year": "1992",
      "journal-title": "Trends Genet"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C6",
      "first-page": "1040",
      "article-title": "Expression of myogenic factors in the mouse: myf-5, the first member of the MyoD gene family to be transcribed during skeletal myogenesis",
      "volume": "316",
      "author": "Buckingham",
      "year": "1993",
      "journal-title": "C. R. Acad. Sci. Paris"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C7",
      "doi-asserted-by": "publisher",
      "first-page": "3155",
      "DOI": "10.1523/JNEUROSCI.13-07-03155.1993",
      "article-title": "Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries",
      "volume": "13",
      "author": "Bulfone",
      "year": "1993",
      "journal-title": "J. Neurosci"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C8",
      "doi-asserted-by": "publisher",
      "first-page": "2254",
      "DOI": "10.1073/pnas.92.6.2254",
      "article-title": "Myoblast differentiation during mammalian somitogenesis is dependent upon a community effect",
      "volume": "92",
      "author": "Cossu",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C9",
      "doi-asserted-by": "publisher",
      "first-page": "987",
      "DOI": "10.1016/0092-8674(87)90585-X",
      "article-title": "Expression of a single transfected cDNA converts fibroblasts to myoblasts",
      "volume": "51",
      "author": "Davis",
      "year": "1987",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C10",
      "doi-asserted-by": "publisher",
      "first-page": "285",
      "DOI": "10.1523/JNEUROSCI.13-01-00285.1993",
      "article-title": "Initial tract formation in the mouse brain",
      "volume": "13",
      "author": "Easter",
      "year": "1993",
      "journal-title": "J. Neurosci"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C11",
      "doi-asserted-by": "publisher",
      "first-page": "1251",
      "DOI": "10.1242/dev.120.5.1251",
      "article-title": "Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis",
      "volume": "120",
      "author": "Edmondson",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C12",
      "doi-asserted-by": "publisher",
      "first-page": "628",
      "DOI": "10.1101/gad.3.5.628",
      "article-title": "A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program",
      "volume": "3",
      "author": "Edmondson",
      "year": "1989",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C13",
      "doi-asserted-by": "publisher",
      "first-page": "630",
      "DOI": "10.1038/363630a0",
      "article-title": "Segmental organization of embryonic diencephalon",
      "volume": "363",
      "author": "Figdor",
      "year": "1993",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C14",
      "doi-asserted-by": "publisher",
      "first-page": "787",
      "DOI": "10.1016/0960-9822(93)90033-K",
      "article-title": "Segmentation moves to the fore",
      "volume": "3",
      "author": "Fraser",
      "year": "1993",
      "journal-title": "Curr. Biol"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C15",
      "doi-asserted-by": "publisher",
      "first-page": "251",
      "DOI": "10.1016/0168-9525(89)90097-8",
      "article-title": "Genesis of the Drosophila peripheral nervous system",
      "volume": "5",
      "author": "Ghysen",
      "year": "1989",
      "journal-title": "Trends Genet"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C16",
      "doi-asserted-by": "publisher",
      "first-page": "463",
      "DOI": "10.1016/0092-8674(93)90381-Y",
      "article-title": "Mammalian Achaete-Scute homolog-1 is required for the early development of olfactory and autonomic neurons",
      "volume": "75",
      "author": "Guillemot",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C17",
      "first-page": "255",
      "article-title": "Myogenesis in Xenopus development",
      "volume": "3",
      "author": "Gurdon",
      "year": "1992",
      "journal-title": "Seminars in Dev. Biol"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C18",
      "doi-asserted-by": "publisher",
      "first-page": "501",
      "DOI": "10.1038/364501a0",
      "article-title": "Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene",
      "volume": "364",
      "author": "Hasty",
      "year": "1993",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C19",
      "doi-asserted-by": "publisher",
      "first-page": "811",
      "DOI": "10.1083/jcb.119.4.811",
      "article-title": "Localization of dystrophin gene transcripts during mouse embryogenesis",
      "volume": "119",
      "author": "Houzelstein",
      "year": "1992",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C20",
      "doi-asserted-by": "crossref",
      "DOI": "10.1007/978-1-4757-4951-9",
      "volume-title": "Developmental Neurobiology",
      "author": "Jacobson",
      "year": "1978"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C21",
      "doi-asserted-by": "publisher",
      "first-page": "1236",
      "DOI": "10.1126/science.7973707",
      "article-title": "Activation of the myogenic lineage by MEF-2A, a factor that induces and cooperates with MyoD",
      "volume": "266",
      "author": "Kaushal",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C22",
      "doi-asserted-by": "publisher",
      "first-page": "111",
      "DOI": "10.1242/jcs.1992.Supplement_16.13",
      "article-title": "Functional conservation of nematode and vertebrate myogenic regulatory factors",
      "volume": "16",
      "author": "Krause",
      "year": "1992",
      "journal-title": "J. Cell Sci. Suppl"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C23",
      "doi-asserted-by": "publisher",
      "first-page": "191",
      "DOI": "10.1016/0092-8674(94)90290-9",
      "article-title": "Hox genes in vertebrate development",
      "volume": "78",
      "author": "Krumlauf",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C24",
      "doi-asserted-by": "publisher",
      "first-page": "586",
      "DOI": "10.1038/281586a0",
      "article-title": "Neurectoderm markers retained in phenotypical skeletal muscle cells arising from a glial cell line",
      "volume": "281",
      "author": "Lennon",
      "year": "1979",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C25",
      "doi-asserted-by": "publisher",
      "first-page": "905",
      "DOI": "10.1242/dev.117.3.905",
      "article-title": "Two enhancer regions in the mouse En-2 locus direct expression to the mid/hindbrain region and mandibular myoblasts",
      "volume": "117",
      "author": "Logan",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C26",
      "doi-asserted-by": "publisher",
      "first-page": "94",
      "DOI": "10.1002/aja.1001940203",
      "article-title": "Expression of NCAM isoforms during skeletal myogenesis in the mouse embryo",
      "volume": "194",
      "author": "Lyons",
      "year": "1992",
      "journal-title": "Dev. Dynamics"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C27",
      "doi-asserted-by": "publisher",
      "first-page": "165",
      "DOI": "10.1038/299165a0",
      "article-title": "Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line",
      "volume": "299",
      "author": "McBurney",
      "year": "1982",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C28",
      "doi-asserted-by": "publisher",
      "first-page": "25244",
      "DOI": "10.1016/S0021-9258(19)74594-3",
      "article-title": "In vitro chamber specification during embryonic stem cell cardiogenesis",
      "volume": "268",
      "author": "Miller-Hance",
      "year": "1993",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C29",
      "doi-asserted-by": "publisher",
      "first-page": "853",
      "DOI": "10.1242/dev.114.4.853",
      "article-title": "Skeletal muscle phenotypes initiated by ectopic MyoD in transgenic mouse heart",
      "volume": "114",
      "author": "Miner",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C30",
      "doi-asserted-by": "publisher",
      "first-page": "1089",
      "DOI": "10.1073/pnas.87.3.1089",
      "article-title": "Herculin a fourth member of the MyoD family of myogenic regulatory genes",
      "volume": "87",
      "author": "Miner",
      "year": "1990",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C31",
      "doi-asserted-by": "publisher",
      "first-page": "567",
      "DOI": "10.1002/cne.902790406",
      "article-title": "Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti- beta-tubulin monoclonal antibody",
      "volume": "279",
      "author": "Moody",
      "year": "1987",
      "journal-title": "J. Comp. Neurol"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C32",
      "doi-asserted-by": "publisher",
      "first-page": "532",
      "DOI": "10.1038/364532a0",
      "article-title": "Myogenin gene disruption results in perinatal lethality because of severe muscle defect [see comments]",
      "volume": "364",
      "author": "Nabeshima",
      "year": "1993",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C33",
      "doi-asserted-by": "publisher",
      "first-page": "108",
      "DOI": "10.1159/000143177",
      "article-title": "The occurrence of striated muscle within the cerebellum of the albino rat",
      "volume": "71",
      "author": "Ohanian",
      "year": "1968",
      "journal-title": "Acta anat"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C34",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1101/gad.8.1.1",
      "article-title": "bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out",
      "volume": "8",
      "author": "Olson",
      "year": "1994",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C35",
      "doi-asserted-by": "publisher",
      "first-page": "1097",
      "DOI": "10.1242/dev.111.4.1097",
      "article-title": "Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo",
      "volume": "111",
      "author": "Ott",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C36",
      "doi-asserted-by": "publisher",
      "first-page": "472",
      "DOI": "10.1016/0166-2236(93)90080-6",
      "article-title": "Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization",
      "volume": "16",
      "author": "Puelles",
      "year": "1993",
      "journal-title": "Trends Neurosci"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C37",
      "doi-asserted-by": "publisher",
      "first-page": "2050",
      "DOI": "10.1101/gad.3.12b.2050",
      "article-title": "Identification of MRF4: a new member of the muscle regulatory factor gene family",
      "volume": "3",
      "author": "Rhodes",
      "year": "1989",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C38",
      "first-page": "71",
      "article-title": "Embryo-derived stem cell lines",
      "volume-title": "Teratocarcinomas and Embryonic Stem Cells: a Practical Approach",
      "author": "Robertson",
      "year": "1987"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C39",
      "doi-asserted-by": "publisher",
      "first-page": "1351",
      "DOI": "10.1016/0092-8674(93)90621-V",
      "article-title": "MyoD or myf-5 is required for the formation of skeletal muscle",
      "volume": "75",
      "author": "Rudnicki",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C40",
      "first-page": "6044",
      "article-title": "Expression of bovine myf-5 induces ectopic skeletal muscle fromation in transgenic mice",
      "volume": "13",
      "author": "Santerre",
      "year": "1993",
      "journal-title": "Mol. Cell Biol"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C41",
      "doi-asserted-by": "publisher",
      "first-page": "303",
      "DOI": "10.1038/341303a0",
      "article-title": "Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis",
      "volume": "341",
      "author": "Sassoon",
      "year": "1989",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C42",
      "doi-asserted-by": "crossref",
      "first-page": "384",
      "DOI": "10.1016/0076-6879(93)25027-Y",
      "article-title": "Detection of messenger RNA by in situ hybridization. In Methods in Enzymology",
      "volume-title": "Guide to Techniques in Mouse Development",
      "author": "Sassoon",
      "year": "1993"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C43",
      "doi-asserted-by": "publisher",
      "first-page": "398",
      "DOI": "10.1083/jcb.61.2.398",
      "article-title": "Characterization of a unique muscle cell line",
      "volume": "61",
      "author": "Schubert",
      "year": "1974",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C44",
      "doi-asserted-by": "publisher",
      "first-page": "747",
      "DOI": "10.1073/pnas.91.2.747",
      "article-title": "Mouse limb muscle is determined in the absence of the earliest myogenic factor myf-5",
      "volume": "91",
      "author": "Tajbakhsh",
      "year": "1994",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C45",
      "doi-asserted-by": "publisher",
      "first-page": "813",
      "DOI": "10.1016/0896-6273(94)90248-8",
      "article-title": "A population of myogenic cells derived from the mouse neural tube",
      "volume": "13",
      "author": "Tajbakhsh",
      "year": "1994",
      "journal-title": "Neuron"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C46",
      "first-page": "364",
      "article-title": "An embryonic origin for medulloblastoma",
      "volume": "3",
      "author": "Valtz",
      "year": "1991",
      "journal-title": "New Biologist"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C47",
      "doi-asserted-by": "publisher",
      "first-page": "805",
      "DOI": "10.1111/j.1471-4159.1990.tb04563.x",
      "article-title": "N-cadherin gene maps to human chromosome 18 and is not linked to the E-cadherin gene",
      "volume": "55",
      "author": "Walsh",
      "year": "1990",
      "journal-title": "J. Neurochem"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C48",
      "doi-asserted-by": "publisher",
      "first-page": "488",
      "DOI": "10.1016/0955-0674(93)90015-I",
      "article-title": "POU-domain proteins: structure and function of developmental regulators",
      "volume": "5",
      "author": "Wegner",
      "year": "1993",
      "journal-title": "Curr. Opin. Cell Biol"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C49",
      "doi-asserted-by": "publisher",
      "first-page": "761",
      "DOI": "10.1126/science.1846704",
      "article-title": "The MyoD gene family: nodal point during specification of the muscle cell lineage",
      "volume": "251",
      "author": "Weintraub",
      "year": "1991",
      "journal-title": "Science"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C50",
      "doi-asserted-by": "publisher",
      "first-page": "607",
      "DOI": "10.1016/0092-8674(89)90583-7",
      "article-title": "Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD",
      "volume": "56",
      "author": "Wright",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515212993800_DEVELOP_121_12_4077C51",
      "doi-asserted-by": "publisher",
      "first-page": "11",
      "DOI": "10.1016/0896-6273(94)90148-1",
      "article-title": "Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors",
      "volume": "12",
      "author": "Zimmerman",
      "year": "1994",
      "journal-title": "Neuron"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/121/12/4077/3120457/develop_121_12_4077.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/121/12/4077/3120457/develop_121_12_4077.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        1,
        15
      ]
    ],
    "date-time": "2025-01-15T15:22:00Z",
    "timestamp": 1736954520000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/121/12/4077/38614/Lineage-restriction-of-the-myogenic-conversion"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1995,
        12,
        1
      ]
    ]
  },
  "references-count": 51,
  "journal-issue": {
    "issue": "12",
    "published-print": {
      "date-parts": [
        [
          1995,
          12,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.121.12.4077",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1995,
        12,
        1
      ]
    ]
  }
}