DOI: 10.1242/dev.125.16.3143. Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells

Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells

10.1242/dev.125.16.3143

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT Using long-term, time-lapse video-microscopy, we investigated how single progenitor cells isolated from the early embryonic cerebral cortex produce neurons and glia over time. Clones of 10 cells or less were produced by short symmetric or asymmetric division patterns, commonly terminating in a ‘pair progenitor’ for two morphologically identical neurons. Larger trees were composites of these short sub-lineages: more prolific neuroblasts underwent repeated asymmetric divisions, each producing a minor neuroblast that typically made ≤10 progeny, and a sister cell capable of generating more progeny. Particular division patterns were seen repeatedly. In contrast, glioblasts underwent a prolonged series of symmetric divisions. These patterned lineage trees were generated from isolated cells growing on plastic, suggesting they are largely intrinsically programmed. Our data demonstrate for the first time that CNS progenitor cells have stereotyped division patterns, and suggest that as in invertebrates, these may play a role in neural development.

Bibliography

Qian, X., Goderie, S. K., Shen, Q., Stern, J. H., & Temple, S. (1998). Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development, 125(16), 3143â3152.

Authors 5

Xueming Qian (first)
Susan K. Goderie (additional)
Qin Shen (additional)
Jeffrey H. Stern (additional)
Sally Temple (additional)

References 60 Referenced 195

{'key': '2025021501321969800_DEVELOP_125_16_3143C1', 'first-page': '107', 'article-title': 'Embryogenesis of an insect nervous system I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria', 'volume': '35', 'author': 'Bate', 'year': '1976', 'journal-title': 'J. Exp. Embryol. Morph'} / J. Exp. Embryol. Morph / Embryogenesis of an insect nervous system I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria by Bate (1976)
{'volume-title': 'Neocortical Development', 'year': '1991', 'author': 'Bayer', 'key': '2025021501321969800_DEVELOP_125_16_3143C2'} / Neocortical Development by Bayer (1991)
10.1006/dbio.1996.0240 / Dev. Biol / The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm by Bossing (1996)
10.1006/exnr.1995.1031 / Exp. Neurol / The earliest patterns of neuronal differentiation and migration in the mammalian central nervous system by Brittis (1995)
10.1016/0166-2236(95)93933-O / Trends Neurosci / Numbers, time and neocortical neurogenesis: a general developmental and evolutionary model by Caviness (1995)
10.1016/0092-8674(95)90035-7 / Cell / Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis by Chenn (1995)
10.1038/374719a0 / Nature / A protein related to extracellular matrix proteins deleted in the mouse mutant reeler by D’Arcangelo (1995)
10.1038/372263a0 / Nature / A self-renewing multipotential stem cell in embryonic rat cerebral cortex by Davis (1994)
{'key': '2025021501321969800_DEVELOP_125_16_3143C9', 'first-page': '67', 'article-title': 'From epithelium to neuroblasts to neurons: the role of cell interactions and cell lineage during insect neurogenesis', 'volume': '312', 'author': 'Doe', 'year': '1985', 'journal-title': 'Phil. Trans. Roy. Soc'} / Phil. Trans. Roy. Soc / From epithelium to neuroblasts to neurons: the role of cell interactions and cell lineage during insect neurogenesis by Doe (1985)
10.1016/0092-8674(91)90463-9 / Cell / The prospero gene specifies cell fates in the Drosophila central nervous system by Doe (1991)
10.1016/S0959-4388(96)80004-3 / Curr. Opin. Neurobiol / Neurogenesis in the insect central nervous system by Doe (1996)
10.1016/0092-8674(90)90493-X / Cell / The unc-86 gene product couples cell lineage and cell identity in C. elegans by Finney (1990)
10.1101/gad.7.5.723 / Genes Dev / Cell interactions and gene interactions in peripheral neurogenesis by Ghysen (1993)
10.1242/dev.122.11.3509 / Development / Asymmetric distribution of the C. elegans HAM-1 protein in neuroblasts enables daughter cells to adopt distinct fates by Guenther (1996)
10.1007/BF00399871 / Roux’s Arch. Dev. Biol / The pattern of proliferation of the neuroblasts in the wild type embryo of Drosophila melanogaster by Hartenstein (1987)
10.1038/377627a0 / Nature / Asymmetric segregation of the homeodomain protein Prospero during Drosophila development by Hirata (1995)
10.1038/ng0595-77 / Nature Genet / The reeler gene encodes a protein with an Egf-like motif expressed by pioneer neurons by Hirotsune (1995)
10.1016/0012-1606(89)90085-7 / Dev. Biol / Drosophila embryonic neuroblasts in culture: autonomous differentiation of specific neurotransmitters by Huff (1989)
10.1016/0896-6273(89)90051-2 / Neuron / Lineage, migration, and morphogenesis of longitudinal glia in the Drosophila CNS as revealed by a molecular lineage marker by Jacobs (1989)
10.1007/978-1-4757-4954-0 / Developmental Neurobiology by Jacobson (1991)
10.1016/0896-6273(95)90235-X / Neuron / Maggot’s hair and Bug’s eye: Role of cell interaction and intrinsic factors in cell fate specification by Jan (1995)
10.1016/0006-8993(86)91222-9 / Brain Res / Cryopreservation of primary neurons for tissue culture by Kawamoto (1986)
10.1006/mcne.1995.1002 / Mol. Cell. Neurosci / The regulation of neural precursor cells within the mammalian brain by Kilpatrick (1995)
10.1016/0896-6273(95)90036-5 / Neuron / Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages by Kornack (1995)
10.1016/S0955-0674(97)80085-3 / Curr. Opin. Cell Biol / Mechanisms of asymmetric cell division during animal development by Knoblich (1997)
10.1523/JNEUROSCI.03-08-01634.1983 / J. Neurosci / Morphological classification of rat cortical neurons in cell culture by Kriegstein (1983)
10.1016/0012-1606(85)90069-7 / Dev. Biol / Neuronal determination during embryonic development of the grasshopper nervous system by Kuwada (1985)
10.1002/(SICI)1097-4547(19970415)48:2<83::AID-JNR1>3.0.CO;2-8 / J. Neurosci. Res / Multipotent and lineage restricted precursors coexist in the mammalian perinatal subventricular zone by Levison (1997)
10.1016/S0092-8674(00)80504-8 / Cell / Inscuteable and staufen mediate asymmetric localization and segregation of prospero RNA during Drosophila neuroblast cell divisions by Li (1997)
10.1242/dev.116.2.377 / Development / Primary culture of single ectodermal precursors of Drosophila reveals a dorsoventral prepattern of intrinsic neurogenic and epidermogenic capabilities at the early gastrula stage by Luer (1992)
10.1242/dev.120.6.1581 / Development / Early phenotypic choices by neuronal precursors, revealed by clonal analysis of the chick embryo hindbrain by Lumsden (1994)
10.1016/0896-6273(88)90163-8 / Neuron / Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus by Luskin (1988)
10.1126/science.254.5029.282 / Science / Cell cycle dependence of laminar determination in developing neocortex by McConnell (1991)
10.1016/0896-6273(88)90173-0 / Neuron / Growth and synapse formation among major classes of adult salamander retinal neurons in vitro by McLeish (1988)
10.1038/382710a0 / Nature / The PIE-1 protein and germline specification in C. elegans embryos by Mello (1996)
{'key': '2025021501321969800_DEVELOP_125_16_3143C36', 'first-page': '41', 'article-title': 'The cell lineage of neuronal subtypes in the mammalian cerebral cortex', 'volume': '193', 'author': 'Parnavelas', 'year': '1995', 'journal-title': 'Ciba Found. Symp'} / Ciba Found. Symp / The cell lineage of neuronal subtypes in the mammalian cerebral cortex by Parnavelas (1995)
10.1093/cercor/1.6.463 / Cerebral Cortex / Separate progenitor cells give rise to pyramidal and non-pyramidal neurons in the rat telencephalon by Parnavelas (1991)
{'key': '2025021501321969800_DEVELOP_125_16_3143C38', 'first-page': '168', 'volume-title': 'Biology of Drosophila', 'author': 'Poulson', 'year': '1950'} / Biology of Drosophila by Poulson (1950)
10.1242/dev.113.Supplement_2.23 / Development / Cell lineage in the cerebral cortex by Price (1991)
10.1016/S0896-6273(01)80048-9 / Neuron / FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells by Qian (1997)
10.1038/333562a0 / Nature / Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture by Raff (1988)
10.1016/S0092-8674(00)80087-2 / Cell / Size control: the regulation of cell numbers in animal development by Raff (1996)
10.1126/science.2648568 / Science / Glial cell diversification in the rat optic nerve by Raff (1989)
10.1016/0166-2236(95)93934-P / Trends Neurosci / A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution by Rakic (1995)
10.1016/0896-6273(95)90035-7 / Neuron / Systematic widespread clonal organization in cerebral cortex by Reid (1995)
10.1242/dev.124.12.2441 / Development / Clonal dispersion and evidence for asymmetric cell division in ferret cortex by Reid (1997)
10.1016/0092-8674(94)90112-0 / Cell / Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells by Rhyu (1994)
10.1016/0045-6039(73)90014-6 / Cell Differentiation / Differentiation of Drosophila neuroblasts to form ganglion-like clusters of neurons in vitro by Seecof (1973)
10.1038/382713a0 / Nature / Repression of gene expression in the embryonic germ lineage of C. elegans by Seydoux (1996)
10.1016/0092-8674(79)90197-1 / Cell / Detailed neurite morphologies of sister neuroblastoma cells are related by Solomon (1979)
10.1016/0012-1606(81)90477-2 / Dev. Biol / Monoclonal antibodies (O1 and O4) to oligodendrocyte cell surfaces: an immunological study in the central nervous system by Sommer (1981)
10.1242/dev.121.10.3187 / Development / The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila by Spana (1995)
10.1146/annurev.ge.18.120184.002421 / Annu. Rev. Genet / The genetic control of cell lineage during nematode development by Sternberg (1984)
10.1016/0012-1606(77)90158-0 / Dev. Biol / Post-embryonic cell lineages of the nematode, Caenorhabditis elegans by Sulston (1977)
10.1016/0012-1606(80)90353-X / Dev. Biol / Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans by Sulston (1980)
10.1016/0012-1606(83)90201-4 / Dev. Biol / The embryonic cell lineage of the nematode, Caenorhabditis elegans by Sulston (1983)
10.1016/S0959-4388(96)80003-1 / Curr. Opin. Neurobiol / Vertebrate neural progenitor cells: subtypes and regulation by Temple (1996)
10.1242/dev.118.3.765 / Development / A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants by Udolph (1993)
10.1126/science.3137660 / Science / Clonally related cortical cells show several migration patterns by Walsh (1988)
10.1016/0012-1606(84)90044-7 / Dev. Biol / Cell lineage, cell-cell interaction and segment formation in the ectoderm of a glossiphoniid leech embryo by Zackson (1984)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 11:23 p.m.)
Deposited	6 months, 2 weeks ago (Feb. 14, 2025, 8:32 p.m.)
Indexed	1 day, 20 hours ago (Aug. 28, 2025, 8:32 a.m.)
Issued	27 years ago (Aug. 15, 1998)
Published	27 years ago (Aug. 15, 1998)
Published Online	27 years ago (Aug. 15, 1998)
Published Print	27 years ago (Aug. 15, 1998)

Funders 0

None

BibTeX

@article{Qian_1998, title={Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells}, volume={125}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.125.16.3143}, DOI={10.1242/dev.125.16.3143}, number={16}, journal={Development}, publisher={The Company of Biologists}, author={Qian, Xueming and Goderie, Susan K. and Shen, Qin and Stern, Jeffrey H. and Temple, Sally}, year={1998}, month=aug, pages={3143–3152} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        28
      ]
    ],
    "date-time": "2025-08-28T12:32:22Z",
    "timestamp": 1756384342660,
    "version": "3.37.1"
  },
  "reference-count": 60,
  "publisher": "The Company of Biologists",
  "issue": "16",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1998,
            8,
            15
          ]
        ],
        "date-time": "1998-08-15T00:00:00Z",
        "timestamp": 903139200000
      },
      "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": [
      [
        1998,
        8,
        15
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>Using long-term, time-lapse video-microscopy, we investigated how single progenitor cells isolated from the early embryonic cerebral cortex produce neurons and glia over time. Clones of 10 cells or less were produced by short symmetric or asymmetric division patterns, commonly terminating in a \u2018pair progenitor\u2019 for two morphologically identical neurons. Larger trees were composites of these short sub-lineages: more prolific neuroblasts underwent repeated asymmetric divisions, each producing a minor neuroblast that typically made \u226410 progeny, and a sister cell capable of generating more progeny. Particular division patterns were seen repeatedly. In contrast, glioblasts underwent a prolonged series of symmetric divisions. These patterned lineage trees were generated from isolated cells growing on plastic, suggesting they are largely intrinsically programmed. Our data demonstrate for the first time that CNS progenitor cells have stereotyped division patterns, and suggest that as in invertebrates, these may play a role in neural development.</jats:p>",
  "DOI": "10.1242/dev.125.16.3143",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T03:23:19Z",
    "timestamp": 1619407399000
  },
  "page": "3143-3152",
  "source": "Crossref",
  "is-referenced-by-count": 195,
  "title": "Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells",
  "prefix": "10.1242",
  "volume": "125",
  "author": [
    {
      "given": "Xueming",
      "family": "Qian",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Amgen inc. 2 , 1 Amgen Center Drive, Mailbox 14-1-B, Thousand Oaks, CA 91320, USA"
        }
      ]
    },
    {
      "given": "Susan K.",
      "family": "Goderie",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pharmacology and Neuroscience 1 , A-136, Albany Medical College, Albany, NY 12208, USA"
        }
      ]
    },
    {
      "given": "Qin",
      "family": "Shen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pharmacology and Neuroscience 1 , A-136, Albany Medical College, Albany, NY 12208, USA"
        }
      ]
    },
    {
      "given": "Jeffrey H.",
      "family": "Stern",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Child\u2019s Hospital 3 , Hackett Boulevard, Albany, NY 12208, USA"
        }
      ]
    },
    {
      "given": "Sally",
      "family": "Temple",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Pharmacology and Neuroscience 1 , A-136, Albany Medical College, Albany, NY 12208, USA"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1998,
        8,
        15
      ]
    ]
  },
  "reference": [
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C1",
      "first-page": "107",
      "article-title": "Embryogenesis of an insect nervous system I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria",
      "volume": "35",
      "author": "Bate",
      "year": "1976",
      "journal-title": "J. Exp. Embryol. Morph"
    },
    {
      "volume-title": "Neocortical Development",
      "year": "1991",
      "author": "Bayer",
      "key": "2025021501321969800_DEVELOP_125_16_3143C2"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C3",
      "doi-asserted-by": "crossref",
      "first-page": "41",
      "DOI": "10.1006/dbio.1996.0240",
      "article-title": "The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm",
      "volume": "179",
      "author": "Bossing",
      "year": "1996",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C4",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1006/exnr.1995.1031",
      "article-title": "The earliest patterns of neuronal differentiation and migration in the mammalian central nervous system",
      "volume": "134",
      "author": "Brittis",
      "year": "1995",
      "journal-title": "Exp. Neurol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C5",
      "doi-asserted-by": "crossref",
      "first-page": "379",
      "DOI": "10.1016/0166-2236(95)93933-O",
      "article-title": "Numbers, time and neocortical neurogenesis: a general developmental and evolutionary model",
      "volume": "18",
      "author": "Caviness",
      "year": "1995",
      "journal-title": "Trends Neurosci"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C6",
      "doi-asserted-by": "crossref",
      "first-page": "631",
      "DOI": "10.1016/0092-8674(95)90035-7",
      "article-title": "Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis",
      "volume": "82",
      "author": "Chenn",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C7",
      "doi-asserted-by": "crossref",
      "first-page": "719",
      "DOI": "10.1038/374719a0",
      "article-title": "A protein related to extracellular matrix proteins deleted in the mouse mutant reeler",
      "volume": "374",
      "author": "D\u2019Arcangelo",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C8",
      "doi-asserted-by": "crossref",
      "first-page": "263",
      "DOI": "10.1038/372263a0",
      "article-title": "A self-renewing multipotential stem cell in embryonic rat cerebral cortex",
      "volume": "372",
      "author": "Davis",
      "year": "1994",
      "journal-title": "Nature"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C9",
      "first-page": "67",
      "article-title": "From epithelium to neuroblasts to neurons: the role of cell interactions and cell lineage during insect neurogenesis",
      "volume": "312",
      "author": "Doe",
      "year": "1985",
      "journal-title": "Phil. Trans. Roy. Soc"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C10",
      "doi-asserted-by": "crossref",
      "first-page": "451",
      "DOI": "10.1016/0092-8674(91)90463-9",
      "article-title": "The prospero gene specifies cell fates in the Drosophila central nervous system",
      "volume": "65",
      "author": "Doe",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C11",
      "doi-asserted-by": "crossref",
      "first-page": "18",
      "DOI": "10.1016/S0959-4388(96)80004-3",
      "article-title": "Neurogenesis in the insect central nervous system",
      "volume": "6",
      "author": "Doe",
      "year": "1996",
      "journal-title": "Curr. Opin. Neurobiol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C12",
      "doi-asserted-by": "crossref",
      "first-page": "895",
      "DOI": "10.1016/0092-8674(90)90493-X",
      "article-title": "The unc-86 gene product couples cell lineage and cell identity in C. elegans",
      "volume": "63",
      "author": "Finney",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C13",
      "doi-asserted-by": "crossref",
      "first-page": "723",
      "DOI": "10.1101/gad.7.5.723",
      "article-title": "Cell interactions and gene interactions in peripheral neurogenesis",
      "volume": "7",
      "author": "Ghysen",
      "year": "1993",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C14",
      "doi-asserted-by": "crossref",
      "first-page": "3509",
      "DOI": "10.1242/dev.122.11.3509",
      "article-title": "Asymmetric distribution of the C. elegans HAM-1 protein in neuroblasts enables daughter cells to adopt distinct fates",
      "volume": "122",
      "author": "Guenther",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C15",
      "doi-asserted-by": "crossref",
      "first-page": "473",
      "DOI": "10.1007/BF00399871",
      "article-title": "The pattern of proliferation of the neuroblasts in the wild type embryo of Drosophila melanogaster",
      "volume": "196",
      "author": "Hartenstein",
      "year": "1987",
      "journal-title": "Roux\u2019s Arch. Dev. Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C16",
      "doi-asserted-by": "crossref",
      "first-page": "627",
      "DOI": "10.1038/377627a0",
      "article-title": "Asymmetric segregation of the homeodomain protein Prospero during Drosophila development",
      "volume": "377",
      "author": "Hirata",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C17",
      "doi-asserted-by": "crossref",
      "first-page": "77",
      "DOI": "10.1038/ng0595-77",
      "article-title": "The reeler gene encodes a protein with an Egf-like motif expressed by pioneer neurons",
      "volume": "10",
      "author": "Hirotsune",
      "year": "1995",
      "journal-title": "Nature Genet"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C18",
      "doi-asserted-by": "crossref",
      "first-page": "146",
      "DOI": "10.1016/0012-1606(89)90085-7",
      "article-title": "Drosophila embryonic neuroblasts in culture: autonomous differentiation of specific neurotransmitters",
      "volume": "134",
      "author": "Huff",
      "year": "1989",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C19",
      "doi-asserted-by": "crossref",
      "first-page": "1625",
      "DOI": "10.1016/0896-6273(89)90051-2",
      "article-title": "Lineage, migration, and morphogenesis of longitudinal glia in the Drosophila CNS as revealed by a molecular lineage marker",
      "volume": "2",
      "author": "Jacobs",
      "year": "1989",
      "journal-title": "Neuron"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C20",
      "doi-asserted-by": "crossref",
      "DOI": "10.1007/978-1-4757-4954-0",
      "volume-title": "Developmental Neurobiology",
      "author": "Jacobson",
      "year": "1991"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C21",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/0896-6273(95)90235-X",
      "article-title": "Maggot\u2019s hair and Bug\u2019s eye: Role of cell interaction and intrinsic factors in cell fate specification",
      "volume": "14",
      "author": "Jan",
      "year": "1995",
      "journal-title": "Neuron"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C22",
      "doi-asserted-by": "crossref",
      "first-page": "84",
      "DOI": "10.1016/0006-8993(86)91222-9",
      "article-title": "Cryopreservation of primary neurons for tissue culture",
      "volume": "384",
      "author": "Kawamoto",
      "year": "1986",
      "journal-title": "Brain Res"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C23",
      "doi-asserted-by": "crossref",
      "first-page": "2",
      "DOI": "10.1006/mcne.1995.1002",
      "article-title": "The regulation of neural precursor cells within the mammalian brain",
      "volume": "6",
      "author": "Kilpatrick",
      "year": "1995",
      "journal-title": "Mol. Cell. Neurosci"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C24",
      "doi-asserted-by": "crossref",
      "first-page": "311",
      "DOI": "10.1016/0896-6273(95)90036-5",
      "article-title": "Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages",
      "volume": "15",
      "author": "Kornack",
      "year": "1995",
      "journal-title": "Neuron"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C25",
      "doi-asserted-by": "crossref",
      "first-page": "833",
      "DOI": "10.1016/S0955-0674(97)80085-3",
      "article-title": "Mechanisms of asymmetric cell division during animal development",
      "volume": "9",
      "author": "Knoblich",
      "year": "1997",
      "journal-title": "Curr. Opin. Cell Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C26",
      "doi-asserted-by": "crossref",
      "first-page": "1634",
      "DOI": "10.1523/JNEUROSCI.03-08-01634.1983",
      "article-title": "Morphological classification of rat cortical neurons in cell culture",
      "volume": "3",
      "author": "Kriegstein",
      "year": "1983",
      "journal-title": "J. Neurosci"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C27",
      "doi-asserted-by": "crossref",
      "first-page": "114",
      "DOI": "10.1016/0012-1606(85)90069-7",
      "article-title": "Neuronal determination during embryonic development of the grasshopper nervous system",
      "volume": "110",
      "author": "Kuwada",
      "year": "1985",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C28",
      "doi-asserted-by": "crossref",
      "first-page": "83",
      "DOI": "10.1002/(SICI)1097-4547(19970415)48:2<83::AID-JNR1>3.0.CO;2-8",
      "article-title": "Multipotent and lineage restricted precursors coexist in the mammalian perinatal subventricular zone",
      "volume": "48",
      "author": "Levison",
      "year": "1997",
      "journal-title": "J. Neurosci. Res"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C29",
      "doi-asserted-by": "crossref",
      "first-page": "437",
      "DOI": "10.1016/S0092-8674(00)80504-8",
      "article-title": "Inscuteable and staufen mediate asymmetric localization and segregation of prospero RNA during Drosophila neuroblast cell divisions",
      "volume": "90",
      "author": "Li",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C30",
      "doi-asserted-by": "crossref",
      "first-page": "377",
      "DOI": "10.1242/dev.116.2.377",
      "article-title": "Primary culture of single ectodermal precursors of Drosophila reveals a dorsoventral prepattern of intrinsic neurogenic and epidermogenic capabilities at the early gastrula stage",
      "volume": "116",
      "author": "Luer",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C31",
      "doi-asserted-by": "crossref",
      "first-page": "1581",
      "DOI": "10.1242/dev.120.6.1581",
      "article-title": "Early phenotypic choices by neuronal precursors, revealed by clonal analysis of the chick embryo hindbrain",
      "volume": "120",
      "author": "Lumsden",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C32",
      "doi-asserted-by": "crossref",
      "first-page": "635",
      "DOI": "10.1016/0896-6273(88)90163-8",
      "article-title": "Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus",
      "volume": "1",
      "author": "Luskin",
      "year": "1988",
      "journal-title": "Neuron"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C33",
      "doi-asserted-by": "crossref",
      "first-page": "282",
      "DOI": "10.1126/science.254.5029.282",
      "article-title": "Cell cycle dependence of laminar determination in developing neocortex",
      "volume": "254",
      "author": "McConnell",
      "year": "1991",
      "journal-title": "Science"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C34",
      "doi-asserted-by": "crossref",
      "first-page": "751",
      "DOI": "10.1016/0896-6273(88)90173-0",
      "article-title": "Growth and synapse formation among major classes of adult salamander retinal neurons in vitro",
      "volume": "1",
      "author": "McLeish",
      "year": "1988",
      "journal-title": "Neuron"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C35",
      "doi-asserted-by": "crossref",
      "first-page": "710",
      "DOI": "10.1038/382710a0",
      "article-title": "The PIE-1 protein and germline specification in C. elegans embryos",
      "volume": "382",
      "author": "Mello",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C36",
      "first-page": "41",
      "article-title": "The cell lineage of neuronal subtypes in the mammalian cerebral cortex",
      "volume": "193",
      "author": "Parnavelas",
      "year": "1995",
      "journal-title": "Ciba Found. Symp"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C37",
      "doi-asserted-by": "crossref",
      "first-page": "463",
      "DOI": "10.1093/cercor/1.6.463",
      "article-title": "Separate progenitor cells give rise to pyramidal and non-pyramidal neurons in the rat telencephalon",
      "volume": "1",
      "author": "Parnavelas",
      "year": "1991",
      "journal-title": "Cerebral Cortex"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C38",
      "first-page": "168",
      "volume-title": "Biology of Drosophila",
      "author": "Poulson",
      "year": "1950"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C39",
      "doi-asserted-by": "crossref",
      "first-page": "23",
      "DOI": "10.1242/dev.113.Supplement_2.23",
      "article-title": "Cell lineage in the cerebral cortex",
      "volume": "2",
      "author": "Price",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C40",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1016/S0896-6273(01)80048-9",
      "article-title": "FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells",
      "volume": "18",
      "author": "Qian",
      "year": "1997",
      "journal-title": "Neuron"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C41",
      "doi-asserted-by": "crossref",
      "first-page": "562",
      "DOI": "10.1038/333562a0",
      "article-title": "Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture",
      "volume": "333",
      "author": "Raff",
      "year": "1988",
      "journal-title": "Nature"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C42",
      "doi-asserted-by": "crossref",
      "first-page": "173",
      "DOI": "10.1016/S0092-8674(00)80087-2",
      "article-title": "Size control: the regulation of cell numbers in animal development",
      "volume": "86",
      "author": "Raff",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C43",
      "doi-asserted-by": "crossref",
      "first-page": "1450",
      "DOI": "10.1126/science.2648568",
      "article-title": "Glial cell diversification in the rat optic nerve",
      "volume": "243",
      "author": "Raff",
      "year": "1989",
      "journal-title": "Science"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C44",
      "doi-asserted-by": "crossref",
      "first-page": "383",
      "DOI": "10.1016/0166-2236(95)93934-P",
      "article-title": "A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution",
      "volume": "18",
      "author": "Rakic",
      "year": "1995",
      "journal-title": "Trends Neurosci"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C45",
      "doi-asserted-by": "crossref",
      "first-page": "299",
      "DOI": "10.1016/0896-6273(95)90035-7",
      "article-title": "Systematic widespread clonal organization in cerebral cortex",
      "volume": "15",
      "author": "Reid",
      "year": "1995",
      "journal-title": "Neuron"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C46",
      "doi-asserted-by": "crossref",
      "first-page": "2441",
      "DOI": "10.1242/dev.124.12.2441",
      "article-title": "Clonal dispersion and evidence for asymmetric cell division in ferret cortex",
      "volume": "124",
      "author": "Reid",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C47",
      "doi-asserted-by": "crossref",
      "first-page": "477",
      "DOI": "10.1016/0092-8674(94)90112-0",
      "article-title": "Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells",
      "volume": "76",
      "author": "Rhyu",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C48",
      "doi-asserted-by": "crossref",
      "first-page": "143",
      "DOI": "10.1016/0045-6039(73)90014-6",
      "article-title": "Differentiation of Drosophila neuroblasts to form ganglion-like clusters of neurons in vitro",
      "volume": "2",
      "author": "Seecof",
      "year": "1973",
      "journal-title": "Cell Differentiation"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C49",
      "doi-asserted-by": "crossref",
      "first-page": "713",
      "DOI": "10.1038/382713a0",
      "article-title": "Repression of gene expression in the embryonic germ lineage of C. elegans",
      "volume": "382",
      "author": "Seydoux",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C50",
      "doi-asserted-by": "crossref",
      "first-page": "165",
      "DOI": "10.1016/0092-8674(79)90197-1",
      "article-title": "Detailed neurite morphologies of sister neuroblastoma cells are related",
      "volume": "16",
      "author": "Solomon",
      "year": "1979",
      "journal-title": "Cell"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C51",
      "doi-asserted-by": "crossref",
      "first-page": "311",
      "DOI": "10.1016/0012-1606(81)90477-2",
      "article-title": "Monoclonal antibodies (O1 and O4) to oligodendrocyte cell surfaces: an immunological study in the central nervous system",
      "volume": "83",
      "author": "Sommer",
      "year": "1981",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C52",
      "doi-asserted-by": "crossref",
      "first-page": "3187",
      "DOI": "10.1242/dev.121.10.3187",
      "article-title": "The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila",
      "volume": "121",
      "author": "Spana",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C53",
      "doi-asserted-by": "crossref",
      "first-page": "489",
      "DOI": "10.1146/annurev.ge.18.120184.002421",
      "article-title": "The genetic control of cell lineage during nematode development",
      "volume": "18",
      "author": "Sternberg",
      "year": "1984",
      "journal-title": "Annu. Rev. Genet"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C54",
      "doi-asserted-by": "crossref",
      "first-page": "110",
      "DOI": "10.1016/0012-1606(77)90158-0",
      "article-title": "Post-embryonic cell lineages of the nematode, Caenorhabditis elegans",
      "volume": "56",
      "author": "Sulston",
      "year": "1977",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C55",
      "doi-asserted-by": "crossref",
      "first-page": "577",
      "DOI": "10.1016/0012-1606(80)90353-X",
      "article-title": "Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans",
      "volume": "78",
      "author": "Sulston",
      "year": "1980",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C56",
      "doi-asserted-by": "crossref",
      "first-page": "64",
      "DOI": "10.1016/0012-1606(83)90201-4",
      "article-title": "The embryonic cell lineage of the nematode, Caenorhabditis elegans",
      "volume": "110",
      "author": "Sulston",
      "year": "1983",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C57",
      "doi-asserted-by": "crossref",
      "first-page": "11",
      "DOI": "10.1016/S0959-4388(96)80003-1",
      "article-title": "Vertebrate neural progenitor cells: subtypes and regulation",
      "volume": "6",
      "author": "Temple",
      "year": "1996",
      "journal-title": "Curr. Opin. Neurobiol"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C58",
      "doi-asserted-by": "crossref",
      "first-page": "765",
      "DOI": "10.1242/dev.118.3.765",
      "article-title": "A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants",
      "volume": "118",
      "author": "Udolph",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C59",
      "doi-asserted-by": "crossref",
      "first-page": "1342",
      "DOI": "10.1126/science.3137660",
      "article-title": "Clonally related cortical cells show several migration patterns",
      "volume": "241",
      "author": "Walsh",
      "year": "1988",
      "journal-title": "Science"
    },
    {
      "key": "2025021501321969800_DEVELOP_125_16_3143C60",
      "doi-asserted-by": "crossref",
      "first-page": "143",
      "DOI": "10.1016/0012-1606(84)90044-7",
      "article-title": "Cell lineage, cell-cell interaction and segment formation in the ectoderm of a glossiphoniid leech embryo",
      "volume": "104",
      "author": "Zackson",
      "year": "1984",
      "journal-title": "Dev. Biol"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/125/16/3143/3139153/develop_125_16_3143.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/125/16/3143/3139153/develop_125_16_3143.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        2,
        15
      ]
    ],
    "date-time": "2025-02-15T01:32:43Z",
    "timestamp": 1739583163000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/125/16/3143/39959/Intrinsic-programs-of-patterned-cell-lineages-in"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1998,
        8,
        15
      ]
    ]
  },
  "references-count": 60,
  "journal-issue": {
    "issue": "16",
    "published-print": {
      "date-parts": [
        [
          1998,
          8,
          15
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.125.16.3143",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1998,
        8,
        15
      ]
    ]
  }
}