DOI: 10.1242/dev.121.6.1719. Differentiating neurons activate transcription of the brain lipid-binding protein gene in radial glia through a novel regulatory element

Differentiating neurons activate transcription of the brain lipid-binding protein gene in radial glia through a novel regulatory element

10.1242/dev.121.6.1719

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT Formation and maintenance of a radial glial scaffold is fundamental for development of the vertebrate central nervous system. In mammals, radial glia arise in the neuroepithelium immediately prior to differentiation and migration of neurons away from the ventricular zones, and they are maintained until neuronal migration subsides. We have previously shown that expression of the brain lipid-binding protein (BLBP) in radial glia throughout the developing CNS is strictly correlated with the differentiation and migration of neurons upon these cells, and that BLBP function is required to maintain differentiation of primary cerebellar glial cells in vitro (Feng, L., Hatten, M. E. and Heintz, N. (1994). Neuron 12, 895-908). In this study, we demonstrate that BLBP transcription in vivo involves multiple regulatory elements, and that the dynamic temporal and spatial pattern of BLBP expression in radial and Bergmann glial cells throughout the developing CNS is programmed by a single radial glial cell-specific element (RGE). Furthermore, we demonstrate that BLBP expression in primary cerebellar glial cells requires coculture with differentiating neurons, and that this induction is regulated by the radial glia-specific element. The fact that transcription of BLBP in response to neurons in vitro and its dynamic regulation in radial glia through-out the CNS in vivo are both controlled by the RGE provides the first direct evidence supporting a role for differentiating neurons in the epigenetic regulation of radial glial cell function in vivo.

Authors 2

Lei Feng (first)
Nathaniel Heintz (additional)

References 29 Referenced 105

10.1146/annurev.nu.07.070187.001541 / Ann. Rev. Nutr / Intracellular vitamin A-binding proteins by Chytil (1987)
10.1101/gad.7.10.2048 / Genes Dev / DNA sequence recognition by Pax proteins: bipartite structure of the paired domain and its binding site by Czerny (1994)
10.1038/342702a0 / Nature / Differential expression of genes encoding alpha, beta, and gamma retinoic acid receptors and CRABP in the developing limbs of the mouse by Dolle (1989)
10.1016/S0021-9258(17)37201-0 / J. Biol. Chem / Identification of a Pax paired domain recognition sequence and evidence for DNA-dependent conformational changes by Epstein (1994)
10.1016/0896-6273(94)90341-7 / Neuron / Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS by Feng (1994)
10.1523/JNEUROSCI.10-04-01276.1990 / J. Neurosci / Neuron-glia interactions of rat hippocampal cells in vitro: glial-guided neuronal migration and neuronal regulation of glial differentiation by Gasser (1994)
10.1097/00041433-199104000-00011 / Curr. Opin. Lipidol / Intracellular fatty acid-binding proteins and their genes: useful models for diverse biological questions by Gordon (1991)
10.1083/jcb.100.2.384 / J. Cell Biol / Neuronal regulation of astroglial morphology and proliferation in vitro by Hatten (1985)
10.1083/jcb.104.5.1353 / J. Cell Biol / Neuronal inhibition of astroglial cell proliferation is membrane mediated by Hatten (1987)
10.1016/0166-2236(90)90044-B / Trends Neurosci / Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain by Hatten (1990)
{'key': '2025011514053902700_DEVELOP_121_6_1719C11', 'article-title': 'Mechanisms of neural patterning and specification in the developing cerebellum', 'volume-title': 'Annual Review of Neuroscience (in press)', 'author': 'Hatten', 'year': '1994'} / Annual Review of Neuroscience (in press) / Mechanisms of neural patterning and specification in the developing cerebellum by Hatten (1994)
{'key': '2025011514053902700_DEVELOP_121_6_1719C12', 'first-page': '19', 'article-title': 'Neurogenetic approaches to mammalian brain development', 'volume': '6', 'author': 'Heintz', 'year': '1993', 'journal-title': 'Genomics'} / Genomics / Neurogenetic approaches to mammalian brain development by Heintz (1993)
{'volume-title': 'Manipulating the Mouse Embryo', 'year': '1986', 'author': 'Hogan', 'key': '2025011514053902700_DEVELOP_121_6_1719C13'} / Manipulating the Mouse Embryo by Hogan (1986)
10.1016/0092-8674(94)90581-9 / Cell / The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS by Kleas (1994)
{'key': '2025011514053902700_DEVELOP_121_6_1719C15', 'volume': '51', 'author': 'Kolliker', 'year': '1890', 'journal-title': 'Z. wiss. Zool'} / Z. wiss. Zool by Kolliker (1890)
10.1242/dev.120.9.2637 / Development / The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial development by Kurtz (1994)
10.1242/dev.113.Supplement_2.87 / Development / The involvement of retinoic acid in the development of the vertebrate central nervous system by Maden (1991)
10.1016/0165-3806(88)90121-6 / Brain Res / Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker by Misson (1988)
{'key': '2025011514053902700_DEVELOP_121_6_1719C19', 'first-page': '183', 'article-title': 'Analysis of CNS development with mutant mice and chimeras. In', 'author': 'Mullen', 'year': '1982'} / Analysis of CNS development with mutant mice and chimeras. In by Mullen (1982)
10.1016/0092-8674(94)90580-0 / Cell / The activities of two Ets related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway by O’Neill (1994)
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10.1002/cne.901450105 / J. Comp. Neurol / Mode of cell migration to the superficial layers of fetal monkey neocortex by Rakic (1972)
{'article-title': 'Histologie du Systeme Nerveux de l’Homme et des Vertebres. Paris: Maloine', 'year': '1911', 'author': 'Ramon y Cajal', 'key': '2025011514053902700_DEVELOP_121_6_1719C23'} / Histologie du Systeme Nerveux de l’Homme et des Vertebres. Paris: Maloine by Ramon y Cajal (1911)
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{'key': '2025011514053902700_DEVELOP_121_6_1719C27', 'first-page': '19', 'article-title': 'Experimental Neurogenetics', 'volume-title': 'Genetics of Neurological and Psychiatric Disorders', 'author': 'Sidman', 'year': '1983'} / Genetics of Neurological and Psychiatric Disorders / Experimental Neurogenetics by Sidman (1983)
10.1002/j.1460-2075.1991.tb07758.x / EMBO J / A retinoic acid response element is present in the mouse cellular retinol binding protein I (mCRBP1) promoter by Smith (1991)
10.1146/annurev.ne.17.030194.002105 / Ann Rev. Neurosci / Determination of neuronal cell fate: lessons from the R7 neuron of Drosophila by Zipursky (1993)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 10:17 p.m.)
Deposited	7 months, 2 weeks ago (Jan. 15, 2025, 9:06 a.m.)
Indexed	1 week, 1 day ago (Aug. 23, 2025, 9:50 p.m.)
Issued	30 years, 3 months ago (June 1, 1995)
Published	30 years, 3 months ago (June 1, 1995)
Published Online	30 years, 3 months ago (June 1, 1995)
Published Print	30 years, 3 months ago (June 1, 1995)

Funders 0

None

BibTeX

@article{Feng_1995, title={Differentiating neurons activate transcription of the brain lipid-binding protein gene in radial glia through a novel regulatory element}, volume={121}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.121.6.1719}, DOI={10.1242/dev.121.6.1719}, number={6}, journal={Development}, publisher={The Company of Biologists}, author={Feng, Lei and Heintz, Nathaniel}, year={1995}, month=jun, pages={1719–1730} }

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  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1995,
        6,
        1
      ]
    ]
  },
  "references-count": 29,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          1995,
          6,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.121.6.1719",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1995,
        6,
        1
      ]
    ]
  }
}