Advertisement
JOURNAL ARTICLES
Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage
P. Malatesta, E. Hartfuss, M. Gotz
Development 2000 127: 5253-5263;

Summary

The developing central nervous system of vertebrates contains an abundant cell type designated radial glial cells. These cells are known as guiding cables for migrating neurons, while their role as precursor cells is less clear. Since radial glial cells express a variety of astroglial characteristics and differentiate as astrocytes after completing their guidance function, they have been considered as part of the glial lineage. Using fluorescence-activated cell sorting, we show here that radial glial cells also are neuronal precursors and only later, after neurogenesis, do they shift towards an exclusive generation of astrocytes. These results thus demonstrate a novel function for radial glial cells, namely their ability to generate two major cell types found in the nervous system, neurons and astrocytes.

REFERENCES

    1. Aaku-Saraste E.,
    2. Hellwig A.,
    3. Huttner W. B.
    (1996) Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure-remodeling of the neuroepithelium prior to neurogenesis. Dev. Biol 180, 664–679
    OpenUrlCrossRefPubMedWeb of Science
    1. Alvarez-Buylla A.,
    2. Theelen M.,
    3. Nottebohm F.
    (1990) Proliferation ‘hot spots’ in adult avian ventricular zone reveal radial cell division. Neuron 5, 101–109
    OpenUrlCrossRefPubMedWeb of Science
    1. Anderson D. J.
    (1989) The neural crest cell lineage problem: neuropoiesis?. Neuron 3, 1–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Barres B. A.
    (1999) A new role for glia: generation of neurons. Cell 97, 667–670
    OpenUrlCrossRefPubMedWeb of Science
    1. Bignami A.,
    2. Eng L. F.,
    3. Dahl D.,
    4. Uyeda C. T.
    (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43, 429–435
    OpenUrlCrossRefPubMedWeb of Science
    1. Brenner M.,
    2. Kisseberth W. C.,
    3. Su Y.,
    4. Besnard F.,
    5. Messing A.
    (1994) GFAP promoter directs astrocyte-specific expression in transgenic mice. J. Neurosci 14, 1030–1037
    OpenUrlAbstract
    1. Bruni J. E.
    (1998) Ependymal development, proliferation, and functions: a review. Microsc. Res. Tech 41, 2–13
    OpenUrlCrossRefPubMedWeb of Science
    1. Cameron R. S.,
    2. Rakic P.
    (1991) Glial cell lineage in the cerebral cortex—a review and synthesis. Glia 4, 124–137
    OpenUrlCrossRefPubMedWeb of Science
    1. Choi B. H.
    (1981) Radial glia of developing human fetal spinal cord: Golgi, immunohistochemical and electron microscopic study. Brain Res 227, 249–267
    OpenUrlPubMed
    1. Culican S. M.,
    2. Baumrind N. L.,
    3. Yamamoto M.,
    4. Pearlman A. L.
    (1990) Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J. Neurosci 10, 684–692
    OpenUrlAbstract
    1. Doetsch F.,
    2. Caille I.,
    3. Lim D. A.,
    4. Garcia-Verdugo J. M.,
    5. Alvarez-Buylla A.
    (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703–716
    OpenUrlCrossRefPubMedWeb of Science
    1. Edwards M. A.,
    2. Yamamoto M.,
    3. Caviness V. S. J.
    (1990) Organization of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience 36, 121–144
    OpenUrlCrossRefPubMedWeb of Science
    1. Feng L.,
    2. Hatten M. E.,
    3. Heintz N.
    (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895–908
    OpenUrlCrossRefPubMedWeb of Science
    1. Frederiksen K.,
    2. McKay R. D.
    (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci 8, 1144–1151
    OpenUrlAbstract
    1. Gaiano N.,
    2. Nye J. S.,
    3. Fishell G.
    (2000) Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26, 395–404
    OpenUrlCrossRefPubMedWeb of Science
    1. Gerdes J.,
    2. Scholzen T.,
    3. Gerlach C.,
    4. Kubbutat M.,
    5. Zentgraf H.
    (1997) Assessment of cell proliferation in murine tissues with a polyclonal antiserum against the murine Ki-67 protein. Eur. J. Cell Biol 72, 263–263
    OpenUrl
    1. Götz M.,
    2. Bolz J.
    (1992) Preservation and formation of cortical layers in slice cultures. J. Neurobiol 23, 783–802
    OpenUrlCrossRefPubMedWeb of Science
    1. Götz M.,
    2. Stoykova A.,
    3. Gruss P.
    (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031–1044
    OpenUrlCrossRefPubMedWeb of Science
    1. Gray G. E.,
    2. Sanes J. R.
    (1992) Lineage of radial glia in the chicken optic tectum. Development 114, 271–283
    OpenUrlAbstract
    1. Grove E. A.,
    2. Williams B. P.,
    3. Li D. Q.,
    4. Hajihosseini M.,
    5. Friedrich A.,
    6. Price J.
    (1993) Multiple restricted lineages in the embryonic rat cerebral cortex. Development 117, 553–561
    OpenUrlAbstract
    1. Hajihosseini M. K.,
    2. Dickson C.
    (1999) A subset of fibroblast growth factors (Fgfs) promote survival, but Fgf-8b specifically promotes astroglial differentiation of rat cortical precursor cells. Mol. Cell. Neurosci 14, 468–485
    OpenUrlCrossRefPubMedWeb of Science
    1. Halliday A. L.,
    2. Cepko C. L.
    (1992) Generation and migration of cells in the developing striatum. Neuron 9, 15–26
    OpenUrlCrossRefPubMedWeb of Science
    1. Hinds J. W.,
    2. Ruffett T. L.
    (1971) Cell proliferation in the neural tube: an electron microscopic and golgi analysis in the mouse cerebral vesicle. Zeitschr. f. Zellforschung 115, 226–264
    OpenUrlCrossRefPubMedWeb of Science
    1. Hunter K. E.,
    2. Hatten M. E.
    (1995) Radial glial cell transformation to astrocytes is bidirectional: regulation by a diffusible factor in embryonic forebrain. Proc. Natl. Acad. Sci. USA 92, 2061–2065
    OpenUrlAbstract/FREE Full Text
    1. Huttner W. B.,
    2. Brand M.
    (1997) Asymmetric division and polarity of neuroepithelial cells. Curr. Opin. Neurobiol 7, 29–39
    OpenUrlCrossRefPubMedWeb of Science
    1. Johansson C. B.,
    2. Momma S.,
    3. Clarke D. L.,
    4. Risling M.,
    5. Lendahl U.,
    6. Frisen J.
    (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96, 25–34
    OpenUrlCrossRefPubMedWeb of Science
    1. Katz L. C.,
    2. Burkhalter A.,
    3. Dreyer W. J.
    (1984) Fluorescent latexmicrospheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310, 498–500
    OpenUrlPubMed
    1. Kornack D. R.,
    2. Rakic P.
    (1995) Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 15, 311–321
    OpenUrlCrossRefPubMedWeb of Science
    1. Kurtz A.,
    2. Zimmer A.,
    3. Schnutgen F.,
    4. Bruning G.,
    5. Spener F.,
    6. Muller T.
    (1994) The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell development. Development 120, 2637–2649
    OpenUrlAbstract/FREE Full Text
    1. Lagenaur C.,
    2. Schachner M.
    (1981) Monoclonal antibody (M2) to glial and neuronal cell surfaces. J. Supramol. Struct. Cell Biochem 15, 335–346
    OpenUrlCrossRefPubMedWeb of Science
    1. Leavitt B. R.,
    2. Hernit-Grant C. S.,
    3. Macklis J. D.
    (1999) Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp. Neurol 157, 43–57
    OpenUrlCrossRefPubMedWeb of Science
    1. Levitt P.,
    2. Rakic P.
    (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J. Comp. Neurol 193, 815–840
    OpenUrlCrossRefPubMedWeb of Science
    1. Levitt P.,
    2. Cooper M. L.,
    3. Rakic P.
    (1981) Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J. Neurosci 1, 27–39
    OpenUrlAbstract
    1. Levitt P.,
    2. Cooper M. L.,
    3. Rakic P.
    (1983) Early divergence and changing proportions of neuronal and glial precursor cells in the primate cerebral ventricular zone. Dev. Biol 96, 472–484
    OpenUrlCrossRefPubMedWeb of Science
    1. Lillien L.
    (1997) Neural development: instructions for neural diversity. Curr. Biol 7, 168–171
    1. Lund R. D.,
    2. Chang F. L.,
    3. Hankin M. H.,
    4. Lagenaur C. F.
    (1985) Use of a species-specific antibody for demonstrating mouse neurons transplanted to rat brains. Neurosci. Lett 61, 221–226
    OpenUrlCrossRefPubMedWeb of Science
    1. Luskin M. B.,
    2. Pearlman A. L.,
    3. Sanes J. R.
    (1988) Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1, 635–647
    OpenUrlCrossRefPubMedWeb of Science
    1. Magavi S. S.,
    2. Leavitt B. R.,
    3. Macklis J. D.
    (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405, 951–955
    OpenUrlCrossRefPubMed
    1. Menezes J. R. L.,
    2. Luskin M. B.
    (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J. Neurosci 14, 5399–5416
    OpenUrlAbstract
    1. Misson J. P.,
    2. Austin C. P.,
    3. Takahashi T.,
    4. Cepko C. L.,
    5. Caviness V. S. J.
    (1991) The alignment of migrating neural cells in relation to the murine neopallial radial glial fiber system. Cereb. Cortex 1, 221–229
    OpenUrlAbstract/FREE Full Text
    1. Misson J. P.,
    2. Edwards M. A.,
    3. Yamamoto M.,
    4. Caviness V. S. J.
    (1988) Mitotic cycling of radial cells of the fetal murine cerebral wall—a combined autoradiographic and immunohistochemical study. Dev. Brain Res 38, 183–190
    OpenUrlCrossRef
    1. Nowakowski R. S.,
    2. Lewin S. B.,
    3. Miller M. W.
    (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J. Neurocytol 18, 311–318
    OpenUrlCrossRefPubMedWeb of Science
    1. Okabe M.,
    2. Ikawa M.,
    3. Kominami K.,
    4. Nakanishi T.,
    5. Nishimune Y.
    (1997) ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett 407, 313–319
    OpenUrlCrossRefPubMedWeb of Science
    1. Qian X.,
    2. Goderie S. K.,
    3. Shen Q.,
    4. Stern J. H.,
    5. Temple S.
    (1998) Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125, 3143–3152
    OpenUrlAbstract
    1. Rakic P.
    (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol 145, 61–83
    OpenUrlCrossRefPubMedWeb of Science
    1. Reh T. A.
    (1992) Cellular interactions determine neuronal phenotypes in rodent retinal cultures. J. Neurobiol 23, 1067–1083
    OpenUrlCrossRefPubMedWeb of Science
    1. Reid C. B.,
    2. Liang I.,
    3. Walsh C.
    (1995) Systematic widespread clonal organization in cerebral cortex. Neuron 15, 299–310
    OpenUrlCrossRefPubMedWeb of Science
    1. Sancho-Tello M.,
    2. Valles S.,
    3. Montoliu C.,
    4. Renau-Piqueras J.,
    5. Guerri C.
    (1995) Developmental pattern of GFAP and vimentin gene expression in rat brain and in radial glial cultures. Glia 15, 157–166
    OpenUrlCrossRefPubMedWeb of Science
    1. Sauer F. C.
    (1935) Mitosis in the neural tube. J. Comp. Neurol 62, 377–405
    OpenUrlCrossRefWeb of Science
    1. Schaper A.
    (1897) The earliest differentiation in the central nervous system of vertebrates. Science 5, 430–431
    1. Schmechel D. E.,
    2. Rakic P.
    (1979) Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Nature 277, 303–305
    OpenUrlCrossRefPubMed
    1. Shibata T.,
    2. Yamada K.,
    3. Watanabe M.,
    4. Ikenaka K.,
    5. Wada K.,
    6. Tanaka K.,
    7. Inoue Y.
    (1997) Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J. Neurosci 17, 9212–9219
    OpenUrlAbstract/FREE Full Text
    1. Sommer I.,
    2. Schachner M.
    (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev. Biol 83, 311–327
    OpenUrlCrossRefPubMedWeb of Science
    1. Soriano E.,
    2. Alvarado-Mallart R. M.,
    3. Dumesnil N.,
    4. Del Rio J. A.,
    5. Sotelo C.
    (1997) Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 18, 563–577
    OpenUrlCrossRefPubMedWeb of Science
    1. Stensaas L. J.,
    2. Stensaas S. S.
    (1968) An electron microscope study of cells in the matrix and intermediate laminae of the cerebral hemisphere of the 45 mm rabbit embryo. Zeitschr. f. Zellforsch 91, 341–365
    OpenUrlCrossRefPubMedWeb of Science
    1. Ullensvang K.,
    2. Lehre K. P.,
    3. Storm-Mathisen J.,
    4. Danbolt N. C.
    (1997) Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur. J. Neurosci 9, 1646–1655
    OpenUrlCrossRefPubMedWeb of Science
    1. Voigt T.
    (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol 289, 74–88
    OpenUrlCrossRefPubMedWeb of Science
    1. Williams B. P.,
    2. Price J.
    (1995) Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron 14, 1181–1188
    OpenUrlCrossRefPubMedWeb of Science
    1. Williams B. P.,
    2. Read J.,
    3. Price J.
    (1991) The generation of neurons and oligodendrocytes from a common precursor cell. Neuron 7, 685–693
    OpenUrlCrossRefPubMedWeb of Science
    1. Zhuo L.,
    2. Sun B.,
    3. Zhang C. L.,
    4. Fine A.,
    5. Chiu S. Y.,
    6. Messing A.
    (1997) Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev. Biol 187, 36–42
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage
P. Malatesta, E. Hartfuss, M. Gotz
Development 2000 127: 5253-5263;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

The people behind the papers – George Britton and Aryeh Warmflash

George and Aryeh

First author George Britton and his supervisor Aryeh Warmflash discuss their new Development paper in which they apply advanced in vitro culturing techniques to investigate embryonic ectoderm patterning.

Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?

Protein function can be controlled by light using optogenetic techniques. In their new Primer, Stefano De Renzis and his colleagues in Heidelberg provide an overview of the most commonly used optogenetic tools and their application in developmental biology.

preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Sundar Naganathan

preLighter Sundar Naganathan explains his selected preprint by Vikas Trivedi, Benjamin Steventon and their co-workers on pescoids, a new in vitro model system to study early zebrafish embryogenesis.

Spotlight – Can laboratory model systems instruct human limb regeneration?

An extract from a schematic demonstrating the possible pipeline for how discovery in lab model systems can influence applications for regenerative therapies.

One of the most challenging objectives of tissue regeneration research is regrowth of a lost or amputated limb. Here, Ben Cox, Maximina Yun and Kenneth Poss outline the research avenues yet to be explored to move closer to this capstone achievement.

Articles of interest in our sister journals

Tox4 modulates cell fate reprogramming

Lotte Vanheer, Juan Song, Natalie De Geest, Adrian Janiszewski, Irene Talon, Caterina Provenzano, Taeho Oh, Joel Chappell, Vincent Pasque
Journal of Cell Science

Drosophila melanogaster: a simple system for understanding complexity

Stephanie E. Mohr, Norbert Perrimon
Disease Models & Mechanisms