Expansion of the neocortex requires symmetric divisions of neuroepithelial cells, the primary progenitor cells of the developing mammalian central nervous system. Symmetrically dividing neuroepithelial cells are known to form a midbody at their apical (rather than lateral) surface. We show that apical midbodies of neuroepithelial cells concentrate prominin-1 (CD133), a somatic stem cell marker and defining constituent of a specific plasma membrane microdomain. Moreover, these apical midbodies are released, as a whole or in part, into the extracellular space, yielding the prominin-1–enriched membrane particles found in the neural tube fluid. The primary cilium of neuroepithelial cells also concentrates prominin-1 and appears to be a second source of the prominin-1–bearing extracellular membrane particles. Our data reveal novel origins of extracellular membrane traffic that enable neural stem and progenitor cells to avoid the asymmetric inheritance of the midbody observed for other cells and, by releasing a stem cell membrane microdomain, to potentially influence the balance of their proliferation versus differentiation.
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12 February 2007
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February 05 2007
Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1
Véronique Dubreuil,
Véronique Dubreuil
1Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
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Anne-Marie Marzesco,
Anne-Marie Marzesco
1Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
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Denis Corbeil,
Denis Corbeil
2Tissue Engineering Laboratories, Biotec, D-01307 Dresden, Germany
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Wieland B. Huttner,
Wieland B. Huttner
1Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
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Michaela Wilsch-Bräuninger
Michaela Wilsch-Bräuninger
1Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
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Véronique Dubreuil
1Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
Anne-Marie Marzesco
1Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
Denis Corbeil
2Tissue Engineering Laboratories, Biotec, D-01307 Dresden, Germany
Wieland B. Huttner
1Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
Michaela Wilsch-Bräuninger
1Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
Correspondence to Wieland B. Huttner: [email protected]
V. Dubreuil's present address is UMR 8542, Centre National de la Recherche Scientifique, Ecole Normale Supèrieure, F-75005 Paris, France.
Abbreviations used in this paper: DIC, differential interference contrast; E, embryonic day; HH, Hamburger and Hamilton; mRFP, monomeric red fluorescent protein; NE, neuroepithelial.
Received:
August 22 2006
Accepted:
January 06 2007
Online ISSN: 1540-8140
Print ISSN: 0021-9525
The Rockefeller University Press
2007
J Cell Biol (2007) 176 (4): 483–495.
Article history
Received:
August 22 2006
Accepted:
January 06 2007
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Citation
Véronique Dubreuil, Anne-Marie Marzesco, Denis Corbeil, Wieland B. Huttner, Michaela Wilsch-Bräuninger; Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1 . J Cell Biol 12 February 2007; 176 (4): 483–495. doi: https://doi.org/10.1083/jcb.200608137
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