Published online
doi:10.1083/jcb.200608137
The Journal of Cell Biology, Vol. 176, No. 4, 483-495
The Rockefeller University Press, 0021-9525 $30.00
© Dubreuil et al.
Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1
Véronique Dubreuil1,
Anne-Marie Marzesco1,
Denis Corbeil2,
Wieland B. Huttner1, and
Michaela Wilsch-Bräuninger1
1 Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany
2 Tissue Engineering Laboratories, Biotec, D-01307 Dresden, Germany
Correspondence to Wieland B. Huttner: huttner{at}mpi-cbg.de
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-1enriched 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-1bearing 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.
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.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
Related Article
-
Pinched off membrane
- Nicole LeBrasseur
J. Cell Biol. 2007 176: 372a.
[Full Text]
[PDF]
This article has been cited by other articles:
-
Schenk, J., Wilsch-Brauninger, M., Calegari, F., Huttner, W. B.
(2009). Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc. Natl. Acad. Sci. USA
106: 16487-16492
[Abstract]
[Full Text]
-
McDonald, B., Martin-Serrano, J.
(2009). No strings attached: the ESCRT machinery in viral budding and cytokinesis. J. Cell Sci.
122: 2167-2177
[Abstract]
[Full Text]
-
Saito, K., Dubreuil, V., Arai, Y., Wilsch-Brauninger, M., Schwudke, D., Saher, G., Miyata, T., Breier, G., Thiele, C., Shevchenko, A., Nave, K.-A., Huttner, W. B.
(2009). Ablation of cholesterol biosynthesis in neural stem cells increases their VEGF expression and angiogenesis but causes neuron apoptosis. Proc. Natl. Acad. Sci. USA
106: 8350-8355
[Abstract]
[Full Text]
-
Zacchigna, S., Oh, H., Wilsch-Brauninger, M., Missol-Kolka, E., Jaszai, J., Jansen, S., Tanimoto, N., Tonagel, F., Seeliger, M., Huttner, W. B., Corbeil, D., Dewerchin, M., Vinckier, S., Moons, L., Carmeliet, P.
(2009). Loss of the Cholesterol-Binding Protein Prominin-1/CD133 Causes Disk Dysmorphogenesis and Photoreceptor Degeneration. J. Neurosci.
29: 2297-2308
[Abstract]
[Full Text]
-
Karbanova, J., Missol-Kolka, E., Fonseca, A.-V., Lorra, C., Janich, P., Hollerova, H., Jaszai, J., Ehrmann, J., Kolar, Z., Liebers, C., Arl, S., Subrtova, D., Freund, D., Mokry, J., Huttner, W. B., Corbeil, D.
(2008). The Stem Cell Marker CD133 (Prominin-1) Is Expressed in Various Human Glandular Epithelia. J. Histochem. Cytochem.
56: 977-993
[Abstract]
[Full Text]
-
Goss, J. W., Toomre, D. K.
(2008). Both daughter cells traffic and exocytose membrane at the cleavage furrow during mammalian cytokinesis. JCB
181: 1047-1054
[Abstract]
[Full Text]
-
Fish, J. L., Dehay, C., Kennedy, H., Huttner, W. B.
(2008). Making bigger brains-the evolution of neural-progenitor-cell division. J. Cell Sci.
121: 2783-2793
[Abstract]
[Full Text]
-
Carlton, J. G., Agromayor, M., Martin-Serrano, J.
(2008). Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc. Natl. Acad. Sci. USA
105: 10541-10546
[Abstract]
[Full Text]
-
Okano, H., Sawamoto, K.
(2008). Neural stem cells: involvement in adult neurogenesis and CNS repair. Phil Trans R Soc B
363: 2111-2122
[Abstract]
[Full Text]
-
Kiprilov, E. N., Awan, A., Desprat, R., Velho, M., Clement, C. A., Byskov, A. G., Andersen, C. Y., Satir, P., Bouhassira, E. E., Christensen, S. T., Hirsch, R. E.
(2008). Human embryonic stem cells in culture possess primary cilia with hedgehog signaling machinery. JCB
180: 897-904
[Abstract]
[Full Text]
-
Fleming, E. S., Zajac, M., Moschenross, D. M., Montrose, D. C., Rosenberg, D. W., Cowan, A. E., Tirnauer, J. S.
(2007). Planar Spindle Orientation and Asymmetric Cytokinesis in the Mouse Small Intestine. J. Histochem. Cytochem.
55: 1173-1180
[Abstract]
[Full Text]
-
Pfenninger, C. V., Roschupkina, T., Hertwig, F., Kottwitz, D., Englund, E., Bengzon, J., Jacobsen, S. E., Nuber, U. A.
(2007). CD133 Is Not Present on Neurogenic Astrocytes in the Adult Subventricular Zone, but on Embryonic Neural Stem Cells, Ependymal Cells, and Glioblastoma Cells. Cancer Res.
67: 5727-5736
[Abstract]
[Full Text]