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Live Imaging at the Onset of Cortical Neurogenesis Reveals Differential Appearance of the Neuronal Phenotype in Apical versus Basal Progenitor Progeny

Attardo, Alessio and Calegari, Federico and Haubensak, Wulf and Wilsch-Bräuninger, Michaela and Huttner, Wieland B. (2008) Live Imaging at the Onset of Cortical Neurogenesis Reveals Differential Appearance of the Neuronal Phenotype in Apical versus Basal Progenitor Progeny. PLoS ONE, 3 (6). e2388. ISSN 1932-6203. PMCID PMC2398773. https://resolver.caltech.edu/CaltechAUTHORS:ATTplosone08

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Image (TIFF) (Figure S1. The BAC construct used to generate the transgenic Tubb3-mGFP mouse line) - Supplemental Material
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Image (GIF) (Figure S1. The BAC construct used to generate the transgenic Tubb3-mGFP mouse line) - Supplemental Material
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Image (TIFF) (Figure S2. Intrinsic GFP fluorescence in the central and peripheral nervous system of embryonic and postnatal Tubb3-mGFP mice) - Supplemental Material
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Image (JPEG) (Figure S2. Intrinsic GFP fluorescence in the central and peripheral nervous system of embryonic and postnatal Tubb3-mGFP mice) - Supplemental Material
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Image (TIFF) (Figure S3. Behavior of individual daughter cell pairs arising from apical and basal progenitors) - Supplemental Material
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Image (JPEG) (Figure S3. Behavior of individual daughter cell pairs arising from apical and basal progenitors) - Supplemental Material
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Image (TIFF) (Figure S4. Early polarization events in neurons at the onset of neurogenesis) - Supplemental Material
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Image (GIF) (Figure S4. Early polarization events in neurons at the onset of neurogenesis) - Supplemental Material
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[img] Video (QuickTime) (Movie S1. A Tis21-nucGFP-positive neurogenic progenitor divides at the basal side of the ventricular zone) - Supplemental Material
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[img] Video (QuickTime) (Movie S2. A Tis21-nucGFP-positive neurogenic progenitor Tis21-nucGFP divides in a subapical location) - Supplemental Material
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[img] Video (QuickTime) (Movie S3. A Tis21-nucGFP-positive neurogenic progenitor migrates rapidly from the basal boundary of the ventricular zone to the apical surface and divides) - Supplemental Material
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[img] Video (QuickTime) (Movie S4. An electroporated cell on the basal side of the neuroepithelium (BP), retracts its apical contact (red arrowhead) prior to mitosis) - Supplemental Material
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[img] Video (QuickTime) (Movie S5. A Tubb3-mGFP-positive neuron, which no longer shows Tis21-nucGFP fluorescence, resides in the ventricular zone, with bright perinuclear fluorescence...) - Supplemental Material
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[img] Video (QuickTime) (Movie S6. The processes of two Tubb3-mGFP-positive neurons grow towards the ventricular surface and flatten) - Supplemental Material
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Abstract

The neurons of the mammalian brain are generated by progenitors dividing either at the apical surface of the ventricular zone (neuroepithelial and radial glial cells, collectively referred to as apical progenitors) or at its basal side (basal progenitors, also called intermediate progenitors). For apical progenitors, the orientation of the cleavage plane relative to their apical-basal axis is thought to be of critical importance for the fate of the daughter cells. For basal progenitors, the relationship between cell polarity, cleavage plane orientation and the fate of daughter cells is unknown. Here, we have investigated these issues at the very onset of cortical neurogenesis. To directly observe the generation of neurons from apical and basal progenitors, we established a novel transgenic mouse line in which membrane GFP is expressed from the beta-III-tubulin promoter, an early pan-neuronal marker, and crossed this line with a previously described knock-in line in which nuclear GFP is expressed from the Tis21 promoter, a pan-neurogenic progenitor marker. Mitotic Tis21-positive basal progenitors nearly always divided symmetrically, generating two neurons, but, in contrast to symmetrically dividing apical progenitors, lacked apical-basal polarity and showed a nearly randomized cleavage plane orientation. Moreover, the appearance of beta-III-tubulin–driven GFP fluorescence in basal progenitor-derived neurons, in contrast to that in apical progenitor-derived neurons, was so rapid that it suggested the initiation of the neuronal phenotype already in the progenitor. Our observations imply that (i) the loss of apical-basal polarity restricts neuronal progenitors to the symmetric mode of cell division, and that (ii) basal progenitors initiate the expression of neuronal phenotype already before mitosis, in contrast to apical progenitors.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1371/journal.pone.0002388DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc2398773/PubMed CentralArticle
Additional Information:© 2008 Alessio et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: December 16, 2007; Accepted: April 29, 2008; Published: June 11, 2008. We thank Dr. S. Agraves for megalin antibody, K. Langenfeld for performing the immunoblotting, the Transgenic Core Facility (R. Naumann), Light Microscopy Facility (K. Anderson and J. Peychl) and Animal Facility (J. Helppi) of MPI-CBG for excellent support, and Dr. J. Fish for helpful comments on the manuscript. A.A. was a member of the International Max Planck Research School for Molecular Cell Biology and Bioengineering. Author Contributions: Conceived and designed the experiments: WH WH FC WH AA. Performed the experiments: MW AA. Analyzed the data: AA. Wrote the paper: WH WH FC AA. Funding: W.B.H. was supported by grants from the DFG (SPP 1109, Hu 275/7-3; SPP 1111, Hu 275/8-3; SFB/TR 13, B1; SFB 655, A2), by the DFG-funded Center for Regenerative Therapies Dresden, by the Fonds der Chemischen Industrie and by the Federal Ministry of Education and Research (BMBF) in the framework of the National Genome Research Network (NGFN-2, SMP RNAi, 01GR0402, PRI-S08T05). Competing interests: The authors have declared that no competing interests exist.
Issue or Number:6
PubMed Central ID:PMC2398773
Record Number:CaltechAUTHORS:ATTplosone08
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:ATTplosone08
Official Citation:Attardo A, Calegari F, Haubensak W, Wilsch-Bräuninger M, Huttner WB (2008) Live Imaging at the Onset of Cortical Neurogenesis Reveals Differential Appearance of the Neuronal Phenotype in Apical versus Basal Progenitor Progeny. PLoS ONE 3(6): e2388. doi:10.1371/journal.pone.0002388
Usage Policy:This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
ID Code:11066
Collection:CaltechAUTHORS
Deposited By: Archive Administrator
Deposited On:25 Jun 2008
Last Modified:06 Jul 2020 22:38

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