Clonal analysis by distinct viral vectors identifies bona fide neural stem cells in the adult zebrafish telencephalon and characterizes their division properties and fate

被引:152
作者
Rothenaigner, Ina [1 ,2 ]
Krecsmarik, Monika [1 ]
Hayes, John A. [3 ]
Bahn, Brigitte [2 ]
Lepier, Alexandra [4 ]
Fortin, Gilles [3 ]
Goetz, Magdalena [4 ,5 ]
Jagasia, Ravi [6 ]
Bally-Cuif, Laure [1 ,2 ]
机构
[1] Inst Neurobiol Alfred Fessard, CNRS UPR 3294, Zebrafish Neurogenet Grp, Lab Neurobiol & Dev N&D, F-91198 Gif Sur Yvette, France
[2] German Res Ctr Environm Hlth, Helmholtz Ctr Munich, Dept Zebrafish Neurogenet, D-85764 Neuherberg, Germany
[3] Inst Neurobiol Alfred Fessard, CNRS UPR 3294, Hindbrain Integrat Neurobiol, Lab Neurobiol & Dev N&D, F-91198 Gif Sur Yvette, France
[4] Univ Munich, Inst Physiol, Dept Physiol Genom, D-80336 Munich, Germany
[5] German Res Ctr Environm Hlth, Helmholtz Ctr Munich, Inst Stem Cell Res, D-85764 Neuherberg, Germany
[6] CNS Discovery Res, CH-4070 Basel, Switzerland
来源
DEVELOPMENT | 2011年 / 138卷 / 08期
关键词
Retroviral transduction; Adult neurogenesis; Neural stem cells; Notch; NEWLY GENERATED NEURONS; LONG-TERM SURVIVAL; OLFACTORY-BULB; IN-VIVO; PROGENITOR CELLS; DENTATE GYRUS; HIPPOCAMPAL NEUROGENESIS; RETROVIRAL VECTORS; SYNAPSE FORMATION; SUBSTANTIA-NIGRA;
D O I
10.1242/dev.058156
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Neurogenesis is widespread in the zebrafish adult brain through the maintenance of active germinal niches. To characterize which progenitor properties correlate with this extensive neurogenic potential, we set up a method that allows progenitor cell transduction and tracing in the adult zebrafish brain using GFP-encoding retro- and lentiviruses. The telencephalic germinal zone of the zebrafish comprises quiescent radial glial progenitors and actively dividing neuroblasts. Making use of the power of clonal viral vector-based analysis, we demonstrate that these progenitors follow different division modes and fates: neuroblasts primarily undergo a limited amplification phase followed by symmetric neurogenic divisions; by contrast, radial glia are capable at the single cell level of both self-renewing and generating different cell types, and hence exhibit bona fide neural stem cell (NSC) properties in vivo. We also show that radial glial cells predominantly undergo symmetric gliogenic divisions, which amplify this NSC pool and may account for its long-lasting maintenance. We further demonstrate that blocking Notch signaling results in a significant increase in proliferating cells and in the numbers of clones, but does not affect clone composition, demonstrating that Notch primarily controls proliferation rather than cell fate. Finally, through long-term tracing, we illustrate the functional integration of newborn neurons in forebrain adult circuitries. These results characterize fundamental aspects of adult progenitor cells and neurogenesis, and open the way to using virus-based technologies for stable genetic manipulations and clonal analyses in the zebrafish adult brain.
引用
收藏
页码:1459 / 1469
页数:11
相关论文
共 58 条
[1]   Notch1 Is Required for Maintenance of the Reservoir of Adult Hippocampal Stem Cells [J].
Ables, Jessica L. ;
DeCarolis, Nathan A. ;
Johnson, Madeleine A. ;
Rivera, Phillip D. ;
Gao, Zhengliang ;
Cooper, Don C. ;
Radtke, Freddy ;
Hsieh, Jenny ;
Eisch, Amelia J. .
JOURNAL OF NEUROSCIENCE, 2010, 30 (31) :10484-10492
[2]   Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon [J].
Adolf, Birgit ;
Chapouton, Prisca ;
Lam, Chen Sok ;
Topp, Stefanie ;
Tannhaeuser, Birgit ;
Straehle, Uwe ;
Goetz, Magdalena ;
Bally-Cuif, Laure .
DEVELOPMENTAL BIOLOGY, 2006, 295 (01) :278-293
[3]   A Dlx2-and Pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb [J].
Brill, Monika S. ;
Snapyan, Marina ;
Wohlfrom, Hilde ;
Ninkovic, Jovica ;
Jawerka, Melanie ;
Mastick, Grant S. ;
Ashery-Padan, Ruth ;
Saghatelyan, Armen ;
Berninger, Benedikt ;
Goetz, Magdalena .
JOURNAL OF NEUROSCIENCE, 2008, 28 (25) :6439-6452
[4]   VESICULAR STOMATITIS-VIRUS G GLYCOPROTEIN PSEUDOTYPED RETROVIRAL VECTORS - CONCENTRATION TO VERY HIGH-TITER AND EFFICIENT GENE-TRANSFER INTO MAMMALIAN AND NONMAMMALIAN CELLS [J].
BURNS, JC ;
FRIEDMANN, T ;
DRIEVER, W ;
BURRASCANO, M ;
YEE, JK .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1993, 90 (17) :8033-8037
[5]   Becoming a new neuron in the adult olfactory bulb [J].
Carleton, A ;
Petreanu, LT ;
Lansford, R ;
Alvarez-Buylla, A ;
Lledo, PM .
NATURE NEUROSCIENCE, 2003, 6 (05) :507-518
[6]   Lineage analysis using retroviral vectors [J].
Cepko, CL ;
Ryder, E ;
Austin, C ;
Golden, J ;
Fields-Berry, S ;
Lin, J .
METHODS-A COMPANION TO METHODS IN ENZYMOLOGY, 1998, 14 (04) :393-406
[7]   Adult neurogenesis in non-mammalian vertebrates [J].
Chapouton, Prisca ;
Jagasia, Ravi ;
Bally-Cuif, Laure .
BIOESSAYS, 2007, 29 (08) :745-757
[8]   Notch Activity Levels Control the Balance between Quiescence and Recruitment of Adult Neural Stem Cells [J].
Chapouton, Prisca ;
Skupien, Paulina ;
Hesl, Birgit ;
Coolen, Marion ;
Moore, John C. ;
Madelaine, Romain ;
Kremmer, Elizabeth ;
Faus-Kessler, Theresa ;
Blader, Patrick ;
Lawson, Nathan D. ;
Bally-Cuif, Laure .
JOURNAL OF NEUROSCIENCE, 2010, 30 (23) :7961-7974
[9]   High-throughput selection of retrovirus producer cell lines leads to markedly improved efficiency of germ line-transmissible insertions in zebra fish [J].
Chen, WB ;
Burgess, S ;
Golling, G ;
Amsterdam, A ;
Hopkins, N .
JOURNAL OF VIROLOGY, 2002, 76 (05) :2192-2198
[10]   CLEAVAGE ORIENTATION AND THE ASYMMETRIC INHERITANCE OF NOTCH1 IMMUNOREACTIVITY IN MAMMALIAN NEUROGENESIS [J].
CHENN, A ;
MCCONNELL, SK .
CELL, 1995, 82 (04) :631-641