 |
The Journal of Neuroscience, November 17, 2004, 24(46):10530-10541; doi:10.1523/JNEUROSCI.3572-04.2004
 Previous Article | Next Article 
Development/Plasticity/Repair
Postnatal Neurogenesis and Gliogenesis in the Olfactory Bulb from NG2-Expressing Progenitors of the Subventricular Zone
Adan Aguirre and
Vittorio Gallo
Center for Neuroscience Research, Children's Research Institute, Children's National Medical Center, Washington, DC 20010
We used a 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNP)-enhanced green fluorescent protein (EGFP) transgenic mouse to study postnatal subventricular zone (SVZ) progenitor fate, with a focus on the olfactory bulb (OB). The postnatal OB of the CNP-EGFP mouse contained EGFP+ interneurons and oligodendrocytes. In the anterior SVZ, the majority of EGFP+ progenitors were NG2+. These NG2+/EGFP+ progenitors expressed the OB interneuron marker Er81, the neuroblast markers doublecortin (DC) and Distalless-related homeobox (DLX), or the oligodendrocyte progenitor marker Nkx2.2. In the rostral migratory stream (RMS), EGFP+ cells displayed a migrating phenotype. A fraction of these cells were either NG2-/Er81+/DC+/DLX+ or NG2+/Nkx2.2+. DiI (1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate) injection into the lateral ventricle (LV) of early postnatal mice demonstrated that NG2+/EGFP+ progenitors migrate from the SVZ through the RMS into the OB. Moreover, fluorescence-activated cell-sorting-purified NG2+/CNP-EGFP+ or NG2+/ -actin-enhanced yellow fluorescent protein-positive (EYFP+) progenitors transplanted into the early postnatal LV displayed extensive rostral and caudal migration. EYFP+ or EGFP+ graft-derived cells within the RMS were DLX+/Er81+ or Nkx2.2+, migrated to the OB, and differentiated to interneurons and oligodendrocytes. In the subcortical white matter (SCWM), grafted cells differentiated to either oligodendrocytes or astrocytes. Transplantation of NG2+/EYFP+ progenitors selectively purified from the SVZ showed that these cells were migratory and generated glia and neurons in the OB, hippocampus, and striatum. In contrast, cortical, OB, or cerebellar NG2+ cells had a very limited migratory potential and gave rise to glia in the SCWM and striatum. Our findings indicate region-specific differences between NG2+ progenitor cells and show that NG2+ cells can migrate throughout the RMS and contribute to both gliogenesis and neurogenesis in the postnatal OB.
Key words: CNP-EGFP transgenic mice; neural progenitor; oligodendrocyte; interneuron; cell migration; rostral migratory stream
Received Aug 30, 2004;
revised October 11, 2004;
accepted October 14, 2004.
This article has been cited by other articles:
|
|
|
|
 
P. He and Y. Shen
Interruption of {beta}-Catenin Signaling Reduces Neurogenesis in Alzheimer's Disease
J. Neurosci.,
May 20, 2009;
29(20):
6545 - 6557.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
X. Li, X. Tang, B. Jablonska, A. Aguirre, V. Gallo, and M. B. Luskin
p27KIP1 Regulates Neurogenesis in the Rostral Migratory Stream and Olfactory Bulb of the Postnatal Mouse
J. Neurosci.,
March 4, 2009;
29(9):
2902 - 2914.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. M. Fagel, Y. Ganat, E. Cheng, J. Silbereis, Y. Ohkubo, L. R. Ment, and F. M. Vaccarino
Fgfr1 Is Required for Cortical Regeneration and Repair after Perinatal Hypoxia
J. Neurosci.,
January 28, 2009;
29(4):
1202 - 1211.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T.-S. Yu, G. Zhang, D. J. Liebl, and S. G. Kernie
Traumatic Brain Injury-Induced Hippocampal Neurogenesis Requires Activation of Early Nestin-Expressing Progenitors
J. Neurosci.,
November 26, 2008;
28(48):
12901 - 12912.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Alonso, I. Ortega-Perez, M. S. Grubb, J.-P. Bourgeois, P. Charneau, and P.-M. Lledo
Turning Astrocytes from the Rostral Migratory Stream into Neurons: A Role for the Olfactory Sensory Organ
J. Neurosci.,
October 22, 2008;
28(43):
11089 - 11102.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Bohl, S. Liu, S. Blanchard, M. Hocquemiller, G. Haase, and J.-M. Heard
Directed Evolution of Motor Neurons from Genetically Engineered Neural Precursors
Stem Cells,
October 1, 2008;
26(10):
2564 - 2575.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Gallo, J.-M. Mangin, M. Kukley, and D. Dietrich
Synapses on NG2-expressing progenitors in the brain: multiple functions?
J. Physiol.,
August 15, 2008;
586(16):
3767 - 3781.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-M. Mangin, A. Kunze, R. Chittajallu, and V. Gallo
Satellite NG2 Progenitor Cells Share Common Glutamatergic Inputs with Associated Interneurons in the Mouse Dentate Gyrus
J. Neurosci.,
July 23, 2008;
28(30):
7610 - 7623.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Gadea, S. Schinelli, and V. Gallo
Endothelin-1 Regulates Astrocyte Proliferation and Reactive Gliosis via a JNK/c-Jun Signaling Pathway
J. Neurosci.,
March 5, 2008;
28(10):
2394 - 2408.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
X. Zhu, D. E. Bergles, and A. Nishiyama
NG2 cells generate both oligodendrocytes and gray matter astrocytes
Development,
January 1, 2008;
135(1):
145 - 157.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Jablonska, A. Aguirre, R. Vandenbosch, S. Belachew, C. Berthet, P. Kaldis, and V. Gallo
Cdk2 is critical for proliferation and self-renewal of neural progenitor cells in the adult subventricular zone
J. Cell Biol.,
December 17, 2007;
179(6):
1231 - 1245.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. A. Lim, S. Cha, M. C. Mayo, M.-H. Chen, E. Keles, S. VandenBerg, and M. S. Berger
Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype
Neuro-oncol,
October 1, 2007;
9(4):
424 - 429.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Liu, Y. R. Han, J. Li, D. Sun, M. Ouyang, M. R. Plummer, and P. Casaccia-Bonnefil
The Glial or Neuronal Fate Choice of Oligodendrocyte Progenitors Is Modulated by Their Ability to Acquire an Epigenetic Memory
J. Neurosci.,
July 4, 2007;
27(27):
7339 - 7343.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Yanagisawa and R. K Yu
The expression and functions of glycoconjugates in neural stem cells
Glycobiology,
July 1, 2007;
17(7):
57R - 74R.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Bovetti, Y.-C. Hsieh, P. Bovolin, I. Perroteau, T. Kazunori, and A. C. Puche
Blood Vessels Form a Scaffold for Neuroblast Migration in the Adult Olfactory Bulb
J. Neurosci.,
May 30, 2007;
27(22):
5976 - 5980.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Roy, J. C. Murtie, B. F. El-Khodor, N. Edgar, S. P. Sardi, B. M. Hooks, M. Benoit-Marand, C. Chen, H. Moore, P. O'Donnell, et al.
Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders
PNAS,
May 8, 2007;
104(19):
8131 - 8136.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Nishiyama
Polydendrocytes: NG2 Cells with Many Roles in Development and Repair of the CNS
Neuroscientist,
February 1, 2007;
13(1):
62 - 76.
[Abstract]
[PDF]
|
|
|
|
|
|
|
C. Dromard, S. Bartolami, L. Deleyrolle, H. Takebayashi, C. Ripoll, L. Simonneau, S. Prome, S. Puech, C. Tran Van Ba, C. Duperray, et al.
NG2 and Olig2 Expression Provides Evidence for Phenotypic Deregulation of Cultured Central Nervous System and Peripheral Nervous System Neural Precursor Cells
Stem Cells,
February 1, 2007;
25(2):
340 - 353.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. J. Ohab, S. Fleming, A. Blesch, and S. T. Carmichael
A Neurovascular Niche for Neurogenesis after Stroke
J. Neurosci.,
December 13, 2006;
26(50):
13007 - 13016.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Kaga, W. J. Shoemaker, M. Furusho, M. Bryant, J. Rosenbluth, S. E. Pfeiffer, L. Oh, M. Rasband, C. Lappe-Siefke, K. Yu, et al.
Mice with Conditional Inactivation of Fibroblast Growth Factor Receptor-2 Signaling in Oligodendrocytes Have Normal Myelin But Display Dramatic Hyperactivity when Combined with Cnp1 Inactivation.
J. Neurosci.,
November 22, 2006;
26(47):
12339 - 12350.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Sohn, J. Natale, L.-J. Chew, S. Belachew, Y. Cheng, A. Aguirre, J. Lytle, B. Nait-Oumesmar, C. Kerninon, M. Kanai-Azuma, et al.
Identification of Sox17 as a transcription factor that regulates oligodendrocyte development.
J. Neurosci.,
September 20, 2006;
26(38):
9722 - 9735.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Balenci, I. D. Clarke, P. B. Dirks, N. Assard, F. Ducray, A. Jouvet, M.-F. Belin, J. Honnorat, and J. Baudier
IQGAP1 Protein Specifies Amplifying Cancer Cells in Glioblastoma Multiforme.
Cancer Res.,
September 15, 2006;
66(18):
9074 - 9082.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. M. Ganat, J. Silbereis, C. Cave, H. Ngu, G. M. Anderson, Y. Ohkubo, L. R. Ment, and F. M. Vaccarino
Early Postnatal Astroglial Cells Produce Multilineage Precursors and Neural Stem Cells In Vivo.
J. Neurosci.,
August 15, 2006;
26(33):
8609 - 8621.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W.-P. Ge, X.-J. Yang, Z. Zhang, H.-K. Wang, W. Shen, Q.-D. Deng, and S. Duan
Long-term potentiation of neuron-glia synapses mediated by Ca2+-permeable AMPA receptors.
Science,
June 9, 2006;
312(5779):
1533 - 1537.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. S. Gal, Y. M. Morozov, A. E. Ayoub, M. Chatterjee, P. Rakic, and T. F. Haydar
Molecular and Morphological Heterogeneity of Neural Precursors in the Mouse Neocortical Proliferative Zones
J. Neurosci.,
January 18, 2006;
26(3):
1045 - 1056.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Zhou, G. P. Schools, and H. K. Kimelberg
Development of GLAST(+) Astrocytes and NG2(+) Glia in Rat Hippocampus CA1: Mature Astrocytes Are Electrophysiologically Passive
J Neurophysiol,
January 1, 2006;
95(1):
134 - 143.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Aguirre, T. A. Rizvi, N. Ratner, and V. Gallo
Overexpression of the Epidermal Growth Factor Receptor Confers Migratory Properties to Nonmigratory Postnatal Neural Progenitors
J. Neurosci.,
November 30, 2005;
25(48):
11092 - 11106.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Komitova, B. Mattsson, B. B. Johansson, and P. S. Eriksson
Enriched Environment Increases Neural Stem/Progenitor Cell Proliferation and Neurogenesis in the Subventricular Zone of Stroke-Lesioned Adult Rats
Stroke,
June 1, 2005;
36(6):
1278 - 1282.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
