 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 12, 249-256, Copyright © 1992 by Society for Neuroscience
Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain
CM Morshead and D van der Kooy
Department of Anatomy, University of Toronto, Ontario, Canada.
The early development of the mammalian forebrain involves the massive
proliferation of the ventricular zone cells lining the lateral ventricles.
A remnant of this highly proliferative region persists into adult life,
where it is known as the subependymal layer. We examined the proliferation
kinetics and fates of the mitotically active cells in the subependyma of
the adult mouse. The medial edge, the lateral edge, and the dorsolateral
corner of the subependymal layer of the rostral portion of the lateral
ventricle each contained mitotically active cells, but the dorsolateral
region had the highest percentage of bromodeoxyuridine (BrdU)-labeled cells
per unit area. Repeated injections of BrdU over 14 hr revealed a
proliferation curve for the dorsolateral population with a growth fraction
of 33%, indicating that 33% of the cells in this subependymal region make
up the proliferating population. The total cell cycle time in this
population was approximately 12.7 hr, with an S-phase of 4.2 hr. To examine
the fate of these proliferating cells, we injected low concentrations of a
replication-deficient, recombinant retrovirus directly into the lateral
ventricles of adult mice for uptake by mitotically active subependymal
cells. Regardless of the survival time postinjection (10 hr, 1 d, 2 d, or 8
d), the number of retrovirally labeled cells per clone remained the same (1
or 2 cells/clone). This suggests that one of the progeny from each cell
division dies. Moreover, the clones remained confined to the subependyma
and labeled cells were not seen in the surrounding brain tissue. Thus,
while 33% of the dorsolateral subependymal cells continue to proliferate in
adult life, the fate of the postmitotic progeny is death.
This article has been cited by other articles:
|
|
|
|
 
S. Pluchino, L. Muzio, J. Imitola, M. Deleidi, C. Alfaro-Cervello, G. Salani, C. Porcheri, E. Brambilla, F. Cavasinni, A. Bergamaschi, et al.
Persistent inflammation alters the function of the endogenous brain stem cell compartment
Brain,
August 30, 2008;
(2008)
awn198v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. G. Golmohammadi, D. G. Blackmore, B. Large, H. Azari, E. Esfandiary, G. Paxinos, K. B. J. Franklin, B. A. Reynolds, and R. L. Rietze
Comparative Analysis of the Frequency and Distribution of Stem and Progenitor Cells in the Adult Mouse Brain
Stem Cells,
April 1, 2008;
26(4):
979 - 987.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. C. Pruitt, K. J. Bailey, and A. Freeland
Reduced Mcm2 Expression Results in Severe Stem/Progenitor Cell Deficiency and Cancer
Stem Cells,
December 1, 2007;
25(12):
3121 - 3132.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Adachi, Z. Mirzadeh, M. Sakaguchi, T. Yamashita, T. Nikolcheva, Y. Gotoh, G. Peltz, L. Gong, T. Kawase, A. Alvarez-Buylla, et al.
{beta}-Catenin Signaling Promotes Proliferation of Progenitor Cells in the Adult Mouse Subventricular Zone
Stem Cells,
November 1, 2007;
25(11):
2827 - 2836.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Vanderluit, C. A. Wylie, K. A. McClellan, N. Ghanem, A. Fortin, S. Callaghan, J. G. MacLaurin, D. S. Park, and R. S. Slack
The Retinoblastoma family member p107 regulates the rate of progenitor commitment to a neuronal fate
J. Cell Biol.,
October 3, 2007;
178(1):
129 - 139.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. A. McClellan, V. A. Ruzhynsky, D. N. Douda, J. L. Vanderluit, K. L. Ferguson, D. Chen, R. Bremner, D. S. Park, G. Leone, and R. S. Slack
Unique Requirement for Rb/E2F3 in Neuronal Migration: Evidence for Cell Cycle-Independent Functions
Mol. Cell. Biol.,
July 1, 2007;
27(13):
4825 - 4843.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Schmidt
The Olfactory Pathway of Decapod Crustaceans--An Invertebrate Model for Life-Long Neurogenesis
Chem Senses,
May 1, 2007;
32(4):
365 - 384.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. D. Merson, M. P. Dixon, C. Collin, R. L. Rietze, P. F. Bartlett, T. Thomas, and A. K. Voss
The transcriptional coactivator querkopf controls adult neurogenesis.
J. Neurosci.,
November 1, 2006;
26(44):
11359 - 11370.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. M. C. Batista, T. E. Kippin, S. Willaime-Morawek, M. K. Shimabukuro, W. Akamatsu, and D. van der Kooy
A Progressive and Cell Non-Autonomous Increase in Striatal Neural Stem Cells in the Huntington's Disease R6/2 Mouse
J. Neurosci.,
October 11, 2006;
26(41):
10452 - 10460.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Matsumoto, M. Morioka, Y. Hasegawa, T. Kawano, Y. Yoshinaga, T. Maeda, S. Yano, Y. Kai, K. Fukunaga, and J.-i. Kuratsu
Sodium Orthovanadate Enhances Proliferation of Progenitor Cells in the Adult Rat Subventricular Zone after Focal Cerebral Ischemia
J. Pharmacol. Exp. Ther.,
September 1, 2006;
318(3):
982 - 991.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. C. Burns, X. R. Ortiz-Gonzalez, M. Gutierrez-Perez, C. D. Keene, R. Sharda, Z. L. Demorest, Y. Jiang, M. Nelson-Holte, M. Soriano, Y. Nakagawa, et al.
Thymidine Analogs Are Transferred from Prelabeled Donor to Host Cells in the Central Nervous System After Transplantation: A Word of Caution
Stem Cells,
April 1, 2006;
24(4):
1121 - 1127.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Bauer and P. H. Patterson
The cell cycle-apoptosis connection revisited in the adult brain
J. Cell Biol.,
November 21, 2005;
171(4):
641 - 650.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. J. Bharali, I. Klejbor, E. K. Stachowiak, P. Dutta, I. Roy, N. Kaur, E. J. Bergey, P. N. Prasad, and M. K. Stachowiak
Organically modified silica nanoparticles: A nonviral vector for in vivo gene delivery and expression in the brain
PNAS,
August 9, 2005;
102(32):
11539 - 11544.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Scheffler, N. M. Walton, D. D. Lin, A. K. Goetz, G. Enikolopov, S. N. Roper, and D. A. Steindler
Phenotypic and functional characterization of adult brain neuropoiesis
PNAS,
June 28, 2005;
102(26):
9353 - 9358.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. E. Kippin, S. Kapur, and D. van der Kooy
Dopamine Specifically Inhibits Forebrain Neural Stem Cell Proliferation, Suggesting a Novel Effect of Antipsychotic Drugs
J. Neurosci.,
June 15, 2005;
25(24):
5815 - 5823.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. N. Abrous, M. Koehl, and M. Le Moal
Adult Neurogenesis: From Precursors to Network and Physiology
Physiol Rev,
April 1, 2005;
85(2):
523 - 569.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. E. Kippin, D. J. Martens, and D. van der Kooy
p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity
Genes & Dev.,
March 15, 2005;
19(6):
756 - 767.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Vanderluit, K. L. Ferguson, V. Nikoletopoulou, M. Parker, V. Ruzhynsky, T. Alexson, S. M. McNamara, D. S. Park, M. Rudnicki, and R. S. Slack
p107 regulates neural precursor cells in the mammalian brain
J. Cell Biol.,
September 13, 2004;
166(6):
853 - 863.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Chmielnicki, A. Benraiss, A. N. Economides, and S. A. Goldman
Adenovirally Expressed Noggin and Brain-Derived Neurotrophic Factor Cooperate to Induce New Medium Spiny Neurons from Resident Progenitor Cells in the Adult Striatal Ventricular Zone
J. Neurosci.,
March 3, 2004;
24(9):
2133 - 2142.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Jin, A. L. Peel, X. O. Mao, L. Xie, B. A. Cottrell, D. C. Henshall, and D. A. Greenberg
Increased hippocampal neurogenesis in Alzheimer's disease
PNAS,
January 6, 2004;
101(1):
343 - 347.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. A. Packer, Y. Stasiv, A. Benraiss, E. Chmielnicki, A. Grinberg, H. Westphal, S. A. Goldman, and G. Enikolopov
Nitric oxide negatively regulates mammalian adult neurogenesis
PNAS,
August 5, 2003;
100(16):
9566 - 9571.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Dihne, C. Bernreuther, M. Sibbe, W. Paulus, and M. Schachner
A New Role for the Cell Adhesion Molecule L1 in Neural Precursor Cell Proliferation, Differentiation, and Transmitter-Specific Subtype Generation
J. Neurosci.,
July 23, 2003;
23(16):
6638 - 6650.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Kaushal, J. J. A. Contos, K. Treuner, A. H. Yang, M. A. Kingsbury, S. K. Rehen, M. J. McConnell, M. Okabe, C. Barlow, and J. Chun
Alteration of Gene Expression by Chromosome Loss in the Postnatal Mouse Brain
J. Neurosci.,
July 2, 2003;
23(13):
5599 - 5606.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Shingo, C. Gregg, E. Enwere, H. Fujikawa, R. Hassam, C. Geary, J. C. Cross, and S. Weiss
Pregnancy-Stimulated Neurogenesis in the Adult Female Forebrain Mediated by Prolactin
Science,
January 3, 2003;
299(5603):
117 - 120.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Jin, Y. Zhu, Y. Sun, X. O. Mao, L. Xie, and D. A. Greenberg
Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo
PNAS,
September 3, 2002;
99(18):
11946 - 11950.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. J. Bernier, A. Bedard, J. Vinet, M. Levesque, and A. Parent
Newly generated neurons in the amygdala and adjoining cortex of adult primates
PNAS,
August 20, 2002;
99(17):
11464 - 11469.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Petreanu and A. Alvarez-Buylla
Maturation and Death of Adult-Born Olfactory Bulb Granule Neurons: Role of Olfaction
J. Neurosci.,
July 15, 2002;
22(14):
6106 - 6113.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. J. Bonthius, J. Mahoney, M. J. Buchmeier, B. Karacay, and D. Taggard
Critical Role for Glial Cells in the Propagation and Spread of Lymphocytic Choriomeningitis Virus in the Developing Rat Brain
J. Virol.,
June 5, 2002;
76(13):
6618 - 6635.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Belvindrah, G. Rougon, and G. Chazal
Increased Neurogenesis in Adult mCD24-Deficient Mice
J. Neurosci.,
May 1, 2002;
22(9):
3594 - 3607.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Rochefort, G. Gheusi, J.-D. Vincent, and P.-M. Lledo
Enriched Odor Exposure Increases the Number of Newborn Neurons in the Adult Olfactory Bulb and Improves Odor Memory
J. Neurosci.,
April 1, 2002;
22(7):
2679 - 2689.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Doetsch, J. M.-G. Verdugo, I. Caille, A. Alvarez-Buylla, M. V. Chao, and P. Casaccia-Bonnefil
Lack of the Cell-Cycle Inhibitor p27Kip1 Results in Selective Increase of Transit-Amplifying Cells for Adult Neurogenesis
J. Neurosci.,
March 15, 2002;
22(6):
2255 - 2264.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Pencea, K. D. Bingaman, S. J. Wiegand, and M. B. Luskin
Infusion of Brain-Derived Neurotrophic Factor into the Lateral Ventricle of the Adult Rat Leads to New Neurons in the Parenchyma of the Striatum, Septum, Thalamus, and Hypothalamus
J. Neurosci.,
September 1, 2001;
21(17):
6706 - 6717.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Chambers, Y Peng, H Nguyen, N Gaiano, G Fishell, and J. Nye
Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors
Development,
January 3, 2001;
128(5):
689 - 702.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R. Raballo, J. Rhee, R. Lyn-Cook, J. F. Leckman, M. L. Schwartz, and F. M. Vaccarino
Basic Fibroblast Growth Factor (Fgf2) Is Necessary for Cell Proliferation and Neurogenesis in the Developing Cerebral Cortex
J. Neurosci.,
July 1, 2000;
20(13):
5012 - 5023.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M.-C. Amoureux, B. A. Cunningham, G. M. Edelman, and K. L. Crossin
N-CAM Binding Inhibits the Proliferation of Hippocampal Progenitor Cells and Promotes Their Differentiation to a Neuronal Phenotype
J. Neurosci.,
May 15, 2000;
20(10):
3631 - 3640.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Gheusi, H. Cremer, H. McLean, G. Chazal, J.-D. Vincent, and P.-M. Lledo
Importance of newly generated neurons in the adult olfactory bulb for odor discrimination
PNAS,
February 15, 2000;
97(4):
1823 - 1828.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. P. Wagner, I. B. Black, and E. DiCicco-Bloom
Stimulation of Neonatal and Adult Brain Neurogenesis by Subcutaneous Injection of Basic Fibroblast Growth Factor
J. Neurosci.,
July 15, 1999;
19(14):
6006 - 6016.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. J. Chiasson, V. Tropepe, C. M. Morshead, and D. van der Kooy
Adult Mammalian Forebrain Ependymal and Subependymal Cells Demonstrate Proliferative Potential, but only Subependymal Cells Have Neural Stem Cell Characteristics
J. Neurosci.,
June 1, 1999;
19(11):
4462 - 4471.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. M. Daadi and S. Weiss
Generation of Tyrosine Hydroxylase-Producing Neurons from Precursors of the Embryonic and Adult Forebrain
J. Neurosci.,
June 1, 1999;
19(11):
4484 - 4497.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Gritti, P. Frolichsthal-Schoeller, R. Galli, E. A. Parati, L. Cova, S. F. Pagano, C. R. Bjornson, and A. L. Vescovi
Epidermal and Fibroblast Growth Factors Behave as Mitogenic Regulators for a Single Multipotent Stem Cell-Like Population from the Subventricular Region of the Adult Mouse Forebrain
J. Neurosci.,
May 1, 1999;
19(9):
3287 - 3297.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Shi, A. Marinovich, and B. A. Barres
Purification and Characterization of Adult Oligodendrocyte Precursor Cells from the Rat Optic Nerve
J. Neurosci.,
June 15, 1998;
18(12):
4627 - 4636.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Morshead, C. Craig, and D van der Kooy
In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain
Development,
January 6, 1998;
125(12):
2251 - 2261.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S.-i. Sakakibara and H. Okano
Expression of Neural RNA-Binding Proteins in the Postnatal CNS: Implications of Their Roles in Neuronal and Glial Cell Development
J. Neurosci.,
November 1, 1997;
17(21):
8300 - 8312.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Tropepe, C. G. Craig, C. M. Morshead, and D. van der Kooy
Transforming Growth Factor-alpha Null and Senescent Mice Show Decreased Neural Progenitor Cell Proliferation in the Forebrain Subependyma
J. Neurosci.,
October 15, 1997;
17(20):
7850 - 7859.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Kempermann, H. G. Kuhn, and F. H. Gage
Genetic influence on neurogenesis in the dentate gyrus of adult mice
PNAS,
September 16, 1997;
94(19):
10409 - 10414.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. G. Kuhn, J. Winkler, G. Kempermann, L. J. Thal, and F. H. Gage
Epidermal Growth Factor and Fibroblast Growth Factor-2 Have Different Effects on Neural Progenitors in the Adult Rat Brain
J. Neurosci.,
August 1, 1997;
17(15):
5820 - 5829.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. McKay
Stem Cells in the Central Nervous System
Science,
April 4, 1997;
276(5309):
66 - 71.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
D. Thomaidou, M. C. Mione, J. F. R. Cavanagh, and J. G. Parnavelas
Apoptosis and Its Relation to the Cell Cycle in the Developing Cerebral Cortex
J. Neurosci.,
February 1, 1997;
17(3):
1075 - 1085.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Schmidt-Kastner, H. Fliss, A. M. Hakim, and M. D. Ginsberg
Subtle Neuronal Death in Striatum After Short Forebrain Ischemia in Rats Detected by In Situ End-Labeling for DNA Damage
Stroke,
January 1, 1997;
28(1):
163 - 170.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
F. Doetsch and A. Alvarez-Buylla
Network of tangential pathways for neuronal migration in adult mammalian brain
PNAS,
December 10, 1996;
93(25):
14895 - 14900.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Weiss, C. Dunne, J. Hewson, C. Wohl, M. Wheatley, A. C. Peterson, and B. A. Reynolds
Multipotent CNS Stem Cells Are Present in the Adult Mammalian Spinal Cord and Ventricular Neuroaxis
J. Neurosci.,
December 1, 1996;
16(23):
7599 - 7609.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. B. Grinspan, M. A. Marchionni, M. Reeves, M. Coulaloglou, and S. S. Scherer
Axonal Interactions Regulate Schwann Cell Apoptosis in Developing Peripheral Nerve: Neuregulin Receptors and the Role of Neuregulins
J. Neurosci.,
October 1, 1996;
16(19):
6107 - 6118.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Redmond, S. Hockfield, and M. A. Morabito
The Divergent Homeobox Gene PBX1 Is Expressed in the Postnatal Subventricular Zone and Interneurons of the Olfactory Bulb
J. Neurosci.,
May 1, 1996;
16(9):
2972 - 2982.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. A. Goldman
Review : Neuronal Precursor Cells and Neurogenesis in the Adult Forebrain
Neuroscientist,
November 1, 1995;
1(6):
338 - 350.
[Abstract]
[PDF]
|
|
|
|
|
|
|
L. B. Thomas and D. A. Steindler
Review : Glial Boundaries and Scars: Programs for Normal Development and Wound Healing in the Brain
Neuroscientist,
May 1, 1995;
1(3):
142 - 154.
[Abstract]
[PDF]
|
|
|
|
|
|
|
C Lois and A Alvarez-Buylla
Long-distance neuronal migration in the adult mammalian brain
Science,
May 20, 1994;
264(5162):
1145 - 1148.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. Acklin and D van der Kooy
Clonal heterogeneity in the germinal zone of the developing rat telencephalon
Development,
January 5, 1993;
118(1):
175 - 192.
[Abstract]
[PDF]
|
|
|
|
|
|
|
B. Reynolds and S Weiss
Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system
Science,
March 27, 1992;
255(5052):
1707 - 1710.
[Abstract]
[PDF]
|
|
|
|
