 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, June 1, 1999, 19(11):4462-4471
Adult Mammalian Forebrain Ependymal and Subependymal Cells Demonstrate Proliferative Potential, but only Subependymal Cells Have Neural Stem Cell Characteristics
Bernard J. Chiasson, Vincent Tropepe, Cindi M. Morshead, and Derek van der Kooy Neurobiology Research Group, Department of Anatomy and Cell Biology, University of Toronto, Toronto, Canada, M5S 1A8
The adult derivatives of the embryonic forebrain germinal zones consist of two morphologically distinct cell layers surrounding the lateral ventricles: the ependyma and the subependyma. Cell cycle analyses have revealed that at least two proliferating populations exist in this region, one that is constitutively proliferating and one that is relatively quiescent and thought to include the endogenous adult neural stem cells. Earlier studies demonstrated that specific dissection of the region surrounding the lateral ventricles was necessary for the in vitro isolation of multipotent, self-renewing neural stem cells. However, in these studies, the ependymal layer was not physically separated from the subependymal layer to identify the specific adult laminar localization of the neural stem cells around the lateral ventricles. To determine which cellular compartment in the adult forebrain contained the neural stem cells, we isolated and cultured the ependyma separately from the subependyma and tested for the presence of neural stem cells using the in vitro neurosphere assay. We demonstrate that the ependymal cells can proliferate in vitro to form sphere-like structures. However, the ependymal cells generating spheres do not have the ability to self-renew (proliferate to form secondary spheres after dissociation) nor to produce neurons, but rather only seem to generate glial fibrillary acidic protein-positive ependymal cells when plated under differentiation conditions in culture. On the other hand, a subpopulation of subependymal cells do possess the self-renewing and multipotential characteristics of neural stem cells. Therefore, the adult forebrain neural stem cell resides within the subependymal compartment.
Key words: ependyma; subependyma; neural stem cells; proliferation; adult; forebrain
Copyright © 1999 Society for Neuroscience 0270-6474/99/19114462-10$05.00/0
This article has been cited by other articles:
J. Luo, B. A. Shook, S. B. Daniels, and J. C. Conover
Subventricular Zone-Mediated Ependyma Repair in the Adult Mammalian Brain
J. Neurosci., April 2, 2008; 28(14): 3804 - 3813.
[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. A. Louis, R. L. Rietze, L. Deleyrolle, R. E. Wagey, T. E. Thomas, A. C. Eaves, and B. A. Reynolds
Enumeration of Neural Stem and Progenitor Cells in the Neural Colony-Forming Cell Assay
Stem Cells, April 1, 2008; 26(4): 988 - 996.
[Abstract] [Full Text] [PDF]
V. Coskun, H. Wu, B. Blanchi, S. Tsao, K. Kim, J. Zhao, J. C. Biancotti, L. Hutnick, R. C. Krueger Jr., G. Fan, et al.
From the Cover: CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain
PNAS, January 22, 2008; 105(3): 1026 - 1031.
[Abstract] [Full Text] [PDF]
F. Balordi and G. Fishell
Mosaic Removal of Hedgehog Signaling in the Adult SVZ Reveals That the Residual Wild-Type Stem Cells Have a Limited Capacity for Self-Renewal
J. Neurosci., December 26, 2007; 27(52): 14248 - 14259.
[Abstract] [Full Text] [PDF]
L. Wang, Z. G. Zhang, S. R. Gregg, R. L. Zhang, Z. Jiao, Y. LeTourneau, X. Liu, Y. Feng, J. Gerwien, L. Torup, et al.
The Sonic Hedgehog Pathway Mediates Carbamylated Erythropoietin-enhanced Proliferation and Differentiation of Adult Neural Progenitor Cells
J. Biol. Chem., November 2, 2007; 282(44): 32462 - 32470.
[Abstract] [Full Text] [PDF]
C. F. Kim
Paving the road for lung stem cell biology: bronchioalveolar stem cells and other putative distal lung stem cells
Am J Physiol Lung Cell Mol Physiol, November 1, 2007; 293(5): L1092 - L1098.
[Abstract] [Full Text] [PDF]
C. Naujokat and T. Saric
Concise Review: Role and Function of the Ubiquitin-Proteasome System in Mammalian Stem and Progenitor Cells
Stem Cells, October 1, 2007; 25(10): 2408 - 2418.
[Abstract] [Full Text] [PDF]
C. V. Pfenninger, T. Roschupkina, F. Hertwig, D. Kottwitz, E. Englund, J. Bengzon, S. E. Jacobsen, and U. A. Nuber
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., June 15, 2007; 67(12): 5727 - 5736.
[Abstract] [Full Text] [PDF]
F. Balordi and G. Fishell
Hedgehog Signaling in the Subventricular Zone Is Required for Both the Maintenance of Stem Cells and the Migration of Newborn Neurons
J. Neurosci., May 30, 2007; 27(22): 5936 - 5947.
[Abstract] [Full Text] [PDF]
P. Karpowicz, T. Inoue, S. Runciman, B. Deveale, R. Seaberg, M. Gertsenstein, L. Byers, Y. Yamanaka, S. Tondat, J. Slevin, et al.
Adhesion Is Prerequisite, But Alone Insufficient, to Elicit Stem Cell Pluripotency
J. Neurosci., May 16, 2007; 27(20): 5437 - 5447.
[Abstract] [Full Text] [PDF]
R. Lan Zhang, Y. LeTourneau, S. R. Gregg, Y. Wang, Y. Toh, A. M. Robin, Z. Gang Zhang, and M. Chopp
Neuroblast Division during Migration toward the Ischemic Striatum: A Study of Dynamic Migratory and Proliferative Characteristics of Neuroblasts from the Subventricular Zone
J. Neurosci., March 21, 2007; 27(12): 3157 - 3162.
[Abstract] [Full Text] [PDF]
N. A. Kassem, R. Deane, M. B. Segal, and J. E. Preston
Role of transthyretin in thyroxine transfer from cerebrospinal fluid to brain and choroid plexus
Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2006; 291(5): R1310 - R1315.
[Abstract] [Full Text] [PDF]
S. Willaime-Morawek, R. M. Seaberg, C. Batista, E. Labbe, L. Attisano, J. A. Gorski, K. R. Jones, A. Kam, C. M. Morshead, and D. van der Kooy
Embryonic cortical neural stem cells migrate ventrally and persist as postnatal striatal stem cells
J. Cell Biol., October 9, 2006; 175(1): 159 - 168.
[Abstract] [Full Text] [PDF]
C. T. Jordan, M. L. Guzman, and M. Noble
Cancer stem cells.
N. Engl. J. Med., September 21, 2006; 355(12): 1253 - 1261.
[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]
M. V. Covey and S. W. Levison
Pathophysiology of Perinatal Hypoxia-Ischemia and the Prospects for Repair from Endogenous and Exogenous Stem Cells
NeoReviews, July 1, 2006; 7(7): e353 - e362.
[Full Text] [PDF]
N. Kosaka, M. Kodama, H. Sasaki, Y. Yamamoto, F. Takeshita, Y. Takahama, H. Sakamoto, T. Kato, M. Terada, and T. Ochiya
FGF-4 regulates neural progenitor cell proliferation and neuronal differentiation
FASEB J, July 1, 2006; 20(9): 1484 - 1485.
[Abstract] [Full Text] [PDF]
T. Wada, J. J. Haigh, M. Ema, S. Hitoshi, R. Chaddah, J. Rossant, A. Nagy, and D. van der Kooy
Vascular endothelial growth factor directly inhibits primitive neural stem cell survival but promotes definitive neural stem cell survival.
J. Neurosci., June 21, 2006; 26(25): 6803 - 6812.
[Abstract] [Full Text] [PDF]
R. J. Felling, M. J. Snyder, M. J. Romanko, R. P. Rothstein, A. N. Ziegler, Z. Yang, M. I. Givogri, E. R. Bongarzone, and S. W. Levison
Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia.
J. Neurosci., April 19, 2006; 26(16): 4359 - 4369.
[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]
S. Yokoo, S. Yamagami, Y. Yanagi, S. Uchida, T. Mimura, T. Usui, and S. Amano
Human Corneal Endothelial Cell Precursors Isolated by Sphere-Forming Assay
Invest. Ophthalmol. Vis. Sci., May 1, 2005; 46(5): 1626 - 1631.
[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]
N. Spassky, F. T. Merkle, N. Flames, A. D. Tramontin, J. M. Garcia-Verdugo, and A. Alvarez-Buylla
Adult Ependymal Cells Are Postmitotic and Are Derived from Radial Glial Cells during Embryogenesis
J. Neurosci., January 5, 2005; 25(1): 10 - 18.
[Abstract] [Full Text] [PDF]
A. Consiglio, A. Gritti, D. Dolcetta, A. Follenzi, C. Bordignon, F. H. Gage, A. L. Vescovi, and L. Naldini
From the Cover: Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors
PNAS, October 12, 2004; 101(41): 14835 - 14840.
[Abstract] [Full Text] [PDF]
C. S. Wong and A. J. Van der Kogel
MECHANISMS OF RADIATION INJURY TO THE CENTRAL NERVOUS SYSTEM: IMPLICATIONS FOR NEUROPROTECTION
Mol. Interv., October 1, 2004; 4(5): 273 - 284.
[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]
T. Ostenfeld and C. N. Svendsen
Requirement for Neurogenesis to Proceed through the Division of Neuronal Progenitors following Differentiation of Epidermal Growth Factor and Fibroblast Growth Factor-2-Responsive Human Neural Stem Cells
Stem Cells, September 1, 2004; 22(5): 798 - 811.
[Abstract] [Full Text] [PDF]
U. Gurok, C. Steinhoff, B. Lipkowitz, H.-H. Ropers, C. Scharff, and U. A. Nuber
Gene Expression Changes in the Course of Neural Progenitor Cell Differentiation
J. Neurosci., June 30, 2004; 24(26): 5982 - 6002.
[Abstract] [Full Text] [PDF]
L. A. Carter, J. L. MacDonald, and A. J. Roskams
Olfactory Horizontal Basal Cells Demonstrate a Conserved Multipotent Progenitor Phenotype
J. Neurosci., June 23, 2004; 24(25): 5670 - 5683.
[Abstract] [Full Text] [PDF]
G. Munoz-Elias, A. J. Marcus, T. M. Coyne, D. Woodbury, and I. B. Black
Adult Bone Marrow Stromal Cells in the Embryonic Brain: Engraftment, Migration, Differentiation, and Long-Term Survival
J. Neurosci., May 12, 2004; 24(19): 4585 - 4595.
[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]
T. Kondo, T. Setoguchi, and T. Taga
Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line
PNAS, January 20, 2004; 101(3): 781 - 786.
[Abstract] [Full Text] [PDF]
C. Gregg and S. Weiss
Generation of Functional Radial Glial Cells by Embryonic and Adult Forebrain Neural Stem Cells
J. Neurosci., December 17, 2003; 23(37): 11587 - 11601.
[Abstract] [Full Text] [PDF]
V. Prevot, A. Cornea, A. Mungenast, G. Smiley, and S. R. Ojeda
Activation of erbB-1 Signaling in Tanycytes of the Median Eminence Stimulates Transforming Growth Factor {beta}1 Release via Prostaglandin E2 Production and Induces Cell Plasticity
J. Neurosci., November 19, 2003; 23(33): 10622 - 10632.
[Abstract] [Full Text] [PDF]
J. Imitola, E. Y. Snyder, and S. J. Khoury
Genetic programs and responses of neural stem/progenitor cells during demyelination: potential insights into repair mechanisms in multiple sclerosis
Physiol Genomics, August 15, 2003; 14(3): 171 - 197.
[Abstract] [Full Text] [PDF]
P. ARLOTTA, S. S. MAGAVI, and J. D. MACKLIS
Induction of Adult Neurogenesis: Molecular Manipulation of Neural Precursors in Situ
Ann. N.Y. Acad. Sci., June 1, 2003; 991(1): 229 - 236.
[Abstract] [Full Text] [PDF]
A. D. Tramontin, J. M. Garcia-Verdugo, D. A. Lim, and A. Alvarez-Buylla
Postnatal Development of Radial Glia and the Ventricular Zone (VZ): a Continuum of the Neural Stem Cell Compartment
Cereb Cortex, June 1, 2003; 13(6): 580 - 587.
[Abstract] [Full Text] [PDF]
S. Belachew, R. Chittajallu, A. A. Aguirre, X. Yuan, M. Kirby, S. Anderson, and V. Gallo
Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons
J. Cell Biol., April 14, 2003; 161(1): 169 - 186.
[Abstract] [Full Text] [PDF]
T. Imura, H. I. Kornblum, and M. V. Sofroniew
The Predominant Neural Stem Cell Isolated from Postnatal and Adult Forebrain But Not Early Embryonic Forebrain Expresses GFAP
J. Neurosci., April 1, 2003; 23(7): 2824 - 2832.
[Abstract] [Full Text] [PDF]
Y. Arsenijevic, N. Taverney, C. Kostic, M. Tekaya, F. Riva, L. Zografos, D. Schorderet, and F. Munier
Non-neural Regions of the Adult Human Eye: A Potential Source of Neurons?
Invest. Ophthalmol. Vis. Sci., February 1, 2003; 44(2): 799 - 807.
[Abstract] [Full Text] [PDF]
C. Vicario-Abejon, M. J. Yusta-Boyo, C. Fernandez-Moreno, and F. de Pablo
Locally Born Olfactory Bulb Stem Cells Proliferate in Response to Insulin-Related Factors and Require Endogenous Insulin-Like Growth Factor-I for Differentiation into Neurons and Glia
J. Neurosci., February 1, 2003; 23(3): 895 - 906.
[Abstract] [Full Text] [PDF]
O. N. Suslov, V. G. Kukekov, T. N. Ignatova, and D. A. Steindler
Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres
PNAS, October 29, 2002; 99(22): 14506 - 14511.
[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]
R. M. Seaberg and D. van der Kooy
Adult Rodent Neurogenic Regions: The Ventricular Subependyma Contains Neural Stem Cells, But the Dentate Gyrus Contains Restricted Progenitors
J. Neurosci., March 1, 2002; 22(5): 1784 - 1793.
[Abstract] [Full Text] [PDF]
J. Evans, C. Sumners, J. Moore, M. J. Huentelman, J. Deng, C. H. Gelband, and G. Shaw
Characterization of Mitotic Neurons Derived From Adult Rat Hypothalamus and Brain Stem
J Neurophysiol, February 1, 2002; 87(2): 1076 - 1085.
[Abstract] [Full Text] [PDF]
A. Gritti, L. Bonfanti, F. Doetsch, I. Caille, A. Alvarez-Buylla, D. A. Lim, R. Galli, J. M. G. Verdugo, D. G. Herrera, and A. L. Vescovi
Multipotent Neural Stem Cells Reside into the Rostral Extension and Olfactory Bulb of Adult Rodents
J. Neurosci., January 15, 2002; 22(2): 437 - 445.
[Abstract] [Full Text] [PDF]
B. Seri, J. M. Garcia-Verdugo, B. S. McEwen, and A. Alvarez-Buylla
Astrocytes Give Rise to New Neurons in the Adult Mammalian Hippocampus
J. Neurosci., September 15, 2001; 21(18): 7153 - 7160.
[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]
S. M. Staugaitis, M. Zerlin, R. Hawkes, J. M. Levine, and J. E. Goldman
Aldolase C/Zebrin II Expression in the Neonatal Rat Forebrain Reveals Cellular Heterogeneity within the Subventricular Zone and Early Astrocyte Differentiation
J. Neurosci., August 15, 2001; 21(16): 6195 - 6205.
[Abstract] [Full Text] [PDF]
P. Crisanti, B. Omri, E. J. Hughes, G. Meduri, C. Hery, E. Clauser, C. Jacquemin, and B. Saunier
The Expression of Thyrotropin Receptor in the Brain
Endocrinology, February 1, 2001; 142(2): 812 - 822.
[Abstract] [Full Text] [PDF]
N. Uchida, D. W. Buck, D. He, M. J. Reitsma, M. Masek, T. V. Phan, A. S. Tsukamoto, F. H. Gage, and I. L. Weissman
Direct isolation of human central nervous system stem cells
PNAS, December 19, 2000; 97(26): 14720 - 14725.
[Abstract] [Full Text] [PDF]
E. D. Laywell, P. Rakic, V. G. Kukekov, E. C. Holland, and D. A. Steindler
Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain
PNAS, November 22, 2000; (2000) 250471697.
[Abstract] [Full Text]
P. J. Horner, A. E. Power, G. Kempermann, H. G. Kuhn, T. D. Palmer, J. Winkler, L. J. Thal, and F. H. Gage
Proliferation and Differentiation of Progenitor Cells Throughout the Intact Adult Rat Spinal Cord
J. Neurosci., March 15, 2000; 20(6): 2218 - 2228.
[Abstract] [Full Text] [PDF]
F. H. Gage
Mammalian Neural Stem Cells
Science, February 25, 2000; 287(5457): 1433 - 1438.
[Abstract] [Full Text]
T. Ohtsuka, M. Sakamoto, F. Guillemot, and R. Kageyama
Roles of the Basic Helix-Loop-Helix Genes Hes1 and Hes5 in Expansion of Neural Stem Cells of the Developing Brain
J. Biol. Chem., August 3, 2001; 276(32): 30467 - 30474.
[Abstract] [Full Text] [PDF]
E. D. Laywell, P. Rakic, V. G. Kukekov, E. C. Holland, and D. A. Steindler
Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain
PNAS, December 5, 2000; 97(25): 13883 - 13888.
[Abstract] [Full Text] [PDF]
|
|
|