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Journal of Neuroscience, Vol 16, 1091-1100, Copyright © 1996 by Society for Neuroscience

ARTICLE

Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor

A Gritti, EA Parati, L Cova, P Frolichsthal, R Galli, E Wanke, L Faravelli, DJ Morassutti, F Roisen, DD Nickel and AL Vescovi
Laboratory of Cellular Neuropharmacology, National Neurological Institute C, Milan, Italy.

It has been established that the adult mouse forebrain contains multipotential (neuronal/glial) progenitor cells that can be induced to proliferate in vitro when epidermal growth factor is provided. These cells are found within the subventricular zone of the lateral ventricles, together with other progenitor cell populations, whose requirements for proliferation remain undefined. Using basic fibroblast growth factor (bFGF), we have isolated multipotential progenitors from adult mouse striatum. These progenitors proliferate and can differentiate into cells displaying the antigenic properties of astrocytes, oligodendrocytes, and neurons. The neuron-like cells possess neuronal features, exhibit neuronal electrophysiological properties, and are immunoreactive for GABA, substance P, choline acetyl-transferase, and glutamate. Clonal analysis confirmed the multipotency of these bFGF-dependent cells. Most significantly, subcloning experiments demonstrated that they were capable of self- renewal, which led to a progressive increase in population size over serial passaging. These results demonstrate that bFGF is mitogenic for multipotential cells from adult mammalian forebrain that possess stem cell properties.


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V. T. Chu and F. H. Gage
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PNAS, July 3, 2001; 98(14): 7652 - 7653.
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L. S. Shihabuddin, P. J. Horner, J. Ray, and F. H. Gage
Adult Spinal Cord Stem Cells Generate Neurons after Transplantation in the Adult Dentate Gyrus
J. Neurosci., December 1, 2000; 20(23): 8727 - 8735.
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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.
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Science, February 25, 2000; 287(5457): 1433 - 1438.
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D. J. Martens, V. Tropepe, and D. van der Kooy
Separate Proliferation Kinetics of Fibroblast Growth Factor-Responsive and Epidermal Growth Factor-Responsive Neural Stem Cells within the Embryonic Forebrain Germinal Zone
J. Neurosci., February 1, 2000; 20(3): 1085 - 1095.
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M. Zappone, R Galli, R Catena, N Meani, S De Biasi, E Mattei, C Tiveron, A. Vescovi, R Lovell-Badge, S Ottolenghi, et al.
Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells
Development, January 6, 2000; 127(11): 2367 - 2382.
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J Xu, Z Liu, and D. Ornitz
Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures
Development, January 5, 2000; 127(9): 1833 - 1843.
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H. Harada, P. Kettunen, H.-S. Jung, T. Mustonen, Y. A. Wang, and I. Thesleff
Localization of Putative Stem Cells in Dental Epithelium and Their Association with Notch and Fgf Signaling
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G. C. Kopen, D. J. Prockop, and D. G. Phinney
Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains
PNAS, September 14, 1999; 96(19): 10711 - 10716.
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P. C. Mabie, M. F. Mehler, and J. A. Kessler
Multiple Roles of Bone Morphogenetic Protein Signaling in the Regulation of Cortical Cell Number and Phenotype
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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.
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C. E. Johanson, J. Szmydynger-Chodobska, A. Chodobski, A. Baird, P. McMillan, and E. G. Stopa
Altered formation and bulk absorption of cerebrospinal fluid in FGF-2-induced hydrocephalus
Am J Physiol Regulatory Integrative Comp Physiol, July 1, 1999; 277(1): R263 - R271.
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D. A. Lim and A. Alvarez-Buylla
Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis
PNAS, June 22, 1999; 96(13): 7526 - 7531.
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B. D. Yandava, L. L. Billinghurst, and E. Y. Snyder
"Global" cell replacement is feasible via neural stem cell transplantation: Evidence from the dysmyelinated shiverer mouse brain
PNAS, June 8, 1999; 96(12): 7029 - 7034.
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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.
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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.
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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.
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B. Kirschenbaum, F. Doetsch, C. Lois, and A. Alvarez-Buylla
Adult Subventricular Zone Neuronal Precursors Continue to Proliferate and Migrate in the Absence of the Olfactory Bulb
J. Neurosci., March 15, 1999; 19(6): 2171 - 2180.
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C. R. Bjornson, R. L. Rietze, B. A. Reynolds, M. C. Magli, and A. L. Vescovi
Turning Brain into Blood: A Hematopoietic Fate Adopted by Adult Neural Stem Cells in Vivo
Science, January 22, 1999; 283(5401): 534 - 537.
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K Sakurada, M Ohshima-Sakurada, T. Palmer, and F. Gage
Nurr1, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain
Development, January 9, 1999; 126(18): 4017 - 4026.
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E. Y. Snyder
Review : Neural Stem-Like Cells: Developmental Lessons with Therapeutic Potential
Neuroscientist, November 1, 1998; 4(6): 408 - 425.
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W. Li, C. A. Cogswell, and J. J. LoTurco
Neuronal Differentiation of Precursors in the Neocortical Ventricular Zone Is Triggered by BMP
J. Neurosci., November 1, 1998; 18(21): 8853 - 8862.
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F. Ciccolini and C. N. Svendsen
Fibroblast Growth Factor 2 (FGF-2) Promotes Acquisition of Epidermal Growth Factor (EGF) Responsiveness in Mouse Striatal Precursor Cells: Identification of Neural Precursors Responding to both EGF and FGF-2
J. Neurosci., October 1, 1998; 18(19): 7869 - 7880.
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T. Ben-Hur, B. Rogister, K. Murray, G. Rougon, and M. Dubois-Dalcq
Growth and Fate of PSA-NCAM+ Precursors of the Postnatal Brain
J. Neurosci., August 1, 1998; 18(15): 5777 - 5788.
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L. Calza, L. Giardino, M. Pozza, C. Bettelli, A. Micera, and L. Aloe
Proliferation and phenotype regulation in the subventricular zone during experimental allergic encephalomyelitis: In vivo evidence of a role for nerve growth factor
PNAS, March 17, 1998; 95(6): 3209 - 3214.
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Y. Arsenijevic and S. Weiss
Insulin-Like Growth Factor-I Is a Differentiation Factor for Postmitotic CNS Stem Cell-Derived Neuronal Precursors: Distinct Actions from Those of Brain-Derived Neurotrophic Factor
J. Neurosci., March 15, 1998; 18(6): 2118 - 2128.
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R Josephson, T Muller, J Pickel, S Okabe, K Reynolds, P. Turner, A Zimmer, and R. McKay
POU transcription factors control expression of CNS stem cell-specific genes
Development, January 8, 1998; 125(16): 3087 - 3100.
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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.
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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.
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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.
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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.
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F. Doetsch, J. M. Garcia-Verdugo, and A. Alvarez-Buylla
Cellular Composition and Three-Dimensional Organization of the Subventricular Germinal Zone in the Adult Mammalian Brain
J. Neurosci., July 1, 1997; 17(13): 5046 - 5061.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J. Ray, A. Baird, and F. H. Gage
A 10-amino acid sequence of fibroblast growth factor 2 is sufficient for its mitogenic activity on neural progenitor cells
PNAS, June 24, 1997; 94(13): 7047 - 7052.
[Abstract] [Full Text] [PDF]


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