Mitogen and substrate differentially affect the lineage restriction of adult rat subventricular zone neural precursor cell populations

Experimental Cell Research

Volumn 252, Issue 1, 1999, Pages 75-95

  Whittemore, Scott R ^a,b   Morassutti, Dante J ^b   Walters, Winston M ^a   Liu, Rong Huan ^b   Magnuson, David S K ^b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBRONECTIN; HEPARIN; LAMININ; MITOGENIC AGENT;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; STEM CELL;

EID: 0033544008     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4621     Document Type: Article

References (61)

1. Bayer S. A., Altman J., Russo R. J., Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. NeuroToxicology. 14:1993;83-144.
2. Kaplan M. S., Hinds J. W. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science. 197:1977;1092-1094.
3. Bayer S. A., Yakel S. W., Puri P. S. Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science. 216:1982;890-892.
4. Kuhn H. J., Dickinson-Anson H., Gage F. H. Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16:1996;2027-2033.
5. Lewis P. D. A quantitative study of cell proliferation in the subependymal layer of the adult rat brain. Exp. Neurol. 20:1968;203-207.
6. Lois C., Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. USA. 90:1993;2074-2077.
7. Morshead C. M., Reynolds B. R., Craig C. G., McBurney M. W., Staines W. A., Morassutti D. J., Weiss S., van der Kooy D. Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron. 13:1994;1071-1082.
8. Levison S. W., Goldman J. E. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron. 10:1993;201-212.
9. Menezes J. R., Smith C. M., Nelson K. C., Luskin M. B. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell. Neurosci. 6:1995;496-508.
10. Cameron H. A., Woolley C. S., McEwen B. S., Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience. 56:1993;337-344.
11. Reynolds B. A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 255:1992;1707-1710.
12. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A. C., Reynolds B. A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16:1996;7599-7609.
13. Gritti A., Parati E. A., Cova L., Frolichsthal P., Galli R., Wanke E., Faravelli L., Morassutti D. J., Roisen F., Nickel D. D., Vescovi A. L. Multipotent stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci. 16:1996;1091-1100.
14. Richards L. J., Kilpatrick T. J., Bartlett P. F. De novo generation of neuronal cells from the adult mouse brain. Proc. Natl. Acad. Sci. USA. 89:1992;8591-8595.
15. Johe K. K., Hazel T. G., Muller T., Dugich-Djordjevic M. M., McKay R. D. G. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10:1996;3129-3140.
16. Gage F. H., Coates P. W., Palmer T. D., Kuhn H. G., Fisher L. J., Suhonen J. O., Peterson D. A., Suhr S. T., Ray J. Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl. Acad. Sci. USA. 92:1995;11879-11883.
17. Palmer T. D., Takahashi J., Gage F. H. The adult rat hippocampus contains primordial neural stem cells. Mol. Cell. Neurosci. 8:1997;389-404.
18. Suhonen J. O., Peterson D. A., Ray J., Gage F. H. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature. 383:1996;624-627.
19. Hockfield S., McKay R. D. G. Identification of major cell classes in the developing mammalian nervous system. J. Neurosci. 5:1985;3310-3328.
20. Shihabuddin L. S., Ray J., Gage F. H. FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp. Neurol. 148:1997;577-586.
21. Kilpatrick T. J., Bartlett P. F. Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J. Neurosci. 15:1995;3563-3661.
22. Craig C. G., Tropepe V., Morshead C. M., Reynolds B. A., Weiss S., van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16:1996;2649-2658.
23. Kuhn H. G., Winkler J., Kempermann G., Thal L. J., Gage F. H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17:1997;5820-5829.
24. Svendsen C. N., Skepper J., Rosser A. E., ter Borg M. G., Tyres P., Ryken T. Restricted growth potential of rat neural precursors as compared to mouse. Dev. Brain Res. 99:1997;253-258.
25. Vescovi A. L., Reynolds B. A., Fraser D. D., Weiss S. bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron. 11:1993;951-966.
26. Reynolds B. A., Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175:1996;1-13.
27. Flax J. D., Aurora S., Yang C., Simonin C., Wills A. M., Billinghurst L. L., Jendoubi M., Sidman R. L., Wolfe J. H., Kim S. U., Snyder E. Y. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nature Biotechnol. 16:1998;1033-1039.
28. Gage F. H., Ray J., Fisher L. J. Isolation, characterization, and use of stem cells from the CNS. Ann. Rev. Neurosci. 18:1995;159-192.
29. McKay R. Stem cells in the central nervous system. Science. 276:1997;66-71.
30. Weiss S., Reynolds B. A., Vescovi A. L., Morshead C., Craig C. G., van der Kooy D. Is there a neural stem cell in the mammalian forebrain. Trends Neurosci. 19:1996;387-393.
31. Whittemore S. R., Snyder E. Y. The physiological relevance and functional potential of central nervous system-derived cell lines. Mol. Neurobiol. 12:1996;13-38.
32. Svendsen C. N., Clarke D. J., Rosser A. E., Dunnett S. B. Survival and differentiation of rat and human epidermal growth factor-responsive precursor cells following grafting into the lesioned adult central nervous system. Exp. Neurol. 137:1996;376-388.
33. Kilpatrick T. J., Cheema S. S., Koblar S. A., Tan S.-S., Bartlett P. F. The engraftment of transplanted primary neuroepithelial cells within the postnatal mouse brain. Neurosci. Lett. 181:1994;129-133.
34. Sabate O., Horellou P., Vigne E., Colin P., Perricaudet M., Buc-Caron M.-H., Mallet J. Transplantation to the rat brain of human neural progenitors that were genetically modified using adenoviruses. Nature Genet. 9:1995;256-260.
35. Studer L., Tabar V., McKay R. D. G. Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats. Nature Neurosci. 1:1998;290-295.
36. Brustle O., Choudhary K., Karram K., Huttner A., Murray K., Dubois-Dalcq M., McKay R. D. G. Chimeric brains generated by intraventricular transplantation of fetal human brain cells into embryonic rats. Nature Biotechnol. 16:1998;1041-1044.
37. Sweetnam P. M., Sanon H. R., White L. A., Brass B. J., Jaye M., Whittemore S. R. Differential effects of acidic and basic fibroblast growth factors on spinal cord cholinergic, GABAergic, and glutamatergic neurons. J. Neurochem. 57:1991;237-249.
38. Kahn M. A., Huang C. J., Caruso A., Barresi V., Nazarian R., Condorelli D. F., de Vellis J. Ciliary neurotrophic factor activates JAK/Stat signal transduction cascade and induces transcriptional expression of glial fibrillary acidic protein in glial cells. J. Neurochem. 68:1997;1413-1423.
39. Rajan P., Symes A. J., Fink J. S. STAT proteins are activated by ciliary neurotrophic factor in cells of central nervous system origin. J. Neurosci. Res. 43:1996;403-411.
40. Rajan P., McKay R. D. G. Multiple routes to astrocytic differentiation in the CNS. J. Neurosci. 18:1998;3620-3629.
41. Bonni A., Sun Y., Nadal-Vicens M., Bhatt A., Frank D. A., Rozovsky I., Stahl N., Yancopoulos G. D., Greenberg M. E. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science. 278:1997;477-483.
42. Gross R. E., Mehler M. F., Mabie P. C., Zang Z., Santschi L., Kessler J. A. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron. 17:1996;595-606.
43. Baas D., Bourbeau D., Sarlieve L. L., Ittel M. E., Dussault J. H., Puymirat J. Oligodendrocyte maturation and progenitor cell proliferation are independently regulated by thyroid hormone. Glia. 19:1997;324-332.
44. Murray K., Dubois-Dalcq M. Emergence of oligodendrocytes from human neural spheres. J. Neurosci. Res. 50:1997;146-156.
45. + precursors of the postnatal brain. J. Neurosci. 18:1998;5777-5788.
46. Walter I. B. Triiodothyronine exerts a trophic action on rat sensory neuron survival and neurite outgrowth through different pathways. Eur. J. Neurosci. 8:1996;455-466.
47. Lindholm D., Castren E., Tsoulfas P., Kolbeck R., Berzaghi M. d. P., Leingartner A., Heisenberg C. P., Tesarollo L., Parada L. F., Thoenen H. Neurotrophin-3 induced by tri-iodothyronine in cerebellar granule cells promotes Purkinje cell differentiation. J. Cell Biol. 122:1993;443-450.
48. Heisenberg C. P., Thoenen H., Lindholm D. Tri-iodothyronine regulates survival and differentiation of rat cerebellar granule neurons. Neuroreport. 3:1992;685-688.
49. Jorgensen O. S., Honegger P. Development of neuronal markers in aggregating fetal rat telencephalon cells cultured in the presence of triiodothyronine. Int. J. Dev. Neurosci. 4:1986;519-524.
50. Williams B. P., Park J. K., Alberta J. A., Muhlebach S. G., Hwang G. Y., Roberts T. M., Stiles C. D. A PDGF-regulated immediate early gene response initiates neuronal differentiation in ventricular zone progenitor cells. Neuron. 18:1997;553-562.
51. Heasley L. E., Johnson G. L. The beta-PDGF receptor induces neuronal differentiation of PC12 cells. Mol. Biol. Cell. 3:1992;545-553.
52. Ahmed S., Reynolds B. A., Weiss S. BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J. Neurosci. 15:1995;5765-5778.
53. Arsenijevic Y., Weiss S. 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. 18:1998;2118-2128.
54. Kirschenbaum B., Goldman S. A. Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc. Natl. Acad. Sci. USA. 92:1995;210-214.
55. Shetty A. K., Turner D. A. In vitro survival and differentiation of neurons derived from epidermal growth factor-responsive postnatal hippocampal stem cells: Inducing effects of brain-derived neurotrophic factor. J. Neurobiol. 35:1998;395-425.
56. Artavanis-Tsakonas S., Matsuno K., Fortini M. E. Notch signalling. Science. 268:1995;225-232.
57. Snyder E. Y., Deitcher D. L., Walsh C., Arnold-Aldea S., Hartwieg E. A., Cepko C. L. Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell. 66:1992;33-51.
58. Renfranz P. J., Cunningham M. G., McKay R. D. G. Region-specific differentiation of the hippocampal stem cell line HiB5 upon implantation into the developing mammalian brain. Cell. 66:1991;713-729.
59. Onifer S. M., Whittemore S. R., Holets V. R. Variable morphological differentiation of a raphe-derived neuronal cell line following transplantation into the adult rat CNS. Exp. Neurol. 122:1993;130-142.
60. Shihabuddin L. S., Hertz J. A., Holets V. R., Whittemore S. R. The adult CNS retains the potential to direct region-specific differentiation of a transplanted neuronal precursor cell line. J. Neurosci. 15:1995;6666-6678.
61. Shihabuddin L. S., Brunschwig J.-P., Holets V. R., Bunge M. B., Whittemore S. R. Induction of mature neuronal properties in immortalized neuronal precursor cells following grafting into the neonatal CNS. J. Neurocytol. 25:1996;101-111.