The adult rat hippocampus contains primordial neural stem cells

Molecular and Cellular Neurosciences

Volumn 8, Issue 6, 1997, Pages 389-404

  Palmer, Theo D ^a   Takahashi, Jun ^a   Gage, Fred H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; CYCLIC AMP; NEUROTROPHIC FACTOR; RETINOIC ACID;

ANIMAL CELL; ARTICLE; CELL CLONE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; HIPPOCAMPUS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; STEM CELL;

ANIMALIA;

EID: 0030438734     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1996.0595     Document Type: Article

References (92)

1. Adam M. A., Ramesh N., Miller A. D., Osborne W. R. Internal initiation of translation in retroviral vectors carrying picornavirus 5′ nontranslated regions. J. Virol. 65:1991;4985-4990.
2. Altman J., Das G. D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124:1965;319-335.
3. Altman J., Das G. D. Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 126:1966;337-389.
4. Anderson K. D., Alderson R. F., Altar C. A., DiStefano P. S., Corcoran T. L., Lindsay R. M., Wiegand S. J. Differential distribution of exogenous BDNF, NGF, and NT-3 in the brain corresponds to the relative abundance and distribution of high-affinity and low-affinity neurotrophin receptors. J. Comp. Neurol. 357:1995;296-317.
5. Barde Y. A. The nerve growth factor family. Prog. Growth Factor. Res. 2:1990;237-248.
6. Bayer S. A. Changes in the total number of dentate granule cells in juvenile and adult rats: A correlated volumetric and 3H-thymidine autoradiographic study. Exp. Brain Res. 46:1982;315-323.
7. Bender M. A., Palmer T. D., Gelinas R. E., Miller A. D. Evidence that the packaging signal of Moloney murine leukemia virus extends into the gag region. J. Virol. 61:1987;1639-1646.
8. Black M. M., Kurdyla J. T. Microtubule-associated proteins of neurons. J. Cell Biol. 97:1983;1020-1028.
9. Blottner D., Bruggemann W., Unsicker K. Ciliary neurotrophic factor supports target-deprived preganglionic sympathetic spinal cord neurons. Neurosci. Lett. 105:1989;316-320.
10. Bonham L., Palmer T. D., Miller A. D. Prolonged expression of therapeutic levels of human granulocyte colony-stimulating factor in rats following gene transfer to skeletal muscle. Human Gene Therapy. 7:1996;1423-1429.
11. Cepko C. Retrovirus vectors and their applications in neurobiology. Neuron. 1:1988;345-353.
12. Collazo D., Takahashi H., McKay R. D. Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron. 9:1992;643-656.
13. Cooper D. M., Mons N., Karpen J. W. Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature. 374:1995;421-424.
14. Davis A. A., Temple S. A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature. 372:1994;263-266.
15. DeChiara T. M., Vejsada R., Poueymirou W. T., Acheson A., Suri C., Conover J. C., Friedman B., McClain J., Pan L., Stahl N. Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth. Cell. 83:1995;313-322.
16. DeHamer M. K., Guevara J. L., Hannon K., Olwin B. B., Calof A. L. Genesis of olfactory receptor neuronsin vitro: Neuron. 13:1994;1083-1097.
17. Drago J., Murphy M., Carroll S. M., Harvey R. P., Bartlett P. F. Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc. Natl. Acad. Sci. USA. 88:1991;2199-2203.
18. Eisenbarth G. S., Walsh F. S., Nirenberg M. Monoclonal antibody to a plasma membrane antigen of neurons. Proc. Natl. Acad. Sci. USA. 76:1979;4913-4917.
19. Friedrich P., Aszodi A. MAP2: A sensitive cross-linker and adjustable spacer in dendritic architecture. FEBS Lett. 295:1991;5-9.
20. 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.
21. Goldman J. E. Lineage, migration, and fate determination of postnatal subventricular zone cells in the mammalian CNS. J. Neurooncol. 24:1995;61-64.
22. 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. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci. 16:1996;1091-1100.
23. Hart I. K., Richardson W. D., Heldin C. H., Westermark B., Raff M. C. PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O-2A) cell lineage. Development. 105:1989;595-603.
24. Hayashi M., Patel A. J. An interaction between thyroid hormone and nerve growth factor in the regulation of choline acetyltransferase activity in neuronal cultures, derived from the septal-diagonal band region of the embryonic rat brain. Brain Res. 433:1987;109-120.
25. Hefti F. Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J. Neurosci. 6:1986;2155-2162.
26. Herman M. A., Schulz C. A., Claude P. Responses to cAMP depend on stage of neuronal differentiation of NGF-treated adrenal chromaffin cells. Dev. Biol. 161:1994;477-489.
27. Heumann R. Neurotrophin signalling. Curr. Opin. Neurobiol. 4:1994;668-679.
28. Hunter S. F., Bottenstein J. E. Bipotential glial progenitors are targets of neuronal cell line-derived growth factors. Brain Res. Dev. Brain Res. 49:1989;33-49.
29. Ip N. Y., Li Y., Yancopoulos G. D., Lindsay R. M. Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J. Neurosci. 13:1993;3394-3405.
30. Iwanaga T., Takahashi Y., Fujita T. Immunohistochemistry of neuron-specific and glia-specific proteins. Arch. Histol. Cytol. 52:1989;13-24.
31. Jelsma T. N., Aguayo A. J. Trophic factors. Curr. Opin. Neurobiol. 4:1994;717-725.
32. Kaplan M. S., Bell D. H. Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J. Neurosci. 4:1984;1429-1441.
33. Kerler R., Rabes H. M. Rat tumor cytogenetics: a critical evaluation of the literature. Crit. Rev. Oncog. 5:1994;271-295.
34. Kilpatrick T. J., Bartlett P. F. Cloning and growth of multipotential neural precursors: Requirements for proliferation and differentiation. Neuron. 10:1993;255-265.
35. 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;3653-3661.
36. Kosik K. S. The molecular and cellular biology of tau. Brain Pathol. 3:1993;39-43.
37. Kromer L. F. Nerve growth factor treatment after brain injury prevents neuronal death. Science. 235:1987;214-216.
38. Kuhn H. G., 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.
39. Le Douarin N. M. Embryonic neural chimaeras in the study of brain development. Trends. Neurosci. 16:1993;64-72.
40. Le Douarin N., Dieterlen-Lievre F., Teillet M. A. Quail-chick transplantations. Methods Cell Biol. 51:1996;23-59.
41. Lee M. K., Rebhun L. I., Frankfurter A. Posttranslational modification of class III beta-tubulin. Proc. Natl. Acad. Sci. USA. 87:1990;7195-7199.
42. Lee M. K., Cleveland D. W. Neurofilament function and dysfunction: involvement in axonal growth and neuronal disease. Curr. Opin. Cell Biol. 6:1994;34-40.
43. Lefkowitz R. J. G protein-coupled receptor kinases. Cell. 74:1993;409-412.
44. Legrand J. Thyroid hormone effects on growth and development. Thyroid Hormone Metabolism. 1986;Dekker, New York. p. 503-534.
45. Lendahl U., Zimmerman L. B., McKay R. D. CNS stem cells express a new class of intermediate filament protein. Cell. 60:1990;585-595.
46. 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.
47. Lois C., Garcia-Verdugo J. M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science. 271:1996;978-981.
48. Luskin M. B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron. 11:1993;173-189.
49. Magal E., Burnham P., Varon S. Effect of CNTF on low-affinity NGF receptor expression by cultured neurons from different rat brain regions. J. Neurosci. Res. 30:1991;560-566.
50. Maisonpierre P. C., Belluscio L., Friedman B., Alderson R. F., Wiegand S. J., Furth M. E., Lindsay R. M., Yancopoulos G. D. NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron. 5:1990;501-509.
51. Mandelkow E. M., Schweers O., Drewes G., Biernat J., Gustke N., Trinczek B., Mandelkow E. Structure, microtubule interactions, and phosphorylation of tau protein. Ann. N. Y. Acad. Sci. 777:1996;96-106.
52. Martens G. J. Molecular biology of G-protein-coupled receptors. Prog. Brain Res. 92:1992;201-214.
53. McConnell S. K. Plasticity and commitment in the developing cerebral cortex. Prog. Brain Res. 105:1995;129-143.
54. McEwen B. S. Steroid hormones: effect on brain development and function. Horm. Res. 37:1992;1-10.
55. Miller A. D., Buttimore C. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol. Cell Biol. 6:1986;2895-2902.
56. Miller A. D., Rosman G. J. Improved retroviral vectors for gene transfer and expression. Biotechniques. 7:1989.
57. Miller D. G., Adam M. A., Miller A. D. Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol. Cell Biol. 10:1990;4239-4242.
58. Miller R. H., Ffrench-Constant C., Raff M. C. The macroglial cells of the rat optic nerve. Annu. Rev. Neurosci. 12:1989;517-534.
59. Morrison R. S. Generation of primary astroglial and neuronal cultures from neonatal rat brain. Shahar A., deVellis J., Vernadakis A., Haber B. A Dissection and Tissue Culture Manual of the Nervous System. 1989;187-192 Wiley-Liss, New York.
60. Morriss-Kay G., Wood H., Chen W. H. Normal neurulation in mammals. Ciba. Found. Symp. 181:1994;51-63.
61. Morshead C. M., Reynolds B. A., Craig C. G., McBurney M. W., Staines W. A., Morassutti D., 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.
62. Mullen R. J., Buck C. R., Smith A. M. NeuN, a neuronal specific nuclear protein in vertebrates. Development. 116:1992;201-211.
63. Munoz A., Wrighton C., Seliger B., Bernal J., Beug H. Thyroid hormone receptor/c-erbA: Control of commitment and differentiation in the neuronal/chromaffin progenitor line PC12. J. Cell Biol. 121:1993;423-438.
64. Murphy M., Drago J., Bartlett P. F. Fibroblast growth factor stimulates the proliferation and differentiation of neural precursor cellsin vitro. J. Neurosci. Res. 25:1990;463-475.
65. Noble M., Wolswijk G., Wren D. The complex relationship between cell division and the control of differentiation in oligodendrocyte-type-2 astrocyte progenitor cells isolated from perinatal and adult rat optic nerves. Prog. Growth Factor. Res. 1:1989;179-194.
66. Noble M., Gutowski N., Bevan K., Engel U., Linskey M., Urenjak J., Bhakoo K., Williams S. From rodent glial precursor cell to human glial neoplasia in the oligodendrocyte-type-2 astrocyte lineage. Glia. 15:1995;222-230.
67. Palmer T. D., Ray J., Gage F. H. FGF-2-Responsive Neuronal Progenitors Reside in Proliferative and Quiescent Regions of the Adult Rodent Brain. Mol. Cell Neurosci. 6:1995;474-486.
68. Price J., Turner D., Cepko C. Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc. Natl. Acad. Sci. USA. 84:1987;156-160.
69. Raff M. C., Mirsky R., Fields K. L., Lisak R. P., Dorfman S. H., Silberberg D. H., Gregson N. A., Leibowitz S., Kennedy M. C. Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture. Nature. 274:1978;813-816.
70. Ranscht B., Clapshaw P. A., Price J., Noble M., Seifert W. Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc. Natl. Acad. Sci. USA. 79:1982;2709-2713.
71. Ray J., Peterson D. A., Schinstine M., Gage F. H. Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc. Natl. Acad. Sci. USA. 90:1993;3602-3606.
72. Reynolds B. A., Tetzlaff W., Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12:1992;4565-4574.
73. Reynolds B. A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system [see comments]. Science. 255:1992;1707-1710.
74. 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.
75. 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.
76. Satoh J., Tabira T., Kim S. U. Rapidly proliferating glial cells isolated from adult mouse brain have a differentiative capacity in response to cyclic AMP. Neurosci. Res. 20:1994;175-184.
77. Sendtner M., Kreutzberg G. W., Thoenen H. Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature. 345:1990;440-441.
78. Shah N. M., Marchionni M. A., Isaacs I., Stroobant P., Anderson D. J. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell. 77:1994;349-360.
79. Sommer I., Schachner M. Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: An immunocytological study in the central nervous system. Dev. Biol. 83:1981;311-327.
80. Sommer I., Schachner M. Cell that are O4 antigen-positive and O1 antigen-negative differentiate into O1 antigen-positive oligodendrocytes. Neurosci. Lett. 29:1982;183-188.
81. Stanfield B. B., Trice J. E. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp. Brain Res. 72:1988;399-406.
82. Stemple D. L., Anderson D. J. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell. 71:1992;973-985.
83. Sucov H. M., Evans R. M. Retinoic acid and retinoic acid receptors in development. Mol. Neurobiol. 10:1995;169-184.
84. Suzumura A., Silberberg D. H. Lymphokines facilitate maturation of oligodendrocytesin vitro. Brain Res. 480:1989;51-57.
85. Temple S. Division and differentiation of isolated CNS blast cells in microculture. Nature. 340:1989;471-473.
86. 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.
87. Vicario-Abejon C., Johe K. K., Hazel T. G., Collazo D., McKay R. D. Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron. 15:1995;105-114.
88. Williams B. P., Read J., Price J. The generation of neurons and oligodendrocytes from a common precursor cell. Neuron. 7:1991;685-693.
89. Williams L. R., Varon S., Peterson G. M., Wictorin K., Fischer W., Bjorklund A., Gage F. H. Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc. Natl. Acad. Sci. USA. 83:1986;9231-9235.
90. Wolswijk G., Noble M. Identification of an adult-specific glial progenitor cell. Development. 105:1989;387-400.
91. Wolswijk G., Noble M. Cooperation between PDGF and FGF converts slowly dividing O-2A adult progenitor cells to rapidly dividing cells with characteristics of O-2Aperinatal progenitor cells. J. Cell Biol. 118:1992;889-900.
92. Yosida T. H. Karyotype evolution and tumor development. Cancer Genet. Cytogenet. 8:1983;153-179.