Neural stem cells in the developing central nervous system: Implications for cell therapy through transplantation

Progress in Brain Research

Volumn 127, Issue , 2000, Pages 13-34

  Svendsen, C N ^a   Caldwell, M A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ASTROCYTE; BRAIN REGION; CELL DIFFERENTIATION; CELL GROWTH; CENTRAL NERVOUS SYSTEM; CULTURE MEDIUM; FUTUROLOGY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL;

EID: 0034589749     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(00)27003-9     Document Type: Article

References (96)

1. Ahmed, S., Reynolds, B.A. and Weiss, S. (1995) BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J. Neurosci., 15: 5765-5778.
2. Alvarez-Buylla, A., Herrera, D.G. and Wichterle, H. (2000) The subventricular zone: Source of neuronal precursors for brain repair. In: S.B. Dunnett and A. Björklund (Eds.), Functional Neural Transplantation II. Novel Cell Therapies for CNS Disorders. Progress in Brain Research, Vol. 127, Elsevier, Amsterdam, pp. 1-11, this volume.
3. Alvarez-Buylla, A. and Temple, S. (1998) Stem cells in the developing and adult nervous system. J. Neurobiol., 36: 105-110.
4. Armstrong, R.J.E. and Svendsen, C.N. (2000a) Neural stem cell: From cell biology to cell replacement. Cell Transplant., 9: 139-52
5. Armstrong, R.J.E., Watts, C., Dunnett, S.B., Svendsen, C.N. and Rosser, A.E. (2000b) Survival, neuronal differentiation and fibre outgrowth of propagated human neural precursor grafts in an animal model of Huntington's disease. J. Cell Transplant., 9: 55-64.
6. Arsenijevic, Y. and Weiss, S. (1998) 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: 2118-2128.
7. Bain, G., Kitchens, D., Yao, M., Huettner, J.E. and Gottlieb, D.I. (1995) Embryonic stem cells express neural properties in vitro. Dev. Biol., 168: 342-357.
8. Bjornson, C.R., Rietze, R.L., Reynolds, B.A., Magli, M.C. and Vescovi, A.L. (1999) Turning brain into blood: A hematopoietic fate adopted by adult neural stem cells in vivo. Science, 283: 534-537.
9. Bodnar, A.G., Ouellette, M., Frolkis, M., Holt, S.E., Chiu, C., Morin, G.B., Harley, C.B., Shay, J.W., Lichtsteiner, S. and Wright, W.E. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science, 279: 349-352.
10. Bouvier, M.M. and Mytilineou, C. (1995) Basic fibroblast growth factor increases division and delays differentiation of dopamine precursors in vitro. J. Neurosci., 15: 7141-7149.
11. Brustle, O., Spiro, A.C., Karram, K., Choudhary, K., Okabe, S. and McKay, R.D.G. (1997) In vitro-generated neural precursors participate in mammalian brain development. Proc. Natl. Acad. Sci. USA, 94: 14809-14814.
12. Brustle, O., Choudhary, K., Karram, K., Huttner, A., Murray, K., Dubois-Dalcq, M. and McKay, R.D.G. (1998) Chimeric brains generated by intraventricular transplantation of fetal human brain cells into embryonic rats. Nat. Biotechnol., 16: 1040-1044.
13. Brustle, O., Jones, K.N., Learish, R.D., Karram, K., Choudhary, K., Wiestler, O.D., Duncan, I.D. and McKay, R.D. (1999) Embryonic stem cell-derived glial precursors: A source of myelinating transplants. Science. 285: 754-756.
14. Caldwell, M.A., and Svendsen, C.N. (1998) Heparin, but not other proteoglycans potentiates the mitogenic effects of FGF-2 on mesencephalic precursor cells. Exp. Neurol., 152: 1-10.
15. Caldwell, M.A., Joly, E., Daley, E.C., Jauniaux, E. and Svendsen, C.N. (1999) Increasing the numbers of neurons developing from human neural precursor cells. Soc. Neurosci. Abstr., 25: 2288-2288.
16. Cameron, H.A., Hazel, T.G. and McKay, R.D.G. (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol., 36: 287-306.
17. Carpenter, M.K., Cui, X., Hu, Z.-Y., Jackson, J., Sherman, S., Seiger, A. and Whalberg, L. (1999) In vitro expansion of a multipotent population of human neural progenitor cells. Exp, Neurol., 158: 265-278.
18. Chandran, S. and Svendsen, C.N. (1999) Neural cells for transplantation. In: S.B. Dunnett, A.A. Boulton and G.B. Baker (Eds.), Neural Transplantation Methods. Humana, Totowa, NJ, pp. 41-54.
19. Ciccolini, F. and Svendsen, C.N. (1998) 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., 18: 7869-7880.
20. Corti, O., Sabate, O., Horellou, P., Colin, P., Dumas, S., Buchet, D., Buc-Caron, M.H. and Mallet, J. (1999) A single adenovirus vector mediates doxycycline-controlled expression of tyrosine hydroxylase in brain grafts of human neural progenitors. Nat. Biotechnol., 17: 349-354.
21. Daadi, M.M. and Weiss, S. (1999) Generation of tyrosine hydroxylase-producing neurons from precursors of the embryonic and adult forebrain. J. Neurosci., 19: 4484-4497.
22. Deacon, T., Dinsmore, J., Costantini, L.C., Ratliff, J. and Isacson, O. (1998) Blastula-stage stem cells can differentiate into dopaminergic and serotonergic neurons after transplantation. Exp. Neurol., 149: 28-41.
23. Dunnett, S.B. and Björklund, A. (1999) Prospects for new restorative and neuroprotective treatments in Parkinson's disease. Nature, 399: A32-A39.
24. Eglitis, M.A. and Mezey, E. (1997) Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc. Natl. Acad. Sci. USA, 94: 4080-4085.
25. Eriksson, P.S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A. and Gage, F.H. (1998) Neurogenesis in the adult human hippocampus. Nat. Med., 4: 1313-1317.
26. 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. and Snyder, E.Y. (1998) Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat. Biotechnol., 16: 1033-1039.
27. Fricker, R.A., Carpenter, M.K., Winkler, C., Creco, C., Gates, M.A. and Björklund, A. (1999) Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J. Neurosci., 19: 5990-6005.
28. Gage, F.H. (1998) Cell therapy. Nature, 392(Suppl.): 18-24.
29. Gage, F.H., Ray, J. and Fisher, L.J. (1995) Isolation, characterisation, and use of stem cells from the CNS. Annu. Rev. Neurosci., 18: 159-192.
30. Gaiano, N. and Fishell, G. (1998) Transplantation as a tool to study progenitors within the vertebrate nervous system. J. Neurobiol., 36: 152-161.
31. Gensburger, C., Labourdette, G. and Sensenbrenner, M. (1987) Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett., 217: 1-5.
32. Golden, J.A. and Cepko, C.L. (1996) Clones in the chick diencephalon contain multiple cell types and siblings are widely dispersed. Development, 122: 65-78.
33. Grinspan, J.B., Stern, J.L., Pustilnik, S.M. and Pleasure, D. (1990) Cerebral white matter contains PDGF-responsive precursors to O2A cells. J. Neurosci., 10: 1866-1873.
34. Gritti, A., Parati, E.A., Cova, L., Frolichsthal, P., Galli, P., Wanke, E., Faravelli, L., Morassutti, D., Roisen, F., Nickel, D.D. and Vescovi, A.L. (1996) Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci., 16: 1091-1100.
35. Hammang, J.P., Archer, D.R. and Duncan, I.D. (1997) Myelination following transplantation of EGF-responsive neural stem cells into a myelin-deficient environment. Exp. Neurol., 147: 84-95.
36. Harley, C.B., Futcher, A.B. and Greider, C.W. (1990) Telomeres shorten during ageing of human fibroblasts. Nature, 345: 458-460.
37. Hayflick, L. (1997) Mortality and immortality at the cellular level. A review. Biochemistry (Mosc.), 62: 1180-1190.
38. lacovitti, L., Lee, J., Joh, T.H. and Reis, D.J. (1987) Expression of tyrosine hydroxylase in neurons of cultured cerebral cortex: Evidence for phenotypic plasticity in neurons of the CNS. J. Neurosci., 7: 1264-1270.
39. Isacson, O. (1999) The neurobiology and neurogenetics of stem cells. Brain Pathol., 9: 495-498.
40. Jacobson, M. (1991) The germinal cell, histiogenesis, and lineages of nerve cells. In: M. Jacobson (Ed.), Developmental Neurobiology. Plenum Press. New York.
41. Joh, K., Hazel, T., Muller, T., Dugich-Djordjevic, M. and McKay, R.D.G. (1996) Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev., 10: 3129-3140.
42. Johansson, C.B., Svennson, M., Wallstedt, L., Janson, A.M. and Frisén, J. (1999) Neural stem cells in the adult human brain, Exp. Cell Res., 253: 733-736.
43. Kageyama, R. and Nakanishi, S. (1997) Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr. Opin. Genet. Dev., 7: 659-665.
44. Keirstead, H.S., Ben-Hur, T., Rogister, B., O'Leary, M.T., Dubois-Dalcq, M. and Blakemore, W.F. (1999) Polysialylated neural cell adhesion molecule-positive CNS precursors generate both oligodendrocytes and Schwann cells to remyelinate the CNS after transplantation. J. Neurosci., 19: 7529-7536.
45. Kilpatrick, T.J. and Bartlett, P.F. (1995) 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: 3653-3661.
46. Kilpatrick, T.J., Richards, L.J. and Bartlett, P.F. (1995) The regulation of neural precursor cells within the mammalian brain. Mol. Cell. Neurosci., 6: 2-15.
47. Kopen, G.C., Prockop, D.J. and Phinney, D.G. (1999) Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. USA, 96: 10711-10716.
48. Kordower, J.H., Chen, E.Y., Winkler, C., Fricker, R., Charles, V., Messing, A., Mufson, E.J., Wong, S.C., Rosenstein, J.M., Björklund, A., Emerich, D.F., Hammang, J. and Carpenter, M.K. (1997) Grafts of EGF-responsive neural stem cells derived from GFAP-hNGF transgenic mice: Trophic and tropic effects in a rodent model of Huntington's disease. J. Comp. Neurol., 387: 96-113.
49. Kuhn, H.G. and Svendsen, C.N. (1999) Origins, functions, and potential of adult neural stem cells. Bioessays, 21: 625-630.
50. Kuhn, H.G., Winkler, J., Kempermann, G., Thal, L.J. and Gage, F.H. (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci., 17: 5820-5829.
51. Kukekov, V.G., Laywell, ED., Suslov, O., Davies, K., Scheffler, B., Thomas, L.B., O'Brien, T.F., Kusakabe, M. and Steindler, D.A. (1999) Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp. Neurol., 156: 333-344.
52. Lee, J.E., Hollenberg, S.M., Snider, L., Turner, D.L., Lipnick, N. and Weintraub, H. (1995) Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science, 268: 836-845.
53. Li, M., Pevny, L., Lovell-Badge, R. and Smith, A. (1998) Generation of purified neural precursors from embryonic stem cells by lineage selection. Curr. Biol., 8: 971-974.
54. Ling, Z.D., Potter, E.D., Lipton, J.W. and Carvey, P.M. (1998) Differentiation of mesencephalic progenitor cells into dopaminergic neurons by cytokines. Exp. Neurol., 149: 411-423.
55. Lumsden, A. and Krumlauf, R. (1996) Patterning the vertebrate neuraxis. Science. 274: 1109-1115.
56. Martinez-Serrano, A. and Björklund, A. (1997) Immortalized neural progenitor cells for CNS gene transfer and repair. Trends Neurosci., 20: 530-538.
57. McKay, R.D.G. (1997) Stem cells in the central nervous system. Science, 276: 66-71.
58. Mujtaba, T., Mayer-Proschel, M. and Rao, M.S. (1998) A common neural progenitor for the CNS and PNS. Dev. Biol., 200: 1-15.
59. Mujtaba, T., Piper, D.R., Kalyani, A., Groves, A.K., Lucero, M.T. and Rao, M.S. (1999) Lineage-restricted neural precursors can be isolated from both the mouse neural tube and cultured ES cells. Dev. Biol., 214: 113-127.
60. Nakagawa, Y., Kaneko, T., Ogura, T., Suzuki, T., Torii, M., Kaibuchi, K., Arai, K., Nakamura, S. and Nakafuku, M. (1996) Roles of cell-autonomous mechanisms for differential expression of region-specific transcription factors in neuroepithelial cells. Development, 122: 2449-2464.
61. Okabe, S., Forsberg-Nilsson, K., Spiro, A.C., Segal, M. and McKay, R.D.G. (1996) Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev., 59: 89-102.
62. Ostenfeld, T., Caldwell, M.A. and Svendsen, C.N. (1999a) Extensive neurite outgrowth following transplantation of human neural precursor cells into the lesioned rodent striatum. Soc. Neurosci. Abstr., 25: 213-213.
63. Ostenfeld, T., Horn, P., Aardal, C., Ørpen, I., Caldwell, M.A. and Svendsen, C.N. (1999b) Mouse epidermal growth factor-responsive neural precursor cells increase the survival and functional capacity of embryonic rat dopamine neurons in vitro. Neuroreport, 10: 1985-1992.
64. Ostenfeld, T., Caldwell, M.A., Prowse, K.R., Linskens, M.H., Jauniaux, E. and Svendsen, C.N. (2000) Human neural precursor cells express low levels of telomerase in vitro and show diminishing cell proliferation with extensive axonal outgrowth following transplantation. Exp. Neurol. (in press).
65. Palmer, T.D., Takahashi, J. and Gage, F.H. (1997) The adult rat hippocampus contains primordial neural stem cells. Mol. Cell. Neurosci., 8: 389-404.
66. Pleasure, S.J. and Lee, V.M.Y. (1993) NTera 2 cells: A human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J. Neurosci. Res., 35: 585-602.
67. Quinn, S.M., Walters, W.M., Vescovi, A.L. and Whittemore, S.R. (1999) Lineage restriction of neuroepithelial precursor cells from fetal human spinal cord. J. Neurosci. Res., 57: 590-602.
68. Raff, M.C., Abney, E.R. and Fok-Seang, J. (1985) Reconstitution of a developmental clock in vitro: A critical role for astrocytes in the timing of oligodendrocyte differentiation. Cell, 42: 61-69.
69. Rao, M.S. (1999) Multipotent and restricted precursors in the central nervous system. Anat. Rec., 257: 137-148.
70. Ray, J., Peterson, D.A., Schinstine, M. and Gage, F.H. (1993) Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc. Natl. Acad. Sci. USA, 90: 3602-3606.
71. Ray, J., Raymon, H.K. and Gage, F.H. (1995) Generation and culturing of precursor cells and neuroblasts from embryonic and adult central nervous system. Meth. Enzymol., 254: 20-37.
72. Reynolds, B.A. and Weiss, S. (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol., 175: 1-13.
73. Reynolds, B.A., Tetzlaff, W. and Weiss, S. (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci., 12: 4565-4574.
74. Robertson, E.J. (1987) Embryo-derived stem cell lines. In: E.J. Robertson (Ed.), Teratocarcinomas and Embryonic Stem Cells: A Practical Approach. IRL Press, Oxford, pp. 71-112.
75. Sabate, O., Horellou, P., Vigne, E., Colin, P., Perricaudet. M., Buc-Caron, M. and Mallet, J. (1995) Transplantation to the rat brain of human neural progenitors that were genetically modified using adenoviruses. Nat. Genet., 9: 256-260.
76. Sakurada, K., Ohshima-Sakurada, M., Palmer, T.D. and Gage, F.H. (1999) Nurrl, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain. Development, 126: 4017-4026.
77. Saporta, S., Borlongan, C.V. and Sanberg, P.R. (1999) Neural transplantation of human neuroteratocarcinoma (hNT) neurons into ischemic rats. A quantitative dose-response analysis of cell survival and behavioural recovery. Neuroscience, 91: 519-525.
78. Shamblott, M.J., Axelman, J., Wang, S., Bugg, E.M., Littlefield, J.W., Donovan, P.J., Blumenthal, P.D., Huggins, G.R. and Gearhart, J.D. (1998) Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc. Natl. Acad. Sci. USA, 95: 13726-13731.
79. Studer, L., Tabar, V. and McKay, R.D. (1998) Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats. Nat. Neurosci., 1: 290-295.
80. Suhonen, J.O., Peterson, D.A., Ray, J. and Gage, F.H. (1996) Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature, 383: 624-627.
81. Svendsen, C.N. and Smith, A.G. (1999) New prospects for human stem-cell therapy in the nervous system. Trends Neurosci., 22: 357-364.
82. Svendsen, C.N., Clarke, D.J., Rosser, A.E. and Dunnett, S.B. (1996) 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: 376-388.
83. Svendsen, C.N., Caldwell, M.A., Shen, J., Ter Borg, M.G., Rosser, A.E., Tyers, P., Karmiol, S. and Dunnett, S.B. (1997a) Long term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinsons Disease. Exp. Neurol., 148: 135-146.
84. Svendsen, C.N., Skepper, J.N., Rosser, A.E., Ter Borg, M., Tyers, P. and Ryken, T. (1997b) Restricted growth potential of rat striatal precursors as compared to mouse. Dev. Brain Res., 99: 253-258.
85. Svendsen, C.N., Ter Borg, M.G., Armstrong, R.J.E., Rosser, A.E., Chandran, S., Ostenfeld, T. and Caldwell, M.A. (1998) A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods, 85: 141-153.
86. Svendsen, C.N., Prowse, KR., Linskens, M.H.K. and Jauniaux, E. (1999) Precursor cells isolated from the developing human CNS show regional specificity and lack telomerase expression. Soc. Neurosci. Abstr., 25: 254-254.
87. Takahashi, M., Palmer, T.D., Takahashi, J. and Gage, F.H. (1998) Widespread integration and survival of adult-derived neural progenitor cells in the developing optic retina. Mol. Cell. Neurosci., 12: 340-348.
88. Takahashi, J., Palmer, T.D. and Gage, F.H. (1999) Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J. Neurobiol., 38: 65-81.
89. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshal, V.S. and Jones, J.M. (1998) Embryonic stem cell lines derived from human blastocysts. Science, 282: 1145-1147.
90. Vescovi, A.L., Parati, E.A., Gritti, A., Poulin, P., Ferrario, M., Wanke, E., Frolichsthal-Schoeller, P., Cova, L., Arcellana-Panlilio, M., Colombo, A. and Galli, R. (1999) Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Exp. Neurol., 156: 71-83.
91. Wagner, J., Akerud, P., Castro, D.S., Holm, P.C., Canals, J.M., Snyder, E.Y., Perlmann, T. and Arenas, E. (1999) Induction of a midbrain dopaminergic phenotype in Nurrl-overexpressing neural stem cells by type I astrocytes. Nat. Biotechnol., 17: 653-659.
92. Wallace, V.A. (1999) Purkinje-cell-derived sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol., 9: 445-448.
93. Whittemore, S.R. and Onifer, S.M. (2000) Immortalized neural cell lines for CNS transplantation. In: S.B. Dunnett and A. Björklund (Eds.), Functional Neural Transplantation II. Novel Cell Therapies for CNS Disorders. Progress in Brain Research, Vol. 127, Elsevier, Amsterdam, pp. 49-65, this volume.
94. Whittemore, S.R., Morassutti, D.J., Walters, W.M., Liu, R.H. and Magnuson, D.S. (1999) Mitogen and substrate differentially affect the lineage restriction of adult rat subventricular zone neural precursor cell populations. Exp. Cell Res., 252: 75-95.
95. Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. and Campbell, K.H. (1997) Viable offspring derived from fetal and adult mammalian cells. [Published erratum appears in Nature 1997; 386: 200.] Nature, 385: 810-813.
96. Winkler, C., Fricker, R.A., Gates, M.A., Olsson, M., Hammang, J.P., Carpenter, M.K. and Björklund, A. (1998) Incorporation and glial differentiation of mouse EGF-responsive neural progenitor cells after transplantation into the embryonic rat brain. Mol. Cell. Neurosci., 11: 99-116.