Central nervous system stem cells in the embryo and adult

Cellular and Molecular Life Sciences

Volumn 54, Issue 9, 1998, Pages 935-945

  Frisen J ^a   Johansson, C B ^a   Lothian, C ^a   Lendahl, U ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Development; Differentiation; Glia; Neuron; Regeneration

Indexed keywords

ASTROCYTE; BRAIN; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; EMBRYO DEVELOPMENT; HIPPOCAMPUS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; OLFACTORY BULB; OLIGODENDROGLIA; REVIEW; SPINAL CORD; STEM CELL;

ADULT; ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASES; HIPPOCAMPUS; HUMANS; NEURONS; OLFACTORY BULB; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 0031709102     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000180050224     Document Type: Review

References (93)

1. Spemann H. (1938) Embryonic development and induction. Yale University Press, New Haven, CT
2. Heldin C.-H., Miyazono K. and ten Dijke P. (1997) TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471
3. Piccolo S., Sasai Y., Lu B. and De Robertis E. (1996) Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86: 589-598
4. Zimmerman L. B., De Jesús-Escobar J. M. and Harland R. M. (1996) The Spemann Organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86: 599-606
5. Hemmati-Brivanlou A. and Melton D. (1997) Vertebrate embryonic cells will become nerve cells unless told otherwise. Cell 88: 13-17
6. Hawley S. H., Wunnenberg-Stapleton K., Hashimoto C., Laurent M. N., Watabe T., Blumberg B. W. et al. (1995) Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev. 9: 2923-2935
7. Suzuki A., Theis R. S., Yamaji N., Song J. J., Wozney J., Murakami K. et al. (1994) A truncated BMP receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA 91: 10255-10259
8. Matzuk M. M., Lu N., Vogel H., Sellheyer K., Roop D. R. and Bradley A. (1995) Multiple defects and perinatal death in mice deficient in follistatin. Nature 374: 360-363
9. Smith J. (1995) Angels on activin's absence. Nature 374: 311-312
10. Karfunkel P. (1971) The role of microtubules and microfilaments in neurulation in Xenopus. Dev. Biol. 25: 30-56
11. Schoenwolf G. C. and Smith J. L. (1990) Mechanisms of neurulation: traditional viewpoint and recent advances. Development 109: 243-270
12. Thomas T. and Dziadek M. (1993) Genes coding for basement membrane glycoproteins laminin, nidogen and collagen IV are differentially expressed in the nervous system and by epithelial, endothelial, and mesenchymal cells of the mouse embryo. Exp. Cell Res. 208: 54-67
13. McConnell S. K. (1995) Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 15: 761-768
14. Sauer F. C. (1935) Mitosis in the neural tube. J. Comp. Neurol. 62: 377-405
15. Rakic P. (1988) Specification of cerebral cortical areas. Science 1988: 170-176
16. Soriano E., Dumesnil N., Auladell C., Cohen-Tannoudji M. and Sotelo C. (1995) Molecular heterogeneity of progenitors and radial migration in the developing cerebral cortex revealed by transgene expression. Proc. Natl. Acad. Sci. USA 92: 11676-11680
17. Tan S.-S. and Breen S. (1993) Radial mosaicism and tangential cell dispersion both contribute to mouse neocortical development. Nature 362: 638-640
18. Tan S.-S., Faulkner-Jones B., Breen S. J., Walsh M., Bertram J. F. and Reese B. E. (1995) Cell dispersion patterns in different cortical regions studied with an X-inactivated transgenic marker. Development 121: 1029-1039
19. Rakic P. (1972) Mode of cell migration to the superficial layers of monkey neocortex. J. Comp. Neurol. 145: 61-84
20. Anton E. S., Cameron R. S. and Rakic P. (1996) Role of neuron-glial junctional domain proteins in the maintenance and termination of neuronal migration across the embryonic cerebral wall. J. Neurosci. 16: 2283-2293
21. Goffinet A. M. (1997) Unscrambling a disabled brain. Nature 389: 668-669
22. Howell B. W., Hawkes R., Soriano P. and Cooper J. A. (1997) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389: 733-737
23. Sheldon M., Rice D. S., D'Arcangelo G., Yoneshima H., Nakajima K., Mikoshiba K. et al. (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389: 730-733
24. Brüstle O., Maskos U. and McKay R. D. G. (1995) Host-guided migration allows targeted introduction of neurons into the embryonic brain. Neuron 15: 1275-1285
25. Campbell K., Olsson M. and Björklund A. (1995) Regional incorporation and site-specific differentiation of striatal precursors transplanted to the embryonic forebrain ventricle. Neuron 15: 1259-1273
26. Fishell G. (1995) Striatal precursors adopt cortical identities in response to local cues. Development 121: 803-812
27. Fishell G., Mason C. A. and Hatten M. E. (1993) Dispersion of neural progenitors within the germinal zones of the forebrain. Nature 362: 636-638
28. Reid C. B., Liang I. and Walsh C. (1995) Systematic widespread clonal organization in cerebral cortex. Neuron 15: 299-310
29. Reid C. B., Tavazoie S. F. and Walsh C. A. (1997) Clonal dispersion and evidence for asymmetric cell division in ferret cortex. Development 124: 2441-2450
30. Kornack D. R. and Rakic P. (1995) Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 15: 311-321
31. Rakic P. (1995) Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc. Natl. Acad. Sci. USA 92: 11323-11327
32. Morrison S. J., Shah N. M. and Anderson D. J. (1997) Regulatory mechanisms in stem cell biology. Cell 88: 287-298
33. McKay R. (1997) Stem cells in the central nervous system. Science 276: 66-71
34. Williams B. P. and Price J. (1995) Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron 14: 1181-1188
35. Temple S. and Qian X. (1996) Vertebrate neural progenitor cells: subtypes and regulation. Curr. Opin. Neurobiol. 6: 11-17
36. Temple S. and Davis A. A. (1994) A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372: 263-266
37. Lendahl U., Zimmerman L. B. and McKay R. D. G. (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595
38. Dahlstrand J., Lardelli M. and Lendahl U. (1995) Nestin mRNA expression correlates with the CNS progenitor cell state in many, but not all, regions of developing CNS. Dev. Brain Res. 84: 109-129
39. 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
40. Broadus J., Fuerstenberg S. and Doe C. Q. (1998) Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature 391: 792-795.
41. Ikeshima-Kataoka H., Skeath J. B., Nabeshima Y., Doe C. Q. and Matsuzaki F. (1997) Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature 390: 625-629
42. Shen C.-P., Jan L. Y. and Jan Y. N. (1997) Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell 90: 449-458
43. Zhong W., Feder J. N., Jiang M.-M., Jan L. Y. and Jan Y. N. (1996) Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17: 43-53
44. Chenn A. and McConnell S. K. (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82: 631-641
45. Lewis J. (1996) Neurogenic genes and vertebrate neurogenesis. Curr. Opin. Neurobiol. 6: 3-10
46. Johe K. K., Hazel T. G., 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
47. 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
48. Hammerschmidt M., Brook A. and McMahon A. P. (1997) The world according to hedgehog. Trends Genet. 13: 14-21
49. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V. et al. (1997) Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signalling. Cell 90: 169-180
50. Alvarez-Byulla A. and Kirn J. R. (1997) Birth, migration, incorporation and death of vocal control neurons in adult songbirds. J. Neurobiol. 33: 585-601
51. Altman J. and Das G. D. (1965) Autoradiographic and histological evidence of postnatal neurogenesis in rats. J. Comp. Neurol. 124: 319-335
52. Calof A. L., Hagiwara N., Holcomb J. D., Mumm J. S. and Shou J. (1996) Neurogenesis and cell death in olfactory epithelium. J. Neurobiol. 30: 67-81
53. Kirschenbaum B., Nedergaard M., Preuss A., Barami K., Fraser R. A. R. and Goldman S. A. (1994) In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb. Cortex 6: 576-589
54. Kuhn P. G., Dickinson-Anson H. and Gage F. H. (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16: 20-27
55. Tropepe V., Craig C. G., Morshead C. M. and van der Kooy D. (1997) Transforming growth factor-α null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J. Neurosci. 17: 7850-7859
56. Reynolds B. A. and Weiss S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710
57. Reynolds B. A. and Weiss S. (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic precursor is a stem cell. Dev. Biol. 175: 1-13
58. Lois C. and Alvarez-Buylla A. (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. USA 90: 2074-2077
59. Morshead C. M., Reynolds, B. A., Craig C. G., McBurney M. W., Staines W. A., Morassutti D. et al. (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13: 1071-1082
60. Palmer T. D., Ray J. and Gage F. H. (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell. Neurosci. 6: 474-486
61. 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
62. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A. C. et al. (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16: 7599-7609
63. Kawamata S., Stumpf W. E. and Bidmon H. J. (1995) Adhesion and fusion of ependyma in rat brain. Acta Anat. (Basel) 152: 205-214
64. Doetsch F., Garcia-Verdugo J. M. and Alvarez-Buylla A. (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17: 5046-5061
65. Gates M. A., Thomas L. B., Howard E. M., Laywell E. D., Sajin B., Faissner A. et al. (1995) Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J. Comp. Neurol. 361: 249-266
66. Morshead C. M. and van der Kooy D. (1992) Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J. Neurosci. 12: 249-256
67. Holder N., Clarke J. D. W., Stephens N., Wilson S. W., Orsi C., Bloomer T. et al. (1991) Continous growth of the motor system in the axolotl. J. Comp. Neurol. 303: 534-550
68. Del Bigio M. R. (1995) The ependyma: a protective barrier between brain and cerebrospinal fluid. Glia 14: 1-13
69. Lois C. and Alvarez-Buylla A. (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145-1148
70. Lois C., García-Verdugo J.-M. and Alvarez-Buylla A. (1996) Chain migration of neuronal precursors. Science 271: 978-981
71. Wichterle H., Garcia-Verdugo J. M. and Alvarez-Buylla A. (1997) Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18: 779-791
72. Doetsch F. and Alvarez-Buylla A. (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. USA 93: 14895-14900
73. Hu H., Tomasiewicz H., Magnusson T. and Rutishauser U. (1996) The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16: 735-743
74. Gould E. and Cameron H. A. (1996) Regulation of neuronal birth, migration and death in the rat dentate gyrus. Dev. Neurosci. 18: 22-35
75. Kaplan M. S., McNelly N. A. and Hinds J. W. (1985) Population dynamics of adult-formed granule neurons of the rat olfactory bulb. J. Comp. Neurol. 239: 117-125
76. Bayer S. A., Yackel J. W. and Puri P. S. (1982) Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216: 890-892
77. Gritti A., Parati E. A., Cova L., Frolichsthal P., Galli R., Wanke E. et al. (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
78. Craig C. G., Tropepe V., Morshead C. M., Reynolds B. A., Weiss S. and van der Kooy D. (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16: 2649-2658
79. 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
80. Kempermann G., Kuhn H. G. and Gage F. H. (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495
81. Gould E., McEwen B. S., Tanapat P., Galea L. A. M. and Fuchs E. (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17: 2492-2498
82. Cameron H. A., McEwen B. S. and Gould E. (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci. 15: 4687-4692
83. Parent J. M., Yu T. W., Leibowitz R., Geschwind D. H., Sloviter R. S. and Lowenstein D. H. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult hippocampus. J. Neurosci. 17: 3727-3738
84. Frisén J., Johansson C. B., Török C., Risling M. and Lendahl U. (1995) Rapid, widespread and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J. Cell Biol. 131: 453-464
85. Holmin S., Almzvist P., Lendahl U. and Mathiesen T. (1997) Adult nestin-expressing subependymal cells differentiate to astrocytes in response to brain injury. Eur. J. Neurosci. 9: 65-75
86. Gould E. and Tanapat P. (1997) Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 80: 427-436
87. Lim D. A., Fishell G. J. and Alvarez-Buylla A. (1997) Postnatal mouse subventricular zone neuronal precursors can migrate and differentiate within multiple levels of the developing neuraxis. Proc. Natl. Acad. Sci. USA 94: 14832-14836
88. Olson L. (1997) Regeneration in the adult central nervous system: experimental repair strategies. Nature Med. 3: 1329-1335
89. Lindvall O. (1997) Neural transplantation: a hope for patients with Parkinson's disease. Neuroreport 8: III-X
90. Deacon T., Schumacher J., Dinsmore J., Thomas C., Palmer P., Kott S. et al. (1997) Histological evidence of fetal pig neural cell survival after transplantation into a patient with Parkinson's disease. Nature Med. 3: 350-353
91. Butler D., Wadman M., Lehrman S. and Schirmeier Q. (1998) Last chance to stop and think on risks of xenotransplantation. Nature 391: 320-325
92. Björklund A. (1994) Long distance axonal growth in the adult central nervous system. J. Neurol. 242: S33-S35
93. Gage F. H., Coates P. W., Palmer T. D., Kuhn H. G., Fisher L. J., Suhonen J. O. et al. (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl. Acad. Sci. USA 92: 11879-11883