Skip to main content
Log in

Glioma Migration: Clues from the Biology of Neural Progenitor Cells and Embryonic CNS Cell Migration

  • Published:
Journal of Neuro-Oncology Aims and scope Submit manuscript

Abstract

Neural stem cells have recently come to the forefront in neurobiology because of the possibilities for CNS repair by transplantation. Further understanding of the biology of these cells is critical for making their use in CNS repair possible. It is likely that these discoveries will also have spin-offs for neuro-oncology as primary brain tumors may arise from a CNS progenitor cell. An understanding of the normal migratory ability of these cells is also likely to have a very important impact on the knowledge of brain tumor invasion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Wechsler-Reya R, Scott MP: The developmental biology of brain tumors. Annu Rev Neurosci 24: 385–428, 2001

    Google Scholar 

  2. Goodrich LV, Milenkovic L, Higgins KM, Scott MP: Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277: 1109–1113, 1997

    Google Scholar 

  3. Pietsch T, Waha A, Koch A, Kraus J, Albrecht S, Tonn J, Sorensen N, Berthold F, Henk B, Schmandt N, Wolf HK, von Deimling A, Wainwright B, Chenevix-Trench G, Wiestler OD, Wicking C: Medulloblastomas of the desmoplastic variant carry mutations of the human homologue of Drosophila patched. Cancer Res 57: 2085–2088, 1997

    Google Scholar 

  4. Raffel C, Jenkins RB, Frederick L, Hebrink D, Alderete B, Fults DW, James CD: Sporadic medulloblastomas contain PTCH mutations. Cancer Res 57: 842–845, 1997

    Google Scholar 

  5. Wechsler-Reya RJ, Scott MP: Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog. Neuron 22: 103–114, 1999

    Google Scholar 

  6. Potten CS, Loeffler M: Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110: 1001–1020, 1990

    Google Scholar 

  7. Hall PA, Watt FM: Stem cells: the generation and maintenance of cellular diversity. Development 106: 619–633, 1989

    Google Scholar 

  8. Morrison SJ, Shah NM, Anderson DJ: Regulatory mechanisms in stem cell biology. Cell 88: 287–298, 1997

    Google Scholar 

  9. Gage FH: Stem cells of the central nervous system. Curr Opin Neurobiol 8: 671–676, 1998

    Google Scholar 

  10. Weiss S, van der Kooy D: CNS stem cells: where's the biology (a.k.a. beef)? J Neurobiol 36: 307–314, 1998

    Google Scholar 

  11. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A: Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703–716, 1999

    Google Scholar 

  12. Johansson CB, Momma S, Clarke DL, Risling M, Lehdahl U, Frisen J: Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25–34, 1999

    Google Scholar 

  13. Morshead CM, van der Kooy DA: new ‘spin’ on neural stem cells? Curr Opin Neurobiol 11: 59–65, 2001

    Google Scholar 

  14. Reynolds BA, Weiss S: Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system (see comments). Science 255: 1707–1710, 1992

    Google Scholar 

  15. 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: 2074–2077, 1993

    Google Scholar 

  16. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van derKooy D: Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13: 1071–1082, 1994

    Google Scholar 

  17. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA: Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16: 7599–7609, 1996

    Google Scholar 

  18. Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A: Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 36: 234–248, 1998

    Google Scholar 

  19. Morshead CM, Craig CG, van der Kooy D: In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 125: 2251–2261, 1998

    Google Scholar 

  20. Temple S, Alvarez-Buylla A: Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 9: 135–141, 1999

    Google Scholar 

  21. Hockfield S, McKay RD: Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5: 3310–3328, 1985

    Google Scholar 

  22. Lendahl U, Zimmerman LB, McKay RD: CNS stem cells express a new class of intermediate filament protein. Cell 60: 585–595, 1990

    Google Scholar 

  23. Gates MA, Thomas LB, Howard EM, Laywell ED, Sajin B, Faissner A, Gotz B, Silver J, Steindler DA: Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J Comp Neurol 361: 249–266, 1995

    Google Scholar 

  24. Zimmerman L, Parr B, Lendahl U, Cunningham M, McKay R, Gavin B, Mann J, Vassileva G, McMahon A: Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors (published erratum appears in Neuron 1994 Jun; 12(6): following 1388). Neuron 12: 11–24, 1994

    Google Scholar 

  25. Frederiksen K, McKay RD: Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8: 1144–1151, 1988

    Google Scholar 

  26. McKay R: Stem cells in the central nervous system. Science 276: 66–71, 1997

    Google Scholar 

  27. Hatten ME, Heintz N: Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18: 385–408, 1995

    Google Scholar 

  28. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL, Jendoubi M, Sidman RL, Wolfe JH, Kim SU, Snyder EY: Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol 16: 1033–1039, 1998

    Google Scholar 

  29. Sah DW, Ray J, Gage FH: Bipotent progenitor cell lines from the human CNS. Nat Biotechnol 15: 574–580, 1997

    Google Scholar 

  30. Jacobson M: Developmental Neurobiology. Plenum Press, New York, 1991

    Google Scholar 

  31. Messier B, LeBlond CP, Smart I: Presence of DNA synthesis and mitosis in the brain of young adult mice. Exp Cell Res 14: 224–226, 1958

    Google Scholar 

  32. Smart I: The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J Comp Neurol 116: 325–347, 1961

    Google Scholar 

  33. Altman J: Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145: 573–591, 1963

    Google Scholar 

  34. Rakic P: Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183: 425–427, 1974

    Google Scholar 

  35. Korr H: Proliferation of Different Cell Types in the Brain. Springer-Verlag, Berlin, 1980.

    Google Scholar 

  36. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH: Neurogenesis in the adult human hippocampus (see comments). Nat Med 4: 1313–1317, 1998

    Google Scholar 

  37. Alvarez-Buylla A, Lois C: Neuronal stem cells in the brain of adult vertebrates. Stem Cells (Dayt) 13: 263–272, 1995

    Google Scholar 

  38. Gage FH, Ray J, Fisher LJ: Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 18: 159–192, 1995

    Google Scholar 

  39. Morshead CM, van der Kooy D: Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J Neurosci 12: 249–256, 1992

    Google Scholar 

  40. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen F, Nickel DD, Vescovi AL: Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16: 1091–1100, 1996

    Google Scholar 

  41. Tropepe V, Craig CG, Morshead CM, van der Kooy D: Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 17: 7850–7859, 1997

    Google Scholar 

  42. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ: Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2: 260–265, 1999

    Google Scholar 

  43. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E: Neurogenesis in the adult is involved in the formation of trace memories. Nature 410: 372–376, 2001

    Google Scholar 

  44. Cameron HA, Gould E: Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61: 203–209, 1994

    Google Scholar 

  45. Cameron HA, Tanapat P, Gould E: Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 82: 349–354, 1998

    Google Scholar 

  46. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E: Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17, 2492–2498, 1997

    Google Scholar 

  47. Traiffort E, Charytoniuk DA, Faure H, Ruat M: Regional distribution of Sonic Hedgehog, patched, and smoothened mRNA in the adult rat brain. J Neurochem 70: 1327–1330, 1998

    Google Scholar 

  48. van Praag H, Christie BR, Sejnowski TJ, Gage FH: Runningenhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96: 13427–13431, 1999

    Google Scholar 

  49. van Praag H, Kempermann G, Gage FH: Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2: 266–270, 1999

    Google Scholar 

  50. Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D: Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 19: 4462–4471, 1999

    Google Scholar 

  51. Hartfuss E, Galli R, Heins N, Gotz M: Characterization of CNS precursor subtypes and radial glia. Dev Biol 229: 15–30, 2001

    Google Scholar 

  52. Malatesta P, Hartfuss E, Gotz M: Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127: 5253–5263, 2000

    Google Scholar 

  53. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR: Neurons derived from radial glial cells establish radial units in neocortex. Nature 409: 714–720, 2001

    Google Scholar 

  54. Johansson CB, Svensson M, Wallstedt L, Janson AM, Frisen J: Neural stem cells in the adult human brain. Exp Cell Res 253: 733–736, 1999

    Google Scholar 

  55. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, Harrison-Restelli C, Fraser RA, Couldwell WT, Kawaguchi A, Okano H, Nedergaard M, Goldman SA: In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 6: 271–277, 2000

    Google Scholar 

  56. Roy NS, Benraiss A, Wang S, Fraser RA, Goodman R, Couldwell WT, Nedergaard M, Kawaguchi A, Okano H, Goldman SA: Promoter-targeted selection and isolation of neural progenitor cells from the adult human ventricular zone. J Neurosci Res 59: 321–331, 2000

    Google Scholar 

  57. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH: Progenitor cells from human brain after death. Nature 411: 42–43, 2001

    Google Scholar 

  58. Hatten ME: Central nervous system migration. Annu Rev Neurosci 22, 511–539, 1999

    Google Scholar 

  59. Altman J: Autoradiographic and histologic studies of postnatal neurogenesis. III. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 136: 269–294, 1969

    Google Scholar 

  60. Lois C, Alvarez-Buylla A: Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145–1148, 1994

    Google Scholar 

  61. Lois C, Garcia-Verdugo J-M: Chain migration of neuronal precursors. Science 271: 978–981, 1996

    Google Scholar 

  62. Luskin MB: Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11: 173–189, 1993

    Google Scholar 

  63. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A: Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17: 5046–5061, 1997

    Google Scholar 

  64. Lin RCS, Matesic DF, Marvin M, McKay RD, Brustle O: Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis 2: 79–85, 1995

    Google Scholar 

  65. Frisen J, Johansson CB, Torok C, Risling M, Lendahl U: Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131: 453–464, 1995

    Google Scholar 

  66. Craig CG, Tropepe V, Morshead CM, Reynolds BA, 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: 2649–2658, 1996

    Google Scholar 

  67. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH: Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17: 5820–5829, 1997

    Google Scholar 

  68. Kaltschmidt JA, Davidson CM, Brown NH, Brand AH: Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nat Cell Biol 2: 7–12, 2000

    Google Scholar 

  69. Embryonic vertebrate central nervous system: revised terminology. The Boulder Committee. Anat Rec 166: 257–261, 1970

  70. Sidman RL, Rakic P: Neuronal migration, with special reference to developing human brain: a review. Brain Res 62: 1–35, 1973

    Google Scholar 

  71. Allendoerfer KL, Shatz CJ: The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 17: 185–218, 1994

    Google Scholar 

  72. Super H, Del Rio JA, Martinez A, Perez-Sust P, Soriano E: Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal– Retzius cells. Cereb Cortex 10: 602–613, 2000

    Google Scholar 

  73. O'Rourke NA, Dailey ME, Smith SJ, McConnell SK: Diverse migratory pathways in the developing cerebral cortex. Science 258: 299–302, 1992

    Google Scholar 

  74. Tan SS, Breen S: Radial mosaicism and tangential cell dispersion both contribute to mouse neocortical development. Nature 362: 638–640, 1993

    Google Scholar 

  75. O'Rourke NA, Sullivan DP, Kaznowski CE, Jacobs AA, McConnell SK: Tangential migration of neurons in the developing cerebral cortex. Development 121: 2165–2176, 1995

    Google Scholar 

  76. Pearlman AL, Faust PL, Hatten ME, Brunstrom JE: New directions for neuronal migration. Curr Opin Neurobiol 8: 45–54, 1998

    Google Scholar 

  77. Schmechel DE, Rakic PA: Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol (Berl) 156: 115–152, 1979

    Google Scholar 

  78. Culican SM, Baumrind NL, Yamamoto M, Pearlman AL: Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J Neurosci 10: 684–692, 1990

    Google Scholar 

  79. Chanas-Sacre G, Rogister B, Moonen G, Leprince P: Radial glia phenotype: origin, regulation, and transdifferentiation. J Neurosci Res 61: 357–363, 2000

    Google Scholar 

  80. Rakic P: Neuron–glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J Comp Neurol 141: 283–312, 1971

    Google Scholar 

  81. Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL: Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4: 143–150, 2001

    Google Scholar 

  82. Tan SS, Kalloniatis M, Sturm K, Tam PP, Reese BE, Faulkner-Jones B: Separate progenitors for radial and tangential cell dispersion during development of the cerebral neocortex. Neuron 21: 295–304, 1998

    Google Scholar 

  83. Lois C, Alvarez-Buylla A: Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145–1148, 1994

    Google Scholar 

  84. Wichterle H, Garcia-Verdugo JM, Alvarez-Buylla A: Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18: 779–791, 1997

    Google Scholar 

  85. Komuro H, Yacubova E, Rakic P: Mode and tempo of tangential cell migration in the cerebellar external granular layer. J Neurosci 21: 527–540, 2001

    Google Scholar 

  86. Edmondson JC, Liem RK, Kuster JE, Hatten ME: Astrotactin: a novel neuronal cell surface antigen that mediates neuron–astroglial interactions in cerebellar microcultures. J Cell Biol 106, 505–517, 1988

    Google Scholar 

  87. Zheng C, Heintz N, Hatten ME: CNS gene encoding astrotactin, which supports neuronal migration along glial fibers. Science 272: 417–419, 1996

    Google Scholar 

  88. Rio C, Rieff HI, Qi P, Khurana TS, Corfas G: Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19: 39–50, 1997

    Google Scholar 

  89. Anton ES, Marchionni MA, Lee KF, Rakic P: Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124: 3501–3510, 1997

    Google Scholar 

  90. Georges-Labouesse E, Mark M, Messaddeq N, Gansmuller A: Essential role of alpha 6 integrins in cortical and retinal lamination. Curr Biol 8: 983–986, 1998

    Google Scholar 

  91. Anton ES, Kreidberg JA, Rakic P: Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22: 277–289, 1999

    Google Scholar 

  92. Jacques TS, Relvas JB, Nishimura S, Pytela R, Edwards GM, Streuli CH, French-Constant C: Neural precursor cell chain migration and division are regulated through different beta1 integrins. Development 125: 3167–3177, 1998

    Google Scholar 

  93. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S: Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367: 455–459, 1994

    Google Scholar 

  94. Tomasiewicz H, Ono K, Yee D, Thompson C, Goridis C, Rutishauser U, Magnuson T: Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11: 1163–1174, 1993

    Google Scholar 

  95. Chazal G, Durbec P, Jankovski A, Rougon G, Cremer H: Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci 20: 1446–1457, 2000

    Google Scholar 

  96. Wu W, Wong K, Chen J, Jiang Z, Dupulis S, Wu JY, Rao Y: Directional guidance of neuronal migration in the olfactory system by the protein Slit (see comments). Nature 400; 331–336, 1999

    Google Scholar 

  97. Zou Y, Stoeckli E, Chen H, Tessier-Lavigne M: Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102: 363–375, 2000

    Google Scholar 

  98. Alcantara S, Ruiz M, De Castro F, Soriano E, Sotelo C: Netrin1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system. Development 127: 1359–1372, 2000

    Google Scholar 

  99. Flanagan JG, Vanderhaeghen P: The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21: 309–345, 1998

    Google Scholar 

  100. Wilkinson DG: Multiple roles of EPH receptors and ephrins in neural development. Nat Rev Neurosci 2: 155–164, 2001

    Google Scholar 

  101. Gerlai R: Eph receptors and neural plasticity. Nat Rev Neurosci 2: 205–209, 2001

    Google Scholar 

  102. Conover JC, Doetsch F, Garcia-Verdugo JM, Gale NW, Yancopoulos GD, Alvarez-Buylla A: Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 3: 1091–1097, 2000

    Google Scholar 

  103. Powell EM, Mars WM, Levitt P: Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30: 79–89, 2001

    Google Scholar 

  104. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, SuhrST, Ray J: Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci USA 92: 11879–11883, 1995

    Google Scholar 

  105. Vescovi AL, Parati EA, Gritti A, Poulin P, Ferrario M, Wanke E, Frolichsthal-Schoeller P, Cova L, Arcellana-Panlilio M, Colombo A, Galli R: 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, 1999

    Google Scholar 

  106. Fricker RA, Carpenter MK, Winkler C, Greco C, Gates MA, Bjorklund A: Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J Neurosci 19: 5990–6005, 1999

    Google Scholar 

  107. Hammang JP, Archer DR, Duncan ID: Myelination following transplantation of EGF-responsive neural stem cells into a myelin-deficient environment. Exp Neurol 147: 84–95, 1997

    Google Scholar 

  108. Zhang SC, Ge B, Duncan ID: Adult brain retains the potential to generate oligodendroglial progenitors with extensive myelination capacity. Proc Natl Acad Sci USA 96: 4089–4094, 1999

    Google Scholar 

  109. Brustle O, Choudhary K, Karram K, Huttner A, Murray K, Dubois-Dalcq M, McKay RD: Chimeric brains generated by intraventricular transplantation of fetal human brain cells into embryonic rats. Nat Biotechnol 16: 1040–1044, 1998

    Google Scholar 

  110. Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, Breakefield XO, Snyder EY: From the cover: neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 97: 12846–12851, 2000

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dirks, P.B. Glioma Migration: Clues from the Biology of Neural Progenitor Cells and Embryonic CNS Cell Migration. J Neurooncol 53, 203–212 (2001). https://doi.org/10.1023/A:1012273922478

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1012273922478

Navigation