Neural stem cells redefined: A FACS perspective

Molecular Neurobiology

Volumn 30, Issue 1, 2004, Pages 49-76

  Maric, Dragan ^a   Barker, Jeffery L ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Cell fate; Central nervous system; Cortex; Development; Fluorescence activated cell sorting; Neural progenitors; Neural stem cells

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GANGLIOSIDE;

CELL DIFFERENTIATION; CELL ISOLATION; CELL POPULATION; CULTURE MEDIUM; CYTOLOGY; DNA MICROARRAY; HUMAN; NERVOUS SYSTEM; NEURAL STEM CELL; NEUROECTODERM; NEUROEPITHELIUM; NONHUMAN; PHENOTYPE; PHYLOGENY; PROTEIN EXPRESSION; REVIEW; TELENCEPHALON; TRANSGENIC MOUSE; ANIMAL; EMBRYO; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; METHODOLOGY; NERVE CELL; PHYSIOLOGY; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; EMBRYO; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; NEURONS; STEM CELLS;

EID: 4644306262     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1385/mn:30:1:049     Document Type: Review

References (97)

1. Gage F.H. (2000) Mammalian neural stem cells. Science 287, 1433-1438.
2. Anderson D.J. (2001) Stem cells and pattern formation in the nervous system: the possible versus the actual. Neuron 30, 19-35.
3. Temple S. (2001) Stem cell plasticity - building the brain of our dreams. Nat. Rev. Neurosci. 2, 513-520.
4. Temple S. (2001) The development of neural stem cells. Nature 414, 112-117.
5. Vaccarino F.M., Ganat Y., Zhang Y., and Zheng W. (2001) Stem cells in neurodevelopment and plasticity. Neuropsychopharmacology 25, 805-815.
6. Vescovi A.L., Galli R., and Gritti A. (2001) The neural stem cells and their transdifferentiation capacity. Biomed. Pharmacother. 55, 201-205.
7. Weissman I.L., Anderson D.J, and Gage F. (2001) Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu. Rev. Cell. Dev. Biol. 17, 387-403.
8. Gottlieb D.I. (2002) Large-scale sources of neural stem cells. Annu. Rev. Neurosci. 25, 381-407.
9. Gritti A., Vescovi A.L., and Galli R. (2002) Adult neural stem cells: plasticity and developmental potential. J. Physiol. 96, 81-90.
10. Kennea N.L. and Mehmet H. (2002) Neural stem cells. J. Pathol. 197, 536-550.
11. Kruger G.M. and Morrison S.J. (2002) Brain repair by endogenous progenitors. Cell 110, 399-402.
12. Panchision D.M. and McKay R.D. (2002) The control of neural stem cells by morphogenic signals. Curr. Opin. Genet. Dev. 12, 478-487.
13. Tsai R.Y., Kittappa R., and McKay R.D. (2002) Plasticity niches, and the use of stem cells. Dev. Cell. 2, 707-712.
14. Cai J. and Rao M.S. (2002) Stem cell and precursor cell therapy. Neuromolecular Med. 2, 233-249.
15. Galli R., Gritti A., Bonfanti L., and Vescovi A.L. (2003) Neural stem cells: an overview. Circ. Res. 92, 598-608.
16. Limke T.L. and Rao M.S. (2002) Neural stem cells in aging and disease. J. Cell. Mol. Med. 6, 475-496.
17. Pevny L. and Rao M.S. (2003) The stem-cell menagerie. Trends Neurosci. 351-359.
18. Arsenijevic Y. (2003) Mammalian neural stem-cell renewal: nature versus nurture. Mol. Neurobiol. 27, 73-98.
19. Seaberg R.M. and van der Kooy D. (2003) Stem and progenitor cells: the premature desertion of rigorous definitions. Trends Neurosci. 26, 125-131.
20. Johansson C.B. (2003) Mechanism of stem cells in the central nervous system. J. Cell. Physiol. 196, 409-418.
21. 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.
22. Galli R., Borello U., Gritti A., Minasi M.G., Bjornson C., Coletta M., et al. (2000) Skeletal myogenic potential of human and mouse neural stem cells. Nat. Neurosci. 3, 986-991.
23. Anderson D.J., Gage F.H., and Weissman I.L. (2001) Can stem cells cross lineage boundaries? Nat. Med. 7, 393-395.
24. Liu Y. and Rao M.S. (2003) Transdifferentiation - fact or artifact. J. Cell. Biochem. 88, 29-40.
25. Tropepe V., Sibilia M., Ciruna B.C., Rossant J., Wagner E.F., and van der Kooy D. (1999) Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telen-cephalon. Dev. Biol. 208, 166-188.
26. Martens D.J., Tropepe V., and van Der Kooy D. (2000) Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebrain germinal zone. J. Neurosci. 20, 1085-1095.
27. Kallos M.S., Sen A., and Behie L.A. (2003) Large-scale expansion of mammalian neural stem cells: a review. Med. Biol. Eng. Comput. 41, 271-282.
28. Davis A.A. and Temple S. (1994) A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372, 263-266.
29. 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.
30. Suslov O.N., Kukekov V.G., Ignatova T.N., and Steindler D.A. (2002) Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proc. Natl. Acad. Sci. USA 99, 14,506-14,511.
31. Kalyani A.J., Mujtaba T., and Rao M.S. (1999) Expression of EGF receptor and FGF receptor isoforms during neuroepithelial stem cell differentiation. J. Neurobiol. 38, 207-224.
32. Qian X., Davis A.A., Goderie S.K., and Temple S. (1997) FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 18, 81-93.
33. Morrison S.J., White P.M., Zock C., and Anderson D.J. (1999) Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96, 737-749.
34. White P.M., Morrison S.J,. Orimoto K., Kubu C.J., Verdi J.M., and Anderson D.J. (2001) Neural crest stem cells undergo cell-intrinsic developmental changes in sensitivity to instructive differentiation signals. Neuron 29, 57-71.
35. Bixby S., Kruger G.M., Mosher J.T., Joseph N.M., and Morrison S.J. (2002) Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron 35, 643-656.
36. Uchida N., Buck D.W., He D., Reitsma M.J., Masek M., Phan T.V., et al. (2000) Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. USA 97, 14,720-14,725.
37. Rietze R.L., Valcanis H., Brooker G.F., Thomas T., Voss A.K., and Bartlett P.F. (2001) Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412, 736-739.
38. Cai J., Wu Y., Mirua T., Pierce J.L., Lucero M.T., Albertine K.H., et al. (2002) Properties of a fetal multipotent neural stem cell (NEP cell). Dev. Biol. 251, 221-240.
39. Leemhuis T., Yoder M.C., Grigsby S., Aguero B., Eder P., and Srour E.F. (1996) Isolation of primitive human bone marrow hematopoietic progenitor cells using Hoechst 33342 and Rhodamine 123. Exp. Hematol. 24, 1215-1224.
40. Radley J.M., Ellis S., Palatsides M., Williams B., and Bertoncello I. (1999) Ultrastructure of primitive hematopoietic stem cells isolated using probes of functional status. Exp. Hematol. 27, 365-369.
41. Kawaguchi A., Miyata T., Sawamoto K., Takashita N., Murayama A., Akamatsu W., et al. (2001) Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol. Cell. Neurosci. 17, 259-273.
42. Hilbig R., Rosner H., and Rahmann H. (1981) Phylogenetic recapitulation of brain ganglioside composition during ontogenetic development. Comp. Biochem. Physiol. 68, 301-305.
43. Hilbig R., Rosner H., Merz G., Segler-Stahl K., and Rahmann H. (1982) Developmental profiles of gangliosides in mouse and rat cerebral cortex. Wilhelm Roux's Archives 191, 281-284.
44. Yu R.K., Macala L.J., Taki T., Weinfield H.M., and Yu F.S. (1988) Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J. Neurochem. 50, 1825-1829.
45. Rogers T.B. and Snyder S.H. (1981) High affinity binding of tetanus toxin to mammalian brain membranes. J. Biol. Chem. 256, 2402-2407.
46. Fishman P.H. (1982) Role of membrane gangliosides in the binding and action of bacterial toxins. J. Membr. Biol. 69, 85-97.
47. Halpern J.L. and Loftus A. (1993) Characterization of the receptor-binding domain of tetanus toxin. J. Biol. Chem. 268, 11,188-11,192.
48. Shapiro R.E., Specht C.D., Collins B.E., Woods A.S., Cotter R.J., and Schnaar R.L. (1997) Identification of a ganglioside recognition domain of tetanus toxin using a novel ganglioside photoaffinity ligand. J. Biol. Chem. 272, 30,380-30,386.
49. Kundu S.K., Pleatman M.A., Redwine W.A., Boyd A.E., and Marcus D.M. (1983) Binding of monoclonal antibody A2B5 to gangliosides. Biochem. Biophys. Res. Commun. 116, 836-842.
50. Kasai N. and Yu R.K. (1983) The monoclonal antibody A2B5 is specific to ganglioside GQ1c. Brain Res. 277, 155-158.
51. Schwarz A. and Futerman A.H. (1996) The localization of gangliosides in neurons of the central nervous system: the use of anti-ganglioside antibodies. Biochim. Biophys. Acta 1286, 247-267.
52. Farrer R.G. and Quarles R.H. (1999) GT3 and its O-acetylated derivative are the principal A2B5-reactive gangliosides in cultured O2A lineage cells and are down-regulated along with O-acetyl GD3 during differentiation to oligodendrocytes. J. Neurosci. Res. 57, 371-380.
53. Raff M.C., Fields K.L., Hakomori S.I., Mirsky R., Pruss R.M., and Winter J. (1979) Cell-type-specific markers for distinguishing and studying neurons and the major classes of glial cells in culture. Brain Res. 174, 283-308.
54. Koulakoff A., Bizzini B., and Berwald-Netter Y. (1983) Neuronal acquisition of tetanus toxin binding sites: relationship with the last mitotic cycle. Dev. Biol. 100, 350-357.
55. Raff M.C., Abney E.R., Cohen J., Lindsay R., and Noble M. (1983) Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J. Neurosci. 3, 1289-1300.
56. Abney E.R., Williams B.P., and Raff M.C. (1983) Tracing the development of oligodendrocytes from precursor cells using monoclonal antibodies, fluorescence-activated cell sorting, and cell culture. Dev. Biol. 100, 166-171.
57. Behar T., McMorris F.A., Novotny E.A., Barker J.L., and Dubois-Dalcq M. (1988) Growth and differentiation properties of O-2A progenitors purified from rat cerebral hemispheres. J. Neurosci. Res. 21, 168-180.
58. Bottenstein J.E., Hunter S.F., and Seidel M. (1998) CNS neuronal cell line-derived factors regulate gliogenesis in neonatal rat brain cultures. J. Neurosci. Res. 20, 291-303.
59. Scolding N.J., Rayner P.J., and Compston D.A. (1999) Identification of A2B5-positive putative oligodendrocyte progenitor cells and A2B5-positive astrocytes in adult human white matter. Neuroscience 89, 1-4.
60. Shindler K.S. and Roth K.A. (1996) Cholera toxin binds to differentiating neurons in the developing murine basal ganglia. Brain Res. Dev. Brain. Res. 92, 199-210.
61. Blum A.S. and Barnstable C.J. (1987) O-acetylation of a cell-surface carbohydrate creates discrete molecular patterns during neural development. Proc. Natl. Acad. Sci. USA 84, 8716-8720.
62. Mendez-Otero R., Schlosshauer B., Barnstable C.J., and Constantine-Paton M. (1988) A developmentally regulated antigen associated with neural cell and process migration. J. Neurosci. 8, 564-579.
63. Santiago M.F., Berredo-Pinho M., Costa M.R., Gandra M., Cavalcante L.A., et al. (2001) Expression and function of ganglioside 9-O-acetyl GD3 in postmitotic granule cell development. Mol. Cell. Neurosci. 17, 488-499.
64. Miyakoshi L.M., Mendez-Otero R., and Hedin-Pereira C. (2001) The 9-O-acetyl GD3 gangliosides are expressed by migrating chains of subventricular zone neurons in vitro. Braz. J. Med. Biol. Res. 34, 669-673.
65. Maric D., Maric I., and Barker J.L. (1999) Flow cytometric strategies to study CNS development. In Neuromethods, vol. 33, (Boulton A.A., and Baker G.B., eds.), Humana Press, Totowa, NJ, pp. 287-318.
66. Maric D., Maric I., Chang Y.H., and Barker J.L. (2000) Stereotypic physiological properties emerge during early neuronal and glial lineage development in the embryonic rat neocortex. Cerebral Cortex 10, 729-747.
67. Maric D., Maric I., Chang Y.H., and Barker J.L. (2003) Prospective cell sorting of embryonic rat neural stem cells and neuronal and glial progenitors reveals selective effects of basic fibroblast growth factor and epidermal growth factor on self-renewal and differentiation. J. Neurosci. 23, 240-251.
68. Koopman G., Reutelingsperger C.P., Kuijten G.A., Keehnen R.M., Pals S.T., and van Oers M.H. (1994) Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84, 1415-1420.
69. Martin S.J., Reutelingsperger C.P., McGahon A.J., Rader J.A., van Schie R.C., LaFace D.M., et al. (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182, 1545-1556.
70. A receptor subunit co-expression by post-mitotic neocortical neurons correlates directly with cell buoyancy. Eur. J. Neurosci. 9, 507-522.
71. Maric D., Maric I., and Barker J.L. (1998) Buoyant density gradient fractionation and flow cytometric analysis of embryonic rat cortical neurons and progenitor cells. Methods 16, 247-259.
72. Geschwind D.H., Ou J., Easterday M.C., Dougherty J.D., Jackson R.L., Chen Z., et al. (2001) A genetic analysis of neural progenitor differentiation. Neuron 29, 325-339.
73. Terskikh A.V., Easterday M.C., Li L., Hood L., Kornblum H.I., Geschwind D.H., et al. (2001) From hematopoiesis to neuropoiesis: evidence of overlapping genetic programs. Proc. Natl. Acad. Sci. USA 98, 7934-7939.
74. Wright L.S., Li J., Caldwell M.A., Wallace K., Johnson J.A., and Svendsen C.N. (2003) Gene expression in human neural stem cells: effects of leukemia inhibitory factor. J. Neurochem. 86, 179-195.
75. Malatesta P., Hartfuss E., and Gotz M. (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253-5263.
76. Tamamaki N., Nakamura K., Okamoto K., and Kaneko T. (2001) Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci. Res. 41, 51-60.
77. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., and Kriegstein A.R. (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714-720.
78. Noctor S.C., Flint A.C., Weissman T.A., Wong W.S., Clinton B.K., and Kriegstein A.R. (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 22, 3161-3173.
79. Luo Y., Cai J., Liu Y., Xue H., Chrest F.J., Wersto R.P., et al. (2002) Microarray analysis of selected genes in neural stem and progenitor cells. J. Neurochem. 83, 1481-1497.
80. LoTurco J.J., Owens D.F., Heath M.J., Davis M.B., and Kriegstein A.R. (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287-1298.
81. Wang C., Pralong W.F., Schulz M.F., Rougon G., Aubry J.M., Pagliusi S., et al. (1996) Functional N-methyl-D-aspartate receptors in O-2A glial precursor cells: a critical role in regulating polysialic acid-neural cell adhesion molecule expression and cell migration. J. Cell. Biol. 135, 1565-1581.
82. A receptor inhibits the proliferative effects of bFGF in cortical progenitor cells. Eur. J. Neurosci. 9, 291-298.
83. Sah D.W., Ray J., and Gage F.H. (1997) Regulation of voltage- and ligand-gated currents in rat hippocampal progenitor cells in vitro. J. Neurobiol. 32, 95-110.
84. Cameron H.A., Hazel T.G., and McKay R.D. (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol. 36, 287-306.
85. Lauder J.M., Liu J., Devaud L., and Morrow A.L. (1998) GABA as a trophic factor for developing monoamine neurons. Perspect. Dev. Neurobiol. 5, 247-259.
86. Weiss E.R., Maness P., and Lauder J.M. (1998) Why do neurotransmitters act like growth factors? Perspect. Dev. Neurobiol. 5, 323-335.
87. - channels in vitro. J. Neurobiol. 35, 277-286.
88. Nguyen L., Rigo J.M., Rocher V., Belachew S., Malgrange B., Register B., et al. (2001) Neurotransmitters as early signals for central nervous system development. Cell Tissue Res. 305, 187-202.
89. Kalyani A.J., Piper D., Mujtaba T., Lucero M.T., and Rao M.S. (1998) Spinal cord neuronal precursors generate multiple neuronal phenotypes in culture. J. Neurosci. 18, 7856-7868.
90. 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.
91. Piper D.R., Mujtaba T., Keyoung H., Roy N.S., Goldman S.A., Rao M.S., et al. (2001) Identification and characterization of neuronal precursors and their progeny from human fetal tissue. J. Neurosci. Res. 66, 356-368.
92. Piper D.R., Mujtaba T., Rao M.S., and Lucero M.T. (2000) Immunocytochemical and physiological characterization of a population of cultured human neural precursors. J. Neurophysiol. 84, 534-548.
93. Ma W., Maric D., Li B.S., Hu Q., Andreadis J.D., Grant G.M., et al. (2000) Acetylcholine stimulates cortical precursor cell proliferation in vitro via muscarinic receptor activation and map kinase phosphorylation. Eur. J. Neurosci. 12, 1-4.
94. Schambra U.B., Sulik K.K., Petrusz P., and Lauder J.M. (1989) Ontogeny of cholinergic neurons in the mouse forebrain. J. Comp. Neurol. 288, 101-122.
95. Maric D., Maric I., and Barker J.L. (2000) Developmental changes in cell calcium homeostasis during neurogenesis of the embryonic rat cerebral cortex. Cerebral Cortex 10, 561-573.
96. Maric D., Maric I., and Barker J.L. (2000) Dual videomicroscopic imaging of membrane potential and cytosolic calcium of immunoidentified embryonic rat cortical cells. Methods 21, 335-347.
97. - channels. J. Neurosci. 21, 2343-2360.