Novel perspectives of neural stem cell differentiation: From neurotransmitters to therapeutics

Cytometry Part A

Volumn 75, Issue 1, 2009, Pages 38-53

  Trujillo, Cleber A ^a   Schwindt, Telma T ^b   Martins, Antonio H ^a   Alves, Janaína M ^b   Mello, Luiz Eugênio ^a,b   Ulrich, Henning ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Cell therapy; Growth factors; Neural stem cells; Neurogenesis; Neurospheres; Neurotransmitters

Indexed keywords

CHOLINERGIC RECEPTOR; GROWTH FACTOR; KALLIKREIN; KININ; NEUROPEPTIDE; NEUROTRANSMITTER; PURINERGIC RECEPTOR; CD133 ANTIGEN; CD24 ANTIGEN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR RECEPTOR; LEVODOPA; NEUROGENIN 2; NEUROPEPTIDE Y; NEUROTRANSMITTER RECEPTOR; ROLIPRAM; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; BIOLOGICAL MARKER;

AMYOTROPHIC LATERAL SCLEROSIS; CELL FATE; CELL ISOLATION; CELL LINEAGE; CELL MIGRATION; EPILEPSY; GLIA CELL; HUMAN; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NEUROLOGIC DISEASE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; ALLODYNIA; ASTROCYTE; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; FLUORESCENCE ACTIVATED CELL SORTING; MOLECULAR MECHANICS; NERVE CELL NETWORK; NEUROSCIENCE; OLIGODENDROGLIA; PARALYSIS; SINDBIS VIRUS; TEMPORAL LOBE EPILEPSY; TISSUE REPAIR; ANIMAL; CYTOLOGY; DRUG EFFECT; METABOLISM; MOUSE; NERVE CELL; PHYSIOLOGY; STEM CELL; STEM CELL TRANSPLANTATION;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; HUMANS; KALLIKREINS; KININS; MICE; NERVOUS SYSTEM DISEASES; NEURONS; NEUROTRANSMITTER AGENTS; RECEPTORS, CHOLINERGIC; RECEPTORS, PURINERGIC; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 59049106946     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.20666     Document Type: Review

References (151)

1. 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 1993;90:2074-2077.
2. McKay R. Stem cells in the central nervous system. Science 1997;276:66-71.
3. Gage FH. Mammalian neural stem cells. Science 2000;287:1433-1438.
4. Hamilton A. The division of differentiated cells in the central nervous system of the white rat. J Comp Neurol 1901;11:297-320.
5. Gross CG. Neurogenesis in the adult brain: Death of a dogma. Nat Rev Neurosci 2000;1:67-73.
6. Sidman RL, Miale IL, Feder N. Cell proliferation and migration in the primitive ependymal zone: An autoradiographic study of histogenesis in the nervous system. Exp Neurol 1959;1:322-333.
7. 3]-thymidine injection. J Comp Neurol 1961;116:325-347.
8. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124:319-335.
9. Altman J, Das GD. 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 1966;126:337-389.
10. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 1969;137:433-457.
11. Goldman SA, Nottebohm F. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 1983;80:2390-2394.
12. Paton JA, Nottebohm FN. Neurons generated in the adult brain are recruited into functional circuits. Science 1984;225:1046-1048.
13. Kaplan MS, Hinds JW. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 1977;197:1092-1094.
14. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-1710.
15. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J Neurosci 1996;16:2027-2033.
16. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005;28:223-250.
17. Rietze R, Poulin P, Weiss S. Mitotically active cells that generate neurons and astrocytes are present in multiple regions of the adult mouse hippocampus. J Comp Neurol 2000;424:397-408.
18. Gould E, Reeves AJ, Graziano MS, Gross CG. Neurogenesis in the neocortex of adult primates. Science 1999;286:548-552.
19. Gage FH, Ray J, Fisher LJ. Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 1995;18:159-192.
20. Frisen J, Johansson CB, Lothian C, Lendahl U. Central nervous system stem cells in
21. the embryo and adult. Cell Mol Life Sci 1998;54:935-945.
22. Gage FH. Cell therapy. Nature1998;392:18-24.
23. Bobbert M. Ethical questions concerning research on human embryos, embryonic stem cells and chimeras. Biotechnol J 2006;1:1352-1369.
24. Przyborski SA. Differentiation of human embryonic stem cells after transplantation in immune-deficient mice. Stem Cells 2005;23:1242-1250.
25. Takahashi KK, Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
26. Yu J, Yu J, Vodyanik M, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-1920.
27. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008;26:101-106.
28. Zuba-Surma EK, Kucia M, Ratajczak J, Ratajczak MZ. "Small stem cells" in adult tissues: Very small embryonic-like stem cells (VSELs) stand up! Cytometry A 2009;75A: in press. DOI: 10.1002/cyto.a.20665 (this issue).
29. Möbius-Winkler S, Höllriegel R, Schuler G, Adams V. Endothelial progenitor cells: Implications for cardiovascular disease. Cytometry A 2009;75A: in press. DOI: 10.1002/cyto.a.20669 (this issue).
30. Takács L, Tóth E, Berta A, Vereb G. Stem cells of the adult cornea: From cytometric markers to therapeutic applications. Cytometry A 2009;75A: in press. DOI: 10.1002/ cyto.a.20671 (this issue).
31. Challen GA, Boles N, Lin KK, Goodell MA. Mouse hematopoietic stem cell identification and analysis. Cytometry A 2009: in press. DOI: 10.1002/cyto.a.20674 (this issue).
32. Cattaneo E, McKay R. Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 1990;347:762-765.
33. Svendsen CN, Rosser AE. Neurones from stem cells? Trends Neurosci 1995;18:465-467.
34. McLaren FH, Svendsen CN, Van der Meide P, Joly E. Analysis of neural stem cells by flow cytometry: Cellular differentiation modifies patterns of MHC expression. J Neuroimmunol 2001;112:35-46.
35. Murayama A, Matsuzaki Y, Kawaguchi A, Shimazaki T, Okano H. Flow cytometric analysis of neural stem cells in the developing and adult mouse brain. J Neurosci Res 2002;69:837-847.
36. Johansson CB, Svensson M, Wallstedt L, Janson AM, Frisen J. Neural stem cells in the adult human brain. Exp Cell Res 1999;253:733-736.
37. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 2000;97:14720-14725.
38. Barraud P, Stott S, Mollgard K, Parmar M, Bjorklund A. In vitro characterization of a human neural progenitor cell coexpressing SSEA4 and CD133. J Neurosci Res 2007;85:250-259.
39. Panchision DM, Chen HL, Pistollato F, Papini D, Ni HT, Hawley TS. Optimized flow cytometric analysis of central nervous system tissue reveals novel functional relationships among cells expressing CD133, CD15, and CD24. Stem Cells 2007;25:1560-1570.
40. Hulspas R, Quesenberry PJ. Characterization of neurosphere cell phenotypes by flow cytometry. Cytometry 2000;40:245-250.
41. Capela A, Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002;35:865-875.
42. Martins AH, Alves JM, Trujillo CA, Schwindt TT, Barnabe GF, Motta FL, Guimaraes AO, Casarini DE, Mello LE, Pesquero JB, Ulrich H. Kinin-B2 receptor expression and activity during differentiation of embryonic rat neurospheres. Cytometry Part A 2008;73A:361-368.
43. Cai J, Wu Y, Mirua T, Pierce JL, Lucero MT, Albertine KH, Spangrude GJ, Rao MS. Properties of a fetal multipotent neural stem cell (NEP cell). Dev Biol 2002;251:221-240.
44. Brewer GJ, Torricelli JR. Isolation and culture of adult neurons and neurospheres. Nat Protoc 2007;2:1490-1498.
45. Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF- responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 1996;175:1-13.
46. Dunnett SB, Bjorklund A. Prospects for new restorative and neuroprotective treatments in Parkinson's disease. Nature 1999;399:A32-A39.
47. Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL. Turning brain into blood: A hematopoietic fate adopted by adult neural stem cells in vivo. Science 1999;283:534-537.
48. Clarke DL, Johansson CB, Wilbertz J, Veress B, Nilsson E, Karlstrom H, Lendahl U, Frisen J. Generalized potential of adult neural stem cells. Science 2000;288:1660-1663.
49. Doetsch F. A niche for adult neural stem cells. Curr Opin Genet Dev 2003;13:543-550.
50. Guillemot F. Cell fate specification in the mammalian telencephalon. Prog Neurobiol 2007;83:37-52.
51. Muotri AR, Gage FH. Generation of neuronal variability and complexity. Nature 2006;441:1087-1093.
52. Fishell G, Kriegstein AR. Neurons from radial glia: The consequences of asymmetric inheritance. Curr Opin Neurobiol 2003;13:34-41.
53. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 2004;131:3133-3145.
54. Song H, Stevens CF, Gage FH. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002;417:39-44.
55. Doetsch F. The glial identity of neural stem cells. Nat Neurosci 2003;6:1127-1134.
56. Cameron RS, Rakic P. Glial cell lineage in the cerebral cortex: A review and synthesis. Glia 1991;4:124-137.
57. Gotz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005;6:777-788.
58. Goldman S. Glia as neural progenitor cells. Trends Neurosci 2003;26:590-596.
59. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2001;2:287-293.
60. Madeddu P, Emanueli C, El-Dahr S. Mechanisms of disease: The tissue kallikreinkinin system in hypertension and vascular remodeling. Nat Clin Pract Nephrol 2007;3:208-221.
61. Sainz IM, Pixley RA, Colman RW. Fifty years of research on the plasma kallikreinkinin system: From protein structure and function to cell biology and in-vivo pathophysiology. Thromb Haemost 2007;98:77-83.
62. Pesquero JB, Bader M. Genetically altered animal models in the kallikrein-kinin system. Biol Chem 2006;387:119-126.
63. Schulze-Topphoff U, Prat A, Bader M, Zipp F, Aktas O. Roles of the kallikrein/kinin system in the adaptive immune system. Int Immunopharmacol 2008;8:155-160.
64. Iwadate H, Kudo M, Kizuki K. Expression of tissue kallikrein mRNA in developing rat brains. Can J Physiol Pharmacol 2002;80:245-248.
65. Xia CF, Yin H, Borlongan CV, Chao L, Chao J. Kallikrein gene transfer protects against ischemic stroke by promoting glial cell migration and inhibiting apoptosis. Hypertension 2004;43:452-459.
66. Xia CF, Yin H, Yao YY, Borlongan CV, Chao L, Chao J. Kallikrein protects against ischemic stroke by inhibiting apoptosis and inflammation and promoting angiogenesis and neurogenesis. Hum Gene Ther 2006;17:206-219.
67. Kizuki K, Iwadate H, Ookubo R. Growth-stimulating effect of kallikrein on rat neural stem cells. II. Immunocytochemical analysis and specificity of the enzyme for neural stem cells. Yakugaku Zasshi 2007;127:919-922.
68. Martins AH, Resende RR, Majumder P, Faria M, Casarini DE, Tarnok A, Colli W, Pesquero JB, Ulrich H. Neuronal differentiation of P19 embryonal carcinoma cells modulates kinin B2 receptor gene expression and function. J Biol Chem 2005;280:19576-19586.
69. Huang Z, Yu J, Toselli P, Bhawan J, Sudireddy V, Taylor L, Polgar P. Angiotensin II type 1 and bradykinin B2 receptors expressed in early stage epithelial cells derived from human embryonic stem cells. J Cell Physiol 2007;211:816-825.
70. Wainer BH, Bolam JP, Freund TF, Henderson Z, Totterdell S, Smith AD. Cholinergic synapses in the rat brain: A correlated light and electron microscopic immunohisto- chemical study employing a monoclonal antibody against choline acetyltransferase. Brain Res 1984;308:69-76.
71. Frotscher M, Schlander M, Leranth C. Cholinergic neurons in the hippocampus. A combined light- and electron-microscopic immunocytochemical study in the rat. Cell Tissue Res 1986;246:293-301.
72. Blennow K, de Leon MJ, Zetterberg H. Alzheimer's disease. Lancet 2006;368:387-403.
73. Balon R. Physical illness and schizophrenia. A review of the evidence. Ann Clin Psychiatry 2008;20:181-182.
74. Picciotto MR, Zoli M. Neuroprotection via nAChRs: The role of nAChRs in neurodegenerative disorders such as Alzheimer's and Parkinson's disease. Front Biosci 2008;13:492-504.
75. Etienne M, Weimer LH. Immune-mediated autonomic neuropathies. Curr Neurol Neurosci Rep 2006;6:57-64.
76. Barrantes FJ, Aztiria E, Rauschemberger MB, Vasconsuelo A. The neuronal nicotinic acetylcholine receptor in some hereditary epilepsies. Neurochem Res 2000;25:583-590.
77. Pauly JR, Charriez CM, Guseva MV, Scheff SW. Nicotinic receptor modulation for neuroprotection and enhancement of functional recovery following brain injury or disease. Ann NY Acad Sci 2004;1035:316-334.
78. Zoli M, Le Novere N, Hill JA Jr, Changeux JP. Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. J Neurosci 1995;15(3, Pt 1):1912-1939.
79. Atluri P, Fleck MW, Shen Q, Mah SJ, Stadfelt D, Barnes W, Goderie SK, Temple S, Schneider AS. Functional nicotinic acetylcholine receptor expression in stem and progenitor cells of the early embryonic mouse cerebral cortex. Dev Biol 2001;240:143-156.
80. Shingo AS, Kito S. Effects of nicotine on neurogenesis and plasticity of hippocampal neurons. J Neural Transm 2005;112:1475-1478.
81. Huang LZ, Abbott LC, Winzer-Serhan UH. Effects of chronic neonatal nicotine exposure on nicotinic acetylcholine receptor binding, cell death and morphology in hippocampus and cerebellum. Neuroscience 2007;146:1854-1868.
82. Williams BP, Milligan CJ, Street M, Hornby FM, Deuchars J, Buckley NJ. Transcription of the M1 muscarinic receptor gene in neurons and neuronal progenitors of the embryonic rat forebrain. J Neurochem 2004;88:70-77.
83. Zhou C, Wen ZX, Shi DM, Xie ZP. Muscarinic acetylcholine receptors involved in the regulation of neural stem cell proliferation and differentiation in vitro. Cell Biol Int 2004;28:63-67.
84. Loreti S, Vilaro MT, Visentin S, Rees H, Levey AI, Tata AM. Rat Schwann cells express M1-M4 muscarinic receptor subtypes. J Neurosci Res 2006;84:97-105.
85. Molina-Holgado E, Khorchid A, Liu HN, Almazan G. Regulation of muscarinic receptor function in developing oligodendrocytes by agonist exposure. Br J Pharmacol 2003;138:47-56.
86. Wu EH, Wong YH. Activation of muscarinic M4 receptor augments NGF-induced pro-survival Akt signaling in PC12 cells. Cell Signal 2006;18:285-293.
87. Parnas D, Linial M. Cholinergic properties of neurons differentiated from an embryonal carcinoma cell-line (P19). Int J Dev Neurosci 1995;13:767-781.
88. Resende RR, Gomes KN, Adhikari A, Britto LR, Ulrich H. Mechanism of acetylcholine-induced calcium signaling during neuronal differentiation of P19 embryonal carcinoma cells in vitro. Cell Calcium 2008;43:107-121.
89. Resende RR, Alves AS, Britto LR, Ulrich H. Role of acetylcholine receptors in proliferation and differentiation of P19 embryonal carcinoma cells. Exp Cell Res 2008;314:1429-1443.
90. Drury AN, Szent-Gyorgyi A. The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart. J Physiol 1929;68:213-237.
91. Burnstock G. Purinergic nerves. Pharmacol Rev 1972;24:509-581.
92. Burnstock G. A basis for distinguishing two types of purinergic receptor. In: Straub RW, Bolis L, editor. Cell Membrane Receptors for Drugs and Hormones: A Multidisciplinary Approach. New York: Raven Press; 1978. pp 107-118.
93. Burnstock GKC. Is there a basis for distinguishing two types of P2-purinoceptor? Gen Pharmacol 1985;16:433-440.
94. Majumder P, Trujillo CA, Lopes CG, Resende RR, Gomes KN, Yuahasi KK, Britto LR, Ulrich H. New insights into purinergic receptor signaling in neuronal differentiation, neuroprotection, and brain disorders. Purinergic Signal 2007;3:317-331.
95. Laasberg T. Ca2(+)-mobilizing receptors of gastrulating chick embryo. Comp Biochem Physiol C 1990;97:9-12.
96. Cheung KK, Chan WY, Burnstock G. Expression of P2X purinoceptors during rat brain development and their inhibitory role on motor axon outgrowth in neural tube explant cultures. Neuroscience 2005;133:937-945.
97. da Silva RL, Resende RR, Ulrich H. Alternative splicing of P2X6 receptors in developing mouse brain and during in vitro neuronal differentiation. Exp Physiol 2007;92:139-145.
98. Hogg RC, Chipperfield H, Whyte KA, Stafford MR, Hansen MA, Cool SM, Nurcombe V, Adams DJ. Functional maturation of isolated neural progenitor cells from the adult rat hippocampus. Eur J Neurosci 2004;19:2410-2420.
99. Zimmermann H. Nucleotide signaling in nervous system development. Pflugers Arch 2006;452:573-588.
100. Lin JH, Takano T, Arcuino G, Wang X, Hu F, Darzynkiewicz Z, Nunes M, Goldman SA, Nedergaard M. Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev Biol 2007;302:356-366.
101. Resende RR, Britto LR, Ulrich H. Pharmacological properties of purinergic receptors and their effects on proliferation and induction of neuronal differentiation of P19 embryonal carcinoma cells. Int J Dev Neurosci 2008;26:763-777.
102. Resende RR, Majumder P, Gomes KN, Britto LR, Ulrich H. P19 embryonal carcinoma cells as in vitro model for studying purinergic receptor expression and modulation of N-methyl-D-aspartate-glutamate and acetylcholine receptors during neuronal differentiation. Neuroscience 2007;146:1169-1181.
103. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 2004;429:523-530.
104. Baynash AG, Hosoda K, Giaid A, Richardson JA, Emoto N, Hammer RE, Yanagisawa M. Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons. Cell 1994;79:1277-1285.
105. Willars GB, Müller-Esterl W, Nahorski SR. Receptor phosphorylation does not mediate cross talk between muscarinic M and bradykinin B receptors. Am J Physiol 1999;277:C859-C869.
106. 2+ activation in a neuroblastoma x glioma hybrid cell line. J Neurochem 1994;62:890-897.
107. Rong Zhou J, Shirasaki T, Soeda F, Takahama K. Potentiation of nicotinic currents by bradykinin in the paratracheal ganglia neurons of rats. Eur J Pharmacol 2006;531:96-102.
108. Patti L, Raiteri L, Grilli M, Parodi M, Raiteri M, Marchi M. P2X(7) receptors exert a permissive role on the activation of release-enhancing presynaptic alpha7 nicotinic receptors co-existing on rat neocortex glutamatergic terminals. Neuropharmacology 2006;50:705-713.
109. Takahashi J, Palmer TD, Gage FH. Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J Neurobiol 1999;38:65-81.
110. Wang X, Li X, Wang K, Zhou H, Xue B, Li L, Wang X. Forskolin cooperating with growth factor on generation of dopaminergic neurons from human fetal mesencephalic neural progenitor cells. Neurosci Lett 2004;362:117-121.
111. Rajan P, Panchision DM, Newell LF, McKay RD. BMPs signal alternately through a SMAD or FRAP-STAT pathway to regulate fate choice in CNS stem cells. J Cell Biol 2003;161:911-921.
112. Asakura K, Hunter SF, Rodriguez M. Effects of transforming growth factor-beta and platelet-derived growth factor on oligodendrocyte precursors: Insights gained from a neuronal cell line. J Neurochem 1997;68:2281-2290.
113. Gibney SM, McDermott KW. Differentiation of oligodendrocytes in neurospheres derived from embryonic rat brain using growth and differentiation factors. J Neurosci Res 2007;85:1912-1920.
114. Walker TL, White A, Black DM, Wallace RH, Sah P, Bartlett PF. Latent stem and progenitor cells in the hippocampus are activated by neural excitation. J Neurosci 2008;28:5240-5247.
115. de Alvaro C, Martinez N, Rojas JM, Lorenzo M. Sprouty-2 overexpression in C2C12 cells confers myogenic differentiation properties in the presence of FGF2. Mol Biol Cell2005;16:4454-4461.
116. Vaccarino FM, Ganat Y, Zhang Y, Zheng W. Stem cells in neurodevelopment and plasticity. Neuropsychopharmacology2001;25:805-815.
117. Thuret S, Moon LD, Gage FH. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 2006;7:628-643.
118. Hofstetter CP, Holmstrom NA, Lilja JA, Schweinhardt P, Hao J, Spenger C, Wiesenfeld-Hallin Z, Kurpad SN, Frisen J, Olson L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 2005;8:346-353.
119. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995;12:1-21.
120. Macias MY, Syring MB, Pizzi MA, Crowe MJ, Alexanian AR, Kurpad SN. Pain with no gain: Allodynia following neural stem cell transplantation in spinal cord injury. Exp Neurol 2006;201:335-348.
121. Deshpande DM, Kim YS, Martinez T, Carmen J, Dike S, Shats I, Rubin LL, Drummond J, Krishnan C, Hoke A, et al. Recovery from paralysis in adult rats using embryonic stem cells. Ann Neurol 2006;60:32-44.
122. Gill SS, Patel NK, Hotton GR, O'Sullivan K, McCarter R, Bunnage M, Brooks DJ, Svendsen CN, Heywood P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat Med 2003;9:589-595.
123. Patel NK, Bunnage M, Plaha P, Svendsen CN, Heywood P, Gill SS. Intraputamenal infusion of glial cell line-derived neurotrophic factor in PD: A two-year outcome study. Ann Neurol 2005;57:298-302.
124. Peck P. AMGEN decision to halt GDNF clinical trials and withdraw the drug triggers protest from researchers and patients. Neurol Today 2005;5:4,7,24.
125. Capowski EE, Schneider BL, Ebert AD, Seehus CR, Szulc J, Zufferey R, Aebischer P, Svendsen CN. Lentiviral vector-mediated genetic modification of human neural progenitor cells for ex vivo gene therapy. J Neurosci Methods 2007;163:338-349.
126. Wernig M, Zhao JP, Pruszak J, Hedlund E, Fu D, Soldner F, Broccoli V, Constantine- Paton M, Isacson O, Jaenisch R. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci USA 2008;105:5856-5861.
127. Cleveland DW, Rothstein JD. From Charcot to Lou Gehrig: Deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2001;2:806-819.
128. Boillee S, Vande Velde C, Cleveland DW. ALS: A disease of motor neurons and their nonneuronal neighbors. Neuron 2006;52:39-59.
129. Andersen PM, Sims KB, Xin WW, Kiely R, O'Neill G, Ravits J, Pioro E, Harati Y, Brower RD, Levine JS, Heinicke HU, Seltzer W, Boss M, Brown RH Jr. Sixteen novel mutations in the Cu/Zn superoxide dismutase gene in amyotrophic lateral sclerosis: A decade of discoveries, defects and disputes. Amyotroph Lateral Scler Other Motor Neuron Disord 2003;4:62-73.
130. Hall ED, Oostveen JA, Gurney ME. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 1998;23:249-256.
131. Howland DS, Liu J, She Y, Goad B, Maragakis NJ, Kim B, Erickson J, KulikJ, DeVito L, Psaltis G, DeGennaro LJ, Cleveland DW, Rothstein JD. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant- mediated amyotrophic lateral sclerosis (ALS). Proc Natl Acad Sci USA 2002;99:1604-1609.
132. Suzuki M, McHugh J, Tork C, Shelley B, Klein SM, Aebischer P, Svendsen CN. GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS. PLoS ONE 2007;2:e689.
133. Cavalheiro EA. The pilocarpine model of epilepsy. Ital J Neurol Sci 1995;16:33-37.
134. Covolan L, Mello LE. Assessment of the progressive nature of cell damage in the pilocarpine model of epilepsy. Braz J Med Biol Res 2006;39:915-924.
135. Chu K, Kim M, Jung KH, Jeon D, Lee ST, Kim J, Jeong SW, Kim SU, Lee SK, Shin HS, et al. Human neural stem cell transplantation reduces spontaneous recurrent seizures following pilocarpine-induced status epilepticus in adult rats. Brain Res 2004;1023:213-221.
136. Noe F, Nissinen J, Pitkanen A, Gobbi M, Sperk G, During M, Vezzani A. Gene therapy in epilepsy: The focus on NPY. Peptides2007;28:377-383.
137. Li T, Steinbeck JA, Lusardi T, Koch P, Lan JQ, Wilz A, Segschneider M, Simon RP, Brustle O, Boison D. Suppression of kindling epileptogenesis by adenosine releasing stem cell-derived brain implants. Brain 2007;130 (Pt5):1276-1288.
138. Shetty AK, Hattiangady B. Concise review: Prospects of stem cell therapy for temporal lobe epilepsy. Stem Cells 2007;25:2396-2407.
139. Lee A, Kessler JD, Read TA, Kaiser C, Corbeil D, Huttner WB, Johnson JE, Wechsler-Reya RJ. Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 2005;8:723-729.
140. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 1999;96:25-34.
141. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 2001;412:736-739.
142. Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, Biancotti JC, Hutnick L, Krueger RC Jr, Fan G, et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA2008;105:1026-1031.
143. Morrison SJ, White PM, Zock C, Anderson DJ. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 1999;96:737-749.
144. Piper DR, Mujtaba T, Rao MS, Lucero MT. Immunocytochemical and physiological characterization of a population of cultured human neural precursors. J Neurophysiol 2000;84:534-548.
145. Pennartz S, Belvindrah R, Tomiuk S, Zimmer C, Hofmann K, Conradt M, Bosio A, Cremer H. Purification of neuronal precursors from the adult mouse brain: Comprehensive gene expression analysis provides new insights into the control of cell migration, differentiation, and homeostasis. Mol Cell Neurosci 2004;25:692-706.
146. Marmur R, Mabie PC, Gokhan S, Song Q, Kessler JA, Mehler MF. Isolation and developmental characterization of cerebral cortical multipotent progenitors. Dev Biol 1998;204:577-591.
147. Klassen H, Schwartz MR, Bailey AH, Young MJ. Surface markers expressed by multipotent human and mouse neural progenitor cells include tetraspanins and non- protein epitopes. Neurosci Lett 2001;312:180-182.
148. Diers-Fenger M, Kirchhoff F, Kettenmann H, Levine JM, Trotter J. AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: Isolation, differentiation, and association with radial glia. Glia 2001;34:213-228.
149. Tracy E, Aldrink J, Panosian J, Beam D, Thacker J, Reese M, Kurtzberg J. Isolation of oligodendrocyte-like cells from human umbilical cord blood. Cytotherapy2008;10:1-8.
150. Pruszak J, Sonntag KC, Aung MH, Sanchez-Pernaute R, Isacson O. Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 2007;25:2257-2268.
151. Stainier DY, Bilder DH, Gilbert W. The B30 ganglioside is a cell surface marker for neural crest-derived neurons in the developing mouse. Dev Biol 1991;144:177-188.