Isolation of neural stem/progenitor cells by using EGF/FGF1 and FGF1B promoter-driven green fluorescence from embryonic and adult mouse brains

Molecular and Cellular Neuroscience

Volumn 41, Issue 3, 2009, Pages 348-363

  Lee, Don Ching ^a   Hsu, Yi Chao ^a   Chung, Yu Fen ^a   Hsiao, Chao Yang ^a   Chen, Su Liang ^a   Chen, Mei Shu ^a   Lin, Hua Kuo ^a   Chiu, Ing Ming ^a,b  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 1BETA; FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL RENEWAL; CONTROLLED STUDY; EMBRYO; MOUSE; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NERVE GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION;

ADULT STEM CELLS; ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL SEPARATION; EMBRYONIC STEM CELLS; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; NEURONS; PROMOTER REGIONS, GENETIC; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECOMBINANT FUSION PROTEINS; REGENERATION;

EID: 67349258579     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.04.010     Document Type: Article

References (117)

1. Alam K.Y., Frostholm A., Hackshaw K.V., Evans J.E., Rotter A., and Chiu I.M. Characterization of the 1B promoter of fibroblast growth factor 1 and its expression in the adult and developing mouse brain. J. Biol. Chem. 271 (1996) 30263-30271
2. Anchan R.M., Reh T.A., Angello J., Balliet A., and Walker M. EGF and TGF-alpha stimulate retinal neuroepithelial cell proliferation in vitro. Neuron 6 (1991) 923-936
3. Aubert J., Stavridis M.P., Tweedie S., O Reilly M., Vierlinger K., Li M., Ghazal P., Pratt T., Mason J.O., Roy D., and Smith A. . Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc. Natl. Acad. Sci. U. S. A 100 Suppl 1 (2003) 11836-11841
4. Barraud P., Stott S., Mollgard K., Parmar M., and Bjorklund A. In vitro characterization of a human neural progenitor cell coexpressing SSEA4 and CD133. J. Neurosci. Res. 85 (2007) 250-259
5. Bartlett P.F., Richards L.R., Kilpatrick T.J., Talman P.S., Bailey K.A., Brooker G.J., Dutton R., Koblar S., Nurcombe V., and Ford M. Regulation of neural precursor differentiation in the embryonic and adult forebrain. Clin. Exp. Pharmacol. Physiol 22 (1995) 559-562
6. Bjugstad K.B., Teng Y.D., Redmond Jr. D.E., Elsworth J.D., Roth R.H., Cornelius S.K., Snyder E.Y., and Sladek Jr. J.R. Human neural stem cells migrate along the nigrostriatal pathway in a primate model of Parkinson's disease. Exp. Neurol 211 (2008) 362-369
7. Brickman Y.G., Ford M.D., Small D.H., Bartlett P.F., and Nurcombe V. Heparan sulfates mediate the binding of basic fibroblast growth factor to a specific receptor on neural precursor cells. J. Biol. Chem. 270 (1995) 24941-24948
8. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., and McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 285 (1999) 754-756
9. Brustle O., Spiro A.C., Karram K., Choudhary K., Okabe S., and McKay R.D. In vitro-generated neural precursors participate in mammalian brain development. Proc. Natl. Acad. Sci. U. S. A 94 (1997) 14809-14814
10. Cao Q., Benton R.L., and Whittemore S.R. Stem cell repair of central nervous system injury. J. Neurosci. Res. 68 (2002) 501-510
11. Chen G.J., and Forough R. Fibroblast growth factors, fibroblast growth factor receptors, diseases, and drugs. Recent Pat Cardiovasc. Drug Discov. 1 (2006) 211-224
12. Chen L., and Deng C.X. Roles of FGF signaling in skeletal development and human genetic diseases. Front Biosci. 10 (2005) 1961-1976
13. Cheng H., Cao Y., and Olson L. Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 273 (1996) 510-513
14. Chipperfield H., Bedi K.S., Cool S.M., and Nurcombe V. Heparan sulfates isolated from adult neural progenitor cells can direct phenotypic maturation. Int. J. Dev. Biol. 46 (2002) 661-670
15. Chiu M., Touhalisky K., Liu Y., Yates A., and Frostholm A. Tumorigenesis in transgenic mice in which the SV40 T antigen is driven by the brain-specific FGF1 promoter. Oncogene 19 (2000) 6229-6239
16. Chiu M., Touhalisky K., and Baran C. Multiple controlling mechanisms of FGF1 gene expression through multiple tissue-specific promoters. Prog. Nucleic Acid Res. Mol. Biol. 70 (2001) 155-174
17. Chojnacki A., and Weiss S. Production of neurons, astrocytes and oligodendrocytes from mammalian CNS stem cells. Nat. Protoc. 3 (2008) 935-940
18. Chotani M.A., Payson R.A., Winkles J.A., and Chiu I.M. Human fibroblast growth factor 1 gene expression in vascular smooth muscle cells is modulated via an alternate promoter in response to serum and phorbol ester. Nucleic Acids Res. 23 (1995) 434-441
19. Ciruna B.G., Schwartz L., Harpal K., Yamaguchi T.P., and Rossant J. Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. Development 124 (1997) 2829-2841
20. Cordey M., Limacher M., Kobel S., Taylor V., and Lutolf M.P. Enhancing the reliability and throughput of neurosphere culture on hydrogel microwell arrays. Stem Cells 26 (2008) 2586-2594
21. Corti S., Nizzardo M., Nardini M., Donadoni C., Locatelli F., Papadimitriou D., Salani S., Del B.R., Ghezzi S., Strazzer S., Bresolin N., and Comi G.P. Isolation and characterization of murine neural stem/progenitor cells based on prominin-1 expression. Exp. Neurol 205 (2007) 547-562
22. D Amour K.A., and Gage F.H. Genetic and functional differences between multipotent neural and pluripotent embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A 100 Suppl 1 (2003) 11866-11872
23. Deng C.X., Wynshaw-Boris A., Shen M.M., Daugherty C., Ornitz D.M., and Leder P. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 8 (1994) 3045-3057
24. Drago J., Murphy M., Carroll S.M., Harvey R.P., and Bartlett P.F. Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc. Natl. Acad. Sci. U. S. A 88 (1991) 2199-2203
25. Fricker-Gates R.A., Lundberg C., and Dunnett S.B. Neural transplantation: restoring complex circuitry in the striatum. Restor. Neurol Neurosci. 19 (2001) 119-138
26. Fukuda H., Takahashi J., Watanabe K., Hayashi H., Morizane A., Koyanagi M., Sasai Y., and Hashimoto N. Fluorescence-activated cell sorting-based purification of embryonic stem cell-derived neural precursors averts tumor formation after transplantation. Stem Cells 24 (2006) 763-771
27. Gage F.H., Ray J., and Fisher L.J. Isolation, characterization, and use of stem cells from the CNS. Annu. Rev. Neurosci. 18 (1995) 159-192
28. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De V.S., Fiocco R., Foroni C., Dimeco F., and Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 64 (2004) 7011-7021
29. Galli R., Gritti A., and Vescovi A.L. Adult neural stem cells. Methods Mol. Biol. 438 (2008) 67-84
30. Gensburger C., Labourdette G., and Sensenbrenner M. Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett. 217 (1987) 1-5
31. Golmohammadi M.G., Blackmore D.G., Large B., Azari H., Esfandiary E., Paxinos G., Franklin K.B., Reynolds B.A., and Rietze R.L. Comparative analysis of the frequency and distribution of stem and progenitor cells in the adult mouse brain. Stem Cells 26 (2008) 979-987
32. Gritti A., Galli R., and Vescovi A.L. Clonal analyses and cryopreservation of neural stem cell cultures. Methods Mol. Biol. 438 (2008) 173-184
33. Gritti A., Parati E.A., Cova L., Frolichsthal P., Galli R., Wanke E., Faravelli L., Morassutti D.J., Roisen F., Nickel D.D., and Vescovi A.L. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci. 16 (1996) 1091-1100
34. Heo C., Chang K.A., Choi H.S., Kim H.S., Kim S., Liew H., Kim J.A., Yu E., Ma J., and Suh Y.H. Effects of the monomeric, oligomeric, and fibrillar Abeta42 peptides on the proliferation and differentiation of adult neural stem cells from subventricular zone. J. Neurochem. 102 (2007) 493-500
35. Hisajima H., Miyagawa T., Saito H., and Nishiyama N. Human acidic fibroblast growth factor has trophic effects on cultured neurons from multiple regions of brain and retina. Jpn. J. Pharmacol. 56 (1991) 495-503
36. Hisajima H., Saito H., Abe K., and Nishiyama N. Effects of acidic fibroblast growth factor on hippocampal long-term potentiation in fasted rats. J. Neurosci. Res. 31 (1992) 549-553
37. Hsu S.H., Su C.H., and Chiu I.M. A novel approach to align adult neural stem cells on micropatterned conduits for peripheral nerve regeneration: a feasibility study. Artif. Organs 33 (2009) 26-35
38. Hsu Y.C., Lee D.C., Chen S.L., Liao W.C., Lin J.W., Chiu W.T., and Chiu I.M. Brain-specific 1B promoter of FGF1 gene facilitates the isolation of neural stem/progenitor cells with self-renewal and multipotent capacities. Dev. Dyn. 238 (2009) 302-314
39. Hsu Y.C., Lee D.C., and Chiu I.M. Neural stem cells, neural progenitors, and neurotrophic factors. Cell Transplant. 16 (2007) 133-150
40. Huhn S.L., Yung Y., Cheshier S., Harsh G., Ailles L., Weissman I., Vogel H., and Tse V. Identification of phenotypic neural stem cells in a pediatric astroblastoma. J. Neurosurg. 103 (2005) 446-450
41. Imayoshi I., Ohtsuka T., Metzger D., Chambon P., and Kageyama R. Temporal regulation of Cre recombinase activity in neural stem cells. Genesis. 44 (2006) 233-238
42. Johe K.K., Hazel T.G., Muller T., Dugich-Djordjevic M.M., and McKay R.D. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10 (1996) 3129-3140
43. Johnson C.E., Crawford B.E., Stavridis M., Ten D.G., Wat A.L., Rushton G., Ward C.M., Wilson V., van Kuppevelt T.H., Esko J.D., Smith A., Gallagher J.T., and Merry C.L. Essential alterations of heparan sulfate during the differentiation of embryonic stem cells to Sox1-enhanced green fluorescent protein-expressing neural progenitor cells. Stem Cells 25 (2007) 1913-1923
44. Kalyani A., Hobson K., and Rao M.S. Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev. Biol. 186 (1997) 202-223
45. Kilpatrick T.J., and Bartlett P.F. Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron 10 (1993) 255-265
46. Kim S.U., Park I.H., Kim T.H., Kim K.S., Choi H.B., Hong S.H., Bang J.H., Lee M.A., Joo I.S., Lee C.S., and Kim Y.S. Brain transplantation of human neural stem cells transduced with tyrosine hydroxylase and GTP cyclohydrolase 1 provides functional improvement in animal models of Parkinson disease. Neuropathology. 26 (2006) 129-140
47. Klein S., Roghani M., and Rifkin D.B. Fibroblast growth factors as angiogenesis factors: new insights into their mechanism of action45. EXS 79 (1997) 159-192
48. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., and Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17 (1997) 5820-5829
49. Lee Y.S., Hsiao I., and Lin V.W. Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats. J. Neurotrauma 19 (2002) 1203-1216
50. Lillien L., and Cepko C. Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF alpha. Development 115 (1992) 253-266
51. Lin W.F., Chen C.J., Chang Y.J., Chen S.L., Chiu I.M., and Chen L. SH2B1beta enhances fibroblast growth factor 1 (FGF1)-induced neurite outgrowth through MEK-ERK1/2-STAT3-Egr1 pathway. Cell Signal (2009)
52. Lin Y.L., Jen J.C., Hsu S.H., and Chiu I.M. Sciatic nerve repair by microgrooved nerve conduits made of chitosan-gold nanocomposites. Surg. Neurol 70 Suppl 1 (2008) S1-18
53. Ma B.F., Liu X.M., Xie X.M., Zhang A.X., Zhang J.Q., Yu W.H., Zhang X.M., Li S.N., Lahn B.T., and Xiang A.P. Slower cycling of nestin-positive cells in neurosphere culture. Neuroreport 17 (2006) 377-381
54. Martens D.J., Tropepe V., and van Der K.D. 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 (2000) 1085-1095
55. McLeod M., Hong M., Sen A., Sadi D., Ulalia R., Behie L.A., and Mendez I. Transplantation of bioreactor-produced neural stem cells into the rodent brain. Cell Transplant. 15 (2006) 689-697
56. Merkle F.T., Mirzadeh Z., and varez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science 317 (2007) 381-384
57. Murayama A., Matsuzaki Y., Kawaguchi A., Shimazaki T., and Okano H. Flow cytometric analysis of neural stem cells in the developing and adult mouse brain. J. Neurosci. Res. 69 (2002) 837-847
58. Myers R.L., Chedid M., Tronick S.R., and Chiu I.M. Different fibroblast growth factor 1 (FGF-1) transcripts in neural tissues, glioblastomas and kidney carcinoma cell lines. Oncogene 11 (1995) 785-789
59. Myers R.L., Payson R.A., Chotani M.A., Deaven L.L., and Chiu I.M. Gene structure and differential expression of acidic fibroblast growth factor mRNA: identification and distribution of four different transcripts. Oncogene 8 (1993) 341-349
60. Myers R.L., Ray S.K., Eldridge R., Chotani M.A., and Chiu I.M. Functional characterization of the brain-specific FGF-1 promoter, FGF-1.B. J. Biol. Chem. 270 (1995) 8257-8266
61. Nurcombe V., Ford M.D., Wildschut J.A., and Bartlett P.F. Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science 260 (1993) 103-106
62. O'Keeffe F.E., Scott S.A., Tyers P., O'Keeffe G.W., Dalley J.W., Zufferey R., and Caldwell M.A. Induction of A9 dopaminergic neurons from neural stem cells improves motor function in an animal model of Parkinson's disease. Brain 131 (2008) 630-641
63. Okita K., Nakagawa M., Hyenjong H., Ichisaka T., and Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 322 (2008) 949-953
64. Ornitz D.M., Yayon A., Flanagan J.G., Svahn C.M., Levi E., and Leder P. Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol. Cell Biol. 12 (1992) 240-247
65. Orr-Urtreger A., Givol D., Yayon A., Yarden Y., and Lonai P. Developmental expression of two murine fibroblast growth factor receptors, flg and bek. Development 113 (1991) 1419-1434
66. Palmer T.D., Ray J., and Gage F.H. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell Neurosci. 6 (1995) 474-486
67. Palmer T.D., Takahashi J., and Gage F.H. The adult rat hippocampus contains primordial neural stem cells. Mol. Cell Neurosci. 8 (1997) 389-404
68. Panchision D.M., Chen H.L., Pistollato F., Papini D., Ni H.T., and Hawley T.S. Optimized flow cytometric analysis of central nervous system tissue reveals novel functional relationships among cells expressing CD133, CD15, and CD24. Stem Cells 25 (2007) 1560-1570
69. Park J.H., Ahn J.I., Kim S.Y., Park K.S., Lee Y.D., Yamaguchi M., and Chung H.J. Genetic modification does not affect the stemness of neural stem cells in nestin promoter-GFP transgenic mice. Neurosci. Lett. 421 (2007) 185-190
70. Parker M.A., Anderson J.K., Corliss D.A., Abraria E., Sidman R.L., Park K.I., Teng Y.D., Cotanche D.A., and Snyder E.Y. Expression profile of an operationally-defined neural stem cell clone. Exp. Neurol 194 (2005) 320-332
71. Patrie K.M., Botelho M.J., Franklin K., and Chiu I.M. Site-directed mutagenesis and molecular modeling identify a crucial amino acid in specifying the heparin affinity of FGF-1. Biochemistry 38 (1999) 9264-9272
72. Payson R.A., Canatan H., Chotani M.A., Wang W.P., Harris S.E., Myers R.L., and Chiu I.M. Cloning of two novel forms of human acidic fibroblast growth factor (aFGF) mRNA. Nucleic Acids Res. 21 (1993) 489-495
73. Pennartz S., Belvindrah R., Tomiuk S., Zimmer C., Hofmann K., Conradt M., Bosio A., and 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. 25 (2004) 692-706
74. Pruszak J., Sonntag K.C., Aung M.H., Sanchez-Pernaute R., and Isacson O. Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 25 (2007) 2257-2268
75. Ray J., and Gage F.H. Differential properties of adult rat and mouse brain-derived neural stem/progenitor cells. Mol. Cell Neurosci. 31 (2006) 560-573
76. Ray J., and Gage F.H. Spinal cord neuroblasts proliferate in response to basic fibroblast growth factor. J. Neurosci. 14 (1994) 3548-3564
77. Ray J., Peterson D.A., Schinstine M., and Gage F.H. Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc. Natl. Acad. Sci. U. S. A 90 (1993) 3602-3606
78. Reynolds B.A., Tetzlaff W., and Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12 (1992) 4565-4574
79. Reynolds B.A., and Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255 (1992) 1707-1710
80. Rietze R.L., and Reynolds B.A. Neural stem cell isolation and characterization. Methods Enzymol. 419 (2006) 3-23
81. Roghani M., Mansukhani A., Dell Era P., Bellosta P., Basilico C., Rifkin D.B., and Moscatelli D. Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding. J. Biol. Chem. 269 (1994) 3976-3984
82. Rydel R.E., and Greene L.A. Acidic and basic fibroblast growth factors promote stable neurite outgrowth and neuronal differentiation in cultures of PC12 cells. J. Neurosci. 7 (1987) 3639-3653
83. Sairanen M., Lucas G., Ernfors P., Castren M., and Castren E. Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J. Neurosci. 25 (2005) 1089-1094
84. Santa-Olalla J., and Covarrubias L. Epidermal growth factor (EGF), transforming growth factor-alpha (TGF-alpha), and basic fibroblast growth factor (bFGF) differentially influence neural precursor cells of mouse embryonic mesencephalon. J. Neurosci. Res. 42 (1995) 172-183
85. Shihabuddin L.S., Ray J., and Gage F.H. FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp. Neurol 148 (1997) 577-586
86. Shindo T., Matsumoto Y., Wang Q., Kawai N., Tamiya T., and Nagao S. Differences in the neuronal stem cells survival, neuronal differentiation and neurological improvement after transplantation of neural stem cells between mild and severe experimental traumatic brain injury. J. Med. Invest 53 (2006) 42-51
87. Singec I., Knoth R., Meyer R.P., Maciaczyk J., Volk B., Nikkhah G., Frotscher M., and Snyder E.Y. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat. Methods 3 (2006) 801-806
88. Smith R., Bagga V., and Fricker-Gates R.A. Embryonic neural progenitor cells: the effects of species, region, and culture conditions on long-term proliferation and neuronal differentiation. J. Hematother. Stem Cell Res. 12 (2003) 713-725
89. Smukler S.R., Runciman S.B., Xu S., and van der K.D. Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J. Cell Biol. 172 (2006) 79-90
90. Snyder E.Y., and Macklis J.D. Multipotent neural progenitor or stem-like cells may be uniquely suited for therapy for some neurodegenerative conditions. Clin. Neurosci. 3 (1995) 310-316
91. Stull N.D., and Iacovitti L. Acidic fibroblast growth factor and catecholamines synergistically up-regulate tyrosine hydroxylase activity in developing and damaged dopamine neurons in culture. J. Neurochem. 67 (1996) 1519-1524
92. Suh H., Consiglio A., Ray J., Sawai T., D Amour K.A., and Gage F.H. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1 (2007) 515-528
93. Takahashi K., Okita K., Nakagawa M., and Yamanaka S. Induction of pluripotent stem cells from fibroblast cultures. Nat. Protoc. 2 (2007) 3081-3089
94. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., and Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131 (2007) 861-872
95. Takahashi K., and Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006) 663-676
96. Tamaki S., Eckert K., He D., Sutton R., Doshe M., Jain G., Tushinski R., Reitsma M., Harris B., Tsukamoto A., Gage F., Weissman I., and Uchida N. Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. J. Neurosci. Res. 69 (2002) 976-986
97. Taupin P. Neural progenitor and stem cells in the adult central nervous system. Ann. Acad. Med. Singapore 35 (2006) 814-820
98. Teng Y.D., Mocchetti I., Taveira-DaSilva A.M., Gillis R.A., and Wrathall J.R. Basic fibroblast growth factor increases long-term survival of spinal motor neurons and improves respiratory function after experimental spinal cord injury. J. Neurosci. 19 (1999) 7037-7047
99. Thorns V., Licastro F., and Masliah E. Locally reduced levels of acidic FGF lead to decreased expression of 28-kda calbindin and contribute to the selective vulnerability of the neurons in the entorhinal cortex in Alzheimer's disease. Neuropathology. 21 (2001) 203-211
100. Thorns V., and Masliah E. Evidence for neuroprotective effects of acidic fibroblast growth factor in Alzheimer disease. J. Neuropathol. Exp. Neurol 58 (1999) 296-306
101. Tropepe V., Hitoshi S., Sirard C., Mak T.W., Rossant J., and van der K.D. Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30 (2001) 65-78
102. Tropepe V., Sibilia M., Ciruna B.G., Rossant J., Wagner E.F., and van der K.D. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev. Biol. 208 (1999) 166-188
103. Uchida N., Buck D.W., He D., Reitsma M.J., Masek M., Phan T.V., Tsukamoto A.S., Gage F.H., and Weissman I.L. Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. U. S. A 97 (2000) 14720-14725
104. Vescovi A.L., Galli R., and Gritti A. Clonal analyses and cryopreservation of neural stem cell cultures. Methods Mol. Biol. 198 (2002) 115-123
105. 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. 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 (1999) 71-83
106. Walicke P., Cowan W.M., Ueno N., Baird A., and Guillemin R. Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neurite extension. Proc. Natl. Acad. Sci. U. S. A 83 (1986) 3012-3016
107. Wanaka A., Milbrandt J., and Johnson Jr. E.M. Expression of FGF receptor gene in rat development. Development 111 (1991) 455-468
108. Wegner M., and Stolt C.C. From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci. 28 (2005) 583-588
109. Weise B., Janet T., and Grothe C. Localization of bFGF and FGF-receptor in the developing nervous system of the embryonic and newborn rat. J. Neurosci. Res. 34 (1993) 442-453
110. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A.C., and Reynolds B.A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16 (1996) 7599-7609
111. Weiss W.A., Israel M., Cobbs C., Holland E., James C.D., Louis D.N., Marks C., McClatchey A.I., Roberts T., Van D.T., Wetmore C., Chiu I.M., Giovannini M., Guha A., Higgins R.J., Marino S., Radovanovic I., Reilly K., and Aldape K. Neuropathology of genetically engineered mice: consensus report and recommendations from an international forum. Oncogene 21 (2002) 7453-7463
112. Werner S., Duan D.S., de V.C., Peters K.G., Johnson D.E., and Williams L.T. Differential splicing in the extracellular region of fibroblast growth factor receptor 1 generates receptor variants with different ligand-binding specificities. Mol. Cell Biol. 12 (1992) 82-88
113. Yamaguchi T.P., Harpal K., Henkemeyer M., and Rossant J. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev 8 (1994) 3032-3044
114. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 1 (2007) 39-49
115. Yamanaka S. Induction of pluripotent stem cells from mouse fibroblasts by four transcription factors. Cell Prolif 41 Suppl 1 (2008) 51-56
116. Yamanaka S. Pluripotency and nuclear reprogramming. Philos. Trans. R. Soc. Lond B Biol. Sci. 363 (2008) 2079-2087
117. Zhao C., Deng W., and Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 132 (2008) 645-660