Maintenance and neuronal cell differentiation of neural stem cells C17.2 correlated to medium availability sets design criteria in microfluidic systems

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Wang, Bu ^a   Jedlicka, Sabrina ^a   Cheng, Xuanhong ^a  

^a Lehigh University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; BETA TUBULIN 3; MICROTUBULE ASSOCIATED PROTEIN 2; UNCLASSIFIED DRUG; CULTURE MEDIUM; DIMETICONE; MICROTUBULE ASSOCIATED PROTEIN; MTAP2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; CULTURE MEDIUM; IMMUNOCYTOCHEMISTRY; MICROFLUIDIC ANALYSIS; MICROFLUIDICS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEURAL STEM CELL; NEURITE LENGTH; NONHUMAN; PROCESS DESIGN; PROTEIN EXPRESSION; STEM CELL CULTURE; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CHEMISTRY; CYTOLOGY; DEVICES; DRUG EFFECTS; EQUIPMENT DESIGN; METABOLISM; NERVE CELL; PHARMACOLOGY; PHENOTYPE; PROCEDURES; REPRODUCIBILITY; STAINING;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CULTURE MEDIA; DIMETHYLPOLYSILOXANES; EQUIPMENT DESIGN; MICE; MICROFLUIDICS; MICROTUBULE-ASSOCIATED PROTEINS; NEURAL STEM CELLS; NEURONS; PHENOTYPE; REPRODUCIBILITY OF RESULTS; STAINING AND LABELING;

EID: 84907943789     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109815     Document Type: Article

References (114)

1. Zhao CM, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132 (4) 645-660.
2. Bjorklund LM, Sanchez-Pernaute R, Chung SM, Andersson T, Chen IYC, et al. (2002) Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model (2002). Proceedings of the National Academy of Sciences of the United States of America 99 (4) 2344- 2349.
3. Kim JH, Auerbach JM, Rodriguez-Gomez JA, Velasco I, Gavin D et al. (2002) Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418 (6893) 50-56.
4. Bjorklund A, Lindvall O (2003) Cell replacement therapies for central nervous system disorders. Nat. Neurosci.3 (6) 537-544.
5. Wernig M, Zhao JP, Pruszak J, Hedlund E, Fu DD, et al. (2008) Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proceedings of the National Academy of Sciences of the United States of America 105 (15) 5856-5861.
6. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, et al. (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110 (4) 429-441.
7. Chen JL, Li Y, Wang L, Zhang ZG, Lu DY, et al. (2001) Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32 (4) 1005-1011.
8. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med.8 (9) 963-970.
9. Yang M, Stull ND, Berk MA, Snyder EY, Iacovitti L (2002) Neural stem cells spontaneously express dopaminergic traits after transplantation into the intact or 6-hydroxydopamine-lesioned rat. Exp. Neurol. 177 (1) 50-60.
10. Snyder EY, Deitcher DL, Walsh C, Arnoldaldea S, Hartwieg EA, et al. (1992) Multipotent Neural Cell-Lines Can Engraft and Participate in Development of Mouse Cerebellum. Cell 68 (1) 33-51.
11. Ryu MY, Lee MA, Ahn YH, Kim KS, Yoon SH, et al. (2005) Brain transplantation of neural stem cells cotransduced with tyrosine hydroxylase and GTP cyclohydrolase 1 in parkinsonian rats. Cell Transplant. 14 (4) 193-202.
12. Liu WG, Lu GQ, Li BA, Chen SD (2007) Dopaminergic neuroprotection by neurturin-expressing c17.2 neural stem cells in a rat model of Parkinson's disease. Parkinsonism Relat. Disord. 13 (2) 77-88.
13. Akerud P, Canals JM, Snyder EY, Arenas E (2001) Neuroprotection through delivery of glial cell line-derived neurotrophic factor by neural stem cells in a mouse model of Parkinson's disease. Journal of Neuroscience 21 (20) 8108- 8118.
14. Pineda JR, Rubio N, Akerud P, Urban N, Badimon L, et al. (2007) Neuroprotection by GDNF-secreting stem cells in a Huntington's disease model: optical neuroimage tracking of brain-grafted cells. Gene Ther. 14 (2) 118-128.
15. Sinden JD, RashidDoubell F, Kershaw TR, Nelson A, Chadwick A, et al. (1997) A Recovery of spatial learning by grafts of a conditionally immortalized hippocampal neuroepithelial cell line into the ischaemia-lesioned hippocampus. Neuroscience 81 (3) 599-608.
16. Zhu JM, Zhao YY, Chen SD, Zhang WH, Lou L, et al. (2011) Functional Recovery after Transplantation of Neural Stem Cells Modified by Brainderived Neurotrophic Factor in Rats with Cerebral Ischaemia. J. Int. Med. Res. 39 (2) 488-498.
17. Singh A, Suri S, Lee T, Chilton JM, Cooke MT, et al. (2013) Adhesion strength-based label-free isolation of human pluripotent stem cells. Nature Methods 10 (5) 4382+.
18. Loewke KE, Camarillo DB, Piyawattanametha W, Mandella MJ, Contag CH, et al. (2011) In Vivo Micro-Image Mosaicing. IEEE Trans. Biomed. Eng. 58 (1) 159-171.
19. Solanki A, Chueng STD, Yin PT, Kappera R, Chhowalla M, et al. (2013) Axonal Alignment and Enhanced Neuronal Differentiation of Neural Stem Cells on Graphene-Nanoparticle Hybrid Structures. Adv. Mater. 25 (38) 5477- 5482.
20. Jung DJ, Minami I, Patel S, Lee J, Jiang B, et al. (2012) Incorporation of functionalized gold nanoparticles into nanofibers for enhanced attachment and differentiation of mammalian cells. J. Nanobiotechnol. 10 10.
21. Cimetta E, Figallo E, Cannizzaro C, Elvassore N, Vunjak-Novakovic G (2009) Micro-bioreactor arrays for controlling cellular environments: Design principles for human embryonic stem cell applications. Methods 47 (2) 81-89.
22. Park JY, Kim SK, Woo DH, Lee E, Kim JH, et al. (2009) Differentiation of Neural Progenitor Cells in a Microfluidic Chip-Generated Cytokine Gradient. Stem Cells 27 (11) 2646-2654.
23. Park JY, Takayama S, Lee SH (2010) Regulating microenvironmental stimuli for stem cells and cancer cells using microsystems. Integrative Biology 2 (5-6) 229-240.
24. Yu HM, Meyvantsson I, Shkel IA, Beebe DJ (2005) Diffusion dependent cell behavior in microenvironments. Lab Chip 5 (10) 1089-1095.
25. Zhang H, Liu KK (2008) Optical tweezers for single cells Journal of the Royal Society Interface 5 (24) 671-690.
26. Cai L, Friedman N, Xie XS (2006) Stochastic protein expression in individual cells at the single molecule level. Nature 440 (7082) 358-362.
27. Warren L, Bryder D, Weissman IL, Quake SR (2006) Transcription factor profiling in individual hematopoietic progenitors by digital RTPCR. Proceedings of the National Academy of Sciences of the United States of America 103 (47) 17807-17812.
28. Zhong JF, Chen Y, Marcus JS, Scherer A, Quake SR, et al. (2008) A microfluidic processor for gene expression profiling of single human embryonic stem cells. Lab Chip 8 (1) 68-74.
29. Kraus T, Verpoorte E, Linder V, Franks W, Hierlemann A, et al. (2006) Characterization of a microfluidic dispensing system for localised stimulation of cellular networks. Lab Chip 6 (2) 218-229.
30. Park TH, Shuler ML (2003) Integration of cell culture and microfabrication technology. Biotechnol. Prog. 19 (2) 243-253.
31. Rajaraman S, Choi SO, Shafer RH, Ross JD, Vukasinovic J, et al. (2007) Microfabrication technologies for a coupled three-dimensional microelectrode microfluidic array. J. Micromech. Microeng. 17 (1) 163-171.
32. Ellison D, Munden A, Levchenko A (2009) Computational model and microfluidic platform for the investigation of paracrine and autocrine signaling in mouse embryonic stem cells. Mol. Biosyst. 5 (9) 1004-1012.
33. Wan CR, Chung S, Kamm RD (2011) Differentiation of Embryonic Stem Cells into Cardiomyocytes in a Compliant Microfluidic System. Annals of Biomedical Engineering 39 (6) 1840-1847.
34. Hemmingsen M, Vedel S, Skafte-Pedersen P, Sabourin D, Collas P, et al. (2013) The Role of Paracrine and Autocrine Signaling in the Early Phase of Adipogenic Differentiation of Adiposederived Stem Cells. PLoS One 8 (5) 14.
35. Khetani SR, Bhatia SN (2006) Engineering tissues for in vitro applications. Curr. Opin. Biotechnol. 17 (5) 524-531.
36. Trkov S, Eng G, Di Liddo R, Parnigotto P, Vunjak-Novakovic G (2010) Micropatterned three-dimensional hydrogel system to study human endothelial - mesenchymal stem cell interactions. J. Tissue Eng. Regen. Med. 4 (3) 205- 215.
37. Zhong WL, Tian K, Zheng XF, Li LN, Zhang WG, et al. (2013) Mesenchymal Stem Cell and Chondrocyte Fates in a Multishear Microdevice Are Regulated by Yes-Associated Protein. Stem Cells Dev. 22 (14) 2083-2093.
38. Labeed FH, Lu J, Mulhall HJ, Marchenko SA, Hoettges KF, et al. (2011) Biophysical Characteristics Reveal Neural Stem Cell Differentiation Potential. PLoS One 6 (9) e25458.
39. Huang CP, Lu J, Seon H, Lee AP, Flanagan LA, Kim, et al. (2009) Engineering microscale cellular niches for three-dimensional multicellular co-cultures. Lab Chip 9 (12) 1740-1748.
40. Flanagan LA, Lu J, Wang L, Marchenko SA, Jeon NL, et al. (2008) Unique dielectric properties distinguish stem cells and their differentiated progeny. Vol. 26 p 656-65.
41. King KR, Wang S, Jayaraman A, Yarmush L, Toner M (2008) Microfluidic flow-encoded switching for parallel control of dynamic cellular microenvironments. Lab Chip 8 (1) 107-116.
42. King KR, Wang SH, Irimia D, Jayaraman A, Toner M, et al. (2007) A highthroughput microfluidic real-time gene expression living cell array. Lab Chip 7 (1) 77-85.
43. Huang NF, Dewi RE, Okogbaa J, Lee JC, JalilRufaihah A, et al. (2013) Chemotaxis of human induced pluripotent stem cell-derived endothelial cells. Am. J. Transl. Res. 5 (5) 510-U96.
44. Shamloo A, Manchandia M, Ferreira M, Mani M, Nguyen C, Jahn T, et al. (2013) Complex chemoattractive and chemorepellent Kit signals revealed by direct imaging of murine mast cells in microfluidic gradient chambers. Integrative Biology 5 (8) 1076-1085.
45. Tavana H, Mosadegh B, Zamankhan P, Grotberg JB, Takayama S (2011) Microprinted Feeder Cells Guide Embryonic Stem Cell Fate. Biotechnol. Bioeng. 108 (10) 2509-2516.
46. Chung C, Pruitt BL, Heilshorn SC (2013) Spontaneous cardiomyocyte differentiation of mouse embryoid bodies regulated by hydrogel crosslink density. Biomaterials Science 1 (10) 1082-1090.
47. Blagovic K, Kim LLY, Voldman J (2011) Microfluidic Perfusion for Regulating Diffusible Signaling in Stem Cells. PLoS One 6 (8) 11.
48. Chung BG, Flanagan LA, Rhee SW, Schwartz PH, Lee AP, et al. (2005) Human neural stem cell growth and differentiation in a gradient-generating microfluidic device. Lab Chip 5 (4) 401-406.
49. Wang JY, Ren L, Li L, Liu WM, Zhou J, et al. (2009) Microfluidics: A new cosset for neurobiology. Lab Chip 9 (5) 644-652.
50. Keenan TM, Grinager JR, Procak AA, Svendsen CN (2012) In vitro localization of human neural stem cell neurogenesis by engineered FGF-2 gradients. Integrative Biology 4 (12) 1522-1531.
51. Lanfer B, Hermann A, Kirsch M, Freudenberg U, Reuner U, et al. (2010) Directed Growth of Adult Human White Matter Stem Cell-Derived Neurons on Aligned Fibrillar Collagen. Tissue Eng. Part A 16 (4) 1103-1113.
52. Chang YJ, Tsai CJ, Tseng FG, Chen T, Wang TW (2013) Micropatterned stretching system for the investigation of mechanical tension on neural stem cells behavior. Nanomed.-Nanotechnol. Biol. Med. 9 (3) 345-355.
53. Jin KL, Peel AL, Mao XO, Xie L, Cottrell BA, et al. (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proceedings of the National Academy of Sciences of the United States of America 101 (1) 343-347.
54. Liu JL, Solway K, Messing RO, Sharp FR (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. Journal of Neuroscience 18 (19) 7768-7778.
55. Zhang RL, Zhang ZG, Zhang L, Chopp M (2001) Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105 (1) 33-41.
56. Horie N, So K, Moriya T, Kitagawa N, Tsutsumi K, et al. (2008) Effects of oxygen concentration on the proliferation and differentiation of mouse neural stem cells in vitro. Cellular and Molecular Neurobiology 28 (6) 833-845.
57. Iwai M, Sato K, Omori N, Nagano I, Manabe Y, et al. (2002) Three steps of neural stem cells development in gerbil dentate gyrus after transient ischemia. J. Cereb. Blood Flow Metab. 22 (4) 411-419.
58. Sun JQ, Zhou WH, Sha B, Yang Y (2010) Ischemia induced neural stem cell proliferation and differentiation in neonatal rat involved vascular endothelial growth factor and transforming growth factor-beta pathways. Brain Dev. 32 (3) 191-200.
59. Kim SJ, Son TG, Kim K, Park HR, Mattson MP, et al. (2007) Interferongamma promotes differentiation of neural progenitor cells via the JNK pathway. Neurochemical Research 32 (8) 1399-1406.
60. Li M, Tsang KS, Choi ST, Li K, Shaw C, et al. (2011) Neuronal Differentiation of C17.2 Neural Stem Cells Induced by a Natural Flavonoid Baicalin. ChemBioChem 12 (3) 449-456.
61. Lu W, Wang J, Wen TQ (2008) Downregulation of Rho-GDI gamma promotes differentiation of neural stem cells. Molecular and Cellular Biochemistry 311 (1-2) 233-240.
62. Bechara S, Wadman L, Popat C (2011) Electroconductive polymeric nanowire templates facilitates in vitro C17.2 neural stem cell line adhesion proliferation and differentiation. Acta Biomater. 7 (7) 2892-2901.
63. Lundqvist J, El Andaloussi-Lilja J, Svensson C, Dorfh HG, Forsby A (2013) Optimisation of culture conditions for differentiation of C17.2 neural stem cells to be used for in vitro toxicity tests. Toxicol. Vitro 27 (5) 1565-1569.
64. Oh JE, Bae GU, Yang YJ, Yi, Lee HJ, et al. (2009) Cdo promotes neuronal differentiation via activation of the p38 mitogen-activated protein kinase pathway. Faseb Journal 23 (7) 2088-2099.
65. Qazi H, Shi ZD, Tarbell JM (2011) Fluid Shear Stress Regulates the Invasive Potential of Glioma Cells via Modulation of Migratory Activity and Matrix Metalloproteinase Expression. PLoS One 6 (5) 13.
66. Kurbel S (2005) Ageing and maintenance of the interstitial fluid traffic: Possible roles of initial lymphatics and circadian hormones. Med. Hypotheses 64 (2) 375-379.
67. Deguchi Y, Inabe K, Tomiyasu K, Nozawa K, Yamada S, et al. (1995) Study on brain interstitial fluid distribution and blood-brain barrier transport of baclofen in rats by microdialysis. Pharm. Res. 12 (12) 1838-1844.
68. Basser PJ (1992) Interstitial Pressure Volume and Flow During Infusion into Brain-Tissue. Microvasc. Res. 44 (2) 143-165.
69. Abbott NJ (2004) Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem. Int. 45 (4) 545-552.
70. Geer CP, Grossman SA (1997) Interstitial fluid flow along white matter tracts: A potentially important mechanism for the dissemination of primary brain tumors. J. Neuro-Oncol. 32 (3) 193-201.
71. Sharma R, Ottenhof T, Rzeczkowska PA, Niles LP (2008) Epigenetic targets for melatonin: induction of histone H3 hyperacetylation and gene expression in C17.2 neural stem cells. Journal of Pineal Research 45 (3) 277-284.
72. Wang HF, Cheng H, Wang K, Wen TQ (2012) Different effects of histone deacetylase inhibitors nicotinamide and trichostatin A (TSA) in C17.2 neural stem cells.J. Neural Transm. 119 (11) 1307-1315.
73. Yang Y, Ren WW, Chen FX (2006) Knockdown of Stat3 in C17.2 neural stem cells facilitates the generation of neurons: A possibility of transplantation with a low level of oncogene. Neuroreport 17 (3) 235-238.
74. Kitchens DL, Snyder EY, Gottlieb DI (1994) FGF and EGF are mitogens for immortalized neural progenitors. J. Neurobiol. 25 (7) 797-807.
75. Garcez RC, Teixeira BL, Schmitt SD, Alvarez-Silva M, Trentin AG (2009) Epidermal Growth Factor (EGF) Promotes the In Vitro Differentiation of Neural Crest Cells to Neurons and Melanocytes. Cellular and Molecular Neurobiology 29 (8) 1087-1091.
76. Schwindt TT, Motta L, Barnabe F, Massant CG, Guimaraes AO, et al. (2009) Effects of FGF-2 and EGF removal on the differentiation of mouse neural precursor cells. An. Acad. Bras. Cienc. 81 (3) 443-452.
77. Trinh NTN, Prive A, Kheir L, Bourret JC, Hijazi T, et al. (2007) Involvement of K-ATP and KvLQT1 K+ channels in EGF-stimulated alveolar epithelial cell repair processes.Am. J. Physiol.-Lung Cell. Mol. Physiol. 293 (4) L870-L882.
78. Masui H, Castro L, Mendelsohn J (1993) Consumption of EGF by A431 cells - evidence for receptor recycling. Journal of Cell Biology 120 (1) 85-93.
79. Schmetsdorf S, Gartner U, Arendt T (2005) Expression of cell cycle-related proteins in developing and adult mouse hippocampus. Int. J. Dev. Neurosci. 23 (1) 101-112.
80. Yang Y, Herrup K (2007) Cell division in the CNS: Protective response or lethal event in post-mitotic neurons? Biochim. Biophys. Acta-Mol. Basis Dis. 1772 (4) 457-466.
81. Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: From precursors to network and physiology. Physiol. Rev. 85 (2) 523-569.
82. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD (2001) A unified hypothesis on the lineage of neural stem cells. Nature Reviews Neuroscience 2 (4) 287-293.
83. Millet LJ, Stewart ME, Sweedler JV, Nuzzo RG, Gillette MU (2007) Microfluidic devices for culturing primary mammalian neurons at low densities. Lab Chip 7 (8) 987-994.
84. Deckwerth L, Johnson EM (1993) Temporal analysis of events associated with programmed cell-death (apoptosis) of sympathetic neurons deprived of nerve growth-factor. Journal of Cell Biology 123 (5) 1207-1222.
85. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: An integrated view Trends Neurosci. 22 (9) 391-397.
86. Dugan LL, Turetsky DM, Du C, Lobner D, Wheeler M, et al. (1997) Carboxyfullerenes as neuroprotective agents. Proceedings of the National Academy of Sciences of the United States of America 94 (17) 9434-9439.
87. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, et al. (1997) Neuronal and glial apoptosis after traumatic spinal cord injury. Journal of Neuroscience 17 (14) 5395-5406.
88. Yu ZF, Luo H, Fu WM, Mattson MP (1999) The endoplasmic reticulum stressresponsive protein GRP78 protects neurons against excitotoxicity and apoptosis: Suppression of oxidative stress and stabilization of calcium homeostasis. Exp. Neurol. 155 (2) 302-314.
89. Loo DT, Copani A, Pike CJ, Whittemore ER, Walencewicz AJ, Cotman CW (1993) Apoptosis is induced by beta-amyloid in cultured central-nervous-system neurons. Proceedings of the National Academy of Sciences of the United States of America 90 (17) 7951-7955.
90. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, et al. (1993) Programmed cell-death and the control of cell-survival - lessons from the nervous-system. Science 262 (5134) 695-700.
91. Xia ZG, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing Effects of Erk and Jnk-P38 Map Kinases on Apoptosis.Science 270 (5240) 1326-1331.
92. Yao RJ, Cooper GM (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth-factor. Science 267 (5206) 2003- 2006.
93. Yuan JY, Yankner BA (2000) Apoptosis in the nervous system. Nature 407 (6805) 802-809.
94. Colleen T Curley KF and Sabrina S Jedlicka (2012) Characterizing the effect of substrate stiffness on neural stem cell differentiation. Mater. Res. Soc. Symp. Proc. 1498.
95. Yang F, Murugan R, Wang S, Ramakrishna S Electrospinning of nano/micro scale poly(L-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 26 (15) 2603-2610.
96. King JA, Miller WM (2005) Bioreactor development for stem cell expansion and controlled differentiation. Curr. Opin. Chem. Biol. (2007) 11 (4) 394-398.
97. Fan YW, Cui FZ, Hou SP, Xu QY, Chen LN, et al. (2002) Culture of neural cells on silicon wafers with nano-scale surface topograph. Journal of Neuroscience Methods 120 (1) 17-23.
98. Henley J, Poo M (2004) Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol. 14 (6) 320-330.
99. Tang FJ, Kalil K (2005) Netrin-1 induces axon branching in developing cortical neurons by frequency-dependent calcium signaling pathways. Journal of Neuroscience 25 (28) 6702-6715.
100. Pearce TM, Wilson JA, Oakes SG, Chiu SY, Williams JC (2005) Integrated microelectrode array and microfluidics for temperature clamp of sensory neurons in culture. Lab Chip 5 (1) 97-100.
101. Cullen DK, Vukasinovic J, Glezer A, LaPlaca MC (2007) Microfluidic engineered high cell density three-dimensional neural cultures. Journal of Neural Engineering 4 (2) 159-172.
102. Culican SM, Baumrind NL, Yamamoto M, Pearlman AL (1990) Cortical Radial Glia - Identification in Tissue-Culture and Evidence for their Transformation to Astrocytes.Journal of Neuroscience 10 (2) 684-692.
103. Gierdalski M, Juliano SL (2003) Factors affecting the morphology of radial glia. Cerebral Cortex 13 (6) 572-579.
104. Fanarraga ML, Avila J, Zabala JC (1999) Expression of unphosphorylated class III beta-tubulin isotype in neuroepithelial cells demonstrates neuroblast commitment and differentiation. Eur. J. Neurosci. 11 (2) 517-527.
105. Katsetos CD, Nakahara C, Agamanolis DP, Karkavelas G, Lebenthal E, et al. (1994) Localization of the Neuronal Class-Iii Beta-Tubulin Isotype in Foci of Early Neuritogenesis Supports Divergent Neuroblastic Differentiation Potential in Wilms-Tumors.Arch. Pathol. Lab. Med. 118 (10) 1002-1006.
106. Roskams AJI, Cai X, Ronnett GV (1998) Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat. Neuroscience 83 (1) 191-200.
107. Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI (1995) Embryonic Stem- Cells Express Neuronal Properties In-Vitro.Developmental Biology 168 (2) 342-357.
108. Ginis I, Luo, Miura T, Thies S, Brandenberger R, et al. (2004) Differences between human and mouse embryonic stem cells. Developmental Biology 269 (2) 360-380.
109. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, et al. (2000) In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat. Med. 6 (3) 271-277.
110. Anton ES, Marchionni MA, Lee KF, Rakic P (1997) Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124 (18) 3501-3510.
111. Diers-Fenger M, Kirchhoff F, Kettenmann H, Levine JM, Trotter J (2001) AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: Isolation differentiation and association with radial glia. Glia 34 (3) 213-228.
112. Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, et al. (2009) Mammalian Par3 Regulates Progenitor Cell Asymmetric Division via Notch Signaling in the Developing Neocortex. Neuron 63 (2) 189-202.
113. Sevc J, Daxnerova Z, Miklosova M (2009) Role of Radial Glia in Transformation of the Primitive Lumen to the Central Canal in the Developing Rat Spinal Cord. Cellular and Molecular Neurobiology 29 (6-7) 927-936.
114. Zhang Y, Niu BH, Yu DM, Cheng XS, Liu B, et al. (2010) Radial glial cells and the lamination of the cerebellar cortex. Brain Structure & Function 215 (2) 115-122.