Efficient generation of astrocytes from human pluripotent stem cells in defined conditions

Stem Cells

Volumn 31, Issue 5, 2013, Pages 941-952

  Shaltouki, Atossa ^a   Peng, Jun ^a   Liu, Qiuyue ^a   Rao, Mahendra S ^b   Zeng, Xianmin ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; CILIARY NEUROTROPHIC FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; MESSENGER RNA; NEU DIFFERENTIATION FACTOR;

ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOME; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PLURIPOTENT STEM CELL; SYNAPSE; XENOTRANSPLANTATION;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; CRYOPRESERVATION; CYTOLOGICAL TECHNIQUES; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; PLURIPOTENT STEM CELLS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84875957053     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1334     Document Type: Article

References (98)

1. Sherwood CC, Stimpson CD, Raghanti MA et al. Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci USA 2006;103:13606-13611. (Pubitemid 44413955)
2. Tardy M, Fages C, Le Prince G et al. Regulation of the glial fibrillary acidic protein (GFAP) and of its encoding mRNA in the developing brain and in cultured astrocytes. Adv Exp Med Biol 1990;265:41-52. (Pubitemid 20189913)
3. Voigt T. Development of glial cells in the cerebral wall of ferrets: Direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 1989;289:74-88. (Pubitemid 19263991)
4. Seri B, Garcia-Verdugo JM, McEwen BS et al. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001;21:7153-7160. (Pubitemid 32846963)
5. Noctor SC, Flint AC, Weissman TA et al. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001;409:714-720. (Pubitemid 32144516)
6. Malatesta P, Hartfuss E, Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000;127:5253-5263. (Pubitemid 32049182)
7. Hartfuss E, Galli R, Heins N et al. Characterization of CNS precursor subtypes and radial glia. Dev Biol 2001;229:15-30. (Pubitemid 32061711)
8. Rowitch DH, Kriegstein AR. Developmental genetics of vertebrate glial-cell specification. Nature 2010;468:214-222.
9. Moretto G, Xu RY, Kim SU. CD44 expression in human astrocytes and oligodendrocytes in culture. J Neuropathol Exp Neurol 1993;52:419-423. (Pubitemid 23199202)
10. Vogel H, Butcher EC, Picker LJ. H-CAM expression in the human nervous system: Evidence for a role in diverse glial interactions. J Neurocytol 1992;21:363-373.
11. Alfei L, Aita M, Caronti B et al. Hyaluronate receptor CD44 is expressed by astrocytes in the adult chicken and in astrocyte cell precursors in early development of the chick spinal cord. Eur J Histochem 1999;43:29-38. (Pubitemid 30000814)
12. Rao MS, Mayer-Proschel M. Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev Biol 1997;188:48-63. (Pubitemid 27360086)
13. Rao MS, Noble M, Mayer-Proschel M. A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci USA 1998;95:3996-4001. (Pubitemid 28173242)
14. Liu Y, Han SS, Wu Y et al. CD44 expression identifies astrocyte-restricted precursor cells. Dev Biol 2004;276:31-46. (Pubitemid 39452844)
15. Liu Y, Wu Y, Lee JC et al. Oligodendrocyte and astrocyte development in rodents: An in situ and immunohistological analysis during embryonic development. Glia 2002;40:25-43. (Pubitemid 35181341)
16. Alonso G. NG2 proteoglycan-expressing cells of the adult rat brain: Possible involvement in the formation of glial scar astrocytes following stab wound. Glia 2005;49:318-338. (Pubitemid 40222911)
17. Lepore AC, Han SS, Tyler-Polsz CJ et al. Differential fate of multipotent and lineage-restricted neural precursors following transplantation into the adult CNS. Neuron Glia Biol 2004;1:113-126.
18. Rosenberg LJ, Zai LJ, Wrathall JR. Chronic alterations in the cellular composition of spinal cord white matter following contusion injury. Glia 2005;49:107-120. (Pubitemid 40023657)
19. Dawson MR, Polito A, Levine JM et al. NG2-expressing glial progenitor cells: An abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 2003;24:476-488. (Pubitemid 37311310)
20. Zai LJ, Wrathall JR. Cell proliferation and replacement following contusive spinal cord injury. Glia 2005;50:247-257. (Pubitemid 40769854)
21. Tatsumi K, Haga S, Matsuyoshi H et al. Characterization of cells with proliferative activity after a brain injury. Neurochem Int 2005;46:381-389. (Pubitemid 40292718)
22. Hill CE, Proschel C, Noble M et al. Acute transplantation of glial-restricted precursor cells into spinal cord contusion injuries: Survival, differentiation, and effects on lesion environment and axonal regeneration. Exp Neurol 2004;190:289-310. (Pubitemid 39504988)
23. Mitsui T, Shumsky JS, Lepore AC et al. Transplantation of neuronal and glial restricted precursors into contused spinal cord improves bladder and motor functions, decreases thermal hypersensitivity, and modifies intraspinal circuitry. J Neurosci 2005;25:9624-9636. (Pubitemid 41510903)
24. Nout YS, Culp E, Schmidt MH et al. Glial restricted precursor cell transplant with cyclic adenosine monophosphate improved some autonomic functions but resulted in a reduced graft size after spinal cord contusion injury in rats. Exp Neurol 2011;227:159-171.
25. Wu YY, Mujtaba T, Han SS et al. Isolation of a glial-restricted tripotential cell line from embryonic spinal cord cultures. Glia 2002;38:65-79.
26. Wu YY, Mujtaba T, Rao MS. Isolation of stem and precursor cells from fetal tissue. Methods Mol Biol 2002;198:29-40.
27. Mujtaba T, Piper DR, Kalyani A et al. Lineage-restricted neural precursors can be isolated from both the mouse neural tube and cultured ES cells. Dev Biol 1999;214:113-127. (Pubitemid 29463360)
28. Swistowski A, Peng J, Han Y et al. Xeno-free defined conditions for culture of human embryonic stem cells, neural stem cells and dopaminergic neurons derived from them. PLoS One 2009;4:e6233.
29. Won CL, Oh YS. cAMP-induced stellation in primary astrocyte cultures with regional heterogeneity. Brain Res 2000;887:250-258. (Pubitemid 32008046)
30. Hall AC, Mira H, Wagner J et al. Region-specific effects of glia on neuronal induction and differentiation with a focus on dopaminergic neurons. Glia 2003;43:47-51. (Pubitemid 36781697)
31. Matyash V, Kettenmann H. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev 2010;63:2-10.
32. Hochstim C, Deneen B, Lukaszewicz A et al. Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell 2008;133:510-522. (Pubitemid 351608691)
33. Krencik R, Weick JP, Liu Y et al. Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat Biotechnol 2011;29:528-534.
34. Takahashi M, Osumi N. Pax6 regulates specification of ventral neurone subtypes in the hindbrain by establishing progenitor domains. Development 2002;129:1327-1338. (Pubitemid 34874154)
35. Muroyama Y, Fujiwara Y, Orkin SH et al. Specification of astrocytes by bHLH protein SCL in a restricted region of the neural tube. Nature 2005;438:360-363. (Pubitemid 41643952)
36. Shirasaki R, Pfaff SL. Transcriptional codes and the control of neuronal identity. Annu Rev Neurosci 2002;25:251-281. (Pubitemid 34748018)
37. Wang L, Schulz TC, Sherrer ES et al. Self-renewal of human embryonic stem cells requires insulin-like growth factor-1 receptor and ERBB2 receptor signaling. Blood 2007;110:4111-4119. (Pubitemid 350248470)
38. Saeed AI, Bhagabati NK, Braisted JC et al. TM4 microarray software suite. Methods Enzymol 2006;411:134-193.
39. Drejer J, Larsson OM, Schousboe A. Characterization of L-glutamate uptake into and release from astrocytes and neurons cultured from different brain regions. Exp Brain Res 1982;47:259-269. (Pubitemid 12041193)
40. Szymocha R, Akaoka H, Dutuit M et al. Human T-cell lymphotropic virus type 1-infected T lymphocytes impair catabolism and uptake of glutamate by astrocytes via Tax-1 and tumor necrosis factor alpha. J Virol 2000;74:6433-6441. (Pubitemid 30429810)
41. Kimelberg HK, Goderie SK, Conley PA et al. Uptake of [3H]serotonin and [3H]glutamate by primary astrocyte cultures. I. Effects of different sera and time in culture. Glia 1992;6:1-8.
42. Garlin AB, Sinor AD, Sinor JD et al. Pharmacology of sodium-dependent high-affinity L-[3H]glutamate transport in glial cultures. J Neurochem 1995;64:2572-2580.
43. Peng J, Mao XO, Stevenson FF et al. The herbicide paraquat induces dopaminergic nigral apoptosis through sustained activation of the JNK pathway. J Biol Chem 2004;279:32626-32632. (Pubitemid 39014720)
44. Swistowski A, Peng J, Liu Q et al. Efficient generation of functional dopaminergic neurons from human induced pluripotent stem cells under defined conditions. Stem Cells 2010;28:1893-1904.
45. Sharif A, Duhem-Tonnelle V, Allet C et al. Differential erbB signaling in astrocytes from the cerebral cortex and the hypothalamus of the human brain. Glia 2009;57:362-379.
46. Ludwin SK, Kosek JC, Eng LF. The topographical distribution of S-100 and GFA proteins in the adult rat brain: An immunohistochemical study using horseradish peroxidase-labelled antibodies. J Comp Neurol 1976;165:197-207.
47. Deneen B, Ho R, Lukaszewicz A et al. The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 2006;52:953-968. (Pubitemid 44909408)
48. Wilczynska KM, Singh SK, Adams B et al. Nuclear factor I isoforms regulate gene expression during the differentiation of human neural progenitors to astrocytes. Stem Cells 2009;27:1173-1181.
49. Vitellaro-Zuccarello L, Mazzetti S, Bosisio P et al. Distribution of Aquaporin 4 in rodent spinal cord: Relationship with astrocyte markers and chondroitin sulfate proteoglycans. Glia 2005;51:148-159. (Pubitemid 41277348)
50. Wu Y, Liu Y, Levine EM et al. Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors. Dev Dyn 2003;226:675-689. (Pubitemid 36396876)
51. Cahoy JD, Emery B, Kaushal A et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. J Neurosci 2008;28:264-278.
52. Campanelli JT, Sandrock RW, Wheatley W et al. Expression profiling of human glial precursors. BMC Dev Biol 2008;8:102.
53. Fath T, Fischer RS, Dehmelt L et al. Tropomodulins are negative regulators of neurite outgrowth. Eur J Cell Biol 2011;90:291-300.
54. Bagchi A, Papazoglu C, Wu Y et al. CHD5 is a tumor suppressor at human 1p36. Cell 2007;128:459-475. (Pubitemid 46198889)
55. Thompson PM, Gotoh T, Kok M et al. CHD5, a new member of the chromodomain gene family, is preferentially expressed in the nervous system. Oncogene 2003;22:1002-1011. (Pubitemid 36313144)
56. Viskochil D, Cawthon R, O'Connell P et al. The gene encoding the oligodendrocyte-myelin glycoprotein is embedded within the neurofibromatosis type 1 gene. Mol Cell Biol 1991;11:906-912. (Pubitemid 21895439)
57. Subramanian L, Sarkar A, Shetty AS et al. Transcription factor Lhx2 is necessary and sufficient to suppress astrogliogenesis and promote neurogenesis in the developing hippocampus. Proc Natl Acad Sci USA 2011;108:E265-274.
58. Kook H, Yung WW, Simpson RJ et al. Analysis of the structure and function of the transcriptional coregulator HOP. Biochemistry 2006;45:10584-10590. (Pubitemid 44335688)
59. Yao J, Liu Y, Husain J et al. Combinatorial expression patterns of individual TLE proteins during cell determination and differentiation suggest non-redundant functions for mammalian homologs of Drosophila Groucho. Dev Growth Differ 1998;40:133-146. (Pubitemid 28180617)
60. Mayer-Proschel M, Kalyani AJ, Mujtaba T et al. Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 1997;19:773-785. (Pubitemid 27471383)
61. Rege TA, Hagood JS. Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. FASEB J 2006;20:1045-1054. (Pubitemid 44943900)
62. Barker TH, Pallero MA, MacEwen MW et al. Thrombospondin-1-induced focal adhesion disassembly in fibroblasts requires Thy-1 surface expression, lipid raft integrity, and Src activation. J Biol Chem 2004;279:23510-23516. (Pubitemid 38685663)
63. Barker TH, Grenett HE, MacEwen MW et al. Thy-1 regulates fibroblast focal adhesions, cytoskeletal organization and migration through modulation of p190 RhoGAP and Rho GTPase activity. Exp Cell Res 2004;295:488-496. (Pubitemid 38490501)
64. Kim SU, de Vellis J. Stem cell-based cell therapy in neurological diseases: A review. J Neurosci Res 2009;87:2183-2200.
65. Mandal A, Tipnis S, Pal R et al. Characterization and in vitro differentiation potential of a new human embryonic stem cell line, ReliCellhES1. Differentiation 2006;74:81-90. (Pubitemid 43376168)
66. Skottman H, Stromberg AM, Matilainen E et al. Unique gene expression signature by human embryonic stem cells cultured under serumfree conditions correlates with their enhanced and prolonged growth in an undifferentiated stage. Stem Cells 2006;24:151-167.
67. Fraichard A, Chassande O, Bilbaut G et al. In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J Cell Sci 1995;108(Pt 10):3181-3188.
68. Shufaro Y, Reubinoff BE. Therapeutic applications of embryonic stem cells. Best Pract Res Clin Obstet Gynaecol 2004;18:909-927. (Pubitemid 40012027)
69. Bonni A, Sun Y, Nadal-Vicens M et al. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 1997;278:477-483. (Pubitemid 27454434)
70. Gross RE, Mehler MF, Mabie PC et al. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 1996;17:595-606. (Pubitemid 26365340)
71. Nakashima K, Yanagisawa M, Arakawa H et al. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 1999;284:479-482. (Pubitemid 29289619)
72. Pinkas-Kramarski R, Eilam R, Spiegler O et al. Brain neurons and glial cells express Neu differentiation factor/heregulin: A survival factor for astrocytes. Proc Natl Acad Sci USA 1994;91:9387-9391. (Pubitemid 24297919)
73. Raabe TD, Clive DR, Wen D et al. Neonatal oligodendrocytes contain and secrete neuregulins in vitro. J Neurochem 1997;69:1859-1863. (Pubitemid 27452730)
74. Raabe TD, Clive DR, Neuberger TJ et al. Cultured neonatal Schwann cells contain and secrete neuregulins. J Neurosci Res 1996;46:263-270. (Pubitemid 26367552)
75. Olayioye MA, Beuvink I, Horsch K et al. ErbB receptor-induced activation of stat transcription factors is mediated by Src tyrosine kinases. J Biol Chem 1999;274:17209-17218.
76. Garcia R, Yu CL, Hudnall A et al. Constitutive activation of Stat3 in fibroblasts transformed by diverse oncoproteins and in breast carcinoma cells. Cell Growth Differ 1997;8:1267-1276. (Pubitemid 28008723)
77. Bowman T, Garcia R, Turkson J et al. STATs in oncogenesis. Oncogene 2000;19:2474-2488. (Pubitemid 30339203)
78. Viehover A, Miller RH, Park SK et al. Neuregulin: An oligodendrocyte growth factor absent in active multiple sclerosis lesions. Dev Neurosci 2001;23:377-386. (Pubitemid 34045232)
79. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997;390:465-471. (Pubitemid 28013118)
80. Satoh M, Sugino H, Yoshida T. Activin promotes astrocytic differentiation of a multipotent neural stem cell line and an astrocyte progenitor cell line from murine central nervous system. Neurosci Lett 2000;284:143-146. (Pubitemid 30204533)
81. Franceschini IA, Barnett SC. Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev Biol 1996;173:327-343. (Pubitemid 26063429)
82. Noctor SC, Martinez-Cerdeno V, Kriegstein AR. Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 2008;508:28-44. (Pubitemid 351532566)
83. Bernardos RL, Barthel LK, Meyers JR et al. Late-stage neuronal progenitors in the retina are radial Muller glia that function as retinal stem cells. J Neurosci 2007;27:7028-7040. (Pubitemid 47015895)
84. Kettenman H, Ransom BR et al. Neuroglia, third edition, Oxford University Press, 2005:601-624.
85. Merkle FT, Tramontin AD, Garcia-Verdugo JM et al. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 2004;101:17528-17532. (Pubitemid 39657437)
86. Raponi E, Agenes F, Delphin C et al. S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 2007;55:165-177. (Pubitemid 46036463)
87. Brozzi F, Arcuri C, Giambanco I et al. S100B protein regulates astrocyte shape and migration via interaction with Src Kinase: Implications for astrocyte development, activation, and tumor growth. J Biol Chem 2009;284:8797-8811.
88. Potts RC, Zhang P, Wurster AL et al. CHD5, a brain-specific paralog of Mi2 chromatin remodeling enzymes, regulates expression of neuronal genes. PLoS One 2011;6:e24515.
89. Gronostajski RM. Roles of the NFI/CTF gene family in transcription and development. Gene 2000;249:31-45. (Pubitemid 30265485)
90. Chaudhry AZ, Lyons GE, Gronostajski RM. Expression patterns of the four nuclear factor I genes during mouse embryogenesis indicate a potential role in development. Dev Dyn 1997;208:313-325. (Pubitemid 27114286)
91. Driller K, Pagenstecher A, Uhl M et al. Nuclear factor I X deficiency causes brain malformation and severe skeletal defects. Mol Cell Biol 2007;27:3855-3867. (Pubitemid 46726191)
92. Campbell CE, Piper M, Plachez C et al. The transcription factor Nfix is essential for normal brain development. BMC Dev Biol 2008;8:52.
93. das Neves L, Duchala CS, Tolentino-Silva F et al. Disruption of the murine nuclear factor I-A gene (Nfia) results in perinatal lethality, hydrocephalus, and agenesis of the corpus callosum. Proc Natl Acad Sci USA 1999;96:11946-11951.
94. Singh SK, Wilczynska KM, Grzybowski A et al. The unique transcriptional activation domain of nuclear factor-I-X3 is critical to specifically induce marker gene expression in astrocytes. J Biol Chem 2011;286:7315-7326.
95. Cebolla B, Vallejo M. Nuclear factor-I regulates glial fibrillary acidic protein gene expression in astrocytes differentiated from cortical precursor cells. J Neurochem 2006;97:1057-1070.
96. Yeh TH, Lee da Y, Gianino SM et al. Microarray analyses reveal regional astrocyte heterogeneity with implications for neurofibromatosis type 1 (NF1)-regulated glial proliferation. Glia 2009;57:1239-1249.
97. De Toni A, Zbinden M, Epstein JA et al. Regulation of survival in adult hippocampal and glioblastoma stem cell lineages by the homeo-domain-only protein HOP. Neural Dev 2008;3:13.
98. Doyle JP, Dougherty JD, Heiman M et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 2008;135:749-762.