Characterization and transformation potential of "synthetic" astrocytes differentiated from murine embryonic stem cells

GLIA

Volumn 56, Issue 4, 2008, Pages 457-470

  Kamnasaran, Deepak ^a   Hawkins, Cynthia ^b   Guha, Abhijit ^a,c,d  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d TORONTO WESTERN HOSPITAL   (Canada)

Author keywords

Cell differentiation; Gene expression; Genetic models; Neoplasms; Pluripotent stem cells

Indexed keywords

ANIMAL CELL; ARTICLE; ASTROCYTE; ASTROCYTOMA; CELL DIFFERENTIATION; CELL TRANSFORMATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GLIOMA; HIPPOCAMPUS; NERVE CELL PLASTICITY; NONHUMAN; OLIGODENDROGLIA; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATIC CELL;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BRAIN; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTOR 2; GANGLIOSIDES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IN SITU NICK-END LABELING; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSDUCTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 38949145082     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20631     Document Type: Article

References (59)

1. Bachoo RM, Kim RS, Ligon KL, Maher EA, Brennan C, Billings N, Chan S, Li C, Rowitch DH, Wong WH, DePinho RA. 2004. Molecular diversity of astrocytes with implications for neurological disorders. Proc Natl Acad Sci USA 101:8384-8389.
2. Bachoo RM, Maher EA, Ligon KL, Sharpless NE, Chan SS, You MJ, Tang Y, DeFrances J, Stover E, Weissleder R, Rowitch DH, Louis DN, DePinho RA. 2002. Epidermal growth factor receptor and Ink4a/Arf: Convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 1:269-277.
3. Bjorklund LM, Sanchez-Pernaute R, Chung S, Andersson T, Chen IY, McNaught KS, Brownell AL, Jenkins BG, Wahlestedt C, Kim KS, Isacson O. 2002. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci USA 99:2344-2349.
4. Bogler O, Nagane M, Gillis J, Huang HJ, Cavenee WK. 1999. Malignant transformation of p53-deficient astrocytes is modulated by environmental cues in vitro. Cell Growth Differ 10:73-86.
5. Brustle O, Jones KN, Learish RD, Karram K, Choudhary K, Wiestler OD, Duncan ID, McKay RD. 1999. Embryonic stem cell-derived glial precursors: A source of myelinating transplants. Science 285:754-756.
6. Chang MY, Son H, Lee YS, Lee SH. 2003. Neurons and astrocytes secrete factors that cause stem cells to differentiate into neurons and astrocytes, respectively. Mol Cell Neurosci 23:414-426.
7. Colombo E, Giannelli SG, Galli R, Tagliafico E, Foroni C, Tenedini E, Ferrari S, Ferrari S, Corte G, Vescovi A, Cossu G, Broccoli V. 2006. Embryonic stem-derived versus somatic neural stem cells: A comparative analysis of their developmental potential and molecular phenotype. Stem Cells 24:825-834.
8. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, Holland EC. 2001. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev 15:1913-1925.
9. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP. 1998. Pten is essential for embryonic development and tumour suppression. Nat Genet 19:348-355.
10. Ding H, Roncari L, Shannon P, Wu X, Lau N, Karaskova J, Gutmann DH, Squire JA, Nagy A, Guha A. 2001. Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas. Cancer Res 61:3826-3836.
11. Doetsch F. 2003. The glial identity of neural stem cells. Nat Neurosci 6:1127-1134.
12. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
13. Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154-156.
14. Fan Y, Melhem MF, Chaillet JR. 1999. Forced expression of the homeobox-containing gene Pem blocks differentiation of embryonic stem cells. Dev Biol 210:481-496.
15. Field SJ, Johnson RS, Mortensen RM, Papaioannou VE, Spiegelman BM, Greenberg ME. 1992. Growth and differentiation of embryonic stem cells that lack an intact c-fos gene. Proc Natl Acad Sci USA 89:9306-9310.
16. Fraichard A, Chassande O, Bilbaut G, Dehay C, Savatier P, Samarut J. 1995. In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J Cell Sci 108:3181-3188.
17. Gomes WA, Mehler MF, Kessler JA. 2003. Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 255:164-177.
18. Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, Kornblum HI, Liu X, Wu H. 2001. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294:2186-2189.
19. Hajihosseini MK, Dickson C. 1999. A subset of fibroblast growth factors (Fgfs) promote survival, but Fgf-8b specifically promotes astroglial differentiation of rat cortical precursor cells. Mol Cell Neurosci 14:468-485.
20. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN. 2000. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 25:55-57.
21. Holland EC, Hively WP, DePinho RA, Varmus HE. 1998. A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev 12:3675-3685.
22. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264.
23. Jori FP, Galderisi U, Piegari E, Cipollaro M, Cascino A, Peluso G, Cotrufo R, Giordano A, Melone MA. 2003. EGF-responsive rat neural stem cells: Molecular follow-up of neuron and astrocyte differentiation in vitro. J Cell Physiol 195:220-233.
24. Kamnasaran D, Qian B, Hawkins C, Stanford WL, Guha A. 2007. GATA6 is an astrocytoma tumor suppressor gene identified by gene trapping of mouse glioma model. Proc Natl Acad Sci USA 104:8053-8058.
25. Kielman MF, Rindapaa M, Gaspar C, van Poppel N, Breukel C, van Leeuwen S, Taketo MM, Roberts S, Smits R, Fodde R. 2002. Apc modulates embryonic stem-cell differentiation by controlling the dosage of β-catenin signaling. Nat Genet 32:594-605.
26. Lee Y, Su M, Messing A, Brenner M. 2006. Astrocyte heterogeneity revealed by expression of a GFAP-LacZ transgene. Glia 53:677-687.
27. Mabie PC, Mehler MF, Marmur R, Papavasiliou A, Song Q, Kessler JA. 1997. Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J Neurosci 17:4112-4120.
28. Martin GR. 1981. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 78:7634-7638.
29. Matsuzaki H, Tamatani M, Mitsuda N, Namikawa K, Kiyama H, Miyake S, Tohyama M. 1999. Activation of Akt kinase inhibits apoptosis and changes in Bcl-2 and Bax expression induced by nitric oxide in primary hippocampal neurons. J Neurochem 73:2037-2046.
30. Merlo A. 2003. Genes and pathways driving glioblastomas in humans and murine disease models. Neurosurg Rev 26:145-158.
31. Mi H, Haeberle H, Barres BA. 2001. Induction of astrocyte differentiation by endothelial cells. J Neurosci 21:1538-1547.
32. Mujtaba T, Rao MS. 2002. Isolation of lineage-restricted neural precusors from cultured ES cells. Methods Mol Biol 185:189-204.
33. Mummery CL, van den Eijnden-van Raaij AJ, Feijen A, Freund E, Hulskotte E, Schoorlemmer J, Kruijer W 1990. Expression of growth factors during the differentiation of embryonic stem cells in monolayer. Dev Biol 142:406-413.
34. Nakashima K, Yanagisawa M, Arakawa H, Taga T. 1999. Astrocyte differentiation mediated by LIF in cooperation with BMP2. FEBS Lett 457:43-46.
35. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH. 2001. Cell culture. Progenitor cells from human brain after death. Nature 411:42-43.
36. Penninger JM, Woodgett J. 2001. Stem cells. PTEN-coupling tumor suppression to stem cells? Science 294:2116-2118.
37. Rajan P, McKay RD. 1998. Multiple routes to astrocytic differentiation in the CNS. J Neurosci 18:3620-3629.
38. Rao MS, Noble M, Mayer-Proschel M. 1998. A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci USA 95:3996-4001.
39. Reubinoff BE, Itsykson P, Turetsky T, Pera MF, Reinhartz E, Itzik A, Ben-Hur T. 2001. Neural progenitors from human embryonic stem cells. Nat Biotechnol 19:1134-1140.
40. Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A. 2000. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat Biotechnol 18:399-404.
41. Rich JN. 2006. The cancer stem cell: A new therapeutic paradigm? Expert Rev Anticancer Ther 6:1531-1533.
42. Rich JN, Guo C, McLendon RE, Bigner DD, Wang XF, Counter CM. 2001. A genetically tractable model of human glioma formation. Cancer Res 61:3556-3560.
43. Sang HU, Alilain W, Saljooque F. 2002. Fetal brain progenitor cells transdifferentiate to fates outside the nervous system. Mol Endocrinol 16:2645-2656.
44. Satoh M, Sugino H, Yoshida T. 2000. Activin promotes astrocytic differentiation of a multipotent neural stem cell line and an astrocyte progenitor cell line from murine central nervous system. Neurosci Lett 284:143-146.
45. Seidman KJ, Teng AL, Rosenkopf R, Spilotro P, Weyhenmeyer JA. 1997. Isolation, cloning and characterization of a putative type-1 astrocyte cell line. Brain Res 753:18-26.
46. Shannon P, Sabha N, Lau N, Kamnasaran D, Gutmann DH, Guha A. 2005. Pathological and molecular progression of astrocytomas in a GFAP:12 V-Ha-Ras mouse astrocytoma model. Am J Pathol 167:859-867.
47. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. 2003. Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821-5828.
48. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. 2004. Identification of human brain tumour initiating cells. Nature 432:396-401.
49. Slager HG, Van Inzen W, Freund E, Van den Eijnden-Van Raaij AJ, Mummery CL. 1993. Transforming growth factor-β in the early mouse embryo: Implications for the regulation of muscle formation and implantation. Dev Genet 14:212-224.
50. Smith AG. 2001. Embryo-derived stem cells: Of mice and men. Annu Rev Cell Dev Biol 17:435-462.
51. Sonoda Y, Ozawa T, Aldape KD, Deen DF, Berger MS, Pieper RO. 2001. Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. Cancer Res 61:6674-6678.
52. Suemori H, Tada T, Torii R, Hosoi Y, Kobayashi K, Imahie H, Kondo Y, Iritani A, Nakatsuji N. 2001. Establishment of embryonic stem cell lines from cynomolgus monkey blastocysts produced by IVF or ICSI. Dev Dyn 222:273-279.
53. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
54. Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Becker RA, Hearn JP. 1995. Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci USA 92:7844-7848.
55. Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Hearn JP. 1996. Pluripotent cell lines derived from common marmoset (Callithrix jacchus) blastocysts. Biol Reprod 55:254-259.
56. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121.
57. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL. 2000. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 97:14720-14725.
58. Uhrbom L, Dai C, Celestino JC, Rosenblum MK, Fuller GN, Holland EC. 2002. Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res 62:5551-5558.
59. Wiles MV, Keller G. 1991. Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development 111:259-267.