Clonal neural stem cells from human embryonic stem cell colonies

Journal of Neuroscience

Volumn 32, Issue 23, 2012, Pages 7771-7781

  Chaddah, Radha ^a   Arntfield, Margot ^a   Runciman, Susan ^a   Clarke, Laura ^a   van der Kooy, Derek ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; BETA TUBULIN; BONE MORPHOGENETIC PROTEIN; CELL SURFACE MARKER; HEPATOCYTE NUCLEAR FACTOR 3BETA; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; LIN28 PROTEIN; MESSENGER RNA; NOGGIN; OCTAMER TRANSCRIPTION FACTOR 4; RNA 18S; RNA BINDING PROTEIN; STAGE SPECIFIC EMBRYO ANTIGEN 4; TRA 1 60 PROTEIN; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CELL CLONE; CONTROLLED STUDY; EMBRYOID BODY; EMBRYONIC STEM CELL; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEWBORN; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CELL SURVIVAL; CELLS, CULTURED; CLONE CELLS; COLONY-FORMING UNITS ASSAY; CULTURE MEDIA, SERUM-FREE; DNA, COMPLEMENTARY; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTORS; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEOSTRIATUM; NEURAL STEM CELLS; POLYMERASE CHAIN REACTION; RHO-ASSOCIATED KINASES; RNA; STEM CELL TRANSPLANTATION;

EID: 84861905970     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3286-11.2012     Document Type: Article

References (52)

1. Balzer E, Heine C, Jiang Q, Lee VM, Moss EG (2010) LIN 28 alters cell fate succession and acts independently of the let-7 microRNA during neurogliogenesis in vitro. Development 137:891-900.
2. Bendall SC, Stewart MH, Menendez P, George D, Vijayaragavan K, Werbowetski-Ogilvie T, Ramos-Mejia V, Rouleau A, Yang J, Bossé M, Lajoie G, BhatiaM (2007) IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 448:1015-1021.
3. Brederlau A, Correia AS, Anisimov SV, Elmi M, Paul G, Roybon L, Morizane A, Bergquist F, Riebe I, Nannmark U, Carta M, Hanse E, Takahashi J, Sasai Y, Funa K, Brundin P, Eriksson PS, Li JY (2006) Transplantation of human embryonic stem cell-derived cells into a rat model of Parkinson's disease: effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells 24:1433-1440.
4. Cai J, Yang M, Poremsky E, Kidd S, Schneider JS, Iacovitti L (2010) Hostdependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. Stem Cells Dev 19:1017-1023.
5. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27:275-280.
6. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A (2005) Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3:e283.
7. Dang SM, Kyba M, Perlingeiro R, Daley GQ, ZandstraPW (2002) Efficiency of embryoid body formation and hematopoietic development from embryonic stem cells in different culture systems. Biotechnol Bioeng 78:442-453.
8. Dhara SK, Stice SL (2008) Neural differentiation of human embryonic stem cells. J Cell Biochem 105:633-640.
9. Draper JS, Smith K, Gokhale P, Moore HD, Maltby E, Johnson J, Meisner L, Zwaka TP, Thomson JA, Andrews PW (2004) Recurrent gain of chromosomes 17q and 12 in cultured embryonic stem cells. Nat Biotechnol 22:53-54.
10. Elkabetz Y, Panagiotakos G, Al Shamy G, Socci ND, Tabar V, Studer L (2008) Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 22:152-165.
11. Erdö F, Bührle C, Blunk J, Hoehn M, Xia Y, Fleischmann B, Föcking M, Küstermann E, Kolossov E, Hescheler J, Hossmann KA, Trapp T (2003) Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J Cereb Blood Flow Metab 23:780-785.
12. Godsave SF, Slack JM (1989) Clonal analysis of mesoderm induction in Xenopus laevis. Dev Biol 134:486-490.
13. Grunz H, Tacke L (1989) Neural differentiation of Xenopus Laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. Cell Differ Dev 28:211-217.
14. Hanna J, Cheng AW, Saha K, Kim J, Lengner CJ, Soldner F, Cassady JP, Muffat J, Carey BW, Jaenisch R (2010) Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci U S A 107:9222-9227.
15. Hemmati-Brivanlou A, Melton DA (1994) Inhibition of activin receptor signalling promotes neuralization in Xenopus. Cell 77:273-281.
16. Henderson JK, Draper JS, Baillie HS, Fishel S, Thomson JA, Moore H, Andrews PW (2002) Preimplantation human embryos and embryonic stem cells show comparable expression of stage-specific embryonic antigens. Stem Cells 20:329-337.
17. Hitoshi S, Seaberg RM, Koscik C, Alexson T, Kusunoki S, Kanazawa I, Tsuji S, van der KooyD (2004) Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signalling. Genes Dev 18:1806-1811.
18. Itsykson P, Ilouz N, Turetsky T, Goldstein RS, Pera MF, Fishbein I, Segal M, Reubinoff BE (2005) Derivation of neural precursors from human embryonic stem cells in the presence of noggin. Mol Cell Neurosci 30:24-36.
19. Kang SM, Cho MS, Seo H, Yoon CJ, Oh SK, Choi YM, Kim DW (2007) Efficient induction of oligodendrocytes from human embryonic stem cells. Stem Cells 25:419-424.
20. Koch P, Opitz T, Steinbeck JA, Ladewig J, Brüstle O (2009) A rosette-type, self-renewing human ES cell-derived neural stem cell with potential for in vitro instruction and synaptic integration. Proc Natl Acad Sci U S A 106(9):3225-3230.
21. Louis SA, Rietze RL, Deleyrolle L, Wagey RE, Thomas TE, Eaves AC, Reynolds BA (2008) Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells 26:988-996.
22. Maitra A, Arking DE, Shivapurkar N, Ikeda M, Stastny V, Kassauei K, Sui G, Cutler DJ, Liu Y, Brimble SN, Noaksson K, Hyllner J, Schulz TC, Zeng X, Freed WJ, Crook J, Abraham S, Colman A, Sartipy P, Matsui S, et al (2005) Genomic alterations in cultured human embryonic stem cells. Nat Genet 37:1099-1103.
23. Mitalipova MM, Rao RR, Hoyer DM, Johnson JA, Meisner LF, Jones KL, Dalton S, Stice SL (2005) Preserving the genetic integrity of human embryonic stem cells. Nat Biotechnol 23:19-20.
24. Muñoz-Sanjuán I, Brivanlou AH (2002) Neural induction, the default model and embryonic stem cells. Nat Rev Neurosci 3:271-280.
25. Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS (2005) Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia 49:385-396.
26. Peerani R, Rao BM, Bauwens C, Yin T, Wood GA, Nagy A, Kumacheva E, Zandstra PW (2007) Niche-mediated control of human embryonic stem cell self renewal and differentiation. EMBO J 26:4744-4755.
27. Piccolo S, Sasai Y, Lu B, De Robertis EM (1996) Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86:589-598.
28. Qiu C, Ma Y, Wang J, Peng S, Huang Y (2010) Lin28-mediated posttranscriptional regulation of Oct4 expression in human embryonic stem cells. Nucleic Acids Res 38:1240-1248.
29. 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.
30. Reynolds BA, Weiss S (1996) Clonal population analyses demonstrate than an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175:1-13.
31. Roy NS, Cleren C, Singh SK, Yang L, Beal MF, Goldman SA (2006) Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized mid-brain astrocytes. Nat Med 12:1259-1268.
32. Sato SM, Sargent TD (1989) Development of neural inducing capacity in dissociated Xenopus embryos. Dev Biol 134:263-266.
33. Schuldiner M, Eiges R, Eden A, Yanuka O, Itskovitz-Eldor J, Goldstein RS, Benvenisty N (2001) Induced neuronal differentiation of human embryonic stem cells. Brain Res 913:201-205.
34. Schulz TC, Noggle SA, Palmarini GM, Weiler DA, Lyons IG, Pensa KA, Meedeniya AC, Davidson BP, Lambert NA, Condie BG (2004) Differentiation of human embryonic stem cells to dopaminergic neurons in suspension culture. Stem Cells 22:1218-1238.
35. Seaberg RM, van der Kooy D (2002) Adult neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci 22:1784-1793.
36. Smukler SR, Runciman SB, Xu S, van der Kooy D (2006) Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J Cell Biol 172:79-90.
37. Sonntag KC, Pruszak J, Yoshizaki T, van Arensbergen J, Sanchez-Pernaute R, Isacson O (2007) Enhanced yield of neuroepithelial precursors and midbrain-like dopaminergic neurons from human embryonic stem cells using the bone morphogenic protein antagonist noggin. Stem Cells 25:411-418.
38. Spemann H, Mangold H (1924) Uber Induktion von embryonanlagen durch implantation artfrender organization. Arch Mikr Anat EntwMech 100:599-638.
39. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663-676.
40. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872.
41. 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.
42. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D (1999) Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208:166-188.
43. Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J, van der Kooy D (2001) Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30:65-78.
44. Ungrin MD, Joshi C, Nica A, Bauwens C, Zandstra PW (2008) Reproducible, ultra high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates. PLoS One 3:e1565.
45. Vallier L, Reynolds D, Pedersen RA (2004) Nodal inhibits differentiation of human embryonic stem cells along the neuroectodermal default pathway. Dev Biol 275:403-421.
46. Vallier L, Touboul T, Chng Z, Brimpari M, Hannan N, Millan E, Smithers LE, Trotter M, Rugg-Gunn P, Weber A, Pedersen RA (2009) Early cell fate decisions of human embryonic stem cells and mouse epiblast stem cells are controlled by the same signaling pathways. PLoS One 4:e6082.
47. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, Wataya T, Takahashi JB, Nishikawa S, Muguruma K, Sasai Y (2007) A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25:681-686.
48. Wilson PA, Hemmati-Brivanlou A (1995) Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376:331-333.
49. Xu C, Rosler E, Jiang J, Lebkowski JS, Gold JD, O'Sullivan C, Delavan-Boorsma K, Mok M, Bronstein A, Carpenter MK (2005a) Basic fibroblast growth factor supports undifferentiated human embryonic stem cell growth without conditioned medium. Stem Cells 23:315-323.
50. Xu RH, Peck RM, Li DS, Feng X, Ludwig T, Thomson JA (2005b) Basic FGF and suppression of BMP signalling sustain undifferentiated proliferation of human ES cells. Nat Methods 2:185-190.
51. Zhang SC, Wernig M, Duncan ID, Brüstle O, Thomson JA (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19:1129-1133.
52. Zimmerman LB, De Jesú s-Escobar JM, Harland RM (1996) The Spemann organizer signal noggin binds and inactivates bone morphogenic protein 4. Cell 86:599-606.