Differentiation of human embryonic stem cells to regional specific neural precursors in chemically defined medium conditions

PLoS ONE

Volumn 3, Issue 5, 2008, Pages

  Erceg, Slaven ^a   Laínez, Sergio ^a   Ronaghi, Mohammad ^a   Stojkovic, Petra ^a   Pérez Aragó, Maria Amparo ^a   Moreno Manzano, Victoria ^a   Moreno Palanques, Rubén ^a   Planells Cases, Rosa ^a   Stojkovic, Miodrag ^a  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT BASIC FIBROBLAST GROWTH FACTOR; RETINOIC ACID; RNA;

ARTICLE; CELL LINEAGE; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; DOPAMINERGIC NERVE CELL; EMBRYO; EMBRYONIC STEM CELL; ENDODERM; FOREBRAIN; HUMAN; HUMAN CELL; IN VITRO STUDY; MESODERM; MOTONEURON; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEURAL STEM CELL; NEUROTRANSMISSION; PATCH CLAMP; ROSETTE FORMATION; SPINAL CORD NERVE CELL; STROMA CELL; ANTIBODY SPECIFICITY; CELL DIFFERENTIATION; CELL LINE; CULTURE TECHNIQUE; CYTOLOGY; ELECTROPHYSIOLOGY; EMBRYO DEVELOPMENT; GENETICS; IMMUNOHISTOCHEMISTRY; ISOLATION AND PURIFICATION; METHODOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CULTURE MEDIA; ELECTROPHYSIOLOGY; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; NEURONS; ORGAN SPECIFICITY; PATCH-CLAMP TECHNIQUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA;

EID: 47749108736     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002122     Document Type: Article

References (62)

1. Odorico JS, Kaufman DS, Thomson JA (2001) Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19: 193-204.
2. Schuldiner M, Eiges R, Eden A, Yanuka O, Itskovitz-Eldor J, et al. (2001) Induced neuronal differentiation of human embryonic stem cells. Brain Res 913: 201-205.
3. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19: 1129-1133.
4. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, et al. (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25: 4694-4705.
5. Carpenter MK, Inokuma MS, Denham J, Mujtaba T, Chiu CP, et al. (2001) Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol 172: 383-397.
6. Gerrard L, Rodgers L, Cui W (2005) Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells 23: 1234-1241.
7. Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, et al. (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28: 31-40.
8. Kawasaki H, Suemori H, Mizuseki K, Watanabe K, Urano F, et al. (2002) Generation of dopaminergic, neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. Proc Natl Acad Sci U S A 99: 1580-1585.
9. Reubinoff BE, Itsykson P, Turetsky T, Pera MF, Reinhartz E, et al. (2001) Neural progenitors from human embryonic stem cells. Nat Biotechnol 19: 1134-1140.
10. Yao S, Chen S, Clark J, Han E, Beattie GM, et al. (2006) Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions. Proc Natl Acad Sci U S A 103: 6907-6912.
11. Joannides AJ, Fiore-Heriche C, Battersby AA, Athauda-Arachchi P, Boubon IA, et al. (2007) A scaleable and defined system for generating neural stem cells from human embryonic stem cells. Stem Cells 25: 731-737.
12. Nat R, Nilbratt M, Narkilahti S, Winblad B, Hovatta O, et al. (2007) Neurogenic: neuroepithelial and radial glial cells generated from six human embryonic stem cell lines in serum-free suspension and adherent cultures. Glia 55: 385-399.
13. Shin S, Mitalipova M, Noggle S, Tibbitts D, Venable A, et al. (2006) Long-term proliferation of human embryonic stem cell-derived neuroepithelial cells using defined adherent culture conditions. Stem Cells 24: 125-138.
14. Benzing C, Segschneider M, Leinhaas A, Itskovitz-Eldor J, Brustle O (2006) Neural conversion of human embryonic stem cell colonies in the presence of fibroblast growth factor-2. Neuroreport 17: 1675-1681.
15. Itsykson P, Houz N, Turetsky T, Goldstein RS, Pera MF, et al. (2005) Derivation of neural precursors from human embryonic stem cells in the presence of noggin. Mol Cell Neurosci 30: 24-36.
16. Ludwig TE, Levenstein ME,Jones JM, Berggren WT, Mitchen ER, et al. (2006) Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24: 185-187.
17. Bibel M, Richter J, Schrenk K, Tucker KL, Staiger V, et al. (2004) Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat Neurosci 7: 1003-1009.
18. Zhou Q Wang S, Anderson DJ (2000) Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25: 331-343.
19. Zhou Y, Yamamoto M, Engel JD (2000) GATA2 is required for the generation of V2 interneurons. Development 127: 3829-3838.
20. Tao W, Lai E (1992) Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 8: 957-966.
21. Xuan S, Baptista CA, Balas G, Tao W, Soares VC, et al. (1995) Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14: 1141-1152.
22. Broccoli V, Boncinelli E, Wurst W (1999) The caudal limit of Otx2 expression positions the isthmic organizer. Nature 401: 164-168.
23. Joyner AL (1996) Engrailed, Wnt and Pax genes regulate midbrain-hindbrain development. Trends Genet 12: 15-20.
24. Cheng L, Chen CL, Luo P, Tan M, Qiu M, et al. (2003) Lmxlb, Pet-1, and Nkx2.2 coordinately specify serotonergic neurotransmitter phenotype. J Neurosci 23:9961-9967.
25. Ding YQ, Marklund U, Yuan W, Yin J, Wegman L, et al. (2003) Lmxlb is essential for the development of serotonergic neurons. Nat Neurosci 6: 933-938.
26. Kania A, Jessell TM (2003) Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38: 581-596.
27. Kania A, Johnson RL, Jessell TM (2000) Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102: 161-173.
28. Davidson D, Graham E, Sime C, Hill R (1988) A gene with sequence siradarity to Drosophila engrailed is expressed during the development of the neural tube and vertebrae in the mouse. Development 104: 305-316.
29. Wallén A, Zetterström RH, Solomin L, Arvidsson M, Olson L, et al. (1999) Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. Exp Cell Res 253: 737-746.
30. Zetterström RH, Solomin L, Jansson L, Hoffer BJ, Olson L, et al. (1997) Dopamine neuron agenesis in Nurrl-deficient mice. Science 276: 248-250.
31. Saucedo-Cardenas O, Quintana-Hau JD, Le WD, Smidt MP, Cox JJ, et al. (1998) Nurrl is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc Natl Acad Sci USA 95: 4013-4018.
32. Le W, Conneely OM, Zou L, He Y, Saucedo-Cardenas O, et al. (1999) Selective agenesis of mesencephalic dopaminergic neurons in Nurrl-deficient mice. ExpNeurol 159: 451-458.
33. Briscoe J, Ericson J (2001) Specification of neuronal fates in the ventral neural tube. Curr Opin Neurobiol 11: 43-49.
34. Jessell TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1: 20-29.
35. Burke AC, Nelson CE, Morgan BA, Tabin C (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121: 333-346.
36. Li XJ, Du ZW, Zarnowska ED, Pankratz, M, Hansen LO, et al. (2005) Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 23: 215-221.
37. Roybon L, Brundin P, Li JY (2005) Stromal cell-derived inducing activity does not promote dopaminergic differentiation, but enhances differentiation and proliferation of neural stem cell-derived astrocytes. Exp Neurol 196: 373-380.
38. Dhara SK, Hasneen K, Machacek DW, Boyd NL, Rao RR, et al. (2008) Human neural progenitor cells derived from embryonic stem cells in feeder-free cultures. Differentiation doi/abs/ 10.1111/j.1432-0436.2007.00256.x.
39. Jelitai M, Anderova M, Chvatal A, Madarasz E (2007) Electrophysiological characterization of neural stem/progenitor cells during in vitro differentiation: study with an immortalized neuroectodermal cell line. J Neurosci Res 85: 1606-1617.
40. Belluzzi O, Benedusi M, Ackman J, LoTurco JJ (2003) Electrophysiological differentiation of new neurons in the olfactory bulb. J Neurosci 23: 10411-10418.
41. Pagani F, Lauro C, Fucile S,.Catalano M, Limatola C, et al. (2006) Functional properties of neurons derived from fetal mouse neurospheres are compatible with those of neuronal precursors in vivo. J Neurosci Res 83: 1494-1501.
42. Tyzio R, Repress A, Jorquera I, Ben-Ari Y, Gozlan H, et al. (1999) The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J Neurosci 19: 10372-10382.
43. Yan Y, Yang D, Zarnowska ED, Du Z, Werbel B, et al. (2005) Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells 23: 781-790.
44. Mizuseki K, Sakamoto T, Watanabe K, Muguruma K, Ikeya M, et al. (2003) Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells. Proc Natl Acad Sci U S A 100: 5828-5833.
45. Munoz-Sarjuan I, Brivanlou AH (2002) Neural induction, the default model and embryonic stem cells. Nat Rev Neurosci 3: 271-280.
46. Du ZW, Zhang SC (2004) Neural differentiation from embryonic stem cells: which way? Stem Cells Dev 13: 372-381.
47. Pankratz MT, Li XJ, Lavaute TM, Lyons EA, Chen X, et al. (2007) Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 25: 1511-1520.
48. Watanabe K, Kamiya D, Nishiyama A, Katayama T, Nozaki S, et al. (2005) Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 8: 288-296.
49. Sakurada K, Ohshima-Sakurada M, Palmer TD, Gage FH (1999) Nurrl, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain. Development 126: 4017-4026.
50. Simon HH, Thuret S, Alberi L (2004) Midbrain dopaminergic neurons: control of their cell fate by the engrailed transcription factors. Cell Tissue Res 318: 53-61.
51. Ye W, Shimmura K, Rubenstein JL, Hynes MA, Rosenthal A (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the aniterior neural plate. Cell 93: 755-766.
52. Cepeda C, Buchwald NA, Levine MS (1993) Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc Natl Acad Sci U S A 90: 9576-9580.
53. Freed WJ, Chen J, Backman CM, Schwartz CM, Vazin T, et al. (2008) Gene expression profile of neuronal progenitor cells derived from hESCs: activation of chromosome 11p15.5 and comparison to human dopaminergic neurons. PLoS ONE 3: e1422.
54. Perrier AL, Tabar V, Barberi T, Rubio ME, BrusesJ, et al. (2004) Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A 101: 12543-12548.
55. Nordstrom U, Maier E, Jessell TM, Edlund T (2006) An early role for WNT signaling in specifying neural patterns of Cris and Hex gene expression and motor neuron subtype identity. PLoS Biol 4: e252.
56. Bel-Vialar S, Itasaki N, Krumlauf R (2002) Initiating Hex gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 129: 5103-5115.
57. Liu JP, Laufer E, Jessell TM (2001) Assigning the positional identity of spinal motor neurons: rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 32: 997-1012.
58. Muhr J, Graziano E, Wilson S, Jessell TM, Edlund T (1999) Convergent inductive signals specify midbrain, hindbrain, and spinal cord identity in gastrula stage chick embryos. Neuron 23: 689-702.
59. Novitch BG, Chen AI,Jessell TM (2001) Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31: 773-789.
60. Ko JY, Park CH, Koh HC, Cho YH, Kyhm JH, et al. (2007) Human embryonic stem cell-derived neural precursors as a continuous, stable, and on-demand source for human dopamine neurons. J Neurochem 103: 1417-1429.
61. Li XJ, Hu BY, Jones SA, Zhang YS, Lavaute T, et al. (2008) Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells doi:lO.1634/ stemcells. 2007-0620.
62. Dottori M, Leung J, Turnley AM, Pebay A (2008) Lysophosphatidic acid inhibits neuronal differentiation of neural stem/progenitor cells derived from human embryonic stem cells. Stem Cells doi:10.1634/ stemcells.2007-1118.