Multipotent caudal neural progenitors derived from human pluripotent stem cells that give rise to lineages of the central and peripheral nervous system

Stem Cells

Volumn 33, Issue 6, 2015, Pages 1759-1770

  Denham, Mark ^a,b   Hasegawa, Kouichi ^c,d   Menheniott, Trevelyan ^e   Rollo, Ben ^e   Zhang, Dongcheng ^e   Hough, Shelley ^a   Alshawaf, Abdullah ^f   Febbraro, Fabia ^b   Ighaniyan, Samiramis ^e   Leung, Jessie ^a   Elliott, David A ^e   Newgreen, Donald F ^e   Pera, Martin F ^a,g,h   Dottori, Mirella ^a,f  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b AARHUS UNIVERSITY   (Denmark)

^c KYOTO UNIVERSITY   (Japan)

^d TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^e MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^h FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

Author keywords

Floor plate; Human embryonic stem cells; Neural crest; Peripheral nervous system; Roof plate

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 8; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN NODAL; SOMATOMEDIN C; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; MESODERM; MULTIPOTENT STEM CELL; NEURAL CREST CELL; NEURAL STEM CELL; NEUROECTODERM; NEUROEPITHELIUM CELL; PERIPHERAL NERVOUS SYSTEM; PLURIPOTENT STEM CELL; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CYTOLOGY; NEURAL CREST; NEURAL TUBE; SPRAGUE DAWLEY RAT;

ERINACEIDAE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; MESODERM; MICE, INBRED C57BL; NEURAL CREST; NEURAL PLATE; NEURAL STEM CELLS; NEURAL TUBE; NEUROEPITHELIAL CELLS; PERIPHERAL NERVOUS SYSTEM; PLURIPOTENT STEM CELLS; RATS, SPRAGUE-DAWLEY;

EID: 84929773702     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1991     Document Type: Article

References (44)

1. Vieira C, Pombero A, Garcia-Lopez R, et al., Molecular mechanisms controlling brain development: An overview of neuroepithelial secondary organizers. Int J Dev Biol 2010; 54: 7-20.
2. Andoniadou CL, Martinez-Barbera JP,. Developmental mechanisms directing early anterior forebrain specification in vertebrates. Cell Mol Life Sci 2013; 70: 3739-3752.
3. Le Dreau G, Marti E,. Dorsal-ventral patterning of the neural tube: A tale of three signals. Dev Neurobiol 2012; 72: 1471-1481.
4. Takemoto T, Uchikawa M, Yoshida M, et al., Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 2011; 470: 394-398.
5. Delfino-Machin M, Lunn JS, Breitkreuz DN, et al., Specification and maintenance of the spinal cord stem zone. Development 2005; 132: 4273-4283.
6. Kondoh H, Takemoto T,. Axial stem cells deriving both posterior neural and mesodermal tissues during gastrulation. Curr Opin Genet Dev 2012; 22: 374-380.
7. Zhang X, Huang CT, Chen J, et al., Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 2010; 7: 90-100.
8. Chambers SM, Fasano CA, Papapetrou EP, et al., Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 2009; 27: 275-280.
9. Kriks S, Shim JW, Piao J, et al., Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 2011; 480: 547-551.
10. Denham M, Bye C, Leung J, et al., Glycogen synthase kinase 3beta and activin/nodal inhibition in human embryonic stem cells induces a pre-neuroepithelial state that is required for specification to a floor plate cell lineage. Stem Cells 2012; 30: 2400-2411.
11. Davis RP, Ng ES, Costa M, et al., Targeting a GFP reporter gene to the MIXL1 locus of human embryonic stem cells identifies human primitive streak-like cells and enables isolation of primitive hematopoietic precursors. Blood 2008; 111: 1876-1884.
12. Conley BJ, Denham M, Gulluyan L, et al., Mouse embryonic stem cell derivation, and mouse and human embryonic stem cell culture and differentiation as embryoid bodies. Curr Protoc Cell Biol 2005;Chapter 23:Unit 23 22.
13. Denham M, Dottori M,. Neural differentiation of induced pluripotent stem cells. Methods Mol Biol 2011; 793: 99-110.
14. Ng ES, Davis R, Stanley EG, et al., A protocol describing the use of a recombinant protein-based, animal product-free medium (APEL) for human embryonic stem cell differentiation as spin embryoid bodies. Nat Protoc 2008; 3: 768-776.
15. Hamburger V, Hamilton HL,. A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 1992; 195: 231-272.
16. Le Douarin NM, Dieterlen-Lievre F, Teillet MA, et al., Interspecific chimeras in avian embryos. Methods Mol Biol 2000; 135: 373-386.
17. Zhang D, Brinas IM, Binder BJ, et al., Neural crest regionalisation for enteric nervous system formation: Implications for Hirschsprung's disease and stem cell therapy. Dev Biol 2010; 339: 280-294.
18. Livak KJ, Schmittgen TD,. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
19. Stoykova A, Fritsch R, Walther C, et al., Forebrain patterning defects in Small eye mutant mice. Development 1996; 122: 3453-3465.
20. Walther C, Gruss P,. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 1991; 113: 1435-1449.
21. Robertshaw E, Matsumoto K, Lumsden A, et al., Irx3 and Pax6 establish differential competence for Shh-mediated induction of GABAergic and glutamatergic neurons of the thalamus. Proc Natl Acad Sci USA 2013; 110: E3919-3926.
22. Kiecker C, Lumsden A,. Hedgehog signaling from the ZLI regulates diencephalic regional identity. Nat Neurosci 2004; 7: 1242-1249.
23. Wassarman KM, Lewandoski M, Campbell K, et al., Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 1997; 124: 2923-2934.
24. Martynoga B, Morrison H, Price DJ, et al., Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev Biol 2005; 283: 113-127.
25. Xuan S, Baptista CA, Balas G, et al., Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 1995; 14: 1141-1152.
26. Oliver G, Mailhos A, Wehr R, et al., Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 1995; 121: 4045-4055.
27. Boncinelli E, Gulisano M, Broccoli V,. Emx and Otx homeobox genes in the developing mouse brain. J Neurobiol 1993; 24: 1356-1366.
28. Larsen KB, Lutterodt MC, Mollgard K, et al., Expression of the homeobox genes OTX2 and OTX1 in the early developing human brain. J Histochem Cytochem 2010; 58: 669-678.
29. Greber B, Coulon P, Zhang M, et al., FGF signalling inhibits neural induction in human embryonic stem cells. Embo J 2011; 30: 4874-4884.
30. Dottori M, Gross MK, Labosky P, et al., The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 2001; 128: 4127-4138.
31. Erskine L, Patel K, Clarke JD,. Progenitor dispersal and the origin of early neuronal phenotypes in the chick embryo spinal cord. Dev Biol 1998; 199: 26-41.
32. Fedtsova NG, Turner EE,. Brn-3.0 expression identifies early post-mitotic CNS neurons and sensory neural precursors. Mech Dev 1995; 53: 291-304.
33. Roelink H, Nusse R,. Expression of two members of the Wnt family during mouse development-restricted temporal and spatial patterns in the developing neural tube. Genes Dev 1991; 5: 381-388.
34. Doble BW, Woodgett JR,. GSK-3: Tricks of the trade for a multi-tasking kinase. J Cell Sci 2003; 116: 1175-1186.
35. Magner NL, Jung Y, Wu J, et al., Insulin and IGFs enhance hepatocyte differentiation from human embryonic stem cells via the PI3K/AKT pathway. Stem Cells 2013; 31: 2095-2103.
36. McLean AB, D'Amour KA, Jones KL, et al., Activin a efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. Stem Cells 2007; 25: 29-38.
37. Singh AM, Reynolds D, Cliff T, et al., Signaling network crosstalk in human pluripotent cells: A Smad2/3-regulated switch that controls the balance between self-renewal and differentiation. Cell Stem Cell 2012; 10: 312-326.
38. Kirkeby A, Grealish S, Wolf DA, et al., Generation of regionally specified neural progenitors and functional neurons from human embryonic stem cells under defined conditions. Cell Reports 2012; 1: 1-12.
39. van Noort M, Meeldijk J, van der Zee R, et al., Wnt signaling controls the phosphorylation status of beta-catenin. J Biol Chem 2002; 277: 17901-17905.
40. Dailey L, Ambrosetti D, Mansukhani A, et al., Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev 2005; 16: 233-247.
41. Torres MA, Eldar-Finkelman H, Krebs EG, et al., Regulation of ribosomal S6 protein kinase-p90(rsk), glycogen synthase kinase 3, and beta-catenin in early Xenopus development. Mol Cell Biol 1999; 19: 1427-1437.
42. Cross DA, Alessi DR, Cohen P, et al., Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995; 378: 785-789.
43. Mica Y, Lee G, Chambers SM, et al., Modeling neural crest induction, melanocyte specification, and disease-related pigmentation defects in hESCs and patient-specific iPSCs. Cell Reports 2013; 3: 1140-1152.
44. Menendez L, Yatskievych TA, Antin PB, et al., Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. Proc Natl Acad Sci USA 2011; 108: 19240-19245.