Embryonic stem cells neural differentiation qualifies the role of Wnt/β-Catenin signals in human telencephalic specification and regionalization

Stem Cells

Volumn 31, Issue 9, 2013, Pages 1763-1774

  Nicoleau, Camille ^a   Varela, Christine ^a   Bonnefond, Caroline ^a   Maury, Yves ^a   Bugi, Aurore ^a   Aubry, Laetitia ^a   Viegas, Pedro ^a   Bourgois Rocha, Fany ^a   Peschanski, Marc ^a   Perrier, Anselme L ^a  

^a I Stem   (France)

Author keywords

Cell therapy; Developmental biology; Forebrain specification; Huntington disease; Neural differentiation; Pluripotent stem cells; Striatum

Indexed keywords

BETA CATENIN; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ARTICLE; BRAIN REGION; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; IN VITRO STUDY; IN VIVO STUDY; PROTEIN FUNCTION; TELENCEPHALON;

CELL THERAPY; DEVELOPMENTAL BIOLOGY; FOREBRAIN SPECIFICATION; HUNTINGTON DISEASE; NEURAL DIFFERENTIATION; PLURIPOTENT STEM CELLS; STRIATUM;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; HEDGEHOG PROTEINS; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; HUNTINGTON DISEASE; MICE; NEURONS; ORGAN SPECIFICITY; RATS; TELENCEPHALON; WNT SIGNALING PATHWAY;

EID: 84885163028     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1462     Document Type: Article

References (53)

1. Ciani L, Salinas PC,. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 2005; 6: 351-362.
2. Echevarria D, Vieira C, Gimeno L, et al. Neuroepithelial secondary organizers and cell fate specification in the developing brain. Brain Res Brain Res Rev 2003; 43: 179-191.
3. Kiecker C, Niehrs C,. A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development 2001; 128: 4189-4201.
4. Glinka A, Wu W, Delius H, et al. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 1998; 391: 357-362.
5. Kazanskaya O, Glinka A, Niehrs C,. The role of Xenopus dickkopf1 in prechordal plate specification and neural patterning. Development 2000; 127: 4981-4992.
6. Mukhopadhyay M, Shtrom S, Rodriguez-Esteban C, et al. Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev Cell 2001; 1: 423-434.
7. Backman M, Machon O, Mygland L, et al. Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev Biol 2005; 279: 155-168.
8. Shimamura K, Rubenstein JL,. Inductive interactions direct early regionalization of the mouse forebrain. Development 1997; 124: 2709-2718.
9. Danesin C, Peres JN, Johansson M, et al. Integration of telencephalic Wnt and hedgehog signaling center activities by Foxg1. Dev Cell 2009; 16: 576-587.
10. Pera MF, Trounson AO,. Human embryonic stem cells: prospects for development. Development 2004; 131: 5515-5525.
11. Danjo T, Eiraku M, Muguruma K, et al. Subregional specification of embryonic stem cell-derived ventral telencephalic tissues by timed and combinatory treatment with extrinsic signals. J Neurosci 2011; 31: 1919-1933.
12. Nat R, Salti A, Suciu L, et al. Pharmacological modulation of the hedgehog pathway differentially affects dorsal/ventral patterning in mouse and human embryonic stem cell models of telencephalic development. Stem Cells Dev 2012; 21: 1016-1046.
13. Watanabe K, Ueno M, Kamiya D, et al. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 2007; 8: 288-296.
14. Aubry L, Bugi A, Lefort N, et al. Striatal progenitors derived from human ES cells mature into DARPP32 neurons in vitro and in quinolinic acid-lesioned rats. Proc Natl Acad Sci U S A 2008; 105: 16707-16712.
15. Li XJ, Zhang X, Johnson MA, et al. Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development 2009; 136: 4055-4063.
16. Mariani J, Simonini MV, Palejev D, et al. Modeling human cortical development in vitro using induced pluripotent stem cells. Proc Natl Acad Sci U S A 2012; 109: 12770-12775.
17. Feyeux M, Bourgois-Rocha F, Redfern A, et al. Early transcriptional changes linked to naturally occurring Huntington's disease mutations in neural derivatives of human embryonic stem cells. Hum Mol Genet 2012; 21: 3883-3895.
18. 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.
19. Benchoua A, Aubry L, Perrier A,. Method and medium for neural differentiation of pluripotent cells. EP2356218A1, WO/2010/063848; 2008.
20. Bulfone A, Puelles L, Porteus M, et al. Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 125 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci 1993; 13: 3155-3227.
21. Martinez-Ferre A, Navarro-Garberi M, Bueno C, et al. Wnt signal specifies the intrathalamic limit and its organizer properties by regulating Shh induction in the alar plate. J Neurosci 2013; 33: 3967-3980.
22. Wilson L, Maden M,. The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev Biol 2005; 282: 1-13.
23. Carri AD, Onorati M, Lelos MJ, et al. Developmentally coordinated extrinsic signals drive human pluripotent stem cell differentiation toward authentic DARPP-32+ medium-sized spiny neurons. Development 2013; 140: 301-312.
24. Ma L, Hu B, Liu Y, et al. Human embryonic stem cell-derived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice. Cell Stem Cell 2012; 10: 455-464.
25. Zhang X, Huang CT, Chen J, et al. Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 2010; 7: 90-100.
26. Mo Z, Zecevic N,. Is Pax6 Critical for neurogenesis in the human fetal brain? Cereb Cortex 2007; 5: 1305-1310.
27. Larsen KB, Lutterodt MC, Laursen H, et al. Spatiotemporal distribution of PAX6 and MEIS2 expression and total cell numbers in the ganglionic eminence in the early developing human forebrain. Dev Neurosci 2010; 32: 149-162.
28. Ouimet CC, Greengard P,. Distribution of DARPP-32 in the basal ganglia: an electron microscopic study. J Neurocytol 1990; 19: 39-52.
29. Walaas SI, Greengard P,. DARPP-32, a dopamine- and adenosine 3′:5′-monophosphate-regulated phosphoprotein enriched in dopamine-innervated brain regions. I. Regional and cellular distribution in the rat brain. J Neurosci 1984; 4: 84-98.
30. Waldvogel HJ, Faull RL, Williams MN, et al. Differential sensitivity of calbindin and parvalbumin immunoreactive cells in the striatum to excitotoxins. Brain Res 1991; 546: 329-335.
31. Holt DJ, Graybiel AM, Saper CB,. Neurochemical architecture of the human striatum. J Comp Neurol 1997; 384: 1-25.
32. Cicchetti F, Beach TG, Parent A,. Chemical phenotype of calretinin interneurons in the human striatum. Synapse 1998; 30: 284-297.
33. Tao W, Lai E,. Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 1992; 8: 957-966.
34. Eagleson KL, Schlueter McFadyen-Ketchum LJ, Ahrens ET, et al. Disruption of Foxg1 expression by knock-in of cre recombinase: effects on the development of the mouse telencephalon. Neuroscience 2007; 148: 385-399.
35. Arlotta P, Molyneaux BJ, Jabaudon D, et al. Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J Neurosci 2008; 28: 622-632.
36. Brene S, Lindefors N, Ehrlich M, et al. Expression of mRNAs encoding ARPP-16/19, ARPP-21, and DARPP-32. Human Brain Tissue J Neurosci 1994; 14: 985-998.
37. Ivkovic S, Ehrlich ME,. Expression of the striatal DARPP-32/ARPP-21 phenotype in GABAergic neurons requires neurotrophins in vivo and in vitro. J Neurosci 1999; 19: 5409-5419.
38. Saavedra A, Giralt A, Rue L, et al. Striatal-enriched protein tyrosine phosphatase expression and activity in Huntington's disease: a STEP in the resistance to excitotoxicity. J Neurosci 2011; 31: 8150-8162.
39. Hutcherson L, Roberts RC,. The immunocytochemical localization of substance P in the human striatum: a postmortem ultrastructural study. Synapse 2005; 57: 191-201.
40. Levine AJ, Brivanlou AH,. Proposal of a model of mammalian neural induction. Dev Biol 2007; 308: 247-256.
41. Perrier AL, Tabar V, Barberi T, et al. Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A 2004; 101: 12543-12548.
42. Kirkeby A, Grealish S, Wolf Daniel A, et al. Generation of regionally specified neural progenitors and functional neurons from human embryonic stem cells under defined conditions. Cell Reports 2012; 1: 703-714.
43. 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.
44. Simeone A, Acampora D, Mallamaci A, et al. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J 1993; 12: 2735.
45. 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.
46. Hashimoto H, Itoh M, Yamanaka Y, et al. Zebrafish Dkk1 functions in forebrain specification and axial mesendoderm formation. Dev Biol 2000; 217: 138-152.
47. Grove EA, Tole S, Limon J, et al. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 1998; 125: 2315-2325.
48. Augustine C, Gunnersen J, Spirkoska V, et al. Place-and time-dependent expression of mouse sFRP-1 during development of the cerebral neocortex. Mech Dev 2001; 109: 395-792.
49. Quinlan R, Graf M, Mason I, et al. Complex and dynamic patterns of Wnt pathway gene expression in the developing chick forebrain. Neural Dev 2009; 4: 35.
50. Perrier A, Peschanski M,. How can human pluripotent stem cells help decipher and cure Huntington's disease? Cell Stem Cell 2012; 11: 153-161.
51. Bachoud-Levi AC, Gaura V, Brugieres P, et al. Effect of fetal neural transplants in patients with Huntington's disease 6 years after surgery: a long-term follow-up study. Lancet Neurol 2006; 5: 303-309.
52. Bachoud-Levi AC, Remy P, Nguyen JP, et al. Motor and cognitive improvements in patients with Huntington's disease after neural transplantation. Lancet 2000; 356: 1975-1979.
53. Nicoleau C, Viegas P, Peschanski M, et al. Human pluripotent stem cell therapy for Huntington's disease: technical, immunological, and safety challenges human pluripotent stem cell therapy for Huntington's disease: technical, immunological, and safety challenges. Neurotherapeutics 2011; 8: 562-576.