Derivation and isolation of NKX2.1-positive basal forebrain progenitors from human embryonic stem cells

Stem Cells and Development

Volumn 22, Issue 10, 2013, Pages 1477-1489

  Germain, Noélle D ^a,b   Banda, Erin C ^a   Becker, Sandy ^a   Naegele, Janice R ^a   Grabel, Laura B ^a  

^a WESLEYAN UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX2.1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL POPULATION; CELL SPECIFICITY; CONTROLLED STUDY; DOSE RESPONSE; EMBRYONIC STEM CELL; FLUORESCENCE ACTIVATED CELL SORTING; FOREBRAIN; GABAERGIC SYSTEM; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNEURON; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TELENCEPHALON;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; EMBRYONIC STEM CELLS; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HEDGEHOG PROTEINS; HUMANS; MICE; NEURAL STEM CELLS; NUCLEAR PROTEINS; PROSENCEPHALON; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS;

EID: 84877318515     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0264     Document Type: Article

References (50)

1. Hendry SH, HD Schwark, EG Jones, J Yan. (1987). Numbers, proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7:1503-1519
2. Freund T, G Buzsaki. (1996). Interneurons of the hippocampus. Hippocampus 6:347-470
3. Markram H, M Toledo-Rodriguez, Y Wang, A Gupta, G Silberberg, C Wu. (2004). Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807
4. Fishell G, B Rudy. (2011). Mechanisms of inhibition within the telencephalon: ''where the wild things are.'' Annu Rev Neurosci 34:535-567
5. Sussel L, O Marin, S Kimura, JL Rubenstein. (1999). Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126:3359-3370
6. Wonders CP, SA Anderson. (2006). The origin, specification of cortical interneurons. Nat Rev Neurosci 7:687-695
7. Gelman DM, FJ Martini, S Nobrega-Pereira, A Pierani, N Kessaris, O Marin. (2009). The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci 29:9380-9389
8. Wichterle H, JM Garcia-Verdugo, DG Herrera, A Alvarez-Buylla. (1999). Young neurons from medial ganglionic eminence disperse in adult, embryonic brain. Nat Neurosci 2:461-466
9. Pleasure SJ, S Anderson, R Hevner, A Bagri, O Marin, DH Lowenstein, JL Rubenstein. (2000). Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727-740
10. Butt SJ, M Fuccillo, S Nery, S Noctor, A Kriegstein, JG Corbin, G Fishell. (2005). The temporal, spatial origins of cortical interneurons predict their physiological subtype. Neuron 48:591-604
11. Corbin JG, SJ Butt. (2011). Developmental mechanisms for the generation of telencephalic interneurons. Dev Neurobiol 71:710-732
12. Liodis P, M Denaxa, M Grigoriou, C Akufo-Addo, Y Yanagawa, V Pachnis. (2007). Lhx6 activity is required for the normal migration, specification of cortical interneuron subtypes. J Neurosci 27:3078-3089
13. Nobrega-Pereira S, N Kessaris, T Du, S Kimura, SA Anderson, O Marin. (2008). Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 59:733-745
14. Nat R, G Dechant. (2011). Milestones of directed differentiation of mouse, human embryonic stem cells into telencephalic neurons based on neural development in vivo. Stem Cells Dev 20:947-958
15. Marin O, J Baker, L Puelles, JL Rubenstein. (2002). Patterning of the basal telencephalon, hypothalamus is essential for guidance of cortical projections. Development 129:761-773
16. Ericson J, J Muhr, M Placzek, T Lints, T Jessell, T Edlund. (1995). Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell 81:747-756
17. Yu W, Y Wang, K McDonnell, D Stephen, CB Bai. (2009). Patterning of ventral telencephalon requires positive function of Gli transcription factors. Dev Biol 334:264-275
18. Wonders CP, L Taylor, J Welagen, IC Mbata, JZ Xiang, SA Anderson. (2008). A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Dev Biol 314:127-136
19. Xu Q, CP Wonders, SA Anderson. (2005). Sonic hedgehog maintains the identity of cortical interneuron progenitors in the ventral telencephalon. Development 132: 4987-4998
20. Xu Q, L Guo, H Moore, RR Waclaw, K Campbell, SA Anderson. (2010). Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates. Neuron 65:328-340
21. Stenman JM, B Wang, K Campbell. (2003). Tlx controls proliferation, patterning of lateral telencephalic progenitor domains. J Neurosci 23:10568-10576
22. Sousa VH, G Miyoshi, J Hjerling-Leffler, T Karayannis, G Fishell. (2009). Characterization of Nkx6-2-derived neocortical interneuron lineages. Cereb Cortex 19 Suppl 1:i1-10
23. Jakovcevski I, N Mayer, N Zecevic. (2011). Multiple origins of human neocortical interneurons are supported by distinct expression of transcription factors. Cereb Cortex 21:1771-1782
24. Rakic S, N Zecevic. (2003). Emerging complexity of layer I in human cerebral cortex. Cereb Cortex 13:1072-1083
25. Westmoreland JJ, CR Hancock, BG Condie. (2001). Neuronal development of embryonic stem cells: a model of GABAergic neuron differentiation. Biochem Biophys Res Commun 284:674-680
26. Barberi T, P Klivenyi, NY Calingasan, H Lee, H Kawamata, K Loonam, AL Perrier, J Bruses, ME Rubio, et al. (2003). Neural subtype specification of fertilization, nuclear transfer embryonic stem cells, application in parkinsonian mice. Nat Biotechnol 21:1200-1207
27. Danjo T, M Eiraku, K Muguruma, K Watanabe, M Kawada, Y Yanagawa, JL Rubenstein, Y Sasai. (2011). Subregional specification of embryonic stem cell-derived ventral telencephalic tissues by timed, combinatory treatment with extrinsic signals. J Neurosci 31:1919-1933
28. Bissonnette CJ, L Lyass, BJ Bhattacharyya, A Belmadani, RJ Miller, JA Kessler. (2011). The controlled generation of functional basal forebrain cholinergic neurons from human embryonic stem cells. Stem Cells 29:802-811
29. Li XJ, X Zhang, MA Johnson, ZB Wang, T Lavaute, SC Zhang. (2009). Coordination of sonic hedgehog, Wnt signaling determines ventral, dorsal telencephalic neuron types from human embryonic stem cells. Development 136:4055-4063
30. Ma L, B Hu, Y Liu, SC Vermilyea, H Liu, L Gao, Y Sun, X Zhang, SC Zhang. (2012). Human embryonic stem cellderived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice. Cell Stem Cell 10:455-464
31. Goulburn AL, D Alden, RP Davis, SJ Micallef, ES Ng, QC Yu, SM Lim, CL Soh, DA Elliott, et al. (2011). A targeted NKX2.1 human embryonic stem cell reporter line enables identification of human basal forebrain derivatives. Stem Cells 29:462-473
32. Gerrard L, L Rodgers, W Cui. (2005). Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells 23:1234-1241
33. Zhang X, CT Huang, J Chen, MT Pankratz, J Xi, J Li, Y Yang, TM Lavaute, XJ Li, et al. (2010). Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 7:90-100
34. Marin O, SA Anderson, JL Rubenstein. (2000). Origin, molecular specification of striatal interneurons. J Neurosci 20:6063-6076
35. Ohyama K, P Ellis, S Kimura, M Placzek. (2005). Directed differentiation of neural cells to hypothalamic dopaminergic neurons. Development 132:5185-5197
36. Conti L, SM Pollard, T Gorba, E Reitano, M Toselli, G Biella, Y Sun, S Sanzone, QL Ying, E Cattaneo, A Smith. (2005). Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3:e283
37. Song HJ, CF Stevens, FH Gage. (2002). Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5:438-445
38. de Lanerolle NC, JH Kim, RJ Robbins, DD Spencer. (1989). Hippocampal interneuron loss, plasticity in human temporal lobe epilepsy. Brain Res 495:387-395
39. Magloczky Z, L Wittner, Z Borhegyi, P Halasz, J Vajda, S Czirjak, T Freund. (2000). Changes in the distribution, connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience 96:7-25
40. Morimoto K, M Fahnestock, RJ Racine. (2004). Kindling, status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73:1-60
41. Houser CR, JE Miyashiro, BE Swartz, GO Walsh, JR Rich, AV Delgado-Escueta. (1990). Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10:267-282
42. Shibley H, BN Smith. (2002). Pilocarpine-induced status epilepticus results in mossy fiber sprouting, spontaneous seizures in C57BL/6, CD-1 mice. Epilepsy Res 49: 109-120
43. Obenaus A, M Esclapez, CR Houser. (1993). Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J Neurosci 13:4470-4485
44. Thind KK, R Yamawaki, I Phanwar, G Zhang, X Wen, PS Buckmaster. (2010). Initial loss but later excess of GABAergic synapses with dentate granule cells in a rat model of temporal lobe epilepsy. J Comp Neurol 518:647-667
45. Baraban SC, DG Southwell, RC Estrada, DL Jones, JY Sebe, C Alfaro-Cervello, JM Garcia-Verdugo, JL Rubenstein, A Alvarez-Buylla. (2009). Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice. Prot Natl Acad Sci U S A 106:15472-15477
46. Zipancic I, ME Calcagnotto, M Piquer-Gil, LE Mello, M Alvarez-Dolado. (2010). Transplant of GABAergic precursors restores hippocampal inhibitory function in a mouse model of seizure susceptibility. Cell Transplant 19:549-564
47. Calcagnotto ME, LP Ruiz, MM Blanco, JG Santos-Junior, MF Valente, C Patti, R Frussa-Filho, MF Santiago, I Zipancic, et al. (2010). Effect of neuronal precursor cells derived from medial ganglionic eminence in an acute epileptic seizure model. Epilepsia 51 Suppl 3:71-75
48. Tagliatela S, E Litvina, X Maisano, N Woods, M Vallo, S Royston, J Gupta, Y Yanagawa, JR Naegele. (2011). Long-term functional integration, persistent seizure suppression by hilar but not entorhinal cortex grafts of fetal GABAergic interneuron progenitors in mice with temporal lobe epilepsy. In: American Epilepsy Society 65th Annual Meeting. Baltimore, MD
49. Cai C, J Thorne, L Grabel. (2008). Hedgehog serves as a mitogen, survival factor during embryonic stem cell neurogenesis. Stem Cells 26:1097-1108
50. Maisano X, E Litvina, S Tagliatela, GB Aaron, LB Grabel, JR Naegele. (2012). Differentiation, functional incorporation of embryonic stem cell-derived GABAergic interneurons in the dentate gyrus of mice with temporal lobe epilepsy. J Neurosci 32:46-61