Striatal cholinergic interneurons in isolated generalized dystonia-rationale and perspectives for stem cell-derived cellular models

Frontiers in Cellular Neuroscience

Volumn 8, Issue JULY, 2014, Pages

  Capetian, Philipp ^a   Pauly, Martje Gesine ^a   Azmitia, Luis Manuel ^b   Klein, Christine ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Development; Differentiation; Disease modeling; Dystonia; Induced pluripotent neurons; Striatal interneurons

Indexed keywords

EID: 84905163975     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00205     Document Type: Review

References (92)

1. Albanese, A., Bhatia, K., Bressman, S. B., Delong, M. R., Fahn, S., Fung, V. S. C., et al. (2013). Phenomenology and classification of dystonia: a consensus update. Mov. Disord.28, 863-873. doi: 10.1002/mds.25475
2. Anderson, S., Mione, M., Yun, K., and Rubenstein, J. L. (1999). Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogenesis. Cereb. Cortex.9, 646-654. doi: 10.1093/cercor/9.6.646
3. Aosaki, T., Tsubokawa, H., Ishida, A., Watanabe, K., Graybiel, A. M., and Kimura, M. (1994). Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning.J. Neurosci.14, 3969-3984.
4. Asanuma, K., Ma, Y., Okulski, J., Dhawan, V., Chaly, T., Carbon, M., et al. (2005). Decreased striatal D2 receptor binding in non-manifesting carriers of the DYT1 dystonia mutation. Neurology.64, 347-349. doi: 10.1212/01.wnl.0000149764.34953.bf
5. Backman, M., Machon, O., Mygland, L., van den Bout, C. J., Zhong, W., Taketo, M. M., et al. (2005). Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev. Biol.279, 155-168. doi: 10.1016/j.ydbio.2004.12.010
6. Bennett, B. D., and Wilson, C. J. (1999). Spontaneous activity of neostriatal cholinergic interneurons in vitro. J. Neurosci.19, 5586-5596.
7. Bissonnette, C. J., Lyass, L., Bhattacharyya, B. J., Belmadani, A., Miller, R. J., and Kessler, J. A. (2011). The controlled generation of functional basal forebrain cholinergic neurons from human embryonic stem cells. Stem Cells.29, 802-811. doi: 10.1002/stem.626
8. Bjorklund, A., and Kordower, J. H. (2013). Cell therapy for Parkinson's disease: what next? Mov. Disord.28, 110-115. doi: 10.1002/mds.25343
9. Butt, S. J. B., Sousa, V. H., Fuccillo, M. V., Hjerling-Leffler, J., Miyoshi, G., Kimura, S., et al. (2008). The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron.59, 722-732. doi: 10.1016/j.neuron.2008.07.031
10. Cabrera-Vera, T. M., Hernandez, S., Earls, L. R., Medkova, M., Sundgren-Andersson, A. K., Surmeier, D. J., et al. (2004). RGS9-2 modulates D2 dopamine receptor-mediated Ca2+ channel inhibition in rat striatal cholinergic interneurons. Proc. Natl. Acad. Sci. U S A.101, 16339-16344. doi: 10.1073/pnas.0407416101
11. Caldwell, G. A., Cao, S., Sexton, E. G., Gelwix, C. C., Bevel, J. P., and Caldwell, K. A. (2003). Suppression of polyglutamine-induced protein aggregation in Caenorhabditis elegans by torsin proteins. Hum. Mol. Genet.12, 307-319. doi: 10.1093/hmg/12.3.307
12. Caneparo, L., Huang, Y.-L., Staudt, N., Tada, M., Ahrendt, R., Kazanskaya, O., et al. (2007). Dickkopf-1 regulates gastrulation movements by coordinated modulation of Wnt/beta catenin and Wnt/PCP activities, through interaction with the Dally-like homolog Knypek. Genes Dev.21, 465-480. doi: 10.1101/gad.406007
13. Cao, S., Gelwix, C. C., Caldwell, K. A., and Caldwell, G. A. (2005). Torsin-mediated protection from cellular stress in the dopaminergic neurons of Caenorhabditis elegans. J. Neurosci.25, 3801-3812. doi: 10.1523/jneurosci.5157-04.2005
14. Carbon, M., Argyelan, M., and Eidelberg, D. (2010a). Functional imaging in hereditary dystonia. Eur. J. Neurol.7(Suppl. 1), 58-64. doi: 10.1111/j.1468-1331.2010.03054.x
15. Carbon, M., Argyelan, M., Habeck, C., Ghilardi, M. F., Fitzpatrick, T., Dhawan, V., et al. (2010b). Increased sensorimotor network activity in DYT1 dystonia: a functional imaging study. Brain.133, 690-700. doi: 10.1093/brain/awq017
16. Carr, D. B., Day, M., Cantrell, A. R., Held, J., Scheuer, T., Catterall, W. A., et al. (2003). Transmitter modulation of slow, activity-dependent alterations in sodium channel availability endows neurons with a novel form of cellular plasticity. Neuron.39, 793-806. doi: 10.1016/s0896-6273(03)00531-2
17. Chambers, S. M., Fasano, C. A., Papapetrou, E. P., Tomishima, M., Sadelain, M., and Studer, L. (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol.27, 275-280. doi: 10.1038/nbt.1529
18. Cho, G.-S., Choi, S.-C., and Han, J.-K. (2013). BMP signal attenuates FGF pathway in anteroposterior neural patterning. Biochem. Biophys. Res. Commun.434, 509-515. doi: 10.1016/j.bbrc.2013.03.105
19. Crompton, L. A., Byrne, M. L., Taylor, H., Kerrigan, T. L., Bru-Mercier, G., Badger, J. L., et al. (2013). Stepwise, non-adherent differentiation of human pluripotent stem cells to generate basal forebrain cholinergic neurons via hedgehog signaling. Stem Cell Res.11, 1206-1221. doi: 10.1016/j.scr.2013.08.002
20. Dang, M. T., Yokoi, F., Cheetham, C. C., Lu, J., Vo, V., Lovinger, D. M., et al. (2012). An anticholinergic reverses motor control and corticostriatal LTD deficits in Dyt1 ΔGAG knock-in mice. Behav. Brain Res.226, 465-472. doi: 10.1016/j.bbr.2011.10.002
21. Danjo, T., Eiraku, M., Muguruma, K., Watanabe, K., Kawada, M., Yanagawa, Y., et al. (2011). Subregional specification of embryonic stem cell-derived ventral telencephalic tissues by timed and combinatory treatment with extrinsic signals. J. Neurosci.31, 1919-1933. doi: 10.1523/JNEUROSCI.5128-10.2011
22. Deacon, T. W., Pakzaban, P., and Isacson, O. (1994). The lateral ganglionic eminence is the origin of cells committed to striatal phenotypes: neural transplantation and developmental evidence. Brain Res.668, 211-219. doi: 10.1016/0006-8993(94)90526-6
23. Diep, D. B., Hoen, N., Backman, M., Machon, O., and Krauss, S. (2004). Characterisation of the Wnt antagonists and their response to conditionally activated Wnt signalling in the developing mouse forebrain. Brain Res. Dev. Brain Res.153, 261-270. doi: 10.1016/j.devbrainres.2004.09.008
24. Ding, J. B., Guzman, J. N., Peterson, J. D., Goldberg, J. A., and Surmeier, D. J. (2010). Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron.67, 294-307. doi: 10.1016/j.neuron.2010.06.017
25. Du, T., Xu, Q., Ocbina, P. J., and Anderson, S. A. (2008). NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development.135, 1559-1567. doi: 10.1242/dev.015123
26. Duan, L., Bhattacharyya, B. J., Belmadani, A., Pan, L., Miller, R. J., and Kessler, J. A. (2014). Stem cell derived basal forebrain cholinergic neurons from Alzheimer's disease patients are more susceptible to cell death. Mol. Neurodegener.9:3. doi: 10.1186/1750-1326-9-3
27. Figueredo-Cardenas, G., Morello, M., Sancesario, G., Bernardi, G., and Reiner, A. (1996). Colocalization of somatostatin, neuropeptide Y, neuronal nitric oxide synthase and NADPH-diaphorase in striatal interneurons in rats. Brain Res.735, 317-324. doi: 10.1016/0006-8993(96)00801-3
28. Flames, N., and Marín, O. (2005). Developmental mechanisms underlying the generation of cortical interneuron diversity. Neuron.46, 377-381. doi: 10.1016/j.neuron.2005.04.020
29. Fragkouli, A., van Wijk, N. V., Lopes, R., Kessaris, N., and Pachnis, V. (2009). LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development.136, 3841-3851. doi: 10.1242/dev.038083
30. Germain, N. D., Banda, E. C., Becker, S., Naegele, J. R., and Grabel, L. B. (2013). Derivation and isolation of NKX2.1-positive basal forebrain progenitors from human embryonic stem cells. Stem Cells Dev.22, 1477-1489. doi: 10.1089/scd.2012.0264
31. Geyer, H. L., and Bressman, S. B. (2006). The diagnosis of dystonia. Lancet Neurol.5, 780-790. doi: 10.1016/S1474-4422(06)70547-6
32. Goldberg, J. A., and Reynolds, J. N. J. (2011). Spontaneous firing and evoked pauses in the tonically active cholinergic interneurons of the striatum. Neuroscience.198, 27-43. doi: 10.1016/j.neuroscience.2011.08.067
33. Goldberg, J. A., and Wilson, C. J. (2005). Control of spontaneous firing patterns by the selective coupling of calcium currents to calcium-activated potassium currents in striatal cholinergic interneurons. J. Neurosci.25, 10230-10238. doi: 10.1523/jneurosci.2734-05.2005
34. Goodchild, R. E., Kim, C. E., and Dauer, W. T. (2005). Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron.48, 923-932. doi: 10.1016/j.neuron.2005.11.010
35. Goto, S., Lee, L. V., Munoz, E. L., Tooyama, I., Tamiya, G., Makino, S., et al. (2005). Functional anatomy of the basal ganglia in X-linked recessive dystonia-parkinsonism. Ann. Neurol.58, 7-17. doi: 10.1002/ana.20513
36. Groenewegen, H. J. (2003). The basal ganglia and motor control. Neural Plast.10, 107-120. doi: 10.1155/NP.2003.107
37. Hanson, P. I., and Whiteheart, S. W. (2005). AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol.6, 519-529. doi: 10.1038/nrm1684
38. Hébert, J. M., and Fishell, G. (2008). The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci.9, 678-685. doi: 10.1038/nrn2463
39. Ibáñez-Sandoval, O., Tecuapetla, F., Unal, B., Shah, F., Koós, T., and Tepper, J. M. (2010). Electrophysiological and morphological characteristics and synaptic connectivity of tyrosine hydroxylase-expressing neurons in adult mouse striatum. J. Neurosci.30, 6999-7016. doi: 10.1523/JNEUROSCI.5996-09.2010
40. Iwabuchi, S., Koh, J.-Y., Wang, K., Ho, K. W. D., and Harata, N. C. (2013). Minimal change in the cytoplasmic calcium dynamics in striatal GABAergic neurons of a DYT1 dystonia knock-in mouse model. PLoS One.8:e80793. doi: 10.1371/journal.pone.0080793. Available online at:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3834333/
41. Jungwirth, M., Dear, M. L., Brown, P., Holbrook, K., and Goodchild, R. (2010). Relative tissue expression of homologous torsinB correlates with the neuronal specific importance of DYT1 dystonia-associated torsinA. Hum. Mol. Genet.19, 888-900. doi: 10.1093/hmg/ddp557
42. Kaji, R., Goto, S., Tamiya, G., Ando, S., Makino, S., and Lee, L. V. (2005). Molecular dissection and anatomical basis of dystonia: X-linked recessive dystonia-parkinsonism (DYT3). J. Med. Invest.52, 280-283. doi: 10.2152/jmi.52.280
43. Kawaguchi, Y. (1993). Physiological, morphological and histochemical characterization of three classes of interneurons in rat neostriatum. J. Neurosci.13, 4908-4923.
44. Kawaguchi, Y., Wilson, C. J., Augood, S. J., and Emson, P. C. (1995). Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci.18, 527-535. doi: 10.1016/0166-2236(95)98374-8
45. Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., and Richardson, W. D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci.9, 173-179. doi: 10.1038/nn1620
46. Kim, S. U., Lee, H. J., and Kim, Y. B. (2013). Neural stem cell-based treatment for neurodegenerative diseases. Neuropathology.33, 491-504. doi: 10.1111/neup.12020
47. Klein, C., and Fahn, S. (2013). Translation of Oppenheim's 1911 paper on dystonia. Mov. Disord.28, 851-862. doi: 10.1002/mds.25546
48. Klein, C., Marras, C., and Münchau, A. (2014). "Dystonia overview, " in GeneReviews®ledR [Internet]. eds R. A. Pagon, M. P. Adam, H. H. Ardinger, T. D. Bird, C. R. Dolan, C.-T. Fong, et al. (Seattle, WA: University of Washington, Seattle). Available online at: http://www.ncbi.nlm.nih.gov/books/NBK1155/
49. Kock, N., Naismith, T. V., Boston, H. E., Ozelius, L. J., Corey, D. P., Breakefield, X. O., et al. (2006). Effects of genetic variations in the dystonia protein torsinA: identification of polymorphism at residue 216 as protein modifier. Hum. Mol. Genet.15, 1355-1364. doi: 10.1093/hmg/ddl055
50. Koh, Y.-H., Rehfeld, K., and Ganetzky, B. (2004). A Drosophila model of early onset torsion dystonia suggests impairment in TGF-beta signaling. Hum. Mol. Genet.13, 2019-2030. doi: 10.1093/hmg/ddh208
51. Kramer, P. L., Heiman, G. A., Gasser, T., Ozelius, L. J., de Leon, D., Brin, M. F., et al. (1994). The DYT1 gene on 9q34 is responsible for most cases of early limb-onset idiopathic torsion dystonia in non-Jews. Am. J. Hum. Genet.55, 468-475.
52. Lanska, D. J. (2010). Chapter 33: the history of movement disorders. Handb. Clin. Neurol.95, 501-546. doi: 10.1016/s0072-9752(08)02133-7
53. Li, X.-J., Zhang, X., Johnson, M. A., Wang, Z.-B., Lavaute, T., and Zhang, S.-C. (2009). Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development.136, 4055-4063. doi: 10.1242/dev.036624
54. Lindvall, O. (2013). Developing dopaminergic cell therapy for Parkinson's disease-give up or move forward? Mov. Disord.28, 268-273. doi: 10.1002/mds.25378
55. Liodis, P., Denaxa, M., Grigoriou, M., Akufo-Addo, C., Yanagawa, Y., and Pachnis, V. (2007). Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J. Neurosci.27, 3078-3089. doi: 10.1523/jneurosci.3055-06.2007
56. Liu, Y., Liu, H., Sauvey, C., Yao, L., Zarnowska, E. D., and Zhang, S.-C. (2013a). Directed differentiation of forebrain GABA interneurons from human pluripotent stem cells. Nat. Protoc.8, 1670-1679. doi: 10.1038/nprot.2013.106
57. Liu, Y., Weick, J. P., Liu, H., Krencik, R., Zhang, X., Ma, L., et al. (2013b). Medial ganglionic eminence-like cells derived from human embryonic stem cells correct learning and memory deficits. Nat. Biotechnol.31, 440-447. doi: 10.1038/nbt.2565
58. Lohmann, K., and Klein, C. (2013). Genetics of dystonia: what's known? What's new? What's next?. Mov. Disord.28, 899-905. doi: 10.1002/mds.25536
59. Lopes, R., Verhey van Wijk, N., Neves, G., and Pachnis, V. (2012). Transcription factor LIM homeobox 7 (Lhx7) maintains subtype identity of cholinergic interneurons in the mammalian striatum. Proc. Natl. Acad. Sci. U S A.09, 3119-3124. doi: 10.1073/pnas.1109251109
60. Marin, O., Anderson, S. A., and Rubenstein, J. L. (2000). Origin and molecular specification of striatal interneurons. J. Neurosci.20, 6063-6076.
61. Martella, G., Tassone, A., Sciamanna, G., Platania, P., Cuomo, D., Viscomi, M. T., et al. (2009). Impairment of bidirectional synaptic plasticity in the striatum of a mouse model of DYT1 dystonia: role of endogenous acetylcholine. Brain.132, 2336-2349. doi: 10.1093/brain/awp194
62. Mink, J. W. (2003). The basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch. Neurol.60, 1365-1368. doi: 10.1001/archneur.60.10.1365
63. Figiel, M., Szlachcic, W. J., Switonski, P. M., Gabka, A., and Krzyzosiak, W. J. (2012). Mouse models of polyglutamine diseases: review and data table. Part I. Mol. Neurobiol.46, 393-429. doi: 10.1007/s12035-012-8315-4
64. Nicholas, C. R., Chen, J., Tang, Y., Southwell, D. G., Chalmers, N., Vogt, D., et al. (2013). Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development. Cell Stem Cell.12, 573-586. doi: 10.1016/j.stem.2013.04.005
65. Nicoleau, C., Varela, C., Bonnefond, C., Maury, Y., Bugi, A., Aubry, L., et al. (2013). ES cells neural differentiation qualifies the role of Wnt/β. catenin signals in human telencephalic specification and regionalization. Stem Cells.31, 1763-1774. doi: 10.1002/stem.1462
66. Oleas, J., Yokoi, F., DeAndrade, M. P., Pisani, A., and Li, Y. (2013). Engineering animal models of dystonia. Mov. Disord.28, 990-1000. doi: 10.1002/mds.25583
67. Oppenheim, H. (1911). Über eine eigenartige Krampfkrankheit des kindlichen und jugendlichen Alters (Dysbasia lordotica progressiva, Dystonia musculorum deformans). Neurol. Zentralbl.30, 1090-1107.
68. Ozelius, L. J., Hewett, J. W., Page, C. E., Bressman, S. B., Kramer, P. L., Shalish, C., et al. (1997). The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat. Genet.17, 40-48. doi: 10.1038/ng0997-40
69. Pankratz, M. T., Li, X.-J., Lavaute, T. M., Lyons, E. A., Chen, X., and Zhang, S.-C. (2007). Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells.25, 1511-1520. doi: 10.1634/stemcells.2006-0707
70. Park, I.-H., Arora, N., Huo, H., Maherali, N., Ahfeldt, T., Shimamura, A., et al. (2008). Disease-specific induced pluripotent stem cells. Cell.134, 877-886. doi: 10.1016/j.cell.2008.07.041
71. Pisani, A., Bernardi, G., Ding, J., and Surmeier, D. J. (2007). Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci.30, 545-553. doi: 10.1016/j.tins.2007.07.008
72. Pisani, A., Martella, G., Tscherter, A., Bonsi, P., Sharma, N., Bernardi, G., et al. (2006). Altered responses to dopaminergic D2 receptor activation and N-type calcium currents in striatal cholinergic interneurons in a mouse model of DYT1 dystonia. Neurobiol. Dis.24, 318-325. doi: 10.1016/j.nbd.2006.07.006
73. Reynolds, J. N. J., Hyland, B. I., and Wickens, J. R. (2004). Modulation of an afterhyperpolarization by the substantia nigra induces pauses in the tonic firing of striatal cholinergic interneurons. J. Neurosci.24, 9870-9877. doi: 10.1523/jneurosci.3225-04.2004
74. Sciamanna, G., Hollis, R., Ball, C., Martella, G., Tassone, A., Marshall, A., et al. (2012a). Cholinergic dysregulation produced by selective inactivation of the dystonia-associated protein torsinA. Neurobiol. Dis.47, 416-427. doi: 10.1016/j.nbd.2012.04.015
75. Sciamanna, G., Tassone, A., Mandolesi, G., Puglisi, F., Ponterio, G., Martella, G., et al. (2012b). Cholinergic dysfunction alters synaptic integration between thalamostriatal and corticostriatal inputs in DYT1 dystonia. J. Neurosci.32, 11991-12004. doi: 10.1523/JNEUROSCI.0041-12.2012
76. Sharma, N., Baxter, M. G., Petravicz, J., Bragg, D. C., Schienda, A., Standaert, D. G., et al. (2005). Impaired motor learning in mice expressing torsinA with the DYT1 dystonia mutation. J. Neurosci.25, 5351-5355. doi: 10.1523/jneurosci.0855-05.2005
77. Shashidharan, P., Sandu, D., Potla, U., Armata, I. A., Walker, R. H., McNaught, K. S., et al. (2005). Transgenic mouse model of early-onset DYT1 dystonia. Hum. Mol. Genet.14, 125-133. doi: 10.1093/hmg/ddi012
78. Smith, Y., and Villalba, R. (2008). Striatal and extrastriatal dopamine in the basal ganglia: an overview of its anatomical organization in normal and Parkinsonian brains. Mov. Disord.23(Suppl. 3), S534-S547. doi: 10.1002/mds.22027
79. Sousa, V. H., and Fishell, G. (2010). Sonic Hedgehog functions through dynamic changes in temporal competence in the developing ventral telencephalon. Curr. Opin. Genet. Dev.20, 391-399. doi: 10.1016/j.gde.2010.04.008
80. Storm, E. E., Garel, S., Borello, U., Hebert, J. M., Martinez, S., McConnell, S. K., et al. (2006). Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development.133, 1831-1844. doi: 10.1242/dev.02324
81. Takahashi, K., Okita, K., Nakagawa, M., and Yamanaka, S. (2007). Induction of pluripotent stem cells from fibroblast cultures. Nat. Protoc.2, 3081-3089. doi: 10.1038/nprot.2007.418
82. Tepper, J. M., Tecuapetla, F., Koos, T., and Ibanez-Sandoval, O. (2010). Heterogeneity and diversity of striatal GABAergic interneurons. Front. Neuroanat.4:150. doi: 10.3389/fnana.2010.00150. Available online at:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3016690/
83. Torres, G. E., Sweeney, A. L., Beaulieu, J.-M., Shashidharan, P., and Caron, M. G. (2004). Effect of torsinA on membrane proteins reveals a loss of function and a dominant-negative phenotype of the dystonia-associated ΔE-torsinA mutant. Proc. Natl. Acad. Sci. U S A.101, 15650-15655. doi: 10.1073/pnas.0308088101
84. Uluǧ, A. M., Vo, A., Argyelan, M., Tanabe, L., Schiffer, W. K., Dewey, S., et al. (2011). Cerebellothalamocortical pathway abnormalities in torsinA DYT1 knock-in mice. Proc. Natl. Acad. Sci. U S A.108, 6638-6643. doi: 10.1073/pnas.1016445108
85. Valente, E. M., Warner, T. T., Jarman, P. R., Mathen, D., Fletcher, N. A., Marsden, C. D., et al. (1998). The role of DYT1 in primary torsion dystonia in Europe. Brain.121, 2335-2339. doi: 10.1093/brain/121.12.2335
86. Warner, T., and Jarman, P. (1998). The molecular genetics of the dystonias. J. Neurol. Neurosurg. Psychiatry.64, 427-429. doi: 10.1136/jnnp.64.4.427
87. Wilson, B. K., and Hess, E. J. (2013). Animal models for dystonia. Mov. Disord.28, 982-989. doi: 10.1002/mds.25526
88. Xu, Q., Guo, L., Moore, H., Waclaw, R. R., Campbell, K., and Anderson, S. A. (2010). Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates. Neuron.65, 328-340. doi: 10.1016/j.neuron.2010.01.004
89. Yamanaka, S. (2009). A fresh look at iPS cells. Cell.137, 13-17. doi: 10.1016/j.cell.2009.03.034
90. Yokoi, F., Dang, M. T., and Li, Y. (2012). Improved motor performance in Dyt1 ΔGAG heterozygous knock-in mice by cerebellar Purkinje-cell specific Dyt1 conditional knocking-out. Behav. Brain Res.230, 389-398. doi: 10.1016/j.bbr.2012.02.029
91. Yokoi, F., Dang, M. T., Mitsui, S., Li, J., and Li, Y. (2008). Motor deficits and hyperactivity in cerebral cortex-specific Dyt1 conditional knockout mice. J. Biochem.143, 39-47. doi: 10.1093/jb/mvm191
92. Zhao, Y., Flandin, P., Long, J. E., Cuesta, M. D., Westphal, H., and Rubenstein, J. L. R. (2008). Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J. Comp. Neurol.510, 79-99. doi: 10.1002/cne.21772