Emerging common molecular pathways for primary dystonia

Movement Disorders

Volumn 28, Issue 7, 2013, Pages 968-981

  Ledoux, Mark S ^a   Dauer, William T ^b   Warner, Thomas T ^c  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cell cycle; DYT genes; Endoplasmic reticulum; Nuclear envelope; Synaptic function

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) ALPHA3 SUBUNIT; ANOCTAMIN 3; BETA TUBULIN 4A; CIP1 INTERACTING ZINC FINGER PROTEIN 1; EPSILON SARCOGLYCAN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; PROTEIN; PROTEIN KINASE; THANATOS ASSOCIATED PROTEIN; TORSIN A; UNCLASSIFIED DRUG;

ANO3 GENE; CELL CYCLE; CELL NUCLEUS MEMBRANE; CIZ1 GENE; DAT GENE; DYSTONIA; DYT GENE; DYT6 GENE; ENDOPLASMIC RETICULUM; GENE; GENE EXPRESSION; GENE MUTATION; GNAL GENE; HUMAN; HYPERKINESIA; MEDLINE; MOLECULAR BIOLOGY; MOTOR DYSFUNCTION; MOTOR NERVE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTIC POTENTIAL; THAP1 GENE; TRANSCRIPTION REGULATION;

EID: 84880833382     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.25547     Document Type: Review

References (132)

1. Phukan J Albanese A, Gasser T, Warner T. Primary dystonia and dystonia-plus syndromes: clinical characteristics, diagnosis, and pathogenesis. Lancet Neurol. 2011;10:1074-1085.
2. Ozelius L, Kramer P, Page CE et al. The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet. 1997;17:40-48.
3. + proteins: have engine will work. Nat Rev Mol Cell. Biol.2005;6:519-529.
4. Kock N, Naismith TV, Boston HE, et al. Effects of genetic variations in the dystonia protein torsinA: identification of polymorphism at residue 216 as protein modifier. Hum Mol Genet. 2006;15:1355-1364.
5. Augood SJ, Penney JB, Friberg IK, et al. Expression of the early onset torsion dystonia gene (DYT1) in human brain. Ann Neurol. 1998;43:669-673.
6. Rostasy K, Augood SJ, Hewett JW, et al. TorsinA protein and neuropathology in early onset generalized dystonia with GAG deletion. Neurobiol Dis. 2003;12:11-24.
7. Xiao J, Gong S, Zhao Y, LeDoux MS. Developmental expression of rat torsinA transcript and protein. Brain Res Dev Brain Res. 2004;152:47-60.
8. Zhao Y, Xiao J, Ueda M, et al. Glial elements contribute to stress-induced torsinA expression in the central and peripheral nervous systems. Neuroscience. 2008;155:439-453.
9. Jungwirth M, Dear ML, Brown P, Holbrook K, Goodchild R. Relative expression of homologous torsinB correlates with the neuronal specific importance of DYT1 dystonia-associated torsinA. Hum Mol Genet. 2010;19:888-900.
10. Hersheson J, Menacci NE, Davis M, et al. Mutations in the autoregulatory domain of β-tubulin 4a cause hereditary dystonia. Ann Neurol. 2012 [Epub ahead of print].
11. Blanchard A, Ea V, Roubertie A, et al. DYT6 dystonia: review of the literature and creation of the UMD Locus-Specific Database (LSDB) for mutations in the THAP1 gene. Hum Mutat. 2011;32:1213-1224.
12. LeDoux MS, Xiao J, Rudzińska M, et al. Genotype-phenotype correlations in THAP1 dystonia: molecular foundations and description of new cases. Parkinsonism Relat Disord. 2012;18:414-425.
13. Fuchs T, Gavarini S, Saunders-Pullman R, et al. Mutations in the THAP1 gene are responsible for DYT6 primary torsion dystonia. Nat Genet. 2009;41:286-288.
14. Djarmati A, Schneider SA, Lohmann K, et al. Mutations in THAP1 (DYT6) and generalised dystonia with prominent spasmodic dysphonia: a genetic screening study. Lancet Neurol. 2009;8:447-452.
15. Bressman SB, Raymond D, Fuchs T, Heiman GA, Ozelius LJ, Saunders-Pullman R. Mutations in THAP1 (DYT6) in early-onset dystonia: a genetic screening study. Lancet Neurol. 2009;8:441-446.
16. Schneider SA, Ramirez A, Shafiee K, et al. Homozygous THAP1 mutations as cause of early-onset generalized dystonia. Mov Disord. 2011;26:858-861.
17. Roussigne M, Cayrol C, Clouaire T, Amalric F, Girard JP. THAP1 is a nuclear proapoptotic factor that links prostate-apoptosis-response-4 (Par-4) to PML nuclear bodies. Oncogene. 2003;22:2432-2442.
18. Cayrol C, Lacroix C, Mathe C, et al. The THAP-zinc finger protein THAP1 regulates endothelial cell proliferation through modulation of pRB/E2F cell-cycle target genes. Blood. 2007;109:584-594.
19. Zimprich A, Grabowski M, Asmus F, et al, T. Mutations in the gene encoding epsilon-sarcoglycan cause myoclonus-dystonia syndrome. Nat Genet. 2001;29:66-69.
20. Sunada Y, Campbell KP. Dystrophin-glycoprotein complex: molecular organization and critical roles in skeletal muscle. Curr Opin Neurol. 1995;8:379-384.
21. Straub V, Campbell KP. Muscular dystrophies and the dystrophin-glycoprotein complex. Curr Opin Neurol. 1997;10:168-175.
22. Chan P, Gonzalez-Maeso J, Ruf F, et al. Epsilon-sarcoglycan immunoreactivity and mRNA expression in mouse brain. J Comp Neurol. 2005;482:50-75.
23. Brunig I, Suter A, Knuesel I, Luscher B, Fritschy JM. GABAergic terminals are required for postsynaptic clustering of dystrophin but not of GABA(A) receptors and gephyrin. J Neurosci. 2002;22:4805-4813.
24. Levi S, Grady RM, Henry MD, Campbell KP, Sanes JR, Craig AM. Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci. 2002;22:4274-4285.
25. Camargos S, Scholz S, Simon-Sanchez J, et al. DYT16, a novel young-onset dystonia-parkinsonism disorder: identification of a segregating mutation in the stress response protein PRKRA. Lancet Neurol. 2008;7:207-215.
26. Bragg DC, Armata IA, Nery FC, et al. Molecular pathways in dystonia. Neurobiol Dis. 2011;42:136-147.
27. Xiao J, Uitti RJ, Zhao Y, et al. Mutations in CIZ1 cause adult-onset primary cervical dystonia. Ann Neurol. 2012;71:458-469.
28. Mitsui K, Matsumoto A, Ohtsuka S, et al. Cloning and characterization of a novel p21(Cip1/Waf1)-interacting zinc finger protein, ciz1. Biochem Biophys Res Commun. 1999;264:457-464.
29. Charlesworth G, Plagnol V, Holmstrom KM, et al. Mutations in ANO3 cause dominant craniocervical dystonia: ion channel implicated in pathogenesis. Am J Hum Genet. 2012;91:1041-1050.
30. Fuchs T, Saunders-Pullman R, Masuho I, et al. Mutations in GNAL cause primary torsion dystonia. Nat Genet. 2013;45:88-92.
31. Vemula SR, Puschmann A, Xiao J, et al. Role of Gα(Olf) in familial and sporadic adult onset primary dystonia. Hum Mol Genet. 2013 [Epub ahead of print].
32. Coverley D, Marr J, Ainscough J. Ciz1 promotes mammalian DNA replication. J Cell Sci. 2005;118:101-112.
33. Warder DE, Keherly MJ. Ciz1, Cip1 interacting zinc finger protein 1 binds the consensus DNA sequence ARYSR(0 2)YYAC. J Biomed Sci. 2003;10:406-417.
34. Ainscough JF, Rahman FA, Sercombe H, et al. C-terminal domains deliver the DNA replication factor Ciz1 to the nuclear matrix. J Cell Sci. 2007;120:115-124.
35. Copeland NA, Sercombe HE, Ainscough JF, Coverley D. Ciz1 cooperates with cyclin-A-CDK2 to activate mammalian DNA replication in vitro. J Cell Sci. 2010;123:1108-1115.
36. den Hollander P, Rayala SK, Coverley D, Kumar R. Ciz1, a novel DNA-binding coactivator of the estrogen receptor alpha, confers hypersensitivity to estrogen action. Cancer Res. 2006;66:11021-11029.
37. Bessiere D, Lacroix C, Campagne S, et al. Structure-function analysis of the THAP zinc finger of THAP1, a large C2CH DNA-binding module linked to Rb/E2F pathways. J Biol Chem. 2008;283:4352-4363.
38. Campagne S, Saurel O, Gervais V, Milon A Structural determinants of specific DNA-recognition by the THAP zinc finger. Nucleic Acids Res. 2010;38:3466-3476.
39. Clouaire T, Roussigne M, Ecochard V, Mathe C, Amalric F, Girard JP. The THAP domain of THAP1 is a large C2CH module with zinc-dependent sequence-specific DNA-binding activity. Proc Natl Acad Sci U S A. 2005;102:6907-6912.
40. Sabogal A, Lyubimov AY, Corn JE, Berger JM, Rio DC THAP proteins target specific DNA sites through bipartite recognition of adjacent major and minor grooves. Nat Struct Mol Biol. 2010;17:117-123.
41. Gavarini S, Cayrol C, Fuchs T, et al. Direct interaction between causative genes of DYT1 and DYT6 primary dystonia. Ann Neurol. 2010;68:549-553.
42. Kaiser FJ, Osmanoric A, Rakovic et al. The dystonia gene DYT1 is repressed by the transcription factor THAP1 (DYT6). Ann Neurol. 2010;68:554-559.
43. Palada V, Stiern S, Glockle et al, K. Lack of sequence variations in THAP1 gene and THAP1-binding sites in TOR1A promoter of DYT1 patients. Mov Disord. 2012;27:917.
44. Kamm C, Uflacker N, Asmus F, et al. No evidence for THAP1/DYT6 variants as disease modifiers in DYT1 dystonia. Mov Disord. 2011;26:2136-2137.
45. Rual JF, Venkatesan K, Hao T, et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature. 2005;437:1173-1178.
46. Lütolf S, Radtke F, Aguet M, Suter U, Taylor V. Notch1 is required for neuronal and glial differentiation in the cerebellum. Development. 2002;129:373-385.
47. Koekkoek SK, Yamaguchi K, Milojkovic BA, et al. Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron. 2005;47:339-352.
48. Andersson T, Södersten E, Duckworth JK, et al. CXXC5 is a novel BMP4-regulated modulator of Wnt signaling in neural stem cells. J Biol Chem. 2009;284:3672-3681.
49. Sadnicka A, Hoffland BS, Bhatia KP, van de Warrenburg BP, Edwards MJ. The cerebellum in dystonia-help or hindrance. Clin Neurophysiol. 2012;123:65-70.
50. Evidente VG, Advincula J, Esteban R, et al. Phenomenology of "Lubag" or X-linked dystonia-parkinsonism. Mov Disord. 2002;17:1271-1277.
51. Makino S, Kaji R, Ando S, et al. Reduced neuron-specific expression of the TAF1 gene is associated with X-linked dystonia-parkinsonism. Am J Hum Genet. 2007;80:393-406.
52. Sako W, Moridaki R, Kaji R, et al. Identification and localization of a neuron-specific isoform of TAF1 in rat brain; implications for neuropathology of DYT3 dystonia. Neuroscience. 2011;189:100-107.
53. Li HH, Li AG, Sheppard HM, Liu X. Phosphorylation on Thr-55 by TAF1 mediates degradation of p53: a role for TAF1 in cell G1 progression. Mol Cell. 2004;13:867-878.
54. Buchmann AM, Skaar JR, DeCaprio JA. Activation of a DNA damage checkpoint response in a TAF1-defective cell line. Mol Cell Biol. 2004;24:5332-5339.
55. Katzenberger RJ, Marengo MS, Wassarman DA. ATM and ATR pathways signal alternative splicing of Drosophila TAF1 pre-mRNA in response to DNA damage. Mol Cell Biol. 2006;26:9256-9267.
56. Basham SE, Rose LS. The Caenorhabditis elegans polarity gene ooc-5 encodes a Torsin-related protein of the AAA ATPase superfamily. Development. 2001;128:4645-4656.
57. Baptista MJ, O'Farrell C, Hardy J, Cookson MR. Microarray analysis reveals induction of heat shock proteins mRNAs by the torsion dystonia protein, TorsinA. Neurosci Lett. 2003;343:5-8.
58. Koh YH, Rehfeld K, Ganetzky B. A Drosophila model of early onset torsion dystonia suggests impairment in TGF-beta signaling. Hum Mol Genet. 2004;13:2019-2030.
59. Erol A. Genotoxic stress-mediated cell cycle activities for the decision of cellular fate. Cell Cycle. 2011;10:3239-3248.
60. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhães TR, Goodman CS. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron. 2002;33:545-558.
61. McCabe BD, Marqués G, Haghighi AP, et al. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron. 2003;39:241-254.
62. Saunders-Pullman R, Raymond D, Stoessl AJ, et al. Variant ataxia-telangiectasia presenting as primary-appearing dystonia in Canadian Mennonites. Neurology. 2012;78:649-657.
63. Pommier Y, Weinstein JN, Aladjem MI, Kohn KW. Chk2 molecular interaction map and rationale for Chk2 inhibitors. Clin Cancer Res. 2006;12:2657-2661.
64. Bertran-Gonzalez J, Håkansson K, Borgkvist A, et al. Histone H3 phosphorylation is under the opposite tonic control of dopamine D2 and adenosine A2A receptors in striatopallidal neurons. Neuropsychopharmacology. 2009;34:1710-1720.
65. Herrup K, Sunter K. Numerical matching during cerebellar development: quantitative analysis of granule cell death in staggerer mouse chimeras. J Neurosci. 1987;7:829-836.
66. Subkhankulova T, Zhang X, Leung C, Marino S. Bmi1 directly represses p21Waf1/Cip1 in Shh-induced proliferation of cerebellar granule cell progenitors. Mol Cell Neurosci. 2010;45:151-162.
67. Wang L, Wang R, Herrup K. E2F1 works as a cell cycle suppressor in mature neurons. J Neurosci. 2007;27:12555-12564.
68. Li J, Chen J, Vinters HV, Gatti RA, Herrup K. Stable brain ATM message and residual kinase-active ATM protein in ataxia-telangiectasia. J Neurosci. 2011;31:7568-7577.
69. Prudente CN, Pardo CA, Xiao J, et al. Neuropathology of cervical dystonia. Exp Neurol. 2013;241:95-104.
70. Song CH, Bernhard D, Bolarinwa C, Hess EJ, Smith Y, Jinnah HA. Subtle microstructural changes of the striatum in a DYT1 knock-in mouse model of dystonia. Neurobiol Dis. 2013;54:362-371.
71. Torres GE, Sweeney AL, Beaulieu JM, Shashidharan P, Caron MG. Effect of torsinA on membrane proteins reveals a loss of function and a dominant-negative phenotype of the dystonia-associated DeltaE-torsinA mutant. Proc Natl Acad Sci U S A. 2004;101:15650-15655.
72. Hewett JW, Tannous B, Niland BP, et al. Mutant torsinA interferes with protein processing through the secretory pathway in DYT1 dystonia cells. Proc Natl Acad Sci U S A. 2007;104:7271-7276.
73. Hewett JW, Nery FC, Niland B, et al. siRNA knock-down of mutant torsinA restores processing through secretory pathway in DYT1 dystonia cells. Hum Mol Genet. 2008;17:1436-1445.
74. Chen P, Burdette AJ, Porter JC, et al. The early-onset torsion dystonia-associated protein, torsinA, is a homeostatic regulator of endoplasmic reticulum stress response. Hum Mol Genet. 2010;19:3502-3515.
75. Nery FC, Armata IA, Farley JE, et al. TorsinA participates in endoplasmic reticulum-associated degradation. Nat Commun. 2011;2:393.
76. Bernasconi R, Molinari M. ERAD and ERAD tuning: disposal of cargo and of ERAD regulators from the mammalian ER. Curr Opin Cell Biol. 2011;23:176-183.
77. Lee ES, Tang N, Thompson S, Miller S, Katze MG. The double-stranded RNA-activated protein kinase (PKR) plays a significant role in a sustained ER stress-induced apoptosis. FEBS J. 2007;581:4325-4332.
78. Gerace, L. TorsinA and torsion dystonia: unraveling the architecture of the nuclear envelope. Proc Natl Acad Sci U S A. 2004;101:8839-8840.
79. Goodchild RE, Dauer WT. Mislocalization to the nuclear envelope: an effect of the dystonia-causing torsinA mutation. Proc Natl Acad Sci U S A. 2004;101:847-852.
80. Goodchild RE, Kim, CE, Dauer WT. Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron. 2005;48:923-932.
81. Naismith TV, Heuser JE, Breakefield XO, Hanson PI. TorsinA in the nuclear envelope. Proc Natl Acad Sci U S A. 2004;101:7612-7617.
82. Gonzalez-Alegre P, Paulson HL. Aberrant cellular behavior of mutant torsinA implicates nuclear envelope dysfunction in DYT1 dystonia. J Neurosci. 2004;24:2593-2601.
83. Giles LM, Chen J, Li L, Chin LS. Dystonia-associated mutations cause premature degradation of torsinA protein and cell-type-specific mislocalization to the nuclear envelope. Hum Mol Genet. 2008;17:2712-2722.
84. Goodchild RE, Dauer WT. The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J Cell Biol. 2005;168:855-862.
85. Worman HJ, Gundersen GG. Here come the SUNs: a nucleocytoskeletal missing link. Trends Cell Biol. 2006;16:67-69.
86. Nery FC, Zeng J, Niland et al. TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J Cell Sci. 2008;121:3476-3486.
87. Esapa CT, Waite A, Locke M, et al. SGCE missense mutations that cause myoclonus-dystonia syndrome impair epsilon-sarcoglycan trafficking to the plasma membrane: modulation by ubiquitination and torsinA. Hum Mol Genet. 2007;16:327-342.
88. Ferrari-Toninelli G, Paccioretti S, Francisconi S, Uberti D, Memo M. TorsinA negatively controls neurite outgrowth of SH-SY5Y human neuronal cell line. Brain Res. 2004;1012:75-81.
89. Hewett JW, Zeng J, Niland BP, Bragg DC, Breakefield XO. Dystonia-causing mutant torsinA inhibits cell adhesion and neurite extension through interference with cytoskeletal dynamics. Neurobiol Dis. 2006;22:98-111.
90. Srsen V, Korfali N, Schirmer EC. Nuclear envelope influences on cell-cycle progression. Biochem Soc Trans. 2011;39:1742-1746.
91. Egecioglu D, Brickner JH. Gene positioning and expression. Curr Opin Cell Biol. 2011;23:338-345.
92. Ichinose H, Ohye T, Takahashi E, et al. Hereditary progressive dystonia with marked diurnal fluctuation caused by mutations in the GTP cyclohydrolase I gene. Nat Genet. 1994;8:236-242.
93. Knappskog PM, Flatmark T, Mallet J, Ludecke B, Bartholome K. Recessively inherited L-DOPA-responsive dystonia caused by a point mutation (Q381K) in the tyrosine hydroxylase gene. Hum Mol Genet. 1995;4:1209-1212.
94. Trender-Gerhard I, Sweeney MG, Schwingenschuh P, et al. Autosomal-dominant GTPCH1-deficient DRD: clinical characteristics and long-term outcome of 34 patients. J Neurol Neurosurg Psychiatry. 2009;80:839-845.
95. Casey DE. Pathophysiology of antipsychotic drug-induced movement disorders. J Clin Psychiatry. 2004;65:25-28.
96. Tolosa E, Compta Y. Dystonia in Parkinson's disease. J Neurol. 2006;(Suppl 7):VII7-VII13.
97. Egami K, Yitta S, Lewers JC, et al. Basal ganglia dopamine loss due to defect in purine cycling. Neurobiol Dis. 2007;26:391-407.
98. Perlmutter JS, Stambuk MK, Markham J, et al. Decreased [18F]spiperone binding in putamen in idiopathic focal dystonia. J Neurosci. 1997;17:843-850.
99. Misbahuddin A, Placzek MR, Chaudhuri KR, Wood NW, Bhatia KP, Warner TT. A polymorphism in the dopamine receptor DRD5 is associated with blepharospasm. Neurology. 2002;58:124-126.
100. Augood SJ, Martin DM, Ozelius LJ, Breakefield XO, Penney JB Jr, Standaert DG. Distribution of the mRNAs encoding torsinA and torsinB in the normal adult human brain. Ann Neurol. 1999;46:761-769.
101. Augood SJ, Hollingsworth Z, Albers DS, et al. Dopamine transmission in DYT1 dystonia: a biochemical and autoradiographical study. Neurology. 2002;59:445-458.
102. Furukawa Y, Hornykiewicz O, Fahn S, Kish SJ. Striatal dopamine in early-onset primary torsion dystonia with the DYT1 mutation. Neurology. 2000;54:1193-1195.
103. Shashidharan P, Sandu D, Potla U, et al. Transgenic mouse model of early-onset DYT1 dystonia. Hum Mol Genet. 2005;14:125-133.
104. Dang MT, Yokoi F, McNaught KS, et al. Generation and characterization of Dyt1 DeltaGAG knock-in mouse as a model for early-onset dystonia. Exp Neurol. 2005;196:452-463.
105. Grundmann K, Hubener J, Habig K, et al. Gene expression changes in a transgenic mouse model overexpressing human wild-type and mutant torsinA. Proteomics Clin Appl. 2008;2:720-736.
106. Zhao Y, Decuypere M, Ledoux MS. Abnormal motor function and dopamine neurotransmission in DYT1 DeltaGAG transgenic mice. Exp Neurol. 2008;210:719-730.
107. Page ME, Bao L, Andre P, et al. Cell-autonomous alteration of dopaminergic transmission by wild type and mutant (DeltaE) TorsinA in transgenic mice. Neurobiol Dis. 2010;39:318-326.
108. Balcioglu A, Kim M-O, Sharma N, Cha J-H, Breakefield XO, Standaert DG. Dopamine release is impaired in a mouse model of DYT1 dystonia. J Neurochem. 2007;102:783-788.
109. Hewett J, Johanson P, Sharma N, Standaert DG, Balcioglu A. Function of dopamine transporter is compromised in DYT1 transgenic animal model in vivo. J Neurochem. 2010;113:228-235.
110. Song CH, Fan X, Exeter CJ, Hess EJ, Jinnah HA. Functional analysis of Dopaminergic system in a DYT1 knock-in mouse model of dystonia. Neurobiol Dis. 2012;48:66-78.
111. Misbahuddin A, Placzek MR, Taanman JW, et al. Mutant torsinA, which causes early-onset primary torsion dystonia, is redistributed to membranous structures enriched in vesicular monoamine transporter in cultured human SH-SY5Y cells. Mov Disord. 2005;20:432-440.
112. Bao L, Patel JC, Walker RH, Shashidharan P, Rice ME. Dysregulation of striatal dopamine release in a mouse model of dystonia. J Neurochem. 2010;114:1781-1791.
113. Augood SJ, Hollingsworth Z, Albers DS, et al. Dopamine transmission in DYT1 dystonia: a biochemical and autoradiographical study. Neurology. 2002;59:445-458.
114. Granata A, Watson R, Collinson L, Schiavo G, Warner TT. The dystonia-associated protein torsinA modulates synaptic vesicle recycling. J Biol Chem. 2008;283:7568-7579.
115. Granata A, Koo SJ, Haucke V, et al. CSN complex controls the stability of selected synaptic proteins via a torsinA-dependent process. EMBO J. 2011;30:181-193.
116. Kakazu Y, Koh J-Y, Ho D, Gonzalez-Alegre P, Harata C. Synaptic vesicle recycling is enhanced by torsinA that harbours the DYT1 dystonia mutation. Synapse. 2012;66;453-464.
117. Kakazu Y, Koh J-Y, Iwabuchi S, Gonzalez-Alegre P, Harata C. Miniature release events of glutamate from hippocampal neurons are influenced by the dystonia-associated protein TorsinA. Synapse. 2012;66:807-822.
118. Pisani A, Martella G, Tscherter A, et al. 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. 2006;24:318-325.
119. Sciamanna G, Bonsi P, Tassone A, et al. Impaired striatal D2 receptor function leads to enhanced GABA transmission in a mouse model of DYT1 dystonia. Neurobiol Dis. 2009;34:133-145.
120. Napolitano F, Pasqualetti M, Usiello A, et al. Dopamine D2 receptor dysfunction is rescued by adenosine A2A receptor antagonism in a model of DYT1 dystonia. Neurobiol Dis. 2010;38:434-445.
121. Asanuma K, Carbon-Correll M, Eidelberg D. Neuroimaging in human dystonia. J Med Invest. 2005;52:272-279.
122. Carbon M, Niethammer M, Peng S, et al. Abnormal striatal and thalamic dopamine neurotransmission: genotype-related features of dystonia. Neurology. 2009;72:2097-2103.
123. Carbon M, Argyelan M, Eidelberg D. Functional imaging in hereditary dystonia. Eur J Neurol. 2010;(Suppl 1):58-64.
124. Quatarone A, Pisani A. Abnormal synaptic plasticity in dystonia: disruption of synaptic homeostasis. Neurobiol Dis. 2011;42:162-170.
125. olf levels are regulated by receptor usage and control dopamine and adenosine action in the striatum. J Neurosci. 2001;21:4390-4399.
126. Ashmore LJ, Hrizo SL, Paul SM, Van Voorhies WA, Beitel GJ, Palladino MJ. Novel mutations affecting the Na, K ATPase alpha model complex neurological diseases and implicate the sodium pump in increased longevity. Hum Genet. 2009;126:431-447.
127. Calderon DP, Fremont R, Kraenzlin F, Khodakhah K. The neural substrates of rapid-onset dystonia-parkinsonism. Nat Neurosci. 2011;14:357-365.
128. Kurian MA, Zhen J, Cheng S Y, et al. Homozygous loss-of-function mutations in the gene encoding the dopamine transporter are associated with infantile parkinsonism-dystonia. J Clin Invest. 2009;119:1595-1603.
129. Kurian MA, Li Y, Zhen J, et al. Clinical and molecular characterisation of hereditary dopamine transporter deficiency syndrome: an observational cohort and experimental study. Lancet Neurol. 2011;10:54-62.
130. Vasudevan A, Breakefield XO, Bhide PG. Developmental patterns of torsinA and torsinB expression. Brain Res. 2006;1073-1074:139-145.
131. Siegert S, Bahn C, Kramer ML, et al. TorsinA expression is detectable in human infants as young as 4 weeks old. Brain Res Dev Brain Res. 2005;757:19-26.
132. Zhao Y, Xiao J, Gong S, Clara JA, Ledoux MD. Neural expression of transcription factor THAP1 during development in rat. Neuroscience. 2013;231:282-295.