Engineering animal models of dystonia

Movement Disorders

Volumn 28, Issue 7, 2013, Pages 990-1000

  Oleas, Janneth ^a   Yokoi, Fumiaki ^a   Deandrade, Mark P ^a   Pisani, Antonio ^b   Li, Yuqing ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Animal model; Dystonia; DYT1; DYT11; DYT12

Indexed keywords

4 AMINOBUTYRIC ACID DERIVATIVE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) ALPHA3 SUBUNIT; AMPICILLIN; BOTULINUM TOXIN; DOPAMINE 2 RECEPTOR; DOPAMINE RECEPTOR STIMULATING AGENT; EPSILON SARCOGLYCAN; PROTEIN; TORSIN A; TRIHEXYPHENIDYL; UNCLASSIFIED DRUG;

ATP13 GENE; BASAL GANGLION; BINDING AFFINITY; BRAIN REGION; CAENORHABDITIS ELEGANS; CEREBELLUM; DROSOPHILA MELANOGASTER; DRUG DEVELOPMENT; DYSTONIA; DYT1 GENE; ELECTROPHYSIOLOGY; EXPERIMENTAL MODEL; GENE; GENOTYPE; HUMAN; INVOLUNTARY MOVEMENT; KNOCKOUT MOUSE; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MYOCLONUS DYSTONIA; NEUROLOGIC DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PRIMARY ONSET TORSION DYSTONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RAPID ONSET DYSTONIA PARKINSONISM; REVIEW; RODENT; ROTAROD TEST; SGCE GENE; TRANSGENIC ANIMAL; TRANSGENIC MOUSE;

EID: 84880780069     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.25583     Document Type: Review

References (115)

1. Albanese A, Bhatia K, Bressman SB, et al. Phenomenology and classification of dystonia: a consensus update. Mov Disord 2013;28:863-873.
2. Fahn S, Eldridge R. Definition of dystonia and classification of the dystonic states. Adv Neurol 1976;14:1-5.
3. Bertram KL, Williams DR. Diagnosis of dystonic syndromes-a new eight-question approach. Nat Rev Neurol 2012;8:275-283.
4. Niethammer M, Carbon M, Argyelan M, Eidelberg D. Hereditary dystonia as a neurodevelopmental circuit disorder: evidence from neuroimaging. Neurobiol Dis 2011;42:202-209.
5. Tinazzi M, Rosso T, Fiaschi A. Role of the somatosensory system in primary dystonia. Mov Disord 2003;18:605-622.
6. Zhuang P, Li Y, Hallett M. Neuronal activity in the basal ganglia and thalamus in patients with dystonia. Clin Neurophysiol 2004;115:2542-2557.
7. Neychev VK, Fan X, Mitev VI, Hess EJ, Jinnah HA. The basal ganglia and cerebellum interact in the expression of dystonic movement. Brain 2008;131(pt 9):2499-2509.
8. Breakefield XO, Blood AJ, Li Y, Hallett M, Hanson PI, Standaert DG. The pathophysiological basis of dystonias. Nat Rev Neurosci 2008;9:222-234.
9. Quartarone A, Pisani A. Abnormal plasticity in dystonia: disruption of synaptic homeostasis. Neurobiol Dis 2011;42:162-170.
10. 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.
11. Calderon DP, Fremont R, Kraenzlin F, Khodakhah K. The neural substrates of rapid-onset dystonia-parkinsonism. Nat Neurosci 2011;14:357-365.
12. Ikeda K, Satake S, Onaka T, et al. Enhanced inhibitory neurotransmission in the cerebellar cortex of the Atp1a3-deficient heterozygous mice. J Physiol 2013.
13. Raike RS, Jinnah HA, Hess EJ. Animal models of generalized dystonia. NeuroRx 2005;2:504-512.
14. Ozelius LJ, Hewett JW, Page CE, et al. The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet 1997;17:40-48.
15. Bressman SB, de Leon D, Brin MF, et al. Idiopathic dystonia among Ashkenazi Jews: evidence for autosomal dominant inheritance. Ann Neurol 1989;26:612-620.
16. Fahn S. The genetics of idiopathic torsion dystonia. Int J Neurol 1991;25-26:70-80.
17. Muller U. The monogenic primary dystonias. Brain 2009;132(pt 8):2005-2025.
18. Ozelius LJ, Hewett JW, Page CE, et al. The gene (DYT1) for early-onset torsion dystonia encodes a novel protein related to the Clp protease/heat shock family. Adv Neurol 1998;78:93-105.
19. Burdette AJ, Churchill PF, Caldwell GA, Caldwell KA. The early-onset torsion dystonia-associated protein, torsinA, displays molecular chaperone activity in vitro. Cell Stress Chaperones 2010;15:605-617.
20. Granata A, Watson R, Collinson LM, Schiavo G, Warner TT. The dystonia-associated protein torsinA modulates synaptic vesicle recycling. J Biol Chem 2008;283:7568-7579.
21. Bargmann CI. Neurobiology of the Caenorhabditis elegans genome. Science 1998;282:2028-2033.
22. Shulman JM, Shulman LM, Weiner WJ, Feany MB. From fruit fly to bedside: translating lessons from Drosophila models of neurodegenerative disease. Curr Opin Neurol 2003;16:443-449.
23. Bilen J, Bonini NM. Drosophila as a model for human neurodegenerative disease. Annu Rev Genet 2005;39:153-171.
24. Consortium CeS. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998;282:2012-2018.
25. 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.
26. Caldwell GA, Cao S, Sexton EG, Gelwix CC, Bevel JP, Caldwell KA. Suppression of polyglutamine-induced protein aggregation in Caenorhabditis elegans by torsin proteins. Hum Mol Genet 2003;12:307-319.
27. Cao S, Gelwix CC, Caldwell KA, Caldwell GA. Torsin-mediated protection from cellular stress in the dopaminergic neurons of Caenorhabditis elegans. J Neurosci 2005;25:3801-3812.
28. 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.
29. 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.
30. Leung JC, Klein C, Friedman J, et al. Novel mutation in the TOR1A (DYT1) gene in atypical early onset dystonia and polymorphisms in dystonia and early onset parkinsonism. Neurogenetics 2001;3:133-143.
31. Lee DW, Seo JB, Ganetzky B, Koh YH. DeltaFY mutation in human torsin A [corrected] induces locomotor disability and aberrant synaptic structures in Drosophila. Mol Cells 2009;27:89-97.
32. Ozelius LJ, Page CE, Klein C, et al. The TOR1A (DYT1) gene family and its role in early onset torsion dystonia. Genomics 1999;62:377-384.
33. Muraro NI, Moffat KG. Down-regulation of torp4a, encoding the Drosophila homologue of torsinA, results in increased neuronal degeneration. J Neurobiol 2006;66:1338-1353.
34. Wakabayashi-Ito N, Doherty OM, Moriyama H, et al. Dtorsin, the Drosophila ortholog of the early-onset dystonia TOR1A (DYT1), plays a novel role in dopamine metabolism [serial online]. PLoS One 2011;6:e26183.
35. 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.
36. Goodchild RE, Kim CE, Dauer WT. Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 2005;48:923-932.
37. Yokoi F, Dang MT, Miller CA, et al. Increased c-fos expression in the central nucleus of the amygdala and enhancement of cued fear memory in Dyt1 DeltaGAG knock-in mice. Neurosci Res 2009;65:228-235.
38. Balas M, Peretz C, Badarny S, Scott RB, Giladi N. Neuropsychological profile of DYT1 dystonia. Mov Disord 2006;21:2073-2077.
39. Song CH, Fan X, Exeter CJ, Hess EJ, Jinnah HA. Functional analysis of dopaminergic systems in a DYT1 knock-in mouse model of dystonia. Neurobiol Dis 2012;48:66-78.
40. Dang MT, Yokoi F, Cheetham CC, et al. An anticholinergic reverses motor control and corticostriatal LTD deficits in Dyt1 ΔGAG knock-in mice. Behav Brain Res 2012;226:465-472.
41. Asanuma K, Ma Y, Okulski J, et al. Decreased striatal D2 receptor binding in non-manifesting carriers of the DYT1 dystonia mutation. Neurology 2005;64:347-349.
42. Ulug AM, Vo A, Argyelan M, et al. Cerebellothalamocortical pathway abnormalities in torsinA DYT1 knock-in mice. Proc Natl Acad Sci U S A 2011;108:6638-6643.
43. Carbon M, Kingsley PB, Su S, et al. Microstructural white matter changes in carriers of the DYT1 gene mutation. Ann Neurol 2004;56:283-286.
44. Carbon M, Ghilardi MF, Argyelan M, Dhawan V, Bressman SB, Eidelberg D. Increased cerebellar activation during sequence learning in DYT1 carriers: an equiperformance study. Brain 2008;131(pt 1):146-154.
45. Argyelan M, Carbon M, Niethammer M, et al. Cerebellothalamocortical connectivity regulates penetrance in dystonia. J Neurosci 2009;29:9740-9747.
46. Kakazu Y, Koh JY, Ho KW, Gonzalez-Alegre P, Harata NC. Synaptic vesicle recycling is enhanced by torsinA that harbors the DYT1 dystonia mutation. Synapse 2012;66:453-464.
47. Kakazu Y, Koh JY, Iwabuchi S, Gonzalez-Alegre P, Harata NC. Miniature release events of glutamate from hippocampal neurons are influenced by the dystonia-associated protein torsinA. Synapse 2012;66:807-822.
48. Yokoi F, Yang G, Li J, DeAndrade MP, Zhou T, Li Y. Earlier onset of motor deficits in mice with double mutations in Dyt1 and Sgce. J Biochem 2010;148:459-466.
49. 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.
50. Gordon KL, Gonzalez-Alegre P. Consequences of the DYT1 mutation on torsinA oligomerization and degradation. Neuroscience 2008;157:588-595.
51. Dang MT, Yokoi F, Pence MA, Li Y. Motor deficits and hyperactivity in Dyt1 knockdown mice. Neurosci Res 2006;56:470-474.
52. Yokoi F, Dang MT, Mitsui S, Li J, Li Y. Motor deficits and hyperactivity in cerebral cortex-specific Dyt1 conditional knockout mice. J Biochem 2008;143:39-47.
53. Yokoi F, Dang MT, Li Y. Improved motor performance in Dyt1 ΔGAG heterozygous knock-in mice by cerebellar Purkinje-cell specific Dyt1 conditional knocking-out. Behav Brain Res 2012;230:389-398.
54. Jin XL, Guo H, Mao C, et al. Emx1-specific expression of foreign genes using "knock-in" approach. Biochem Biophys Res Commun 2000;270:978-982.
55. Dang MT, Yokoi F, Yin HH, Lovinger DM, Wang Y, Li Y. Disrupted motor learning and long-term synaptic plasticity in mice lacking NMDAR1 in the striatum. Proc Natl Acad Sci U S A 2006;103:15254-15259.
56. Yokoi F, Dang MT, Li J, Standaert DG, Li Y. Motor deficits and decreased striatal dopamine receptor 2 binding activity in the striatum-specific Dyt1 conditional knockout mice [serial online]. PLoS One 2011;6:e24539.
57. Rossi J, Balthasar N, Olson D, et al. Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab 2011;13:195-204.
58. Sciamanna G, Hollis R, Ball C, et al. Cholinergic dysregulation produced by selective inactivation of the dystonia-associated protein torsinA. Neurobiol Dis 2012;47:416-427.
59. LeDoux MS, Lorden JF, Ervin JM. Cerebellectomy eliminates the motor syndrome of the genetically dystonic rat. Exp Neurol 1993;120:302-310.
60. Campbell DB, North JB, Hess EJ. Tottering mouse motor dysfunction is abolished on the Purkinje cell degeneration (pcd) mutant background. Exp Neurol 1999;160:268-278.
61. Barski JJ, Dethleffsen K, Meyer M. Cre recombinase expression in cerebellar Purkinje cells. Genesis 2000;28(3-4):93-98.
62. Zhang L, Yokoi F, Jin YH, et al. Altered Dendritic Morphology of Purkinje cells in Dyt1 DeltaGAG knock-in and Purkinje cell-specific Dyt1 conditional knockout mice [serial online]. PLoS One 2011;6:e18357.
63. Hoshi E, Tremblay L, Feger J, Carras PL, Strick PL. The cerebellum communicates with the basal ganglia. Nat Neurosci 2005;8:1491-1493.
64. Shashidharan P, Sandu D, Potla U, et al. Transgenic mouse model of early-onset DYT1 dystonia. Hum Mol Genet 2005;14:125-133.
65. Lange N, Hamann M, Shashidharan P, Richter A. Behavioural and pharmacological examinations in a transgenic mouse model of early-onset torsion dystonia. Pharmacol Biochem Behav 2011;97:647-655.
66. Sharma N, Baxter MG, Petravicz J, et al. Impaired motor learning in mice expressing torsinA with the DYT1 dystonia mutation. J Neurosci 2005;25:5351-5355.
67. Zhao Y, DeCuypere M, LeDoux MS. Abnormal motor function and dopamine neurotransmission in DYT1 DeltaGAG transgenic mice. Exp Neurol 2008;210:719-730.
68. Balcioglu A, Kim MO, Sharma N, Cha JH, Breakefield XO, Standaert DG. Dopamine release is impaired in a mouse model of DYT1 dystonia. J Neurochem 2007;102:783-788.
69. Hewett J, Johanson P, Sharma N, Standaert D, Balcioglu A. Function of dopamine transporter is compromised in DYT1 transgenic animal model in vivo. J Neurochem 2010;113:228-235.
70. Martella G, Tassone A, Sciamanna G, et al. Impairment of bidirectional synaptic plasticity in the striatum of a mouse model of DYT1 dystonia: role of endogenous acetylcholine. Brain 2009;132(pt 9):2336-2349.
71. Sciamanna G, Tassone A, Mandolesi G, et al. Cholinergic dysfunction alters synaptic integration between thalamostriatal and corticostriatal inputs in DYT1 dystonia. J Neurosci 2012;32:11991-12004.
72. 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.
73. Sciamanna G, Tassone A, Martella G, et al. Developmental profile of the aberrant dopamine D2 receptor response in striatal cholinergic interneurons in DYT1 dystonia [serial online]. PLoS One 2011;6:e24261.
74. 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.
75. 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.
76. 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.
77. Grundmann K, Reischmann B, Vanhoutte G, et al. Overexpression of human wildtype torsinA and human DeltaGAG torsinA in a transgenic mouse model causes phenotypic abnormalities. Neurobiol Dis 2007;27:190-206.
78. Grundmann K, Glockle N, Martella G, et al. Generation of a novel rodent model for DYT1 dystonia. Neurobiol Dis 2012;47:61-74.
79. Zimprich A, Grabowski M, Asmus F, et al. Mutations in the gene encoding epsilon-sarcoglycan cause myoclonus-dystonia syndrome. Nat Genet 2001;29:66-69.
80. Asmus F, Zimprich A, Tezenas Du Montcel S, et al. Myoclonus-dystonia syndrome: epsilon-sarcoglycan mutations and phenotype. Ann Neurol 2002;52:489-492.
81. Foncke EM, Gerrits MC, van Ruissen F, et al. Distal myoclonus and late onset in a large Dutch family with myoclonus-dystonia. Neurology 2006;67:1677-1680.
82. Piras G, El Kharroubi A, Kozlov S, et al. Zac1 (Lot1), a potential tumor suppressor gene, and the gene for epsilon-sarcoglycan are maternally imprinted genes: identification by a subtractive screen of novel uniparental fibroblast lines. Mol Cell Biol 2000;20:3308-3315.
83. Yokoi F, Dang MT, Mitsui S, Li Y. Exclusive paternal expression and novel alternatively spliced variants of epsilon-sarcoglycan mRNA in mouse brain. FEBS Lett 2005;579:4822-4828.
84. Ritz K, van Schaik BD, Jakobs ME, et al. SGCE isoform characterization and expression in human brain: implications for myoclonus-dystonia pathogenesis? Eur J Hum Genet 2011;19:438-444.
85. Ettinger AJ, Feng G, Sanes JR. epsilon-Sarcoglycan, a broadly expressed homologue of the gene mutated in limb-girdle muscular dystrophy 2D. J Biol Chem 1997;272:32534-32538.
86. Ettinger AJ, Feng G, Sanes JR. epsilon-Sarcoglycan, a broadly expressed homologue of the gene mutated in limb-girdle muscular dystrophy 2D [erratum]. J Biol Chem 1998;273:19922.
87. Yokoi F, Dang MT, Li J, Li Y. Myoclonus, motor deficits, alterations in emotional responses and monoamine metabolism in epsilon-sarcoglycan deficient mice. J Biochem 2006;140:141-146.
88. Lancioni A, Rotundo IL, Kobayashi YM, et al. Combined deficiency of alpha and epsilon sarcoglycan disrupts the cardiac dystrophin complex. Hum Mol Genet 2011;20:4644-4654.
89. Schwenk F, Baron U, Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 1995;23:5080-5081.
90. Hubsch C, Vidailhet M, Rivaud-Pechoux S, et al. Impaired saccadic adaptation in DYT11 dystonia. J Neurol Neurosurg Psychiatry 2011;82:1103-1106.
91. Prsa M, Thier P. The role of the cerebellum in saccadic adaptation as a window into neural mechanisms of motor learning. Eur J Neurosci 2011;33:2114-2128.
92. Nagano A, Arahata K. Nuclear envelope proteins and associated diseases. Curr Opin Neurol 2000;13:533-539.
93. Yokoi F, Dang MT, Zhou T, Li Y. Abnormal nuclear envelopes in the striatum and motor deficits in DYT11 myoclonus-dystonia mouse models. Hum Mol Genet 2012;21:916-925.
94. Yokoi F, Dang MT, Yang G, et al. Abnormal nuclear envelope in the cerebellar Purkinje cells and impaired motor learning in DYT11 myoclonus-dystonia mouse models. Behav Brain Res 2012;227:12-20.
95. Beukers RJ, Booij J, Weisscher N, Zijlstra F, van Amelsvoort TA, Tijssen MA. Reduced striatal D2 receptor binding in myoclonus-dystonia. Eur J Nucl Med Mol Imaging 2009;36:269-274.
96. Zhang L, Yokoi F, Parsons DS, Standaert DG, Li Y. Alteration of striatal dopaminergic neurotransmission in a mouse model of DYT11 myoclonus-dystonia [serial online]. PLoS One 2012;7:e33669.
97. Brashear A, Dobyns WB, de Carvalho Aguiar P, et al. The phenotypic spectrum of rapid-onset dystonia-parkinsonism (RDP) and mutations in the ATP1A3 gene. Brain 2007;130(pt 3):828-835.
98. Dobyns WB, Ozelius LJ, Kramer PL, et al. Rapid-onset dystonia-parkinsonism. Neurology 1993;43:2596-2602.
99. Linazasoro G, Indakoetxea B, Ruiz J, Van Blercom N, Lasa A. Possible sporadic rapid-onset dystonia-parkinsonism. Mov Disord 2002;17:608-609.
100. Pittock SJ, Joyce C, O'Keane V, et al. Rapid-onset dystonia-parkinsonism: a clinical and genetic analysis of a new kindred. Neurology 2000;55:991-995.
101. Zaremba J, Mierzewska H, Lysiak Z, Kramer P, Ozelius LJ, Brashear A. Rapid-onset dystonia-parkinsonism: a fourth family consistent with linkage to chromosome 19q13. Mov Disord 2004;19:1506-1510.
102. Brashear A, DeLeon D, Bressman SB, Thyagarajan D, Farlow MR, Dobyns WB. Rapid-onset dystonia-parkinsonism in a second family. Neurology 1997;48:1066-1069.
103. de Carvalho Aguiar P, Sweadner KJ, Penniston JT, et al. Mutations in the Na+/K+-ATPase alpha3 gene ATP1A3 are associated with rapid-onset dystonia parkinsonism. Neuron 2004;43:169-175.
104. Cannon SC. Pathomechanisms in channelopathies of skeletal muscle and brain. Annu Rev Neurosci 2006;29:387-415.
105. Moseley AE, Williams MT, Schaefer TL, et al. Deficiency in Na, K-ATPase alpha isoform genes alters spatial learning, motor activity, and anxiety in mice. J Neurosci 2007;27:616-626.
106. DeAndrade MP, Yokoi F, van Groen T, Lingrel JB, Li Y. Characterization of Atp1a3 mutant mice as a model of rapid-onset dystonia with parkinsonism. Behav Brain Res 2011;216:659-665.
107. Kirshenbaum GS, Saltzman K, Rose B, Petersen J, Vilsen B, Roder JC. Decreased neuronal Na+, K+-ATPase activity in Atp1a3 heterozygous mice increases susceptibility to depression-like endophenotypes by chronic variable stress. Genes Brain Behav 2011;10:542-550.
108. Karp BI. Botulinum toxin physiology in focal hand and cranial dystonia. Toxins (Basel) 2012;4:1404-1414.
109. Yu H, Neimat JS. The treatment of movement disorders by deep brain stimulation. Neurotherapeutics 2008;5:26-36.
110. Cao S, Hewett JW, Yokoi F, et al. Chemical enhancement of torsinA function in cell and animal models of torsion dystonia. Dis Model Mech 2010;3(5-6):386-396.
111. Carroll D. Genome engineering with zinc-finger nucleases. Genetics 2011;188:773-782.
112. Yan Z, Sun X, Engelhardt JF. Progress and prospects: techniques for site-directed mutagenesis in animal models. Gene Ther 2009;16:581-588.
113. Maeder ML, Thibodeau-Beganny S, Osiak A, et al. Rapid "open-source" engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell 2008;31:294-301.
114. Reyon D, Kirkpatrick JR, Sander JD, et al. ZFNGenome: a comprehensive resource for locating zinc finger nuclease target sites in model organisms [serial online]. BMC Genomics 2011;12:83.
115. Tanabe LM, Martin C, Dauer WT. Genetic background modulates the phenotype of a mouse model of DYT1 dystonia [serial online]. PLoS One 2012;7:e32245.