Of rodents and men: Understanding the emergence of motor and cognitive symptoms in Huntington disease

Behavioural Pharmacology

Volumn 27, Issue 5, 2016, Pages 403-414

  Abada, Yah Se K ^a   Ellenbroek, Bart A ^b  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

animal models; chorea; cognitive symptoms; Huntington disease; motor impairments; neurodegeneration; preclinical

Indexed keywords

CENTRAL NERVOUS SYSTEM AGENTS; TOXIN;

ANIMAL MODEL; COGNITION ASSESSMENT; COGNITIVE DEFECT; DRUG SCREENING; GENETIC MODEL; HUMAN; HUNTINGTON CHOREA; MOTOR DYSFUNCTION; MOUSE MODEL; NONHUMAN; PRECLINICAL STUDY; RAT MODEL; REVIEW; ANIMAL; BIOASSAY; COGNITION DISORDERS; DISEASE MODEL; GENETICS; MOUSE; PATHOPHYSIOLOGY; PROCEDURES; RAT; SPECIES DIFFERENCE; TRANSLATIONAL RESEARCH;

ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; ENDPOINT DETERMINATION; HUMANS; HUNTINGTON DISEASE; MICE; RATS; SPECIES SPECIFICITY; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84958824545     PISSN: 09558810     EISSN: 14735849     Source Type: Journal    
DOI: 10.1097/FBP.0000000000000217     Document Type: Review

References (131)

1. Abada YS, Schreiber R, Ellenbroek B (2013a). Motor, emotional and cognitive deficits in adult BACHD mice: a model for Huntington's disease. Behav Brain Res 238:243-251.
2. Abada YS, Nguyen HP, Schreiber R, Ellenbroek B (2013b). Assessment of motor function, sensory motor gating and recognition memory in a novel BACHD transgenic rat model for huntington disease. PLoS One 8:e68584.
3. Abada YS, Nguyen HP, Ellenbroek B, Schreiber R (2013c). Reversal learning and associative memory impairments in a BACHD rat model for Huntington disease. PLoS One 8:e71633.
4. Ahmari SE, Risbrough VB, Geyer MA, Simpson HB (2012). Impaired sensorimotor gating in unmedicated adults with obsessive-compulsive disorder. Neuropsychopharmacology 37:1216-1223.
5. Amende I, Kale A, McCue S, Glazier S, Morgan JP, Hampton TG (2005). Gait dynamics in mouse models of Parkinson's disease and Huntington's disease. J Neuroeng Rehabil 2:20.
6. Antoniades CA, Ober J, Hicks S, Siuda G, Carpenter RH, Kennard C, Nemeth AH (2012). Statistical characteristics of finger-tapping data in Huntington's disease. Med Biol Eng Comput 50:341-346.
7. Armstrong MJ, Miyasaki JM (2012). Evidence-based guideline: pharmacologic treatment of chorea in Huntington disease: report of the guideline development subcommittee of the American Academy of Neurology. Neurology 79:597-603.
8. Bezprozvanny I, Hayden MR (2004). Deranged neuronal calcium signaling and Huntington disease. Biochem Biophys Res Commun 322:1310-1317.
9. Birrell JM, Brown VJ (2000). Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20:4320-4324.
10. Bolivar VJ, Manley K, Messer A (2003). Exploratory activity and fear conditioning abnormalities develop early in R6/2 Huntington's disease transgenic mice. Behav Neurosci 117:1233-1242.
11. Braff DL, Geyer MA, Swerdlow NR (2001). Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156:234-258.
12. Brooks S, Higgs G, Jones L, Dunnett SB (2012a). Longitudinal analysis of the behavioural phenotype in Hdh(CAG)150 Huntington's disease knock-in mice. Brain Res Bull 88:182-188.
13. Brooks SP, Janghra N, Higgs GV, Bayram-Weston Z, Heuer A, Jones L, Dunnett SB (2012). Selective cognitive impairment in the YAC128 Huntington's disease mouse. Brain Res Bull 88:121-129.
14. Brouillet E, Hantraye P, Ferrante RJ, Dolan R, Leroy-Willig A, Kowall NW, Beal MF (1995). Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc Natl Acad Sci USA 92:7105-7109.
15. Brouillet E, Guyot MC, Mittoux V, Altairac S, Condé F, Palfi S, Hantraye P (1998). Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in rat. J Neurochem 70:794-805.
16. Browne SE, Bowling AC, MacGarvey U, Baik MJ, Berger SC, Muqit MM, et al. (1997). Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann Neurol 41: 646-653.
17. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, et al. (1999). Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 19:3248-3257.
18. Caviston JP, Holzbaur EL (2009). Huntingtin as an essential integrator of intracellular vesicular trafficking. Trends Cell Biol 19:147-155.
19. Chiu CT, Liu G, Leeds P, Chuang DM (2011). Combined treatment with the mood stabilizers lithium and valproate produces multiple beneficial effects in transgenic mouse models of Huntington's disease. Neuropsychopharmacology 36:2406-2421.
20. Chuang CS, Su HL, Cheng FC, Hsu SH, Chuang CF, Liu CS (2010). Quantitative evaluation of motor function before and after engraftment of dopaminergic neurons in a rat model of Parkinson's disease. J Biomed Sci 17:9.
21. Chen X, Wu J, Lvovskaya S, Herndon E, Supnet C, Bezprozvanny I (2011). Dantrolene is neuroprotective in Huntington's disease transgenic mouse model. Mol Neurodegener 6:81.
22. Ciamei A, Morton AJ (2009). Progressive imbalance in the interaction between spatial and procedural memory systems in the R6/2 mouse model of Huntington's disease. Neurobiol Learn Mem 92:417-428.
23. Cisbani G, Cicchetti F (2012). An in vitro perspective on the molecular mechanisms underlying mutant huntingtin protein toxicity. Cell Death Dis 3: e382.
24. Crawley JN (2008). Behavioral phenotyping strategies for mutant mice. Neuron 57:809-818.
25. Crook ZR, Housman D (2011). Huntington's disease: can mice lead the way to treatment? Neuron 69:423-435.
26. Delval A, Krystkowiak P, Blatt JL, Labyt E, Dujardin K, Destée A, et al. (2006). Role of hypokinesia and bradykinesia in gait disturbances in Huntington's disease: a biomechanical study. J Neurol 253:73-80.
27. Deumens R, Jaken RJ, Marcus MA, Joosten EA (2007). The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection. J Neurosci Methods 164:120-130.
28. Dias R, Robbins TW, Roberts AC (1996). Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:69-72.
29. Doria JG, Silva FR, de Souza JM, Vieira LB, Carvalho TG, Reis HJ, et al. (2013). Metabotropic glutamate receptor 5 positive allosteric modulators are neuroprotective in a mouse model of Huntington's disease. Br J Pharmacol 169:909-921.
30. Doria JG, de Souza JM, Andrade JN, Rodrigues HA, Guimaraes IM, Carvalho TG, et al. (2015). The mGluR5 positive allosteric modulator, CDPPB, ameliorates pathology and phenotypic signs of a mouse model of Huntington's disease. Neurobiol Dis 73:163-173.
31. Drug Discovery News (2013). Two ways to look at it. June; vol. 9 No. 6.
32. Ehrlich ME (2012). Huntington's disease and the striatal medium spiny neuron: cell-autonomous and non-cell-autonomous mechanisms of disease. Neurotherapeutics 9:270-284.
33. European Huntington Disease Network News (EHDN News, 2014). Issue 23; p. 2; http://www.euro-hd.net/html/disease/archive/ehdn-newsletter-nov2014. pdf.
34. Fekete R, Davidson A, Jankovic J (2012). Clinical assessment of the effect of tetrabenazine on functional scales in huntington disease: a pilot open label study. Tremor Other Hyperkinet Mov (N Y) 2pii:tre-02-86-476-4.
35. Fernagut PO, Diguet E, Stefanova N, Biran M, Wenning GK, Canioni P, et al. (2002). Subacute systemic 3-nitropropionic acid intoxication induces a distinct motor disorder in adult C57Bl/6 mice: behavioural and histopathological characterization. Neuroscience 114:1005-1017.
36. Ferrante RJ, Andreassen OA, Dedeoglu A, Ferrante KL, Jenkins BG, Hersch SM, Beal MF (2002). Therapeutic effects of coenzyme Q10 and remacemide in transgenic mouse models of Huntington's disease. J Neurosci 22:1592-1599.
37. Fisher SP, Black SW, Schwartz MD,Wilk AJ, Chen TM, LincolnWU, et al. (2013). Longitudinal analysis of the electroencephalogram and sleep phenotype in the R6/2 mousemodel of Huntington's disease. Brain 136 (Pt 7):2159-2172.
38. Francelle L, Galvan L, Brouillet E (2014). Possible involvement of self-defense mechanisms in the preferential vulnerability of the striatum in Huntington's disease. Front Cell Neurosci 8:295.
39. Garner JP, Thogerson CM, Würbel H, Murray JD, Mench JA (2006). Animal neuropsychology: validation of the Intra-Dimensional Extra-Dimensional set shifting task for mice. Behav Brain Res 173:53-61.
40. Georgiou N, Bradshaw JL, Phillips JG, Chiu E, Bradshaw JA (1995). Reliance on advance information and movement sequencing in Huntington's disease. Mov Disord 10:472-481.
41. Giralt A, Saavedra A, Carretón O, Xifró X, Alberch J, Pérez-Navarro E (2011). Increased PKA signaling disrupts recognition memory and spatial memory: role in Huntington's disease. Hum Mol Genet 20:4232-4247.
42. Gray M, Shirasaki DI, Cepeda C, André VM, Wilburn B, Lu XH, et al. (2008). Fulllength human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice. J Neurosci 28:6182-6195.
43. Grimbergen YA, Knol MJ, Bloem BR, Kremer BP, Roos RA, Munneke M (2008). Falls and gait disturbances in Huntington's disease. Mov Disord 23:970-976.
44. Hamers FP, Lankhorst AJ, van Laar TJ, Veldhuis WB, Gispen WH (2001). Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J Neurotrauma 18:187-201.
45. Hamm RJ, Pike BR, O'Dell DM, Lyeth BG, Jenkins LW (1994). The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J Neurotrauma 11:187-196.
46. Hedreen JC, Folstein SE (1995). Early loss of neostriatal striosome neurons in Huntington's disease. J Neuropathol Exp Neurol 54:105-120.
47. Heikkinen T, Lehtimäki K, Vartiainen N, Puoliväli J, Hendricks SJ, Glaser JR, et al. (2012). Characterization of neurophysiological and behavioral changes, MRI brain volumetry and 1H MRS in zQ175 knock-in mouse model of Huntington's disease. PLoS One 7:e50717.
48. Herbin M, Hackert R, Gasc JP, Renous S (2007). Gait parameters of treadmill versus overground locomotion in mouse. Behav Brain Res 181:173-179.
49. Hsiao HY, Chiu FL, Chen CM, Wu YR, Chen HM, Chen YC, et al. (2014). Inhibition of soluble tumor necrosis factor is therapeutic in Huntington's disease. Hum Mol Genet 23:4328-4344.
50. Huerta JJ, Llamosas MM, Cernuda-Cernuda R, García-Fernández JM (1999). Spatio-temporal analysis of light-induced Fos expression in the retina of rd mutant mice. Brain Res 834:122-127.
51. Huntington Study Group (1996). Unified Huntington's Disease Rating Scale: reliability and consistency. Huntington Study Group. Mov Disord 11: 136-142.
52. Huntington Study Group (2001). A randomized, placebo-controlled trial of coenzyme Q10 and remacemide in Huntington's disease. Neurology 57: 397-404.
53. Huntington Study Group Pre2CARE Investigators, Hyson HC, Kieburtz K, Shoulson I, McDermott M, Ravina B, de Blieck EA, et al. (2010). Safety and tolerability of high-dosage coenzyme Q10 in Huntington's disease and healthy subjects. Mov Disord 25:1924-1928.
54. Huntington's Disease Collaborative Research Group (1993). A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell 72:971-983.
55. Jackson GR, Salecker I, Dong X, Yao X, Arnheim N, Faber PW, et al. (1998). Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron 21:633-642.
56. Jansson EK, Clemens LE, Riess O, Nguyen HP (2014). Reduced motivation in the BACHD rat model of Huntington disease is dependent on the choice of food deprivation strategy. PLoS One 9:e105662.
57. Jenkins JB, Conneally PM (1989). The paradigm of Huntington disease. Am J Hum Genet 45:169-175.
58. Jia H, Kast RJ, Steffan JS, Thomas EA (2012). Selective histone deacetylase (HDAC) inhibition imparts beneficial effects in Huntington's disease mice: implications for the ubiquitin-proteasomal and autophagy systems. Hum Mol Genet 21:5280-5293.
59. Kohl S, Heekeren K, Klosterkötter J, Kuhn J (2013). Prepulse inhibition in psychiatric disorders-apart from schizophrenia. J Psychiatr Res 47:445-452.
60. Koller WC, Trimble J (1985). The gait abnormality of Huntington's disease. Neurology 35:1450-1454.
61. Kordasiewicz HB, Stanek LM, Wancewicz EV, Mazur C, McAlonis MM, Pytel KA, et al. (2012). Sustained therapeutic reversal of Huntington's disease by transient repression of huntingtin synthesis. Neuron 74:1031-1044.
62. Krobitsch S, Kazantsev AG (2011). Huntington's disease: from molecular basis to therapeutic advances. Int J Biochem Cell Biol 43:20-24.
63. Kudwa AE, Menalled LB, Oakeshott S, Murphy C, Mushlin R, Fitzpatrick J, et al. (2013). Increased body weight of the BAC HD transgenic mouse model of huntington's disease accounts for some but not all of the observed HD-like motor deficits. PLoS Curr 5:Edition 1.
64. Lange KW, Sahakian BJ, Quinn NP, Marsden CD, Robbins TW (1995). Comparison of executive and visuospatial memory function in Huntington's disease and dementia of Alzheimer type matched for degree of dementia. J Neurol Neurosurg Psychiatry 58:598-606.
65. Lawrence AD, Sahakian BJ, Hodges JR, Rosser AE, Lange KW, Robbins TW (1996). Executive and mnemonic functions in early Huntington's disease. Brain 119 (Pt 5):1633-1645.
66. Lawrence AD, Hodges JR, Rosser AE, Kershaw A, ffrench-Constant C, Rubinsztein DC, et al. (1998). Evidence for specific cognitive deficits in preclinical Huntington's disease. Brain 121 (Pt 7):1329-1341.
67. Lawrence AD, Sahakian BJ, Rogers RD, Hodge JR, Robbins TW (1999). Discrimination, reversal, and shift learning in Huntington's disease: mechanisms of impaired response selection. Neuropsychologia 37:1359-1374.
68. Lawrence AD, Watkins LH, Sahakian BJ, Hodges JR, Robbins TW (2000). Visual object and visuospatial cognition in Huntington's disease: implications for information processing in corticostriatal circuits. Brain 123 (Pt 7): 1349-1364.
69. Li XJ, Li S (2012). Influence of species differences on the neuropathology of transgenic Huntington's disease animal models. J Genet Genomics 39: 239-245.
70. Lin CH, Tallaksen-Greene S, Chien WM, Cearley JA, Jackson WS, Crouse AB, et al. (2001). Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum Mol Genet 10:137-144.
71. Lione LA, Carter RJ, Hunt MJ, Bates GP, Morton AJ, Dunnett SB (1999). Selective discrimination learning impairments in mice expressing the human Huntington's disease mutation. J Neurosci 19:10428-10437.
72. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, et al. (1996). Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87: 493-506.
73. Mann J, Chiu E (1978). Platelet monoamine oxidase activity in Huntington's chorea. J Neurol Neurosurg Psychiatry 41:809-812.
74. Menalled L, Brunner D (2014). Animal models of Huntington's disease for translation to the clinic: best practices. Mov Disord 29:1375-1390.
75. Menalled L, El-Khodor BF, Patry M, Suárez-Fariñas M, Orenstein SJ, Zahasky B, et al. (2009). Systematic behavioral evaluation of Huntington's disease transgenic and knock-in mouse models. Neurobiol Dis 35:319-336.
76. Menalled LB, Kudwa AE, Miller S, Fitzpatrick J,Watson-Johnson J, Keating N, et al. (2012). Comprehensive behavioral and molecular characterization of a new knock-in mouse model of Huntington's disease: zQ175. PLoS One 7:e49838.
77. Menalled LB, Kudwa AE, Oakeshott S, Farrar A, Paterson N, Filippov I, et al. (2014). Genetic deletion of transglutaminase 2 does not rescue the phenotypic deficits observed in R6/2 and zQ175 mouse models of Huntington's disease. PLoS One 9:e99520.
78. Mestre T, Ferreira J, Coelho MM, Rosa M, Sampaio C (2009). Therapeutic interventions for symptomatic treatment in Huntington's disease. Cochrane Database Syst Rev :CD006456.
79. Mittal SK, Eddy C (2013). The role of dopamine and glutamate modulation in Huntington disease. Behav Neurol 26:255-263.
80. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, et al., Mouse Genome Sequencing Consortium (2002). Initial sequencing and comparative analysis of the mouse genome. Nature 420:520-562.
81. National Institute of Neurological Disorders and Stroke (NINDS) (2014). Announcement of 2CARE Early study Closure. NINDS Clinical Trials http:// www.ninds.nih.gov/disorders/clinical-trials/2CARE-Early-Study-Closure.htm.
82. Nguyen HP, Kobbe P, Rahne H, Wörpel T, Jäger B, Stephan M, et al. (2006). Behavioral abnormalities precede neuropathological markers in rats transgenic for Huntington's disease. Hum Mol Genet 15:3177-3194.
83. Norflus F, Nanje A, Gutekunst CA, Shi G, Cohen J, Bejarano M, et al. (2004). Antiinflammatory treatment with acetylsalicylate or rofecoxib is not neuroprotective in Huntington's disease transgenic mice. Neurobiol Dis 17:319-325.
84. Novak MJ, Tabrizi SJ (2010). Huntington's disease Clinical Review. BMJ 340: c3109.
85. Ouary S, Bizat N, Altairac S, Ménétrat H, Mittoux V, Condé F, et al. (2000). Major strain differences in response to chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid in rats: implications for neuroprotection studies. Neuroscience 97:521-530.
86. Pallier PN, Drew CJ, Morton AJ (2009). The detection and measurement of locomotor deficits in a transgenic mouse model of Huntington's disease are task-and protocol-dependent: influence of non-motor factors on locomotor function. Brain Res Bull 78:347-355.
87. Paulsen JS, Langbehn DR, Stout JC, Aylward E, Ross CA, Nance M, et al. (2008). Detection of Huntington's disease decades before diagnosis: the Predict-HD study. J Neurol Neurosurg Psychiatry 79:874-880.
88. Pereira JE, Cabrita AM, Filipe VM, Bulas-Cruz J, Couto PA, Melo-Pinto P, et al. (2006). A comparison analysis of hindlimb kinematics during overground and treadmill locomotion in rats. Behav Brain Res 172:212-218.
89. Pidgeon C, Rickards H (2013). The pathophysiology and pharmacological treatment of Huntington disease. Behav Neurol 26:245-253.
90. Ponomareva N, Klyushnikov S, Abramycheva N, Malina D, Scheglova N, Fokin V, et al. (2014). Alpha-theta border EEG abnormalities in preclinical Huntington's disease. J Neurol Sci 344:114-120.
91. Pouladi MA, Stanek LM, Xie Y, Franciosi S, Southwell AL, Deng Y, et al. (2012). Marked differences in neurochemistry and aggregates despite similar behavioural and neuropathological features of Huntington disease in the full-length BACHD and YAC128 mice. Hum Mol Genet 21:2219-2232.
92. Ramaswamy S, McBride JL, Kordower JH (2007). Animal models of Huntington's disease. ILAR J 48:356-373.
93. Ramaswamy S, McBride JL, Han I, Berry-Kravis EM, Zhou L, Herzog CD, et al. (2009). Intrastriatal CERE-120 (AAV-Neurturin) protects striatal and cortical neurons and delays motor deficits in a transgenic mouse model of Huntington's disease. Neurobiol Dis 34:40-50.
94. Rao AK, Gordon AM, Marder KS (2011). Coordination of fingertip forces during precision grip in premanifest Huntington's disease26:862-869.
95. Robinson L, Riedel G (2014). Comparison of automated home-cage monitoring systems: emphasis on feeding behaviour, activity and spatial learning following pharmacological interventions. J Neurosci Methods 234:13-25.
96. Sanberg PR, Calderon SF, Giordano M, Tew JM, Norman AB (1989). The quinolinic acid model of Huntington's disease: locomotor abnormalities. Exp Neurol 105:45-53.
97. Schilling G, Becher MW, Sharp AH, Jinnah HA, Duan K, Kotzuk JA, et al. (1999). Intranuclear inclusions and neuritic aggregates in transgenic mice expressing a mutant N-terminal fragment of huntingtin. Hum Mol Genet 8:397-407.
98. Schilling G, Coonfield ML, Ross CA, Borchelt DR (2001). Coenzyme Q10 and remacemide hydrochloride ameliorate motor deficits in a Huntington's disease transgenic mouse model. Neurosci Lett 315:149-153.
99. Schwarcz R, Guidetti P, Sathyasaikumar KV, Muchowski PJ (2010). Of mice, rats and men: revisiting the quinolinic acid hypothesis of Huntington's disease. Prog Neurobiol 90:230-245.
100. Scott LJ (2011). Tetrabenazine: for chorea associated with Huntington's disease. CNS Drugs 25:1073-1085.
101. Shelbourne PF, Killeen N, Hevner RF, Johnston HM, Tecott L, Lewandoski M, et al. (1999). A Huntington's disease CAG expansion at the murine Hdh locus is unstable and associated with behavioural abnormalities in mice. Hum Mol Genet 8:763-774.
102. Slow EJ, van Raamsdonk J, Rogers D, Coleman SH, Graham RK, Deng Y, et al. (2003). Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum Mol Genet 12:1555-1567.
103. Smith MA, Brandt J, Shadmehr R (2000). Motor disorder in Huntington's disease begins as a dysfunction in error feedback control. Nature 403:544-549.
104. Smith KM, Matson S, Matson WR, Cormier K, Del Signore SJ, Hagerty SW, et al. (2006). Dose ranging and efficacy study of high-dose coenzyme Q10 formulations in Huntington's disease mice. Biochem Biophys Acta 1762:616-626.
105. Southwell AL, Ko J, Patterson PH (2009). Intrabody gene therapy ameliorates motor, cognitive, and neuropathological symptoms in multiple mouse models of Huntington's disease. J Neurosci 29:13589-13602.
106. Stack EC, Kubilus JK, Smith K, Cormier K, Del Signore SJ, Guelin E, et al. (2005). Chronology of behavioral symptoms and neuropathological sequela in R6/2 Huntington's disease transgenic mice. J Comp Neurol 490:354-370.
107. Stout JC, Paulsen JS, Queller S, Solomon AC, Whitlock KB, Campbell JC, et al. (2011). Neurocognitive signs in prodromal Huntington disease. Neuropsychology 25:1-14.
108. Sun Z, Xie J, Reiner A (2002). The differential vulnerability of striatal projection neurons in 3-nitropropionic acid-treated rats does not match that typical of adult-onset Huntington's disease. Exp Neurol 176:55-65.
109. Swerdlow NR, Geyer MA (1998). Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 24:285-301.
110. Swerdlow NR, Paulsen J, Braff DL, Butters N, Geyer MA, Swenson MR (1995). Impaired prepulse inhibition of acoustic and tactile startle response in patients with Huntington's disease. J Neurol Neurosurg Psychiatry 58:192-200.
111. Swerdlow NR, Geyer MA, Braff DL (2001). Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl) 156:194-215.
112. Taketo M, Schroeder AC, Mobraaten LE, Gunning KB, Hanten G, Fox RR, et al. (1991). FVB/N: an inbred mouse strain preferable for transgenic analyses. Proc Natl Acad Sci USA 88:2065-2069.
113. Tang TS, Chen X, Liu J, Bezprozvanny I (2007). Dopaminergic signaling and striatal neurodegeneration in Huntington's disease. J Neurosci 27:7899-7910.
114. Trushina E, Dyer RB, Badger JD, Ure D, Eide L, Tran DD, et al. (2004). Mutant huntingtin impairs axonal trafficking in mammalian neurons in vivo and in vitro. Mol Cell Biol 24:8195-8209.
115. Urbach YK, Raber KA, Canneva F, Plank AC, Andreasson T, Ponten H, et al. (2014). Automated phenotyping and advanced data mining exemplified in rats transgenic for Huntington's disease. J Neurosci Methods 234:38-53.
116. van Raamsdonk JM, Pearson J, Slow EJ, Hossain SM, Hayden MR (2005). Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington's disease. J Neurosci 25: 4169-4180.
117. Vandeputte C, Taymans JM, Casteels C, Coun F, Ni Y, Van Laere K, Baekelandt V (2010). Automated quantitative gait analysis in animal models of movement disorders. BMC Neurosci 11:92.
118. Vlamings R, Zeef DH, Janssen ML, Oosterloo M, Schaper F, Jahanshahi A, Temel Y (2012). Lessons learned from the transgenic Huntington's disease rats. Neural Plast 2012:682712.
119. von Hörsten S, Schmitt I, Nguyen HP, Holzmann C, Schmidt T, Walther T, et al. (2003). Transgenic rat model of Huntington's disease. Hum Mol Genet 12:617-624.
120. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP Jr (1985). Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44:559-577.
121. Walker FO (2007). Huntington's disease. Lancet 369:218-228.
122. Wheeler VC, White JK, Gutekunst CA, Vrbanac V, Weaver M, Li XJ, et al. (2000). Long glutamine tracts cause nuclear localization of a novel form of huntingtin in medium spiny striatal neurons in HdhQ92 and HdhQ111 knock-in mice. Hum Mol Genet 9:503-513.
123. Woodman B, Butler R, Landles C, Lupton MK, Tse J, Hockly E, et al. (2007). The Hdh(Q150/Q150) knock-in mouse model of HD and the R6/2 exon 1 model develop comparable and widespread molecular phenotypes. Brain Res Bull 72:83-97.
124. Wooley CM, Xing S, Burgess RW, Cox GA, Seburn KL (2009). Age, experience and genetic background influence treadmill walking in mice. Physiol Behav 96:350-361.
125. Yang XW, Gray M (2011). Mouse models for validating preclinical candidates for Huntington's disease. In: Lo DC, Hughes RE, editors. Neurobiology of Huntington's disease: applications to drug discovery. Boca Raton, FL: CRC Press. pp. 166-186.
126. Yang XW, Model P, Heintz N (1997). Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat Biotechnol 15:859-865.
127. Yang SH, Cheng PH, Banta H, Piotrowska-Nitsche K, Yang JJ, Cheng EC, et al. (2008). Towards a transgenic model of Huntington's disease in a non-human primate. Nature 453:921-924.
128. Yu-Taeger L, Petrasch-Parwez E, Osmand AP, Redensek A, Metzger S, Clemens LE, et al. (2012). A novel BACHD transgenic rat exhibits characteristic neuropathological features of Huntington disease. J Neurosci 32:15426-15438.
129. Zeef DH, Vlamings R, Lim LW, Tan S, Janssen ML, Jahanshahi A, et al. (2012a). Motor and non-motor behaviour in experimental Huntington's disease. Behav Brain Res 226:435-439.
130. Zeef DH, van Goethem NP, Vlamings R, Schaper F, Jahanshahi A, Hescham S, et al. (2012b). Memory deficits in the transgenic rat model of Huntington's disease. Behav Brain Res 227:194-198.
131. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, Conti L, et al. (2001). Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293:493-498.