Large genetic animal models of huntington’s disease

Journal of Huntington's Disease

Volumn 2, Issue 1, 2013, Pages 3-19

  Jennifer Morton, A ^a   Howland, David S ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CHDI MANAGEMENT CHDI FOUNDATION   (United States)

Author keywords

CAG repeat; Circadian; Minipig; Monkey; Neurodegeneration; Non human primate; Polyglutamine; Sheep; Sleep

Indexed keywords

POLYGLUTAMINE;

ANIMAL; CAG REPEAT; CIRCADIAN; DISEASE MODEL; HAPLORHINI; HUMAN; HUNTINGTON CHOREA; MINIPIG; NERVE DEGENERATION; NON-HUMAN PRIMATE; REVIEW; SHEEP; SLEEP; TRANSGENIC ANIMAL;

CAG REPEAT; CIRCADIAN; MINIPIG; MONKEY; NEURODEGENERATION; NON-HUMAN PRIMATE; POLYGLUTAMINE; SHEEP; SLEEP;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; HUMANS; HUNTINGTON DISEASE;

EID: 84902330133     PISSN: 18796397     EISSN: 18796400     Source Type: Journal    
DOI: 10.3233/JHD-130050     Document Type: Article

References (110)

1. The Huntington’s Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cell. 1993;72: 971.
2. Strong TV, Tagle DA, Valdes JM, Elmer LW, Boehm K, Swaroop M, Kaatz KW, Collins FS, Albin RL. Widespread expression of the human and rat Huntington’s disease gene in brain and nonneural tissues. Nat Genet. 1993;5(3): 259.
3. Sharp AH, Loev SJ, Schilling G, Li SH, Li XJ, Bao J, Wagster MV, Kotzuk JA, Steiner JP, Lo A, et al. Widespread expression of Huntington’s disease gene (IT15) protein product. Neuron. 1995;14(5): 1065.
4. Gusella JF, MacDonald ME. Huntington’s disease: CAG genetics expands neurobiology. Curr Opin Neurobiol. 1995;5(5): 656.
5. Zoghbi HY, Orr HT. Glutamine repeats and neurodegeneration. Annu Rev Neurosci. 2000;23: 217.
6. Moseley ML, Zu T, Ikeda Y, Gao W, Mosemiller AK, Daughters RS, Chen G, WeatherspoonMR, Clark HB, Ebner TJ, Day JW, Ranum LP. Bidirectional expression of CUG and CAG expansion transcripts and intranuclear polyglutamine inclusions in spinocerebellar ataxia type 8. Nat Genet. 2006;38(7): 758.
7. Bañez-Coronel M, Porta S, Kagerbauer B, Mateu-Huertas E, Pantano L, Ferrer I, Guzmán M, Estivill X, Martí E. A pathogenic mechanism in Huntington’s disease involves small CAG-repeated RNAs with neurotoxic activity. PLoS Genet. 2012;8(2): e1002481.
8. Pearson CE. Repeat associated non-ATG translation initiation: One DNA, two transcripts, seven reading frames, potentially nine toxic entities! PLoS Genet. 2011;7(3): e1002018.
9. Wojciechowska M, Krzyzosiak WJ. CAG repeat RNA as an auxiliary toxic agent in polyglutamine disorders. RNA Biol. 2011;8(4): 565.
10. SmithMM, Mills JA, Epping EA, Westervelt HJ, Paulsen JS; PREDICT-HDInvestigators of the Huntington Study Group. Depressive symptom severity is related to poorer cognitive performance in prodromal Huntington disease. Neuropsychology. 2012;26(5): 664.
11. Harrington DL, Smith MM, Zhang Y, Carlozzi NE, Paulsen JS; PREDICT-HD Investigators of the Huntington Study Group. Cognitive domains that predict time to diagnosis in prodromal Huntington disease. J Neurol Neurosurg Psychiatry. 2012;83(6): 612.
12. Schulte J, Littleton JT. The biological function of the Huntingtin protein and its relevance to Huntington’s Disease pathology. Curr Trends Neurol. 2011;5: 65.
13. Raymond LA, André VM, Cepeda C, Gladding CM, Milnerwood AJ, Levine MS. Pathophysiology of Huntington’s disease: Time-dependent alterations in synaptic and receptor function. Neuroscience. 2011;198: 252.
14. Jones L, Hughes A. Pathogenic mechanisms in Huntington’s disease. Int Rev Neurobiol. 2011;98: 373.
15. Reiner A, Dragatsis I, Dietrich P. Genetics and neuropathology of Huntington’s disease. Int Rev Neurobiol. 2011;98: 325.
16. Shoulson I, Young AB. Milestones in Huntington disease. Mov Disord. 2011;26(6): 1127.
17. Morton AJ. Circadian and sleep disorder in Huntington’s disease. Exp Neurol. 2012. (Epub ahead of print)
18. Ha AD, Fung VS. Huntington’s disease. Curr Opin Neurol. 2012;25(4): 491.
19. Zheng Z, Diamond MI. Huntington disease and the huntingtin protein. Prog Mol Biol Transl Sci. 2012;107: 189.
20. van den Bogaard S, Dumas E, van der Grond J, van Buchem M, Roos R. MRI biomarkers in Huntington’s disease. Front Biosci (Elite Ed). 2012;4: 1910.
21. Shang H, Danek A, Landwehrmeyer B, Burgunder JM. Huntington’s disease: New aspects on phenotype and genotype. Parkinsonism Relat Disord. 2012;18(Suppl 1): S107.
22. Brooks SP, Jones L, Dunnett SB. Comparative analysis of pathology and behavioural phenotypes in mouse models of Huntington’s disease. Brain Res Bull. 2012;88(2-3): 81.
23. Mestre TA, Ferreira JJ. An evidence-based approach in the treatment of Huntington’s disease. Parkinsonism Relat Disord. 2012;18(4): 316.
24. Venuto CS, McGarry A, Ma Q, Kieburtz K. Pharmacologic approaches to the treatment of Huntington’s disease. Mov Disord. 2012;27(1): 31.
25. Ross CA, Tabrizi SJ. Huntington’s disease: From molecular pathogenesis to clinical treatment. Lancet Neurol. 2011: 10(1): 83.
26. Munoz-Sanjuan I, Bates GP. The importance of integrating basic and clinical research toward the development of new therapies for Huntington disease. J Clin Invest. 2011;121(2): 476.
27. Sah DW, Aronin N. Oligonucleotide therapeutic approaches for Huntington disease. J Clin Invest. 2011;121(2): 500.
28. Johnson CD, Davidson BL. Huntington’s disease: Progress toward effective disease-modifying treatments and a cure. Hum Mol Genet. 2010;19(R1): R98-R102
29. McBride JL, Pitzer MR, Boudreau RL, Dufour B, Hobbs T, Ojeda SR, Davidson BL. Preclinical safety of RNAimediated HTT suppression in the rhesus macaque as a potential therapy for Huntington’s disease. Mol Ther. 2011;19(12): 2152.
30. Mangiarini L, SathasivamK, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell. 1996;87(3): 493.
31. Schilling G, Becher MW, Sharp AH, Jinnah HA, Duan K, Kotzuk JA, Slunt HH, Ratovitski T, Cooper JK, Jenkins NA, Copeland NG, Price DL, Ross CA, Borchelt DR. Intranuclear inclusions and neuritic aggregates in transgenic mice expressing a mutant N-terminal fragment of huntingtin. Hum Mol Genet. 1999;8(3): 397. Erratum in: Hum Mol Genet. 1999;8(5): 943.
32. de Almeida LP, Ross CA, Zala D, Aebischer P, Déglon N. Lentiviral-mediated delivery of mutant huntingtin in the striatum of rats induces a selective neuropathology modulated by polyglutamine repeat size, huntingtin expression levels, and protein length. J Neurosci. 2002;22(9): 3473.
33. Slow EJ, van Raamsdonk J, Rogers D, Coleman SH, Graham RK, Deng Y, Oh R, Bissada N, Hossain SM, Yang YZ, Li XJ, Simpson EM, Gutekunst CA, Leavitt BR, Hayden MR. Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease.HumMol Genet. 2003: 12(13); 1555.
34. Gray M, Shirasaki DI, Cepeda C, André VM, Wilburn B, Lu XH, Tao J, Yamazaki I, Li SH, Sun YE, Li XJ, Levine MS, Yang XW. Full-length human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice. J Neurosci. 2008;28(24): 6182.
35. vonHörsten S, Schmitt I, Nguyen HP, Holzmann C, Schmidt T, Walther T, Bader M, Pabst R, Kobbe P, Krotova J, Stiller D, Kask A, Vaarmann A, Rathke-Hartlieb S, Schulz JB, Grasshoff U, Bauer I, Vieira-Saecker AM, Paul M, Jones L, Lindenberg KS, Landwehrmeyer B, Bauer A, Li XJ, Riess O. Transgenic rat model of Huntington’s disease. Hum Mol Genet. 2003;12(6): 617.
36. Yu-Taeger L, Petrasch-Parwez E, Osmand AP, Redensek A, Metzger S, Clemens LE, Park L, Howland D, Calaminus C, Gu X, Pichler B, Yang XW, Riess O, Nguyen HP. A Novel BACHD Transgenic Rat Exhibits Characteristic Neuropathological Features of Huntington Disease. J Neurosci. 2012;32(44): 15426.
37. Wheeler VC, Auerbach W, White JK, Srinidhi J, Auerbach A, Ryan A, Duyao MP, Vrbanac V, Weaver M, Gusella JF, Joyner AL, MacDonald ME. A novel BACHD transgenic rat exhibits characteristic neuropathological features of huntington disease. Hum Mol Genet. 1999;8(1): 115.
38. Lin CH, Tallaksen-Greene S, Chien WM, Cearley JA, Jackson WS, Crouse AB, Ren S, Li XJ, Albin RL, Detloff PJ. Neurological abnormalities in a knock-in mouse model of Huntington’s disease. Hum Mol Genet. 2001;10(2): 137.
39. Menalled LB, Sison JD, Dragatsis I, Zeitlin S, ChesseletMF. Time course of early motor and neuropathological anomalies in a knock-in mouse model of Huntington’s disease with 140 CAG repeats. J Comp Neurol. 2003;465(1): 11.
40. Menalled LB, Kudwa AE, Miller S, Fitzpatrick J, Watson-Johnson J, Keating N, Ruiz M, Mushlin R, Alosio W, McConnell K, Connor D, Murphy C, Oakeshott S, Kwan M, Beltran J, Ghavami A, Brunner D, Park LC, Ramboz S, Howland D. Comprehensive behavioral and molecular characterization of a new knock-in mouse model of huntington’s disease: zQ175. PLoS One. 2012;7(12): e49838
41. Heng MY, Duong DK, Albin RL, Tallaksen-Greene SJ, Hunter JM, Lesort MJ, Osmand A, Paulson HL, Detloff PJ. Early autophagic response in a novel knock-in model of Huntington disease.HumMol Genet. 2010;19(19): 3702.
42. Sathasivam K, Neueder A, Gipson TA, Landles C, Benjamin AC, Bondulich MK, Smith DL, Faull RL, Roos RA, Howland D, Detloff PJ, Housman DE, Bates GP. Aberrant splicing of HTT generates the pathogenic exon 1 protein in Huntington disease. Proc Natl Acad Sci U S A. 2013;110(6): 2366-70.
43. Bowles KR, Brooks SP, Dunnett SB, Jones L. Gene expression and behaviour in mouse models of HD. Brain Res Bull. 2012;88(2-3): 276.
44. Davies SW, Turmaine M, Cozens BA, DiFiglia M, Sharp AH, Ross CA, Scherzinger E, Wanker EE, Mangiarini L, Bates GP. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell. 1997;90(3): 537.
45. Ransome MI, Renoir T, Hannan AJ. Hippocampal neurogenesis, cognitive deficits and affective disorder in Huntington’s disease. Neural Plast. 2012;2012: 874387.
46. Ramaswamy S, McBride JL, Kordower JH. Animal models of Huntington’s disease. ILAR J. 2007;48(4): 356.
47. Scahill RI, Hobbs NZ, Say MJ, Bechtel N, Henley SM, Hyare H, Langbehn DR, Jones R, Leavitt BR, Roos RA, Durr A, Johnson H, Lehéricy S, Craufurd D, Kennard C, Hicks SL, Stout JC, Reilmann R, Tabrizi SJ; the TRACKHD investigators. Clinical impairment in premanifest and early Huntington’s disease is associated with regionally specific atrophy. Hum Brain Mapp. 2013;34(3): 519.
48. Wolf RC, Sambataro F, Vasic N, Wolf ND, Thomann PA, Saft C, Landwehrmeyer GB, Orth M. Default-mode network changes in preclinical Huntington’s disease. Exp Neurol. 2012;237(1): 191.
49. Novak MJ, Warren JD, Henley SM, Draganski B, Frackowiak RS, Tabrizi SJ. Altered brain mechanisms of emotion processing in pre-manifest Huntington’s disease. Brain. 2012;135(Pt 4): 1165.
50. Delmaire C, Dumas EM, Sharman MA, van den Bogaard SJ, Valabregue R, Jauffret C, Justo D, Reilmann R, Stout JC, Craufurd D, Tabrizi SJ, Roos RA, Durr A, Lehéricy S. The structural correlates of functional deficits in early huntington’s disease. Hum Brain Mapp. 2012; doi: 10.1002/hbm.22055 (Epub ahead of print)
51. Paulsen JS, Langbehn DR, Stout JC, Aylward E, Ross CA, Nance M, Guttman M, Johnson S, MacDonald M, Beglinger LJ, Duff K, Kayson E, Biglan K, Shoulson I, Oakes D, Hayden M. Predict-HD Investigators and Coordinators of the Huntington Study Group. Detection of Huntington’s disease decades before diagnosis: The Predict-HD study. J Neurol Neurosurg Psychiatry. 2008;79(8): 874.
52. Orth M, Schippling S, Schneider SA, Bhatia KP, Talelli P, Tabrizi SJ, Rothwell JC. Abnormal motor cortex plasticity in premanifest and very early manifest Huntington disease. J Neurol Neurosurg Psychiatry. 2010;81(3): 267.
53. Wadman, M. Animal rights: Chimpanzee research on trial. Nature. 2011;474(7351): 268.
54. Krasemann S, Sikorska B, Liberski PP, Glatzel M. Nonhuman primates in prion research. Folia Neuropathol. 2012;50(1): 57.
55. Löw K, Aebischer P. Use of viral vectors to create animal models for Parkinson’s disease. Neurobiol Dis. 2012;48(2): 189.
56. Fernagut PO, Tison F. Animal models of multiple system atrophy. Neuroscience. 2012;211: 77.
57. Webster SJ, Wilson CA, Lee CH, Mohler EG, Terry AV Jr, Buccafusco JJ. The acute effects of dimebolin, a potential Alzheimer’s disease treatment, on working memory in rhesus monkeys. Br J Pharmacol. 2011;164(3): 970.
58. Porter JN, Olsen AS, Gurnsey K, Dugan BP, Jedema HP, Bradberry CW. Chronic cocaine self-administration in rhesus monkeys: Impact on associative learning, cognitive control, and working memory. J Neurosci. 2011;31(13): 4926.
59. Uslaner JM, Eddins D, PuriV, Cannon CE, Sutcliffe J, Chew CS, Pearson M, Vivian JA, Chang RK, Ray WJ, Kuduk SD, Wittmann M. The muscarinic M1 receptor positive allosteric modulator PQCA improves cognitive measures in rat, cynomolgus macaque, and rhesus macaque. Psychopharmacology (Berl). 2013;225(1): 21.
60. Burns LH, Pakzaban P, Deacon TW, Brownell AL, Tatter SB, Jenkins BG, Isacson O. Selective putaminal excitotoxic lesions in non-human primates model the movement disorder of Huntington disease. Neuroscience. 1995;64(4): 1007.
61. Kendall AL, David F, Rayment G, Torres EM, Annett LE, Dunnett SB. The influence of excitotoxic basal ganglia lesions on motor performance in the common marmoset. Brain. 2000;123(Pt 7): 1442.
62. Palfi S, Brouillet E, Jarraya B, Bloch J, Jan C, Shin M, Condé F, Li XJ, Aebischer P, Hantraye P, Déglon N. Expression of mutated huntingtin fragment in the putamen is sufficient to produce abnormal movement in non-human primates. Mol Ther. 2007;15(8): 1444.
63. Yang SH, Cheng PH, Banta H, Piotrowska-Nitsche K, Yang JJ, Cheng EC, Snyder B, Larkin K, Liu J, Orkin J, Fang ZH, Smith Y, Bachevalier J, Zola SM, Li SH, Li XJ, Chan AW. Towards a transgenic model of Huntington’s disease in a non-human primate. Nature. 2008;453(7197): 921.
64. ChanAW, Yang SH. Generation of transgenic monkeys with human inherited genetic disease. Methods. 2009;49(1): 78-84
65. Morton AJ, Lagan MA, Skepper JN, Dunnett SB. Progressive formation of inclusions in the striatum and hippocampus of mice transgenic for the human Huntington’s disease mutation. J Neurocytol. 2000;29(9): 679.
66. Wang CE, Tydlacka S, Orr AL, Yang SH, Graham RK, Hayden MR, Li S, ChanAW, Li XJ. Accumulation of N-terminal mutant huntingtin in mouse and monkey models implicated as a pathogenic mechanism in Huntington’s disease. Hum Mol Genet. 2008;17(17): 2738-51
67. Putkhao K, Kocerha J, Cho IK, Yang J, Parnpai R, ChanAW. Pathogenic Cellular Phenotypes are GermlineTransmissible in a Transgenic Primate Model of Huntington’s Disease. Stem Cells Dev. 2013. (Epub ahead of print)
68. Laowtammathron C, Cheng ECh, Cheng PH, Snyder BR, Yang SH, Johnson Z, Lorthongpanich C, Kuo HC, Parnpai R, Chan AW. Monkey hybrid stem cells develop cellular features of Huntington’s disease. BMC Cell Biol. 2010;11: 12.
69. Chan AW, Cheng PH, Neumann A, Yang JJ. Reprogramming Huntington monkey skin cells into pluripotent stem cells. Cell Reprogram. 2010;12(5): 509-17
70. Sparman ML, Tachibana M, Mitalipov SM. Cloning of nonhuman primates: The road "less traveled by". Int J Dev Biol. 2010;54(11-12): 1671.
71. Clarke IJ. Control of GnRH secretion: One step back. Front Neuroendocrinol. 2011;32(3): 367.
72. Kendrick KM, da Costa AP, Leigh AE, Hinton MR, Peirce JW. Sheep don’t forget a face. Nature. 2001;414(6860): 165. Erratum in: Nature. 2007;447(7142): 346.
73. Tate AJ, Fischer H, Leigh AE, Kendrick KM. Behavioural and neurophysiological evidence for face identity and face emotion processing in animals. Philos Trans R Soc Lond B Biol Sci. 2006;361(1476): 2155.
74. Morton AJ, Avanzo L. Executive decision-making in the domestic sheep. PLoS One. 2011;31: 6(1): e15752.
75. Opdam HI, Federico P, Jackson GD, Buchanan J, Abbott DF, Fabinyi GC, Syngeniotis A, Vosmansky M, Archer JS, Wellard RM, Bellomo R. A sheep model for the study of focal epilepsy with concurrent intracranial EEG and functional MRI. Epilepsia. 2002;43(8): 779.
76. Bjarkam CR, Cancian G, Glud AN, Ettrup KS, Jørgensen RL, Sørensen JC. MRI-guided stereotaxic targeting in pigs based on a stereotaxic localizer box fitted with an isocentric frame and use of SurgiPlan computer-planning software. J Neurosci Methods. 2009;183(2): 119.
77. van der Bom IM, Moser RP, Gao G, Sena-EstevesM, Aronin N, Gounis MJ. Frameless multimodal image guidance of localized convection-enhanced delivery of therapeutics in the brain. J Neurointerv Surg. 2013;5(1): 69.
78. Wells AJ, Vink R, Blumbergs PC, Brophy BP, Helps SC, Knox SJ, Turner RJ. A surgical model of permanent and transient middle cerebral artery stroke in the sheep. PLoS One. 2012;7(7): e42157.
79. Sánchez-Andrade G, James BM, Kendrick KM. Neural encoding of olfactory recognition memory. J Reprod Dev. 2005;51(5): 547.
80. Nowak R, Keller M, Lévy F. Mother-young relationships in sheep: A model for a multidisciplinary approach of the study of attachment in mammals. J Neuroendocrinol. 2011;23(11): 1042.
81. Hunter N, Goldmann W, Marshall E, O’Neill G. Sheep and goats: Natural and experimental TSEs and factors influencing incidence of disease. Arch Virol Suppl. 2000;16: 181.
82. Mallucci G, Collinge J. Update on Creutzfeldt-Jakob disease. Curr Opin Neurol. 2004;17(6): 641.
83. Palmer D, Tammen I, Drögemüller C, Johnson G, Katz M, Lingaas F. Large Animal Models. In The Neuronal Ceroid LIPOFUSCINOSES (Batten Disease) 2011; pp. 284-320. New York, US: Oxford University Press.
84. Karageorgos L, Lancaster MJ, Nimmo JS, Hopwood JJ. Gaucher disease in sheep. J Inherit Metab Dis. 2011; 34(1): 209.
85. Jacobsen JC, Bawden CS, Rudiger SR, McLaughlan CJ, Reid SJ, Waldvogel HJ, MacDonald ME, Gusella JF, Walker SK, Kelly JM, Webb GC, Faull RL, Rees MI, Snell RG. An ovine transgenic Huntington’s disease model. Hum Mol Genet. 2010;19(10): 1873.
86. Chiang C, Jacobsen JC, Ernst C, Hanscom C, Heilbut A, Blumenthal I, Mills RE, Kirby A, Lindgren AM, Rudiger SR, McLaughlan CJ, Bawden CS, Reid SJ, Faull RL, Snell RG, Hall IM, Shen Y, Ohsumi TK, BorowskyML, Daly MJ, Lee C, Morton CC, MacDonald ME, Gusella JF, Talkowski ME. Complex reorganization and predominant non-homologous repair following chromosomal breakage in karyotypically balanced germline rearrangements and transgenic integration. Nat Genet. 2012;44(4): 390.
87. Reid SJ, Handley RR, Patassini S, Rudiger SR, Keynes, P, McLaughhlan, CJ, Waldvogel, HJ, Jacobsen, JC, Macdonald, ME, Gusella, JF, Morton, AJ, Bawden, CS, Faull, RLM, Snell, RG. Clinical Genetics Special Issue: Clinical Genetics Special Issue: Abstracts for the 2011World Congress on Huntington’s Disease, 11-14 September 2011, Melbourne, Australia, September 2011, Volume 80, Issue Supplement s1; Abstract 144.
88. Handley, RR, Reid, SJ, Tsai, P, Faull, RLM, Snell, RG. Clinical Genetics Special Issue: Abstracts for the 2011 World Congress on Huntington’s Disease, 11-14 September 2011, Melbourne, Australia, September 2011, Volume 80, Issue Supplement s1; Abstract 112.
89. Bourke CA, Bunker EC, Reece RI, Whittaker SJ. Cerebellar ataxia in sheep grazing pastures infested with Romulea rosea (onion grass or Guildford grass). AustVet J. 2008;86(9): 354.
90. Vodicka P, SmetanaKJr, Dvoránková B, Emerick T, Xu YZ, Ourednik J, Ourednik V, Motlík J. The miniature pig as an animal model in biomedical research. Ann N Y Acad Sci. 2005;1049: 161.
91. Archibald AL, Bolund L, Churcher C, Fredholm M, Groenen MA, Harlizius B, et al. Pig genome sequence- analysis and publication strategy.BMCGenomics. 2010;11: 438.
92. Jiang Z, Rothschild MF. Swine genome science comes of age. International Journal of Biological Sciences. 2007;3(3): 129.
93. Jorgensen FG, Hobolth A, Hornshoj H, Bendixen C, Fredholm M, Schierup MH. Comparative analysis of protein coding sequences from human, mouse and the domesticated pig. BMC Biology. 2005;3: 2.
94. Wernersson R, Schierup MH, Jorgensen FG, Gorodkin J, Panitz F, Staerfeldt HH, et al. Pigs in sequence space: A 0.66X coverage pig genome survey based on shotgun sequencing. BMC Genomics. 2005;6: 70.
95. Hofmann A, Kessler B, Ewerling S, Weppert M, Vogg B, Ludwig H, Stojkovic M, Boelhauve M, Brem G, Wolf E, Pfeifer A. Efficient transgenesis in farm animals by lentiviral vectors. EMBO Rep. 2003;4(11): 1054.
96. Nagashima H, Fujimura T, TakahagiY, Kurome M, Wako N, Ochiai T, Esaki R, Kano K, Saito S, Okabe M, Murakami H. Development of efficient strategies for the production of genetically modified pigs. Theriogenology. 2003;59(1): 95.
97. Kurome M, Ueda H, Tomii R, Naruse K, Nagashima H. Production of transgenic-clone pigs by the combination of ICSI-mediated gene transfer with somatic cell nuclear transfer. Transgenic Res. 2006;15(2): 229.
98. Yang D, Wang CE, Zhao B, LiW, Ouyang Z, Liu Z, Yang H, Fan P, O’Neill A, GuW, Yi H, Li S, Lai L, Li XJ. Expression of Huntington’s disease protein results in apoptotic neurons in the brains of cloned transgenic pigs. Hum Mol Genet. 2010;19(20): 3983.
99. Tabrizi SJ, Reilmann R, Roos RA, Durr A, Leavitt B, Owen G, Jones R, Johnson H, Craufurd D, Hicks SL, Kennard C, Landwehrmeyer B, Stout JC, Borowsky B, Scahill RI, Frost C, Langbehn DR. TRACK-HD investigators. Potential endpoints for clinical trials in premanifest and early Huntington’s disease in the TRACK-HD study: Analysis of 24 month observational data. Lancet Neurol. 2012;11(1): 42.
100. Tabrizi SJ, Langbehn DR, Leavitt BR, Roos RA, Durr A, Craufurd D, Kennard C, Hicks SL, Fox NC, Scahill RI, Borowsky B, Tobin AJ, Rosas HD, Johnson H, Reilmann R, Landwehrmeyer B, Stout JC. TRACK-HD investigators. Biological and clinical manifestations of Huntington’s dis ease in the longitudinal TRACK-HD study: Cross-sectional analysis of baseline data. Lancet Neurol. 2009;8(9): 791.
101. Gizewski ER, Schanze T, Bolle I, de Greiff A, Forsting M, Laube T. Visualization of the visual cortex in minipigs using fMRI. Res Vet Sci. 2007;82(3): 281.
102. Vial F, Serriere S, Barantin L, Montharu J, Nadal-Desbarats L, Pourcelot L, Seguin F. A newborn piglet study of moderate hypoxic-ischemic brain injury by 1H-MRS and MRI. Magn Reson Imaging. 2004;22(4): 457.
103. Watanabe H, Andersen F, Simonsen CZ, Evans SM, Gjedde A, Cumming P. DaNeX Study Group. MR-based statistical atlas of the Göttingen minipig brain. Neuroimage. 2001;14(5): 1089.
104. Ishizu K, Smith DF, Bender D, Danielsen E, Hansen SB, Wong DF, Cumming P, Gjedde A. Positron emission tomography of radioligand binding in porcine striatum in vivo: Haloperidol inhibition linked to endogenous ligand release. Synapse. 2000;38(1): 87.
105. Rosa-Neto P, Doudet DJ, Cumming P. Gradients of dopamine D1- and D2/3-binding sites in the basal ganglia of pig and monkey measured by PET. Neuroimage. 2004;22(3): 1076.
106. Cumming P, Rosa-Neto P, Watanabe H, Smith D, Bender D, Clarke PB, Gjedde A. 24.Effects of acute nicotine on hemodynamics and binding of (11C) raclopride to dopamine D2,3 receptors in pig brain. Neuroimage. 2003;19(3): 1127.
107. Gonzalo-Orden JM, Díez A, Altónaga JR, Gonzalo JM, Orden MA. Computed tomographic findings in ovine coenurosis. Vet Radiol Ultrasound. 1999;40(5): 441.
108. Van Raamsdonk JM, Gibson WT, Pearson J, Murphy Z, Lu G, Leavitt BR, Hayden MR. Body weight is modulated by levels of full-length huntingtin. Hum Mol Genet. 2006;15(9): 1513.
109. Pouladi MA, Stanek LM, Xie Y, Franciosi S, Southwell AL, Deng Y, Butland S, Zhang W, Cheng SH, Shihabuddin LS, Hayden MR. 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. 2012;21(10): 2219.
110. Comparative Anatomy and Histology: AMouse and Human Atlas; edited by Piper Treuting, Suzanne M. Dintzis, Elsevier, 2011.