Further molecular characterisation of the OVT73 transgenic sheep model of huntington’s disease identifies cortical aggregates

Journal of Huntington's Disease

Volumn 2, Issue 3, 2013, Pages 279-295

  Reid, Suzanne J ^a   Patassini, Stefano ^a   Handley, Renée R ^a   Rudiger, Skye R ^b   McLaughlan, Clive J ^b   Osmand, Alex ^d   Jacobsen, Jessie C ^c   Jennifer Morton, A ^e   Weiss, Andreas ^f   Waldvogel, Henry J ^a   MacDonald, Marcy E ^c   Gusella, James F ^c   Simon Bawden, C ^b   Faull, Richard L M ^a   Snell, Russell G ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b South Australian and Research Development Institute   (Australia)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF TENNESSEE   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f IRBM   (Italy)

Author keywords

Huntington disease; Neurosciences; Ovis aries; Sheep; Transgenic animal

Indexed keywords

HTT PROTEIN, HUMAN; NERVE PROTEIN;

ANIMAL; ARTICLE; BRAIN CORTEX; CELL NUCLEUS INCLUSION BODY; DISEASE MODEL; DOMESTIC SHEEP; GENETICS; HUMAN; HUNTINGTON CHOREA; NEUROSCIENCE; PATHOLOGY; SHEEP; TRANSGENIC ANIMAL;

HUNTINGTON DISEASE; NEUROSCIENCES; OVIS ARIES; SHEEP; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; HUMANS; HUNTINGTON DISEASE; INTRANUCLEAR INCLUSION BODIES; NERVE TISSUE PROTEINS; SHEEP, DOMESTIC;

EID: 84902318722     PISSN: 18796397     EISSN: 18796400     Source Type: Journal    
DOI: 10.3233/JHD-130067     Document Type: Article

References (46)

1. HDCRG. 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. 1993;72:971-83.
2. 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. Hum Mol Genet. 2003;12:1555-67.
3. Yu-Taeger L, Petrasch-Parwez E, Osmand AP, Redensek A, Metzger S, Clemens LE, Park L, Howland D, Calaminus C, Gu X, Pichler B, YangXW, Riess O, NguyenHP. AnovelBACHD transgenic rat exhibits characteristic neuropathological features of Huntington disease. J Neurosci. 2012;32:15426-38.
4. Wheeler VC, White JK, Gutekunst CA, Vrbanac V, Weaver M, Li XJ, Li SH, Yi H, Vonsattel JP, Gusella JF, Hersch S, Auerbach W, Joyner AL, MacDonald ME. 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. 2000;9:503-13.
5. Wheeler VC, AuerbachW, White JK, Srinidhi J, Auerbach A, Ryan A, DuyaoMP, VrbanacV, Weaver M, Gusella JF, Joyner AL, MacDonald ME. Length-dependent gametic CAG repeat instability in the Huntington’s disease knock-in mouse. Hum Mol Genet. 1999;8:115-22.
6. 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;19:1873-82.
7. 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, Borowsky ML, 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;44:390-7, S391.
8. Waldvogel HJ, Curtis MA, Baer K, Rees MI, Faull RL. Immunohistochemical staining of post-mortem adult human brain sections. Nat Protoc. 2006;1:2719-32.
9. Weiss A, Abramowski D, Bibel M, Bodner R, Chopra V, DiFiglia M, Fox J, Kegel K, Klein C, Grueninger S, Hersch S, Housman D, Regulier E, Rosas HD, Stefani M, Zeitlin S, Bilbe G, Paganetti P. Single-step detection of mutant huntingtin in animal and human tissues: A bioassay for Huntington’s disease. Anal Biochem. 2009;395:8-15.
10. Benn CL, Fox H, Bates GP. Optimisation of region-specific reference gene selection and relative gene expression analysis methods for pre-clinical trials of Huntington’s disease. Mol Neurodegener. 2008;3:17.
11. Fukudome Y, Ohno-Shosaku T, Matsui M, Omori Y, Fukaya M, Tsubokawa H, Taketo MM, Watanabe M, Manabe T, Kano M. Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mediated indirect suppression through endocannabinoid signalling. Eur J Neurosci. 2004;19:2682-92.
12. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, Meyer M. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci U S A. 1997;94:1488-93.
13. Waldvogel HJ, Kubota Y, Fritschy J, Mohler H, Faull RL. Regional and cellular localisation of GABA(A) receptor subunits in the human basal ganglia: An autoradiographic and immunohistochemical study. J Comp Neurol. 1999;415:313-40.
14. Narushima M, Uchigashima M, Hashimoto K, Watanabe M, Kano M. Depolarization-induced suppression of inhibition mediated by endocannabinoids at synapses from fast-spiking interneurons to medium spiny neurons in the striatum. Eur J Neurosci. 2006;24:2246-52.
15. Osmand AP, Berthelier V, Wetzel R. Imaging polyglutamine deposits in brain tissue. Methods Enzymol. 2006;412: 106-22.
16. Llewellyn-Smith IJ, Minson JB. Complete penetration of antibodies into vibratome sections after glutaraldehyde fixation and ethanol treatment: Light and electron microscopy for neuropeptides. J Histochem Cytochem. 1992;40:1741-49.
17. Gundersen HJ, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987;147: 229-63.
18. Landles C, Sathasivam K, Weiss A, Woodman B, Moffitt H, Finkbeiner S, Sun B, Gafni J, Ellerby LM, TrottierY, Richards WG, Osmand A, Paganetti P, Bates GP. Proteolysis of mutant huntingtin produces an exon 1 fragment that accumulates as an aggregated protein in neuronal nuclei in Huntington disease. J Biol Chem. 2010;285:8808-23.
19. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science. 1997;277:1990-93.
20. Pfister EL, Kennington L, Straubhaar J, Wagh S, Liu W, DiFiglia M, Landwehrmeyer B, Vonsattel JP, Zamore PD, Aronin N. Five siRNAs targeting three SNPs may provide therapy for three-quarters of Huntington’s disease patients. Curr Biol. 2009;19:774-8.
21. Deng YP, Albin RL, Penney JB, Young AB, Anderson KD, Reiner A. Differential loss of striatal projection systems in Huntington’s disease: A quantitative immunohistochemical study. J Chem Neuroanat. 2004;27:143-64.
22. Faull RL, Waldvogel HJ, Nicholson LF, Synek BJ. The distribution of GABAA-benzodiazepine receptors in the basal ganglia in Huntington’s disease and in the quinolinic acidlesioned rat. Prog Brain Res. 1993;99:105-23.
23. Reiner A, Albin RL, Anderson KD, D’Amato CJ, Penney JB, Young AB. Differential loss of striatal projection neurons in Huntington disease. Proc Natl Acad SciUSA. 1988;85:5733-7.
24. Glass M, Dragunow M, Faull RL. The pattern of neurodegeneration in Huntington’s disease: A comparative study of cannabinoid, dopamine, adenosine and GABA(A) receptor alterations in the human basal ganglia in Huntington’s disease. Neuroscience. 2000;97:505-19.
25. Allen KL, Waldvogel HJ, Glass M, Faull RL. Cannabinoid (CB(1)), GABA(A) and GABA(B) receptor subunit changes in the globus pallidus in Huntington’s disease. J Chem Neuroanat. 2009;37:266-81.
26. Guo Z, Rudow G, Pletnikova O, Codispoti KE, Orr BA, Crain BJ, Duan W, Margolis RL, Rosenblatt A, Ross CA, Troncoso JC. Striatal neuronal loss correlates with clinical motor impairment in Huntington’s disease. Mov Disord. 2012;27:1379-86.
27. 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;21:2219-32.
28. Hickey MA, Kosmalska A, Enayati J, Cohen R, Zeitlin S, Levine MS, Chesselet MF. Extensive early motor and nonmotor behavioral deficits are followed by striatal neuronal loss in knock-in Huntington’s disease mice. Neuroscience. 2008;157:280-95.
29. Augood SJ, Faull RL, Emson PC. DopamineD1andD2receptor gene expression in the striatum in Huntington’s disease. Ann Neurol. 1997;42:215-21.
30. Augood SJ, Faull RL, Love DR, Emson PC. Reduction in enkephalin and substance P messenger RNA in the striatum of early grade Huntington’s disease: A detailed cellular in situ hybridization study. Neuroscience. 1996;72:1023-36.
31. Desplats PA, Kass KE, Gilmartin T, Stanwood GD, Woodward EL, Head SR, Sutcliffe JG, Thomas EA. Selective deficits in the expression of striatal-enrichedmRNAs in Huntington’s disease. J Neurochem. 2006;96:743-57.
32. Richfield EK, Maguire-Zeiss KA, Cox C, Gilmore J, Voorn P. Reduced expression of preproenkephalin in striatal neurons from Huntington’s disease patients. Ann Neurol. 1995;37:335-43.
33. Hodges A, Strand AD, Aragaki AK, Kuhn A, Sengstag T, Hughes G, Elliston LA, Hartog C, Goldstein DR, Thu D, Hollingsworth ZR, Collin F, Synek B, Holmans PA, Young AB, Wexler NS, Delorenzi M, Kooperberg C, Augood SJ, Faull RL, Olson JM, Jones L, Luthi-Carter R. Regional and cellular gene expression changes in human Huntington’s disease brain. Hum Mol Genet. 2006;15:965-77.
34. Mazarei G, Neal SJ, Becanovic K, Luthi-Carter R, Simpson EM, Leavitt BR. Expression analysis of novel striatalenriched genes in Huntington disease. Hum Mol Genet. 2010;19:609-22.
35. Hodgson JG, Agopyan N, Gutekunst CA, Leavitt BR, LePiane F, Singaraja R, Smith DJ, Bissada N, McCutcheon K, Nasir J, Jamot L, Li XJ, Stevens ME, Rosemond E, Roder JC, Phillips AG, Rubin EM, Hersch SM, Hayden MR. A YAC mouse model for Huntington’s disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron. 1999;23:181-92.
36. Chan EY, Luthi-Carter R, Strand A, Solano SM, Hanson SA, DeJohn MM, Kooperberg C, Chase KO, DiFiglia M, Young AB, Leavitt BR, Cha JH, Aronin N, Hayden MR, Olson JM. Increased huntingtin protein length reduces the number of polyglutamine-induced gene expression changes in mouse models of Huntington’s disease. Hum Mol Genet. 2002;11:1939-51.
37. Vonsattel JP. Huntington disease models and human neuropathology: Similarities and differences. Acta Neuropathol. 2008;115:55-69.
38. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP, Jr. Neuropathological classification of Huntington’s disease. J Neuropathol Exp Neurol. 1985;44: 559-77.
39. Gomez-Tortosa E, MacDonald ME, Friend JC, Taylor SA, Weiler LJ, Cupples LA, Srinidhi J, Gusella JF, Bird ED, Vonsattel JP, Myers RH. Quantitative neuropathological changes in presymptomatic Huntington’s disease. Ann Neurol. 2001;49:29-34.
40. Gutekunst CA, Li SH, Yi H, Mulroy JS, Kuemmerle S, Jones R, Rye D, Ferrante RJ, Hersch SM, Li XJ. Nuclear and neuropil aggregates in Huntington’s disease: Relationship to neuropathology. J Neurosci. 1999;19:2522-34.
41. Bolam JP, Hanley JJ, Booth PA, Bevan MD. Synaptic organisation of the basal ganglia. J Anat. 2000;196(Pt 4):527-42.
42. 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;90:537-48.
43. Gray M, Shirasaki DI, Cepeda C, Andre 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;28:6182-95.
44. van Roon-MomWM, Hogg VM, Tippett LJ, Faull RL. Aggregate distribution in frontal and motor cortex in Huntington’s disease brain. Neuroreport. 2006;17:667-70.
45. van der Bom IMJ, Moser RP, Gao G, Mondo E, O’Connell D, Gounis MJ, McGowan S, Chaurette J, Bishop N, Sena-Esteves MS, Mueller C, Aronin N. Finding the striatum in sheep: Use of a multi-modal guided approach for convection enhanced delivery. J Huntingtons Dis. 2013;2:41-5.
46. Baxa M, Hruska-Plochan M, Juhas S, Vodicka P, Pavlok A, Juhasova J, Miyanohara A, Nejime T, Klima J, Macakova M, Marsala S, Weiss A, Kubickova S, Musilova P, Vrtel R, Sontag EM, Thompson LM, Schier J, Hansikova H, Howland DS, Cattaneo E, DiFiglia M, Marsala M, Motlik J. A transgenic minipig model of Huntington’s disease. J Huntingtons Dis. 2013;2:47-68.