A novel transgenic rat model for spinocerebellar ataxia type 17 recapitulates neuropathological changes and supplies in vivo imaging biomarkers

Journal of Neuroscience

Volumn 33, Issue 21, 2013, Pages 9068-9081

  Kelp, Alexandra ^a,c   Koeppen, Arnulf H ^d   Petrasch Parwez, Elisabeth ^e   Calaminus, Carsten ^b   Bauer, Claudia ^a,c   Portal, Esteban ^a,c   Yu Taeger, Libo ^a,c   Pichler, Bernd ^b   Bauer, Peter ^a,c   Riess, Olaf ^a,c   Nguyen, Huu Phuc ^a,c  

^a Institute of Medical Genetics and Applied Genomics   (Germany)

^b Imaging Technology of the Werner Siemens Foundation   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d Department of Neuropathology and Neurology ^*  (United States)

^e RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; COMPLEMENTARY DNA; POLYGLUTAMINE; TATA BINDING PROTEIN;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; CEREBELLUM; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; ELECTRON MICROSCOPY; FEMALE; GENE; GENOTYPING TECHNIQUE; HYPERACTIVITY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MORPHOLOGY; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PHENOTYPE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RAT; SPINOCEREBELLAR DEGENERATION; WEIGHT REDUCTION; WESTERN BLOTTING;

ANIMALS; ANXIETY; AUTOMATIC DATA PROCESSING; BODY WEIGHT; BRAIN; DIFFUSION TENSOR IMAGING; DISEASE MODELS, ANIMAL; FEMALE; GENOTYPE; HUMANS; MALE; MAZE LEARNING; MOTOR ACTIVITY; NEUROLOGIC EXAMINATION; POSITRON-EMISSION TOMOGRAPHY; PSYCHOMOTOR PERFORMANCE; RACLOPRIDE; RATS; RATS, TRANSGENIC; ROTAROD PERFORMANCE TEST; SEVERITY OF ILLNESS INDEX; SPINOCEREBELLAR ATAXIAS; TATA-BOX BINDING PROTEIN; TRINUCLEOTIDE REPEAT EXPANSION; TUBULIN;

EID: 84877948396     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5622-12.2013     Document Type: Article

References (76)

1. André M, Cepeda C, Fisher YE, Huynh M, Bardakjian N, Singh S, Yang XW, Levine MS (2011) Differential electrophysiological changes in striatal output neurons in Huntington's disease. J Neurosci 31:1170-1182.
2. Antonsen BT, Jiang Y, Veraart J, Qu H, Nguyen HP, Sijbers J, Von Hörsten S, Johnson GA, Leergaard TB (2012) Altered diffusion tensor imaging measurements in aged transgenic Huntington disease rats. Brain Struct Funct. Advance online publication. Retrieved July 27, 2012.
3. Beaumont V (2012) cGMP-hydrolyzing PDEs are therapeutic targets for Huntington's disease. PLoS One 7:e44498.
4. Bichelmeier U, Schmidt T, Hubener J, Boy J, Ruttiger L, Häbig K, Poths S, Bonin M, Knipper M, Schmidt WJ, Wilbertz J, Wolburg H, Laccone F, Riess O (2007) Nuclear localization of ataxin-3 is required for the manifestation of symptoms in SCA3: in vivo evidence. J Neurosci 27: 7418-7428.
5. Blockx I, Verhoye M, Van Audekerke J, Bergwerf I, Kane JX, Delgado Y Palacios R, Veraart J, Jeurissen B, Raber K, Von Hörsten S, Ponsaerts P, Sijbers J, Leergaard TB, Van der Linden A (2012) Identification and characterization of Huntington related pathology: an in vivo DKI imaging study. Neuroimage 63:653-662.
6. Bohanna I, Georgiou-Karistianis N, Hannan AJ, Egan GF (2008) Magnetic resonance imaging as an approach towards identifying neuropathological biomarkers for Huntington's disease. Brain Res Rev 58:209-225.
7. Borchelt DR, Davis J, Fischer M, Lee MK, Slunt HH, Ratovitsky T, Regard J, Copeland NG, Jenkins NA, Sisodia SS, Price DL (1996) A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet Anal 13:159-163.
8. Boska MD, Hasan KM, Kibuule D, Banerjee R, McIntyre E, Nelson JA, Hahn T, Gendelman HE, Mosley RL (2007) Quantitative diffusion tensor im-aging detects dopaminergic neuronal degeneration in a murine model of Parkinson's disease. Neurobiol Dis 26:590-596.
9. Boy J, Schmidt T, Wolburg H, Mack A, Nuber S, Böttcher M, Schmitt I, Holzmann C, Zimmermann F, Servadio A, Riess O (2009) Reversibility of symptoms in a conditional mouse model of spinocerebellar ataxia type 3. Hum Mol Genet 18:4282-4295.
10. Brockmann K, Reimold M, Globas C, Hauser TK, Walter U, Machulla HJ, Rolfs A, Schöls L (2012) PET and MRI reveal early evidence of neurode-generation in spinocerebellar ataxia type 17. J Nuclear Med 53:1074-1080.
11. Burley SK, Roeder RG (1996) Biochemistry and structural biology of tran-scription factor IID (TFIID). Annu Rev Biochem 65:769-799.
12. Casteels C, Vandeputte C, Rangarajan JR, Dresselaers T, Riess O, Bormans G, Maes F, Himmelreich U, Nguyen H, Van Laere K (2011) Metabolic and type 1 cannabinoid receptor imaging of a transgenic rat model in the early phase of Huntington disease. Exp Neurol 229:440-449.
13. Chang YC, Lin CY, Hsu CM, Lin HC, Chen YH, Lee-Chen GJ, Su MT, Ro LS, Chen CM, Hsieh-Li HM (2011) Neuroprotective effects of granulocyte-colony stimulating factor in a novel transgenic mouse model of SCA17. J Neurochem 118:288-303.
14. Della Nave R, Ginestroni A, Tessa C, Giannelli M, Piacentini S, Filippi M, Mascalchi M (2010) Regional distribution and clinical correlates of white matter structural damage in Huntington disease: a tract-based spa-tial statistics study. AJNR Am journal Neuroradiol 31:1675-1681.
15. Douaud G, Behrens TE, Poupon C, Cointepas Y, Jbabdi S, Gaura V, Golestani N, Krystkowiak P, Verny C, Damier P, Bachoud-Lévi AC, Hantraye P, Remy P (2009) In vivo evidence for the selective subcortical degenera-tioninHuntington'sdisease. Neuroimage 46:958-966.
16. Farde L, Ehrin E, Eriksson L, Greitz T, Hall H, Hedström CG, Litton JE, Sedvall G (1985) Substituted benzamides as ligands for visualization of dopamine receptor binding in the human brain by positron emission tomography. Proc Natl Acad Sci U S A 82:3863-3867.
17. File SE (1990) New strategies in the search for anxiolytics. Drug Des Deliv 5:195-201.
18. Franklin K, Paxinos G (2001) Stereotactic brain atlas, Ed 2. San Diego: Ac-ademic.
19. Friedman MJ, Shah AG, Fang ZH, Ward EG, Warren ST, Li S, Li X-J (2007) Polyglutamine domain modulates the TBP-TFIIB interaction: implica-tions for its normal function and neurodegeneration. Nat Neurosci 10: 1519-1528.
20. Fujigasaki H, Martin JJ, De Deyn PP, Camuzat A, Deffond D, Stevanin G, Dermaut B, Van Broeckhoven C, Durr A, Brice A (2001) CAG repeat expansionintheTATAbox-bindingproteingenecausesautosomaldom-inant cerebellar ataxia. Brain 124:1939-1947.
21. Garden GA, Libby RT, Fu YH, Kinoshita Y, Huang J, Possin DE, Smith AC, Martinez RA, Fine GC, Grote SK, Ware CB, Einum DD, Morrison RS, Ptacek LJ, Sopher BL, La Spada AR (2002) Polyglutamine-expanded ataxin-7 promotes non-cell-autonomous Purkinje cell degeneration and displays proteolytic cleavage in ataxic transgenic mice. J Neurosci 22: 4897-4905.
22. Grundmann K, Glöckle N, Martella G, Sciamanna G, Hauser TK, Yu L, Cas-taneda S, Pichler B, Fehrenbacher B, Schaller M, Nuscher B, Haass C, Hettich J, Yue Z, Nguyen HP, Pisani A, Riess O, Ott T (2012) Generation of a novel rodent model for DYT1 dystonia. Neurobiol Dis 47:61-74.
23. Grunewald T, Beal MF (1999) Bioenergetics in Huntington's disease. Ann NYAcadSci893:203-213.
24. Guyenet SJ, Furrer SA, Damian VM, Baughan TD, La Spada AR, Garden GA (2010) A simple composite phenotype scoring system for evaluating mouse models of cerebellar ataxia. J Vis Exp 39:2-4.
25. Herrmann KH, Schmidt S, Kretz A, Haenold R, Krumbein I, Metzler M, Gaser C, Witte OW, Reichenbach JR (2012) Possibilities and limitations for high resolution small animal MRI on a clinical whole-body 3T scan-ner. MAGMA 25:233-244.
26. Huang HY, Lee HW, Chen SD, Shaw FZ (2012) Lamotrigine ameliorates seizures and psychiatric comorbidity in a rat model of spontaneous ab-sence epilepsy. Epilepsia 53:2005-2014.
27. Huang S, Ling JJ, Yang S, Li XJ, Li S (2011) Neuronal expression of TATA box-binding protein containing expanded polyglutamine in knock-in mice reduces chaperone protein response by impairing the function of nuclear factor-Y transcription factor. Brain 134:1943-1958.
28. Klöppel S, Draganski B, Golding CV, Chu C, Nagy Z, Cook PA, Hicks SL, Kennard C, Alexander DC, Parker GJ, Tabrizi SJ, Frackowiak RS (2008) Whitematterconnectionsreflectchangesinvoluntary-guidedsaccadesin pre-symptomatic Huntington's disease. Brain 131:196-204.
29. Koeppen AH, Morral JA, McComb RD, Feustel PJ (2011) The neuropathol-ogy of late-onset Friedreich's ataxia. Cerebellum 10:96-103.
30. Koide R, Kobayashi S, Shimohata T, Ikeuchi T, Maruyama M, Saito M, Yamada M, Takahashi H, Tsuji S (1999) A neurological disease caused by an expanded CAG trinucleotide repeat in the TATA-binding protein gene: a new polyglutamine disease? Hum Mol Genet 8:2047-2053.
31. Korenova M, Zilka N, Stozicka Z, Bugos O, Vanicky I, Novak M (2009) NeuroScale, the battery of behavioral tests with novel scoring system for phenotyping of transgenic rat model of tauopathy. J Neurosci Methods 177:108-114.
32. Kujpers M (1999) Report of the NIH rat model priority. Bethesda, MD: NIH.
33. Laccone F, Maiwald R, Bingemann S (1999) A fast polymerase chain reaction-mediated strategy for introducing repeat expansions into CAG-repeat containing genes. Hum Mutat 13:497-502.
34. Lin CH, Tallaksen-Greene S, Chien WM, Cearley JA, Jackson WS, Crouse AB, Ren S, Li X J, Albin RL, Detloff PJ (2001) Neurologicalabnormalitiesina knock-inmousemodelofHuntington'sdisease. HumMolGenet 10:137-144.
35. Lope-Piedrafita S, Garcia-Martin ML, Galons JP, Gillies RJ, Trouard TP (2008) Longitudinal diffusion tensor imaging in a rat brain glioma model. NMR Biomed 21:799-808.
36. Maltecca F, Filla A, Castaldo I, Coppola G, Fragassi NA, Carella M, Bruni A, Cocozza S, Casari G, Servadio A, DeMichele G (2003) Intergenerational instability and marked anticipation in SCA-17. Neurology 61:1441-1443.
37. Mandelli ML, Savoiardo M, Minati L, Mariotti C, Aquino D, Erbetta A, Geni-trini S, Di Donato S, Bruzzone MG, Grisoli M (2010) Decreased diffu-sivity in the caudate nucleus of presymptomatic Huntington disease gene carriers: which explanation? Am J Neuroradiol 31:706-710.
38. Mariotti C, Alpini D, Fancellu R, Soliveri P, Grisoli M, Ravaglia S, Lovati C, Fetoni V, Giaccone G, Castucci A, Taroni F, Gellera C, DiDonato S (2007) Spino-cerebellar ataxia type 17 (SCA17): oculomotor phenotype and clinical char-acterizationof15Italianpatients. JNeurol254:1538-1546.
39. Mascalchi M, Lolli F, Nave R Della, Tessa C, Petralli R, Gavazzi C, Politi LS, Macucci M, Filippi M, Piacentini S (2004) Huntington disease: volu-metric, diffusion-weighted, and magnetization transfer MR imaging of brain. Radiology 232:867-873.
40. Menalled LB, Sison JD, Wu Y, Olivieri M, Li X, Li H, Zeitlin S (2002) Early motordysfunctionandstriosomaldistributionofhuntingtinmicroaggre-gates in Huntington's disease knock-in mice. J Neurosci 22:8266-8276.
41. Miller BR, Walker AG, Fowler SC, von Hörsten S, Riess O, Johnson MA, Rebec GV (2010) Dysregulation of coordinated neuronal firing patterns in striatum of freely behaving transgenic rats that model Huntington's disease. Neurobiol Dis 37:106-113.
42. Nakamura K, Jeong SY, Uchihara T, Anno M, Nagashima K, Nagashima T, Ikeda S, Tsuji S, KanazawaI (2001) SCA17, anovelautosomaldominant cerebellar ataxia caused by an expanded polyglutamine in TATA-binding protein. Hum Mol Genet 10:1441-1448.
43. Ortiz AN, Osterhaus GL, Lauderdale K, Mahoney L, Fowler SC, von Hörsten S, Riess O, Johnson MA (2012) Motor function and dopamine release measurements in transgenic Huntington's disease model rats. Brain Res 1450:148-156.
44. Pellow S, Chopin P, File SE, Briley M (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J of neuroscience methods 14:149-167.
45. Petrasch-Parwez E, Nguyen HP, Löbbecke-Schumacher M, Habbes HW, Wieczorek S, Riess O, Andres KH, Dermietzel R, Von Hörsten S (2007) Cellular and subcellular localization of Huntingtin [corrected] aggregates in the brain of a rat transgenic for Huntington disease. J Comp Neurol 501:716-730.
46. Quarrell OWJ, Brewer HM, Squitieri F, Barker RA, Nance MA LB (2009) Juvenile Huntington's disease and other trinucleotide repeat disorders. Oxford, UK: Oxford UP.
47. Rath A, Klein A, Papazoglou A, Pruszak J, Garciaa J, Krause M, Maciaczyk J, Dunnett SB, Nikkhah G (2012) Survival and functional restoration of human fetal ventral mesencephalon following transplantation in a rat model of Parkinson's disease. Cell Transplant. Advance online publica-tion.
48. Reading SA, Yassa MA, Bakker A, Dziorny AC, Gourley LM, Yallapragada V, Rosenblatt A, Margolis RL, Aylward EH, Brandt J, Mori S, van Zijl P, Bassett SS, Ross CA (2005) Regional white matter change in pre-symptomaticHuntington'sdisease:adiffusiontensorimagingstudy. Psy-chiatry Res 140:55-62.
49. Rehbinder C, Baneux P, Forbes D, van Herck H, Nicklas W, Rugaya Z, Win-kler G (1996) FELASA recommendations for the health monitoring of mouse, rat, hamster, gerbil, guinea pig and rabbit experimental units. Report of the Federation of European Laboratory Animal Science Asso-ciations (FELASA) Working Group on Animal Health accepted by the. Lab Anim 30:193-208.
50. Ribeiro D, Goya RL, Ravindran G, Vuono R, Parish CL, Foldi C, Piroth T, Yang S, Parmar M, Nikkhah G, Hjerling-Leffler J, Lindvall O, Barker RA, Arenas E (2012) Efficient expansion and dopaminergic differentiation of human fetal ventral midbrain neural stem cells by midbrain morpho-gens. Neurobiol Dis 49C:118-127.
51. Riley BE, Orr HT (2006) Polyglutamine neurodegenerative diseases and regulation of transcription: assembling the puzzle. Genes Dev 20:2183-2192.
52. Rodriguiz RM, Wetsel WC (2006) Assessments of cognitive deficits in mu-tant mice. In: Animal models of cognitive impairment, Chap 12.
53. Rolfs A, Koeppen AH, Bauer I, Bauer P, Buhlmann S, Topka H, Schöls L, Riess O (2003) Clinical features and neuropathology of autosomal dominant spinocerebellar ataxia (SCA17). Ann Neurol 54:367-375.
54. Rosas HD, Tuch DS, Hevelone ND, Zaleta AK, Vangel M, Hersch SM, Salat DH (2006) DiffusiontensorimaginginpresymptomaticandearlyHun-tington's disease: selective white matter pathology and its relationship to clinical measures. Movement Dis 21:1317-1325.
55. Rosas HD, Lee SY, Bender AC, Zaleta AK, Vangel M, Yu P, Fischl B, Pappu V, Onorato C, Cha JH, Salat DH, Hersch SM (2010) Altered white matter microstructure in the corpus callosum in Huntington's disease: implica-tions for cortical "disconnection." Neuroimage 49:2995-3004.
56. 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 (1999a) Intranuclear inclusions and neuritic aggre-gates in transgenic mice expressing a mutant N-terminal fragment of huntingtin. Human molecular genetics 8:397-407.
57. Schilling G, Wood JD, Duan K, Slunt HH, Gonzales V, Yamada M, Cooper JK, Margolis RL, Jenkins NA, Copeland NG, Takahashi H, Tsuji S, Price DL, Borchelt DR, Ross CA (1999b) Nuclear accumulation of truncated atrophin-1 fragments in a transgenic mouse model of DRPLA. Neuron 24:275-286.
58. Seppi K, Schocke MF, Mair KJ, Esterhammer R, Weirich-Schwaiger H, Uter-mann B, Egger K, Brenneis C, Granata R, Boesch S, Poewe W, Wenning GK (2006) Diffusion-weighted imaging in Huntington's disease. Move-ment Dis 21:1043-1047.
59. Siesling S, Vegter-van der Vlis M, Roos RA (1997) Juvenile Huntington dis-ease in the Netherlands. Pediatric Neurol 17:37-43.
60. Slow EJ, van Raamsdonk J, Rogers D, Coleman SH, Graham RK, Deng Y, Oh R, Bissada N, Hossain SM, Yang Y, Li X, Simpson EM, Gutekunst C, Leavitt BR, Hayden MR (2003) Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum Mol Genet 12:1555-1567.
61. Song SK, Kim JH, Lin SJ, Brendza RP, Holtzman DM (2004) Diffusion ten-sor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition. Neurobiol Dis 15:640-647.
62. Squitieri F, Frati L, Ciarmiello A, Lastoria S, Quarrell O (2006) Juvenile Huntington's disease: does a dosage-effect pathogenic mechanism differ from the classical adult disease? Mechanisms of ageing and development 127:208-212.
63. Sritharan A, Egan GF, Johnston L, Horne M, Bradshaw JL, Bohanna I, Asadi H, Cunnington R, Churchyard AJ, Chua P, Farrow M, Georgiou-Karistianis N (2010) A longitudinal diffusion tensor imaging study in symptomatic Huntington's disease. J Neurol Neurosurg Psychiatry 81: 257-262.
64. Starr PA, Kang GA, Heath S, Shimamoto S, Turner RS (2008) Pallidal neu-ronal discharge in Huntington's disease: support for selective loss of stri-atal cells originating the indirect pathway. Exp Neurol 211:227-233.
65. Tecott LH, Nestler EJ (2004) Neurobehavioral assessment in the informa-tion age. Nat Neurosci 7:462-466.
66. Threlfell S, Sammut S, Menniti FS, Schmidt CJ, West AR (2009) Inhibition of phosphodiesterase 10A increases the responsiveness of striatal projec-tion neurons to cortical stimulation. J Pharmacol Exp Ther 328:785-795.
67. Tomiuk J, Bachmann L, Bauer C, Rolfs A, Schöls L, Roos C, Zischler H, Schuler MM, Bruntner S, Riess O, Bauer P (2007) Repeat expansion in spinocerebellar ataxia type 17 alleles of the TATA-box binding protein gene: an evolutionary approach. Eur J Hum Genet 15:81-87.
68. Urbach YK, Bode FJ, Nguyen HP, Riess O, Hörsten S Von (2010) Rat Genomics (Anegon I, ed). Totowa, NJ: Humana.
69. Van Camp N, Blockx I, Verhoye M, Casteels C, Coun F, Leemans A, Sijbers J, Baekelandt V, Van Laere K, Van der Linden A (2009) Diffusion tensor imaging in a rat model of Parkinson's disease after lesioning of the nigro-striatal tract. NMR Biomed 22:697-706.
70. Van Camp N, Blockx I, Camón L, de Vera N, Verhoye M, Veraart J, Van Hecke W, Martínez E, Soria G, Sijbers J, Planas AM, Van der Linden A (2012) A complementary diffusion tensor imaging (DTI)-histological study in a model of Huntington's disease. Neurobiol Aging 33:945-959.
71. van der Burg JMM, Bacos K, Wood NI, Lindqvist A, Wierup N, Woodman B, Wamsteeker JI, Smith R, Deierborg T, Kuhar MJ, Bates GP, Mulder H, Erlanson-Albertsson C, Morton AJ, Brundin P, Petersén A, Björkqvist M (2008) Increased metabolism in the R6/2 mouse model of Huntington's disease. Neurobiol Dis 29:41-51.
72. Weydt P, Pineda VV, Torrence AE, Libby RT, Satterfield TF, Lazarowski ER, Gilbert ML, Morton GJ, Bammler TK, Strand AD, Cui L, Beyer RP, Easley CN, Smith AC, Krainc D, Luquet S, Sweet IR, Schwartz MW, La Spada AR (2006) Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurode-generation. Cell Metab 4:349-362.
73. Wheeler VC, White JK, Gutekunst C, Vrbanac V, Weaver M, Li X, Li S, Yi H, Vonsattel J, Gusella JF, Hersch S, Auerbach W, Joyner AL, Macdonald ME (2000) Long glutamine tracts cause nuclear localization of a novel form of huntingtin in medium spiny striatal neurons in Hdh Q92 and Hdh Q111 knock-in mice. Hum Mol Genet 9:503-514.
74. Yu-Taeger L, Petrasch-Parwez E, Osmand A, Redensek A, Metzger S, Clem-ens LE, Park L, Howland D, Calaminus C, Gu X, Pichler B, Yang XW, Riess O NH (2012) A novel BACHD transgenic rat exhibits characteris-tic neuropathological features of Huntington's disease. J Neurosci 32: 15426-15438.
75. Zoghbi HY, Orr HT (2000) Glutamine repeats and neurodegeneration. Annu Rev Neurosci 23:217-247.
76. Zuhlke C, Hellenbroich Y, Dalski A, Kononowa N, Hagenah J, Vieregge P, Riess O, Klein C, Schwinger E (2001) Differenttypesofrepeatexpansion in the TATA-binding protein gene are associated with a new form of inherited ataxia. Eur J Hum Genet 9:160-164.