Genotype specific age related changes in a transgenic rat model of Huntington's disease

NeuroImage

Volumn 58, Issue 4, 2011, Pages 1006-1016

  Blockx, Ines ^a   Van Camp, Nadja ^a,b   Verhoye, Marleen ^a   Boisgard, Raphael ^b,c   Dubois, Albertine ^b,c   Jego, Benoit ^b,c   Jonckers, Elisabeth ^a   Raber, Kerstin ^d   Siquier, Karine ^b,c   Kuhnast, Bertrand ^b   Dollé, Frédéric ^b   Nguyen, Huu Phuc ^e   Von Hörsten, Stephan ^d   Tavitian, Bertrand ^b,c   Van der Linden, Annemie ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b DIF   (France)

^c INSERM   (France)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Diffusion Tensor Imaging; Huntington's Disease; Neuroimaging; Positron Emission Tomography; Transgenic rat model

Indexed keywords

FALLYPRIDE F 18; FLUORODEOXYGLUCOSE F 18; TRACER; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTORADIOGRAPHY; BRAIN REGION; BRAIN SIZE; BRAIN VENTRICLE; BRAIN VENTRICLE VOLUME; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; DIFFUSION TENSOR IMAGING; DISEASE MODEL; GENOTYPE; HUNTINGTON CHOREA; IMAGE RECONSTRUCTION; LEFT CAUDATE PUTAMEN; LONGITUDINAL STUDY; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RAT; RIGHT CAUDATE PUTAMEN; STRIATAL VOLUME; THREE DIMENSIONAL IMAGING; TRANSGENIC RAT; WHITE MATTER;

AGING; ANIMALS; AUTORADIOGRAPHY; BENZAMIDES; BIOLOGICAL MARKERS; BRAIN; CEREBRAL VENTRICLES; CORPUS STRIATUM; DIFFUSION TENSOR IMAGING; FLUORODEOXYGLUCOSE F18; GENOTYPE; HUNTINGTON DISEASE; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; PHENOTYPE; POSITRON-EMISSION TOMOGRAPHY; PYRROLIDINES; RADIOPHARMACEUTICALS; RATS; RATS, TRANSGENIC;

EID: 80052638721     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.07.007     Document Type: Article

References (70)

1. Alexander A.L., Lee J.E., Lazar M., Field A.S. Diffusion tensor imaging of the brain. Neurotherapeutics 2007, 4:316-329.
2. Andrews T.C., Weeks R.A., Turjanski N., Gunn R.N., Watkins L.H., Sahakian B., Hodges J.R., Rosser A.E., Wood N.W., Brooks D.J. Huntington's disease progression. PET and clinical observations. Brain 1999, 122(Pt 12):2353-2363.
3. Aylward E.H. Change in MRI striatal volumes as a biomarker in preclinical Huntington's disease. Brain Res. Bull. 2007, 72:152-158.
4. Aylward E.H., Li Q., Stine O.C., Ranen N., Sherr M., Barta P.E., Bylsma F.W., Pearlson G.D., Ross C.A. Longitudinal change in basal ganglia volume in patients with Huntington's disease. Neurology 1997, 48:394-399.
5. Bartzokis G., Lu P.H., Tishler T.A., Fong S.M., Oluwadara B., Finn J.P., Huang D., Bordelon Y., Mintz J., Perlman S. Myelin breakdown and iron changes in Huntington's disease: pathogenesis and treatment implications. Neurochem. Res. 2007, 32:1655-1664.
6. Basser P.J., Jones D.K. Diffusion-tensor MRI: theory, experimental design and data analysis - a technical review. NMR Biomed. 2002, 15:456-467.
7. Basser P.J., Mattiello J., LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J.Magn Reson.B 1994, 103:247-254.
8. Bauer A., Zilles K., Matusch A., Holzmann C., Riess O., von Horsten S. Regional and subtype selective changes of neurotransmitter receptor density in a rat transgenic for the Huntington's disease mutation. J. Neurochem. 2005, 94:639-650.
9. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15:435-455.
10. Beaulieu C., Allen P.S. Determinants of anisotropic water diffusion in nerves. Magn Reson. Med. 1994, 31:394-400.
11. Bhagat Y.A., Beaulieu C. Diffusion anisotropy in subcortical white matter and cortical gray matter: changes with aging and the role of CSF-suppression. J. Magn Reson. Imaging 2004, 20:216-227.
12. Bode F.J., Stephan M., Suhling H., Pabst R., Straub R.H., Raber K.A., Bonin M., Nguyen H.P., Riess O., Bauer A., Sjoberg C., Petersen A., von Horsten S. Sex differences in a transgenic rat model of Huntington's disease: decreased 17beta-estradiol levels correlate with reduced numbers of DARPP32+ neurons in males. Hum. Mol. Genet. 2008, 17:2595-2609.
13. Bohanna I., Georgiou-Karistianis N., Hannan A.J., Egan G.F. Magnetic resonance imaging as an approach towards identifying neuropathological biomarkers for Huntington's disease. Brain Res. Rev. 2008, 58:209-225.
14. Cao C., Temel Y., Blokland A., Ozen H., Steinbusch H.W., Vlamings R., Nguyen H.P., von Horsten S., Schmitz C., Visser-Vandewalle V. Progressive deterioration of reaction time performance and choreiform symptoms in a new Huntington's disease transgenic ratmodel. Behav. Brain Res. 2006, 170:257-261.
15. Casteels C., Vermaelen P., Nuyts J., Van der Linden A., Baekelandt V., Mortelmans L., Bormans G., Van Laere K. Construction and evaluation of multitracer small-animal PET probabilistic atlases for voxel-based functional mapping of the rat brain. J. Nucl. Med. 2006, 47:1858-1866.
16. Ciarmiello A., Cannella M., Lastoria S., Simonelli M., Frati L., Rubinsztein D.C., Squitieri F. Brain white-matter volume loss and glucose hypometabolism precede the clinical symptoms of Huntington's disease. J. Nucl. Med. 2006, 47:215-222.
17. Constantinescu C.C., Coleman R.A., Pan M.L., Mukherjee J. Striatal and extrastriatal microPET imaging of D2/D3 dopamine receptors in rat brain with [(18)F]fallypride and [(18)F]desmethoxyfallypride. Synapse 2011, 65:778-787.
18. Dalley J.W., Fryer T.D., Brichard L., Robinson E.S., Theobald D.E., Laane K., Pena Y., Murphy E.R., Shah Y., Probst K., Abakumova I., Aigbirhio F.I., Richards H.K., Hong Y., Baron J.C., Everitt B.J., Robbins T.W. Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 2007, 315:1267-1270.
19. de Almeida L.P., Ross C.A., Zala D., Aebischer P., Deglon 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, 22:3473-3483.
20. Douaud G., Behrens T.E., Poupon C., Cointepas Y., Jbabdi S., Gaura V., Golestani N., Krystkowiak P., Verny C., Damier P., Bachoud-Levi A.C., Hantraye P., Remy P. In vivo evidence for the selective subcortical degeneration in Huntington's disease. NeuroImage 2009, 46:958-966.
21. Dubois A., Dauguet J., Herard A.S., Besret L., Duchesnay E., Frouin V., Hantraye P., Bonvento G., Delzescaux T. Automated three-dimensional analysis of histological and autoradiographic rat brain sections: application to an activation study. J. Cereb. Blood Flow Metab 2007, 27:1742-1755.
22. Feigin A., Leenders K.L., Moeller J.R., Missimer J., Kuenig G., Spetsieris P., Antonini A., Eidelberg D. Metabolic network abnormalities in early Huntington's disease: an [(18)F]FDG PET study. J. Nucl. Med. 2001, 42:1591-1595.
23. Fennema-Notestine C., Archibald S.L., Jacobson M.W., Corey-Bloom J., Paulsen J.S., Peavy G.M., Gamst A.C., Hamilton J.M., Salmon D.P., Jernigan T.L. In vivo evidence of cerebellar atrophy and cerebral white matter loss in Huntington disease. Neurology 2004, 63:989-995.
24. Ferrante R.J. Mouse models of Huntington's disease and methodological considerations for therapeutic trials. Biochim. Biophys. Acta 2009, 1792:506-520.
25. Gil J.M., Rego A.C. Mechanisms of neurodegeneration in Huntington's disease. Eur. J. Neurosci. 2008, 27:2803-2820.
26. Gomez-Tortosa E., MacDonald M.E., Friend J.C., Taylor S.A., Weiler L.J., Cupples L.A., Srinidhi J., Gusella J.F., Bird E.D., Vonsattel J.P., Myers R.H. Quantitative neuropathological changes in presymptomatic Huntington's disease. Ann. Neurol. 2001, 49:29-34.
27. Heng M.Y., Detloff P.J., Albin R.L. Rodent genetic models of Huntington disease. Neurobiol. Dis. 2008, 32:1-9.
28. Henley S.M., Frost C., MacManus D.G., Warner T.T., Fox N.C., Tabrizi S.J. Increased rate of whole-brain atrophy over 6months in early Huntington disease. Neurology 2006, 67:694-696.
29. Honer M., Bruhlmeier M., Missimer J., Schubiger A.P., Ametamey S.M. Dynamic imaging of striatal D2 receptors in mice using quad-HIDAC PET. J. Nucl. Med. 2004, 45:464-470.
30. Ishiwata K., Ogi N., Hayakawa N., Oda K., Nagaoka T., Toyama H., Suzuki F., Endo K., Tanaka A., Senda M. Adenosine A2A receptor imaging with [11C]KF18446 PET in the rat brain after quinolinic acid lesion: comparison with the dopamine receptor imaging. Ann. Nucl. Med. 2002, 16:467-475.
31. Jagoda E.M., Vaquero J.J., Seidel J., Green M.V., Eckelman W.C. Experiment assessment of mass effects in the rat: implications for small animal PET imaging. Nucl. Med. Biol. 2004, 31:771-779.
32. Kantor O., Temel Y., Holzmann C., Raber K., Nguyen H.P., Cao C., Turkoglu H.O., Rutten B.P., Visser-Vandewalle V., Steinbusch H.W., Blokland A., Korr H., Riess O., von Horsten S., Schmitz C. Selective striatal neuron loss and alterations in behavior correlate with impaired striatal function in Huntington's disease transgenic rats. Neurobiol. Dis. 2006, 22:538-547.
33. Kuhnast B., Hinnen F., Dollé F. Production of [18f]fallypride on a TRACERLab FX-FN synthesizer. J. Label. Comp. Radiopharm. 2009, 52.
34. Lammertsma A.A., Hume S.P. Simplified reference tissue model for PET receptor studies. NeuroImage 1996, 4:153-158.
35. Lerch J.P., Carroll J.B., Dorr A., Spring S., Evans A.C., Hayden M.R., Sled J.G., Henkelman R.M. Cortical thickness measured from MRI in the YAC128 mouse model of Huntington's disease. NeuroImage 2008, 41:243-251.
36. Lundberg C., Bjorklund T., Carlsson T., Jakobsson J., Hantraye P., Deglon N., Kirik D. Applications of lentiviral vectors for biology and gene therapy of neurological disorders. Curr. Gene Ther. 2008, 8:461-473.
37. Mascalchi M., Lolli F., Della N.R., Tessa C., Petralli R., Gavazzi C., Politi L.S., Macucci M., Filippi M., Piacentini S. Huntington disease: volumetric, diffusion-weighted, and magnetization transfer MR imaging of brain. Radiology 2004, 232:867-873.
38. Mori S., van Zijl P.C. A motion correction scheme by twin-echo navigation for diffusion-weighted magnetic resonance imaging with multiple RF echo acquisition. Magn. Reson. Med. 1998, 40:511-516.
39. Mukherjee J., Yang Z.Y., Das M.K., Brown T. Fluorinated benzamide neuroleptics-III. Development of (S)-N-[(1-allyl-2-pyrrolidinyl)methyl]-5-(3-[18F]fluoropropyl)-2, 3-dimethoxybenzamide as an improved dopamine D-2 receptor tracer. Nucl. Med. Biol. 1995, 22:283-296.
40. Mukherjee J., Christian B.T., Narayanan T.K., Shi B., Mantil J. Evaluation of dopamine D-2 receptor occupancy by clozapine, risperidone, and haloperidol in vivo in the rodent and nonhuman primate brain using 18F-fallypride. Neuropsychopharmacology 2001, 25:476-488.
41. Myers R.H., Vonsattel J.P., Paskevich P.A., Kiely D.K., Stevens T.J., Cupples L.A., Richardson E.P., Bird E.D. Decreased neuronal and increased oligodendroglial densities in Huntington's disease caudate nucleus. J. Neuropathol. Exp. Neurol. 1991, 50:729-742.
42. Nguyen H.P., Kobbe P., Rahne H., Worpel T., Jager B., Stephan M., Pabst R., Holzmann C., Riess O., Korr H., Kantor O., Petrasch-Parwez E., Wetzel R., Osmand A., von Horsten S. Behavioral abnormalities precede neuropathological markers in rats transgenic for Huntington's disease. Hum. Mol. Genet. 2006, 15:3177-3194.
43. Paulsen J.S., Magnotta V.A., Mikos A.E., Paulson H.L., Penziner E., Andreasen N.C., Nopoulos P.C. Brain structure in preclinical Huntington's disease. Biol. Psychiatry 2006, 59:57-63.
44. Paulsen J.S., Langbehn D.R., Stout J.C., Aylward E., Ross C.A., Nance M., Guttman M., Johnson S., MacDonald M., Beglinger L.J., Duff K., Kayson E., Biglan K., Shoulson I., Oakes D., Hayden M. Detection of Huntington's disease decades before diagnosis: the Predict-HD study. J. Neurol. Neurosurg. Psychiatry 2008, 79:874-880.
45. Pavese N., Andrews T.C., Brooks D.J., Ho A.K., Rosser A.E., Barker R.A., Robbins T.W., Sahakian B.J., Dunnett S.B., Piccini P. Progressive striatal and cortical dopamine receptor dysfunction in Huntington's disease: a PET study. Brain 2003, 126:1127-1135.
46. Petrasch-Parwez E., Nguyen H.P., Lobbecke-Schumacher M., Habbes H.W., Wieczorek S., Riess O., Andres K.H., Dermietzel R., von Horsten S. Cellular and subcellular localization of Huntingtin [corrected] aggregates in the brain of a rat transgenic for Huntington disease. J. Comp. Neurol. 2007, 501:716-730.
47. Pfefferbaum A., Sullivan E.V., Hedehus M., Lim K.O., Adalsteinsson E., Moseley M. Age-related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magn. Reson. Med. 2000, 44:259-268.
48. Politis M., Pavese N., Tai Y.F., Tabrizi S.J., Barker R.A., Piccini P. Hypothalamic involvement in Huntington's disease: an in vivo PET study. Brain 2008, 131:2860-2869.
49. Ramaswamy S., McBride J.L., Kordower J.H. Animal models of Huntington's disease. ILAR J. 2007, 48:356-373.
50. Reading S.A., Yassa M.A., Bakker A., Dziorny A.C., Gourley L.M., Yallapragada V., Rosenblatt A., Margolis R.L., Aylward E.H., Brandt J., Mori S., van, Z.P., Bassett S.S., Ross C.A. Regional white matter change in pre-symptomatic Huntington's disease: a diffusion tensor imaging study. Psychiatry Res. 2005, 140:55-62.
51. Rominger A., Wagner E., Mille E., Boning G., Esmaeilzadeh M., Wangler B., Gildehaus F.J., Nowak S., Bruche A., Tatsch K., Bartenstein P., Cumming P. Endogenous competition against binding of [(18)F]DMFP and [(18)F]fallypride to dopamine D(2/3) receptors in brain of living mouse. Synapse 2010, 64:313-322.
52. Rosas H.D., Koroshetz W.J., Chen Y.I., Skeuse C., Vangel M., Cudkowicz M.E., Caplan K., Marek K., Seidman L.J., Makris N., Jenkins B.G., Goldstein J.M. Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology 2003, 60:1615-1620.
53. Rosas H.D., Tuch D.S., Hevelone N.D., Zaleta A.K., Vangel M., Hersch S.M., Salat D.H. Diffusion tensor imaging in presymptomatic and early Huntington's disease: Selective white matter pathology and its relationship to clinical measures. Mov. Disord. 2006, 21:1317-1325.
54. Saatman K.E., Abai B., Grosvenor A., Vorwerk C.K., Smith D.H., Meaney D.F. Traumatic axonal injury results in biphasic calpain activation and retrograde transport impairment in mice. J. Cereb. Blood Flow Metab. 2003, 23:34-42.
55. Seppi K., Schocke M.F., Mair K.J., Esterhammer R., Weirich-Schwaiger H., Utermann B., Egger K., Brenneis C., Granata R., Boesch S., Poewe W., Wenning G.K. Diffusion-weighted imaging in Huntington's disease. Mov. Disord. 2006, 21:1043-1047.
56. Song S.K., Sun S.W., Ramsbottom M.J., Chang C., Russell J., Cross A.H. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 2002, 17:1429-1436.
57. Song S.K., Yoshino J., Le T.Q., Lin S.J., Sun S.W., Cross A.H., Armstrong R.C. Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage 2005, 26:132-140.
58. Sritharan A., Egan G.F., Johnston L., Horne M., Bradshaw J.L., Bohanna I., Asadi H., Cunnington R., Churchyard A.J., Chua P., Farrow M., Georgiou-Karistianis N. A longitudinal diffusion tensor imaging study in symptomatic Huntington's disease. J. Neurol. Neurosurg. Psychiatry 2010, 81:257-262.
59. Stoffers D., Sheldon S., Kuperman J.M., Goldstein J., Corey-Bloom J., Aron A.R. Contrasting gray and white matter changes in preclinical Huntington disease: an MRI study. Neurology 2010, 74:1208-1216.
60. Sun S.W., Song S.K., Harms M.P., Lin S.J., Holtzman D.M., Merchant K.M., Kotyk J.J. Detection of age-dependent brain injury in a mouse model of brain amyloidosis associated with Alzheimer's disease using magnetic resonance diffusion tensor imaging. Exp. Neurol. 2005, 191:77-85.
61. Tabrizi S.J., Langbehn D.R., Leavitt B.R., Roos R.A., Durr A., Craufurd D., Kennard C., Hicks S.L., Fox N.C., Scahill R.I., Borowsky B., Tobin A.J., Rosas H.D., Johnson H., Reilmann R., Landwehrmeyer B., Stout J.C. Biological and clinical manifestations of Huntington's disease in the longitudinal TRACK-HD study: cross-sectional analysis of baseline data. Lancet Neurol. 2009, 8:791-801.
62. Tantawy M.N., Jones C.K., Baldwin R.M., Ansari M.S., Conn P.J., Kessler R.M., Peterson T.E. [(18)F]Fallypride dopamine D2 receptor studies using delayed microPET scans and a modified Logan plot. Nucl. Med. Biol. 2009, 36:931-940.
63. Van Camp N., Blockx I., Verhoye M., Casteels C., Coun F., Leemans A., Sijbers J., Baekelandt V., Van Laere K., Van der Linden A. Diffusion tensor imaging in a rat model of Parkinson's disease after lesioning of the nigrostriatal tract. NMR Biomed. 2009, 22:697-706.
64. Van Camp N., Blockx I., Camon L., de Vera N., Verhoye M., Veraart J., Van H.W., Martinez E., Soria G., Sijbers J., Planas A.M., Van der Linden A. A complementary diffusion tensor imaging (DTI)-histological study in a model of Huntington's disease. Neurobiol. Aging. 2010, (Aug 17, Electronic publication ahead of print).
65. van Oostrom J.C., Maguire R.P., Verschuuren-Bemelmans C.C., Veenma-van der Duin L., Pruim J., Roos R.A., Leenders K.L. Striatal dopamine D2 receptors, metabolism, and volume in preclinical Huntington disease. Neurology 2005, 65:941-943.
66. von Horsten S., Schmitt I., Nguyen H.P., Holzmann C., Schmidt T., Walther T., Bader M., Pabst R., Kobbe P., Krotova J., Stiller D., Kask A., Vaarmann A., Rathke-Hartlieb S., Schulz J.B., Grasshoff U., Bauer I., Vieira-Saecker A.M., Paul M., Jones L., Lindenberg K.S., Landwehrmeyer B., Bauer A., Li X.J., Riess O. Transgenic rat model of Huntington's disease. Hum. Mol. Genet. 2003, 12:617-624.
67. Wang X., Sarkar A., Cicchetti F., Yu M., Zhu A., Jokivarsi K., Saint-Pierre M., Brownell A.L. Cerebral PET imaging and histological evidence of transglutaminase inhibitor cystamine induced neuroprotection in transgenic R6/2 mouse model of Huntington's disease. J. Neurol. Sci. 2005, 231:57-66.
68. Weaver K.E., Richards T.L., Liang O., Laurino M.Y., Samii A., Aylward E.H. Longitudinal diffusion tensor imaging in Huntington's Disease. Exp. Neurol. 2009, 216:525-529.
69. Yakushev I.Y., Dupont E., Buchholz H.G., Tillmanns J., Debus F., Cumming P., Heimann A., Fellgiebel A., Luhmann H.J., Landvogt C., Werhahn K.J., Schreckenberger M., Potschka H., Bartenstein P. In vivo imaging of dopamine receptors in a model of temporal lobe epilepsy. Epilepsia 2010, 51:415-422.
70. Zhang J., Peng Q., Li Q., Jahanshad N., Hou Z., Jiang M., Masuda N., Langbehn D.R., Miller M.I., Mori S., Ross C.A., Duan W. Longitudinal characterization of brain atrophy of a Huntington's disease mouse model by automated morphological analyses of magnetic resonance images. NeuroImage 2010, 49:2340-2351.