Longitudinal characterization of brain atrophy of a Huntington's disease mouse model by automated morphological analyses of magnetic resonance images

NeuroImage

Volumn 49, Issue 3, 2010, Pages 2340-2351

  Zhang, Jiangyang ^a   Peng, Qi ^a   Li, Qing ^a   Jahanshad, Neda ^a   Hou, Zhipeng ^a   Jiang, Mali ^a   Masuda, Naoki ^a   Langbehn, Douglas R ^b   Miller, Michael I ^a,c   Mori, Susumu ^a,d   Ross, Christopher A ^a   Duan, Wenzhen ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c Johns Hopkins University   (United States)

^d KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

Automated morphological analysis; Biomarker; Brain atrophy; Huntington's disease; MRI

Indexed keywords

ACCURACY; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOMATION; BRAIN ATROPHY; BRAIN REGION; CONTROLLED STUDY; DISEASE COURSE; EX VIVO STUDY; FEMALE; HUNTINGTON CHOREA; IMAGE ANALYSIS; IN VIVO STUDY; MALE; MORPHOLOGY; MOUSE; NERVE DEGENERATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SURVIVAL; TRANSGENIC MOUSE;

ANIMALS; ATROPHY; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; HUNTINGTON DISEASE; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MICE; MICE, TRANSGENIC;

EID: 71849109192     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.10.027     Document Type: Article

References (53)

1. Ali A.A., Dale A.M., Badea A., and Johnson G.A. Automated segmentation of neuroanatomical structures in multispectral MR microscopy of the mouse brain. NeuroImage 27 (2005) 425-435
2. Ashburner J., and Friston K.J. Nonlinear spatial normalization using basis functions. Hum. Brain Mapp. 7 (1999) 254-266
3. Ashburner J., and Friston K.J. Voxel-based morphometry-the methods. NeuroImage 11 (2000) 805-821
4. Aylward E.H. Change in MRI striatal volumes as a biomarker in preclinical Huntington's disease. Brain Res. Bull. 72 (2007) 152-158
5. Badea A., Ali-Sharief A.A., and Johnson G.A. Morphometric analysis of the C57BL/6J mouse brain. NeuroImage (2007)
6. Badea A., Ali-Sharief A.A., and Johnson G.A. Morphometric analysis of the C57BL/6J mouse brain. NeuroImage 37 (2007) 683-693
7. Bae M.H., Pan R., Wu T., and Badea A. Automated segmentation of mouse brain images using extended MRF. NeuroImage 46 (2009) 717-725
8. Beal M.F., and Ferrante R.J. Experimental therapeutics in transgenic mouse models of Huntington's disease. Nat. Rev., Neurosci. 5 (2004) 373-384
9. Bertrand J.B., Langlois J.B., Begou M., Volle J., Brun P., d'Amato T., Saoud M., and Suaud-Chagny M.F. Longitudinal MRI monitoring of brain damage in the neonatal ventral hippocampal lesion rat model of schizophrenia. Hippocampus (2009) (May 18, Electronic publication ahead of print)
10. Bock N.A., Kovacevic N., Lipina T.V., Roder J.C., Ackerman S.L., and Henkelman R.M. In vivo magnetic resonance imaging and semiautomated image analysis extend the brain phenotype for cdf/cdf mice. J. Neurosci. 26 (2006) 4455-4459
11. Borg J., and Chereul E. Differential MRI patterns of brain atrophy in double or single transgenic mice for APP and/or SOD. J. Neurosci. Res. 86 (2008) 3275-3284
12. Chan E., Kovacevic N., Ho S.K., Henkelman R.M., and Henderson J.T. Development of a high resolution three-dimensional surgical atlas of the murine head for strains 129S1/SvImJ and C57Bl/6J using magnetic resonance imaging and micro-computed tomography. Neuroscience 144 (2007) 604-615
13. Chiang M.C., Leow A.D., Klunder A.D., Dutton R.A., Barysheva M., Rose S.E., McMahon K.L., de Zubicaray G.I., Toga A.W., and Thompson P.M. Fluid registration of diffusion tensor images using information theory. IEEE Trans. Med. Imaging 27 (2008) 442-456
14. Davatzikos C. Why voxel-based morphometric analysis should be used with great caution when characterizing group differences. NeuroImage 23 (2004) 17-20
15. Delatour B., Guegan M., Volk A., and Dhenain M. In vivo MRI and histological evaluation of brain atrophy in APP/PS1 transgenic mice. Neurobiol. Aging 27 (2006) 835-847
16. Ferrante R.J., Andreassen O.A., Jenkins B.G., Dedeoglu A., Kuemmerle S., Kubilus J.K., Kaddurah-Daouk R., Hersch S.M., and Beal M.F. Neuroprotective effects of creatine in a transgenic mouse model of Huntington's disease. J. Neurosci. 20 (2000) 4389-4397
17. Ferrante R.J., Andreassen O.A., Dedeoglu A., Ferrante K.L., Jenkins B.G., Hersch S.M., and Beal M.F. Therapeutic effects of coenzyme Q10 and remacemide in transgenic mouse models of Huntington's disease. J. Neurosci. 22 (2002) 1592-1599
18. Filippi M., Mastronardo G., Bastianello S., Rocca M.A., Rovaris M., Gasperini C., Pozzilli C., and Comi G. A longitudinal brain MRI study comparing the sensitivities of the conventional and a newer approach for detecting active lesions in multiple sclerosis. J. Neurol. Sci. 159 (1998) 94-101
19. Genovese C.R., Lazar N.A., and Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 15 (2002) 870-878
20. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., and Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 14 (2001) 21-36
21. Hersch S.M., and Ferrante R.J. Translating therapies for Huntington's disease from genetic animal models to clinical trials. NeuroRx 1 (2004) 298-306
22. Huntington's disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72 (1993) 971-983
23. Jacobs R.E., Ahrens E.T., Dickinson M.E., and Laidlaw D. Towards a microMRI atlas of mouse development. Comput. Med. Imaging Graph 23 (1999) 15-24
24. Johnson G.A., Ali-Sharief A., Badea A., Brandenburg J., Cofer G., Fubara B., Gewalt S., Hedlund L.W., and Upchurch L. High-throughput morphologic phenotyping of the mouse brain with magnetic resonance histology. NeuroImage 37 (2007) 82-89
25. Kovacevic N., Henderson J.T., Chan E., Lifshitz N., Bishop J., Evans A.C., Henkelman R.M., and Chen X.J. A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cereb. Cortex 15 (2005) 639-645
26. Kusakabe M., Mangiarini L., Laywell E.D., Bates G.P., Yoshiki A., Hiraiwa N., Inoue J., and Steindler D.A. Loss of cortical and thalamic neuronal tenascin-C expression in a transgenic mouse expressing exon 1 of the human Huntington disease gene. J. Comp. Neurol. 430 (2001) 485-500
27. Lau J.C., Lerch J.P., Sled J.G., Henkelman R.M., Evans A.C., and Bedell B.J. Longitudinal neuroanatomical changes determined by deformation-based morphometry in a mouse model of Alzheimer's disease. NeuroImage 42 (2008) 19-27
28. Lerch J.P., Carroll J.B., Dorr A., Spring S., Evans A.C., Hayden M.R., Sled J.G., and Henkelman R.M. Cortical thickness measured from MRI in the YAC128 mouse model of Huntington's disease. NeuroImage 41 (2008) 243-251
29. Lerch J.P., Carroll J.B., Spring S., Bertram L.N., Schwab C., Hayden M.R., and Henkelman R.M. Automated deformation analysis in the YAC128 Huntington disease mouse model. NeuroImage 39 (2008) 32-39
30. Li J.Y., Popovic N., and Brundin P. The use of the R6 transgenic mouse models of Huntington's disease in attempts to develop novel therapeutic strategies. NeuroRx 2 (2005) 447-464
31. Ma Y., Hof P.R., Grant S.C., Blackband S.J., Bennett R., Slatest L., McGuigan M.D., and Benveniste H. A three-dimensional digital atlas database of the adult C57BL/6J mouse brain by magnetic resonance microscopy. Neuroscience 135 (2005) 1203-1215
32. MacKenzie-Graham A., Lee E.F., Dinov I.D., Bota M., Shattuck D.W., Ruffins S., Yuan H., Konstantinidis F., Pitiot A., Ding Y., Hu G., Jacobs R.E., and Toga A.W. A multimodal, multidimensional atlas of the C57BL/6J mouse brain. J. Anat. 204 (2004) 93-102
33. Maheswaran S., Barjat H., Bate S.T., Aljabar P., Hill D.L., Tilling L., Upton N., James M.F., Hajnal J.V., and Rueckert D. Analysis of serial magnetic resonance images of mouse brains using image registration. NeuroImage 44 (2009) 692-700
34. Mann D.M., Oliver R., and Snowden J.S. The topographic distribution of brain atrophy in Huntington's disease and progressive supranuclear palsy. Acta Neuropathol. 85 (1993) 553-559
35. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S.W., and Bates G.P. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87 (1996) 493-506
36. Maheswaran S., Barjat H., Rueckert D., Bate S.T., Howlett D.R., Tilling L., Smart S.C., Pohlmann A., Richardson J.C., Hartkens T., Hill D.L., Upton N., Hajnal J.V., and James M.F. Longitudinal regional brain volume changes quantified in normal aging and Alzheimer's APP x PS1 mice using MRI. Brain Res. 1270 (2009) 19-32
37. Mazziotta J., Toga A., Evans A., Fox P., Lancaster J., Zilles K., Woods R., Paus T., Simpson G., Pike B., Holmes C., Collins L., Thompson P., MacDonald D., Iacoboni M., Schormann T., Amunts K., Palomero-Gallagher N., Geyer S., Parsons L., Narr K., Kabani N., Le Goualher G., Boomsma D., Cannon T., Kawashima R., and Mazoyer B. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos. Trans. R. Soc. Lond., B Biol. Sci. 356 (2001) 1293-1322
38. McDaniel B., Sheng H., Warner D.S., Hedlund L.W., and Benveniste H. Tracking brain volume changes in C57BL/6J and ApoE-deficient mice in a model of neurodegeneration: a 5-week longitudinal micro-MRI study. NeuroImage 14 (2001) 1244-1255
39. Miller M.I., Trouve A., and Younes L. On the metrics and Euler-Lagrange equations of computational anatomy. Annu. Rev. Biomed. Eng. 4 (2002) 375-405
40. Myers R.H., Vonsattel J.P., Stevens T.J., Cupples L.A., Richardson E.P., Martin J.B., and Bird E.D. Clinical and neuropathologic assessment of severity in Huntington's disease. Neurology 38 (1988) 341-347
41. Oishi K., Faria A., Jiang H., Li X., Akhter K., Zhang J., Hsu J.T., Miller M.I., van Zijl P.C., Albert M., Lyketsos C.G., Woods R., Toga A.W., Pike G.B., Rosa-Neto P., Evans A., Mazziotta J., and Mori S. Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: application to normal elderly and Alzheimer's disease participants. NeuroImage 46 (2009) 486-499
42. Oishi K., Faria A., Jiang H., Li X., Akhter K., Zhang J., Hsu J.T., Miller M.I., van Zijl P.C., Albert M., Lyketsos C.G., Woods R., Toga A.W., Pike G.B., Rosa-Neto P., Evans A., Mazziotta J., and Mori S. Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: application to normal elderly and Alzheimer's disease participantstlas. NeuroImage 46 (2009) 486-499
43. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates. 2nd ed. (2003), Academic Press, Scan Diego
44. Sawiak S.J., Wood N.I., Williams G.B., Morton A.J., and Carpenter T.A. Use of magnetic resonance imaging for anatomical phenotyping of the R6/2 mouse model of Huntington's disease. Neurobiol. Dis. 33 (2009) 12-19
45. Sawiak S.J., Wood N.I., Williams G.B., Morton A.J., and Carpenter T.A. Voxel-based morphometry in the R6/2 transgenic mouse reveals differences between genotypes not seen with manual 2D morphometry. Neurobiol. Dis. 33 (2009) 20-27
46. Saydoff J.A., Garcia R.A., Browne S.E., Liu L., Sheng J., Brenneman D., Hu Z., Cardin S., Gonzalez A., von Borstel R.W., Gregorio J., Burr H., and Beal M.F. Oral uridine pro-drug PN401 is neuroprotective in the R6/2 and N171-82Q mouse models of Huntington's disease. Neurobiol. Dis. 24 (2006) 455-465
47. Sharief A.A., Badea A., Dale A.M., and Johnson G.A. Automated segmentation of the actively stained mouse brain using multi-spectral MR microscopy. NeuroImage 39 (2008) 136-145
48. Sieradzan K., Mann D.M., and Dodge A. Clinical presentation and patterns of regional cerebral atrophy related to the length of trinucleotide repeat expansion in patients with adult onset Huntington's disease. Neurosci. Lett. 225 (1997) 45-48
49. Stack E.C., Kubilus J.K., Smith K., Cormier K., Del Signore S.J., Guelin E., Ryu H., Hersch S.M., and Ferrante R.J. Chronology of behavioral symptoms and neuropathological sequela in R6/2 Huntington's disease transgenic mice. J. Comp. Neurol. 490 (2005) 354-370
50. Turmaine M., Raza A., Mahal A., Mangiarini L., Bates G.P., and Davies S.W. Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 8093-8097
51. Vonsattel J.P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., and Richardson Jr. E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44 (1985) 559-577
52. Ward B.C., Agarwal S., Wang K., Berger-Sweeney J., and Kolodny N.H. Longitudinal brain MRI study in a mouse model of Rett Syndrome and the effects of choline. Neurobiol. Dis. 31 (2008) 110-119
53. Wright I.C., McGuire P.K., Poline J.B., Travere J.M., Murray R.M., Frith C.D., Frackowiak R.S., and Friston K.J. A voxel-based method for the statistical analysis of gray and white matter density applied to schizophrenia. NeuroImage 2 (1995) 244-252