Light and electron microscopic characterization of the evolution of cellular pathology in the Hdh (CAG)150 Huntington's disease knock-in mouse

Brain Research Bulletin

Volumn 88, Issue 2-3, 2012, Pages 189-198

  Bayram Weston, Zubeyde ^a   Torres, Eduardo M ^a   Jones, Lesley ^b   Dunnett, Stephen B ^a   Brooks, Simon P ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Aggregations; HdhQ150 Q150; Huntington's disease; Inclusions; Knock in; Transmission electron microscope (TEM)

Indexed keywords

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN CORTEX; CELL NUCLEUS; CELL NUCLEUS INCLUSION BODY; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; CORPUS STRIATUM; CYTOPLASM; DISEASE COURSE; ELECTRON MICROSCOPY; FEMALE; GENE TARGETING; HUNTINGTON CHOREA; MALE; MITOCHONDRION SWELLING; MOUSE; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; OLFACTORY BULB; PHENOTYPE; PRIORITY JOURNAL; STAINING;

ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; FEMALE; GENE KNOCK-IN TECHNIQUES; GLIAL FIBRILLARY ACIDIC PROTEIN; HUNTINGTON DISEASE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS;

EID: 84860841633     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2011.03.014     Document Type: Article

References (48)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 1946, 239-247.
2. Bates G.P., Harper P.S., Jones L. Huntington's Disease 2002, vol. 5. Oxford University Press.
3. Bignami A., Eng L.F., Dahl D., Uyeda C.T. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 1972, 43:429-435.
4. Brooks S., Higgs G., Jones L., Dunnett S.B. Longitudinal analysis of the behavioural phenotype in Hdh((CAG)150) Huntington's disease knock-in mice. Brain Res. Bull. 2010.
5. D'Angelo M.A., Raices M., Panowski S.H., Hetzer M.W. Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 2009, 136:284-295.
6. Dahl D., Bignami A., Weber K., Osborn M. Filament proteins in rat optic nerves undergoing Wallerian degeneration: localization of vimentin, the fibroblastic 100-A filament protein, in normal and reactive astrocytes. Exp. Neurol. 1981, 73:496-506.
7. Davies S.W., Turmaine M., Cozens B.A., DiFiglia M., Sharp A.H., Ross C.A., Scherzinger E., Wanker E.E., Mangiarini L., Bates G.P. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 1997, 90:537-548.
8. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.P., Vonsattel J.P., Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997, 277:1990-1993.
9. Ferrante R.J., Kowall N.W., Beal M.F., Richardson E.P., Bird E.D., Martin J.B. Selective sparing of a class of striatal neurons in Huntington's disease. Science 1985, 230:561-563.
10. Galatioto S. Immunohistochemical findings in Huntington's Chorea: report of 9 cases. Pathologica 1996, 88:491-499.
11. Gutekunst C.A., Li S.H., Yi H., Mulroy J.S., Kuemmerle S., Jones R., Rye D., Ferrante R.J., Hersch S.M., Li X.J. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci. 1999, 19:2522-2534.
12. Heng M.Y., Duong D.K., Albin R.L., Tallaksen-Greene S.J., Hunter J.M., Lesort M.J., Osmand A., Paulson H.L., Detloff P.J. Early autophagic response in a novel knock-in model of Huntington disease. Hum. Mol. Genet. 2010, 19:3702-3720.
13. Heng M.Y., Tallaksen-Greene S.J., Detloff P.J., Albin R.L. Longitudinal evaluation of the Hdh(CAG)150 knock-in murine model of Huntington's disease. J. Neurosci. 2007, 27:8989-8998.
14. Kopito R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 2000, 10:524-530.
15. Li H., Li S.H., Cheng A.L., Mangiarini L., Bates G.P., Li X.J. Ultrastructural localization and progressive formation of neuropil aggregates in Huntington's disease transgenic mice,. Hum. Mol. Genet. 1999, 8:1227-1236.
16. Li H., Li S.H., Johnston H., Shelbourne P.F., Li X.J. Amino-terminal fragments of mutant huntingtin show selective accumulation in striatal neurons and synaptic toxicity. Nat. Genet. 2000, 25:385-389.
17. Lin C.H., Tallaksen-Greene S., Chien W.M., Cearley J.A., Jackson W.S., Crouse A.B., Ren S., Li X.J., Albin R.L., Detloff P.J. Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum. Mol. Genet. 2001, 10:137-144.
18. Lunkes A., Mandel J.L. A cellular model that recapitulates major pathogenic steps of Huntington's disease. Hum. Mol. Genet. 1998, 7:1355-1361.
19. Macdonald V., Halliday G. Pyramidal cell loss in motor cortices in Huntington's disease. Neurobiol. Dis. 2002, 10:378-386.
20. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S.W., 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 1996, 87:493-506.
21. Milnerwood A.J., Cummings D.M., Dallerac G.M., Brown J.Y., Vatsavayai S.C., Hirst M.C., Rezaie P., Murphy K.P. Early development of aberrant synaptic plasticity in a mouse model of Huntington's disease. Hum. Mol. Genet. 2006, 15:1690-1703.
22. Morton A.J., Lagan M.A., Skepper J.N., Dunnett S.B. Progressive formation of inclusions in the striatum and hippocampus of mice transgenic for the human Huntington's disease mutation. J. Neurocytol. 2000, 29:679-702.
23. Ordway J.M., Tallaksen-Greene S., Gutekunst C.A., Bernstein E.M., Cearley J.A., Wiener H.W., Dure L.S., Lindsey R., Hersch S.M., Jope R.S., Albin R.L., Detloff P.J. Ectopically expressed CAG repeats cause intranuclear inclusions and a progressive late onset neurological phenotype in the mouse. Cell 1997, 91:753-763.
24. Panov A.V., Gutekunst C.A., Leavitt B.R., Hayden M.R., Burke J.R., Strittmatter W.J., Greenamyre J.T. Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Nat. Neurosci. 2002, 5:731-736.
25. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego CA. 2nd ed.
26. Reddy P.H., Williams M., Charles V., Garrett L., Pike-Buchanan L., Whetsell W.O., Miller G., Tagle D.A. Behavioural abnormalities and selective neuronal loss in HD transgenic mice expressing mutated full-length HD cDNA. Nat. Genet. 1998, 20:198-202.
27. Reddy P.H., Williams M., Tagle D.A. Recent advances in understanding the pathogenesis of Huntington's disease. Trends Neurosci. 1999, 22:248-255.
28. Reiner A., Del Mar N., Deng Y.P., Meade C.A., Sun Z., Goldowitz D. R6/2 neurons with intranuclear inclusions survive for prolonged periods in the brains of chimeric mice. J. Comp. Neurol. 2007, 505:603-629.
29. Roos R.A., Bots G.T. Nuclear membrane indentations in Huntington's chorea. J. Neurol. Sci. 1983, 61:37-47.
30. Roos R.A., Pruyt J.F., de Vries J., Bots G.T. Neuronal distribution in the putamen in Huntington's disease. J. Neurol. Neurosurg. Psychiatry 1985, 48:422-425.
31. Rosas H.D., Liu A.K., Hersch S., Glessner M., Ferrante R.J., Salat D.H., van der K.A., Jenkins B.G., Dale A.M., Fischl B. Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology 2002, 58:695-701.
32. Ross C.A. Intranuclear neuronal inclusions: a common pathogenic mechanism for glutamine-repeat neurodegenerative diseases?. Neuron 1997, 19:1147-1150.
33. Sapp E., Schwarz C., Chase K., Bhide P.G., Young A.B., Penney J., Vonsattel J.P., Aronin N., DiFiglia M. Huntingtin localization in brains of normal and Huntington's disease patients. Ann. Neurol. 1997, 42:604-612.
34. Saudou F., Finkbeiner S., Devys D., Greenberg M.E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 1998, 95:55-66.
35. Shin J.Y., Fang Z.H., Yu Z.X., Wang C.E., Li S.H., Li X.J. Expression of mutant huntingtin in glial cells contributes to neuronal excitotoxicity. J. Cell Biol. 2005, 171:1001-1012.
36. Singhrao S.K., Thomas P., Wood J.D., MacMillan J.C., Neal J.W., Harper P.S., Jones A.L. Huntingtin protein colocalizes with lesions of neurodegenerative diseases: an investigation in Huntington's, Alzheimer's, and Pick's diseases. Exp. Neurol. 1998, 150:213-222.
37. Sisodia S.S. Nuclear inclusions in glutamine repeat disorders: are they pernicious, coincidental, or beneficial?. Cell 1998, 95:1-4.
38. Tallaksen-Greene S.J, Crouse A.B., Hunter J.M., Detloff P.J., Albin R.L. Neuronal intranuclear inclusions and neuropil aggregates in HdhCAG(150) knockin mice. Neuroscience 2005, 131:843-852.
39. Tellez-Nagel I., Johnson A.B., Terry R.D. Studies on brain biopsies of patients with Huntington's chorea. J. Neuropathol. Exp. Neurol. 1974, 33:308-332.
40. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 1993, 72:971-983. The Huntington's Disease Collaborative Research Group.
41. Trueman R.C., Brooks S.P., Jones L., Dunnett S.B. The operant serial implicit learning task reveals early onset motor learning deficits in the Hdh knock-in mouse model of Huntington's disease. Eur. J. Neurosci. 2007, 25:551-558.
42. Turmaine M., Raza A., Mahal A., Mangiarini L., Bates G.P., Davies S.W. Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8093-8097.
43. Vis J.C., Nicholson L.F., Faull R.L., Evans W.H., Severs N.J., Green C.R. Connexin expression in Huntington's diseased human brain. Cell Biol. Int. 1998, 22:837-847.
44. Vonsattel J.P., DiFiglia M. Huntington disease. J. Neuropathol. Exp. Neurol. 1998, 57:369-384.
45. Vonsattel J.P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., Richardson E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 1985, 44:559-577.
46. Wheeler V.C., White J.K., Gutekunst C.A., Vrbanac V., Weaver M., Li X.J., Li S.H., Yi H., Vonsattel J.P., Gusella J.F., Hersch S., Auerbach W., Joyner A.L., MacDonald M.E. 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, 9:503-513.
47. Woodman B., Butler R., Landles C., Lupton M.K., Tse J., Hockly E., Moffitt H., Sathasivam K., Bates G.P. The Hdh(Q150/Q150) knock-in mouse model of HD and the R6/2 exon 1 model develop comparable and widespread molecular phenotypes. Brain Res. Bull. 2007, 72:83-97.
48. Yu Z.X., Li S.H., Evans J., Pillarisetti A., Li H., Li X.J. Mutant huntingtin causes context-dependent neurodegeneration in mice with Huntington's disease. J. Neurosci. 2003, 23:2193-2202.