Time course of early motor and neuropathological anomalies in a knock-in mouse model of Huntington's disease with 140 CAG repeats

Journal of Comparative Neurology

Volumn 465, Issue 1, 2003, Pages 11-26

  Menalled, Liliana B ^a   Sison, Jessica D ^a   Dragatsis, Ioannis ^b   Zeitlin, Scott ^c   Chesselet, Marie Françoise ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Behavior; Huntingtin protein; Immunohistochemistry; Neurodegenerative disease

Indexed keywords

DOPAMINE; HUNTINGTIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CELL NUCLEUS; CHIMERA; CONTROLLED STUDY; CORPUS STRIATUM; DEGENERATIVE DISEASE; EXON; GAIT; GENE EXPRESSION; GENETIC CODE; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MOTOR DYSFUNCTION; MOUSE; NEUROPATHOLOGY; NEUROPIL; NONHUMAN; NUCLEOTIDE REPEAT; NUCLEUS ACCUMBENS; OLFACTORY BULB; OLFACTORY SYSTEM; PRIORITY JOURNAL;

ANIMALS; BRAIN; CEREBRAL CORTEX; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; FEMALE; GROOMING; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; INCLUSION BODIES; LAMENESS, ANIMAL; MALE; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEURONS; NEUROPIL; NUCLEAR PROTEINS; NUCLEUS ACCUMBENS; OLFACTORY PATHWAYS; RECOMBINANT FUSION PROTEINS; TIME FACTORS; TRINUCLEOTIDE REPEATS;

EID: 0041691176     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10776     Document Type: Article

References (79)

1. Albin RL, Greenamyre JT. 1992. Alternative excitotoxic hypotheses. Neurology 42:733-738.
2. Beal MF, Kowall NW, Ellison DW, Mazurek MF, Swartz KJ, Martin JB. 1986. Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid. Nature 321:168-171.
3. Beal MF, Ferrante RJ, Swartz KJ, Kowall NW. 1991. Chronic quinolinic acid lesions in rats closely resemble Huntington's disease. J Neurosci 11:1649-1659.
4. Becher MW, Kotzuk JA, Sharp AH, Davies SW, Bates GP, Price DL, Ross CA. 1998. Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length. Neurobiol Dis 4:387-397.
5. Bibb JA, Yan Z, Svenningsson P, Snyder GL, Pieribone VA, Horiuchi A, Nairn AC, Messer A, Greengard P. 2000. Severe deficiencies in dopamine signaling in presymptomatic Huntington's disease mice. Proc Natl Acad Sci U S A 97:6809-6814.
6. Bradley A. 1987. Production and analysis of chaimaeric mice. Oxford: IRL Press.
7. Bylsma FW, Moberg PJ, Doty RL, Brandt J. 1997. Odor identification in Huntington's disease patients and asymptomatic gene carriers. J Neuropsychiatry Clin Neurosci 9:598-600.
8. Cepeda C, Ariano MA, Calvert CR, Flores-Hernandez J, Chandler SH, Leavitt BR, Hayden MR, Levine MS. 2001. NMDA receptor function in mouse models of Huntington disease. J Neurosci Res 66:525-539.
9. Cha JH, Kosinski CM, Kerner JA, Alsdorf SA, Mangiarini L, Davies SW, Penney JB, Bates GP, Young AB. 1998. Altered brain neurotransmitter receptors in transgenic mice expressing a portion of an abnormal human huntington disease gene. Proc Natl Acad Sci U S A 95:6480-6485.
10. Cheng N, Maeda T, Kume T, Kaneko S, Kochiyama H, Akaike A, Goshima Y, Misu Y. 1996. Differential neurotoxicity induced by L-DOPA and dopamine in cultured striatal neurons. Brain Res 743:278-283.
11. Cooper JK, Schilling G, Peters MF, Herring WJ, Sharp AH, Kaminsky Z, Masone J, Khan FA, Delanoy M, Borchelt DR, Dawson VL, Dawson TM, Ross CA. 1998. Truncated N-terminal fragments of huntingtin with expanded glutamine repeats form nuclear and cytoplasmic aggregates in cell culture. Hum Mol Genet 7:783-790.
12. Davies SW, Turmaine M, Cozens BA, DiFiglia M, Sharp AH, Ross CA, Scherzinger E, Wanker EE, Mangiarini L, Bates GP. 1997. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90:537-548.
13. Descarries L, Lemay B, Doucet G, Berger B. 1987. Regional and laminar density of the dopamine innervation in adult rat cerebral cortex. Neuroscience 21:807-824.
14. DiFiglia M. 1990. Excitotoxic injury of the neostriatum: a model for Huntington's disease. Trends Neurosci 13:286-289.
15. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N. 1997. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277:1990-1993.
16. Fallon JH, Moore RY. 1978a. Catecholamine innervation of the basal forebrain. III. Olfactory bulb, anterior olfactory nuclei, olfactory tubercle and piriform cortex. J Comp Neurol 180:533-544.
17. Fallon JH, Moore RY. 1978b. Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J Comp Neurol 180:545-580.
18. Fallon JH, Koziell DA, Moore RY. 1978. Catecholamine innervation of the basal forebrain. II. Amygdala, suprarhinal cortex and entorhinal cortex. J Comp Neurol 180:509-532.
19. Ferrante RJ, Kowall NW, Cipolloni PB, Storey E, Beal MF. 1993. Excitotoxin lesions in primates as a model for Huntington's disease: histopathologic and neurochemical characterization. Exp Neurol 119:46-71.
20. Filloux F, Townsend JJ. 1993. Pre- and postsynaptic neurotoxic effects of dopamine demonstrated by intrastriatal injection. Exp Neurol 119:79-88.
21. Franklin KBJ, Paxinos G. 1997. The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
22. Fuxe K. 1964. The distribution of monoamine terminals in the central nervous system. Acta Physiol Scand Suppl 247:39-85.
23. Globus MY, Ginsberg MD, Dietrich WD, Busto R, Scheinberg P. 1987. Substantia nigra lesion protects against ischemic damage in the striatum. Neurosci Lett 80:251-256.
24. Goldberg YP, Nicholson DW, Rasper DM, Kalchman MA, Koide HB, Graham RK, Bromm M, Kazemi-Esfarjani P, Thornberry NA, Vaillancourt JP, Hayden MR. 1996. Cleavage of huntingtin by apopain, a proapoptotic cysteine protease, is modulated by the polyglutamine tract. Nat Genet 13:442-449.
25. Gourfinkel-An I, Cancel G, Duyckaerts C, Faucheux B, Hauw JJ, Trottier Y, Brice A, Agid Y, Hirsch EC. 1998. Neuronal distribution of intranuclear inclusions in Huntington's disease with adult onset. Neuroreport 9:1823-1826.
26. Gusella JF, MacDonald ME. 2000. Molecular genetics: unmasking polyglutamine triggers in neurodegenerative disease. Nat Rev Neurosci 1:109-115.
27. Gutekunst CA, Li SH, Yi H, Mulroy JS, Kuemmerle S, Jones R, Rye D, Ferrante RJ, Hersch SM, Li XJ. 1999. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J Neurosci 19:2522-2534.
28. Hamilton JM, Murphy C, Paulsen JS. 1999. Odor detection, learning, and memory in Huntington's disease. J Int Neuropsychol Soc 5:609-615.
29. Harper PS. 1996. Huntington's disease. Philadelphia: W.B. Saunders.
30. Hastings TG, Lewis DA, Zigmond MJ. 1996. Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc Natl Acad Sci U S A 93:1956-1961.
31. Hattori A, Luo Y, Umegaki H, Munoz J, Roth GS. 1998. Intrastriatal injection of dopamine results in DNA damage and apoptosis in rats. Neuroreport 9:2569-2572.
32. Hedreen JC, Peyser CE, Folstein SE, Ross CA. 1991. Neuronal loss in layers V and VI of cerebral cortex in Huntington's disease. Neurosci Lett 133:257-261.
33. Jakel RJ, Maragos WF. 2000. Neuronal cell death in Huntington's disease: a potential role for dopamine. Trends Neurosci 23:239-245.
34. Klapstein GJ, Fisher RS, Zanjani H, Cepeda C, Jokel ES, Chesselet MF, Levine MS. 2001. Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice. J Neurophysiol 86:2667-2677.
35. Klement IA, Skinner PJ, Kaytor MD, Yi H, Hersch SM, Clark HB, Zoghbi HY, Orr HT. 1998. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 95:41-53.
36. Kosinski CM, Luesse HG, Sprueken A, Puls C, Schiefer J. 2000. Usefulness of rotarod, open field and watermaze testing in the evaluation of treatment strategies in R6/2 Huntington's disease exon 1 transgenic mice. Soc Neurosci Abstr 26:182.7.
37. Kovacs T, Cairns NJ, Lantos PL. 2001. Olfactory centers in Alzheimer's disease: olfactory bulb is involved in early Braak's stages. Neuroreport 12:285-288.
38. Laforet GA, Sapp E, Chase K, McIntyre C, Boyce FM, Campbell M, Cadigan BA, Warzecki L, Tagle DA, Reddy PH, Cepeda C, Calvert CR, Jokel ES, Klapstein GJ, Ariano MA, Levine MS, DiFiglia M, Aronin N. 2001. Changes in cortical and striatal neurons predict behavioral and electrophysiological abnormalities in a transgenic murine model of Huntington's disease. J Neurosci 21:9112-9123.
39. Levine MS, Klapstein GJ, Koppel A, Gruen E, Cepeda C, Vargas ME, Jokel ES, Carpenter EM, Zanjani H, Hurst RS, Efstratiadis A, Zeitlin S, Chesselet MF. 1999. Enhanced sensitivity to N-methyl-D-aspartate receptor activation in transgenic and knockin mouse models of Huntington's disease. J Neurosci Res 58:515-532.
40. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, Yen SH, Sahara N, Skipper L, Yager D, Eckman C, Hardy J, Hutton M, McGowan E. 2001. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293:1487-1491.
41. Li H, Li SH, Cheng AL, Mangiarini L, Bates GP, Li XJ. 1999. Ultrastructural localization and progressive formation of neuropil aggregates in Huntington's disease transgenic mice. Hum Mol Genet 8:1227-1236.
42. Li H, Li SH, Johnston H, Shelbourne PF, Li XJ. 2000. Amino-terminal fragments of mutant huntingtin show selective accumulation in striatal neurons and synaptic toxicity. Nat Genet 25:385-389.
43. Li H, Li SH, Yu ZX, Shelbourne P, Li XJ. 2001. Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. J Neurosci 21:8473-8481.
44. Lin CH, Tallaksen-Greene S, Chien WM, Cearley JA, Jackson WS, Crouse AB, Ren S, Li XJ, Albin RL, Detloff PJ. 2001. Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum Mol Genet 10:137-144.
45. Lindvall O, Bjorklund A. 1978. Anatomy of the dopaminergic neuron systems in the rat brain. Adv Biochem Psychopharmacol 19:1-23.
46. Luthi-Carter R, Strand A, Peters NL, Solano SM, Hollingsworth ZR, Menon AS, Frey AS, Spektor BS, Penney EB, Schilling G, Ross CA, Borchelt DR, Tapscott SJ, Young AB, Cha JH, Olson JM. 2000. Decreased expression of striatal signaling genes in a mouse model of Huntington's disease. Hum Mol Genet 9:1259-1271.
47. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP. 1996. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87:493-506.
48. Mansour SL, Thomas KR, Capecchi MR. 1988. Disruption of the protooncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature 336:348-352.
49. Martin-Aparicio E, Yamamoto A, Hernandez F, Hen R, Avila J, Lucas JJ. 2001. Proteasomal-dependent aggregate reversal and absence of cell death in a conditional mouse model of Huntington's disease. J Neurosci 21:8772-8781.
50. Masliah E, Rockenstein E, Veinbergs I, Mallory M, Hashimoto M, Takeda A, Sagara Y, Sisk A, Mucke L. 2000. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287:1265-1269.
51. McLaughlin BA, Nelson D, Erecinska M, Chesselet MF. 1998. Toxicity of dopamine to striatal neurons in vitro and potentiation of cell death by a mitochondrial inhibitor. J Neurochem 70:2406-2415.
52. Menalled LB, Chesselet MF. 2002. Mouse models of Huntington's disease. Trends Phamacol Sci 23:32-39.
53. Menalled LB, Sison JD, Wu Y, Olivieri M, Li X-J, Li H, Zeitlin S, Chesselet MF. 2002. Early motor dysfunction and striosomal distribution of huntingtin microaggregates in Huntington's disease knock-in mice. J Neurosci 22:8266-8276.
54. Menalled LB, Zanjani H, MacKenzie L, Koppel A, Carpenter E, Zeitlin S, Chesselet MF. 2000. Decrease in striatal enkephalin mRNA in mouse models of Huntington's disease. Exp Neurol 162:328-342.
55. Mende-Mueller LM, Toneff T, Hwang SR, Chesselet MF, Hook VY. 2001. Tissue-specific proteolysis of Huntingtin (htt) in human brain: evidence of enhanced levels of N- and C-terminal htt fragments in Huntington's disease striatum. J Neurosci 21:1830-1837.
56. Mesholam RI, Moberg PJ, Mahr RN, Doty RL. 1998. Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases. Arch Neurol 55:84-90.
57. Moberg PJ, Doty RL. 1997. Olfactory function in Huntington's disease patients and at-risk offspring. Int J Neurosci 89:133-139.
58. Muchowski PJ, Ning K, D'Souza-Schorey C, Fields S. 2002. Requirement of an intact microtubule cytoskeleton for aggregation and inclusion body formation by a mutant huntingtin fragment. Proc Natl Acad Sci U S A 99:727-732.
59. Nordin S, Paulsen JS, Murphy C. 1995. Sensory- and memory-mediated olfactory dysfunction in Huntington's disease. J Int Neuropsychol Soc 1:281-290.
60. Nucifora FC Jr, Sasaki M, Peters MF, Huang H, Cooper JK, Yamada M, Takahashi H, Tsuji S, Troncoso J, Dawson VL, Dawson TM, Ross CA. 2001. Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291:2423-2428.
61. Persichetti F, Ambrose CM, Ge P, McNeil SM, Srinidhi J, Anderson MA, Jenkins B, Barnes GT, Duyao MP, Kanaley L, et al. 1995. Normal and expanded Huntington's disease gene alleles produce distinguishable proteins due to translation across the CAG repeat. Mol Med 1:374-383.
62. Petersen A, Larsen KE, Behr GG, Romero N, Przedborski S, Brundin P, Sulzer D. 2001. Expanded CAG repeats in exon 1 of the Huntington's disease gene stimulate dopamine-mediated striatal neuron autophagy and degeneration. Hum Mol Genet 10:1243-1254.
63. Reddy PH, Williams M, Charles V, Garrett L, Pike-Buchanan L, Whetsell WO Jr, Miller G, Tagle DA. 1998. Behavioural abnormalities and selective neuronal loss in HD transgenic mice expressing mutated full-length HD cDNA. Nat Genet 20:198-202.
64. Reiner A, Albin RL, Anderson KD, D'Amato CJ, Penney JB, Young AB. 1988. Differential loss of striatal projection neurons in Huntington disease. Proc Natl Acad Sci U S A 85:5733-5737.
65. Rockenstein E, Mallory M, Mante M, Sisk A, Masliah E. 2001. Early formation of mature amyloid-beta protein deposits in a mutant APP transgenic model depends on levels of Abeta(1-42). J Neurosci Res 66:573-582.
66. Roizin L, Stellar S, Liu JD. 1979. Neuronal nuclear-cytoplasmic changes in Huntington chorea: electron microscope investigations. In: Chase TN, Wexler NS, Barbeau A, editors. Advances in neurology: Huntington's disease. New York: Raven Press. p 95-122.
67. Sapp E, Ge P, Aizawa H, Bird E, Penney J, Young AB, Vonsattel JP, DiFiglia M. 1995. Evidence for a preferential loss of enkephalin immunoreactivity in the external globus pallidus in low grade Huntington's disease using high resolution image analysis. Neuroscience 64:397-404.
68. Saudou F, Finkbeiner S, Devys D, Greenberg ME. 1998. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95:55-66.
69. 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. 1999. Intranuclear inclusions and neuritic aggregates in transgenic mice expressing a mutant N-terminal fragment of huntingtin. Hum Mol Genet 8:397-407.
70. Smith MA, Brandt J, Shadmehr R. 2000. Motor disorder in Huntington's disease begins as a dysfunction in error feedback control. Nature 403:544-549.
71. Sotrel A, Paskevich PA, Kiely DK, Bird ED, Williams RS, Myers RH. 1991. Morphometric analysis of the prefrontal cortex in Huntington's disease. Neurology 41:1117-1123.
72. Suhr ST, Senut MC, Whitelegge JP, Faull KF, Cuizon DB, Gage FH. 2001. Identities of sequestered proteins in aggregates from cells with induced polyglutamine expression. J Cell Biol 153:283-294.
73. The Huntington's Disease Collaborative Research Group. 1993. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72:971-983.
74. Ungerstedt U. 1971. Stereotaxic mapping of the monoamine pathways in the rat brain. Acta Physiol Scand Suppl 367:1-48.
75. 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. 2000. 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 9:503-513.
76. Wszolek ZK, Markopoulou K. 1998. Olfactory dysfunction in Parkinson's disease. Clin Neurosci 5:94-101.
77. Yamamoto A, Lucas JJ, Hen R. 2000. Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 101:57-66.
78. Zeron MM, Hansson O, Chen N, Wellington CL, Leavitt BR, Brundin P, Hayden MR, Raymond LA. 2002. Increased sensitivity to N-methyl-D-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 33:849-860.
79. Zoghbi HY, Orr HT. 2000. Glutamine repeats and neurodegeneration. Annu Rev Neurosci 23:217-247.