Abnormal synaptic plasticity and impaired spatial cognition in mice transgenic for exon 1 of the human Huntington's disease mutation

Journal of Neuroscience

Volumn 20, Issue 13, 2000, Pages 5115-5123

  Murphy, Kerry P S J ^a,g   Carter, Rebecca J ^b   Lione, Lisa A ^c   Mangiarini, Laura ^d   Mahal, Amarbirpal ^e   Bates, Gillian P ^f   Dunnett, Stephen B ^g   Jennifer Morton, A ^a  

^a Department of Pharmacology ^*  (United Kingdom)

^b Centre for Brain Repair   (United Kingdom)

^c Parke Davis Neuroscience Research   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f OPEN UNIVERSITY   (United Kingdom)

^g CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Cognition; Hippocampus; Huntington's disease; Intranuclear inclusions; NMDA receptor; Long term depression; Long term potentiation

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL NUCLEUS INCLUSION BODY; COGNITION; DEPRESSION; HIPPOCAMPUS; HUNTINGTON CHOREA; LONG TERM POTENTIATION; MAZE TEST; MOUSE; MUTATION; NERVE CELL PLASTICITY; NERVE FIBER TRANSPORT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TRANSGENIC ANIMAL;

EID: 0034234519     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-13-05115.2000     Document Type: Article

References (62)

1. 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.
2. Biessels G-J, Kamal A, Urban IJA, Spruijt BM, Erkelens DW, Gispen WH (1998) Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: effects of insulin treatment. Brain Res 800:125-135.
3. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
4. Blitzer RD, Wong T, Nouranifar R, Iyengar R, Landau EM (1995) Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15:1403-1414.
5. Bortolotto ZA, Bashir ZI, Davies CH, Collingridge GL (1994) A molecular switch activated by mctabotropic glutamate receptors regulates induction of long-term potentiation. Nature 368:740-743.
6. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, Dunnett SB, Morion AJ (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 19:3248-3257.
7. Cha JHJ, 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 USA 95:6480-6485.
8. Chabot C, Massicotte G, Milot M, Trudeau F, Gagne J (1997) Impaired modulation of AMPA receptors by calcium-dependent processes in streptozotocin-induccd diabetic rats. Brain Res 768:249-256.
9. Chapman PF, White GL, Jones MW, Cooper Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276.
10. Chen NS, Luo T, Wellington C, Metzler M, McCutcheon K, Hayden MR, Raymond LA (1999) Subtype-specific enhancement of NMDA receptor currents by mutant Huntingtin. J Neurochem 72:1890-1898.
11. Cochilla AJ, Alford S (1999) NMDA receptor-mediated control of pre-synaptic calcium and neurotransmitter release. J Neurosci 19:193-205.
12. Collingridge GL, Kehl SJ, McLennan H (1983) Excitatory amino acids in synaptic transmission in the Schauer collateral-commissural pathway of the rat hippocampus. J Physiol (Lond) 334:33-46.
13. Davits SW, Turmaine M, Cozens BA, Raza AS, Mahal A, Mangiarini L, Bates GP (1999) From neuronal inclusions to neurodegeneration: neuropathological investigation of a transgenic mouse model of Hunlington's disease. Philos Trans R Soc Lond B Biol Sci 354:971-979.
14. 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.
15. DiFiglia M, Sapp E, Chase K, Schwarz C, Meloni A, Young C, Martin E, Vonsattel JP, Carraway R, Reeves SA, Boye FM, Aronin N (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14:1075-1081.
16. 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.
17. Dudek SM, Bear MF (1992) Homosynaptic long-term depression and effects of N-Methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 89:4363-4367.
18. Folstein SE (1990) Huntington's disease. Baltimore: John Hopkins University.
19. Foroud T, Siemers E, Kleindorfer D, Bill DJ, Hodes ME, Norton JA, Conneally PM, Christian JC (1995) Cognitive scores in carriers of Huntington's Disease gene compared to noncarriers. Ann Neurol 37:657-664.
20. Franceschi M, Cecchetto R, Minicucci F, Smizne S, Baio G, Canal N (1984) Cognitive processes in insulin-dependent diabetes. Diabetes Care 7:228-231.
21. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
22. Frey U, Matthies H, Reymann KG, Matthies H (1991) The effect of dopaminergic D1-rcceptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci Lett 129:111-114.
23. Gustafsson B, Wigstrom H, Abraham WC, Huang YY (1987) Long-term potentiation in the hippoeampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J Neurosci 7:774-780.
24. Gutekunst CA, Levey AI, Heilman CJ, Whaley WL, Yi H, Nash NR, Rees HD, Madden JJ, Hersch SM (1995) Identification and localization of huntingtin in brain and human lymphoblastoid cell lines with anti-fusion protein antibodies. Proc Natl Acad Sci USA 92:8710-8714.
25. 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.
26. Hanse E, Gustafsson B (1992) Long-term potentiation and field epsps in the lateral and medial perforant paths in the dentate gyrus in vitro: a comparison. Eur J Neurosci 4:1191-1201.
27. Harper PS (1996) Huntington's disease. Major problems in neurology, Vol 31, Ed 2. Philadelphia: W. B. Saunders.
28. 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.
29. Herrero I, Miras-Portugal MT, Sanchez-Pricto J (1992) Positive feedback of glutamate exocytosis by metabotropic presynaptic receptor stimulation. Nature 360:163-166.
30. Hodgson JG, Agopyan N, Gutekunst C-A, Leavitt BR, LePaine F, Singaraja R, Smith DJ, Bissada N, McCutcheon K, Nasir J, Jamot L, Li X-J, Stevens ME, Rosemond E, Rader JC, Phillips AG, Rubin EM, Hersch SM, Hayden MR (1999) A YAC mouse model for Huntington's disease with full-length mutant huntingtin. cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron 23:181-192.
31. Hurlbert MS, Zhou W, Wasmeier C, Kaddis FG, Hutton JC, Freed CR (1999) Mice transgenic for an expanded CAG repeat in the Huntington's disease gene develop diabetes. Diabetes 48:649-651.
32. Jenkins B, Koroshetz W, Beal M, Rosen B (1993) Evidence for impairment of energy metabolism in vivo in Huntington's disease using localized 1H NMR spectroscopy. Neurology 43:2689-2695.
33. Lange KW, Sahakian BJ, Quinn NP, Marsden CD, Robbins TW (1995) Comparison of executive and visuospatial memory function in Huntingtons disease and dementia of Alzheimer-type matched for degree of dementia. J Neurol Neurosurg Psychiatry 58:598-606.
34. Lawrence AD, Hodges JR, Rosser AE, Kershaw A, Ffrench-Constant C, Rubinsztein DC, Robbins TW, Sahakian BJ (1998) Evidence for specific cognitive deficits in preclinical Huntington's disease. Brain 121:1329-1341.
35. Lawrence AD, Sahakian BJ, Hodges JR, Rosser AE, Lange KW, Robbins TW (1996) Executive and mnemonic functions in early Huntington's disease. Brain 119:1633-1645.
36. Levine MS, Klapstein GJ, Koppel A, Gruen E, Cepeda C, Vargus ME, Jokel ES, Carpenter EM, Zanjani H, Hurst RS, Efstratiadis A, Zeitlin S, Chesselet M-F (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.
37. Lione LA, Carter RJ, Hunt MJ, Bates GP, Morton AJ, Dunnett SB (1999) Selective discrimination learning impairments in mice expressing the human Huntington's disease mutation. J Neurosci 19:10428-10437.
38. 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.
39. Mohr E, Brouwers P, Claus JJ, Mann UM, Fedio P, Chase TN (1991) Visuospatial cognition in Huntingtons disease. Mov Disord 6:127-132.
40. Morris R, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774-776.
41. Moser EI, Krobert KA, Moser MB, Morris RG (1998) Impaired spatial learning after saturation of long-term potentiation. Science 281:2038-2042.
42. Mulkey RM, Herron CE, Malenka RC (1993) An essential role for protein phosphatases in hippocampal long-term depression. Science 261:1051-1055.
43. Murphy KPSJ, Williams JH, Bettache N, Bliss TVP (1994) Photolytic release of nitric oxide modulates NMDA receptor transmission hut does not induce long-term potentiation. Neuropharmacology 33:1375-1385.
44. Murphy KPSJ, Bliss TVP (1999) Photolytically released nitric oxide produces a delayed but persistent suppression of LTP in area CA1 of the rat hippocampal slice. J Physiol (Lond) 515:453-462.
45. Nalbantogluet J, Tirado Santiago G, Lahsaini A, Poirier J, Goncalves O, Verge G, Momoli F, Welner SA, Massicotte G, Julien JP, Shapiro ML (1997) Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature 387:500-505.
46. Nosten-Bertrand M, Errington ML, Murphy KPSJ, Tokugawa Y, Barboni E, Kozlova E, Michalovich D, Morris RGM, Silver J, Stewart CL, Bliss TVP, Morris RJ (1996) Normal spatial learning despite regional inhibition of LTP in mice lacking Thy-1. Nature 379:826-829.
47. Ona V, Li MW, Vonsattel J, Andrews L, Khan S, Chung W, Frey A, Menon A, Li X, Stieg P, Yuan J, Penney J, Young AB, Cha JH, Friedlander RM (1999) Inhibition of caspase-1 slows disease progression in a mouse model of Huntington's disease. Nature 399:263-267.
48. Paulson HL, Fischbeck KH (1996) Trinucleotide repeats in neurogenetic disorders. Annu Rev Neurosci 19:79-107.
49. Perutz M (1999) Glutamine repeats and neurodegenerative diseases: molecular aspects. Trends Biochem Sci 24:58-63.
50. Reddy PH, Williams M, Charles V, Garrett L, Pike Buchanan L, Whetsell Jr WO, 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.
51. Reynolds DS, Carter RJ, Morton AJ (1998) Dopamine modulates the susceptibility of striatal neurons to 3-nitropropionic acid the rat model of Huntington's disease. J Neurosci 18:10116-10127.
52. Sanchezprieto J, Budd DC, Herrero I, Vazquez E, Nicholls DG (1996) Presynaptic receptors and the control of glutamate exocytosis. Trends Neurosci 19:235-239.
53. 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.
54. Scherzinger E, Sittler A, Schweiger K, Heiser V, Lurz R, Hasenbank R, Bates GP, Lehrach H, Wanker EE (1999) Self-assembly of polyglutamine-containing huntirigtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc Natl Acad Sci USA 96:4604-4609.
55. Schilling G, Becher MW, Sharp AH, Jinnah HA, Duan K, Kotsuk 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.
56. Sharp AH, Loev SJ, Schilling G, Li SH, Li XJ, Bao J, Wagster MV, Kolzuk JA, Steiner JP, Lo A (1995) Widespread expression of Huntington's disease gene (IT15) protein product. Neuron 14:1065-1074.
57. Shelbourne PF, Killeen N, Hevner RF, Johnston HM, Tecott L, Lewandoski M, Ennis M, Ramirez L, Li Z, Iannicola C, Littman DR, Myers RM (1999) A Huntington's disease CAG expansion at the murine Hdh locus is unstable and associated with behavioural abnormalities in mice. Hum Mol Genet 8:763-774.
58. Spargo E, Everall IP, Lantos PL (1993) Neuronal loss in the hippocampus in Huntington's disease: a comparison with HIV infection. J Neurol Neurosurg Psychiatry 56:487-491.
59. Stewart CA, Morris RGM (1993) The watermaze. In: Behavioural neuroscience: a practical approach (Shagal A, ed), pp 107-122. Oxford: IRL.
60. Usdin MT, Shelbourne PF, Myers RM, Madison DV (1999) Impaired synaptic plasticity in mice carrying the Huntington's disease mutation. Hum Mol Genet 8:839-846.
61. Utal AK, Stopka AL, Roy M, Coleman PD (1998) PEP-19 immunohistoehemistry defines the basal ganglia and associated structures in the adult human brain, and is dramatically reduced in Huntington's disease. Neuroscience 86:1055-1063.
62. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP (1985) Neuropathological classification of Huntington's Disease. J Neuropathol Exp Neurol 44:559-577.