Abnormal APP, cholinergic and cognitive function in Ts65Dn Down's model mice

Experimental Neurology

Volumn 193, Issue 2, 2005, Pages 469-480

  Seo, Hyemyung ^a   Isacson, Ole ^a  

^a MCLEAN HOSPITAL   (United States)

Author keywords

APP processing; Cholinergic transmission; Cognition; Muscarinic agonist; NGF expression; Septohippocampal function

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLINE ACETYLTRANSFERASE; MUSCARINIC M1 RECEPTOR AGONIST; NERVE GROWTH FACTOR;

AGE DETERMINATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; COGNITION; CONTROLLED STUDY; DOWN SYNDROME; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; MAZE TEST; MOUSE; MOUSE STRAIN; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION;

EID: 18244388693     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.11.017     Document Type: Article

References (68)

1. X. Altafaj, M. Dierssen, C. Baamonde, E. Marti, J. Visa, J. Guimera, M. Oset, J.R. Gonzalez, J. Florez, C. Fillat, and X. Estivill Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome Hum. Mol. Genet. 10 2001 1915 1923
2. F. Asztely, M. Kokaia, K. Olofsdotter, U. Ortegren, and O. Lindvall Afferent-specific modulation of short-term synaptic plasticity by neurotrophins in dentate gyrus Eur. J. Neurosci. 12 2000 662 669
3. R.T. Bartus, and D.F. Emerich Cholinergic markers in Alzheimer disease JAMA 282 1999 2208 2209
4. F. Baskin, R.N. Rosenberg, L. Iyer, L. Hynan, and C.M. Cullum Platelet APP isoform ratios correlate with declining cognition in AD Neurology 54 2000 1907 1909
5. L. Becker, T. Mito, S. Takashima, and K. Onodera Growth and development of the brain in Down syndrome Prog. Clin. Biol. Res. 373 1991 133 152
6. J. Berger-Sweeney, D.L. McPhie, J.A. Arters, J. Greenan, M.L. Oster-Granite, and R.L. Neve Impairments in learning and memory accompanied by neurodegeneration in mice transgenic for the carboxyl-terminus of the amyloid precursor protein Brain Res. Mol. Brain Res. 66 1999 150 162
7. H.A. Bimonte, A.C. Granholm, H. Seo, and O. Isacson Spatial memory testing decreases hippocampal amyloid precursor protein in young, but not aged, female rats Neurosci. Lett. 328 2002 50 54
8. H.A. Bimonte-Nelson, C.L. Hunter, M.E. Nelson, and A.C. Granholm Frontal cortex BDNF levels correlate with working memory in an animal model of Down syndrome Behav. Brain Res. 139 2003 47 57
9. S.E. Browne, L. Lin, A. Mattsson, B. Georgievska, and O. Isacson Selective antibody-induced cholinergic cell and synapse loss produce sustained hippocampal and cortical hypometabolism with correlated cognitive deficits Exp. Neurol. 170 2001 36 47
10. S. Capsoni, G. Ugolini, A. Comparini, F. Ruberti, N. Berardi, and A. Cattaneo Alzheimer-like neurodegeneration in aged antinerve growth factor transgenic mice Proc. Natl. Acad. Sci. U. S. A. 97 2000 6826 6831
11. S. Capsoni, S. Giannotta, and A. Cattaneo Beta-amyloid plaques in a model for sporadic Alzheimer's disease based on transgenic anti-nerve growth factor antibodies Mol. Cell. Neurosci. 21 2002 15 28
12. S. Capsoni, S. Giannotta, and A. Cattaneo Nerve growth factor and galantamine ameliorate early signs of neurodegeneration in anti-nerve growth factor mice Proc. Natl. Acad. Sci. U. S. A. 99 2002 12432 12437
13. M.F. Casanova, L.C. Walker, P.J. Whitehouse, and D.L. Price Abnormalities of the nucleus basalis in Down's syndrome Ann. Neurol. 18 1985 310 313
14. J.D. Cooper, A. Salehi, J.D. Delcroix, C.L. Howe, P.V. Belichenko, J. Chua-Couzens, J.F. Kilbridge, E.J. Carlson, C.J. Epstein, and W.C. Mobley Failed retrograde transport of NGF in a mouse model of Down's syndrome: reversal of cholinergic neurodegenerative phenotypes following NGF infusion Proc. Natl. Acad. Sci. U. S. A. 98 2001 10439 10444
15. K.A. Crutcher, S.A. Scott, S. Liang, W.V. Everson, and J. Weingartner Detection of NGF-like activity in human brain tissue: increased levels in Alzheimer's disease J. Neurosci. 13 1993 2540 2550
16. M. Davisson, C. Schmidt, R. Reeves, N. Irving, E. Akeson, B. Harris, and R. Bronson Segmental trisomy as a model for Down syndrome and other aneuploid conditions The Phenotypic Mapping of Down Syndrome and Other Aneuploid Conditions 1993 Wiley-Liss New York 117 133
17. G.E. Demas, R.J. Nelson, B.K. Krueger, and P.J. Yarowsky Spatial memory deficits in segmental trisomic Ts65Dn mice Behav. Brain Res. 82 1996 85 92
18. M. Dierssen, I.F. Vallina, C. Baamonde, M.A. Lumbreras, C. Martinez-Cue, S.G. Calatayud, and J. Florez Impaired cyclic AMP production in the hippocampus of a Down syndrome murine model Brain Res. Dev. Brain Res. 95 1996 122 124
19. M. Dierssen, I.F. Vallina, C. Baamonde, S. Garcia-Calatayud, M.A. Lumbreras, and J. Florez Alterations of central noradrenergic transmission in Ts65Dn mouse, a model for Down syndrome Brain Res. 749 1997 238 244
20. S.G. Dorsey, L.L. Bambrick, R.J. Balice-Gordon, and B.K. Krueger Failure of brain-derived neurotrophic factor-dependent neuron survival in mouse trisomy 16 J. Neurosci. 22 2002 2571 2578
21. C.J. Epstein Developmental genetics Experientia 42 1986 1117 1128
22. M. Fahnestock, S.A. Scott, N. Jette, J.A. Weingartner, and K.A. Crutcher Nerve growth factor mRNA and protein levels measured in the same tissue from normal and Alzheimer's disease parietal cortex Brain Res. Mol. Brain Res. 42 1996 175 178
23. M. Fahnestock, D. Garzon, R.M. Holsinger, and B. Michalski Neurotrophic factors and Alzheimer's disease: are we focusing on the wrong molecule? J. Neural Transm. 2002 241 252
24. F. Fonnum A rapid and sensitive method for the determination of choline acetyltransferase J. Neurochem. 24 1975 407 409
25. S.J. French, T. Humby, C.H. Horner, M.V. Sofroniew, and M. Rattray Hippocampal neurotrophin and trk receptor mRNA levels are altered by local administration of nicotine, carbachol and pilocarpine Brain Res. Mol. Brain Res. 67 1999 124 136
26. D. Garzon, G. Yu, and M. Fahnestock A new brain-derived neurotrophic factor transcript and decrease in brain-derived neurotrophic factor transcripts 1, 2 and 3 in Alzheimer's disease parietal cortex J. Neurochem. 82 2002 1058 1064
27. M. Goedert, A. Fine, S.P. Hunt, and A. Ullrich Nerve growth factor mRNA in peripheral and central rat tissues and in the human central nervous system: lesion effects in the rat brain and levels in Alzheimer's disease Brain Res. 387 1986 85 92
28. A.C. Granholm, L.A. Sanders, and L.S. Crnic Loss of cholinergic phenotype in basal forebrain coincides with cognitive decline in a mouse model of Down's syndrome Exp. Neurol. 161 2000 647 663
29. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356
30. C. Hock, S. Golombowski, F. Muller-Spahn, W. Naser, K. Beyreuther, U. Monning, D. Schenk, C. Vigo-Pelfrey, A.M. Bush, R. Moir, R.E. Tanzi, J.H. Growdon, and R.M. Nitsh Cerebrospinal fluid levels of amyloid precurser protein and amyloid β-peptide in Alzheimer's disease and major depression-inverse correlation with dementia severity Eur. Neurol. 39 1998 111 118
31. R.M. Holsinger, J. Schnarr, P. Henry, V.T. Castelo, and M. Fahnestock Quantitation of BDNF mRNA in human parietal cortex by competitive reverse transcription-polymerase chain reaction: decreased levels in Alzheimer's disease Brain Res. Mol. Brain Res. 76 2000 347 354
32. D.M. Holtzman, Y. Li, S.J. Dearmond, M.P. McKinley, F.H. Gage, C.J. Epstein, and W.C. Mobley Mouse model of neurodegeneration: Atrophy of basal forebrain cholinergic neurons in trisomy 16 transplants Proc. Natl. Acad. Sci. U. S. A. 89 1992 1383 1387
33. D.M. Holtzman, D. Santucci, J. Kilbridge, J. Chua-Couzens, D.J. Fontana, S. Danies, R.M. Johnson, K. Chen, Y. Sun, E. Carlson, E. Alleva, C. Epstein, and W.C. Mobley Developmental abnormalities and aged-related neurodegeneration in a mouse model of Down syndrome Proc. Natl. Acad. Sci. U. S. A. 93 1996 13333 13338
34. C.L. Hunter, H.A. Bimonte, and A.C. Granholm Behavioral comparison of 4 and 6 month-old Ts65Dn mice: age-related impairments in working and reference memory Behav. Brain Res. 138 2003 121 131
35. L.A. Hyde, and L.S. Crnic Age-related deficits in context discrimination learning in Ts65Dn mice that model Down syndrome and Alzheimer's disease Behav. Neurosci. 115 2001 1239 1246
36. O. Isacson, H. Seo, L. Lin, D. Albeck, and A.C. Granholm Alzheimer's disease and Down's syndrome: roles of APP, trophic factors and ACh Trends Neurosci. 25 2002 79 84
37. E. Jensen, and H. Gundersen The rotator J. Microsc. 170 1993 35 44
38. F. Kamenetz, T. Tomita, H. Hsieh, G. Seabrook, D. Borchelt, T. Iwatsubo, S. Sisodia, and R. Malinow APP processing and synaptic function Neuron 37 2003 925 937
39. W.E. Kaufmann, and H.W. Moser Dendritic anomalies in disorders associated with mental retardation Cereb. Cortex 10 2000 981 991
40. M.A. Kurt, D.C. Davies, M. Kidd, M. Dierssen, and J. Florez Synaptic deficit in the temporal cortex of partial trisomy 16 (Ts65Dn) mice Brain Res. 858 2000 191 197
41. C.J. LeBlanc, T.W. Deacon, B.R. Whatley, J. Dinsmore, L. Lin, and O. Isacson Morris water maze analysis of 192-IgG-saporin-lesioned rats and porcine cholinergic transplants to the hippocampus Cell Transplant 8 1999 131 142
42. L. Lin, C. Leblanc, T. Deacon, and O. Isacson Chronic cognitive deficits and amyloid precursor protein elevation after immunotoxin lesions of the basal forebrain cholinergic system NeuroReport 9 1998 547 552
43. L. Lin, A. Gjorgijevska, A. Mattsson, and O. Isacson Cognitive changes and modified processing of amyloid precursor protein in the cortical and hippocampal system after cholinergic synapse loss and muscarinic receptor activation Proc. Natl. Acad. Sci. U. S. A. 96 1999 12108 12113
44. D. Liu, J. Diorio, J.C. Day, D.D. Francis, and M.J. Meaney Maternal care, hippocampal synaptogenesis and cognitive development in rats Nat. Neurosci. 3 2000 799 806
45. A.R. Massaro, C. Soranzo, E. Bigon, S. Battiston, A. Morandi, A. Carnevale, and L. Callegaro Nerve growth factor (NGF) in cerebrospinal fluid (CSF) from patients with various neurological disorders Ital. J. Neurol. Sci. 15 1994 105 108
46. M.P. Mattson, and K. Furukawa Signaling events regulating the neurodevelopmental triad. Glutamate and secreted forms of beta-amyloid precursor protein as examples Perspect. Dev. Neurobiol. 5 1998 337 352
47. E.J. Mufson, J.M. Conner, and J.H. Kordower Nerve growth factor in Alzheimer's disease: defective retrograde transport to nucleus basalis NeuroReport 6 1995 1063 1066
48. E.J. Mufson, J.S. Kroin, Y.T. Liu, T. Sobreviela, R.D. Penn, J.A. Miller, and J.H. Kordower Intrastriatal and intraventricular infusion of brain-derived neurotrophic factor in the cynomologous monkey: distribution, retrograde transport and co-localization with substantia nigra dopamine-containing neurons Neuroscience 71 1996 179 191
49. E.J. Mufson, N. Lavine, S. Jaffar, J.H. Kordower, R. Quirion, and H.U. Saragovi Reduction in p140-TrkA receptor protein within the nucleus basalis and cortex in Alzheimer's disease Exp. Neurol. 146 1997 91 103
50. J.M. Palacios, G. Bolliger, A. Closse, A. Enz, G. Gmelin, and J. Malanowski The pharmacological assessment of RS 86 (2-ethyl-8-methyl-2,8- diazaspiro-[4,5]-decan-1,3-dion hydrobromide). A potent, specific muscarinic acetylcholine receptor agonist Eur. J. Pharmacol. 125 1986 45 62
51. F.R. Poulsen, H. Jahnsen, M. Blaabjerg, and J. Zimmer Pilocarpine-induced seizure-like activity with increased BNDF and neuropeptide Y expression in organotypic hippocampal slice cultures Brain Res. 950 2002 103 118
52. R.H. Reeves, N.G. Irving, T.H. Moran, A. Wohn, C. Kitt, S.S. Sisodia, C. Schmidt, R.T. Bronson, and M.T. Davisson A mouse model for Down syndrome exhibits learning and behaviour deficits Nat. Genet. 11 1995 177 184
53. S. Rossner, U. Ueberham, R. Schliebs, J. Perez-Polo, and V. Bigl The regulation of amyloid precursor protein metabolism by cholinergic mechanism and neurotrophin receptor signaling Prog. Neurol. 56 1998 541 569
54. N.M.J. Rupniak, S.J. Tye, and S.D. Iversen Comparison of the effects of selective and nonselective muscarinic agonist on cognition and thermoregulation in primates J. Neurol. Sci. 110 1992 222 227
55. A. Salehi, J. Verhaagen, and D.F. Swaab Neurotrophin receptors in Alzheimer's disease Prog. Brain Res. 117 1998 71 89
56. H.E. Scharfman, A.L. Sollas, K.L. Smith, M.B. Jackson, and J.H. Goodman Structural and functional asymmetry in the normal and epileptic rat dentate gyrus J. Comp. Neurol. 454 2002 424 439
57. S.A. Scott, E.J. Mufson, J.A. Weingartner, K.A. Skau, and K.A. Crutcher Nerve growth factor in Alzheimer's disease: increased levels throughout the brain coupled with declines in nucleus basalis J. Neurosci. 15 1995 6213 6221
58. H. Seo, A.W. Ferree, and O. Isacson Cortico-hippocampal APP and NGF levels are dynamically altered by cholinergic muscarinic antagonist or M1 agonist treatment in normal mice Eur. J. Neurosci. 15 2002 498 506
59. J.G. Sheng, D.L. Price, and V.E. Koliatsos Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Abeta amyloidosis J. Neurosci. 22 2002 9794 9799
60. R.J. Siarey, J. Stoll, S.I. Rapoport, and Z. Galdzicki Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down syndrome Neuropharmacology 36 1997 1549 1554
61. S. Takashima, K. Iida, T. Mito, and M. Arima Dendritic and histochemical development and ageing in patients with Down's syndrome J. Intellect. Disabil. Res. 38 Pt. 3 1994 265 273
62. D. Van Gool, B. De Strooper, F. Van Leuven, and R. Dom Amyloid precursor protein accumulation in Lewy body dementia and Alzheimer's disease Dementia 6 1995 63 68
63. F. Wanibuchi, T. Konishi, M. Harada, M. Terai, K. Hidaka, T. Tamura, S.-i. Tsukamoto, and S. Usuda Pharmacological studies on novel muscarinic agonists, 1-oxa-8-azaspiro[4.5]decane derivatives, YM 796 and YM954 Eur. J. Pharmacol. 187 1990 479 486
64. R.L. West, J.M. Lee, and L.E. Maroun Hypomethylation of the amyloid precursor protein gene in the brain of an Alzheimer's disease patient J. Mol. Neurosci. 6 1995 141 146
65. H.M. Wisniewski, and A. Rabe Discrepancy between Alzheimer-type neuropathology and dementia in persons with Down's syndrome Ann. N. Y. Acad. Sci. 477 1986 247 260
66. K. Wisniewski, H. Wisniewski, and G. Wen Occurrence of neuropathological changes and dementia of Alzheimer's disease in Down's syndrome Ann. Neurol. 17 1985 278
67. C.M. Yates, J. Simpson, A. Gordon, A.F. Maloney, Y. Allison, I.M. Ritchie, and A. Urquhart Catecholamines and cholinergic enzymes in pre-senile and senile Alzheimer-type dementia and Down's syndrome Brain Res. 280 1983 119 126
68. C. Zettler, D.C. Bridges, X.F. Zhou, and R.A. Rush Detection of increased tissue concentrations of nerve growth factor with an improved extraction procedure J. Neurosci. Res. 46 1996 581 594