Mouse models of Alzheimer's disease: The long and filamentous road

Neurological Research

Volumn 25, Issue 6, 2003, Pages 590-600

  Phinney, Amie L ^a   Horne, Patrick ^a   Yang, Jing ^a   Janus, Chris ^a   Bergeron, Catherine ^a,b   Westaway, David ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

A ; Amyloid cascade hypothesis; Plaques; Tangles; Tau; Transgenic

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; CONTROLLED STUDY; DEMENTIA; GENE MUTATION; MEMORY DISORDER; MOUSE; NEUROFIBRILLARY TANGLE; NONHUMAN; PROTEIN PHOSPHORYLATION; REVIEW; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; MICE; MICE, TRANSGENIC; NEUROFIBRILLARY TANGLES; TAU PROTEINS;

EID: 0042888866     PISSN: 01616412     EISSN: None     Source Type: Journal    
DOI: 10.1179/016164103101202020     Document Type: Review

References (122)

1. Arriagada PV, Growdon JH, Hedley-Whyte ET, Hyman BT. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's Disease. Neurology 1992; 42: 631-639
2. McLean CA, et al. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 1999; 46: 860-866
3. Wang J, Dickson DW, Trojanowski JQ, Lee VM. The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging. Exp Neurol 1999; 158: 328-337
4. Lue LF, et al. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 1999; 155: 853-862
5. Beach TG, et al. The cholinergic deficit coincides with Abeta deposition at the earliest histopathologic stages of Alzheimer disease. J Neuropathol Exp Neurol 2000; 59: 308-313
6. Dooley M, Lamb HM. Donepezil: A review of its use in Alzheimer's disease. Drugs Aging 2000; 16: 199-226
7. Citron M, et al. Mutation of the B-amyloid precursor protein in familial Alzheimer's Disease increases B-protein production. Nature 1992; 360: 672-674
8. Johnston JA, et al. Increased beta-amyloid release and levels of amyloid precursor protein (APP) in fibroblast cell lines from family members with the Swedish Alzheimer's disease APP670/671 mutation. FEBS Lett 1994; 354: 274-278
9. Suzuki N, et al. An increased percentage of long amyloid B protein secreted by Familial Amyloid β Protein Precursor (βAPP717) mutants. Science 1994; 264: 1336-1340
10. Thinakaran G, Teplow DB, Siman R, Greenberg B, Sisodia SS. Metabolism of the 'Swedish' amyloid precursor protein variant in neuro2a (N2a) cells. Evidence that cleavage at the 'beta-secretase' site occurs in the golgi apparatus. J Biol Chem 1996; 271: 9390-9397
11. Nilsberth C, et al. The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation. Nat Neurosci 2001; 4: 887-893
12. Scheuner D, et al. Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat Med 1996; 2: 864-870
13. Duff K, et al. Increased amyloid-β42(43) in brains of mice expressing presenilin 1. Nature 1996; 383: 710-713
14. Borchelt DR, et al. Familial Alzheimer's disease-linked presenilin 1 variants elevate Aβ 1-42/1-40 ratio in vitro and in vivo. Neuron 1996; 17: 1005-1013
15. Citron M, et al. Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid β-protein in both transfected cells and transgenic mice. Nat Med 1997; 3: 67-72
16. De Stroooper B, et al. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 1998; 391: 387-390
17. De Strooper B, et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain [see comments]. Nature 1999; 398: 518-522
18. Chen F, et al. Carboxyl-terminal fragments of Alzheimer beta-amyloid precursor protein accumulate in restricted and unpredicted intracellular compartments in presenilin 1-deficient cells. J Biol Chem 2000; 275: 36794-36802
19. Weihofen A, Binns K, Lemberg MK, Ashman K, Martoglio B. Identification of signal peptidepeptidase, a presenilin-type aspartic protease. Science 2002; 296: 2215-2218
20. Ertekin-Taner N, et al. Linkage of plasma Abeta42 to a quantitative locus on chromosome 10 in late-onset Alzheimer's disease pedigrees. Science 2000; 290: 2303-2304
21. Hardy JA, Higgins GA. The amyloid cascade hypothesis. Science 1992; 256: 184-185
22. Jarrett JT, Berger EP, Lansbury PT Jr. The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: Implications for the pathogenesis of Alzheimer's disease. Biochemistry 1993; 32: 4693-4697
23. Stine WB Jr, et al. The nonometer-scale structure of amyloid-beta visualized by atomic force microscopoy. J Protein Chem 1996; 15: 193-203
24. Lambert MP, et al. Diffusible, nonfibrillar ligands derived from Abeta 1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 1998; 95: 6448-6453
25. Walsh DM, et al. Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 1999; 274: 25945-25952
26. Tjernberg LO, et al. Amyloid beta-peptide polymerization studied using fluorescence correlation spectroscopy. Chem Biol 1999; 6: 53-62
27. Rober AE, et al. Oligomerization and fibril assembly of the amyloid-beta protein. Biochim Biophys Acta 2000; 1502: 31-43
28. Parvathy S, et al. Correlation between Abetax-40-, Abetax-42-, and Abetax-43-containing amyloid plaques and cognitive decline. Arch Neurol 2001; 58: 2025-2032
29. Crook R, et al. A variant of Alzheimer's disease with spastic paraparesis and unusual plaques due to deletion of exon 9 of presenilin. Nature Med 1998; 4: 452-455
30. Teller JK, et al. Presence of soluble amyloid beta-peptide precedes amyloid plaque formation in Down's syndrome. Nat Med 1996; 2: 93-95
31. Hutton M, et al. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998; 393: 702-705
32. Goedert M, Crowther RA, Spillantini MG. Tau mutations cause frontotemporal dementias. Neuron 1998; 21: 955-958
33. Poorkaj P, et al. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 1998; 43: 815-825
34. Spillantini MG, et al. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA 1998; 95: 7737-7741
35. Polymeropoulos M, et al. Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 1997; 276: 2045-2047
36. Ueda K, et al. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc Natl Acad Sci USA 1993; 90: 11282-11286
37. von Koch CS, et al. Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol Aging 1997; 18: 661-669
38. White AR, et al. Copper levels are increased in the cerebral cortex and liver of APP and APLP2 knockout mice. Brain Res 1999; 842: 439-444
39. Martson MP, et al. Evidence for excitoprotective and intra-neuronal calcium-regulating roles for secreted forms of the beta-amyloid precursor protein. Neuron 1993; 10: 243-254
40. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS. Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 2001; 414: 643-648
41. Janus C, Chishti MA, Westaway D. Transgenic mouse models of Alzheimer's disease. BBA 2000; 1502: 63-75
42. Games D, et al. Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein [see comments]. Nature 1995; 373: 523-527
43. Hsiao KH, et al. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 1996; 274: 99-102
44. Sturchler-Pierrat C, et al. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA 1997; 94: 13287-13292
45. Moechars D, et al. Early phenotype changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem 1999; 274: 6483-6492
46. Kulnane LS, Lamb BT. Neuropathological characterization of mutant amyloid precursor protein yeast artificial chromosome transgenic mice. Neurobiol Dis 2001; 8: 982-992
47. Hsiao KK, et al. Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron 1995; 15: 1203-1218
48. Carlson GA, et al. Genetic modification of the phenotypes produced by amyloid precursor protein overexpression in transgenic mice. Hum Mol Genet 1997; 6: 1951-1959
49. Multhaup G, et al. The amyloid precursor protein of Alzheimer's disease in the reduction of Copper (II) to Copper (I). Science 1996; 271: 1406-1409
50. Barnham KJ, et al. Structure of the Alzheimer's disease amyloid precursor protein copper binding domain: A regulator of neuronal copper homeostasis. J Biol Chem 2003; 278: 17401-17407
51. Maynard CJ, et al. Overexpression of Alzheimer's disease amyloid-beta opposes the age-dependent elevations of brain copper and iron. J Biol Chem 2002; 277: 44670-44676
52. Bayer T, et al. Dietary Cu rescues premature death, stabilizes brain SOD-1 activity and rescues amyloid Aβ production in APP23 transgenic mice. Submitted
53. Phinney AL, et al. In vivo reduction of Aβ by a mutant CuATPAse7b copper transporter. Submitted
54. Lu DC, et al. A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor [see comments]. Nat Med 2000; 6: 397-404
55. Hsia AY, et al. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 1999; 96: 3228-3233
56. Winkler DT, et al. Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci 2001; 21: 1619-1627
57. Holtzman DM, et al. Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 2000; 97: 2892-2897
58. Irizarry MC, et al. Apolipoprotein E affects the amount, form, and anatomical distribution of amyloid beta-peptide deposition in homozygous APP(V717F) transgenic mice. Acta Neuropathol (Berl) 2000; 100: 451-458
59. Buttini M, et al. Modulation of Alzheimer-like synaptic and Cholinergic deficits in transgenic mice by human apolipoprotein E depends on isoform, aging, and overexpression of amyloid beta peptides but not on plaque formation. J Neurosci 2002; 22: 10539-10548
60. Corder EH, et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993; 261: 921-923
61. Kuo YM, et al. Comparative analysis of amyloid-beta chemical structure and amyloid plaque morphology of transgenic mouse and alzheimer's disease brains. J Biol Chem 2001; 276: 12991-12998
62. Kalback W, et al. APP transgenic mice Tg2576 accumulate Abeta peptides that are distinct from the chemically modified and insoluble peptides deposited in Alzheimer's disease senile plaques. Biochemistry 2002; 41: 922-928
63. Suh SW, et al. Histochemically-reactive zinc in amyloid plaques, angiopathy, and degenerating neurons of Alzheimer's diseased brains. Brain Res 2000; 852: 274-278
64. Lee JY, Cole TB, Palmiter RD, Suh SW, Koh JY. Contribution by synaptic zinc to the gender-disparate plaque formation in human Swedish mutant APP transgenic mice. Proc Natl Acad Sci USA 2002; 99: 7705-7710
65. Kampers T, Pangalos M, Geerts H, Wiech H, Mandelkow E. Assembly of paired helical filaments from mouse tau: Implications for the neurofibrillary pathology in transgenic mouse models for Alzheimer's disease. FEBS Lett 1999; 451: 39-44
66. Lewis J, et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 2000; 25: 402-405
67. Calhoun ME, et al. Neuron loss in APP transgenic mice. Nature 1998; 395: 755-756
68. Chishti MA, et al. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 2001; 276: 21562-21570
69. Kelly PH, et al. Progressive age-related impairment of cognitive behavior in APP23 transgenic mice. Neurobiol Aging 2003; 24: 365-378
70. Chapman PF, et al. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 1999; 2: 271-276
71. Mucke L, et al. High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation [In Process Citation]. J Neurosci 2000; 20: 4050-4058
72. Dewachter I, et al. Neuronal deficiency of presenilin 1 inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V717I] transgenic mice. J Neurosci 2002; 22: 3445-3453
73. Janus C, et al. Aβ-Immunization reduces behavioural impairment and dense-cored plaques in a model of Alzheimer's disease. Nature 2000; 408: 979-982
74. Kotilinek LA, et al. Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J Neurosci 2002; 22: 6331-6335
75. Morgan D, et al. A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 2000; 408: 982-985
76. Dodart JC, et al. Behavioral disturbances in transgenic mice overexpressing the V717F beta-amyloid precursor protein. Behav Neurosci 1999; 113: 982-990
77. Schenk D, et al. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PD-APP mouse [In Process Citation]. Nature 1999; 400: 173-177
78. Weiner HL, et al. Nasal administration of amyloid-beta peptide decreases cerebral amyloid burden in a mouse model of Alzheimers disease. Ann Neurol 2000; 48: 567-579
79. Bacskai BJ, et al. Imaging of amyloid-beta deposits in brains of living mice permits direct observation of clearance of plaques with immunotherapy. Nat Med 2001; 7: 369-372
80. Das P, Murphy MP, Younkin LH, Younkin SG, Golde TE. Reduced effectiveness of Abeta 1-42 immunization in APP transgenic mice with significant amyloid deposition. Neurobiol Aging 2001; 22: 721-727
81. Nicoll JA, et al. Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: A case report. Nat Med 2001; 9: 448-452
82. Dodart JC, et al. Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat Neurosci 2002; 5: 452-457 83
83. Weggen S, et al. A subset of NSAIDs lower amyloidogenic Abeta42 independently of cyclooxygenase activity. Nature 2001; 414: 212-216
84. Refolo LM, et al. A cholesterol-lowering drug reduces beta-amyloid pathology in a transgenic mouse model of Alzheimer's disease. Neurobiol Dis 2001; 8: 890-899
85. Cherny RA, et al. Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 2001; 30: 665-676
86. Dovey HF, et al. Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J Neurochem 2001; 76: 173-181
87. Permanne B, et al. Reduction of amyloid load and cerebral damage in a transgenic mouse model of Alzheimer's disease by treatment with a beta-sheet breaker peptide. Faseb J 2002; 16: 860-862
88. Götz J, et al. Somatodendritic localization and hyper-phosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. Embo J 1995; 14: 1304-1313
89. Spittaels K, et al. Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 1999; 155: 2153-2165
90. Probst A, et al. Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol (Berl) 2000; 99: 469-481
91. Brion JP, Tremp G, Octave JN. Transgenic expression of the shortest human tau affects its compartmentalization and its phosphorylation as in the pretangle stage of Alzheimer's disease. Am J Pathol 1999; 154: 255-270
92. Ishihara T, et al. Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice. Am J Pathol 2001; 158: 555-562
93. Duff K, et al. Characterization of pathology in transgenic mice over-expressing human genomic and cDNA tau transgenes. Neurobiol Dis 2000; 7: 87-98
94. Götz J, Chen F, Barmettler R, Nitsch RM. Tau filament formation in transgenic mice expressing P301L tau. J Biol Chem 2001; 276: 529-534
95. Higuchi M, et al. Transgenic mouse model of tauopathies with glial pathology and nervous system degeneration. Neuron 2002; 35: 433
96. Gotz J. Tau and transgenic animal models. Brain Res Rev 2002; 35: 266-286
97. Ahlijanian MK, et al. Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc Natl Acad Sci USA 2000; 97: 2910-2915
98. Spittaels K, et al. Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J Biol Chem 2000; 275: 41340-41349
99. Tesseur I, et al. Expression of human apolipoprotein E4 in neurons causes hyper-phosphorylation of protein tau in the brains of transgenic mice. Am J Pathol 2000; 156: 951-964
100. Alonso A, Zaidi T, Novak M, Grundke-Iqbal I, Iqbal K. Hyper-phosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc Natl Acad Sci USA 2001; 98: 6923-6928
101. Schweers O, Mandelkow AM, Biernat J, Mandelkow E. Oxidation of cysteine-322 in the repeat domain of microtubule-associated protein tau controls the in vitro assembly of paired helical filaments. Proc Natl Acad Sci USA 1995; 92: 8463-8467
102. Wille H, Drewes G, Biernat J, Mandelkow EM, Mandelkow E. Alzheimer-like paired helical filaments and antiparallel dimers formed from microtubule-associated protein tau in vitro. J Cell Biol 1992; 118: 573-584
103. Schweers O, Schonbrunn-Hanebeck E, Marx A, Mandelkow E. Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure. J Biol Chem 1994; 269: 24290-24297
104. von Bergen M, et al. Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif ((306)VQIVYK(311)) forming beta structure. Proc Natl Acad Sci USA 2000; 97: 5129-5134
105. von Bergen M, et al. Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local beta-structure. J Biol Chem 2001; 276: 48165-48174
106. Sadqi M, et al. Alpha-helix structure in Alzheimer's disease aggregates of tau-protein. Biochemistry 2002; 41: 7150-7155
107. Carmel G, Mager EM, Binder LI, Kuret J. The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J Biol Chem 1996; 271: 32789-32795
108. Jicha GA, Bowser R, Kazam IG, Davies P. Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J Neurosci Res 1997; 48: 128-132
109. Jicha GA, et al. A conformation- and phosphorylation-dependent antibody recognizing the paired helical filaments of Alzheimer's disease. J Neurochem 1997; 69: 2087-2095
110. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82: 239-259
111. Weaver CL, Espinoza M, Kress Y, Davies P. Conformational change as one of the earliest alterations of tau in Alzheimer's disease. Neurobiol Aging 2000; 21: 719-727
112. Hsiao K, et al. Mutant prion proteins in Gerstmann-Strä ussler-Scheinker disease with neurofibrillary tangles. Nat Genet 1992; 1: 68-71
113. Ghetti B, et al. Vascular variant of prion protein cerebral amyloidosis with τ-positive neurofibrillary tangles: The phenotype of a stop codon 145 mutation in PRNP. Proc Natl Acad Sci USA 1996; 93: 744-748
114. Vidal R, et al. A stop-codon mutation in the BRI gene associated with familial British dementia. Nature 1999; 399: 776-781
115. Lorenzo A, et al. Amyloid beta interacts with the amyloid precursor protein: A potential toxic mechanism in Alzheimer's disease. Nat Neurosci 2000; 3: 460-464
116. Van Uden E, et al. Increased extracellular amyloid deposition and neurodegeneration in human amyloid precursor protein transgenic mice deficient in receptor-associated protein. J Neurosci 2002; 22: 9298-9304
117. Ji ZS, et al. Apolipoprotein E4 potentiates amyloid beta peptide-induced lysosomal leakage and apoptosis in neuronal cells. J Biol Chem 2002; 277: 21821-21828
118. Yu G, Chen F, Levesque G, Fraser PE, St George Hyslop P. Presenilins form protein complexes which include beta-catenin. J Biol Chem 1998; 273: 16470-16475
119. Nishimura M, et al. Presenilin mutations associated with Alzheimer disease cause defective intracellular trafficking of beta-catenin, a component of the presenilin protein complex [see comments]. Nat Med 1999; 5: 164-169
120. Lewis J, et al. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001; 293: 1487-1491
121. Götz J, Chen F, Barmettler R, Nitsch RM. Tau filament formation in transgenic mice expressing P30/L tau. J Biol Chem 2001; 276: 529-534
122. Götz J, Chen F, van Dorpe J, Nitsch RM. Formation of neurofibrillary tangles in P301I tau transgenic mice induced by Abeta 42 fibrils. Science 2001; 293: 1491-1495