Amyloid precursor protein transgenic mouse models and Alzheimer's disease: Understanding the paradigms, limitations, and contributions

Alzheimer's and Dementia

Volumn 5, Issue 4, 2009, Pages 340-347

  Kokjohn, Tyler A ^a,b   Roher, Alex E ^a  

^a SUN HEALTH RESEARCH INSTITUTE   (United States)

^b MIDWESTERN UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Amyloid precursor protein; Amyloid beta vaccine; Transgenic mice

Indexed keywords

ALZHEIMER DISEASE VACCINE; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL BEHAVIOR; ANIMAL MODEL; DISEASE MODEL; DRUG RESEARCH; ENCEPHALITIS; HUMAN; MOUSE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROCESSING; REVIEW; RODENT; SENILE PLAQUE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VASCULAR AMYLOIDOSIS;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; HUMANS; MICE; MICE, TRANSGENIC; NEURONS; SPECIES SPECIFICITY; TREATMENT FAILURE;

EID: 67649805281     PISSN: 15525260     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jalz.2009.03.002     Document Type: Review

References (84)

1. Holmes C., Boche D., Wilkinson D., Yadegarfar G., Hopkins V., Bayer A., et al. Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 372 (2008) 216-223
2. Patton R.L., Kalback W.M., Esh C.L., Kokjohn T.A., Van Vickle G.D., Luehrs D.C., et al. Amyloid-beta peptide remnants in AN-1792-immunized Alzheimer's disease patients: a biochemical analysis. Am J Pathol 169 (2006) 1048-1063
3. Roher A.E., Lowenson J.D., Clarke S., Wolkow C., Wang R., Cotter R.J., et al. Structural alterations in the peptide backbone of beta-amyloid core protein may account for its deposition and stability in Alzheimer's disease. J Biol Chem 268 (1993) 3072-3083
4. Gowing E., Roher A.E., Woods A.S., Cotter R.J., Chaney M., Little S.P., et al. Chemical characterization of A beta 17-42 peptide, a component of diffuse amyloid deposits of Alzheimer disease. J Biol Chem 269 (1994) 10987-10990
5. Kuo Y.M., Emmerling M.R., Vigo-Pelfrey C., Kasunic T.C., Kirkpatrick J.B., Murdoch G.H., et al. Water-soluble Abeta (N-40, N-42) oligomers in normal and Alzheimer disease brains. J Biol Chem 271 (1996) 4077-4081
6. Roher A.E., Chaney M.O., Kuo Y.M., Webster S.D., Stine W.B., Haverkamp L.J., et al. Morphology and toxicity of Abeta-(1-42) dimer derived from neuritic and vascular amyloid deposits of Alzheimer's disease. J Biol Chem 271 (1996) 20631-20635
7. Kuo Y.M., Emmerling M.R., Woods A.S., Cotter R.J., and Roher A.E. Isolation, chemical characterization, and quantitation of A beta 3-pyroglutamyl peptide from neuritic plaques and vascular amyloid deposits. Biochem Biophys Res Commun 237 (1997) 188-191
8. Giulian D., Haverkamp L.J., Yu J., Karshin W., Tom D., Li J., et al. The HHQK domain of beta-amyloid provides a structural basis for the immunopathology of Alzheimer's disease. J Biol Chem 273 (1998) 29719-29726
9. Roher A.E., and Kokjohn T.A. Appraisal of AbetaPP transgenic mice as models for Alzheimer's disease amyloid cascade. Curr Med Chem Immun Endo Metab Agents 3 (2003) 85-90
10. Roher A.E., and Kokjohn T.A. Of mice and men: the relevance of transgenic mice Abeta immunizations to Alzheimer's disease. J Alzheimers Dis 4 (2002) 431-434
11. Kalback W., Watson M.D., Kokjohn T.A., Kuo Y.M., Weiss N., Luehrs D.C., 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 41 (2002) 922-928
12. Kuo Y.M., Kokjohn T.A., Beach T.G., Sue L.I., Brune D., Lopez J.C., et al. Comparative analysis of amyloid-beta chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer's disease brains. J Biol Chem 276 (2001) 12991-12998
13. Esh C., Patton L., Kalback W., Kokjohn T.A., Lopez J., Brune D., et al. Altered APP processing in PDAPP (Val717 → Phe) transgenic mice yields extended-length Abeta peptides. Biochemistry 44 (2005) 13807-13819
14. Van Vickle G.D., Esh C.L., Kalback W.M., Patton R.L., Luehrs D.C., Kokjohn T.A., et al. TgCRND8 amyloid precursor protein transgenic mice exhibit an altered gamma-secretase processing and an aggressive, additive amyloid pathology subject to immunotherapeutic modulation. Biochemistry 46 (2007) 10317-10327
15. Van Vickle G.D., Esh C.L., Daugs I.D., Kokjohn T.A., Kalback W.M., Patton R.L., et al. Tg-SwDI transgenic mice exhibit novel alterations in AbetaPP processing, Abeta degradation, and resilient amyloid angiopathy. Am J Pathol 173 (2008) 483-493
16. Kuo Y.M., Webster S., Emmerling M.R., De L.N., and Roher A.E. Irreversible dimerization/tetramerization and post-translational modifications inhibit proteolytic degradation of A beta peptides of Alzheimer's disease. Biochim Biophys Acta 1406 (1998) 291-298
17. Atwood C.S., Perry G., Zeng H., Kato Y., Jones W.D., Ling K.Q., et al. Copper mediates dityrosine cross-linking of Alzheimer's amyloid-beta. Biochemistry 43 (2004) 560-568
18. Miravalle L., Calero M., Takao M., Roher A.E., Ghetti B., and Vidal R. Amino-terminally truncated Abeta peptide species are the main component of cotton wool plaques. Biochemistry 44 (2005) 10810-10821
19. Hung L.W., Ciccotosto G.D., Giannakis E., Tew D.J., Perez K., Masters C.L., et al. Amyloid-beta peptide (Abeta) neurotoxicity is modulated by the rate of peptide aggregation: Abeta dimers and trimers correlate with neurotoxicity. J Neurosci 28 (2008) 11950-11958
20. Roher A.E., Palmer K.C., Capodilupo J., Wakade A.R., and Ball M.J. New biochemical insights to unravel the pathogenesis of Alzheimer's lesions. Can J Neurol Sci 18 (1991) 408-410
21. Roher A.E., Palmer K.C., Yurewicz E.C., Ball M.J., and Greenberg B.D. Morphological and biochemical analyses of amyloid plaque core proteins purified from Alzheimer disease brain tissue. J Neurochem 61 (1993) 1916-1926
22. Loerch P.M., Lu T., Dakin K.A., Vann J.M., Isaacs A., Geula C., et al. Evolution of the aging brain transcriptome and synaptic regulation. PLoS ONE 3 (2008) e3329
23. Maarouf C.L., Daugs I.D., Spina S., Vidal R., Kokjohn T.A., Patton R.L., et al. Histopathological and molecular heterogeneity among individuals with dementia associated with presenilin mutations. Mol Neurodegener 3 (2008) 20
24. Roher A.E., Kokjohn T.A., Esh C., Weiss N., Childress J., Kalback W., et al. The human amyloid-beta precursor protein770 mutation V717F generates peptides longer than amyloid-beta-(40-42) and flocculent amyloid aggregates. J Biol Chem 279 (2004) 5829-5836
25. Kuo Y.M., Beach T.G., Sue L.I., Scott S., Layne K.J., Kokjohn T.A., et al. The evolution of A beta peptide burden in the APP23 transgenic mice: implications for A beta deposition in Alzheimer disease. Mol Med 7 (2001) 609-618
26. Kuo Y.M., Crawford F., Mullan M., Kokjohn T.A., Emmerling M.R., Weller R.O., et al. Elevated A beta and apolipoprotein E in A betaPP transgenic mice and its relationship to amyloid accumulation in Alzheimer's disease. Mol Med 6 (2000) 430-439
27. Roher A.E., Lowenson J.D., Clarke S., Woods A.S., Cotter R.J., Gowing E., et al. Beta-amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer disease. Proc Natl Acad Sci USA 90 (1993) 10836-10840
28. Roher A.E., and Kuo Y.M. Isolation of amyloid deposits from brain. Methods Enzymol 309 (1999) 58-67
29. Lowenson J.D., Clarke S., and Roher A.E. Chemical modifications of deposited amyloid-beta peptides. Methods Enzymol 309 (1999) 89-105
30. Puente X.S., and Lopez-Otin C. A genomic analysis of rat proteases and protease inhibitors. Genome Res 14 (2004) 609-622
31. Puente X.S., Sanchez L.M., Overall C.M., and Lopez-Otin C. Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 4 (2003) 544-558
32. Mirnics K., Norstrom E.M., Garbett K., Choi S.H., Zhang X., Ebert P., et al. Molecular signatures of neurodegeneration in the cortex of PS1/PS2 double knockout mice. Mol Neurodegener 3 (2008) 14
33. Haass C., and Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8 (2007) 101-112
34. Watson D., Castano E., Kokjohn T.A., Kuo Y.M., Lyubchenko Y., Pinsky D., et al. Physicochemical characteristics of soluble oligomeric Abeta and their pathologic role in Alzheimer's disease. Neurol Res 27 (2005) 869-881
35. Walsh D.M., and Selkoe D.J. Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration. Protein Pept Lett 11 (2004) 213-228
36. Walsh D.M., and Selkoe D.J. A beta oligomers-a decade of discovery. J Neurochem 101 (2007) 1172-1184
37. Morrissette D.A., Parachikova A., Green K.N., and LaFerla F.M. Relevance of transgenic mouse models to human Alzheimer disease. J Biol Chem 284 (2009) 6033-6037
38. Li C.K., and Ting S.Y. Possible phylogenetic relationships of eurymylids and rodents, with comments on mimotonids. In: Luckett W.P., and Hartenberger J.L. (Eds). Evolutionary relationships among rodents. A multidisciplinary analysis (1985), Plenum and Springer, New York 35-58
39. Yankner B.A., Lu T., and Loerch P. The aging brain. Annu Rev Pathol 3 (2008) 41-66
40. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39 (2003) 409-421
41. Pietropaolo S., Feldon J., and Yee B.K. Age-dependent phenotypic characteristics of a triple transgenic mouse model of Alzheimer disease. Behav Neurosci 122 (2008) 733-747
42. Pietropaolo S., Sun Y., Li R., Brana C., Feldon J., and Yee B.K. The impact of voluntary exercise on mental health in rodents: a neuroplasticity perspective. Behav Brain Res 192 (2008) 42-60
43. Mastrangelo M.A., and Bowers W.J. Detailed immunohistochemical characterization of temporal and spatial progression of Alzheimer's disease-related pathologies in male triple-transgenic mice. BMC Neurosci 9 (2008) 81
44. Roher A.E., Kuo Y.M., Roher A.A., Emmerling M.R., and Goux W.J. Chemical analysis of amyloid beta protein in CAA. In: Verbeek M.M., de Waal R.M.W., and Vinters H.V. (Eds). Cerebral amyloid angiopathy in Alzheimer's disease and related disorders (2000), Kluwer Academic Publishers, Dordrecht 157-177
45. Weller R.O., Massey A., Newman T.A., Hutchings M., Kuo Y.M., and Roher A.E. Cerebral amyloid angiopathy: amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer's disease. Am J Pathol 153 (1998) 725-733
46. Weller R.O., Massey A., Kuo Y.M., and Roher A.E. Cerebral amyloid angiopathy: accumulation of A beta in interstitial fluid drainage pathways in Alzheimer's disease. Ann NY Acad Sci 903 (2000) 110-117
47. Roher A.E., Kuo Y.M., Esh C., Knebel C., Weiss N., Kalback W., et al. Cortical and leptomeningeal cerebrovascular amyloid and white matter pathology in Alzheimer's disease. Mol Med 9 (2003) 112-122
48. Roher A.E., Weiss N., Kokjohn T.A., Kuo Y.M., Kalback W., Anthony J., et al. Increased Abeta peptides and reduced cholesterol and myelin proteins characterize white matter degeneration in Alzheimer's disease. Biochemistry 41 (2002) 11080-11090
49. Kalback W., Esh C., Castano E.M., Rahman A., Kokjohn T., Luehrs D.C., et al. Atherosclerosis, vascular amyloidosis and brain hypoperfusion in the pathogenesis of sporadic Alzheimer's disease. Neurol Res 26 (2004) 525-539
50. Wilcock D.M., Jantzen P.T., Li Q., Morgan D., and Gordon M.N. Amyloid-beta vaccination, but not nitro-nonsteroidal anti-inflammatory drug treatment, increases vascular amyloid and microhemorrhage while both reduce parenchymal amyloid. Neuroscience 144 (2007) 950-960
51. Nicoll J.A., Wilkinson D., Holmes C., Steart P., Markham H., and Weller R.O. Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nat Med 9 (2003) 448-452
52. Schenk D., Barbour R., Dunn W., Gordon G., Grajeda H., Guido T., et al. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400 (1999) 173-177
53. Morgan D., Diamond D.M., Gottschall P.E., Ugen K.E., Dickey C., Hardy J., et al. A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408 (2000) 982-985
54. Racke M.M., Boone L.I., Hepburn D.L., Parsadainian M., Bryan M.T., Ness D.K., et al. Exacerbation of cerebral amyloid angiopathy-associated microhemorrhage in amyloid precursor protein transgenic mice by immunotherapy is dependent on antibody recognition of deposited forms of amyloid beta. J Neurosci 25 (2005) 629-636
55. Pfeifer M., Boncristiano S., Bondolfi L., Stalder A., Deller T., Staufenbiel M., et al. Cerebral hemorrhage after passive anti-Abeta immunotherapy. Science 298 (2002) 1379
56. Wilcock D.M., Rojiani A., Rosenthal A., Subbarao S., Freeman M.J., Gordon M.N., et al. Passive immunotherapy against Abeta in aged APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage. J Neuroinflamm 1 (2004) 24
57. Schroeter S., Khan K., Barbour R., Doan M., Chen M., Guido T., et al. Immunotherapy reduces vascular amyloid-beta in PDAPP mice. J Neurosci 28 (2008) 6787-6793
58. Roher A.E., Esh C.L., Kokjohn T.A., Castano E.M., Van Vickle G.D., Kalback W.M., et al. Amyloid beta peptides in human plasma and tissues and their significance for Alzheimer's disease. Alzheimers Dement 5 (2009) 18-29
59. Dodart J.C., Bales K.R., Gannon K.S., Greene S.J., DeMattos R.B., Mathis C., et al. Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat Neurosci 5 (2002) 452-457
60. Janus C., Pearson J., McLaurin J., Mathews P.M., Jiang Y., Schmidt S.D., et al. A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408 (2000) 979-982
61. Morgan D. Mechanisms of A beta plaque clearance following passive A beta immunization. Neurodegener Dis 2 (2005) 261-266
62. Ferrer I., Boada R.M., Sanchez Guerra M.L., Rey M.J., and Costa-Jussa F. Neuropathology and pathogenesis of encephalitis following amyloid-beta immunization in Alzheimer's disease. Brain Pathol 14 (2004) 11-20
63. Masliah E., Hansen L., Adame A., Crews L., Bard F., Lee C., et al. Abeta vaccination effects on plaque pathology in the absence of encephalitis in Alzheimer disease. Neurology 64 (2005) 129-131
64. Nicoll J.A., Barton E., Boche D., Neal J.W., Ferrer I., Thompson P., et al. Abeta species removal after abeta42 immunization. J Neuropathol Exp Neurol 65 (2006) 1040-1048
65. Meyer-Luehmann M., Spires-Jones T.L., Prada C., Garcia-Alloza M., de Calignon A., Rozkalne A., et al. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 451 (2008) 720-724
66. Gervais F., Paquette J., Morissette C., Krzywkowski P., Yu M., Azzi M., et al. Targeting soluble Abeta peptide with Tramiprosate for the treatment of brain amyloidosis. Neurobiol Aging 28 (2007) 537-547
67. Kukar T., Prescott S., Eriksen J.L., Holloway V., Murphy M.P., Koo E.H., et al. Chronic administration of R-flurbiprofen attenuates learning impairments in transgenic amyloid precursor protein mice. BMC Neurosci 8 (2007) 54
68. McGeer P.L., and McGeer E.G. NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies. Neurobiol Aging 28 (2007) 639-647
69. Augustin S., Rimbach G., Augustin K., Schliebs R., Wolffram S., and Cermak R. Effect of a short- and long-term treatment with ginkgo biloba extract on amyloid precursor protein levels in a transgenic mouse model relevant to Alzheimer's disease. Arch Biochem Biophys 481 (2009) 177-182
70. Chauhan N.B., Siegel G.J., and Feinstein D.L. Effects of lovastatin and pravastatin on amyloid processing and inflammatory response in TgCRND8 brain. Neurochem Res 29 (2004) 1897-1911
71. Heininger K. A unifying hypothesis of Alzheimer's disease. IV. Causation and sequence of events. Rev Neurosci 11 (2000) 213-328
72. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 430 (2004) 631-639
73. Muller T., Meyer H.E., Egensperger R., and Marcus K. The amyloid precursor protein intracellular domain (AICD) as modulator of gene expression, apoptosis, and cytoskeletal dynamics-relevance for Alzheimer's disease. Prog Neurobiol 85 (2008) 393-406
74. Turner P.R. O'Connor K, Tate WP, Abraham WC. Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog Neurobiol 70 (2003) 1-32
75. Liu S.J., Zhang A.H., Li H.L., Wang Q., Deng H.M., Netzer W.J., et al. Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of tau and impairment of spatial memory. J Neurochem 87 (2003) 133-144
76. Engel T., Hernandez F., Avila J., and Lucas J.J. Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. J Neurosci 26 (2006) 5083-5090
77. Heininger K. A unifying hypothesis of Alzheimer's disease. I. Ageing sets the stage. Hum Psychopharmacol 14 (1999) 363-414
78. Heininger K. A unifying hypothesis of Alzheimer's disease. II. Pathophysiological processes. Hum Psychopharmacol 14 (1999) 525-581
79. Heininger K. A unifying hypothesis of Alzheimer's disease. III. Risk factors. Hum Psychopharmacol 15 (2000) 1-70
80. Roher A.E., Kokjohn T.A., and Beach T.G. An association with great implications: vascular pathology and Alzheimer disease. Alzheimer Dis Assoc Disord 20 (2006) 73-75
81. Baloyannis S.J. Mitochondrial alterations in Alzheimer's disease. J Alzheimers Dis 9 (2006) 119-126
82. Devi L., Prabhu B.M., Galati D.F., Avadhani N.G., and Anandatheerthavarada H.K. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J Neurosci 26 (2006) 9057-9068
83. Manczak M., Anekonda T.S., Henson E., Park B.S., Quinn J., and Reddy P.H. Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum Mol Genet 15 (2006) 1437-1449
84. Chen J.X., and Yan S.D. Amyloid-beta-induced mitochondrial dysfunction. J Alzheimers Dis 12 (2007) 177-184