Early accumulation of intracellular fibrillar oligomers and late congophilic amyloid angiopathy in mice expressing the Osaka intra-Aβ APP mutation

Translational Psychiatry

Volumn 2, Issue , 2012, Pages

  Kulic, L ^a,b   McAfoose, J ^a   Welt, T ^a   Tackenberg, C ^a   Spani C ^a   Wirth, F ^a   Finder, V ^a   Konietzko, U ^a   Giese, M ^c   Eckert, A ^c   Noriaki, K ^d   Shimizu, T ^e   Murakami, K ^f   Irie, K ^f   Rasool, S ^g   Glabe, C ^g   Hock, C ^a   Nitsch, R M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d Immuno Biological Laboratories Co Ltd   (Japan)

^e CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f KYOTO UNIVERSITY   (Japan)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; APP; congophilic amyloid angiopathy; intraneuronal A ; Osaka mutation

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; OLIGOMER; THIOFLAVINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONGOPHILIC AMYLOID ANGIOPATHY; CONTROLLED STUDY; DISEASE ASSOCIATION; EXPERIMENTAL MODEL; FEMALE; HETEROZYGOSITY; KINETICS; MALE; MOUSE; MUTATION; NONHUMAN; VASCULAR AMYLOIDOSIS; AGE; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL; ANIMAL BEHAVIOR; BRAIN; DISEASE MODEL; GENETICS; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CEREBRAL AMYLOID ANGIOPATHY; DISEASE MODELS, ANIMAL; MICE; MICE, TRANSGENIC; MUTATION; PLAQUE, AMYLOID;

EID: 84869842244     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2012.109     Document Type: Article

References (60)

1. Thal DR, Del Tredici K, Braak H. Neurodegeneration in normal brain aging and disease. Sci Aging Knowledge Environ 2004; 2004: pe26
2. Thal DR, Griffin WS, Braak H. Parenchymal and vascular Abeta-deposition and its effects on the degeneration of neurons and cognition in Alzheimer's disease. J Cell Mol Med 2008; 12: 1848-1862.
3. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002; 297: 353-356. (Pubitemid 34790756)
4. Tanzi RE, Bertram L. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 2005; 120: 545-555. (Pubitemid 40269768)
5. Citron M, Oltersdorf T, Haass C, McConlogue L, Hung AY, Seubert P et al. Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 1992; 360: 672-674. (Pubitemid 23007680)
6. Haass C, Lemere CA, Capell A, Citron M, Seubert P, Schenk D et al. The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway. Nat Med 1995; 1: 1291-1296.
7. Mullan M, Crawford F, Axelman K, Houlden H, Lilius L, Winblad B et al. A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of betaamyloid. Nat Genet 1992; 1: 345-347.
8. Goate AM. Monogenetic determinants of Alzheimer's disease: APP mutations. Cell Mol Life Sci 1998; 54: 897-901. (Pubitemid 28461677)
9. Tomiyama T, Nagata T, Shimada H, Teraoka R, Fukushima A, Kanemitsu H et al. A new amyloid beta variant favoring oligomerization in Alzheimer's-type dementia. Ann Neurol 2008; 63: 377-387. (Pubitemid 351499867)
10. Levy E, Carman MD, Fernandez-Madrid IJ, Power MD, Lieberburg I, van Duinen SG et al. Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. Science 1990; 248: 1124-1126.
11. Hendriks L, van Duijn CM, Cras P, Cruts M, Van Hul W, van Harskamp F et al. Presenile dementia and cerebral haemorrhage linked to a mutation at codon 692 of the beta-amyloid precursor protein gene. Nat Genet 1992; 1: 218-221.
12. Bugiani O, Giaccone G, Rossi G, Mangieri M, Capobianco R, Morbin M et al. Hereditary cerebral hemorrhage with amyloidosis associated with the E693K mutation of APP. Arch Neurol 2010; 67: 987-995.
13. Grabowski TJ, Cho HS, Vonsattel JP, Rebeck GW, Greenberg SM. Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy. Ann Neurol 2001; 49: 697-705. (Pubitemid 32530235)
14. Nilsberth C, Westlind-Danielsson A, Eckman CB, Condron MM, Axelman K, Forsell C et al. The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation. Nat Neurosci 2001; 4: 887-893. (Pubitemid 32801591)
15. Haass C, Hung AY, Selkoe DJ, Teplow DB. Mutations associated with a locus for familial Alzheimer's disease result in alternative processing of amyloid beta-protein precursor. J Biol Chem 1994; 269: 17741-17748.
16. Fraser PE, Nguyen JT, Inouye H, Surewicz WK, Selkoe DJ, Podlisny MB et al. Fibril formation by primate, rodent, and Dutch-hemorrhagic analogues of Alzheimer amyloid beta-protein. Biochemistry 1992; 31: 10716-10723.
17. Murakami K, Irie K, Morimoto A, Ohigashi H, Shindo M, Nagao M et al. Neurotoxicity and physicochemical properties of Abeta mutant peptides from cerebral amyloid angiopathy: implication for the pathogenesis of cerebral amyloid angiopathy and Alzheimer's disease. J Biol Chem 2003; 278: 46179-46187. (Pubitemid 37432769)
18. Kumar-Singh S. Hereditary and sporadic forms of abeta-cerebrovascular amyloidosis and relevant transgenic mouse models. Int J Mol Sci 2009; 10: 1872-1895.
19. Takuma H, Teraoka R, Mori H, Tomiyama T. Amyloid-beta E22Delta variant induces synaptic alteration in mouse hippocampal slices. NeuroReport 2008; 19: 615-619. (Pubitemid 351489355)
20. Suzuki T, Murakami K, Izuo N, Kume T, Akaike A, Nagata T et al. E22Delta mutation in amyloid beta-protein promotes beta-sheet transformation, radical production, and synaptotoxicity, but not neurotoxicity. Int J Alzheimer's Dis 2011; 2011: 431320.
21. Nishitsuji K, Tomiyama T, Ishibashi K, Ito K, Teraoka R, Lambert MP et al. The E693Delta mutation in amyloid precursor protein increases intracellular accumulation of amyloid beta oligomers and causes endoplasmic reticulum stress-induced apoptosis in cultured cells. Am J Pathol 2009; 174: 957-969.
22. Tomiyama T, Matsuyama S, Iso H, Umeda T, Takuma H, Ohnishi K et al. A mouse model of amyloid beta oligomers: their contribution to synaptic alteration, abnormal tau phosphorylation, glial activation, and neuronal loss in vivo. J Neurosci 2010; 30: 4845-4856.
23. Umeda T, Tomiyama T, Sakama N, Tanaka S, Lambert MP, Klein WL et al. Intraneuronal amyloid beta oligomers cause cell death via endoplasmic reticulum stress, endosomal/ lysosomal leakage, and mitochondrial dysfunction in vivo. J Neurosci Res 2011; 89: 1031-1042.
24. Ovchinnikova OY, Finder VH, Vodopivec I, Nitsch RM, Glockshuber R. The Osaka FAD mutation E22Delta leads to the formation of a previously unknown type of amyloid beta fibrils and modulates Abeta neurotoxicity. J Mol Biol 2011; 408: 780-791.
25. Borchelt DR, Davis J, Fischer M, Lee MK, Slunt HH, Ratovitsky T et al. A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet Anal 1996; 13: 159-163. (Pubitemid 27063321)
26. Murakami K, Horikoshi-Sakuraba Y, Murata N, Noda Y, Masuda Y, Kinoshita N et al. Monoclonal antibody against the turn of the 42-residue amyloid b-protein at positions 22 and 23. ACS Chem Neurosci 2010; 1: 747-756.
27. Knobloch M, Konietzko U, Krebs DC, Nitsch RM. Intracellular Abeta and cognitive deficits precede beta-amyloid deposition in transgenic arcAbeta mice. Neurobiol Aging 2007; 28: 1297-1306. (Pubitemid 47081235)
28. Finder VH, Vodopivec I, Nitsch RM, Glockshuber R. The recombinant amyloid-beta peptide Abeta1-42 aggregates faster and is more neurotoxic than synthetic Abeta1-42. J Mol Biol 2010; 396: 9-18.
29. Crawley JN. Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol 2007; 17: 448-459. (Pubitemid 47537604)
30. Paul CM, Magda G, Abel S. Spatial memory: theoretical basis and comparative review on experimental methods in rodents. Behav Brain Res 2009; 203: 151-164.
31. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996; 274: 99-102. (Pubitemid 26332733)
32. Kawarabayashi T, Younkin LH, Saido TC, Shoji M, Ashe KH, Younkin SG. Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 2001; 21: 372-381. (Pubitemid 32107428)
33. Kayed R, Head E, Sarsoza F, Saing T, Cotman CW, Necula M et al. Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol Neurodegener 2007; 2: 18.
34. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003; 300: 486-489. (Pubitemid 36444329)
35. Di Fede G, Catania M, Morbin M, Rossi G, Suardi S, Mazzoleni G et al. A recessive mutation in the APP gene with dominant-negative effect on amyloidogenesis. Science 2009; 323: 1473-1477.
36. Shimada H, Ataka S, Tomiyama T, Takechi H, Mori H, Miki T. Clinical course of patients with familial early-onset Alzheimer's disease potentially lacking senile plaques bearing the E693Delta mutation in amyloid precursor protein. Dement Geriatr Cogn Disord 2011; 32: 45-54.
37. Cleary JP,Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ et al. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 2005; 8: 79-84. (Pubitemid 41236735)
38. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT,WoodM et al. Abeta oligomerinduced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 2007; 27: 796-807. (Pubitemid 46174498)
39. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 1998; 95: 6448-6453.
40. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006; 440: 352-357.
41. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 2007; 27: 2866-2875. (Pubitemid 46438992)
42. Townsend M, Shankar GM, Mehta T, Walsh DM, Selkoe DJ. Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: a potent role for trimers. J Physiol 2006; 572(Part 2): 477-492.
43. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002; 416: 535-539. (Pubitemid 34288854)
44. Inayathullah M, Teplow DB. Structural dynamics of the DeltaE22 (Osaka) familial Alzheimer's disease-linked amyloid beta-protein. Amyloid 2011; 18: 98-107.
45. Kumar-Singh S. Cerebral amyloid angiopathy: pathogenetic mechanisms and link to dense amyloid plaques. Genes Brain Behav 2008; 7((Suppl 1)): 67-82.
46. Kumar-Singh S, Cras P, Wang R, Kros JM, van Swieten J, Lubke U et al. Dense-core senile plaques in the Flemish variant of Alzheimer's disease are vasocentric. Am J Pathol 2002; 161: 507-520. (Pubitemid 36142160)
47. Herzig MC, Winkler DT, Burgermeister P, Pfeifer M, Kohler E, Schmidt SD et al. Abeta is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis. Nat Neurosci 2004; 7: 954-960. (Pubitemid 39129504)
48. Deane R, Wu Z, Sagare A, Davis J, Du Yan S, Hamm K et al. LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 2004; 43: 333-344. (Pubitemid 39061126)
49. Monro OR, Mackic JB, Yamada S, Segal MB, Ghiso J, Maurer C et al. Substitution at codon 22 reduces clearance of Alzheimer's amyloid-beta peptide from the cerebrospinal fluid and prevents its transport from the central nervous system into blood. Neurobiol Aging 2002; 23: 405-412. (Pubitemid 34312024)
50. LaFerla FM, Green KN, Oddo S. Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 2007; 8: 499-509.
51. Gouras GK, Tampellini D, Takahashi RH, Capetillo-Zarate E. Intraneuronal beta-amyloid accumulation and synapse pathology in Alzheimer's disease. Acta Neuropathol 2010; 119: 523-541.
52. Tampellini D, Gouras GK. Synapses, synaptic activity and intraneuronal abeta in Alzheimer's disease. Front Aging Neurosci 2010 2.
53. Winton MJ, Lee EB, Sun E, Wong MM, Leight S, Zhang B et al. Intraneuronal APP, not free Abeta peptides in 3-Tg-AD mice: implications for tau versus Abeta-mediated Alzheimer neurodegeneration. J Neurosci 2011; 31: 7691-7699.
54. Ferretti MT, Bruno MA, Ducatenzeiler A, Klein WL, Cuello AC. Intracellular Abetaoligomers and early inflammation in a model of Alzheimer's disease. Neurobiol Aging 2012; 33: 1329-1342.
55. Oddo S, Caccamo A, Tran L, Lambert MP, Glabe CG, Klein WL et al. Temporal profile of amyloid-beta (Abeta) oligomerization in an in vivo model of Alzheimer disease. A link between Abeta and tau pathology. J Biol Chem 2006; 281: 1599-1604.
56. Tomic JL, Pensalfini A, Head E, Glabe CG. Soluble fibrillar oligomer levels are elevated in Alzheimer's disease brain and correlate with cognitive dysfunction. Neurobiol Dis 2009; 35: 352-358.
57. Murakami K, Masuda Y, Shirasawa T, Shimizu T, Irie K. The turn formation at positions 22 and 23 in the 42-mer amyloid beta peptide: the emerging role in the pathogenesis of Alzheimer's disease. Geriatr Gerontol Int 2010; 10((Suppl 1)): S169-S179.
58. Sahlin C, Lord A, Magnusson K, Englund H, Almeida CG, Greengard P et al. The Arctic Alzheimer mutation favors intracellular amyloid-beta production by making amyloid precursor protein less available to alpha-secretase. J Neurochem 2007; 101: 854-862. (Pubitemid 46646626)
59. Stenh C, Nilsberth C, Hammarback J, Engvall B, Naslund J, Lannfelt L. The Arctic mutation interferes with processing of the amyloid precursor protein. NeuroReport 2002; 13: 1857-1860. (Pubitemid 35398949)
60. Lammich S, Kojro E, Postina R, Gilbert S, Pfeiffer R, Jasionowski M et al. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease.Proc Natl Acad Sci USA 1999; 96: 3922-3927.