A lifespan observation of a novel mouse model: In vivo evidence supports Aβ oligomer hypothesis

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Zhang, Yichi ^a   Lu, Lu ^a   Jia, Jianping ^a,b,c   Jia, Longfei ^d   Geula, Changiz ^f   Pei, Jinjing ^e   Xu, Zhiqing ^g   Qin, Wei ^a,b,c   Liu, Ruiqin ^a,b,c   Li, Dan ^a,b,c   Pan, Na ^g  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b Beijing Key Laboratory of Geriatric Cognitive Disorders ^*  (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^d CAPITAL MEDICAL UNIVERSITY   (China)

^e KAROLINSKA INSTITUTE   (Sweden)

^f NORTHWESTERN UNIVERSITY   (United States)

^g CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; OLIGOMER; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BIOACCUMULATION; BIOCHEMISTRY; CELL ACTIVATION; CELL FUNCTION; CELL LOSS; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; GENE; GLIA CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIFESPAN; MAZE TEST; MEMORY CELL; MOUSE; MOUSE MODEL; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PS1 GENE;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; HUMANS; LONGEVITY; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MODELS, ANIMAL; MODELS, BIOLOGICAL; NEUROFIBRILLARY TANGLES; NEURONAL PLASTICITY; NEURONS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PLAQUE, AMYLOID; PROTEIN MULTIMERIZATION; SYNAPSES; TAU PROTEINS;

EID: 84908191419     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085885     Document Type: Article

References (64)

1. Rockenstein EM, McConlogue L, Tan H, Power M, Masliah E, et al. (1995) Levels and alternative splicing of amyloid beta protein precursor (APP) transcripts in brains of APP transgenic mice and humans with Alzheimer's disease. J Biol Chem 270: 28257-28267.
2. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, et al. (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274: 99-102. (Pubitemid 26332733)
3. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, et al. (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci U S A 94: 13287-13292. (Pubitemid 27518514)
4. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, et al. (1997) Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19: 939-945. (Pubitemid 27471397)
5. Citron M, Westaway D, Xia W, Carlson G, Diehl T, et al. (1997) Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nat Med 3: 67-72. (Pubitemid 27019143)
6. Duff K, Eckman C, Zehr C, Yu X, Prada CM, et al. (1996) Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1. Nature 383: 710-713. (Pubitemid 26360645)
7. Zhang B, Higuchi M, Yoshiyama Y, Ishihara T, Forman MS, et al. (2004) Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative tauopathy. J Neurosci 24: 4657-4667. (Pubitemid 38656621)
8. Andorfer C, Kress Y, Espinoza M, de Silva R, Tucker KL, et al. (2003) Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J Neurochem 86: 582-590. (Pubitemid 36897439)
9. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, et al. (2005) Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 25: 10637-10647. (Pubitemid 41681911)
10. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, et al. (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4: 97-100. (Pubitemid 28133087)
11. Oakley H, Cole SL, Logan S, Maus E, Shao P, et al. (2006) Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 26: 10129-10140. (Pubitemid 44527407)
12. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, et al. (2003) Triple-Transgenic Model of Alzheimer's Disease with Plaques and Tangles. Neuron 39: 409-421.
13. Bettens K, Sleegers K, Van Broeckhoven C (2013) Genetic insights in Alzheimer's disease. Lancet Neurol 12: 92-104.
14. Jia J, Xu E, Shao Y, Sun Y, Li D (2005) One novel presenilin-1 gene mutation in a Chinese pedigree of familial Alzheimer's disease. J Alzheimers Dis 7: 119-124; discussion 173-180.
15. Wang Y, Cheng Z, Qin W, Jia J (2012) Val97Leu mutant presenilin-1 induces tau hyperphosphorylation and spatial memory deficit in mice and the underlying mechanisms. J Neurochem 121: 135-145.
16. Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1: 848-858.
17. Mathis DM, Furman JL, Norris CM (2011) Preparation of acute hippocampal slices from rats and transgenic mice for the study of synaptic alterations during aging and amyloid pathology. J Vis Exp.
18. Zheng K, Kuteeva E, Xia S, Bartfai T, Hokfelt T, et al. (2005) Age-related impairments of synaptic plasticity in the lateral perforant path input to the dentate gyrus of galanin overexpressing mice. Neuropeptides 39: 259-267. (Pubitemid 40804595)
19. Hurtado DE, Molina-Porcel L, Iba M, Aboagye AK, Paul SM, et al. (2010) A{beta} accelerates the spatiotemporal progression of tau pathology and augments tau amyloidosis in an Alzheimer mouse model. Am J Pathol 177: 1977-1988.
20. Bussiere T, Bard F, Barbour R, Grajeda H, Guido T, et al. (2004) Morphological characterization of Thioflavin-S-positive amyloid plaques in transgenic Alzheimer mice and effect of passive Abeta immunotherapy on their clearance. Am J Pathol 165: 987-995. (Pubitemid 39129305)
21. Takahashi RH, Milner TA, Li F, Nam EE, Edgar MA, et al. (2002) Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol 161: 1869-1879. (Pubitemid 35265544)
22. Alafuzoff I, Pikkarainen M, Al-Sarraj S, Arzberger T, Bell J, et al. (2006) Interlaboratory comparison of assessments of Alzheimer disease-related lesions: a study of the BrainNet Europe Consortium. J Neuropathol Exp Neurol 65: 740-757. (Pubitemid 44200315)
23. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112: 389-404. (Pubitemid 44469160)
24. Allsop D, Wong CW, Ikeda S, Landon M, Kidd M, et al. (1988) Immunohistochemical evidence for the derivation of a peptide ligand from the amyloid beta-protein precursor of Alzheimer disease. Proc Natl Acad Sci U S A 85: 2790-2794.
25. Selkoe DJ (1989) Amyloid beta protein precursor and the pathogenesis of Alzheimer's disease. Cell 58: 611-612.
26. Hardy JA, Higgins GA (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science 256: 184-185.
27. Kowall NW, Beal MF, Busciglio J, Duffy LK, Yankner BA (1991) An in vivo model for the neurodegenerative effects of beta amyloid and protection by substance P. Proc Natl Acad Sci U S A 88: 7247-7251. (Pubitemid 21915127)
28. Lorenzo A, Yankner BA (1994) Beta-amyloid neurotoxicity requires fibril formation and is inhibited by congo red. Proc Natl Acad Sci U S A 91: 12243-12247. (Pubitemid 24368641)
29. Pike CJ, Walencewicz AJ, Glabe CG, Cotman CW (1991) Aggregation-related toxicity of synthetic beta-amyloid protein in hippocampal cultures. Eur J Pharmacol 207: 367-368.
30. Pike CJ, Walencewicz AJ, Glabe CG, Cotman CW (1991) In vitro aging of beta-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res 563: 311-314.
31. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356. (Pubitemid 34790756)
32. Pimplikar SW (2009) Reassessing the amyloid cascade hypothesis of Alzheimer's disease. Int J Biochem Cell Biol 41: 1261-1268.
33. Walsh DM, Selkoe DJ (2007) A beta oligomers - a decade of discovery. J Neurochem 101: 1172-1184.
34. Benilova I, Karran E, De Strooper B (2012) The toxic Ab oligomer and Alzheimer's disease: an emperor in need of clothes. Nat Neurosci 15: 349-357.
35. Ferreira ST, Klein WL (2011) The Ab oligomer hypothesis for synapse failure and memory loss in Alzheimer's disease. Neurobiol Learn Mem 96: 529-543.
36. Leon WC, Canneva F, Partridge V, Allard S, Ferretti MT, et al. (2010) A novel transgenic rat model with a full Alzheimer's-like amyloid pathology displays preplaque intracellular amyloid-beta-associated cognitive impairment. J Alzheimers Dis 20: 113-126.
37. Tomiyama T, Matsuyama S, Iso H, Umeda T, Takuma H, et al. (2010) A mouse model of amyloid beta oligomers: their contribution to synaptic alteration, abnormal tau phosphorylation, glial activation, and neuronal loss in vivo. J Neurosci 30: 4845-4856.
38. Jankowsky JL, Younkin LH, Gonzales V, Fadale DJ, Slunt HH, et al. (2007) Rodent A beta modulates the solubility and distribution of amyloid deposits in transgenic mice. J Biol Chem 282: 22707-22720. (Pubitemid 47267316)
39. Borchelt DR, Thinakaran G, Eckman CB, Lee MK, Davenport F, et al. (1996) Familial Alzheimer's disease-linked presenilin 1 variants elevate Abeta1-42/1-40 ratio in vitro and in vivo. Neuron 17: 1005-1013. (Pubitemid 26424026)
40. Citron M, Oltersdorf T, Haass C, McConlogue L, Hung AY, et al. (1992) Mutation of the [beta]-amyloid precursor protein in familial Alzheimer's disease increases [beta]-protein production. Nature 360: 672-674. (Pubitemid 23007680)
41. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, et al. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-489. (Pubitemid 36444329)
42. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT, et al. (2007) Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 27: 796-807. (Pubitemid 46174498)
43. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, et al. (2000) High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20: 4050-4058. (Pubitemid 30365675)
44. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, et al. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539. (Pubitemid 34288854)
45. Dodart JC, Bales KR, Gannon KS, Greene SJ, DeMattos RB, et al. (2002) Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat Neurosci 5: 452-457. (Pubitemid 34454251)
46. Kotilinek LA, Bacskai B, Westerman M, Kawarabayashi T, Younkin L, et al. (2002) Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J Neurosci 22: 6331-6335. (Pubitemid 35386387)
47. Arriagada PV, Growdon JH, Hedley-Whyte ET, Hyman BT (1992) Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42: 631-639.
48. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, et al. (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30: 572-580.
49. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95: 6448-6453.
50. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, et al. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
51. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45: 675-688. (Pubitemid 40320703)
52. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, et al. (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8: 79-84. (Pubitemid 41236735)
53. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440: 352-357.
54. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, et al. (2007) Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 27: 2866-2875. (Pubitemid 46438992)
55. De Felice FG, Wu D, Lambert MP, Fernandez SJ, Velasco PT, et al. (2008) Alzheimer's disease-type neuronal tau hyperphosphorylation induced by A beta oligomers. Neurobiol Aging 29: 1334-1347. (Pubitemid 351970596)
56. Jin M, Shepardson N, Yang T, Chen G, Walsh D, et al. (2011) Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc Natl Acad Sci U S A 108: 5819-5824.
57. Zempel H, Thies E, Mandelkow E, Mandelkow EM (2010) Abeta oligomers cause localized Ca(2+) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J Neurosci 30: 11938-11950.
58. Clinton LK, Blurton-Jones M, Myczek K, Trojanowski JQ, LaFerla FM (2010) Synergistic Interactions between Abeta, tau, and alpha-synuclein: acceleration of neuropathology and cognitive decline. J Neurosci 30: 7281-7289.
59. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, et al. (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 142: 387-397.
60. Ferretti MT, Bruno MA, Ducatenzeiler A, Klein WL, Cuello AC (2012) Intracellular Abeta-oligomers and early inflammation in a model of Alzheimer's disease. Neurobiol Aging 33: 1329-1342.
61. Duyckaerts C, Potier MC, Delatour B (2008) Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol 115: 5-38. (Pubitemid 50005258)
62. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
63. Yoshiyama Y, Higuchi M, Zhang B, Huang SM, Iwata N, et al. (2007) Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 53: 337-351. (Pubitemid 46161268)
64. Fuhrmann M, Bittner T, Jung CK, Burgold S, Page RM, et al. (2010) Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat Neurosci 13: 411-413.