Acute amnestic encephalopathy in amyloid-β oligomer-injected mice is due to their widespread diffusion invivo

Neurobiology of Aging

Volumn 36, Issue 6, 2015, Pages 2043-2052

  Epelbaum, Stéphane ^a,b   Youssef, Ihsen ^a   Lacor, Pascale N ^c   Chaurand, Pierre ^d   Duplus, Eric ^e   Brugg, Bernard ^e   Duyckaerts, Charles ^a,b   Delatour, Benoît ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e Université Pierre et Marie Curie   (France)

Author keywords

Alzheimer's disease; Amyloid ; Invivo animal model; Neurotoxicity; Oligomers

Indexed keywords

AMYLOID BETA PROTEIN; OLIGOMER; POSTSYNAPTIC DENSITY PROTEIN 95; TAU PROTEIN; BIOPOLYMER; DLGH4 PROTEIN, MOUSE; GUANYLATE KINASE; MEMBRANE PROTEIN;

AMNESIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DIFFUSION; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR WEIGHT; MOUSE; NEUROPATHOLOGY; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ACUTE DISEASE; ALZHEIMER DISEASE; ANIMAL; BRAIN; BRAIN DISEASE; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; HIPPOCAMPUS; INJECTION; METABOLISM; PHOSPHORYLATION; SYNAPSE; TIME; TRANSPORT AT THE CELLULAR LEVEL;

ACUTE DISEASE; ALZHEIMER DISEASE; AMNESIA; AMYLOID BETA-PEPTIDES; ANIMALS; BIOLOGICAL TRANSPORT; BIOPOLYMERS; BRAIN; BRAIN DISEASES; DIFFUSION; GUANYLATE KINASE; HIPPOCAMPUS; INJECTIONS; MALE; MEMBRANE PROTEINS; MICE, INBRED C57BL; MOLECULAR WEIGHT; PHOSPHORYLATION; SYNAPSES; TAU PROTEINS; TIME FACTORS;

EID: 84929275414     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.03.005     Document Type: Article

References (67)

1. Abbott N.J. Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem. Int. 2004, 45:545-552.
2. Amieva H., Mokri H., Le Goff M., Meillon C., Jacqmin-Gadda H., Foubert-Samier A., Orgogozo J.M., Stern Y., Dartigues J.F. Compensatory mechanisms in higher-educated subjects with Alzheimer's disease: a study of 20 years of cognitive decline. Brain 2014, 137(Pt 4):1167-1175.
3. Bakker A., Krauss G.L., Albert M.S., Speck C.L., Jones L.R., Stark C.E., Yassa M.A., Bassett S.S., Shelton A.L., Gallagher M. Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 2012, 74:467-474.
4. Balducci C., Beeg M., Stravalaci M., Bastone A., Sclip A., Biasini E., Tapella L., Colombo L., Manzoni C., Borsello T., Chiesa R., Gobbi M., Salmona M., Forloni G. Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2295-2300.
5. Bateman R.J., Xiong C., Benzinger T.L., Fagan A.M., Goate A., Fox N.C., Marcus D.S., Cairns N.J., Xie X., Blazey T.M., Holtzman D.M., Santacruz A., Buckles V., Oliver A., Moulder K., Aisen P.S., Ghetti B., Klunk W.E., McDade E., Martins R.N., Masters C.L., Mayeux R., Ringman J.M., Rossor M.N., Schofield P.R., Sperling R.A., Salloway S., Morris J.C. Clinical and biomarker changes in dominantly inherited Alzheimer's disease. N.Engl. J. Med. 2012, 367:795-804. DominantlyInheritedAlzheimerNetwork.
6. Benilova I., Karran E., De Strooper B. The toxic Aß oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 2012, 15:349-357.
7. Braak H., Braak E. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol. Aging 1997, 18:351-357.
8. Braudeau J., Dauphinot L., Duchon a., Loistron a., Dodd R.H., Hérault Y., Delatour B., Potier M.C. Chronic treatment with a promnesiant GABA-a α5-selective inverse agonist increases immediate early genes expression during memory processing in mice and rectifies their expression levels in a Down syndrome mouse model. Adv. Pharmacol. Sci. 2011, 2011:153218.
9. Brouillette J., Caillierez R., Zommer N., Alves-Pires C., Benilova I., Blum D., De Strooper B., Buée L. Neurotoxicity and memory deficits induced by soluble low-molecular-weight amyloid-ß1-42 oligomers are revealed invivo by using a novel animal model. J.Neurosci. 2012, 32:7852-7861.
10. Carare R.O., Bernardes-Silva M., Newman T.A., Page A.M., Nicoll J.A.R., Perry V.H., Weller R.O. Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol. Appl. Neurobiol. 2008, 34:131-144.
11. Chaurand P. Imaging mass spectrometry of thin tissue sections: a decade of collective efforts. J.Proteomics 2012, 75:4883-4892.
12. Chaurand P., Schriver K.E., Caprioli R.M. Instrument design and characterization for high resolution MALDI-MS imaging of tissue sections. J.Mass Spectrom. 2007, 42:476-489.
13. Chromy B.A., Nowak R.J., Lambert M.P., Viola K.L., Chang L., Velasco P.T., Jones B.W., Fernandez S.J., Lacor P.N., Horowitz P., Finch C.E., Krafft G.A., Klein W.L. Self-assembly of Abeta(1-42) into globular neurotoxins. Biochemistry 2003, 42:12749-12760.
14. Cleary J.P., Walsh D.M., Hofmeister J.J., Shankar G.M., Kuskowski M.A., Selkoe D.J., Ashe K.H. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci. 2005, 8:79-84.
15. Cornett D.S., Reyzer M.L., Chaurand P., Caprioli R.M. MALDI imaging mass spectrometry: molecular snapshots of biochemical systems. Nat. Methods 2007, 4:828-833.
16. de Chaumont F., Dallongeville S., Chenouard N., Herve N., Pop S., Provoost T., Meas-Yedid V., Pankajakshan P., Lecomte T., Le Montagner Y., Lagache T., Dufour A., Olivo-Marin J.C. Icy: an open bioimage informatics platform for extended reproducible research. Nat. Methods 2012, 9:690-696.
17. De Felice F.G., Wu D., Lambert M.P., Fernandez S.J., Velasco P.T., Lacor P.N., Bigio E.H., Jerecic J., Acton P.J., Shughrue P.J., Chen-Dodson E., Kinney G.G., Klein W.L. Alzheimer's disease-type neuronal tau hyperphosphorylation induced by A beta oligomers. Neurobiol. Aging 2008, 29:1334-1347.
18. Dickerson B.C., Sperling R.A. Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer's disease: insights from functional MRI studies. Neuropsychologia 2008, 46:1624-1635.
19. Doody R.S., Thomas R.G., Farlow M., Iwatsubo T., Vellas B., Joffe S., Kieburtz K., Raman R., Sun X., Aisen P.S., Siemers E., Liu-Seifert H., Mohs R. Phase 3 trials of solanezumab for mild-to-moderate Alzheimer's disease. N.Engl. J. Med. 2014, 370:311-321. Alzheimer's DiseaseCooperative Study Steering Committee;SolanezumabStudy Group.
20. Dubois A., Herard A.S., Delatour B., Hantraye P., Bonvento G., Dhenain M., Delzescaux T. Detection by voxel-wise statistical analysis of significant changes in regional cerebral glucose uptake in an APP/PS1 transgenic mouse model of Alzheimer's disease. Neuroimage 2010, 51:586-598.
21. Duyckaerts C., Delatour B.T., Potier M.-C. Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 2009, 118:5-36.
22. Eisele Y.S. From soluble abeta to progressive abeta aggregation: could prion-like templated misfolding play a role?. Brain Pathol. 2013, 23:333-341.
23. Fantini J., Di Scala C., Yahi N., Troadec J.D., Sadelli K., Chahinian H., Garmy N. Bexarotene blocks calcium-permeable ion channels formed by neurotoxic Alzheimer's ss-amyloid peptides. ACS Chem. Neurosci. 2014, 5:216-224.
24. Figueiredo C.P., Clarke J.R., Ledo J.H., Ribeiro F.C., Costa C.V., Melo H.M., Mota-Sales A.P., Saraiva L.M., Klein W.L., Sebollela A., De Felice F.G., Ferreira S.T. Memantine rescues transient cognitive impairment caused by high-molecular-weight abeta oligomers but not the persistent impairment induced by low-molecular-weight oligomers. J.Neurosci. 2013, 33:9626-9634.
25. Fukumoto H., Tokuda T., Kasai T., Ishigami N., Hidaka H., Kondo M., Allsop D., Nakagawa M. High-molecular-weight beta-amyloid oligomers are elevated in cerebrospinal fluid of Alzheimer patients. FASEB J. 2010, 24:2716-2726.
26. Games D., Khan K.M., Soriano F.G., Keim P.S., Davis D.L., Bryant K., Lieberburg I. Lack of Alzheimer pathology after beta-amyloid protein injections in rat brain. Neurobiol. Aging 1992, 13:569-576.
27. Garcia P., Youssef I., Utvik J.K., Florent-Béchard S., Barthélémy V., Malaplate-Armand C., Kriem B., Stenger C., Koziel V., Olivier J.-L., Escanye M.-C., Hanse M., Allouche A., Desbène C., Yen F.T., Bjerkvig R., Oster T., Niclou S.P., Pillot T. Ciliary neurotrophic factor cell-based delivery prevents synaptic impairment and improves memory in mouse models of Alzheimer's disease. J.Neurosci. 2010, 30:7516-7527.
28. Gilman S., Koller M., Black R.S., Jenkins L., Griffith S.G., Fox N.C., Eisner L., Kirby L., Rovira M.B., Forette F., Orgogozo J.M. Clinical effects of Abeta immunization (AN1792) in patients with AD in an interrupted trial. Neurology 2005, 64:1553-1562.
29. Goure W.F., Krafft G.A., Jerecic J., Hefti F. Targeting the proper amyloid-beta neuronal toxins: a path forward for Alzheimer's disease immunotherapeutics. Alzheimers Res. Ther. 2014, 6:42.
30. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
31. Hardy J.A., Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992, 256:184-185.
32. Holmes C., Boche D., Wilkinson D., Yadegarfar G., Hopkins V., Bayer A., Jones R.W., Bullock R., Love S., Neal J.W., Zotova E., Nicoll J.A.R. Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 2008, 372:216-223.
33. Hong S., Ostaszewski B.L., Yang T., O'Malley T.T., Jin M., Yanagisawa K., Li S., Bartels T., Selkoe D.J. Soluble abeta oligomers are rapidly sequestered from brain ISF invivo and bind GM1 ganglioside on cellular membranes. Neuron 2014, 82:308-319.
34. Jin M., Shepardson N., Yang T., Chen G., Walsh D., Selkoe D.J. Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5819-5824.
35. Jucker M., Walker L.C. Pathogenic protein seeding in alzheimer disease and other neurodegenerative disorders. Ann. Neurol. 2011, 70:532-540.
36. Kayed R., Head E., Sarsoza F., Saing T., Cotman C.W., Necula M., Margol L., Wu J., Breydo L., Thompson J.L., Rasool S., Gurlo T., Butler P., Glabe C.G. 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.
37. Klein W.L. Abeta toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem. Int. 2002, 41:345-352.
38. Lacor P.N. Advances on the understanding of the origins of synaptic pathology in AD. Curr. Genomics 2007, 8:486-508.
39. Lacor P.N., Buniel M.C., Chang L., Fernandez S.J., Gong Y., Viola K.L., Lambert M.P., Velasco P.T., Bigio E.H., Finch C.E., Krafft G.A., Klein W.L. Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J.Neurosci. 2004, 24:10191-10200.
40. Lacor P.N., Buniel M.C., Furlow P.W., Clemente A.S., Velasco P.T., Wood M., Viola K.L., Klein W.L. Abeta oligomer-induced 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.
41. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6448-6453.
42. Lambert M.P., Velasco P.T., Chang L., Viola K.L., Fernandez S., Lacor P.N., Khuon D., Gong Y., Bigio E.H., Shaw P., De Felice F.G., Krafft G.A., Klein W.L. Monoclonal antibodies that target pathological assemblies of Abeta. J.Neurochem. 2007, 100:23-35.
43. Lesne S.E. Breaking the code of amyloid- oligomers. Int. J. Cell Biol. 2013, 2013:950783.
44. Lesne S.E., Sherman M.A., Grant M., Kuskowski M., Schneider J.A., Bennett D.A., Ashe K.H. Brain amyloid-beta oligomers in ageing and Alzheimer's disease. Brain 2013, 136(Pt 5):1383-1398.
45. Martins I.C., Kuperstein I., Wilkinson H., Maes E., Vanbrabant M., Jonckheere W., Van Gelder P., Hartmann D., D'Hooge R., De Strooper B., Schymkowitz J., Rousseau F. Lipids revert inert Abeta amyloid fibrils to neurotoxic protofibrils that affect learning in mice. EMBO J. 2008, 27:224-233.
46. McLean C.A., Cherny R.A., Fraser F.W., Fuller S.J., Smith M.J., Beyreuther K., Bush A.I., Masters C.L. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 1999, 46:860-866.
47. Moon M., Choi J.G., Nam D.W., Hong H.S., Choi Y.J., Oh M.S., Mook-Jung I. Ghrelin ameliorates cognitive dysfunction and neurodegeneration in intrahippocampal amyloid-beta1-42 oligomer-injected mice. J.Alzheimers Dis. 2011, 23:147-159.
48. Moser M.B., Moser E.I., Forrest E., Andersen P., Morris R.G. Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9697-9701.
49. Olivo-Marin J.C. Extraction of spots in biological images using multiscale products. Pattern Recognition 2002, 35:1986-1996.
50. Palop J.J., Chin J., Roberson E.D., Wang J., Thwin M.T., Bien-Ly N., Yoo J., Ho K.O., Yu G.Q., Kreitzer A., Finkbeiner S., Noebels J.L., Mucke L. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007, 55:697-711.
51. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates: Compact Second Edition 2004, San Diego, CA: Academic Press.
52. Pearson-Leary J., McNay E.C. Intrahippocampal administration of amyloid-beta(1-42) oligomers acutely impairs spatial working memory, insulin signaling, and hippocampal metabolism. J.Alzheimers Dis. 2012, 30:413-422.
53. Renner M., Lacor P.N., Velasco P.T., Xu J., Contractor A., Klein W.L., Triller A. Deleterious effects of amyloid ß oligomers acting as an extracellular scaffold for mGluR5. Neuron 2010, 66:739-754.
54. Salloway S., Sperling R., Fox N.C., Blennow K., Klunk W., Raskind M., Sabbagh M., Honig L.S., Porsteinsson A.P., Ferris S., Reichert M., Ketter N., Nejadnik B., Guenzler V., Miloslavsky M., Wang D., Lu Y., Lull J., Tudor I.C., Liu E., Grundman M., Yuen E., Black R., Brashear H.R. Two phase 3 trials of bapineuzumab in mild-to-moderate Alzheimer's disease. N.Engl. J. Med. 2014, 370:322-333. Bapineuzumab301 and 302 Clinical Trial Investigators.
55. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
56. Selkoe D.J. Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav. Brain Res. 2008, 192:106-113.
57. Stine W.B., Dahlgren K.N., Krafft G.A., LaDu M.J. Invitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J.Biol. Chem. 2003, 278:11612-11622.
58. Sykova E., Vargova L. Extrasynaptic transmission and the diffusion parameters of the extracellular space. Neurochem. Int. 2008, 52:5-13.
59. Takeda S., Hashimoto T., Roe A.D., Hori Y., Spires-Jones T.L., Hyman B.T. Brain interstitial oligomeric amyloid beta increases with age and is resistant to clearance from brain in a mouse model of Alzheimer's disease. FASEB J. 2013, 27:3239-3248.
60. Terleph T.A., Tremere L.A. The Use of Immediate Early Genes as Mapping Tools for Neuronal Activation: Concepts and Methods 2006, 1-10. New York: Springer Science.
61. Thal D.R., Rub U., Orantes M., Braak H. Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 2002, 58:1791-1800.
62. Townsend M., Shankar G.M., Mehta T., Walsh D.M., Selkoe D.J. Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: a potent role for trimers. J.Physiol. 2006, 572(Pt 2):477-492.
63. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation invivo. Nature 2002, 416:535-539.
64. Wilcox K.C., Lacor P.N., Pitt J., Klein W.L. Aß oligomer-induced synapse degeneration in Alzheimer's disease. Cell Mol. Neurobiol. 2011, 31:939-948.
65. Xie L., Kang H., Xu Q., Chen M.J., Liao Y., Thiyagarajan M., O'Donnell J., Christensen D.J., Nicholson C., Iliff J.J., Takano T., Deane R., Nedergaard M. Sleep drives metabolite clearance from the adult brain. Science 2013, 342:373-377.
66. Youssef I., Florent-Béchard S., Malaplate-Armand C., Koziel V., Bihain B., Olivier J.-L., Leininger-Muller B., Kriem B., Oster T., Pillot T. N-truncated amyloid-beta oligomers induce learning impairment and neuronal apoptosis. Neurobiol. Aging 2008, 29:1319-1333.
67. Zempel H., Thies E., Mandelkow E., Mandelkow E.-M. Abeta oligomers cause localized Ca(2+) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J.Neurosci. 2010, 30:11938-11950.