Conversion of synthetic Aβ to In Vivo active seeds and amyloid plaque formation in a hippocampal slice culture model

Journal of Neuroscience

Volumn 36, Issue 18, 2016, Pages 5084-5093

  Novotny, Renata ^a,b,c   Langer, Franziska ^a,b   Mahler, Jasmin ^a,b,c   Skodras, Angelos ^a,b   Vlachos, Andreas ^d   Wegenast Braun, Bettina M ^a,b   Kaeser, Stephan A ^a,b   Neher, Jonas J ^a,b   Eisele, Yvonne S ^a,b   Pietrowski, Marie J ^e   Nilsson, K Peter R ^f   Deller, Thomas ^d   Staufenbiel, Matthias ^a,b   Heimrich, Bernd ^e   Jucker, Mathias ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d GOETHE UNIVERSITY   (Germany)

^e UNIVERSITY OF FREIBURG   (Germany)

^f LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Alzheimer; Amyloid; Neurodegeneration; Prion like seeding; Slice culture

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; PRION PROTEIN; SYNTHETIC PEPTIDE;

ALZHEIMER DISEASE; AMYLOID PLAQUE; AMYLOIDOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHEMILUMINESCENCE IMMUNOASSAY; CONTROLLED STUDY; DEPLETION; DYSTROPHY; ELECTRON MICROSCOPY; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; IMMUNOHISTOCHEMISTRY; INFANT; MALE; MICROGLIA; MORPHOMETRICS; MOUSE; NERVE DEGENERATION; NEWBORN; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; SPECTROSCOPY; TISSUE HOMOGENATE; ANIMAL; C57BL MOUSE; HIPPOCAMPUS; METABOLISM; NERVE CELL; NEURITE; ORGAN CULTURE TECHNIQUE; PATHOLOGY; TRANSGENIC MOUSE;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOIDOSIS; ANIMALS; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; NEURITES; NEURONS; ORGAN CULTURE TECHNIQUES; PLAQUE, AMYLOID;

EID: 84965036141     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0258-16.2016     Document Type: Article

References (58)

1. Bahr BA (1995) Long-term hippocampal slices: a model system for investigating synaptic mechanisms and pathologic processes. J Neurosci Res 42: 294-305. CrossRef Medline
2. Bittner T, Fuhrmann M, Burgold S, Ochs SM, Hoffmann N, Mitteregger G, Kretzschmar H, LaFerla FM, Herms J (2010) Multiple events lead to dendritic spine loss in triple transgenic Alzheimer’s disease mice. PLoS One 5: e15477. CrossRef Medline
3. Bondolfi L, Calhoun M, Ermini F, Kuhn HG, Wiederhold KH, Walker L, Staufenbiel M, Jucker M (2002) Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J Neurosci 22: 515-522. Medline
4. Brinks H, Conrad S, Vogt J, Oldekamp J, Sierra A, Deitinghoff L, Bechmann I, Alvarez-Bolado G, Heimrich B, Monnier PP, Mueller BK, Skutella T (2004) The repulsive guidance molecule RGMa is involved in the formation of afferent connections in the dentate gyrus. J Neurosci 24: 3862-3869. CrossRef Medline
5. Calhoun ME, Wiederhold KH, Abramowski D, Phinney AL, Probst A, Sturchler-Pierrat C, Staufenbiel M, Sommer B, JuckerM (1998) Neuron loss in APP transgenic mice. Nature 395: 755-756. CrossRef Medline
6. Choi SH, Kim YH, Hebisch M, Sliwinski C, Lee S, D’Avanzo C, Chen H, Hooli B, Asselin C, Muffat J, Klee JB, Zhang C, Wainger BJ, Peitz M, Kovacs DM, Woolf CJ, Wagner SL, Tanzi RE, Kim DY (2014) A three-dimensional human neural cell culture model of Alzheimer’s disease. Nature 515: 274-278. CrossRef Medline
7. Dasilva KA, Shaw JE, McLaurin J (2010) Amyloid-beta fibrillogenesis: structural insight and therapeutic intervention. Exp Neurol 223: 311-321. CrossRef Medline
8. Del Turco D, Deller T (2007) Organotypic entorhino-hippocampal slice cultures: a tool to study the molecular and cellular regulation of axonal regeneration and collateral sprouting in vitro. Methods Mol Biol 399: 55-66. CrossRef Medline
9. Du D, Murray AN, Cohen E, Kim HE, Simkovsky R, Dillin A, Kelly JW (2011) A kinetic aggregation assay allowing selective and sensitive amyloid-beta quantification in cells and tissues. Biochemistry 50: 1607-1617. CrossRef Medline
10. Duyckaerts C, Potier MC, Delatour B (2008) Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol 115: 5-38. CrossRef Medline
11. Eisele YS, Obermüller U, Heilbronner G, Baumann F, Kaeser SA, Wolburg H, Walker LC, Staufenbiel M, Heikenwalder M, JuckerM (2010) Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis. Science 330: 980-982. CrossRef Medline
12. Eisele YS, Fritschi SK, Hamaguchi T, Obermüller U, Füger P, Skodras A, Schäfer C, Odenthal J, Heikenwalder M, Staufenbiel M, JuckerM (2014) Multiple factors contribute to the peripheral induction of cerebral betaamyloidosis. J Neurosci 34: 10264-10273. CrossRef Medline
13. Eisenberg D, Jucker M (2012) The amyloid state of proteins in human diseases. Cell 148: 1188-1203. CrossRef Medline
14. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51. CrossRef Medline
15. Friedrich RP, Tepper K, Rönicke R, Soom M, Westermann M, Reymann K, Kaether C, FändrichM (2010) Mechanism of amyloid plaque formation suggests an intracellular basis of Abeta pathogenicity. Proc Natl Acad Sci U S A 107: 1942-1947. CrossRef Medline
16. Fritschi SK, Cintron A, Ye L, Mahler J, Bühler A, Baumann F, Neumann M, Nilsson KP, Hammarström P, Walker LC, JuckerM (2014) Abeta seeds resist inactivation by formaldehyde. Acta Neuropathol 128: 477-484. CrossRef Medline
17. Frotscher M, Heimrich B (1993) Formation of layer-specific fiber projections to the hippocampus in vitro. Proc Natl Acad Sci U S A 90: 10400-10403. CrossRef Medline
18. Frotscher M, Zafirov S, Heimrich B (1995) Development of identified neuronal types and of specific synaptic connections in slice cultures of rat hippocampus. Prog Neurobiol 45: vii-xxviii. Medline
19. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373: 523-527. CrossRef Medline
20. Grathwohl SA, Kälin RE, Bolmont T, Prokop S, Winkelmann G, Kaeser SA, Odenthal J, Radde R, Eldh T, Gandy S, Aguzzi A, Staufenbiel M, Mathews PM, Wolburg H, Heppner FL, JuckerM (2009) Formation and mainte-nance of Alzheimer’s disease beta-amyloid plaques in the absence of microglia. Nat Neurosci 12: 1361-1363. CrossRef Medline
21. Hailer NP, Jarhult JD, Nitsch R (1996) Resting microglial cells in vitro: analysis of morphology and adhesion molecule expression in organotypic hippocampal slice cultures. Glia 18: 319-331. CrossRef Medline
22. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297: 353-356. CrossRef Medline
23. Harper JD, Lansbury PT Jr (1997) Models of amyloid seeding in Alzheimer’s disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu Rev Biochem 66: 385-407. CrossRef Medline
24. Harris-White ME, Chu T, Balverde Z, Sigel JJ, Flanders KC, Frautschy SA (1998) Effects of transforming growth factor-beta (isoforms 1-3) on amyloid-beta deposition, inflammation, and cell targeting in organotypic hippocampal slice cultures. J Neurosci 18: 10366-10374. Medline
25. Heilbronner G, Eisele YS, Langer F, Kaeser SA, Novotny R, Nagarathinam A, Aslund A, HammarströmP, Nilsson KP, JuckerM (2013) Seeded strainlike transmission of beta-amyloid morphotypes in APP transgenic mice. EMBO Rep 14: 1017-1022. CrossRef Medline
26. Holtzman DM, Morris JC, Goate AM (2011) Alzheimer’s disease: the challenge of the second century. Sci Transl Med 3: 77sr71. CrossRef Medline
27. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, abeta elevation, and amyloid plaques in transgenic mice. Science 274: 99-102. CrossRef Medline
28. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D (1989) Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol 24: 173-182. CrossRef Medline
29. Johansson S, Radesäter AC, Cowburn RF, Thyberg J, Luthman J (2006) Modelling of amyloid beta-peptide induced lesions using roller-drum incubation of hippocampal slice cultures from neonatal rats. Exp Brain Res 168: 11-24. CrossRef Medline
30. Jucker M (2010) The benefits and limitations of animal models for translational research in neurodegenerative diseases. Nat Med 16: 1210-1214. CrossRef Medline
31. Jucker M, Walker LC (2013) Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501: 45-51. CrossRef Medline
32. Klingstedt T, Aslund A, Simon RA, Johansson LB, Mason JJ, Nyström S, Hammarström P, Nilsson KP (2011) Synthesis of a library of oligothiophenes and their utilization as fluorescent ligands for spectral assignment of protein aggregates. Org Biomol Chem 9: 8356-8370. CrossRef Medline
33. Kohl A, Dehghani F, Korf HW, Hailer NP (2003) The bisphosphonate clodronate depletes microglial cells in excitotoxically injured organotypic hippocampal slice cultures. Exp Neurol 181: 1-11. CrossRef Medline
34. Langer F, Eisele YS, Fritschi SK, Staufenbiel M, Walker LC, JuckerM (2011) Soluble Abeta seeds are potent inducers of cerebral beta-amyloid deposition. J Neurosci 31: 14488-14495. CrossRef Medline
35. Lu JX, Qiang W, Yau WM, Schwieters CD, Meredith SC, Tycko R (2013) Molecular structure of beta-amyloid fibrils in Alzheimer’s disease brain tissue. Cell 154: 1257-1268. CrossRef Medline
36. Mackenzie IR, Hao C, Munoz DG (1995) Role of microglia in senile plaque formation. Neurobiol Aging 16: 797-804. CrossRef Medline
37. Masliah E, Sisk A, Mallory M, Mucke L, Schenk D, Games D (1996) Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein and Alzheimer’s disease. J Neurosci 16: 5795-5811. Medline
38. Mayer D, Fischer H, Schneider U, Heimrich B, SchwemmleM (2005) Borna disease virus replication in organotypic hippocampal slice cultures from rats results in selective damage of dentate granule cells. J Virol 79: 11716-11723. CrossRef Medline
39. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E, Neuenschwander A, Abramowski D, Frey P, Jaton AL, Vigouret JM, Paganetti P, Walsh DM, Mathews PM, Ghiso J, Staufenbiel M, Walker LC, Jucker M (2006) Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 313: 1781-1784. CrossRef Medline
40. Morales-Corraliza J, Mazzella MJ, Berger JD, Diaz NS, Choi JH, Levy E, Matsuoka Y, Planel E, Mathews PM (2009) In vivo turnover of tau and APP metabolites in the brains of wild-type and Tg2576 mice: greater stability of sAPP in the beta-amyloid depositing mice. PLoS One 4: e7134. CrossRef Medline
41. Nagarathinam A, Hoflinger P, Bühler A, Schäfer C, McGovern G, Jeffrey M, Staufenbiel M, Jucker M, Baumann F (2013) Membrane-anchored Abeta accelerates amyloid formation and exacerbates amyloid-associated toxicity in mice. J Neurosci 33: 19284-19294. CrossRef Medline
42. Paravastu AK, Qahwash I, Leapman RD, Meredith SC, Tycko R (2009) Seeded growth of beta-amyloid fibrils from Alzheimer’s brain-derived fibrils produces a distinct fibril structure. Proc Natl Acad Sci U S A 106: 7443-7448. CrossRef Medline
43. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP, Tycko R (2005) Self-propagating, molecular-level polymorphism in Alzheimer’s betaamyloid fibrils. Science 307: 262-265. CrossRef Medline
44. Phinney AL, Deller T, Stalder M, Calhoun ME, Frotscher M, Sommer B, Staufenbiel M, Jucker M (1999) Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J Neurosci 19: 8552-8559. Medline
45. Probst A, Basler V, Bron B, Ulrich J (1983) Neuritic plaques in senile dementia of Alzheimer type: a Golgi analysis in the hippocampal region. Brain Res 268: 249-254. CrossRef Medline
46. Radde R, Bolmont T, Kaeser SA, Coomaraswamy J, Lindau D, Stoltze L, Calhoun ME, Jäggi F, Wolburg H, Gengler S, Haass C, Ghetti B, Czech C, Hölscher C, Mathews PM, Jucker M (2006) Abeta42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep 7: 940-946. CrossRef Medline
47. Raj A, LoCastro E, Kuceyeski A, Tosun D, Relkin N, WeinerM (2015) Network diffusion model of progression predicts longitudinal patterns of atrophy and metabolism in Alzheimer’s disease. Cell Rep 10: 359-369. CrossRef Medline
48. Rupp NJ, Wegenast-Braun BM, Radde R, Calhoun ME, Jucker M (2011) Early onset amyloid lesions lead to severe neuritic abnormalities and local, but not global neuron loss in APPPS1 transgenic mice. Neurobiol Aging 32: 2324-2326. CrossRef Medline
49. Shi Y, Kirwan P, Smith J, MacLean G, Orkin SH, Livesey FJ (2012) A human stem cell model of early Alzheimer’s disease pathology in Down syndrome. Sci Transl Med 4: 124ra129. CrossRef Medline
50. Skibo GG, Nikonenko IR, Savchenko VL, McKanna JA (2000) Microglia in organotypic hippocampal slice culture and effects of hypoxia: ultrastructure and lipocortin-1 immunoreactivity. Neuroscience 96: 427-438. CrossRef Medline
51. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, Bacskai BJ, Hyman BT (2005) Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 25: 7278-7287. CrossRef Medline
52. Stalder M, Phinney A, Probst A, Sommer B, Staufenbiel M, JuckerM (1999) Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am J Pathol 154: 1673-1684. CrossRef Medline
53. Stalder M, Deller T, Staufenbiel M, Jucker M (2001) 3D-Reconstruction of microglia and amyloid in APP23 transgenic mice: no evidence of intracellular amyloid. Neurobiol Aging 22: 427-434. CrossRef Medline
54. Stöhr J, Watts JC, Mensinger ZL, Oehler A, Grillo SK, DeArmond SJ, Prusiner SB, Giles K (2012) Purified and synthetic Alzheimer’s amyloid beta (Abeta) prions. Proc Natl Acad Sci U S A 109: 11025-11030. CrossRef Medline
55. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Bürki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci U S A 94: 13287-13292. CrossRef Medline
56. Terry RD, Gonatas NK, Weiss M (1964) Ultrastructural studies in Alzheimer’s presenile dementia. Am J Pathol 44: 269-297. Medline
57. Vlachos A, Müller-Dahlhaus F, Rosskopp J, Lenz M, Ziemann U, Deller T (2012) Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures. J Neurosci 32: 17514-17523. CrossRef Medline
58. Waters J (2010) The concentration of soluble extracellular amyloid-beta protein in acute brain slices from CRND8 mice. PLoS One 5: e15709. CrossRef Medline