Amyloid-β Protofibrils: Size, Morphology and Synaptotoxicity of an Engineered Mimic

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Dubnovitsky, Anatoly ^a,e   Sandberg, Anders ^b   Rahman, M Mahafuzur ^a   Benilova, Iryna ^c,d   Lendel, Christofer ^a   Härd, Torleif ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b Alzinova AB   (Sweden)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E; NANOPARTICLE;

ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; ARTICLE; BETA SHEET; BINDING AFFINITY; BRAIN REGION; CONTROLLED STUDY; HIPPOCAMPUS; HUMAN; HYDROPHOBICITY; MOUSE; NERVE CELL; NERVE FIBER; NEUROBLASTOMA; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PARTICLE SIZE; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTOFIBRIL; SURFACE PROPERTY; SYNAPTOTOXICITY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEINS E; BINDING SITES; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; HUMANS; MICE; MICROSCOPY, ATOMIC FORCE; MOLECULAR MIMICRY; NEURONS; PARTICLE SIZE; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN STRUCTURE, SECONDARY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84879773805     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066101     Document Type: Article

References (46)

1. Querfurth HW, LaFerla FM, (2010) Alzheimer's disease. N Engl J Med 362: 329-344.
2. Hepler RW, Grimm KM, Nahas DD, Breese R, Dodson EC, et al. (2006) Solution state characterization of amyloid β-derived diffusible ligands. Biochemistry 45: 15157-15167.
3. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, et al. (1998) Diffusible, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95: 6448-6453.
4. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, et al. (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440: 352-357.
5. Martins IC, Kuperstein I, Wilkinson H, Maes E, Vanbrabant M, et al. (2008) Lipids revert inert Aβ amyloid fibrils to neurotoxic protofibrils that affect learning in mice. EMBO J 27: 224-233.
6. Ono K, Condron MM, Teplow DB, (2009) Structure-neurotoxicity relationships of amyloid β-protein oligomers. Proc Natl Acad Sci USA 106: 14745-14750.
7. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, et al. (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
8. Hartley DM, Walsh DM, Ye CP, Diehl T, Vasquez S, et al. (1999) Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J Neurosci 19: 8876-8884.
9. Kuperstein I, Broersen K, Benilova I, Rozenski J, Jonckheere W, et al. (2010) Neurotoxicity of Alzheimer's disease Aβ peptides is induced by small changes in the Aβ42 to Aβ40 ratio. EMBO J 29: 3408-3420.
10. Jan A, Adolfsson O, Allaman I, Buccarello A-L, Magistretti PJ, et al. (2011) Aβ42 neurotoxicity is mediated by ongoing nucleated polymerization process rather than by discrete Aβ42 species. J Biol Chem 286: 8585-8596.
11. Wogulis M, Wright S, Cunningham D, Chilote T, Powell K, et al. (2005) Nucleation-dependent polymerization is an essential component of amyloid-mediated neuronal cell death. J Neurosci 21: 1071-1080.
12. Jan A, Hartley DM, Lashuel HA, (2010) Preparation and characterization of toxic Aβ aggregates for structural and functional studies in Alzheimer's disease research. Nat Protoc 5: 1186-1209.
13. Roychaudhuri R, Yang M, Hoshi MM, Teplow DB, (2009) Amyloid β-protein assembly and Alzheimer disease. J Biol Chem 284: 4749-4753.
14. Chiti F, Dobson CM, (2006) Protein misfolding, functional amyloid, and human disease. Ann Rev Biochem 75: 333-366.
15. Härd T, (2011) Protein engineering to stabilize soluble amyloid β-protein aggregates for structural and functional studies. FEBS J 278: 3884-3392.
16. Sandberg A, Luheshi LM, Söllvander S, de Barros TP, Macao B, et al. (2010) Stabilization of neurotoxic Alzheimer amyloid-β oligomers by protein engineering. Proc Natl Acad Sci USA 107: 15595-19600.
17. Caughey B, Lansbury PT, (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Ann Rev Neurosci 26: 267-298.
18. Hoyer W, Grönwall C, Jonsson A, Ståhl S, Härd T, (2008) Stabilization of a β-hairpin in monomeric Alzheimer's amyloid-β peptide inhibits amyloid formation. Proc Natl Acad Sci USA 105: 5099-5104.
19. Macao B, Hoyer W, Sandberg A, Brorsson A-C, Dobson CM, et al. (2008) Recombinant amyloid β-peptide production by coexpression with an Affibody ligand. BMC Biotechnology 8: 82.
20. Schuck P, (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78: 1606-1619.
21. Kayed R, Head E, Sarsoza F, Saing T, Cotman CW, et al. (2007) Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol Neurodegeneration 2: 18.
22. Perkins DN, Pappin DJC, Creasy DM, Cottrell JS, (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
23. Goldsbury CS, Wirtz S, Müller SA, Sunderji S, Wicki P, et al. (2000) Studies on the in vitro assembly of Aβ 1-40: implications for the search for Aβ fibril formation inhibitors. J Struct Biol 130: 217-231.
24. Walsh DM, Lomakin A, Benedek GB, Condron MM, Teplow DB, (1997) Amyloid β-protein fibrillogenesis. Detection of a protofibrillar intermediate. J Biol Chem 272: 22364-22372.
25. Nichols MR, Moss MA, Reed DK, Lin W-L, Mukhopadhyay R, et al. (2002) Growth of β-amyloid(1-40) protofibrils by monomer elongation and lateral association. Characterization of distinct products by light scattering and atomic force microscopy. Biochemistry 41: 6115-6127.
26. Cantor CR, Schimmel PR (1980) Biophysical Chemistry: W.H. Freeman and Company.
27. Filipe V, Poole R, Kutscher M, Forier K, Braeckmans K, et al. (2011) Fluorescence single particle tracking for the characterization of submicron protein aggregates in biological fluids and complex formulations. Pharm Res 28: 1112-1120.
28. Hawe A, Sutter M, Jiskoot W, (2008) Extrinsic fluorescent dyes as tools for protein characterization. Pharm Res 25: 1487-1489.
29. Matthews C, (1993) Pathways of protein folding. Ann Rev Biochem 62: 653-683.
30. Bolognesi B, Kumita J, Barros T, Esbjörner E, Luheshi L, et al. (2010) ANS binding reveals common features of cytotoxic amyloid species. ACS Chem Biol 5: 735-740.
31. Englund H, Sehlin D, Johansson A-S, Nilsson LNG, Gellerfors P, et al. (2007) Sensitive detection of amyloid-β protofibrils in biological samples. J Neurochem 103: 334-345.
32. 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.
33. Glabe CG, (2008) Structural classification of toxic amyloid oligomers. J Biol Chem 283: 29639-29643.
34. Cerf E, Gustot A, Goormaghtigh E, Ruysschaert J-M, Raussens V, (2011) High ability of apolipoprotein E4 to stabilize amyloid-β peptide oligomers, the pathological entities responsible for Alzheimer's disease. FASEB J 25: 1585-1595.
35. Harper JD, Wong SS, Lieber CM, Lansbury PT, (1997) Observation of metastable Aβ amyloid protofibrils by atomic force microscopy. Chem Biol 4: 119-125.
36. Nilsberth C, Westlind-Danielsson A, Eckman CB, Condron MM, Axelman K, et al. (2001) The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Aβ protofibril formation. Nat Neurosci 4: 887-893.
37. Luheshi LM, Hoyer W, de Barros TP, Härd IvD, Brorsson A-C, et al. (2010) Sequestration of the Aβ peptide prevents toxicity and promotes degradation in vivo. PLoS Biology 8: e1000334.
38. Stroud JC, Liu C, Teng PK, Eisenberg D, (2012) Toxic fibrillar oligomers of amyloid-β have cross-β structure. Proc Natl Acad Sci USA 109: 7717-7722.
39. Hoyer W, Härd T, (2008) Interaction of Alzheimer's Aβ peptide with an engineered binding protein-thermodynamics and kinetics of coupled folding-binding. J Mol Biol 378: 398-411.
40. Lam AR, Teplow DB, Stanely HE, Urbanc B, (2008) Effects of the Arctic (E22->G) mutation on amyloid β-protein folding: discrete molecular dynamics study. J Am Chem Soc 130: 17413-17422.
41. Lazo ND, Grant MA, Condron MC, Rigby AC, Teplow DB, (2005) On the nucleation of amyloid β-protein monomer folding. Protein Sci 14: 1581-1596.
42. Mitternacht S, Staneva I, Härd T, Irbäck A, (2010) Comparing the folding free-energy landscape of Aβ42 variants with different aggregation properties. Proteins 78: 2600-2608.
43. Sgourakis NG, Yan Y, McCallum SA, Wang C, Garcia AE, (2007) The Alzheimer's peptides Aβ40 and 42 adopt distinct conformations in water: a combined MD/NMR study. J Mol Biol 368: 1448-1457.
44. Yu L, Edalji R, Harlan J, Holzman T, Lopez A, et al. (2009) Structural characterization of a soluble amyloid β-peptide oligomer. Biochemistry 48: 1870-1877.
45. Cerf E, Sarroukh R, Tamamizu-Kato S, Breydo L, Derclaye S, et al. (2009) Antiparallel β-sheet: a signature structure of the oligomeric amyloid β-peptide. Biochem J 421: 415-423.
46. Jin M, Shepardson N, Yang T, Chen G, Walsh D, et al. (2011) Soluble amyloid β-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosporylation and neuritic degeneration. Proc Natl Acad Sci USA 108: 5819-5824.