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Single-molecule studies of amyloid proteins: from biophysical properties to diagnostic perspectives

Published online by Cambridge University Press:  05 November 2020

Jinming Wu ,
Chan Cao ,
Rolf Antonie Loch ,
Ann Tiiman  and
Jinghui Luo Open the ORCID record for Jinghui Luo [Opens in a new window]
Jinming Wu
Affiliation:
Department of Biology and Chemistry, Paul Scherrer Institute, 5232, Villigen, Switzerland
Chan Cao
Affiliation:
Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015, Lausanne, Switzerland Swiss Institute of Bioinformatics (SIB), 1015, Lausanne, Switzerland
Rolf Antonie Loch
Affiliation:
Department of Biology and Chemistry, Paul Scherrer Institute, 5232, Villigen, Switzerland
Ann Tiiman
Affiliation:
Department of Clinical Neuroscience (CNS), Center for Molecular Medicine CMM L8:01, Karolinska Institutet, 17176, Stockholm, Sweden
Jinghui Luo*
Affiliation:
Department of Biology and Chemistry, Paul Scherrer Institute, 5232, Villigen, Switzerland
*
Author for correspondence: Jinghui Luo, E-mail: Jinghui.luo@psi.ch
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Abstract

In neurodegenerative diseases, a wide range of amyloid proteins or peptides such as amyloid-beta and α-synuclein fail to keep native functional conformations, followed by misfolding and self-assembling into a diverse array of aggregates. The aggregates further exert toxicity leading to the dysfunction, degeneration and loss of cells in the affected organs. Due to the disordered structure of the amyloid proteins, endogenous molecules, such as lipids, are prone to interact with amyloid proteins at a low concentration and influence amyloid cytotoxicity. The heterogeneity of amyloid proteinscomplicates the understanding of the amyloid cytotoxicity when relying only on conventional bulk and ensemble techniques. As complementary tools, single-molecule techniques (SMTs) provide novel insights into the different subpopulations of a heterogeneous amyloid mixture as well as the cytotoxicity, in particular as involved in lipid membranes. This review focuses on the recent advances of a series of SMTs, including single-molecule fluorescence imaging, single-molecule force spectroscopy and single-nanopore electrical recording, for the understanding of the amyloid molecular mechanism. The working principles, benefits and limitations of each technique are discussed and compared in amyloid protein related studies.. We also discuss why SMTs show great potential and are worthy of further investigation with feasibility studies as diagnostic tools of neurodegenerative diseases and which limitations are to be addressed.

Keywords

Amyloid proteinsingle-molecule techniquessingle-molecule fluorescence imagingsingle-molecule force spectroscopysingle-nanopore electrical recordingneurodegenerative diseases

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Type
Review
Information
Quarterly Reviews of Biophysics , Volume 53 , 2020 , e12
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Adamcik, J and Mezzenga, R (2012) Study of amyloid fibrils via atomic force microscopy. Current Opinion in Colloid & Interface Science 17, 369–376.CrossRefGoogle Scholar
Adamcik, J and Mezzenga, R (2018) Amyloid polymorphism in the protein folding and aggregation energy landscape. Angewandte Chemie International Edition 57, 8370–8382.CrossRefGoogle ScholarPubMed
Adamcik, J, Jung, J-M, Flakowski, J, De Los Rios, P, Dietler, G and Mezzenga, R (2010) Understanding amyloid aggregation by statistical analysis of atomic force microscopy images. Nature Nanotechnology 5, 423–428.CrossRefGoogle ScholarPubMed
Agnarsson, B, Lundgren, A, Gunnarsson, A, Rabe, M, Kunze, A, Mapar, M, Simonsson, L, Bally, M, Zhdanov, VP and Höök, F (2015) Evanescent light-scattering microscopy for label-free interfacial imaging: from single sub-100 nm vesicles to live cells. ACS Nano 9, 11849–11862.CrossRefGoogle ScholarPubMed
Andersen, CB, Yagi, H, Manno, M, Martorana, V, Ban, T, Christiansen, G, Otzen, DE, Goto, Y and Rischel, C (2009) Branching in amyloid fibril growth. Biophysical Journal 96, 1529–1536.CrossRefGoogle ScholarPubMed
Arispe, N, Pollard, HB and Rojas, E (1993a) Giant multilevel cation channels formed by Alzheimer disease amyloid beta-protein A beta 1–40 in bilayer membranes. Proceedings of the National Academy of Sciences 90, 10573–10577.CrossRefGoogle Scholar
Arispe, N, Rojas, E, and Pollard, HB (1993b) Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum.. Proceedings of the National Academy of Sciences 90, 567–571.CrossRefGoogle ScholarPubMed
Arispe, N, Pollard, HB and Rojas, E. (1996) Zn2+ interaction with Alzheimer amyloid beta protein calcium channels. Proceedings of the National Academy of Sciences 93, 1710–1715.CrossRefGoogle ScholarPubMed
Asandei, A, Schiopu, I, Iftemi, S, Mereuta, L and Luchian, T (2013) Investigation of Cu2+ binding to human and rat amyloid fragments Aβ (1–16) with a protein nanopore. Langmuir 29, 15634–15642.CrossRefGoogle Scholar
Asandei, A, Iftemi, S, Mereuta, L, Schiopu, I and Luchian, T (2014) Probing of various physiologically relevant metals-amyloid-β peptide interactions with a lipid membrane-immobilized protein nanopore. Journal of Membrane Biology 247, 523–530.CrossRefGoogle ScholarPubMed
Axelrod, D, Koppel, DE, Schlessinger, J, Elson, E and Webb, WW (1976) Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophysical Journal 16, 1055–1069.CrossRefGoogle ScholarPubMed
Azouz, M, Cullin, C, Lecomte, S and Lafleur, M (2019) Membrane domain modulation of Aβ 1–42 oligomer interactions with supported lipid bilayers: an atomic force microscopy investigation. Nanoscale 11, 20857–20867.CrossRefGoogle Scholar
Balme, S, Coulon, PE, Lepoitevin, M, Charlot, B, Yandrapalli, N, Favard, C, Muriaux, D, Bechelany, M and Janot, JM (2016) Influence of adsorption on proteins and amyloid detection by silicon nitride nanopore. Langmuir 32, 8916–8925.CrossRefGoogle ScholarPubMed
Ban, T, Hoshino, M, Takahashi, S, Hamada, D, Hasegawa, K, Naiki, H and Goto, Y (2004) Direct observation of abeta amyloid fibril growth and inhibition. Journal of Molecular Biology 344, 757–767.CrossRefGoogle ScholarPubMed
Bayley, H, Cronin, B, Heron, A, Holden, MA, Hwang, WL, Syeda, R, Thompson, J and Wallace, M (2008) Droplet interface bilayers. Molecular BioSystems 4, 1191–1208.CrossRefGoogle ScholarPubMed
Benilova, I, Karran, E and De strooper, B (2012) The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nature Neuroscience 15, 349–357.CrossRefGoogle ScholarPubMed
Bertrand, D, Lee, CH, Flood, D, Marger, F and Donnelly-Roberts, D (2015) Therapeutic potential of α7 nicotinic acetylcholine receptors. Pharmacological Reviews 67, 1025–1073.CrossRefGoogle ScholarPubMed
Binnig, G, Quate, CF and Gerber, C (1986) Atomic force microscope. Physical Review Letters 56, 930–933.CrossRefGoogle ScholarPubMed
Blennow, K and Hampel, H (2003) CSF markers for incipient Alzheimer's disease. Lancet Neurology 2, 605–613.CrossRefGoogle ScholarPubMed
Bonito-Oliva, A, Schedin-Weiss, S, Younesi, SS, Tiiman, A, Adura, C, Paknejad, N, Brendel, M, Romin, Y, Parchem, RJ, Graff, C, Vukojević, V, Tjernberg, LO, Terenius, L, Winblad, B, Sakmar, TP and Graham, WV (2019) Conformation-specific antibodies against multiple amyloid protofibril species from a single amyloid immunogen. Journal of Cellular and Molecular Medicine 23, 2103–2114.CrossRefGoogle ScholarPubMed
Brothers, HM, Gosztyla, ML and Robinson, SR (2018) The physiological roles of amyloid-beta peptide hint at new ways to treat Alzheimer's disease. Frontiers in Aging Neuroscience 10, 118.CrossRefGoogle ScholarPubMed
Bu, B, Tong, X, Li, DC, Hu, Y, He, WX, Zhao, CY, Hu, R, Li, XQ, Shao, YP, Liu, C, Zhao, Q, Ji, BH and Diao, JJ (2017) N-Terminal Acetylation Preserves α-Synuclein from Oligomerization by Blocking Intermolecular Hydrogen Bonds. ACS Chemical Neuroscience 8, 2145–2151.CrossRefGoogle ScholarPubMed
Castro, CE, Dong, J, Boyce, MC, Lindquist, S and Lang, MJ (2011) Physical properties of polymorphic yeast prion amyloid fibers. Biophysical Journal 101, 439–448.CrossRefGoogle ScholarPubMed
Cecon, E, Dam, J, Luka, M, Gautier, C, Chollet, AM, Delagrange, P, Danober, L and Jockers, R (2019) Quantitative assessment of oligomeric amyloid β peptide binding to α7 nicotinic receptor. British Journal of Pharmacology 176, 3475–3488.CrossRefGoogle ScholarPubMed
Chaari, A, Horchani, H, Frikha, F, Verger, R, Gargouri, Y and Ladjimi, M (2013) Surface behavior of α-synuclein and its interaction with phospholipids using the Langmuir monolayer technique: a comparison between monomeric and fibrillar α-synuclein. International Journal of Biological Macromolecules 58, 190–198.CrossRefGoogle ScholarPubMed
Chen, Q and Liu, Z (2019) Fabrication and applications of solid-state nanopores. Sensors 19, 8.Google ScholarPubMed
Chen, GF, Xu, TH, Yan, Y, Zhou, YR, Jiang, Y, Melcher, K and Xu, HE (2017) Amyloid beta: structure, biology and structure-based therapeutic development. Acta Pharmacologica Sinica 38, 1205–1235.CrossRefGoogle ScholarPubMed
Chiou, A, Hägglöf, P, Orte, A, Chen, AY, Dunne, PD, Belorgey, D, Karlsson-LI, S, Lomas, DA and Klenerman, D (2009) Probing neuroserpin polymerization and interaction with amyloid-beta peptides using single molecule fluorescence. Biophysical Journal 97, 2306–2315.CrossRefGoogle ScholarPubMed
Chiti, F and Dobson, CM (2006) Protein Misfolding, Functional Amyloid, and Human Disease. Annual Review of Biochemistry 75, 333–366.CrossRefGoogle ScholarPubMed
Chiti, F and Dobson, CM (2017) Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annual Review of Biochemistry 86, 27–68.CrossRefGoogle ScholarPubMed
Connelly, L, Jang, H, Arce, FT, Capone, R, Kotler, SA, Ramachandran, S, Kagan, BL, Nussinov, R and Lal, R (2012) Atomic force microscopy and MD simulations reveal pore-like structures of all-D-enantiomer of Alzheimer's β-amyloid peptide: relevance to the ion channel mechanism of AD pathology. Journal of Physical Chemistry B 116, 1728–1735.CrossRefGoogle ScholarPubMed
Conway, KA, Lee, SJ, Rochet, JC, Ding, TT, Williamson, RE and Lansbury, PT Jr (2000) Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proceedings of the National Academy of Sciences 97, 571–576.CrossRefGoogle Scholar
Cremades, N, Cohen, SI, Deas, E, Abramov, AY, Chen, AY, Orte, A, Sandal, M, Clarke, RW, Dunne, P, Aprile, FA, Bertoncini, CW, Wood, NW, Knowles, TP, Dobson, CM and Klenerman, D (2012) Direct observation of the interconversion of normal and toxic forms of α-synuclein. Cell 149, 1048–1059.CrossRefGoogle ScholarPubMed
De, S, Whiten, DR, Ruggeri, FS, Hughes, C, Rodrigues, M, Sideris, DI, Taylor, CG, Aprile, FA, Muyldermans, S, Knowles, TPJ, Vendruscolo, M, Bryant, C, Blennow, K, Skoog, I, Kern, S, Zetterberg, H and Klenerman, D (2019) Soluble aggregates present in cerebrospinal fluid change in size and mechanism of toxicity during Alzheimer's disease progression. Acta Neuropathologica Communications 7, 120.CrossRefGoogle ScholarPubMed
Devic, I, Hwang, H, Edgar, JS, Izutsu, K, Presland, R, Pan, C, Goodlett, DR, Wang, Y, Armaly, J, Tumas, V, Zabetian, CP, Leverenz, JB, Shi, M and Zhang, J (2011) Salivary α-synuclein and DJ-1: potential biomarkers for Parkinson's disease. Brain 134, e178–e178.CrossRefGoogle ScholarPubMed
Ding, H, Wong, PT, Lee, EL, Gafni, A and Steel, DG (2009) Determination of the oligomer size of amyloidogenic protein beta-amyloid(1–40) by single-molecule spectroscopy. Biophysical Journal 97, 912–921.CrossRefGoogle ScholarPubMed
Ding, H, Schauerte, JA, Steel, DG and Gafni, A (2012) β-Amyloid (1–40) peptide interactions with supported phospholipid membranes: a single-molecule study. Biophysical Journal 103, 1500–1509.CrossRefGoogle ScholarPubMed
Dobson, CM (2003) Protein folding and misfolding. Nature 426, 884–890.CrossRefGoogle ScholarPubMed
Dong, J, Castro, CE, Boyce, MC, Lang, MJ and Lindquist, S (2010) Optical trapping with high forces reveals unexpected behaviors of prion fibrils. Nature Structural & Molecular Biology 17, 1422–1430.CrossRefGoogle ScholarPubMed
Drews, A, Flint, J, Shivji, N, Jönsson, P, Wirthensohn, D, De Genst, E, Vincke, C, Muyldermans, S, Dobson, C and Klenerman, D (2016) Individual aggregates of amyloid beta induce temporary calcium influx through the cell membrane of neuronal cells. Scientific Reports 6, 31910.CrossRefGoogle ScholarPubMed
Drews, A, De, S, Flagmeier, P, Wirthensohn, DC, Chen, WH, Whiten, DR, Rodrigues, M, Vincke, C, Muyldermans, S, Paterson, RW, Slattery, CF, Fox, NC, Schott, JM, Zetterberg, H, Dobson, CM, Gandhi, S and Klenerman, D (2017) Inhibiting the Ca(2+) influx induced by human CSF. Cell Reports 21, 3310–3316.CrossRefGoogle ScholarPubMed
Eichner, T and Radford, SE (2011) A diversity of assembly mechanisms of a generic amyloid fold. Molecular Cell 43, 8–18.CrossRefGoogle ScholarPubMed
Elson, EL (2018) Introduction to fluorescence correlation spectroscopy-brief and simple. Methods 140–141, 3–9.CrossRefGoogle ScholarPubMed
Fandos, N, Pérez-Grijalba, V, Pesini, P, Olmos, S, Bossa, M, Villemagne, VL, Doecke, J, Fowler, C, Masters, CL, Sarasa, M and Group, AR (2017) Plasma amyloid β 42/40 ratios as biomarkers for amyloid β cerebral deposition in cognitively normal individuals. Alzheimer's & Dementia 8, 179–187.CrossRefGoogle ScholarPubMed
Flagmeier, P, De, S, Wirthensohn, DC, Lee, SF, Vincke, C, Muyldermans, S, Knowles, TPJ, Gandhi, S, Dobson, CM and Klenerman, D (2017) Ultrasensitive measurement of Ca2+ influx into lipid vesicles induced by protein aggregates. Angewandte Chemie International Edition in English 56, 7750–7754.CrossRefGoogle ScholarPubMed
Fowler, DM, Koulov, AV, Balch, WE and Kelly, JW (2007) Functional amyloid – from bacteria to humans. Trends in Biochemical Sciences 32, 217–224.CrossRefGoogle ScholarPubMed
Fränzl, M, Thalheim, T, Adler, J, Huster, D, Posseckardt, J, Mertig, M and Cichos, F (2019) Thermophoretic trap for single amyloid fibril and protein aggregation studies. Nature Methods 16, 611–614.CrossRefGoogle ScholarPubMed
Fukumoto, H, Asami-Odaka, A, Suzuki, N and Iwatsubo, T (1996) Association of A beta 40-positive senile plaques with microglial cells in the brains of patients with Alzheimer's disease and in non-demented aged individuals. Neurodegeneration 5, 13–17.CrossRefGoogle ScholarPubMed
Fukumoto, H, Tennis, M, Locascio, JJ, Hyman, BT, Growdon, JH and Irizarry, MC (2003) Age but not diagnosis is the main predictor of plasma amyloid beta-protein levels. Archives of Neurology 60, 958–964.CrossRefGoogle Scholar
Funke, SA, Birkmann, E, Henke, F, Görtz, P, Lange-Asschenfeldt, C, Riesner, D and Willbold, D (2007) Single particle detection of Aβ aggregates associated with Alzheimer's disease. Biochemical and Biophysical Research Communications 364, 902–907.CrossRefGoogle ScholarPubMed
Galvagnion, C, Buell, AK, Meisl, G, Michaels, TC, Vendruscolo, M, Knowles, TP and Dobson, CM (2015) Lipid vesicles trigger α-synuclein aggregation by stimulating primary nucleation. Nature Chemical Biology 11, 229–234.CrossRefGoogle ScholarPubMed
Ganzinger, KA, Narayan, P, Qamar, SS, Weimann, L, Ranasinghe, RT, Aguzzi, A, Dobson, CM, Mccoll, J, St George-Hyslop, P and Klenerman, D (2014) Single-molecule imaging reveals that small amyloid-β1–42 oligomers interact with the cellular prion protein (PrP(C)). Chembiochem 15, 2515–2521.CrossRefGoogle Scholar
Garai, K, Sengupta, P, Sahoo, B and Maiti, S (2006) Selective destabilization of soluble amyloid β oligomers by divalent metal ions. Biochemical and Biophysical Research Communications 345, 210–215.CrossRefGoogle ScholarPubMed
Garai, K, Sureka, R and Maiti, S (2007) Detecting amyloid-β aggregation with fiber-based fluorescence correlation spectroscopy. Biophysical Journal 92, L55–L57.CrossRefGoogle ScholarPubMed
Garai, K, Sahoo, B, Sengupta, P and Maiti, S (2008) Quasihomogeneous nucleation of amyloid beta yields numerical bounds for the critical radius, the surface tension, and the free energy barrier for nucleus formation. Journal of Chemical Physics 128, 045102.CrossRefGoogle ScholarPubMed
Gitler, AD, Dhillon, P and Shorter, J (2017) Neurodegenerative disease: models, mechanisms, and a new hope. Disease Models & Mechanisms 10, 499–502.CrossRefGoogle Scholar
Goennenwein, S, Tanaka, M, Hu, B, Moroder, L and Sackmann, E (2003) Functional incorporation of integrins into solid supported membranes on ultrathin films of cellulose: impact on adhesion. Biophysical Journal 85, 646–655.CrossRefGoogle ScholarPubMed
Goldmann, WH (2000) Binding of tropomyosin–troponin to actin increases filament bending stiffness. Biochemical and Biophysical Research Communications 276, 1225–1228.CrossRefGoogle ScholarPubMed
Gorbenko, G, Trusova, V, Girych, M, Adachi, E, Mizuguchi, C, Akaji, K and Saito, H (2015) FRET evidence for untwisting of amyloid fibrils on the surface of model membranes. Soft Matter 11, 6223–6234.CrossRefGoogle ScholarPubMed
Gosse, C and Croquette, V (2002) Magnetic tweezers: micromanipulation and force measurement at the molecular level. Biophysical Journal 82, 3314–3329.CrossRefGoogle ScholarPubMed
Greenleaf, WJ, Woodside, MT. and Block, SM (2007) High-Resolution, Single-Molecule Measurements of Biomolecular Motion. Annual Review of Biophysics and Biomolecular Structure 36, 171–190.CrossRefGoogle ScholarPubMed
Guan, Y, Cao, KJ, Cantlon, A, Elbel, K, Theodorakis, EA, Walsh, DM, Yang, J and Shah, JV (2015) Real-time monitoring of Alzheimer's-related amyloid aggregation via probe enhancement-fluorescence correlation spectroscopy. ACS Chemical Neuroscience 6, 1503–1508.CrossRefGoogle ScholarPubMed
Gurnev, PA, Yap, TL, Pfefferkorn, CM, Rostovtseva, TK, Berezhkovskii, AM, Lee, JC, Parsegian, VA and Bezrukov, SM (2014) Alpha-synuclein lipid-dependent membrane binding and translocation through the α-hemolysin channel. Biophysical Journal 106, 556–565.CrossRefGoogle ScholarPubMed
Hampel, H, O'bryant, SE, Molinuevo, JL, Zetterberg, H, Masters, CL, Lista, S, Kiddle, SJ, Batrla, R and Blennow, K (2018) Blood-based biomarkers for Alzheimer disease: mapping the road to the clinic. Nature Reviews Neurology 14, 639–652.CrossRefGoogle ScholarPubMed
Hane, F, Drolle, E, Gaikwad, R, Faught, E and Leonenko, Z (2011) Amyloid-β aggregation on model lipid membranes: an atomic force microscopy study. Journal of Alzheimer's Disease 26, 485–494.CrossRefGoogle Scholar
Hane, FT, Lee, BY, Petoyan, A, Rauk, A and Leonenko, Z (2014) Testing synthetic amyloid-β aggregation inhibitor using single molecule atomic force spectroscopy. Biosensors and Bioelectronics 54, 492–498.CrossRefGoogle ScholarPubMed
Hannestad, JK, Rocha, S, Agnarsson, B, Zhdanov, VP, Wittung-Stafshede, P and Höök, F (2020) Single-vesicle imaging reveals lipid-selective and stepwise membrane disruption by monomeric α-synuclein. Proceedings of the National Academy of Sciences 117, 14178–14186.Google ScholarPubMed
Haque, F, Li, J, Wu, HC, Liang, XJ and Guo, P (2013) Solid-state and biological nanopore for real-time sensing of single chemical and sequencing of DNA. Nano Today 8, 56–74.CrossRefGoogle ScholarPubMed
Hebda, JA and Miranker, AD (2009) The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from type II diabetes. Annual Review of Biophysics 38, 125–152.CrossRefGoogle ScholarPubMed
Hellstrand, E, Grey, M, Ainalem, ML, Ankner, J, Forsyth, VT, Fragneto, G, Haertlein, M, Dauvergne, MT, Nilsson, H, Brundin, P, Linse, S, Nylander, T and Sparr, E (2013) Adsorption of α-synuclein to supported lipid bilayers: positioning and role of electrostatics. ACS Chemical Neuroscience 4, 1339–1351.CrossRefGoogle ScholarPubMed
Hipp, MS, Kasturi, P and Hartl, FU (2019) The proteostasis network and its decline in ageing. Nature Reviews Molecular Cell Biology 20, 421–435.CrossRefGoogle ScholarPubMed
Hirakura, Y and Kagan, BL (2001) Pore formation by beta-2-microglobulin: a mechanism for the pathogenesis of dialysis associated amyloidosis. Amyloid 8, 94–100.CrossRefGoogle ScholarPubMed
Hong, DP, Han, S, Fink, AL and Uversky, VN (2011) Characterization of the non-fibrillar α-synuclein oligomers. Protein & Peptide Letters 18, 230–240.CrossRefGoogle ScholarPubMed
Horrocks, MH, Tosatto, L, Dear, AJ, Garcia, GA, Iljina, M, Cremades, N, Dalla Serra, M, Knowles, TP, Dobson, CM and Klenerman, D (2015) Fast flow microfluidics and single-molecule fluorescence for the rapid characterization of α-synuclein oligomers. Analytical Chemistry 87, 8818–8826.CrossRefGoogle ScholarPubMed
Horrocks, MH, Lee, SF, Gandhi, S, Magdalinou, NK, Chen, SW, Devine, MJ, Tosatto, L, Kjaergaard, M, Beckwith, JS, Zetterberg, H, Iljina, M, Cremades, N, Dobson, CM, Wood, NW and Klenerman, D (2016) Single-molecule imaging of individual amyloid protein aggregates in human biofluids. ACS Chemical Neuroscience 7, 399–406.CrossRefGoogle ScholarPubMed
Houghtaling, J, List, J and Mayer, M (2018) Nanopore-based, rapid characterization of individual amyloid particles in solution: concepts, challenges, and prospects. Small 14, e1802412.CrossRefGoogle ScholarPubMed
Hu, R, Diao, JJ, Li, J, Tang, ZP, Li, XQ, Leitz, J, Long, JG, Liu, JK, Yu, DP and Zhao, Q (2016) Intrinsic and membrane-facilitated α-synuclein oligomerization revealed by label-free detection through solid-state nanopores. Scientific Reports 11, 20776.CrossRefGoogle Scholar
Hu, YX, Ying, YL, Gu, Z, Cao, C, Yan, BY, Wang, HF and Long, YT (2016) Single molecule study of initial structural features on the amyloidosis process. Chemical Communications 52, 5542–5545.CrossRefGoogle ScholarPubMed
Hugel, T, Grosholz, M, Clausen-Schaumann, H, Pfau, A, Gaub, H and Seitz, M (2001) Elasticity of single polyelectrolyte chains and their desorption from solid supports studied by AFM based single molecule force spectroscopy. Macromolecules 34, 1039–1047.CrossRefGoogle Scholar
Ide, T and Yanagida, T (1999) An artificial lipid bilayer formed on an agarose-coated glass for simultaneous electrical and optical measurement of single ion channels. Biochemical and Biophysical Research Communications 265, 595–599.CrossRefGoogle Scholar
Iljina, M, Garcia, GA, Dear, AJ, Flint, J, Narayan, P, Michaels, TC, Dobson, CM, Frenkel, D, Knowles, TP and Klenerman, D (2016a) Quantitative analysis of co-oligomer formation by amyloid-beta peptide isoforms. Scientific Reports 6, 28658.CrossRefGoogle Scholar
Iljina, M, Garcia, GA, Horrocks, MH, Tosatto, L, Choi, ML, Ganzinger, KA, Abramov, AY, Gandhi, S, Wood, NW, Cremades, N, Dobson, CM, Knowles, TP and Klenerman, D (2016b) Kinetic model of the aggregation of alpha-synuclein provides insights into prion-like spreading. Proceedings of the National Academy of Sciences 113, E1206–1215.CrossRefGoogle Scholar
Iljina, M, Dear, AJ, Garcia, GA, De, S, Tosatto, L, Flagmeier, P, Whiten, DR, Michaels, TCT, Frenkel, D, Dobson, CM, Knowles, TPJ and Klenerman, D (2018) Quantifying co-oligomer formation by α-synuclein. ACS Nano 12, 10855–10866.CrossRefGoogle ScholarPubMed
Jagannathan, B and Marqusee, S (2013) Protein folding and unfolding under force. Biopolymers 99, 860–869.CrossRefGoogle ScholarPubMed
Jahn, TR and Radford, SE (2008) Folding versus aggregation: polypeptide conformations on competing pathways. Archives of Biochemistry and Biophysics 469, 100–117.CrossRefGoogle ScholarPubMed
Jaiswal, JK, Mattoussi, H, Mauro, JM and Simon, SM (2003) Long-term multiple color imaging of live cells using quantum dot bioconjugates. Nature Biotechnology 21, 47–51.CrossRefGoogle ScholarPubMed
Janelidze, S, Stomrud, E, Palmqvist, S, Zetterberg, H, Van Westen, D, Jeromin, A, Song, L, Hanlon, D, Tan Hehir, CA, Baker, D, Blennow, K and Hansson, O (2016) Plasma β-amyloid in Alzheimer's disease and vascular disease. Scientific Reports 6, 26801.CrossRefGoogle ScholarPubMed
Jarosz-Griffiths, HH, Noble, E, Rushworth, JV and Hooper, NM (2016) Amyloid-β receptors: the good, the bad, and the prion protein. Journal of biological chemistry 291, 3174–3183.CrossRefGoogle ScholarPubMed
Jaul, E and Barron, J (2017) Age-related diseases and clinical and public health implications for the 85 years old and over population. Frontiers in Public Health 5, 335–335.CrossRefGoogle ScholarPubMed
Ji, M, Arbel, M, Zhang, L, Freudiger, CW, Hou, SS, Lin, D, Yang, X, Bacskai, BJ and Xie, XS (2018) Label-free imaging of amyloid plaques in Alzheimer's disease with stimulated Raman scattering microscopy. Science Advances 4, eaat7715.CrossRefGoogle ScholarPubMed
Johnson, RD, Steel, DG and Gafni, A (2014) Structural evolution and membrane interactions of Alzheimer's amyloid-beta peptide oligomers: new knowledge from single-molecule fluorescence studies. Protein Science 23, 869–883.CrossRefGoogle ScholarPubMed
Kaminski Schierle, GS, Bertoncini, CW, Chan, FTS, Van Der Goot, AT, Schwedler, S, Skepper, J, Schlachter, S, Van Ham, T, Esposito, A, Kumita, JR, Nollen, EAA, Dobson, CM and Kaminski, CF (2011) A FRET sensor for non-invasive imaging of amyloid formation in vivo. ChemPhysChem 12, 673–680.CrossRefGoogle ScholarPubMed
Keppler, A, Gendreizig, S, Gronemeyer, T, Pick, H, Vogel, H and Johnsson, K (2003) A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nature Biotechnology 21, 86–89.CrossRefGoogle ScholarPubMed
Kim, BH and Lyubchenko, YL (2014) Nanoprobing of misfolding and interactions of amyloid β 42 protein. Nanomedicine: Nanotechnology, Biology, and Medicine 10, 871–878.CrossRefGoogle ScholarPubMed
Kim, BH, Palermo, NY, Lovas, S, Zaikova, T, Keana, JF and Lyubchenko, YL (2011) Single-molecule atomic force microscopy force spectroscopy study of Aβ-40 interactions. Biochemistry 50, 5154–5162.CrossRefGoogle ScholarPubMed
Kitamura, A and Kinjo, M (2018) State-of-the-art fluorescence fluctuation-based spectroscopic techniques for the study of protein aggregation. International Journal of Molecular Sciences 19, 964.CrossRefGoogle Scholar
Klein, WL, Krafft, GA and Finch, CE (2001) Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends in Neurosciences 24, 219–224.CrossRefGoogle Scholar
Knight, JD, Hebda, JA and Miranker, AD (2006) Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide. Biochemistry 45, 9496–9508.CrossRefGoogle ScholarPubMed
Korshavn, KJ, Satriano, C, Lin, Y, Zhang, R, Dulchavsky, M, Bhunia, A, Ivanova, MI, Lee, YH, La Rosa, C, Lim, MH and Ramamoorthy, A (2017) Reduced lipid bilayer thickness regulates the aggregation and cytotoxicity of amyloid-β. Journal of Biological Chemistry 292, 4638–4650.CrossRefGoogle ScholarPubMed
Kransnoslobodtsev, AV, Shlyakhtenko, LS, Ukraintsev, E, Zaikova, TO, Keana, JF and Lyubchenko, YL (2005) Nanomedicine and protein misfolding diseases. Nanomedicine: Nanotechnology, Biology, and Medicine 1, 300–305.CrossRefGoogle ScholarPubMed
Krasnoslobodtsev, AV, Volkov, IL, Asiago, JM, Hindupur, J, Rochet, JC and Lyubchenko, YL (2013) α-Synuclein misfolding assessed with single molecule AFM force spectroscopy: effect of pathogenic mutations. Biochemistry 52, 7377–7386.CrossRefGoogle ScholarPubMed
Krasnoslobodtsev, AV, Zhang, Y, Viazovkina, E, Gall, A, Bertagni, C and Lyubchenko, YL (2015) A flexible nanoarray approach for the assembly and probing of molecular complexes. Biophysical Journal 108, 2333–2339.CrossRefGoogle ScholarPubMed
Kumar, A, Singh, A and Ekavali, E (2015) A review on Alzheimer's disease pathophysiology and its management: an update. Pharmacological Reports 67, 195–203.CrossRefGoogle ScholarPubMed
Lashuel, HA and Lansbury, PT Jr (2006). Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Quarterly Reviews of Biophysics, 39, 167–201.CrossRefGoogle ScholarPubMed
Lashuel, HA, Hartley, D, Petre, BM, Walz, T and Lansbury, PT Jr (2002) Amyloid pores from pathogenic mutations. Nature 418, 291–291.CrossRefGoogle ScholarPubMed
Last, NB and Miranker, AD (2013) Common mechanism unites membrane poration by amyloid and antimicrobial peptides. Proceedings of the National Academy of Sciences 110, 6382–6387.CrossRefGoogle ScholarPubMed
Lee, J, Kim, Y, Arce, F, Gillman, AL, Jang, H, Kagan, BL, Nussinov, R, Yang, J and Lal, R (2017) Amyloid beta ion channels in a membrane comprising brain total lipid extracts. ACS Chemical Neuroscience 8, 1348–1357.CrossRefGoogle Scholar
Lee, HJ, Lee, YG, Kang, J, Yang, SH, Kim, JH, Ghisaidoobe, ABT, Kang, HJ, Lee, SR, Lim, MH and Chung, SJ (2019) Monitoring metal-amyloid-β complexation by a FRET-based probe: design, detection, and inhibitor screening. Chemical Science 10, 1000–1007.CrossRefGoogle ScholarPubMed
Li, H, Zhang, W, Zhang, X, Shen, J, Liu, B, Gao, C and Zou, G (1998) Single molecule force spectroscopy on poly(vinyl alcohol) by atomic force microscopy. Macromolecular Rapid Communications 19, 609–611.3.0.CO;2-2>CrossRefGoogle Scholar
Li, S, Micic, M, Orbulescu, J, Whyte, JD and Leblanc, RM (2012) Human islet amyloid polypeptide at the air-aqueous interface: a Langmuir monolayer approach. Journal of the Royal Society Interface 9, 3118–3128.CrossRefGoogle ScholarPubMed
Li, X, Wan, M, Gao, L and Fang, W (2016) Mechanism of inhibition of human islet amyloid polypeptide-induced membrane damage by a small organic fluorogen. Scientific Reports 6, 21614.CrossRefGoogle ScholarPubMed
Liang, Y, Lynn, DG and Berland, KM (2010) Direct observation of nucleation and growth in amyloid self-assembly. Journal of the American Chemical Society 132, 6306–6308.CrossRefGoogle ScholarPubMed
Lin, MC, Mirzabekov, T and Kagan, BL (1997) Channel formation by a neurotoxic prion protein fragment. Journal of Biological Chemistry 272, 44–47.CrossRefGoogle ScholarPubMed
Lindberg, DJ, Wesén, E, Björkeroth, J, Rocha, S and Esbjörner, EK (2017) Lipid membranes catalyse the fibril formation of the amyloid-β (1–42) peptide through lipid-fibril interactions that reinforce secondary pathways. Biochimica et Biophysica Acta (BBA) – Biomembranes 1859, 1921–1929.CrossRefGoogle ScholarPubMed
Lord, SJ, Lee, HL and Moerner, WE (2010) Single-molecule spectroscopy and imaging of biomolecules in living cells. Analytical Chemistry 82, 2192–2203.CrossRefGoogle ScholarPubMed
Lue, LF, Kuo, YM, Roher, AE, Brachova, L, Shen, Y, Sue, L, Beach, T, Kurth, JH, Rydel, RE and Rogers, J (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. American Journal of Pathology 155, 853–862.CrossRefGoogle ScholarPubMed
Maass, F, Rikker, S, Dambeck, V, Warth, C, Tatenhorst, L, Csoti, I, Schmitz, M, Zerr, I, Leha, A, Bähr, M and Lingor, P (2020) Increased alpha-synuclein tear fluid levels in patients with Parkinson's disease. Scientific Reports 10, 8507.CrossRefGoogle ScholarPubMed
Madampage, C, Tavassoly, O, Christensen, C, Kumari, M and Lee, JS (2012) Nanopore analysis: an emerging technique for studying the folding and misfolding of proteins. Prion 6, 116–123.CrossRefGoogle ScholarPubMed
Maity, S and Lyubchenko, YL (2016) Probing of amyloid Aβ (14–23) trimers by single-molecule force spectroscopy. Jacobs Journal of Molecular and Translational Medicine 1, 004.Google ScholarPubMed
Maity, S and Lyubchenko, YL (2020) AFM probing of amyloid-beta 42 dimers and trimers. Frontiers in Molecular Biosciences 7, 69.CrossRefGoogle ScholarPubMed
Maity, S, Viazovkina, E, Gall, A and Lyubchenko, Y (2016) A metal-free click chemistry approach for the assembly and probing of biomolecules. Journal of Nature and Science 2, e187.Google ScholarPubMed
Maity, S, Viazovkina, E, Gall, A and Lyubchenko, YL (2017) Single-molecule probing of amyloid nano-ensembles using the polymer nanoarray approach. Physical Chemistry Chemical Physics 19, 16387–16394.CrossRefGoogle ScholarPubMed
Maity, S, Pramanik, A and Lyubchenko, YL (2018) Probing intermolecular interactions within the amyloid β trimer using a tethered polymer nanoarray. Bioconjugate Chemistry 29, 2755–2762.CrossRefGoogle ScholarPubMed
Marguet, D, Lenne, PF, Rigneault, H and He, HT (2006) Dynamics in the plasma membrane: how to combine fluidity and order. EMBO Journal 25, 3446–3457.CrossRefGoogle Scholar
Martyushenko, N, Bell, NA, Lamboll, RD and Keyser, UF (2015) Nanopore analysis of amyloid fibrils formed by lysozyme aggregation. Analyst 140, 4882–4886.CrossRefGoogle ScholarPubMed
Mastrangelo, IA, Ahmed, M, Sato, T, Liu, W, Wang, C, Hough, P and Smith, SO (2006) High-resolution atomic force microscopy of soluble Abeta42 oligomers. Journal of Molecular Biology 358, 106–119.CrossRefGoogle ScholarPubMed
Matsuzaki, K (2007) Physicochemical interactions of amyloid beta-peptide with lipid bilayers. Biochimica et Biophysica Acta 1768, 1935–1942.CrossRefGoogle ScholarPubMed
Mattsson, N, Andreasson, U, Persson, S, Carrillo, MC, Collins, S, Chalbot, S, Cutler, N, Dufour-Rainfray, D, Fagan, AM, Heegaard, NH, Robin Hsiung, GY, Hyman, B, Iqbal, K, Kaeser, SA, Lachno, DR, Lleó, A, Lewczuk, P, Molinuevo, JL, Parchi, P, Regeniter, A, Rissman, RA, Rosenmann, H, Sancesario, G, Schröder, J, Shaw, LM, Teunissen, CE, Trojanowski, JQ, Vanderstichele, H, Vandijck, M, Verbeek, MM, Zetterberg, H and Blennow, K (2013) CSF biomarker variability in the Alzheimer's association quality control program. Alzheimer's & Dementia 9, 251–261.CrossRefGoogle ScholarPubMed
Mcallister, C, Karymov, MA, Kawano, Y, Lushnikov, AY, Mikheikin, A, Uversky, VN and Lyubchenko, YL (2005) Protein interactions and misfolding analyzed by AFM force spectroscopy. Journal of Molecular Biology 354, 1028–1042.CrossRefGoogle ScholarPubMed
Mclean, CA, Cherny, RA, Fraser, FW, Fuller, SJ, Smith, MJ, Beyreuther, K, Bush, AI and Masters, CL (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Annals of Neurology 46, 860–866.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Medina, MA and Schwille, P (2002) Fluorescence correlation spectroscopy for the detection and study of single molecules in biology. Bioessays 24, 758–764.CrossRefGoogle ScholarPubMed
Meker, S, Chin, H, Sut, TN and Cho, NJ (2018) Amyloid-β peptide triggers membrane remodeling in supported lipid bilayers depending on their hydrophobic thickness. Langmuir 34, 9548–9560.CrossRefGoogle ScholarPubMed
Middleton, ER and Rhoades, E (2010) Effects of curvature and composition on α-synuclein binding to lipid vesicles. Biophysical Journal 99, 2279–2288.CrossRefGoogle ScholarPubMed
Miraglia, F, Ricci, A, Rota, L and Colla, E (2018) Subcellular localization of alpha-synuclein aggregates and their interaction with membranes. Neural Regeneration Research 13, 1136–1144.Google ScholarPubMed
Mirzabekov, TA, Lin, MC and Kagan, BL (1996) Pore formation by the cytotoxic islet amyloid peptide amylin. Journal of Biological Chemistry 271, 1988–1992.CrossRefGoogle ScholarPubMed
Mittag, JJ, Milani, S, Walsh, DM, Rädler, JO and Mcmanus, JJ (2014) Simultaneous measurement of a range of particle sizes during Aβ1–42 fibrillogenesis quantified using fluorescence correlation spectroscopy. Biochemical and Biophysical Research Communications 448, 195–199.CrossRefGoogle ScholarPubMed
Molinuevo, JL, Blennow, K, Dubois, B, Engelborghs, S, Lewczuk, P, Perret-Liaudet, A, Teunissen, CE and Parnetti, L (2014) The clinical use of cerebrospinal fluid biomarker testing for Alzheimer's disease diagnosis: a consensus paper from the Alzheimer's biomarkers standardization initiative. Alzheimer's & Dementia 10, 808–817.CrossRefGoogle ScholarPubMed
Mollenhauer, B, Cullen, V, Kahn, I, Krastins, B, Outeiro, TF, Pepivani, I, Ng, J, Schulz-Schaeffer, W, Kretzschmar, HA, McLean, PJ, Trenkwalder, C, Sarracino, DA, VonSattel, J-P, Locascio, JJ, El-Agnaf, OM.A and Schlossmacher, MG. (2008) Direct quantification of CSF α-synuclein by ELISA and first cross-sectional study in patients with neurodegeneration. Experimental Neurology 213, 315–325.CrossRefGoogle ScholarPubMed
Mukhopadhyay, S, Krishnan, R, Lemke, EA, Lindquist, S and Deniz, AA (2007) A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures. Proceedings of the National Academy of Sciences 104, 2649–2654.CrossRefGoogle ScholarPubMed
Nag, S, Chen, J, Irudayaraj, J and Maiti, S (2010) Measurement of the attachment and assembly of small amyloid-β oligomers on live cell membranes at physiological concentrations using single-molecule tools. Biophysical Journal 99, 1969–1975.CrossRefGoogle ScholarPubMed
Narayan, P, Orte, A, Clarke, RW, Bolognesi, B, Hook, S, Ganzinger, KA, Meehan, S, Wilson, MR, Dobson, CM and Klenerman, D (2011) The extracellular chaperone clusterin sequesters oligomeric forms of the amyloid-β(1–40) peptide. Nature Structural & Molecular Biology 19, 79–83.CrossRefGoogle ScholarPubMed
Narayan, P, Meehan, S, Carver, JA, Wilson, MR, Dobson, CM and Klenerman, D (2012) Amyloid-β oligomers are sequestered by both intracellular and extracellular chaperones. Biochemistry 51, 9270–9276.CrossRefGoogle ScholarPubMed
Neuman, KC and Nagy, A (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nature Methods 5, 491–505.CrossRefGoogle ScholarPubMed
Neupane, K, Solanki, A, Sosova, I, Belov, M and Woodside, MT (2014) Diverse metastable structures formed by small oligomers of α-synuclein probed by force spectroscopy. PLoS ONE 9, e86495.CrossRefGoogle ScholarPubMed
Nirmalraj, PN, List, J, Battacharya, S, Howe, G, Xu, L, Thompson, D and Mayer, M (2020) Complete aggregation pathway of amyloid β (1–40) and (1–42) resolved on an atomically clean interface. Science Advances 6, eaaz6014.CrossRefGoogle Scholar
Noguchi-Shinohara, M, Tokuda, T, Yoshita, M, Kasai, T, Ono, K, Nakagawa, M, El-Agnaf, OMA and Yamada, M (2009) CSF alpha-synuclein levels in dementia with Lewy bodies and Alzheimer's disease. Brain Research 1251, 1–6.CrossRefGoogle ScholarPubMed
Novo, M, Freire, S and Al-Soufi, W (2018) Critical aggregation concentration for the formation of early amyloid-β (1–42) oligomers. Scientific Reports 8, 1783–1783.CrossRefGoogle ScholarPubMed
Olsson, B, Lautner, R, Andreasson, U, Öhrfelt, A, Portelius, E, Bjerke, M, Hölttä, M, Rosén, C, Olsson, C, Strobel, G, Wu, E, Dakin, K, Petzold, M, Blennow, K and Zetterberg, H (2016) CSF and blood biomarkers for the diagnosis of Alzheimer's disease: a systematic review and meta-analysis. The Lancet Neurology 15, 673–684.CrossRefGoogle Scholar
Orte, A, Birkett, NR, Clarke, RW, Devlin, GL, Dobson, CM and Klenerman, D (2008) Direct characterization of amyloidogenic oligomers by single-molecule fluorescence. Proceedings of the National Academy of Sciences 105, 14424–14429.CrossRefGoogle ScholarPubMed
Orte, A, Clarke, R and Klenerman, D (2010) Single-molecule two-colour coincidence detection to probe biomolecular associations. Biochemical Society Transactions 38, 914–918.CrossRefGoogle ScholarPubMed
Pasternak, SH, Callahan, JW and Mahuran, DJ (2004) The role of the endosomal/lysosomal system in amyloid-beta production and the pathophysiology of Alzheimer's disease: reexamining the spatial paradox from a lysosomal perspective. Journal of Alzheimer's Disease 6, 53–65.CrossRefGoogle ScholarPubMed
Patil, SM, Mehta, A, Jha, S and Alexandrescu, AT (2011) Heterogeneous amylin fibril growth mechanisms imaged by total internal reflection fluorescence microscopy. Biochemistry 50, 2808–2819.CrossRefGoogle ScholarPubMed
Pham, CL, Kwan, AH and Sunde, M (2014) Functional amyloid: widespread in nature, diverse in purpose. Essays in Biochemistry 56, 207–219.Google ScholarPubMed
Pitschke, M, Prior, R, Haupt, M and Riesner, D (1998) Detection of single amyloid β-protein aggregates in the cerebrospinal fluid of Alzheimer's patients by fluorescence correlation spectroscopy. Nature Medicine 4, 832–834.CrossRefGoogle ScholarPubMed
Quist, A, Doudevski, I, Lin, H, Azimova, R, Ng, D, Frangione, B, Kagan, B, Ghiso, J and Lal, R (2005) Amyloid ion channels: a common structural link for protein-misfolding disease. Proceedings of the National Academy of Sciences 102, 10427–10432.CrossRefGoogle ScholarPubMed
Reits, EA and Neefjes, JJ (2001) From fixed to FRAP: measuring protein mobility and activity in living cells. Nature Cell Biology 3, E145–147.CrossRefGoogle ScholarPubMed
Reynolds, NP, Soragni, A, Rabe, M, Verdes, D, Liverani, E, Handschin, S, Riek, R and Seeger, S (2011) Mechanism of membrane interaction and disruption by α-synuclein. Journal of the American Chemical Society 133, 19366–19375.CrossRefGoogle ScholarPubMed
Rhoades, E, Ramlall, TF, Webb, WW and Eliezer, D (2006) Quantification of alpha-synuclein binding to lipid vesicles using fluorescence correlation spectroscopy. Biophysical Journal 90, 4692–4700.CrossRefGoogle ScholarPubMed
Rief, M, Oesterhelt, F, Heymann, B and Gaub, HE (1997) Single molecule force spectroscopy on polysaccharides by atomic force microscopy. Science 275, 1295–1297.CrossRefGoogle ScholarPubMed
Rigler, R (2010) Fluorescence and single molecule analysis in cell biology. Biochemical and Biophysical Research Communications 396, 170–175.CrossRefGoogle ScholarPubMed
Roberti, MJ, Jovin, TM and Jares-Erijman, E (2011) Confocal fluorescence anisotropy and FRAP imaging of α-synuclein amyloid aggregates in living cells. PLoS ONE 6, e23338.CrossRefGoogle ScholarPubMed
Rostovtseva, TK, Gurnev, PA, Protchenko, O, Hoogerheide, DP, Yap, TL, Philpott, CC, Lee, JC and Bezrukov, SM (2015) α-Synuclein shows high affinity interaction with voltage-dependent anion channel, suggesting mechanisms of mitochondrial regulation and toxicity in Parkinson disease. Journal of Biological Chemistry 290, 18467–18477.CrossRefGoogle ScholarPubMed
Roy, R, Hohng, S and Ha, T (2008) A practical guide to single-molecule FRET. Nature Methods 5, 507–516.CrossRefGoogle ScholarPubMed
Ruggeri, FS, Adamcik, J, Jeong, JS, Lashuel, HA, Mezzenga, R and Dietler, G (2015) Influence of the β-sheet content on the mechanical properties of aggregates during amyloid fibrillization. Angewandte Chemie International Edition in English 54, 2462–2466.CrossRefGoogle ScholarPubMed
Ruggeri, FS, Benedetti, F, Knowles, TPJ, Lashuel, HA, Sekatskii, S and Dietler, G (2018) Identification and nanomechanical characterization of the fundamental single-strand protofilaments of amyloid α-synuclein fibrils. Proceedings of the National Academy of Sciences 115, 7230.CrossRefGoogle ScholarPubMed
Santos, AN, Torkler, S, Nowak, D, Schlittig, C, Goerdes, M, Lauber, T, Trischmann, L, Schaupp, M, Penz, M, Tiller, F-W and Böhm, G (2007) Detection of amyloid-β oligomers in human cerebrospinal fluid by flow cytometry and fluorescence resonance energy transfer. Journal of Alzheimer's Disease 11, 117–125.CrossRefGoogle ScholarPubMed
Sarkar, R and Rybenkov, VV (2016) A guide to magnetic tweezers and their applications. Frontiers in Physics 4, 48.CrossRefGoogle Scholar
Sarkar, B, Das, A and Maiti, S (2013) Thermodynamically stable amyloid-β monomers have much lower membrane affinity than the small oligomers. Frontiers in Physiology 4, 84.CrossRefGoogle Scholar
Sasahara, K, Morigaki, K, Okazaki, T and Hamada, D (2012) Binding of islet amyloid polypeptide to supported lipid bilayers and amyloid aggregation at the membranes. Biochemistry 51, 6908–6919.CrossRefGoogle ScholarPubMed
Sasahara, K, Morigaki, K and Shinya, K (2013) Effects of membrane interaction and aggregation of amyloid β-peptide on lipid mobility and membrane domain structure. Physical Chemistry Chemical Physics 15, 8929–8939.CrossRefGoogle ScholarPubMed
Sasahara, K, Morigaki, K and Shinya, K (2014) Amyloid aggregation and deposition of human islet amyloid polypeptide at membrane interfaces. The FEBS Journal 281, 2597–2612.CrossRefGoogle ScholarPubMed
Savage, MJ, Kalinina, J, Wolfe, A, Tugusheva, K, Korn, R, Cash-Mason, T, Maxwell, JW, Hatcher, NG, Haugabook, SJ, Wu, G, Howell, BJ, Renger, JJ, Shughrue, PJ and Mccampbell, A (2014) A sensitive Aβ oligomer assay discriminates Alzheimer's and aged control cerebrospinal fluid. The Journal of Neuroscience 34, 2884–2897.CrossRefGoogle ScholarPubMed
Schauerte, JA, Wong, PT, Wisser, KC, Ding, H, Steel, DG and Gafni, A (2010) Simultaneous single-molecule fluorescence and conductivity studies reveal distinct classes of Abeta species on lipid bilayers. Biochemistry 49, 3031–3039.CrossRefGoogle ScholarPubMed
Schneckenburger, H (2005) Total internal reflection fluorescence microscopy: technical innovations and novel applications. Current Opinion in Biotechnology 16, 13–18.CrossRefGoogle ScholarPubMed
Schreiber, A, Fischer, S and Lang, T (2012) The amyloid precursor protein forms plasmalemmal clusters via its pathogenic amyloid-β Domain. Biophysical Journal 102, 1411–1417.CrossRefGoogle ScholarPubMed
Schuler, B and Eaton, WA (2008) Protein folding studied by single-molecule FRET. Current Opinion in Structural Biology 18, 16–26.CrossRefGoogle ScholarPubMed
Schweikhard, V, Baral, A, Krishnamachari, V, Hay, WC and Fuhrmann, M (2019) Label-free characterization of amyloid-β-plaques and associated lipids in brain tissues using stimulated Raman scattering microscopy. bioRxiv, 789248.Google Scholar
Schwille, P, Meyer-Almes, FJ and Rigler, R (1997) Dual-color fluorescence cross-correlation spectroscopy for multicomponent diffusional analysis in solution. Biophysical Journal 72, 1878–1886.CrossRefGoogle ScholarPubMed
Seisenberger, G, Ried, MU, Endreß, T, Büning, H, Hallek, M and Bräuchle, C (2001) Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science 294, 1929–1932.CrossRefGoogle ScholarPubMed
Selkoe, DJ (2003) Folding proteins in fatal ways. Nature 426, 900–904.CrossRefGoogle ScholarPubMed
Sergeeva, AV, Sopova, JV, Belashova, TA, Siniukova, VA, Chirinskaite, AV, Galkin, AP and Zadorsky, SP (2019) Amyloid properties of the yeast cell wall protein Toh1 and its interaction with prion proteins Rnq1 and Sup35. Prion 13, 21–32.CrossRefGoogle ScholarPubMed
Shammas, SL, Garcia, GA, Kumar, S, Kjaergaard, M, Horrocks, MH, Shivji, N, Mandelkow, E, Knowles, TP, Mandelkow, E and Klenerman, D (2015) A mechanistic model of tau amyloid aggregation based on direct observation of oligomers. Nature Communications 6, 7025.CrossRefGoogle Scholar
Shashkova, S and Leake, MC (2017) Single-molecule fluorescence microscopy review: shedding new light on old problems. Bioscience Reports 37, 4.CrossRefGoogle ScholarPubMed
Shi, M, Zabetian, CP, Hancock, AM, Ginghina, C, Hong, Z, Yearout, D, Chung, KA, Quinn, JF, Peskind, ER, Galasko, D, Jankovic, J, Leverenz, JB and Zhang, J (2010) Significance and confounders of peripheral DJ-1 and alpha-synuclein in Parkinson's disease. Neuroscience Letters 480, 78–82.CrossRefGoogle ScholarPubMed
Simpson, LW, Szeto, GL, Boukari, H, Good, TA and Leach, JB (2020) Collagen hydrogel confinement of amyloid-β (Aβ) accelerates aggregation and reduces cytotoxic effects. Acta Biomaterialia 112, 164–173.CrossRefGoogle ScholarPubMed
Spies, PE, Melis, RJ, Sjögren, MJ, Rikkert, MG and Verbeek, MM (2009) Cerebrospinal fluid alpha-synuclein does not discriminate between dementia disorders. Journal of Alzheimer's Disease 16, 363–369.CrossRefGoogle Scholar
Strick, TR, Allemand, JF, Bensimon, D, Bensimon, A and Croquette, V (1996) The elasticity of a single supercoiled DNA molecule. Science 271, 1835–1837.CrossRefGoogle ScholarPubMed
Sweers, KKM, Van Der Werf, KO, Bennink, ML and Subramaniam, V (2012) Atomic force microscopy under controlled conditions reveals structure of C-terminal region of α-synuclein in amyloid fibrils. ACS Nano 6, 5952–5960.CrossRefGoogle ScholarPubMed
Tagliavini, F, Giaccone, G, Frangione, B and Bugiani, O (1988) Preamyloid deposits in the cerebral cortex of patients with Alzheimer's disease and nondemented individuals. Neuroscience Letters 93, 191–196.CrossRefGoogle ScholarPubMed
Talaga, DS and Li, J (2009) Single-molecule protein unfolding in solid state nanopores. Journal of the American Chemical Society 131, 9287–9297.CrossRefGoogle ScholarPubMed
Tanaka, M and Sackmann, E (2005) Polymer-supported membranes as models of the cell surface. Nature 437, 656–663.CrossRefGoogle ScholarPubMed
Tanaka, H, Sakaguchi, D and Hirano, T (2019) Amyloid-β oligomers suppress subunit-specific glutamate receptor increase during LTP. Alzheimer's & Dementia 5, 797–808.CrossRefGoogle ScholarPubMed
Terzi, E, Hölzemann, G and Seelig, J (1995) Self-association of β-amyloid peptide (1–40) in solution and binding to lipid membranes. Journal of Molecular Biology 252, 633–642.CrossRefGoogle ScholarPubMed
Tiiman, A, Jarvet, J, Gräslund, A and Vukojević, V (2015) Heterogeneity and turnover of intermediates during amyloid-β (Aβ) peptide aggregation studied by fluorescence correlation spectroscopy. Biochemistry 54, 7203–7211.CrossRefGoogle ScholarPubMed
Tiiman, A, Jelić, V, Jarvet, J, Järemo, P, Bogdanović, N, Rigler, R, Terenius, L, Gräslund, A and Vukojević, V (2019) Amyloidogenic nanoplaques in blood serum of patients with Alzheimer's disease revealed by time-resolved Thioflavin T fluorescence intensity fluctuation analysis. Journal of Alzheimer's Disease 68, 571–582.CrossRefGoogle ScholarPubMed
Tipping, KW, Van Oosten-Hawle, P, Hewitt, EW and Radford, SE (2015) Amyloid fibres: inert end-stage aggregates or key players in disease? Trends in Biochemical Sciences 40, 719–727.CrossRefGoogle ScholarPubMed
Tjernberg, LO, Pramanik, A, Björling, S, Thyberg, P, Thyberg, J, Nordstedt, C, Berndt, KD, Terenius, L and Rigler, R (1999) Amyloid beta-peptide polymerization studied using fluorescence correlation spectroscopy. Chemistry & Biology 6, 53–62.CrossRefGoogle ScholarPubMed
Tong, Z, Mikheikin, A, Krasnoslobodtsev, A, Lv, Z and Lyubchenko, YL (2013) Novel polymer linkers for single molecule AFM force spectroscopy. Methods 60, 161–168.CrossRefGoogle ScholarPubMed
Tosatto, L, Horrocks, MH, Dear, AJ, Knowles, TP, Dalla Serra, M, Cremades, N, Dobson, CM and Klenerman, D (2015) Single-molecule FRET studies on alpha-synuclein oligomerization of Parkinson's disease genetically related mutants. Scientific Reports 5, 16696.CrossRefGoogle ScholarPubMed
Trexler, AJ and Rhoades, E (2010) Single molecule characterization of α-synuclein in aggregation-prone states. Biophysical Journal 99, 3048–3055.CrossRefGoogle ScholarPubMed
Trojanowski, JQ, Vandeerstichele, H, Korecka, M, Clark, CM, Aisen, PS, Petersen, RC, Blennow, K, Soares, H, Simon, A, Lewczuk, P, Dean, R, Siemers, E, Potter, WZ, Weiner, MW, Jack, CR, Jagust, JR, Toga, W, Lee, AW, & Shaw, VM and M L (2010) Update on the biomarker core of the Alzheimer's disease neuroimaging initiative subjects. Alzheimer's & Dementia 6, 230–238.CrossRefGoogle ScholarPubMed
Vereb, G, Szöllosi, J, Matkó, J, Nagy, P, Farkas, T, Vigh, L, Mátyus, L, Waldmann, TA and Damjanovich, S (2003) Dynamic, yet structured: the cell membrane three decades after the Singer–Nicolson model. Proceedings of the National Academy of Sciences 100, 8053–8058.CrossRefGoogle ScholarPubMed
Verwey, NA, Van Der Flier, WM, Blennow, K, Clark, C, Sokolow, S, De Deyn, PP, Galasko, D, Hampel, H, Hartmann, T, Kapaki, E, Lannfelt, L, Mehta, PD, Parnetti, L, Petzold, A, Pirttila, T, Saleh, L, Skinningsrud, A, Swieten, JC, Verbeek, MM, Wiltfang, J, Younkin, S, Scheltens, P and Blankenstein, MA (2009) A worldwide multicentre comparison of assays for cerebrospinal fluid biomarkers in Alzheimer's disease. Annals of Clinical Biochemistry 46, 235–240.CrossRefGoogle ScholarPubMed
Wagner, ML and Tamm, LK (2001) Reconstituted syntaxin1a/SNAP25 interacts with negatively charged lipids as measured by lateral diffusion in planar supported bilayers. Biophysical Journal 81, 266–275.CrossRefGoogle ScholarPubMed
Walsh, DM and Selkoe, DJ (2007) A beta oligomers – a decade of discovery. Journal of Neurochemistry 101, 1172–1184.CrossRefGoogle Scholar
Wang, HY, Ying, YL, Li, Y, Kraatz, HB and Long, YT (2011) Nanopore analysis of β-amyloid peptide aggregation transition induced by small molecules. Analytical Chemistry 83, 1746–1752.CrossRefGoogle ScholarPubMed
Wennmalm, S, Chmyrov, V, Widengren, J and Tjernberg, L (2015) Highly sensitive FRET–FCS detects amyloid β-peptide oligomers in solution at physiological concentrations. Analytical Chemistry 87, 11700–11705.CrossRefGoogle ScholarPubMed
Whiten, DR, Cox, D, Horrocks, MH, Taylor, CG, De, S, Flagmeier, P, Tosatto, L, Kumita, JR, Ecroyd, H, Dobson, CM, Klenerman, D and Wilson, MR (2018) Single-molecule characterization of the interactions between extracellular chaperones and toxic α-synuclein oligomers. Cell Reports 23, 3492–3500.CrossRefGoogle ScholarPubMed
Whitmore, L and Wallace, BA (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89, 392–400.CrossRefGoogle ScholarPubMed
Widenbrant, MJO, Rajadas, J, Sutardja, C and Fuller, GG (2006) Lipid-induced β-amyloid peptide assemblage fragmentation. Biophysical Journal 91, 4071–4080.CrossRefGoogle ScholarPubMed
Wiesehan, K, Stöhr, J, Nagel-Steger, L, Van Groen, T, Riesner, D and Willbold, D (2008) Inhibition of cytotoxicity and amyloid fibril formation by a D-amino acid peptide that specifically binds to Alzheimer's disease amyloid peptide. Protein Engineering, Design and Selection 21, 241–246.CrossRefGoogle ScholarPubMed
Williams, TL and Serpell, LC (2011) Membrane and surface interactions of Alzheimer's Abeta peptide–insights into the mechanism of cytotoxicity. The FEBS Journal 278, 3905–3917.CrossRefGoogle ScholarPubMed
Wong, PT, Schauerte, JA, Wisser, KC, Ding, H, Lee, EL, Steel, DG and Gafni, A (2009) Amyloid-β membrane binding and permeabilization are distinct processes influenced separately by membrane charge and fluidity. Journal of Molecular Biology 386, 81–96.CrossRefGoogle ScholarPubMed
Yu, J and Lyubchenko, YL (2009) Early stages for Parkinson's development: alpha-synuclein misfolding and aggregation. Journal of Neuroimmune Pharmacology 4, 10–16.CrossRefGoogle ScholarPubMed
Yu, J, Malkova, S and Lyubchenko, YL (2008) Alpha-synuclein misfolding: single molecule AFM force spectroscopy study. Journal of Molecular Biology 384, 992–1001.CrossRefGoogle ScholarPubMed
Yu, J, Warnke, J and Lyubchenko, YL (2011) Nanoprobing of α-synuclein misfolding and aggregation with atomic force microscopy. Nanomedicine: Nanotechnology, Biology, and Medicine 7, 146–152.CrossRefGoogle ScholarPubMed
Yu, H, Liu, X, Neupane, K, Gupta, AN, Brigley, AM, Solanki, A, Sosova, I and Woodside, MT (2012) Direct observation of multiple misfolding pathways in a single prion protein molecule. Proceedings of the National Academy of Sciences 109, 5283–5288.CrossRefGoogle Scholar
Yu, H, Dee, DR and Woodside, MT (2013) Single-molecule approaches to prion protein misfolding. Prion 7, 140–146.CrossRefGoogle ScholarPubMed
Yu, RJ, Lu, SM, Xu, SW, Li, YJ, Xu, Q, Ying, YL and Long, YT (2019) Single molecule sensing of amyloid-β aggregation by confined glass nanopores. Chemical Science 10, 10728–10732.CrossRefGoogle ScholarPubMed
Yusko, EC, Johnson, JM, Majd, S, Prangkio, P, Rollings, RC, Li, J, Yang, J and Mayer, M (2011) Controlling protein translocation through nanopores with bio-inspired fluid walls. Nature Nanotechnology 6, 253–260.CrossRefGoogle ScholarPubMed
Yusko, EC, Prangkio, P, Sept, D, Rollings, RC, Li, J and Mayer, M (2012) Single-particle characterization of Aβ oligomers in solution. ACS Nano 6, 5909–5919.CrossRefGoogle ScholarPubMed
Yusko, EC, Bruhn, BR, Eggenberger, OM, Houghtaling, J, Rollings, RC, Walsh, NC, Nandivada, S, Pindrus, M, Hall, AR, Sept, D, Li, J, Kalonia, DS and Mayer, M (2017) Real-time shape approximation and fingerprinting of single proteins using a nanopore. Nature Nanotechnology 12, 360–367.CrossRefGoogle ScholarPubMed
Zetterberg, H and Burnham, SC (2019) Blood-based molecular biomarkers for Alzheimer's disease. Molecular Brain 12, 26.CrossRefGoogle ScholarPubMed
Zhang, Y, Ha, T and Marqusee, S (2018) Editorial overview: single-molecule approaches up to difficult challenges in folding and dynamics. Journal of Molecular Biology 430, 405–408.CrossRefGoogle ScholarPubMed
Zhao, Q, Jayawardhana, DA, Wang, D and Guan, X (2009) Study of peptide transport through engineered protein channels. The Journal of Physical Chemistry B 113, 3572–3578.CrossRefGoogle ScholarPubMed
Zheng, Y, Tian, S, Peng, X, Yang, J, Fu, Y, Jiao, Y, Zhao, J, He, J and Hong, T (2016) Kinesin-1 inhibits the aggregation of amyloid-β Peptide as detected by fluorescence cross-correlation spectroscopy. FEBS Letters 590, 1028–1037.CrossRefGoogle ScholarPubMed
Zheng, Y, Xu, L, Yang, J, Peng, X, Wang, H, Yu, N, Hua, Y, Zhao, J, He, J and Hong, T (2018) The effects of fluorescent labels on Aβ(42) aggregation detected by fluorescence correlation spectroscopy. Biopolymers 109, e23237.CrossRefGoogle ScholarPubMed