Single-particle characterization of Aβ oligomers in solution

ACS Nano

Volumn 6, Issue 7, 2012, Pages 5909-5919

  Yusko, Erik C ^a   Prangkio, Panchika ^a   Sept, David ^a   Rollings, Ryan C ^b   Li, Jiali ^b   Mayer, Michael ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF ARKANSAS   (United States)

Author keywords

amyloid aggregate; amyloid fiber; amyloid beta oligomer; bilayer coated nanopore; bootstrap resampling; cluster analysis; Coulter counter; cumulative distribution function; nanopore; probability density function; protofibril; resistive pulse; single molecule; size distribution

Indexed keywords

AMYLOID BETAS; AMYLOID FIBERS; BOOTSTRAP RESAMPLING; COULTER COUNTERS; CUMULATIVE DISTRIBUTION FUNCTION; PROTOFIBRIL; RESISTIVE PULSE; SINGLE MOLECULE;

AGGREGATES; CLUSTER ANALYSIS; LIPID BILAYERS; NANOPORES; OLIGOMERS; PROBABILITY DENSITY FUNCTION; SIZE DISTRIBUTION;

GLYCOPROTEINS;

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; PEPTIDE FRAGMENT;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; IN VITRO STUDY; LIPID BILAYER; MICROFLUIDIC ANALYSIS; NANOPORE; NANOTECHNOLOGY; PATCH CLAMP; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; SOLUTION AND SOLUBILITY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AMYLOID BETA-PEPTIDES; HUMANS; LIPID BILAYERS; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; NANOPORES; NANOTECHNOLOGY; PATCH-CLAMP TECHNIQUES; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; SOLUTIONS;

EID: 84864191240     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn300542q     Document Type: Article

References (99)

1. Trojanowski, J. Q.; Mattson, M. P. Overview of Protein Aggregation in Single, Double, and Triple Neurodegenerative Brain Amyloidoses Neuromol. Med. 2003, 4, 1-5 (Pubitemid 37315181)
2. Morgado, I.; Fandrich, M. Assembly of Alzheimer's A-Beta Peptide into Nanostructured Amyloid Fibrils Curr. Opin. Colloid Interface Sci. 2011, 16, 508-514
3. Querfurth, H. W.; LaFerla, F. M. Mechanisms of Disease Alzheimer's Disease N. Engl. J. Med. 2010, 362, 329-344
4. Selkoe, D. J. Clearing the Brain's Amyloid Cobwebs Neuron 2001, 32, 177-180 (Pubitemid 33030186)
5. Selkoe, D. J. Resolving Controversies on the Path to Alzheimer's Therapeutics Nat. Med. 2011, 17, 1060-1065
6. Hardy, J. A Hundred Years of Alzheimer's Disease Research Neuron 2006, 52, 3-13 (Pubitemid 44472602)
7. Schnabel, J. Little Proteins, Big Clues Nature 2011, 475, S12-S14
8. Ding, H.; Wong, P. T.; Lee, E. L.; Gafni, A.; Steel, D. G. Determination of the Oligomer Size of Amyloidogenic Protein Beta-Amyloid(1-40) by Single-Molecule Spectroscopy Biophys. J. 2009, 97, 912-921
9. Johnson, R. D.; Schauerte, J. A.; Wisser, K. C.; Gafni, A.; Steel, D. G. Direct Observation of Single Amyloid-Beta(1-40) Oligomers on Live Cells: Binding and Growth at Physiological Concentrations. PLoS One 2011, 6.
10. Ono, K.; Condron, M. M.; Teplow, D. B. Structure-Neurotoxicity Relationships of Amyloid Beta-Protein Oligomers Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 14745-14750
11. Cabriolu, R.; Kashchiev, D.; Auer, S. Size Distribution of Amyloid Nanofibrils Biophys. J. 2011, 101, 2232-2241
12. Kellermayer, M. S. Z.; Karsai, á.; Benke, M.; Soós, K.; Penke, B. Stepwise Dynamics of Epitaxially Growing Single Amyloid Fibrils Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 141-144
13. Goldsbury, C. S.; Wirtz, S.; Müller, S. A.; Sunderji, S.; Wicki, P.; Aebi, U.; Frey, P. Studies on the In Vitro Assembly of Aβ 1-40: Implications for the Search for Aβ Fibril Formation Inhibitors J. Struct. Biol. 2000, 130, 217-231
14. Lines, R. W. The Electrical Sensing Zone Method (the Coulter Principle). In Particle Size Analysis, Stanley-Wood, N. G.; Lines, R. W., Eds.; The Royal Society of Chemistry: Cambridge, 1992; p 352.
15. Demuro, A.; Mina, E.; Kayed, R.; Milton, S. C.; Parker, I.; Glabe, C. G. Calcium Dysregulation and Membrane Disruption as a Ubiquitous Neurotoxic Mechanism of Soluble Amyloid Oligomers J. Biol. Chem. 2005, 280, 17294-17300 (Pubitemid 41389198)
16. Giuffrida, M. L.; Caraci, F.; Pignataro, B.; Cataldo, S.; De Bona, P.; Bruno, V.; Molinaro, G.; Pappalardo, G.; Messina, A.; Palmigiano, A. et al. Beta-Amyloid Monomers are Neuroprotective J. Neurosci. 2009, 29, 10582-10587
17. Hartley, D. M.; Walsh, D. M.; Ye, C. P. P.; Diehl, T.; Vasquez, S.; Vassilev, P. M.; Teplow, D. B.; Selkoe, D. J. Protofibrillar Intermediates of Amyloid Beta-Protein Induce Acute Electrophysiological Changes and Progressive Neurotoxicity in Cortical Neurons J. Neurosci. 1999, 19, 8876-8884 (Pubitemid 30226709)
18. Bucciantini, M.; Giannoni, E.; Chiti, F.; Baroni, F.; Formigli, L.; Zurdo, J. S.; Taddei, N.; Ramponi, G.; Dobson, C. M.; Stefani, M. Inherent Toxicity of Aggregates Implies a Common Mechanism for Protein Misfolding Diseases Nature 2002, 416, 507-511 (Pubitemid 34288846)
19. Hortschansky, P.; Schroeckh, V.; Christopeit, T.; Zandomeneghi, G.; Fandrich, M. The Aggregation Kinetics of Alzheimer's Beta-Amyloid Peptide is Controlled by Stochastic Nucleation Protein Sci. 2005, 14, 1753-1759 (Pubitemid 40994145)
20. Zagorski, M. G.; Shao, H.; Ma, K.; Li, H.; Yang, J.; Zeng, H. Amyloid Abeta-the Peptide from Hell Regul. Pept. 2001, 97, 31
21. Zagorski, M. G.; Yang, J.; Shao, H. Y.; Ma, K.; Zeng, H.; Hong, A. Methodological and Chemical Factors Affecting Amyloid Beta Peptide Amyloidogenicity Methods Enzymol. 1999, 309, 189-204 (Pubitemid 29446450)
22. Parihar, M. S.; Hemnani, T. Alzheimer's Disease Pathogenesis and Therapeutic Interventions J. Clin. Neurosci. 2004, 11, 456-467 (Pubitemid 38869470)
23. Walsh, D. M.; Hartley, D. M.; Kusumoto, Y.; Fezoui, Y.; Condron, M. M.; Lomakin, A.; Benedek, G. B.; Selkoe, D. J.; Teplow, D. B. Amyloid Beta-Protein Fibrillogenesis-Structure and Biological Activity of Protofibrillar Intermediates J. Biol. Chem. 1999, 274, 25945-25952
24. Jan, A.; Hartley, D. M.; Lashuel, H. A. Preparation and Characterization of Toxic A-Beta Aggregates for Structural and Functional Studies in Alzheimer's Disease Research Nat. Protoc. 2010, 5, 1186-1209
25. Roychaudhuri, R.; Yang, M.; Hoshi, M. M.; Teplow, D. B. Amyloid Beta-Protein Assembly and Alzheimer Disease J. Biol. Chem. 2009, 284, 4749-4753
26. Schmidt, M.; Sachse, C.; Richter, W.; Xu, C.; Fandrich, M.; Grigorieff, N. Comparison of Alzheimer A-Beta(1-40) and A-Beta(1-42) Amyloid Fibrils Reveals Similar Protofilament Structures Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 19813-19818
27. Sachse, C.; Fandrich, M.; Grigorieff, N. Paired Beta-Sheet Structure of an A-Beta(1-40) Amyloid Fibril Revealed by Electron Microscopy Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 7462-7466 (Pubitemid 351830040)
28. Capone, R.; Quiroz, F. G.; Prangkio, P.; Saluja, I.; Sauer, A. M.; Bautista, M. R.; Turner, R. S.; Yang, J.; Mayer, M. Amyloid-Beta-Induced Ion Flux in Artificial Lipid Bilayers and Neuronal Cells: Resolving a Controversy Neurotox. Res. 2009, 16, 1-13
29. Bitan, G.; Fradinger, E. A.; Spring, S. M.; Teplow, D. B. Neurotoxic Protein Oligomers-What You See Is Not Always What You Get Amyloid-J. Protein Fold. Disord. 2005, 12, 88-95 (Pubitemid 40978716)
30. Adamcik, J.; Jung, J. M.; Flakowski, J.; De Los Rios, P.; Dietler, G.; Mezzenga, R. Understanding Amyloid Aggregation by Statistical Analysis of Atomic Force Microscopy Images Nat. Nanotechnol. 2010, 5, 423-428
31. Meinhardt, J.; Sachse, C.; Hortschansky, P.; Grigorieff, N.; Fandrich, M. A Beta(1-40) Fibril Polymorphism Implies Diverse Interaction Patterns in Amyloid Fibrils J. Mol. Biol. 2009, 386, 869-877
32. Kremer, J. J.; Pallitto, M. M.; Sklansky, D. J.; Murphy, R. M. Correlation of Beta-Amyloid Aggregate Size and Hydrophobicity with Decreased Bilayer Fluidity of Model Membranes Biochemistry 2000, 39, 10309-10318 (Pubitemid 30663053)
33. Chou, I. H.; Benford, M.; Beier, H. T.; Coté, G. L.; Wang, M.; Jing, N.; Kameoka, J.; Good, T. A. Nanofluidic Biosensing for B-Amyloid Detection Using Surface Enhanced Raman Spectroscopy Nano Lett. 2008, 8, 1729-1735
34. Knowles, T. P. J.; White, D. A.; Abate, A. R.; Agresti, J. J.; Cohen, S. I. A.; Sperling, R. A.; De Genst, E. J.; Dobson, C. M.; Weitz, D. A. Observation of Spatial Propagation of Amyloid Assembly from Single Nuclei Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 14746-14751
35. Schierle, G. S. K.; van de Linde, S.; Erdelyi, M.; Esbjorner, E. K.; Klein, T.; Rees, E.; Bertoncini, C. W.; Dobson, C. M.; Sauer, M.; Kaminski, C. F. In Situ Measurements of the Formation and Morphology of Intracellular Beta-Amyloid Fibrils by Super-Resolution Fluorescence Imaging J. Am. Chem. Soc. 2011, 133, 12902-12905
36. Wang, H. Y.; Ying, Y. L.; Li, Y.; Kraatz, H. B.; Long, Y. T. Nanopore Analysis of Beta-Amyloid Peptide Aggregation Transition Induced by Small Molecules Anal. Chem. 2011, 83, 1746-1752
37. Dukes, K. D.; Rodenberg, C. F.; Lammi, R. K. Monitoring the Earliest Amyloid-Beta Oligomers via Quantized Photobleaching of Dye-Labeled Peptides Anal. Biochem. 2008, 382, 29-34
38. Schauerte, J. A.; Wong, P. T.; Wisser, K. C.; Ding, H.; Steel, D. G.; Gafni, A. Simultaneous Single-Molecule Fluorescence and Conductivity Studies Reveal Distinct Classes of A-Beta Species on Lipid Bilayers Biochemistry 2010, 49, 3031-3039
39. Yusko, E. C.; Johnson, J. M.; Majd, S.; Prangkio, P.; Rollings, R. C.; Li, J.; Yang, J.; Mayer, M. Controlling Protein Translocation through Nanopores with Bio-Inspired Fluid Walls Nat. Nanotechnol. 2011, 6, 253-260
40. Actis, P.; Rogers, A.; Nivala, J.; Vilozny, B.; Seger, R. A.; Jejelowo, O.; Pourmand, N. Reversible Thrombin Detection by Aptamer Functionalized Sting Sensors Biosens. Bioelectron. 2011, 26, 4503-4507
41. Coulter, W. H. Means for Counting Particles Suspended in a Fluid. U.S. Patent 2,656,508, October 20, 1953.
42. Dekker, C. Solid-State Nanopores Nat. Nanotechnol. 2007, 2, 209-215 (Pubitemid 46739810)
43. Kowalczyk, S. W.; Blosser, T. R.; Dekker, C. Biomimetic Nanopores: Learning from and about Nature Trends Biotechnol. 2011, 29, 607-614
44. Howorka, S.; Siwy, Z. Nanopore Analytics: Sensing of Single Molecules Chem. Soc. Rev. 2009, 38, 2360-2384
45. Majd, S.; Yusko, E. C.; Billeh, Y. N.; Macrae, M. X.; Yang, J.; Mayer, M. Applications of Biological Pores in Nanomedicine, Sensing, and Nanoelectronics Curr. Opin. Biotechnol. 2010, 21, 439-476
46. Yusko, E. C.; Billeh, Y. N.; Yang, J.; Mayer, M. Nanopore Recordings to Quanitify Activity-Related Properties of Proteins. In Nanopores: Sensing and Fundamental Biological Interactions, Iqbal, S. M.; Bashir, R., Eds.; Springer Publishing Co.: New York, 2011; pp 203-225.
47. Stanley-Wood, N. G.; Lines, R. W. Particle Size Analysis; The Royal Society of Chemistry: Cambridge, 1992; p 352.
48. Branton, D.; Deamer, D. W.; Marziali, A.; Bayley, H.; Benner, S. A.; Butler, T.; Di Ventra, M.; Garaj, S.; Hibbs, A.; Huang, X. H. et al. The Potential and Challenges of Nanopore Sequencing Nat. Biotechnol. 2008, 26, 1146-1153
49. Keyser, U. F. Controlling Molecular Transport through Nanopores J. R. Soc. Interface 2011, 8, 1369-1378
50. Ivanov, A. P.; Instuli, E.; McGilvery, C. M.; Baldwin, G.; McComb, D. W.; Albrecht, T.; Edel, J. B. DNA Tunneling Detector Embedded in a Nanopore Nano Lett. 2011, 11, 279-285
51. Iqbal, S. M.; Bashir, R. Nanoelectronic-Based Detection for Biology and Medicine; Springer-Verlag: Berlin, 2009; pp 1433-1449.
52. Actis, P.; Jejelowo, O.; Pourmand, N. Ultrasensitive Mycotoxin Detection by Sting Sensors Biosens. Bioelectron. 2010, 26, 333-337
53. Grover, N. B.; Naaman, J.; Ben-sasson, S.; Doljansk, F. Electrical Sizing of Particles in Suspensions. I. Theory Biophys. J. 1969, 9, 1398-1414
54. Grover, N. B.; Naaman, J.; Ben-sasson, S.; Doljansk, F.; Nadav, E. Electrical Sizing of Particles in Suspensions. 2. Experiments with Rigid Spheres Biophys. J. 1969, 9, 1415-1425
55. Solomentsev, Y.; Anderson, J. L. Electrophoresis of Slender Particles J. Fluid Mech. 1994, 279, 197-215
56. Han, A. P.; Creus, M.; Schurmann, G.; Linder, V.; Ward, T. R.; de Rooij, N. F.; Staufer, U. Label-Free Detection of Single Protein Molecules and Protein-Protein Interactions Using Synthetic Nanopores Anal. Chem. 2008, 80, 4651-4658 (Pubitemid 351842344)
57. Sexton, L. T.; Mukaibo, H.; Katira, P.; Hess, H.; Sherrill, S. A.; Horne, L. P.; Martin, C. R. An Adsorption-Based Model for Pulse Duration in Resistive-Pulse Protein Sensing J. Am. Chem. Soc. 2010, 132, 6755-6763
58. Cai, Q.; Ledden, B.; Krueger, E.; Golovchenko, J. A.; Li, J. L. Nanopore Sculpting with Noble Gas Ions J. Appl. Phys. 2006, 100, 024914
59. Li, J.; Stein, D.; McMullan, C.; Branton, D.; Aziz, M. J.; Golovchenko, J. A. Ion-Beam Sculpting at Nanometre Length Scales Nature 2001, 412, 166-169 (Pubitemid 32674708)
60. Prangkio, P. Investigation of Cytotoxicity and Ion Flux Induced by Various Aggregation States of Amyloid-Beta Peptides. Ph.D. Thesis. University of Michigan: Ann Arbor, MI, August 9, 2011.
61. Horiuchi, M.; Maezawa, I.; Itoh, A.; Wakayama, K.; Jin, L. W.; Itoh, T.; DeCarli, C. Amyloid Beta 1-42 Oligomer Inhibits Myelin Sheet Formation in Vitro Neurobiol. Aging 2012, 33, 499-509
62. Brining, S. K. Predicting the in Vitro Toxicity of Synthetic Beta-Amyloid (1-40) Neurobiol. Aging 1997, 18, 581-589 (Pubitemid 28046411)
63. Pedone, D.; Firnkes, M.; Rant, U. Data Analysis of Translocation Events in Nanopore Experiments Anal. Chem. 2009, 81, 9689-9694
64. Fologea, D.; Brandin, E.; Uplinger, J.; Branton, D.; Li, J. DNA Conformation and Base Number Simultaneously Determined in a Nanopore Electrophoresis 2007, 28, 3186-3192 (Pubitemid 47506447)
65. Storm, A. J.; Storm, C.; Chen, J. H.; Zandbergen, H.; Joanny, J. F.; Dekker, C. Fast DNA Translocation through a Solid-State Nanopore Nano Lett. 2005, 5, 1193-1197 (Pubitemid 41084390)
66. Meller, A.; Nivon, L.; Branton, D. Voltage-Driven DNA Translocations through a Nanopore Phys. Rev. Lett. 2001, 86, 3435-3438 (Pubitemid 32380654)
67. Li, J. L.; Talaga, D. S. The Distribution of DNA Translocation Times in Solid-State Nanopores J. Phys.-Condens. Matter 2010, 22
68. Rousseeuw, P. J.; Kaufman, L. Finding Groups in Data: An Introduction to Cluster Analysis; John Wiley & Sons, Inc.: New York, 1990.
69. Kerr, M. K.; Churchill, G. A. Bootstrapping Cluster Analysis: Assessing the Reliability of Conclusions from Microarray Experiments Proc. National Acad. Sci. 2001, 98, 8961-8965 (Pubitemid 32743852)
70. Talaga, D. S.; Li, J. L. Single-Molecule Protein Unfolding in Solid State Nanopores J. Am. Chem. Soc. 2009, 131, 9287-9297
71. Ito, T.; Sun, L.; Crooks, R. M. Simultaneous Determination of the Size and Surface Charge of Individual Nanoparticles Using a Carbon Nanotube-Based Coulter Counter Anal. Chem. 2003, 75, 2399-2406 (Pubitemid 36582825)
72. Fologea, D.; Ledden, B.; David, S. M.; Li, J. Electrical Characterization of Protein Molecules by a Solid-State Nanopore Appl. Phys. Lett. 2007, 91, 053901
73. Uram, J. D.; Ke, K.; Hunt, A. J.; Mayer, M. Submicrometer Pore-Based Characterization and Quantification of Antibody-Virus Interactions Small 2006, 2, 967-972 (Pubitemid 44230993)
74. Uram, J. D.; Ke, K.; Hunt, A. J.; Mayer, M. Label-Free Affinity Assays by Rapid Detection of Immune Complexes in Submicrometer Pores Angew. Chem., Int. Ed. 2006, 45, 2281-2285 (Pubitemid 44105163)
75. DeBlois, R. W.; Uzgiris, E. E.; Cluxton, D. H.; Mazzone, H. M. Comparative Measurements of Size and Polydispersity of Several Insect Viruses Anal. Biochem. 1978, 90, 273-288 (Pubitemid 9062253)
76. Golibersuch, D. C. Observation of Aspherical Particle Rotation in Poiseuille Flow via the Resistance Pulse Technique. Part 2. Application to Fused Sphere Dumbbells J. Appl. Phys. 1973, 44, 2580-2584
77. Golibersuch, D. C. Observation of Aspherical Particle Rotation in Poiseuille Flow via the Resistance Pulse Technique. Part 1. Application to Human Erythrocytes Biophys. J. 1973, 13, 265-280
78. Kozak, D.; Anderson, W.; Vogel, R.; Trau, M. Advances in Resistive Pulse Sensors: Devices Bridging the Void between Molecular and Microscopic Detection Nano Today 2011, 6, 531-545
79. Hille, B. Ion Channels of Excitable Membranes; Sinauer Associaties, Inc.: Sunderland, 2001; pp 347-349.
80. 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. et al. Diffusible, Nonfibrillar Ligands Derived from Aβ1-42 Are Potent Central Nervous System Neurotoxins Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 6448-6453
81. Matthews, B. W. Solvent Content of Protein Crystals J. Mol. Biol. 1968, 33, 491.
82. Adler, J. R in a Nutshell; O'Reilly Media, Inc.: Sebastopol, CA, 2010; p 333.
83. Whitlock, M. C.; Schluter, D. The Analysis of Biological Data; Roberts and Company Publishers: Greenwood Village, CO, 2009; pp 550-557.
84. Solomentsev, Y.; Anderson, J. L. Electrophoretic Transport of Spheroidal Colloids in Nonhomogeneous Electric Fields Ind. Eng. Chem. Res. 1995, 34, 3231-3238
85. Wanunu, M.; Morrison, W.; Rabin, Y.; Grosberg, A. Y.; Meller, A. Electrostatic Focusing of Unlabelled DNA into Nanoscale Pores Using a Salt Gradient Nat. Nanotechnol. 2010, 5, 160-165
86. Bretherton, F. P. The Motion of Rigid Particles in a Shear Flow at Low Reynolds Number J. Fluid Mech. 1962, 14, 284-304
87. Ai, Y.; Qian, S. Direct Numerical Simulation of Electrokinetic Translocation of a Cylindrical Particle through a Nanopore Using a Poisson-Boltzmann Approach Electrophoresis 2011, 32, 996-1005
88. Berg, H. C. Random Walks in Biology; Princeton University Press: Princeton, NJ, 1993.
89. Guo, M.; Gorman, P. M.; Rico, M.; Chakrabartty, A.; Laurents, D. V. Charge Substitution Shows That Repulsive Electrostatic Interactions Impede the Oligomerization of Alzheimer Amyloid Peptides FEBS Lett. 2005, 579, 3574-3578 (Pubitemid 40897694)
90. An, R.; Uram, J. D.; Yusko, E. C.; Ke, K.; Mayer, M.; Hunt, A. J. Ultrafast Laser Fabrication of Submicrometer Pores in Borosilicate Glass Opt. Lett. 2008, 33, 1153-1155
91. Sun, L.; Crooks, R. M. Single Carbon Nanotube Membranes: A Well-Defined Model for Studying Mass Transport through Nanoporous Materials J. Am. Chem. Soc. 2000, 122, 12340-12345 (Pubitemid 32062272)
92. Lee, S.; Zhang, Y. H.; White, H. S.; Harrell, C. C.; Martin, C. R. Electrophoretic Capture and Detection of Nanoparticles at the Opening of a Membrane Pore Using Scanning Electrochemical Microscopy Anal. Chem. 2004, 76, 6108-6115 (Pubitemid 39382959)
93. Bikwemu, R.; Wolfe, A. J.; Xing, X. J.; Movileanu, L. Facilitated Translocation of Polypeptides through a Single Nanopore. J. Phys.-Condens. Matter 2010, 22.
94. Bacri, L.; Oukhaled, A. G.; Schiedt, B.; Patriarche, G.; Bourhis, E.; Gierak, J.; Pelta, J.; Auvray, L. Dynamics of Colloids in Single Solid-State Nanopores J. Phys. Chem. B 2011, 115, 2890-2898
95. Harper, J. D.; Lansbury, P. T. Models of Amyloid Seeding in Alzheimier's Disease and Scrapie: Mechanistic Truths and Physiological Consequences of the Time-Dependent Solubility of Amyloid Proteins Annu. Rev. Biochem. 1997, 66, 385-407 (Pubitemid 27274662)
96. Simakova, O.; Arispe, N. J. The Cell-Selective Neurotoxicity of the Alzheimer's A-Beta Peptide is Determined by Surface Phosphatidylserine and Cytosolic ATP Levels. Membrane Binding Is Required for a Beta Toxicity J. Neurosci. 2007, 27, 13719-13729 (Pubitemid 350278273)
97. Vestergaard, M.; Hamada, T.; Takagi, M. Using Model Membranes for the Study of Amyloid Beta: Lipid Interactions and Neurotoxicity Biotechnol. Bioeng. 2008, 99, 753-763 (Pubitemid 351316617)
98. Williams, T. L.; Serpell, L. C. Membrane and Surface Interactions of Alzheimer's A-Beta Peptide-Insights into the Mechanism of Cytotoxicity Febs J. 2011, 278, 3905-3917
99. Uram, J. D.; Ke, K.; Mayer, M. Noise and Bandwidth of Current Recordings from Submicrometer Pores and Nanopores ACS Nano 2008, 2, 857-872