Probing the sources of the apparent irreproducibility of amyloid formation: Drastic changes in kinetics and a switch in mechanism due to micellelike oligomer formation at critical concentrations of IAPP

Journal of Physical Chemistry B

Volumn 119, Issue 7, 2015, Pages 2886-2896

  Brender, Jeffrey R ^a   Krishnamoorthy, Janarthanan ^a   Sciacca, Michele F M ^a,b   Vivekanandan, Subramanian ^a   D'Urso, Luisa ^b   Chen, Jennifer ^a   La Rosa, Carmelo ^b   Ramamoorthy, Ayyalusamy ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEINS; OLIGOMERS; PYRENE; TEMPERATURE;

AMYLOID FORMATION; AMYLOIDOGENIC PROTEINS; CRITICAL CONCENTRATION; CRITICAL TEMPERATURES; ISLET AMYLOID POLYPEPTIDES; OLIGOMER FORMATIONS; PYRENE FLUORESCENCE; SELF-INTERACTIONS;

PROTEINS;

AMYLIN; MICELLE; PYRENE; PYRENE DERIVATIVE;

CHEMISTRY; FLUORESCENCE; KINETICS; MICELLE; PH; PROTEIN MULTIMERIZATION; SPECTROSCOPY; TEMPERATURE;

FLUORESCENCE; HYDROGEN-ION CONCENTRATION; ISLET AMYLOID POLYPEPTIDE; KINETICS; MICELLES; PROTEIN MULTIMERIZATION; PYRENES; SPECTRUM ANALYSIS; TEMPERATURE;

EID: 84923326755     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp511758w     Document Type: Article

References (96)

1. Ross, C. A.; Poirier, M. A. Protein Aggregation and Neurodegenerative Disease Nat. Med. 2004, 10, S10-S17
2. Harrison, R. S.; Sharpe, P. C.; Singh, Y.; Fairlie, D. P. Amyloid Peptides and Proteins in Review Rev. Physiol. Biochem. Pharm. 2007, 159, 1-77
3. Hamley, I. W. The Amyloid Beta Peptide: A Chemist's Perspective. Role in Alzheimer's and Fibrillization Chem. Rev. 2012, 112, 5147-5192
4. Marchesi, V. T. Alzheimer's Disease 2012: The Great Amyloid Gamble Am. J. Pathol. 2012, 180, 1762-1767
5. Liu, T. Y.; Bitan, G. Modulating Self-Assembly of Amyloidogenic Proteins as a Therapeutic Approach for Neurodegenerative Diseases: Strategies and Mechanisms ChemMedChem. 2012, 7, 359-374
6. 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
7. Giehm, L.; Otzen, D. E. Strategies to Increase the Reproducibility of Protein Fibrillization in Plate Reader Assays Anal. Biochem. 2010, 400, 270-281
8. Teplow, D. B. On the Subject of Rigor in the Study of Amyloid Beta-Protein Assembly Alzheimer's Res. Ther. 2013, 5, 39
9. Veeraraghavalu, K.; Zhang, C.; Miller, S.; Hefendehl, J. K.; Rajapaksha, T. W.; Ulrich, J.; Jucker, M.; Holtzman, D. M.; Tanzi, R. E.; Vassar, R. Comment on "ApoE-Directed Therapeutics Rapidly Clear Beta-Amyloid and Reverse Deficits in AD Mouse Models" Science 2013, 340, 924
10. Tesseur, I.; Lo, A. C.; Roberfroid, A.; Dietvorst, S.; Van Broeck, B.; Borgers, M.; Gijsen, H.; Moechars, D.; Mercken, M.; Kem J. Comment on "ApoE-Directed Therapeutics Rapidly Clear Beta-Amyloid and Reverse Deficits in AD Mouse Models" Science 2013, 340, 924
11. Landreth, G. E.; Cramer, P. E.; Lakner, M. M.; Cirrito, J. R.; Wesson, D. W.; Brunden, K. R.; Wilson, D. A. Response to Comments on "ApoE-Directed Therapeutics Rapidly Clear Beta-Amyloid and Reverse Deficits in Ad Mouse Models" Science 2013, 340, 924
12. Price, A. R.; Xu, G. L.; Siemienski, Z. B.; Smithson, L. A.; Borchelt, D. R.; Golde, T. E.; Felsenstein, K. M. Comment on "ApoE-Directed Therapeutics Rapidly Clear Beta-Amyloid and Reverse Deficits in AD Mouse Models" Science 2013, 340, 924
13. Fitz, N. F.; Cronican, A. A.; Lefterov, I.; Koldamova, R. Comment on "ApoE-Directed Therapeutics Rapidly Clear Beta-Amyloid and Reverse Deficits in AD Mouse Models" Science 2013, 340, 924
14. Cramer, P. E.; Cirrito, J. R.; Wesson, D. W.; Lee, C. Y. D.; Karlo, J. C.; Zinn, A. E.; Casali, B. T.; Restivo, J. L.; Goebel, W. D.; James, M. J. ApoE-Directed Therapeutics Rapidly Clear Beta-Amyloid and Reverse Deficits in AD Mouse Models Science 2012, 335, 1503-1506
15. Pimplikar, S. W. Reassessing the Amyloid Cascade Hypothesis of Alzheimer's Disease Int. J. Biochem. Cell B 2009, 41, 1261-1268
16. Benilova, I.; Karran, E.; De Strooper, B. The Toxic Aβ Oligomer and Alzheimer's Disease: An Emperor in Need of Clothes Nat. Neurosci. 2012, 15, 349-357
17. Haataja, L.; Gurlo, T.; Huang, C. J.; Butler, P. C. Islet Amyloid in Type 2 Diabetes, and the Toxic Oligomer Hypothesis Endocr. Rev. 2008, 29, 303-316
18. Fandrich, M. Oligomeric Intermediates in Amyloid Formation: Structure Determination and Mechanisms of Toxicity J. Mol. Biol. 2012, 421, 427-440
19. Haass, C.; Selkoe, D. J. Soluble Protein Oligomers in Neurodegeneration: Lessons from the Alzheimer's Amyloid Beta-Peptide Nat..Rev. Mol. Cell. Biol. 2007, 8, 101-112
20. Garvey, M.; Tepper, K.; Haupt, C.; Knupfer, U.; Klement, K.; Meinhardt, J.; Horn, U.; Balbach, J.; Fandrich, M. Phosphate and HEPES Buffers Potently Affect the Fibrillation and Oligomerization Mechanism of Alzheimer's Aβ Peptide Biochem. Biophys. Res. Commun. 2011, 409, 385-388
21. Olsen, J. S.; DiMaio, J. T. M.; Doran, T. M.; Brown, C.; Nilsson, B. L.; Dewhurst, S. Seminal Plasma Accelerates Semen-Derived Enhancer of Viral Infection (SEVI) Fibril Formation by the Prostatic Acid Phosphatase (Pap(248-286)) Peptide J. Biol. Chem. 2012, 287, 11842-11849
22. Pronchik, J.; He, X. L.; Giurleo, J. T.; Talaga, D. S. In Vitro Formation of Amyloid from Alpha-Synuclein Is Dominated by Reactions at Hydrophobic Interfaces J. Am. Chem. Soc. 2010, 132, 9797-9803
23. Teplow, D. B. Preparation of Amyloid Beta-Protein for Structural and Functional Studies Methods Enzymol. 2006, 413, 20-33
24. Stine, W. B.; Jungbauer, L.; Yu, C. J.; Ladu, M. J. Preparing Synthetic a Beta in Different Aggregation States Methods Mol. Biol. 2011, 670, 13-32
25. Hellstrand, E.; Boland, B.; Walsh, D. M.; Linse, S. Amyloid Beta-Protein Aggregation Produces Highly Reproducible Kinetic Data and Occurs by a Two-Phase Process ACS Chem. Neurosci. 2010, 1, 13-18
26. Westermark, P.; Andersson, A.; Westermark, G. T. Islet Amyloid Polypeptide, Islet Amyloid, and Diabetes Mellitus Physiol Rev. 2011, 91, 795-826
27. Uversky, V. N.; Fink, A. L. Conformational Constraints for Amyloid Fibrillation: The Importance of Being Unfolded Biochim. Biophys. Acta 2004, 1698, 131-153
28. Yonemoto, I. T.; Kroon, G. J.; Dyson, H. J.; Balch, W. E.; Kelly, J. W. Amylin Proprotein Processing Generates Progressively More Amyloidogenic Peptides That Initially Sample the Helical State Biochemistry 2008, 47, 9900-9910
29. Tu, L.-H.; Serrano, A. L.; Zanni, M. T.; Raleigh, D. P. Mutational Analysis of Preamyloid Intermediates: The Role of His-Tyr Interactions in Islet Amyloid Formation Biophys. J. 2014, 106, 1520-1527
30. Wei, L.; Jiang, P.; Xu, W. X.; Li, H.; Zhang, H.; Yan, L. Y.; Chan-Park, M. B.; Liu, X. W.; Tang, K.; Mu, Y. G. The Molecular Basis of Distinct Aggregation Pathways of Islet Amyloid Polypeptide J. Biol. Chem. 2011, 286, 6291-6300
31. Padrick, S. B.; Miranker, A. D. Islet Amyloid Polypeptide: Identification of Long-Range Contacts and Local Order on the Fibrillogenesis Pathway J. Mol. Biol. 2001, 308, 783-794
32. Nanga, R. P. R.; Brender, J. R.; Vivekanandan, S.; Ramamoorthy, A. Structure and Membrane Orientation of IAPP in Its Natively Amidated Form at Physiological pH in a Membrane Environment Biochim. Biophys. Acta 2011, 1808, 2337-2342
33. Lomakin, A.; Chung, D. S.; Benedek, G. B.; Kirschner, D. A.; Teplow, D. B. On the Nucleation and Growth of Amyloid Beta-Protein Fibrils: Detection of Nuclei and Quantitation of Rate Constants Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 1125-1129
34. Lomakin, A.; Teplow, D. B.; Kirschner, D. A.; Benedek, G. B. Kinetic Theory of Fibrillogenesis of Amyloid Beta-Protein Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 7942-7947
35. Kashchiev, D.; Cabriolu, R.; Auer, S. Confounding the Paradigm: Peculiarities of Amyloid Fibril Nucleation J. Am. Chem. Soc. 2013, 135, 1531-1539
36. Pellarin, R.; Friedman, R.; Caflisch, A. Amyloid Aggregation on Lipid Bilayers and Its Impact on Membrane Permeability J. Mol. Biol. 2009, 387, 407-415
37. Oosawa, F.; Asakura, S. Thermodynamics of the Polymerization of Protein; Academic Press: London, 1975; pg. 204.
38. Hong, L.; Qi, X. H.; Zhang, Y. Dissecting the Kinetic Process of Amyloid Fiber Formation through Asymptotic Analysis J. Phys. Chem. B 2012, 116, 6611-6617
39. Yong, W.; Lomakin, A.; Kirkitadze, M. D.; Teplow, D. B.; Chen, S. H.; Benedek, G. B. Structure Determination of Micelle-Like Intermediates in Amyloid Beta-Protein Fibril Assembly by Using Small Angle Neutron Scattering Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 150-154
40. Sabate, R.; Estelrich, J. Evidence of the Existence of Micelles in the Fibrillogenesis of Beta-Amyloid Peptide J. Phys. Chem. B 2005, 109, 11027-11032
41. Rhoades, E.; Gafni, A. Micelle Formation by a Fragment of Human Islet Amyloid Polypeptide Biophys. J. 2003, 84, 3480-3487
42. Jean, L.; Lee, C. F.; Lee, C.; Shaw, M.; Vaux, D. J. Competing Discrete Interfacial Effects Are Critical for Amyloidogenesis FASEB J. 2010, 24, 309-317
43. Padrick, S. B.; Miranker, A. D. Islet Amyloid: Phase Partitioning and Secondary Nucleation Are Central to the Mechanism of Fibrillogenesis Biochemistry 2002, 41, 4694-4703
44. Rhoades, E.; Agarwal, J.; Gafni, A. Aggregation of an Amyloidogenic Fragment of Human Islet Amyloid Polypeptide Biochim. Biophys. Acta 2000, 1476, 230-238
45. Kalyanasundaram, K.; Thomas, J. K. Environmental Effects on Vibronic Band Intensities in Pyrene Monomer Fluorescence and Their Application in Studies of Micellar Systems J. Am. Chem. Soc. 1977, 99, 2039-2044
46. Ruiz, C. C.; Aguiar, J.; Carpena, P.; Molina-Bolivar, J. A. On the Determination of the Critical Micelle Concentration by the Pyrene 1:3 Ratio Method J. Colloid Interface Sci. 2003, 258, 116-122
47. Reinke, A. A.; Ung, P. M. U.; Quintero, J. J.; Carlson, H. A.; Gestwicki, J. E. Chemical Probes That Selectively Recognize the Earliest Aβ Oligomers in Complex Mixtures J. Am. Chem. Soc. 2010, 132, 17655-17657
48. Israelachvili, J. N. Intermolecular and Surface Forces, 3 rd ed.; Academic Press: Burlington, MA, 2011; p 674.
49. Jan, A.; Hartley, D. M.; Lashuel, H. A. Preparation and Characterization of Toxic Aβ Aggregates for Structural and Functional Studies in Alzheimer's Disease Research Nat. Protoc. 2010, 5, 1186-1209
50. Pan, J.; Han, J.; Borchers, C. H.; Konermann, L. Structure and Dynamics of Small Soluble Aβ(1-40) Oligomers Studied by Top-Down Hydrogen Exchange Mass Spectrometry Biochemistry 2012, 51, 3694-3703
51. Woodbury, R. L.; Hardy, S. J.; Randall, L. L. Complex Behavior in Solution of Homodimeric Seca Protein Sci. 2002, 11, 875-882
52. Barbar, E. NMR Characterization of Partially Folded and Unfolded Conformational Ensembles of Proteins Biopolymers 1999, 51, 191-207
53. Brender, J. R.; Hartman, K.; Reid, K. R.; Kennedy, R. T.; Ramamoorthy, A. A Single Mutation in the Nonamyloidogenic Region of Islet Amyloid Polypeptide Greatly Reduces Toxicity Biochemistry 2008, 47, 12680-12688
54. Cao, P.; Abedini, A.; Wang, H.; Tu, L. H.; Zhang, X.; Schmidt, A. M.; Raleigh, D. P. Islet Amyloid Polypeptide Toxicity and Membrane Interactions Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 19279-19284
55. Radovan, D.; Smirnovas, V.; Winter, R. Effect of Pressure on Islet Amyloid Polypeptide Aggregation: Revealing the Polymorphic Nature of the Fibrillation Process Biochemistry 2008, 47, 6352-6360
56. Narayanan, S.; Reif, B. Characterization of Chemical Exchange between Soluble and Aggregated States of Beta-Amyloid by Solution-State NMR Upon Variation of Salt Conditions Biochemistry 2005, 44, 1444-1452
57. Huang, R.; Vivekanandan, S.; Brender, J. R.; Abe, Y.; Naito, A.; Ramamoorthy, A. NMR Characterization of Monomeric and Oligomeric Conformations of Human Calcitonin and Its Interaction with EGCG J. Mol. Biol. 2012, 416, 108-120
58. Krishnamoorthy, J.; Brender, J. R.; Vivekanandan, S.; Jahr, N.; Ramamoorthy, A. Side-Chain Dynamics Reveals Transient Association of Aβ(1-40) Monomers with Amyloid Fibers J. Phys. Chem. B 2012, 116, 13618-13623
59. Dorgeret, B.; Khemtemourian, L.; Correia, I.; Soulier, J. L.; Lequin, O.; Ongeri, S. Sugar-Based Peptidomimetics Inhibit Amyloid Beta-Peptide Aggregation Eur. J. Med. Chem. 2011, 46, 5959-5969
60. Soong, R.; Brender, J. R.; Macdonald, P. M.; Ramamoorthy, A. Association of Highly Compact Type Ii Diabetes Related Islet Amyloid Polypeptide Intermediate Species at Physiological Temperature Revealed by Diffusion NMR Spectroscopy J. Am. Chem. Soc. 2009, 131, 7079-7085
61. Fawzi, N. L.; Ying, J.; Torchia, D. A.; Clore, G. M. Kinetics of Amyloid Beta Monomer-to-Oligomer Exchange by Nmr Relaxation J. Am. Chem. Soc. 2010, 132, 9948-9951
62. Fawzi, N. L.; Ying, J. F.; Ghirlando, R.; Torchia, D. A.; Clore, G. M. Atomic-Resolution Dynamics on the Surface of Amyloid-Beta Protofibrils Probed by Solution NMR Nature 2011, 480, 268-272
63. Fawzi, N. L.; Ying, J. F.; Torchia, D. A.; Clore, G. M. Probing Exchange Kinetics and Atomic Resolution Dynamics in High-Molecular-Weight Complexes Using Dark-State Exchange Saturation Transfer Nmr Spectroscopy Nat. Protoc. 2012, 7, 1523-1533
64. Esposito, V.; Das, R.; Melacini, G. Mapping Polypeptide Self-Recognition through H-1 Off-Resonance Relaxation J. Am. Chem. Soc. 2005, 127, 9358-9359
65. Algamal, M.; Milojevic, J.; Jafari, N.; Zhang, W.; Melacini, G. Mapping the Interactions between the Alzheimer's Abeta-Peptide and Human Serum Albumin Beyond Domain Resolution Biophys. J. 2013, 105, 1700-1709
66. Milojevic, J.; Costa, M.; Ortiz, A. M.; Jorquera, J. I.; Melacini, G. In Vitro Amyloid-Beta Binding and Inhibition of Amyloid-Beta Self-Association by Therapeutic Albumin J. Alzheimer's Dis. 2014, 38, 753-765
67. Milojevic, J.; Melacini, G. Stoichiometry and Affinity of the Human Serum Albumin-Alzheimer's Abeta Peptide Interactions Biophys. J. 2011, 100, 183-92
68. Milojevic, J.; Raditsis, A.; Melacini, G. Human Serum Albumin Inhibits Abeta Fibrillization through a Monomer-Competitor Mechanism Biophys. J. 2009, 97, 2585-2594
69. Raditsis, A. V.; Milojevic, J.; Melacini, G. Aβ Association Inhibition by Transferrin Biophys. J. 2013, 105, 473-480
70. Abedini, A.; Meng, F. L.; Raleigh, D. P. A Single-Point Mutation Converts the Highly Amyloidogenic Human Islet Amyloid Polypeptide into a Potent Fibrillization Inhibitor J. Am. Chem. Soc. 2007, 129, 11300-11301
71. Buchanan, L. E.; Dunkelberger, E. B.; Tran, H. Q.; Cheng, P. N.; Chiu, C. C.; Cao, P.; Raleigh, D. P.; de Pablo, J. J.; Nowick, J. S.; Zanni, M. T. Mechanism of IAPP Amyloid Fibril Formation Involves an Intermediate with a Transient Beta-Sheet Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 19285-19290
72. Pan, W.; Vekilov, P. G.; Lubchenko, V. Origin of Anomalous Mesoscopic Phases in Protein Solutions J. Phys. Chem. B 2010, 114, 7620-7630
73. Li, Y.; Lubchenko, V.; Vorontsova, M. A.; Filobelo, L.; Vekilov, P. G. Ostwald-Like Ripening of the Anomalous Mesoscopic Clusters in Protein Solutions J. Phys. Chem. B 2012, 116, 10657-10664
74. Lifshitz, I. M.; Slyozov, V. V. The Kinetics of Precipitation from Supersaturated Solid Solutions J. Phys. Chem. Solids 1961, 19, 35-50
75. Linse, B.; Linse, S. Monte Carlo Simulations of Protein Amyloid Formation Reveal Origin of Sigmoidal Aggregation Kinetics Mol. Biosyst. 2011, 7, 2296-2303
76. Soreghan, B.; Kosmoski, J.; Glabe, C. Surfactant Properties of Alzheimer's a Beta Peptides and the Mechanism of Amyloid Aggregation J. Biol. Chem. 1994, 269, 28551-28554
77. Lei, L. Z. Ph.D. Thesis. Mechanism of Early Stage Abeta Amyloid Formation. Case Western Reserve University, 2008.
78. Suzuki, Y.; Brender, J. R.; Hartman, K.; Ramamoorthy, A.; Marsh, E. N. G. Alternative Pathways of Human Islet Amyloid Polypeptide Aggregation Distinguished by F-19 Nuclear Magnetic Resonance-Detected Kinetics of Monomer Consumption Biochemistry 2012, 51, 8154-8162
79. Suzuki, Y.; Brender, J. R.; Soper, M. T.; Krishnamoorthy, J.; Zhou, Y. L.; Ruotolo, B. T.; Kotov, N. A.; Ramamoorthy, A.; Marsh, E. N. G. Resolution of Oligomeric Species During the Aggregation of Aβ(1-40) Using F-19 NMR Biochemistry 2013, 52, 1903-1912
80. Kusumoto, Y.; Lomakin, A.; Teplow, D. B.; Benedek, G. B. Temperature Dependence of Amyloid Beta-Protein Fibrillization Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 12277-12282
81. Marek, P. J.; Patsalo, V.; Green, D. F.; Raleigh, D. P. Ionic Strength Effects on Amyloid Formation by Amylin Are a Complicated Interplay among Debye Screening, Ion Selectivity, and Hofmeister Effects Biochemistry 2012, 51, 8478-8490
82. Yeh, V.; Broering, J. M.; Romanyuk, A.; Chen, B.; Chernoff, Y. O.; Bommarius, A. S. The Hofmeister Effect on Amyloid Formation Using Yeast Prion Protein Protein Sci. 2010, 19, 47-56
83. Mishra, R.; Geyer, M.; Winter, R. Nmr Spectroscopic Investigation of Early Events in IAPP Amyloid Fibril Formation ChemBioChem 2009, 10, 1769-72
84. Mazor, Y.; Gilead, S.; Benhar, I.; Gazit, E. Identification and Characterization of a Novel Molecular-Recognition and Self-Assembly Domain within the Islet Amyloid Polypeptide J. Mol.. Biol. 2002, 322, 1013-1024
85. Shim, S. H.; Gupta, R.; Ling, Y. L.; Strasfeld, D. B.; Raleigh, D. P.; Zanni, M. T. Two-Dimensional IR Spectroscopy and Isotope Labeling Defines the Pathway of Amyloid Formation with Residue-Specific Resolution Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 6614-6619
86. Ladiwala, A. R. A.; Litt, J.; Kane, R. S.; Aucoin, D. S.; Smith, S. O.; Ranjan, S.; Davis, J.; Van Nostrand, W. E.; Tessier, P. M. Conformational Differences between Two Amyloid Beta Oligomers of Similar Size and Dissimilar Toxicity J. Biol. Chem. 2012, 287, 24765-24773
87. Hu, X. Y.; Crick, S. L.; Bu, G. J.; Frieden, C.; Pappu, R. V.; Lee, J. M. Amyloid Seeds Formed by Cellular Uptake, Concentration, and Aggregation of the Amyloid-Beta Peptide Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 20324-20329
88. Kuo, Y. M.; Emmerling, M. R.; Lampert, H. C.; Hempelman, S. R.; Kokjohn, T. A.; Woods, A. S.; Cotter, R. J.; Roher, A. E. High Levels of Circulating Abeta42 Are Sequestered by Plasma Proteins in Alzheimer's Disease Biochem. Biophys. Res. Commun. 1999, 257, 787-791
89. 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
90. 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, e23970
91. Sengupta, P.; Garai, K.; Sahoo, B.; Shi, Y.; Callaway, D. J. E.; Maiti, S. The Amyloid Beta Peptide (a Beta(1-40)) Is Thermodynamically Soluble at Physiological Concentrations Biochemistry 2003, 42, 10506-10513
92. Nag, S.; Sarkar, B.; Bandyopadhyay, A.; Sahoo, B.; Sreenivasan, V. K.; Kombrabail, M.; Muralidharan, C.; Maiti, S. Nature of the Amyloid-Beta Monomer and the Monomer-Oligomer Equilibrium J. Biol. Chem. 2011, 286, 13827-33
93. Friedrich, R. P.; Tepper, K.; Roznicke, R.; Soom, M.; Westermann, M.; Reymann, K.; Kaether, C.; Fandrich, M. Mechanism of Amyloid Plaque Formation Suggests an Intracellular Basis of Aβ Pathogenicity Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 1942-1947
94. Knight, J. D.; Williamson, J. A.; Miranker, A. D. Interaction of Membrane-Bound Islet Amyloid Polypeptide with Soluble and Crystalline Insulin Protein Sci. 2008, 17, 1850-1856
95. Butler, P. C.; Chou, J.; Carter, W. B.; Wang, Y. N.; Bu, B. H.; Chang, D.; Chang, J. K.; Rizza, R. A. Effects of Meal Ingestion on Plasma Amylin Concentration in Niddm and Nondiabetic Humans Diabetes 1990, 39, 752-756
96. Munch, J.; Rucker, E.; Standker, L.; Adermann, K.; Goffinet, C.; Schindler, M.; Wildum, S.; Chinnadurai, R.; Rajan, D.; Specht, A. Semen-Derived Amyloid Fibrils Drastically Enhance HIV Infection Cell 2007, 131, 1059-1071