Dye-binding assays for evaluation of the effects of small molecule inhibitors on amyloid (Aβ) self-assembly

ACS Chemical Neuroscience

Volumn 3, Issue 11, 2012, Pages 807-819

  Jameson, Laramie P ^a   Smith, Nicholas W ^a   Dzyuba, Sergei V ^a  

^a TEXAS CHRISTIAN UNIVERSITY   (United States)

Author keywords

Alzheimers disease; amyloid peptide; dye binding assay; fluorescence; small molecule inhibitor; thioflavin T

Indexed keywords

AMPHOTERICIN B; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; BAICALEIN; BASIC BLUE 41; BETA CYCLODEXTRIN; BOVINE SERUM ALBUMIN; COLLAGEN FIBRIL; CONGO RED; CURCUMIN; DYE; GLYCEROL; MEROZOITE SURFACE PROTEIN 2; PHTHALIMIDE DERIVATIVE; QUERCETIN; RESVERATROL; RIFAMPICIN; TANNIN; TETRACYCLINE; THIOFLAVINE; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ALZHEIMER DISEASE; APOPTOSIS; ATOMIC FORCE MICROSCOPY; BETA SHEET; BINDING ASSAY; BINDING KINETICS; BINDING SITE; BIREFRINGENCE; CELL STRAIN HEK293; CIRCULAR DICHROISM; COMPLEX FORMATION; DYE BINDING ASSAY; ELECTRON MICROSCOPY; ENCAPSULATION; FLUORESCENCE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LABORATORY DIAGNOSIS; LIPID PEROXIDATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR INTERACTION; MOLECULAR PROBE; NEUROTOXICITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; REVIEW; THERMODYNAMICS; TRANSMISSION ELECTRON MICROSCOPY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; COLORING AGENTS; CONGO RED; DRUG DISCOVERY; FALSE POSITIVE REACTIONS; FLUORESCENT DYES; HUMANS; REPRODUCIBILITY OF RESULTS; THIAZOLES;

EID: 84869811189     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn300076x     Document Type: Review

References (126)

1. Galimberti, D. and Scarpini, E. (2011) Alzheimers disease: from pathogenesis to disease-modifying approaches CNS Neurol. Disord.: Drug Targets 10, 163-174
2. Smith, M. A., Drew, K. L., Nunomure, A., Takeda, A., Hirai, K., Zhu, X., Atwood, C. S., Raina, A. K., Rottkamp, C. A., and Sayer, L. M. 2002, Amyloid-β, tau alterations and mitochondrial dysfanctioun in Alzheimer disease: the chickens or the eggs? Neurochem. Int. 40, 527-531
3. Garcia-Ayllon, M.-S., Small, D. H., Avila, J., and Saez-Valero, J. (2011) Revisiting the role of acetylcholinesterase in Alzheimers disease: cross-talk with P-tau and β-amyloid Front. Mol. Neurosci. 4, 1-9
4. Mao, P. and Reddy, H. P. (2011) Aging and amyloid beta-induced oxidative DNA damage and mitochondrial dysfunction in Alzheimers disease: Implications for early interventaion and therapeutics Biochim. Biophys. Acta, Mol. Basis Dis. 1812, 1359-1370
5. Hardy, J. A. and Higgins, G. A. (1992) Alzheimers disease: the amyloid cascade hypothesis Science 256, 184-185
6. Tanzi, R. E. and Bertram, L. (2005) Twenty years of the Alzhemers disease amyloid hypothesis: a genetic perspective Cell 120, 545-555
7. Jakob-Roetne, R. and Jacobsen, H. (2009) Alzhemiers disease: from pathology to therapeutic approach Angew. Chem., Int. Ed. 48, 3030-3059
8. Reitz, C. (2012) Azlheimers disease and the amyloid cascade hypothesis: a critical review Int. J. Alzheimers Dis. 2012, 369808
9. Haass, C. and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from Alzheimers amyloid β-peptide Nat. Rev. Mol. Cell Biol. 8, 101-112
10. Wang, Z., Yang, L., and Zheng, H. (2012) Role of APP and Aβ in synaptic physiology Curr. Alzheimer Res. 9, 217-226
11. Cole, S. L. and Vassar, R. (2008) The role of amyloid precursor proteins processing by BACE1, the β-secretase, in Alzheimer disease pathophysiology J. Biol. Chem. 283, 29621-29625
12. Caughey, B. and Lansbury, P. T. (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders Annu. Rev. Neurosci. 26, 267-298
13. Larson, M. E. and Lesne, S. E. (2012) Soluble Aβ oligomer production and toxicity J. Neurochem. 120 (suppl. 1) 125-139
14. Krafft, G. A. and Klein, W. L. (2010) ADDLs and the signalling web that leads to Alzhemiers disease Neuropharmacology 59, 230-242
15. Selkoe, D. J. (2008) Soluble oligomers of the amyloid β-protein impair synaptic plasticity and behavior Behav. Brain Res. 192, 106-113
16. Saraiva, A. M., Cardoso, I., Pereira, M. C., Coelho, M. A. N., Saraiva, M. J., Moehwald, H., and Brezesinski, G. (2010) Controlling amyloid-β peptide(1-42) oligomerization and toxicity by fluorinated nanoparticles ChemBioChem 11, 1905-1913
17. Cerf, E., Sarroukh, R., Tiamamizu-Kato, S., Breydo, L., Derclaye, S., Dufrene, Y. F., Narayanaswami, V., Goormaghting, E., Ryusschaert, J.-M., and Raussens, V. (2009) Antiparallel β-sheet: a signature structure of the oligomeric amyloid β-peptide Biochem. J. 421, 415-423
18. Sgourakis, N. G., Yan, Y., McCallum, S. A., Wang, C., and Garcia, A. E. (2007) The Alzeimers Aβ40 and 42 adopt distinct confromations in water: a combined MD/NMR study J. Mol. Biol. 368, 1448-1457
19. Liao, M. Q., TRzeng, Y. J., Chang, L. Y. X., Huang, H. B., Lin, T. H., Chyan, C. L., and Chen, Y. C. (2007) The correlation between neurotoxocity, aggregative ability and secondary structure studies by sequence truncated Aβ peptides FEBS Lett. 581, 1161-1165
20. Barrow, C. J. and Zagorski, M. G. (1991) Solution structures of β peptide and its constituent fragments: relation to amyloid deposition Science 253, 179-182
21. Roychaudhuri, R., Yang, M., Hoshi, M. M., and Teplow, D. B. (2009) Amyloid-protein assembly and Alzheimers disease J. Biol. Chem. 284, 4749-4753
22. Mohamed, T. and Rao, P. P. N. (2011) Alzhemiers disease: emerging trends in small molecule therapies Curr. Med. Chem. 18, 4299-4320
23. Masuda, M., Suzuki, N., Taniguchi, S., Oikawa, T., Nonaka, T., Iwatsubo, T., Hisagana, S., Goedert, M., and Hasegawa, M. (2006) Small molecule inhibitors of α-synuclein filament assembly Biochemistry 45, 6085-6094
24. Dolphin, G. T., Ouberai, M., Dumy, P., and Garcia, J. (2007) Designed amyloid β peptide fibril - a tool for high-throughput screening of fibril inhibitors ChemMedChem 2, 1613-1623
25. Bartolini, M., Bertucci, C., Bolognesi, M. L., Cavalli, A., Melchiorre, C., and Andrisano, V. (2007) Insight into the kinetics of amyloid β (1-42) peptide self-aggregation: elucidation of inhibitors mechanism of action ChemBioChem 8, 2152-2161
26. Necula, M., Kayed, R., Milton, S., and Glabe, C. G. (2007) Small molecule inhibitors of aggregation indicate that amyloid β oligomerization and fibrillization pathways are independent and distinct J. Biol. Chem. 282, 10311-10324
27. Hawe, A., Sutter, M., and Jiskoot, W. (2008) Extrinsic fluorescent dyes as tools for protein characterization Pharm. Res. 25, 1487-1499
28. Buell, A. K., Dobson, C. M., Knowles, T. P. J., and Welland, M. E. (2010) Interactions between amyloidophilic dyes and their relevnace to studies of amyloid inhibitors Biophys. J. 99, 3492-3497
29. Nilsson, M. R. (2004) Techniques to study amyloid fibril formation in vitro Methods 34, 151-160
30. Klunk, W. E., Jacob, R. F., and Mason, R. P. (1999) Quantifying amyloid β-peptide (Aβ) aggregation using the Congo red-Aβ (CR-Aβ) spectrophotometric assay Anal. Biochem. 266, 66-76
31. Eisert, R., Felau, L., and Brown, L. R. (2006) Methods for enhancing the accuracy and reproducibility of Congo red and thiolavin T assays Anal. Biochem. 353, 144-146
32. Hudson, S. A., Ecroyd, H., Kee, T. W., and Carver, J. A. (2009) The thioflavin T fluorescence assay for amyloid fibril detection can be biased by the presence of exogenous compounds FEBS J. 276, 5960-5972
33. Klunk, W. E., Pettegrew, J. W., and Abraham, D. J. (1989) Quantitative evaluation of Congo red binding amyloid-like proteins with a beta-pleated sheet conformation J. Histochem. Cytochem. 37, 1273-128
34. Furumoto, S., Okamura, N., Iwata, R., Yanai, K., Arai, H., and Kudo, Y. (2007) Recent advances in the development of amyloid imaging agents Curr. Top. Med. Chem. (Sharjah, United Arab Emirates) 7, 1773-1789
35. Frid, P., Anisimov, S. V., and Popovic, N. (2007) Congo red and protein aggregation in neurodegenerative diseases Brain Res. Rev. 53, 135-160
36. Howie, A. J. and Brewer, D. B. (2009) Optical properties of amyloid stained by Congo red: History and mechanisms Micron 40, 285-301
37. Wang, C.-C., Huang, H-b., Tsay, H.-J., Shiao, M.-S., Wu, W-J. W., Chen, Y.-C., and Lin, T.-H. (2012) Characterization of Aβ aggregation mechanism probed by congo red J. Biomol. Struct. Dyn. 30, 160-169
38. Cavillon, F., Elhaddaoui, A., Alix, A. J. P., Turrell, S., and Dachez, M. (1997) Identification of the importance of the secondary structure of Alzheimers disease amyloid J. Mol. Struct. 408-409, 185-189
39. Li, L., Darden, T. A., Bartolotti, L., Kominos, D., and Pedersen, L. G. (1999) An atomic model for the pleated β-sheet structure, of Aβ amyloid protofilaments Biophys. J. 76, 2871-2878
40. Lendel, C., Bolognesi, B., Wahlstrom, A., Dobson, C., and Graslund, A. (2010) Detergent-like interaction of Congo red with the amyloid β peptide Biochemistry 49, 1358-1360
41. Feng, B. Y., Toyama, B. H., Wille, H., Colby, D. W., Collins, S. R., May, B. C. H., Pruisner, S. B., Weissman, J., and Scoichet, B. K. (2008) Small-molecule aggregates inhibit amyloid polymerization Nat. Chem. Biol. 4, 197-199
42. Podlisny, M. B., Walsh, D. M., Amarante, P., Ostaszewski, B. L., Stimson, E. R., Maggio, J. E., Teplow, D. B., and Selkoe, D. J. (1998) Oligomerization of endogenous and synthetic amyloid β-protein at nanomolar levels in cell culture and stabilization of monomer by Congo red Biochemistry 37, 3602-3611
43. Hong, H.-S., Rana, S., Barrigan, L., Shi, A., Zhang, Y., Zhou, F., Jin, L.-W., and Hua, D. H. (2009) Inbibition of Alzheimers amyloid toxicity with a tricyclic pyrone molecule in vitro and in vivo J. Neurochem. 108, 1097-1108
44. Yang, F., Lim, G. P., Begum, A. N., Ubeda, O. J., Simmons, M. R., Ambegaokar, S. S., Chen, P., Kayed, R., Glabe, C. G., Frautschy, S. A., and Cole, G. M. (2005) Curcumin inhibits formation of amyloid β oligomers and fibrils, binds plaques, and reduces amyloid in vivo J. Biol. Chem. 280, 5892-5901
45. Nakagami, Y., Nishimura, S., Murasugi, T., Kaneko, I., Meguro, M., Marumoto, S. K., H., Koyama, K., and Oda, T. (2002) A novel β-sheet breaker, RS-0406, reverses amyloid β-induced cytotoxicity and impairment of long-term potentiation in vitro Br. J. Pharmacol. 137, 676-682
46. Klunk, W. E., Debnath, M. L., and Pettegrew, J. W. (1994) Development of small molecule probes for the beta-amyloid protein of Alzhemiers disease Neurobiol. Aging 15, 691-698
47. Patrovi-Nia, R., Beheshti, S., Qin, Z., Mandal, H. S., Long, Y.-T., Girault, H. H., and Kraatz, H.-H. (2012) Study of amyloid β-peptide (Aβ12-28-Cys) interactions with Congo Red and β-sheet breaker peptides using electrochemical impedance spectroscopy Langmuir 28, 6377-6385
48. Kim, Y.-S., Randolph, T. W., Manning, M. C., Stevens, F. J., and Carpenter, J. F. (2003) Congo red populates partially unfolded states of an amyloidogenic protein to enhance aggregation and amyloid fibril formation J. Biol. Chem. 278, 10842-10850
49. Biancalana, M. and Koide, S. (2010) Molecular mechanism of thioflavin-T binding to amyloid fibrils Biochim. Biophys. Acta, Proteins Proteomics 1804, 1405-1412
50. Rodriguez-Rodriguez, C., Rimola, A., Rodriguez-Santiago, L., Ugliengo, P., Alvarez-Larena, A., Gutierrez-de-Teran, H., Sodupe, M., and Gonzalez-Duarte, P. (2010) Crystal structure of thioflavin-T and binding to amyloid fibrils: insights at the molecular level Chem. Commun. 46, 1156-1158
51. Mao, X., Cuo, Y., Wang, C., Zhang, M., Ma, X., Liu, L., Niu, L., Zeng, Q., Yang, Y., and Wang, C. (2011) Binding modes of thioflavin T molecules to prion peptide assemblies identified by using scanning tunneling microscopy ACS Chem. Neurosci. 2, 281-287
52. Middleton, C. T., Marek, P., Cao, P., Chiu, C-c., Singh, S., Woys, A. M., de Pablo, J. J., Raleigh, D. P., and Zanni, M. T. (2012) Two-dimensional infrared spectroscopy reveals the complex behaviour of an amyloid fibril inhibitor Nat. Chem. 4, 355-360
53. Khurana, R., Coleman, C., Ionescu-Zanetti, C., Carter, S. A., Krishna, V., Grover, R. K., Roy, R., and Singh, S. (2005) Mechanism of thioflavin T binding to amyloid fibrils J. Struct. Biol. 151, 229-238
54. Cisek, K. and Kuret, J. (2012) QSAR studies for prediction of cross-β sheet aggregate binding affinity and selectivity Bioorg. Med. Chem. 20, 1434-1441
55. Ono, M., Hayashi, S., Kimura, H., Kawashima, H., Nakayama, M., and Saji, H. (2009) Push-pull benzothiazole derivatives as probes for detecting β-amyloid plaques in Alzheimers brains Bioorg. Med. Chem. 17, 7002-7007
56. Yona, R. L., Mazerez, S., Faller, P., and Gras, E. (2008) Thioflavin derivatives as markers for amyloid-β fibrils: insights into structural features important for high-affinity binding ChemMedChem 3, 63-66
57. Inbar, P., Li, C. Q., Takayama, S. A., Bautista, M. R., and Yang, J. (2006) Oligo(ethylene glycol) derivaitives of thioflavin T as inhibitors of protein-amyloid interactions ChemBioChem 7, 1563-1566
58. Bartolini, M., Naldi, M., Fiori, J., Valle, F., Biscarini, F., Nicolau, D. V., and Andrisano, V. (2011) Kinetic characterization of amyloid-beta 1-42 aggregation with a multimethodological approach Anal. Biochem. 414, 215-225
59. Amaro, M., Birch, D. J. S., and Rolinski, O. J. (2011) Beta-amyloid oligomerization monitored by intrinsic tyrosin fluorescence Phys. Chem. Chem. Phys. 13, 6434-6441
60. Benseny-Cases, N., Cocera, M., and Cladera, J. (2007) Conversion of non-fibrillar β-sheet oligomers into amyloid fibrils in Alzhemiers disease amyloid peptide aggregation Biochim. Biophys. Res. Commun. 361, 916-921
61. LeVine, H., III. (1993) Thioflavin T interaction with synthetic Alzhemers disease β-amyloid peptides: Detection of amyloid aggregation in solution Protein Sci. 2, 404-410
62. Maezawa, I., Hong, H.-S., Liu, R., Wu, C.-Y., Cheng, R. H., Kung, M.-P., Kung, H. F., Lam, K. S., Oddo, S., and LaFerla, F. M. 2008, Congo red and thioflavin-T analogues detect Aβ oligomers J. Neurochem. 104, 457-468
63. Ryan, D. A., Narrow, W. C., Federoff, H. J., and Bowers, W. J. (2010) An improved method for generating consistent soluble amyloid-beta oligomers preparations for in vitro neurotoxicity studies J. Neurosci. Methods 190, 171-179
64. Walsh, D. M., Hartley, D. M., Kusumoto, Y., Fezoui, Y., Condron, M. M., Lomakin, A., Benedek, G. B., Selkoe, D. J., and Teplow (1999) Amyloid beta-fibrillogenesis. Structure and biological activity of protofibrillar intermediates J. Biol. Chem. 274, 25945-25952
65. Reinke, A. A. and Gestwicki, J. E. (2011) Insight into amyloid structure using chemical probes Chem. Biol. Drug Des. 77, 399-411
66. Gorbenko, G., Trusova, V., Kirilova, E., Kirilov, G., Kalnina, I., Vasilev, A., Kaloyanova, S., and Deligeorgiev, T. (2010) New fluorescent probes for detection and characterization of amyloid fibrils Chem. Phys. Lett. 495, 275-279
67. Ahn, J. S., Lee, J.-H., Kim, J.-H., and Paik, S. R. (2007) Novel method for quantitative determination of amyloid fibrils of α-synuclein and amyloid β/A4 protein by using resveratrol Anal. Biochem. 367, 259-265
68. Ono, K., Yoshilke, Y., Takashima, A., Hasegawa, K., Naiki, H., and Yamada, M. (2003) Potent anti-amyloidogenic and fibril-destabilizing effects of polyphenols in vitro: implications for the prevention and therapeutics of Alzhemiers disease J. Neurochem. 87, 172-181
69. Ahmed, M., Davis, J., Aucoin, D., Sato, T., Ahuja, S., Aimoto, S., Elliott, J. I., Van Nostrand, W. E., and Smith, S. O. (2010) Structural conversion of neurotoxic amyloid-β1-42 oligomers to fibrils Nat. Struct. Mol. Bio. 17, 561-567
70. Hamaguchi, T., Ono, K., and Yamada, M. (2010) Curcumin and Alzheimers disease CNS Neurosci. Ther. 16, 285-297
71. Akaishi, T., Morimoto, T., Shibao, M., Watanabe, S., Sakai-Kato, K., Utsunomiya-Tate, N., and Abe, K. (2008) Structural requirements for the flavanoid fisetin in inhibiting fibril formation of amyloid β protein Neurosci. Lett. 444, 280-285
72. Noormagi, A., Primar, K., Tougu, V., and Palumaa, P. (2012) Interference of low-molecular substances with the thioflavin-T fluorescence assay of amyloid fibrils J. Pept. Sci. 18, 59-64
73. Zovo, K., Helk, E., Karafin, A., Tougu, V., and Palumaa, P. (2010) Label-free high-throuput screening assay for inhibitors of Alzheimers amyloid-β peptide aggregation based on MALDI MS Anal. Chem. 82, 8558-8565
74. Liu, K.-N., Wang, H.-Y., Chen, C.-Y., and Wang, S. S.-S. (2010) L-Argenine reduces thioflavin T fluorescence but not fibrillization of bovine serum albumin Amino Acids 39, 821-829
75. Cole, G. M., Yang, F., Lim, G. P., Cummings, J. L., Masterman, D. L., and Frautschy, S. A. (2003) A rationale for curcuminoids for the prevention or treatment of Alzhemiers disease Curr. Med. Chem.: Immunol., Endocr. Metab. Agents 3, 15-25
76. Mansuco, C., Siciliano, R., and Barone, E. (2011) Curcumin and Alzheimer disease: this marriage is not to be performed J. Biol. Chem. 286, le3
77. Ono, K., Hasegawa, K., Naiki, H., and Yamada, M. (2004) Curcumin has potent anti-amyloidogenic effects for Alzhemiers β-amyloid fibrils in vitro J. Neurosci. Res. 75, 742-750
78. Reinke, A. A. and Gestwicki, J. E. (2007) Structure-activity relationships of amyloid beta-aggregation inhibitors based on curcumin: influence of linker length and flexibility Chem. Biol. Drug Des. 70, 206-215
79. Kim, H., Park, B.-S., Lee, K.-G., Choi, C. Y., Jang, S. S., Kim, Y. H., and Lee, S. E. (2005) Effects of naturally occuring compounds on fibril formation and oxidative stress of β-amyloid J. Agric. Food Chem. 53, 8537-8541
80. Jagota, S. and Rajada, J. (2012) Effect of phenolic compounds against Aβ aggregation and Aβ-induced toxicity in transgenic C. elegans Neurochem. Res. 37, 40-48
81. Shi, C., Zhao, L., Zhu, B., Li, Q., Yew, D. T., Yao, Z., and Xu, J. (2009) Protective effects of Ginkgo biloba (EGb761) and its constituents quercetin and ginkgolide B against β-amyloid peptide-induced toxicity in SH-SY5Y cell Chem.-Biol. Interact. 181, 115-123
82. Jiménez-Aliaga, K., Bermejo-Bescós, P., Benedí, J., and Martín-Aragón, S. (2011) Quercetin and rutin exhibit antiamyloidogenic and fibril-disaggregating effect in vitro and potent antioxidant activity in APPswe cells Life Sci. 89, 939-945
83. Ohta, K., Mizuno, A., Li, S., Itoh, M., Ueda, M., Ohta, E., Hida, Y., Wang, M.-x., Furoi, M., and Tsuzuki, Y 2011, Endoplasmic reticulum stress enhances γ-secretase activity Biochem. Biophys. Res. Commun. 416, 362-366
84. Ansari, M. A., Abdul, H. M., Joshi, G., Wycliffe, O., and Butterfiled, D. A. (2009) Protective effect of quercetin in primary neurons against Aβ(1-42): relevance to Alzheimers disease J. Nutr. Biochem. 20, 269-275
85. Hirohata, M., Hagesawa, K., Tsutsumi-Yasuhara, Ohhashi, Y., Ookoshi, T., Ono, K., Yamada, M., and Naiki, H. (2007) The anti-amyloidogenic effect is exerted against Alzhemiers β-amyloid fibrils in vitro by preferential and reversible binding of flavonoids to the amyloid fibril structure Biochemistry 46, 1888-1899
86. Ladiwala, A. R. A., More-Pale, M., Lin, J. C., Shyam, S., Fishman, Z. S., Dordick, J. S., and Tessier, P. M. (2011) Polyphenolic glycosides and aglycones utilize opposing pathways to selectively remodel and inactivate toxic oligomers of amyloid β ChemBioChem 12, 1749-1758
87. 1-42-mediated synapse damage in vitro Mol. Neurodegener. 3, 1
88. Marambaud, P., Zhao, H., and Davies, P. (2005) Resveratrol promotes clearance of Alzhemiers desease amyloid-β peptides J. Biol. Chem. 280, 37377-37382
89. Carver, J. A., Duggan, P. J., Ecroyd, H. L., Liu, Y., Meyer, A. G., and Tranberg, C. E. (2010) Carboxymethylated-κ-casein: a convenient tool for the identification of the polyphenolic inhibitors of amyloid fibril formation Bioorg. Med. Chem. 18, 222-228
90. Hartsel, S. C. and Weiland, T. R. (2003) Amphotericin B binds amyloid fibrils and delays their formation: a therapeutic mechanism? Biochemistry 42, 6228-6233
91. Taniguchi, S., Susuki, N., Masuda, M., Hisanaga, S., Iwatsubo, T., Goedert, M., and Hasegawa, M. (2005) Inhibition of heparin-induced tau filament formation by phenothiazines, polyphenols, and porphyrins J. Biol. Chem. 280, 7614-7623
92. Smith, N. W., Annunziata, O., and Dzyuba, S. V. (2009) Amphotericin B interactions with soluble oligomers of amyloid Aβ1-42 peptide Bioorg. Med. Chem. 17, 2366-2370
93. Camilleri, P., Haskins, N. J., and Howlett, D. R. (1994) β-Cyclodextrin interacts with the Alzhemer amyloid β-A4 peptide FEBS Lett. 341, 256-258
94. Waite, J., Cole, G. M., Frautschy, S. A., Connor, D. J., and Thakl, L. J. (1992) Solvent effects on beta protein toxicity in vivo Neurobiol. Aging 13, 595-599
95. Yu, J., Bakhos, L., Chang, L., Holterman, M. J., Klein, W. L., and Venton, D. L. (2002) Per-6-substituted β-cyclodextrin libraries inhibit formation of β-amyloid-peptide (Aβ)-derived, soluble oligomers J. Mol. Neurosci. 19, 51-55
96. Wang, Z., Chang, L., Klein, W. L., Thatcher, G. R. J., and Venton, D. L. (2004) Per-6-substituted-per-6-deoxy-β-cyclodextrins inhibit the formation of β-amyloid peptide derived soluble oligomers J. Med. Chem. 47, 3329-3333
97. Wang, M. S., Boddapati, S., and Sierks, M. R. (2009) Cyclodextrins promote protein aggregation posing risks for therapeutic applications Biophys. Biochem. Res. Commun. 386, 526-531
98. Singh, P. K., Kumbhakar, M., Pal, H., and Nath, S. (2011) Confined ultrafast torsional dynamics of thiolfavin-T in a nanocavity Phys. Chem. Chem. Phys. 13, 8008-8014
99. Qin, X., Abe, H., and Nakanishi, H. (2002) NMR and CD studies on the interaction of Alzheimer β-amyloid (12-28) with β-cyclodextrin Biochem. Biophys. Res. Commun. 297, 1011-1015
100. Danielsson, J., Jarvet, J., Damberg, P., and Graslund, A. (2004) Two-site binding of β-cyclodextrin to the Alzheimer Aβ(1-40) peptide measured with combined PFG-NMR diffusion and induced chemical shifts Biochemistry 43, 6261-6269
101. Wang, H.-Y., Ying, Y.-L., Li, Y., Kraatz, H.-B., and Long, Y. T. (2010) Nanopore analysis of β-amyloid peptide aggregation transition induced by small molecules Anal. Chem. 83, 1746-1752
102. Forloni, G., Colombo, L., Girola, L., Tagliavini, F., and Salmona, M. (2001) Anti-amyloidogenic activity of tetracyclines: studies in vitro FEBS Lett. 487, 404-407
103. Ono, K., Hasegawa, K., Naiki, H., and Yamada, M. (2004) Anti-amyloidogenic activity of tannic acidand its activity to destabilize Alzhemiers β-amyloid fibrils in vitro Biochim. Biophys. Acta, Mol. Basis Dis. 1690, 193-202
104. Airoldi, C., Colombo, L., Manzoni, C., Sironi, E., Natalello, A., Doglia, S. M., Forloni, G., Tagliavini, F., Del Favero, E., Cantu, L., Nicotra, F., and Salmona, M. (2011) Tetracycline prevents Aβ oligomer toxicity through an atypical supramolecular interaction Org. Biomol. Chem. 9, 463-472
105. Han, Y.-S., Zheng, W.-H., Bastianetto, S., Chabot, J.-G., and Quirion, R. (2004) Neuroprotective effects of resveratrol against β-amyloid-induced neurotoxicity in rat hippocampal neurons: involvement of protein kinase C Br. J. Pharmacol. 141, 997-1005
106. Vingtdeaux, V., Giliberto, L., Zhao, H., Chandakkar, P., Wu, Q., Simon, J. E., Janle, E. M., Lobo, J., Ferruzzi, M. G., Davies, P., and Marambaud, P. (2010) AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-β peptide mechanism J. Biol. Chem. 285, 9100-9113
107. Huang, T.-C., Lu, K.-T., Wo, Y.-Y. P., Wu, Y.-J., and Yang, Y.-L. (2011) Resveratrol protect rats from Aβ-induced neurotoxicity by the reduction of iNOS expression and lipid peroxidation PLoS One 6, e29102
108. Ladiwala, A. R., Lin, J. C., Bale, S. S., Marcelin-Cruz, A. M., Bhattacharya, M., Dordick, J. S., and Tessler, P. M. (2010) Resveratrol selectively remodels soluble oligomers and fibrils of amyloid Aβ into off-pathway conformers J. Biol. Chem. 285, 24228-24237
109. Feng, Y., Wang, X-p., Yang, S-g., Wang, Y-j., Zhang, X., Du, X-t., Sun, X-x., Zhao, M., Huang, L., and Liu, R-t. (2009) Resveratrol inhibits beta-amyloid oligomeric cytotoxicity but does not prevent oligomer formation NeuroToxicology 30, 986-995
110. Schmuck, C., Frey, P., and Heil, M. (2005) Inhibition of fibril formation of Aβ by guanidiniocarbonyl pyrrole receptors ChemBioChem 6, 628-631
111. Ryu, J., Kanapathipillai, M., Lentzen, G., and Park, C. B. (2008) Inhibition of β-amyloid peptide aggregation and neurotoxicity by α-D-mannosylglycerate, a natural extremolyte Peptides 29, 578-584
112. Meng, F., Marek, P., Potter, K. J., Verchere, C. B., and Raleigh, D. P. (2008) Rifampicin does not prevent amyloid fibril formation by human islet amyloid polyptide but does inhibit fibril thioflavin-T interactions: implications for mechanistic studies of β-cell death Biochemistry 47, 6016-6024
113. Chandrashekaran, I. R., Adda, C. G., MacRaild, C. A., Anders, R. F., and Norton, R. S. (2010) Inhibition by flavanoids of amyloid-like fibril formation by Plasmodium falciparum merozoite surface protein 2 Biochemistry 49, 5899-5908
114. Kroes-Nijboer, A., Lubbersen, Y. S., Venema, P., and van der Linden, E. (2009) Thioflavin T fluorescence assay for β-lactoglobulin fibrils hindered by DAPH J. Struct. Biol. 165, 140-145
115. Carrotta, R., Canale, C., Diasporo, A., Trapani, A., San Biagio, P. L., and Bulone, D. (2012) Inhibiting effect of αs1-casein on Aβ1-40 fibrillogensis Biochim. Biophys. Acta, Gen. Subj. 1820, 124-132
116. Goldsbury, C., Baxa, U., Simon, M. N., Steven, A. C., Engel, A., Wall, J. S., Aebi, U., and Mueller, S. A. (2011) Amyloid structure and assembly: insights from scanning transmission electron microscopy J. Struct. Biol. 173, 1-13
117. 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 Nat. Biotechnol. 5, 423-428
118. Buell, A. K., Esbjoerner, E. K., Riss, P. J., White, D. A., Aibirhio, F. I., Toth, G., Welland, M. E., Dobson, C. M., and Knowles, T. P. J. (2011) Probing small molecule binding to amyloid fibrils Phys. Chem. Chem. Phys. 13, 20044-20052
119. Ono, K., Li, L., Takamura, Y., Yoshiike, Y., Zhu, L., Han, F., Mao, X., Ikeda, T., Takasaki, J.-i., Nishijo, H., Takashima, A., Teplow, D. B., Zagorski, M. G., and Yamada, M. (2012) Phenolic compounds prevent amyloid β-protein oligomerization and synaptic dysfunction by site-specific binding J. Biol. Chem. 287, 14631-14643
120. Tycko, R. (2011) Solid-state NMR studies of amyloid fibril structure Annu. Rev. Phys. Chem. 62, 279-299
121. Wang, L., Middleton, C. T., Singh, S., Reddy, A. S., Woys, A. M., Strasfeld, D. B., Marek, P., Raleigh, D. P., de Pablo, J. J., Zanni, M. T., and Skinner, J. L. (2011) 2DIR spectroscopy of human amylid fibrils reflects stable β-sheet structure J. Am. Chem. Soc. 133, 16062-16071
122. Smith, N. W., Alonso, A., Brown, C. M., and Dzyuba, S. V. (2010) Triazole-containing BODIPY dyes as novel fluorescent probes for soluble oligomers of amyloid Aβ-142 peptide Biochem. Biophys. Res. Commun. 391, 1455-1458
123. Ono, M., Ishikawa, M., Kimura, H., Hayashi, S., Matsumura, K., Watanabe, H., Shimizu, Y., Cheng, Y., Cui, M., Kawashima, H., and Saji, H. (2010) Development of dual functional SPECT/fluorescent probes for imaging cerebral β-amyloid plaques Bioorg. Med. Chem. Lett. 20, 3885-3888
124. Ono, M., Watanabe, H., Kimura, H., and Saji, H. (2012) BODIPY-based molecular probe for imaging of cerebral β-amyloid plaques ACS Chem. Neurosci. 3, 319-324
125. Kitts, C. C., Beke-Somfai, T., and Norden, B. (2011) Michlers hydrol blue: a sensitive probe for amyloid fibril detection Biochemistry 50, 3451-3461
126. Reinke, A. A., She, H. Y., and Gestwicki, J. E. (2009) A chemical screening approach reveals that indole fluorescence is quenched by pre-fibrillar but not fibrillar amyloid-β Bioorg. Med. Chem. Lett. 19, 4952-4957