Validation and characterization of a novel peptide that binds monomeric and aggregated β-amyloid and inhibits the formation of neurotoxic oligomers

Journal of Biological Chemistry

Volumn 291, Issue 2, 2016, Pages 547-559

  Barr, Renae K ^a,b   Verdile, Giuseppe ^c,d,e   Wijaya, Linda K ^a   Morici, Michael ^a   Taddei, Kevin ^b,d   Gupta, Veer B ^a,b,d   Pedrini, Steve ^a,b   Jin, Liang ^f   Nicolazzo, Joseph A ^f   Knock, Erin ^g   Fraser, Paul E ^g   Martins, Ralph N ^a,b,e  

^a EDITH COWAN UNIVERSITY   (Australia)

^b Alzhyme Pty Ltd   (Australia)

^c CURTIN UNIVERSITY   (Australia)

^d Hollywood Medical Centre   (Australia)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^f MONASH UNIVERSITY   (Australia)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; DIAGNOSIS; GLYCOPROTEINS; MAMMALS; NEURODEGENERATIVE DISEASES; OLIGOMERS; PHAGE DISPLAY; PLASMONS; SURFACE PLASMON RESONANCE;

ALZHEIMER DISEASE; CO-IMMUNOPRECIPITATIONS; EFFECTIVE THERAPY; INSOLUBLE AGGREGATES; PHAGE DISPLAY SCREENING; PROTEOLYTIC RESISTANCE; THERAPEUTIC POTENTIALS; THERAPEUTIC STRATEGY;

PEPTIDES;

3H ARGINYLLYSYLLEUCYLMETHIONYLGLUTAMINYLPROPYLTHREONYLARGINYLASPARAGINYLARGINYLARGINYLASPARAGINYLPROPYLASPARAGINYLTHREONINE AMIDE; AMYLOID BETA PROTEIN[1-42]; ARGINYLASPARAGINYLPROPYLLYSYLMETHIONYLGLUTAMINYLARGINYLTHREONYLLEUCINE AMIDE; ARGINYLLYSYLLEUCYLMETHIONYLGLUTAMINYLPROPYLTHREONYLARGINYLASPARAGINE AMIDE; ARGINYLLYSYLLEUCYLMETHIONYLGLUTAMINYLPROPYLTHREONYLARGINYLASPARAGINYLARGINYLARGINYLASPARAGINYLPROPYLASPARAGINYLTHREONINE AMIDE; ASPARAGINYLARGINYLTHREONYLPROPYLGLUTAMINYLMETHIONYLLEUCYLLYSYLARGININE AMIDE; CENTRAL NERVOUS SYSTEM AGENTS; LEUCYLTHREONYLARGINYLGLUTAMINYLMETHIONYLLYSYLPROPYLASPARAGINYLARGININE AMIDE; MONOMER; OLIGOMER; THREONYLASPARAGINYLPROPYLASPARAGINYLARGINYLARGINYLASPARAGINYLARGINYLTHREONYLPROPYLGLUTAMINYLMETHIONYLLEUCYLLYSYLARGININE AMIDE; THREONYLLEUCYLGLYCYLSERYLGLYCYLPROPYLARGINYLTHREONYLTHREONINE AMIDE; UNCLASSIFIED DRUG; AMYLOID; NEUROTOXIN; PEPTIDE; PROTEIN AGGREGATE; TRITIUM;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIAGNOSTIC IMAGING; DRUG ACTIVITY; DRUG PENETRATION; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG TARGETING; EX VIVO STUDY; HUMAN; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR WEIGHT; MOUSE; NEUROTOXICITY; NONHUMAN; OLIGOMERIZATION; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN ISOLATION; PROTEIN STABILITY; PROTEIN TARGETING; SURFACE PLASMON RESONANCE; VALIDATION STUDY; ANIMAL; BRAIN; DISEASE MODEL; DRUG EFFECTS; IMMUNOHISTOCHEMISTRY; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; PROTEIN MULTIMERIZATION; REPRODUCIBILITY; SOLUBILITY; TRANSGENIC MOUSE;

ADMINISTRATION, INTRAVENOUS; ALZHEIMER DISEASE; AMYLOID; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MICE, TRANSGENIC; NEUROTOXINS; PEPTIDES; PROTEIN AGGREGATES; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; REPRODUCIBILITY OF RESULTS; SOLUBILITY; SURFACE PLASMON RESONANCE; TRITIUM;

EID: 84954107115     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.679993     Document Type: Article

References (64)

1. Taddei, K., Laws, S. M., Verdile, G., Munns, S., D'Costa, K., Harvey, A. R., Martins, I. J., Hill, F., Levy, E., Shaw, J. E., and Martins, R. N. (2010) Novel phage peptides attenuate β amyloid-42 catalysed hydrogen peroxide production and associated neurotoxicity. Neurobiol. Aging 31, 203-214
2. Evans, D. A., Funkenstein, H. H., Albert, M. S., Scherr, P. A., Cook, N. R., Chown, M. J., Hebert, L. E., Hennekens, C. H., and Taylor, J. O. (1989) Prevalence of Alzheimer's disease in a community population of older persons: higher than previously reported. JAMA 262, 2551-2556
3. Burdick, D., Soreghan, B., Kwon, M., Kosmoski, J., Knauer, M., Henschen, A., Yates, J., Cotman, C., and Glabe, C. (1992) Assembly and aggregation properties of synthetic Alzheimer's A4/β amyloid peptide analogs. J. Biol. Chem. 267, 546-554
4. Jarrett, J. T., Berger, E. P., and Lansbury, P. T., Jr. (1993) The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32, 4693-4697
5. Ono, K., and Yamada, M. (2011) Low-n oligomers as therapeutic targets of Alzheimer's disease. J. Neurochem. 117, 19-28
6. 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., Wals, P., Zhang, C., Finch, C. E., Krafft, G. A., and Klein, W. L. (1998) Diffusible, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453
7. Nimmrich, V., Grimm, C., Draguhn, A., Barghorn, S., Lehmann, A., Schoemaker, H., Hillen, H., Gross, G., Ebert, U., and Bruehl, C. (2008) Amyloid β oligomers (Aβ(1-42) globulomer) suppress spontaneous synaptic activity by inhibition of P/Q-type calcium currents. J. Neurosci. 28, 788-797
8. Walsh, D. M., Hartley, D. M., Kusumoto, Y., Fezoui, Y., Condron, M. M., Lomakin, A., Benedek, G. B., Selkoe, D. J., and Teplow, D. B. (1999) Amyloid α-protein fibrillogenesis: structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 274, 25945-25952
9. Ono, K., Naiki, H., and Yamada, M. (2006) The development of preventives and therapeutics for Alzheimer's disease that inhibit the formation of β-amyloid fibrils (fAβ), as well as destabilize preformed fAβ. Curr. Pharm. Des. 12, 4357-4375
10. Näslund, J., Haroutunian, V., Mohs, R., Davis, K. L., Davies, P., Greengard, P., and Buxbaum, J. D. (2000) Correlation between elevated levels of amyloid β-peptide in the brain and cognitive decline. JAMA 283, 1571-1577
11. Gong, Y., Chang, L., Viola, K. L., Lacor, P. N., Lambert, M. P., Finch, C. E., Krafft, G. A., and Klein, W. L. (2003) Alzheimer's disease-affected brain: presence of oligomeric Aβ ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl. Acad. Sci. U.S.A. 100, 10417-10422
12. Cleary, J. P., Walsh, D. M., Hofmeister, J. J., Shankar, G. M., Kuskowski, M. A., Selkoe, D. J., and Ashe, K. H. (2005) Natural oligomers of the amyloid-β protein specifically disrupt cognitive function. Nat. Neurosci. 8, 79-84
13. Shankar, G. M., Bloodgood, B. L., Townsend, M., Walsh, D. M., Selkoe, D. J., and Sabatini, B. L. (2007) Natural oligomers of the Alzheimer amyloid-β protein induce reversible synapse loss by modulating an NMDAtype glutamate receptor-dependent signaling pathway. J. Neurosci. 27, 2866-2875
14. Hung, L. W., Ciccotosto, G. D., Giannakis, E., Tew, D. J., Perez, K., Masters, C. L., Cappai, R., Wade, J. D., and Barnham, K. J. (2008) Amyloid-β peptide (Aβ) neurotoxicity is modulated by the rate of peptide aggregation: Aβ dimers and trimers correlate with neurotoxicity. J. Neurosci. 28, 11950-11958
15. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., Regan, C. M., Walsh, D. M., Sabatini, B. L., and Selkoe, D. J. (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842
16. Westerman, M. A., Cooper-Blacketer, D., Mariash, A., Kotilinek, L., Kawarabayashi, T., Younkin, L. H., Carlson, G. A., Younkin, S. G., and Ashe, K. H. (2002) The relationship between Aβ and memory in the Tg2576 mouse model of Alzheimer's disease. J. Neurosci. 22, 1858-1867
17. Billings, L. M., Oddo, S., Green, K. N., McGaugh, J. L., and LaFerla, F. M. (2005) Intraneuronal Aβ causes the onset of early Alzheimer's diseaserelated cognitive deficits in transgenic mice. Neuron 45, 675-688
18. Oddo, S., Caccamo, A., Kitazawa, M., Tseng, B. P., and LaFerla, F. M. (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol. Aging 24, 1063-1070
19. Ma, Q. L., Yang, F., Rosario, E. R., Ubeda, O. J., Beech, W., Gant, D. J., Chen, P. P., Hudspeth, B., Chen, C., Zhao, Y., Vinters, H. V., Frautschy, S. A., and Cole, G. M. (2009) β-Amyloid oligomers induce phosphorylation of Tau and inactivation of insulin receptor substrate via c-Jun N-terminal kinase signaling: suppression by omega-3 fatty acids and curcumin. J. Neurosci. 29, 9078-9089
20. Tomiyama, T., Matsuyama, S., Iso, H., Umeda, T., Takuma, H., Ohnishi, K., Ishibashi, K., Teraoka, R., Sakama, N., Yamashita, T., Nishitsuji, K., Ito, K., Shimada, H., Lambert, M. P., Klein, W. L., and Mori, H. (2010)Amouse model of amyloid β oligomers: their contribution to synaptic alteration, abnormal Tau phosphorylation, glial activation, and neuronal loss in vivo. J. Neurosci. 30, 4845-4856
21. Benilova, I., Karran, E., and De Strooper, B. (2012) The toxic Aβ oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 15, 349-357
22. Stine, W. B., Jungbauer, L., Yu, C., and LaDu, M. J. (2011) Preparing synthetic Aβ in different aggregation states. Methods Mol. Biol. 670, 13-32
23. Cerf, E., Gustot, A., Goormaghtigh, E., Ruysschaert, J. M., and Raussens, V. (2011) High ability of apolipoprotein E4 to stabilize amyloid-β peptide oligomers, the pathological entities responsible for Alzheimer's disease. FASEB J. 25, 1585-1595
24. Binley, J. M., Lybarger, E. A., Crooks, E. T., Seaman, M. S., Gray, E., Davis, K. L., Decker, J. M., Wycuff, D., Harris, L., Hawkins, N., Wood, B., Nathe, C., Richman, D., Tomaras, G. D., Bibollet-Ruche, F., Robinson, J. E., Morris, L., Shaw, G. M., Montefiori, D. C., and Mascola, J. R. (2008) Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82, 11651-11668
25. Miles, L. A., Wun, K. S., Crespi, G. A., Fodero-Tavoletti, M. T., Galatis, D., Bagley, C. J., Beyreuther, K., Masters, C. L., Cappai, R., McKinstry, W. J., Barnham, K. J., and Parker, M. W. (2008) Amyloid-β-anti-amyloid-β complex structure reveals an extended conformation in the immunodominant B-cell epitope. J. Mol. Biol. 377, 181-192
26. Taylor, M., Moore, S., Mayes, J., Parkin, E., Beeg, M., Canovi, M., Gobbi, M., Mann, D. M., and Allsop, D. (2010) Development of a proteolytically stable retro-inverso peptide inhibitor of β-amyloid oligomerization as a potential novel treatment for Alzheimer's disease. Biochemistry 49, 3261-3272
27. Jungbauer, L. M., Yu, C., Laxton, K. J., and LaDu, M. J. (2009) Preparation of fluorescently-labeled amyloid-β peptide assemblies: the effect of fluorophore conjugation on structure and function. J. Mol. Recognit. 22, 403-413
28. Oakley, H., Cole, S. L., Logan, S., Maus, E., Shao, P., Craft, J., Guillozet-Bongaarts, A., Ohno, M., Disterhoft, J., Van Eldik, L., Berry, R., and Vassar, R. (2006) Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26, 10129-10140
29. Drummond, E. S., Muhling, J., Martins, R. N., Wijaya, L. K., Ehlert, E. M., and Harvey, A. R. (2013) Pathology associated withAAVmediated expression of β amyloid or C100 in adult mouse hippocampus and cerebellum. PLoS ONE 8, e59166
30. Youmans, K. L., Tai, L. M., Nwabuisi-Heath, E., Jungbauer, L., Kanekiyo, T., Gan, M., Kim, J., Eimer, W. A., Estus, S., Rebeck, G. W., Weeber, E. J., Bu, G., Yu, C., and Ladu, M. J. (2012) APOE4-specific changes in Aβ accumulation in a new transgenic mouse model of Alzheimer disease. J. Biol. Chem. 287, 41774-41786
31. Jin, L., Li, J., Nation, R. L., and Nicolazzo, J. A. (2011) Impact of P-glycoprotein inhibition and lipopolysaccharide administration on blood-brain barrier transport of colistin in mice. Antimicrob. Agents Chemother. 55, 502-507
32. Bergström, C. A., Charman, S. A., and Nicolazzo, J. A. (2012) Computational prediction of CNS drug exposure based on a novel in vivo dataset. Pharm. Res. 29, 3131-3142
33. Bitan, G., Fradinger, E. A., Spring, S. M., and Teplow, D. B. (2005) Neurotoxic protein oligomers: what you see is not always what you get. Amyloid 12, 88-95
34. Funke, S. A., Bartnik, D., Glück, J. M., Piorkowska, K., Wiesehan, K., Weber, U., Gulyas, B., Halldin, C., Pfeifer, A., Spenger, C., Muhs, A., and Willbold, D. (2012) Development of a small D-enantiomeric Alzheimer's amyloid-β binding peptide ligand for future in vivo imaging applications. PLoS ONE 7, e41457
35. Cohen, S. I., Linse, S., Luheshi, L. M., Hellstrand, E., White, D. A., Rajah, L., Otzen, D. E., Vendruscolo, M., Dobson, C. M., and Knowles, T. P. (2013) Proliferation of amyloid-β42 aggregates occurs through a secondary nucleation mechanism. Proc. Natl. Acad. Sci. U.S.A. 110, 9758-9763
36. Tarawneh, R., and Holtzman, D. M. (2010) Biomarkers in translational research of Alzheimer's disease. Neuropharmacology 59, 310-322
37. Mintun, M. A., Larossa, G. N., Sheline, Y. I., Dence, C. S., Lee, S. Y., Mach, R. H., Klunk, W. E., Mathis, C. A., DeKosky, S. T., and Morris, J. C. (2006) [11C]PIB in a nondemented population: potential antecedent marker of Alzheimer disease. Neurology 67, 446-452
38. Price, J. L., McKeel, D. W., Jr., Buckles, V. D., Roe, C. M., Xiong, C., Grundman, M., Hansen, L. A., Petersen, R. C., Parisi, J. E., Dickson, D. W., Smith, C. D., Davis, D. G., Schmitt, F. A., Markesbery, W. R., Kaye, J., Kurlan, R., Hulette, C., Kurland, B. F., Higdon, R., Kukull, W., and Morris, J. C. (2009) Neuropathology of nondemented aging: presumptive evidence for preclinical Alzheimer disease. Neurobiol. Aging 30, 1026-1036
39. Ladner, R. C., Sato, A. K., Gorzelany, J., and de Souza, M. (2004) Phage display-derived peptides as therapeutic alternatives to antibodies. Drug Discov. Today 9, 525-529
40. Demattos, R. B., Lu, J., Tang, Y., Racke, M. M., Delong, C. A., Tzaferis, J. A., Hole, J. T., Forster, B. M., McDonnell, P. C., Liu, F., Kinley, R. D., Jordan, W. H., and Hutton, M. L. (2012) A plaque-specific antibody clears existing β-amyloid plaques in Alzheimer's disease mice. Neuron 76, 908-920
41. Funamoto, S., Sasaki, T., Ishihara, S., Nobuhara, M., Nakano, M., Watanabe-Takahashi, M., Saito, T., Kakuda, N., Miyasaka, T., Nishikawa, K., Saido, T. C., and Ihara, Y. (2013) Substrate ectodomain is critical for substrate preference and inhibition of γ-secretase. Nat. Commun. 4, 2529
42. Austen, B. M., Paleologou, K. E., Ali, S. A., Qureshi, M. M., Allsop, D., and El-Agnaf, O. M. (2008) Designing peptide inhibitors for oligomerization and toxicity of Alzheimer's β-amyloid peptide. Biochemistry 47, 1984-1992
43. Tjernberg, L. O., Näslund, J., Lindqvist, F., Johansson, J., Karlström, A. R., Thyberg, J., Terenius, L., and Nordstedt, C. (1996) Arrest of β-amyloid fibril formation by a pentapeptide ligand. J. Biol. Chem. 271, 8545-8548
44. Amijee, H., Madine, J., Middleton, D. A., and Doig, A. J. (2009) Inhibitors of protein aggregation and toxicity. Biochem. Soc. Trans. 37, 692-696
45. Chacón, M. A., Barría, M. I., Soto, C., and Inestrosa, N. C. (2004) β-Sheet breaker peptide prevents Aβ-induced spatial memory impairments with partial reduction of amyloid deposits. Mol. Psychiatry 9, 953-961
46. Granic, I., Masman, M. F., Kees Mulder, C., Nijholt, I. M., Naude, P. J., de Haan, A., Borbély, E., Penke, B., Luiten, P. G., and Eisel, U. L. (2010) LPYFDa neutralizes amyloid-β-induced memory impairment and toxicity. J. Alzheimers Dis. 19, 991-1005
47. 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 Eng. Des. Sel. 21, 241-246
48. van Groen, T., Wiesehan, K., Funke, S. A., Kadish, I., Nagel-Steger, L., and Willbold, D. (2008) Reduction of Alzheimer's disease amyloid plaque load in transgenic mice by D3, A D-enantiomeric peptide identified by mirror image phage display. ChemMedChem 3, 1848-1852
49. Wiesehan, K., Buder, K., Linke, R. P., Patt, S., Stoldt, M., Unger, E., Schmitt, B., Bucci, E., and Willbold, D. (2003) Selection of D-amino-acid peptides that bind to Alzheimer's disease amyloid peptideAβ1-42 by mirror image phage display. Chembiochem 4, 748-753
50. Fluharty, B. R., Biasini, E., Stravalaci, M., Sclip, A., Diomede, L., Balducci, C., La Vitola, P., Messa, M., Colombo, L., Forloni, G., Borsello, T., Gobbi, M., and Harris, D. A. (2013) An N-terminal fragment of the prion protein binds to amyloid-β oligomers and inhibits their neurotoxicity in vivo. J. Biol. Chem. 288, 7857-7866
51. Chakravarthy, B., Ménard, M., Brown, L., Hewitt, M., Atkinson, T., and Whitfield, J. (2013) A synthetic peptide corresponding to a region of the human pericentriolar material 1 (PCM-1) protein binds β-amyloid (Aβ1-42) oligomers. J. Neurochem. 126, 415-424
52. Sundaram, R. K., Kasinathan, C., Stein, S., and Sundaram, P. (2012) Novel detox gel depot sequesters β-amyloid peptides in a mouse model of Alzheimer's disease. Int. J. Pept Res. Ther. 18, 99-106
53. Jokerst, J. V., Lobovkina, T., Zare, R. N., and Gambhir, S. S. (2011) Nanoparticle PEGylation for imaging and therapy. Nanomedicine 6, 715-728
54. Harris, J. M., and Chess, R. B. (2003) Effect of pegylation on pharmaceuticals. Nat. Rev. Drug Discov. 2, 214-221
55. Sumbria, R. K., Boado, R. J., and Pardridge, W. M. (2012) Imaging amyloid plaque in Alzheimer's disease brain with a biotinylated Aβ peptide radiopharmaceutical conjugated to an IgG-avidin fusion protein. Bioconjug. Chem. 23, 1318-1321
56. Tanifum, E. A., Dasgupta, I., Srivastava, M., Bhavane, R. C., Sun, L., Berridge, J., Pourgarzham, H., Kamath, R., Espinosa, G., Cook, S. C., Eriksen, J. L., and Annapragada, A. (2012) Intravenous delivery of targeted liposomes to amyloid-β pathology in APP/PSEN1 transgenic mice. PLoS ONE 7, e48515
57. Campbell M., Hanrahan, F., Gobbo, O. L., Kelly, M. E., Kiang, A. S., Humphries, M. M., Nguyen, A. T., Ozaki, E., Keaney, J., Blau, C. W., Kerskens, C. M., Cahalan, S. D., Callanan, J. J., Wallace, E., Grant, G. A., Doherty, C.P., and Humphries, P. (2012) Targeted suppression of claudin-5 decreases cerebral oedema and improves cognitive outcome following traumatic brain injury. Nat. Commun. 3, 849
58. Klunk, W. E., Engler, H., Nordberg, A., Wang, Y., Blomqvist, G., Holt, D. P., Bergström, M., Savitcheva, I., Huang, G. F., Estrada, S., Ausén, B., Debnath, M. L., Barletta, J., Price, J. C., Sandell, J., Lopresti, B. J., Wall, A., Koivisto, P., Antoni, G., Mathis, C. A., and Långström, B. (2004) Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann. Neurol 55, 306-319
59. Okamura, N., and Yanai, K. (2010) Florbetapir (18F), a PET imaging agent that binds to amyloid plaques for the potential detection of Alzheimer's disease. IDrugs 13, 890-899
60. Rinne, J. O., Wong, D. F., Wolk, D. A., Leinonen, V., Arnold, S. E., Buckley, C., Smith, A., McLain, R., Sherwin, P. F., Farrar, G., Kailajärvi, M., and Grachev, I. D. (2012) [18F]Flutemetamol PET imaging and cortical biopsy histopathology for fibrillar amyloid β detection in living subjects with normal pressure hydrocephalus: pooled analysis of four studies. Acta Neuropathol. 124, 833-845
61. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W., and Glabe, C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489
62. Lambert, M. P., Velasco, P. T., Chang, L., Viola, K. L., Fernandez, S., Lacor, P. N., Khuon, D., Gong, Y., Bigio, E. H., Shaw, P., De Felice, F. G., Krafft, G. A., and Klein, W. L. (2007) Monoclonal antibodies that target pathological assemblies of Aβ. J. Neurochem. 100, 23-35
63. Mathis, C. A., Wang, Y., and Klunk, W. E. (2004) Imaging β-amyloid plaques and neurofibrillary tangles in the aging human brain. Curr. Pharm. Des. 10, 1469-1492
64. Yates, E. A., Owens, S. L., Lynch, M. F., Cucco, E. M., Umbaugh, C. S., and Legleiter, J. (2013) Specific domains of Aβ facilitate aggregation on and association with lipid bilayers. J. Mol. Biol. 425, 1915-1933