Methylene blue inhibits amyloid Aβ oligomerization by promoting fibrillization

Biochemistry

Volumn 46, Issue 30, 2007, Pages 8850-8860

  Necula, Mihaela ^a   Breydo, Leonid ^a   Milton, Saskia ^a   Kayed, Rakez ^a   Van Der Veer, Wytze E ^a   Tone, Paul ^b,c   Glabe, Charles G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ST VINCENT S HOSPITAL   (United States)

^c NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATED SPECIES; AMYLOID PLAQUES; FIBRILLIZATION; NONFIBRILLAR OLIGOMERS; THERAPEUTIC INTERVENTION;

AGGLOMERATION; DISEASES; NEUROLOGY; OLIGOMERIZATION; PATHOLOGY; TRANSMISSION ELECTRON MICROSCOPY;

DYES;

AMYLOID A BETA PROTEIN; AMYLOID A PROTEIN; METHYLENE BLUE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; IMMUNOREACTIVITY; NEUROPATHOLOGY; NEUROTOXICITY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; SENILE PLAQUE; STOICHIOMETRY; TRANSMISSION ELECTRON MICROSCOPY;

AMYLOID BETA-PROTEIN; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; KINETICS; METHYLENE BLUE; MICROSCOPY, ELECTRON, TRANSMISSION; NEPHELOMETRY AND TURBIDIMETRY; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT PROTEINS; SENILE PLAQUES; SOLUBILITY;

EID: 34547672881     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700411k     Document Type: Article

References (95)

1. 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.
2. Selkoe, D. J. (1991) The molecular pathology of Alzheimer's disease, Neuron 6, 487-498.
3. 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.
4. Harper, J. D., and Lansbury, P. T., Jr. (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: Mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins, Annu. Rev. Biochem. 66, 385-407.
5. Howlett, D. R., Jennings, K. H., Lee, D. C., Clark, M. S., Brown, F., Wetzel, R., Wood, S. J., Camilleri, P., and Roberts, G. W. (1995) Aggregation state and neurotoxic properties of Alzheimer β-amyloid peptide, Neurodegeneration 4, 23-32.
6. Pike, C. J., Walencewicz, A. J., Glabe, C. G., and Cotman, C. W. (1991) In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity, Brain Res. 563, 311-314.
7. Pike, C. J., Burdick, D., Walencewicz, A. J., Glabe, C. G., and Cotman, C. W. (1993) Neurodegeneration induced by β-amyloid peptides in vitro: The role of peptide assembly state, J. Neurosci. 13, 1676-1687.
8. Seilheimer, B., Bohrmann, B., Bondolfi, L., Muller, F., Stuber, D., and Dobeli, H. (1997) The toxicity of the Alzheimer's β-amyloid peptide correlates with a distinct fiber morphology, J. Struct. Biol. 119, 59-71.
9. Lorenzo, A., and Yankner, B. A. (1994) β-Amyloid neurotoxicity requires fibril formation and is inhibited by congo red, Proc. Natl. Acad. Sci. U.S.A. 91, 12243-12247.
10. Sabate, R., and Estelrich, J. (2005) Stimulatory and inhibitory effects of alkyl bromide surfactants on β-amyloid fibrillogenesis, Langmuir 21, 6944-6949.
11. Kuner, P., Bohrmann, B., Tjernberg, L. O., Naslund, J., Huber, G., Celenk, S., Gruninger-Leitch, F., Richards, J. G., Jakob-Roetne, R., Kemp, J. A., and Nordstedt, C. (2000) Controlling polymerization of β-amyloid and prion-derived peptides with synthetic small molecule ligands, J. Biol. Chem. 275, 1673-1678.
12. Ono, K., Hasegawa, K., Naiki, H., and Yamada, M. (2004) Curcumin has potent anti-amyloidogenic effects for Alzheimer's β-amyloid fibrils in vitro, J. Neurosci. Res. 75, 742-750.
13. Cheng, X., and van Breemen, R. B. (2005) Mass spectrometry-based screening for inhibitors of β-amyloid protein aggregation, Anal. Chem. 77, 7012-7015.
14. De Felice, F. G., Houzel, J. C., Garcia-Abreu, J., Louzada, P. R., Jr., Afonso, R. C., Meirelles, M. N., Lent, R., Neto, V. M., and Ferreira, S. T. (2001) Inhibition of Alzheimer's disease β-amyloid aggregation, neurotoxicity, and in vivo deposition by nitrophenols: Implications for Alzheimer's therapy, FASEB J. 15, 1297-1299.
15. Bohrmann, B., Adrian, M., Dubochet, J., Kuner, P., Muller, F., Huber, W., Nordstedt, C., and Dobeli, H. (2000) Self-assembly of β-amyloid 42 is retarded by small molecular ligands at the stage of structural intermediates, J. Struct. Biol. 130, 232-246.
16. Howlett, D. R., George, A. R., Owen, D. E., Ward, R. V., and Markwell, R. E. (1999) Common structural features determine the effectiveness of carvedilol, daunomycin and rolitetracycline as inhibitors of Alzheimer β-amyloid fibril formation, Biochem. J. 343 (Part 2), 419-423.
17. Tomiyama, T., Asano, S., Suwa, Y., Morita, T., Kataoka, K., Mori, H., and Endo, N. (1994) Rifampicin prevents the aggregation and neurotoxicity of amyloid β protein in vitro, Biochem. Biophys. Res. Commun. 204, 76-83.
18. Wood, S. J., MacKenzie, L., Maleeff, B., Hurle, M. R., and Wetzel, R. (1996) Selective inhibition of Aβ fibril formation, J. Biol. Chem. 271, 4086-4092.
19. Pappolla, M., Bozner, P., Soto, C., Shao, H., Robakis, N. K., Zagorski, M., Frangione, B., and Ghiso, J. (1998) Inhibition of Alzheimer β-fibrillogenesis by melatonin, J. Biol. Chem. 273, 7185-7188.
20. Lashuel, H. A., Hartley, D. M., Balakhaneh, D., Aggarwal, A., Teichberg, S., and Callaway, D. J. (2002) New class of inhibitors of amyloid-β fibril formation. Implications for the mechanism of pathogenesis in Alzheimer's disease, J. Biol. Chem. 277, 42881-42890.
21. Howlett, D. R., Perry, A. E., Godfrey, F., Swatton, J. E., Jennings, K. H., Spitzfaden, C., Wadsworth, H., Wood, S. J., and Markwell, R. E. (1999) Inhibition of fibril formation in β-amyloid peptide by a novel series of benzofurans, Biochem. J. 340 (Part 1), 283-289.
22. Williams, A. D., Sega, M., Chen, M., Kheterpal, I., Geva, M., Berthelier, V., Kaleta, D. T., Cook, K. D., and Wetzel, R. (2005) Structural properties of Aβ protofibrils stabilized by a small molecule, Proc. Natl. Acad. Sci. U.S.A. 102, 7115-7120.
23. Ono, K., Hasegawa, K., Naiki, H., and Yamada, M. (2004) Anti-amyloidogenic activity of tannic acid and its activity to destabilize Alzheimer's β-amyloid fibrils in vitro, Biochim. Biophys. Acta 1690, 193-202.
24. De Felice, F. G., Vieira, M. N., Saraiva, L. M., Figueroa-Villar, J. D., Garcia-Abreu, J., Liu, R., Chang, L., Klein, W. L., and Ferreira, S. T. (2004) Targeting the neurotoxic species in Alzheimer's disease: Inhibitors of Aβ oligomerization, FASEB J. 18, 1366-1372.
25. Pollack, S. J., Sadler, I. I., Hawtin, S. R., Tailor, V. J., and Shearman, M. S. (1995) Sulfonated dyes attenuate the toxic effects of β-amyloid in a structure-specific fashion, Neurosci. Lett. 197, 211-214.
26. Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., and Katzman, R. (1991) Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment, Ann. Neurol. 30, 572-580.
27. 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.
28. Hartley, D. M., Walsh, D. M., Ye, C. P., Diehl, T., Vasquez, S., Vassilev, P. M., Teplow, D. B., and Selkoe, D. J. (1999) Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons, J. Neurosci. 19, 8876-8884.
29. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., and Selkoe, D. J. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo, Nature 416, 535-539.
30. Dahlgren, K. N., Manelli, A. M., Stine, W. B., Jr., Baker, L. K., Krafft, G. A., and LaDu, M. J. (2002) Oligomeric and fibrillar species of amyloid-β peptides differentially affect neuronal viability, J. Biol. Chem. 277, 32046-32053.
31. Hoshi, M., Sato, M., Matsumoto, S., Noguchi, A., Yasutake, K., Yoshida, N., and Sato, K. (2003) Spherical aggregates of β-amyloid (amylospheroid) show high neurotoxicity and activate tau protein kinase I/glycogen synthase kinase-3β, Proc. Natl. Acad. Sci. U.S.A. 100, 6370-6375.
32. Klein, W. L., Krafft, G. A., and Finch, C. E. (2001) Targeting small Aβ oligomers: The solution to an Alzheimer's disease conundrum? Trends Neurosci. 24, 219-224.
33. 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.
34. Klein, W. L., Stine, W. B., Jr., and Teplow, D. B. (2004) Small assemblies of unmodified amyloid β-protein are the proximate neurotoxin in Alzheimer's disease, Neurobiol. Aging 25, 569-580.
35. McLean, C. A., Cherny, R. A., Fraser, F. W., Fuller, S. J., Smith, M. J., Beyreuther, K., Bush, A. I., and Masters, C. L. (1999) Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease, Ann. Neurol. 46, 860-866.
36. Lue, L. F., Kuo, Y. M., Roher, A. E., Brachova, L., Shen, Y., Sue, L., Beach, T., Kurth, J. H., Rydel, R. E., and Rogers, J. (1999) Soluble amyloid β peptide concentration as a predictor of synaptic change in Alzheimer's disease, Am. J. Pathol. 155, 853-862.
37. Necula, M., Kayed, R., Milton, S., and Glabe, C. G. (2007) Small-molecule inhibitors distinguish between amyloid β oligomerization and fibrillization pathways, J. Biol. Chem. 282, 10311-10324.
38. Gorman, P. M., Yip, C. M., Fraser, P. E., and Chakrabartty, A. (2003) Alternate aggregation pathways of the Alzheimer β-amyloid peptide: Aβ association kinetics at endosomal pH, J. Mol. Biol. 325, 743-757.
39. Soreghan, B., Kosmoski, J., and Glabe, C. (1994) Surfactant properties of Alzheimer's A β peptides and the mechanism of amyloid aggregation, J. Biol. Chem. 269, 28551-28554.
40. Harper, J. D., Lieber, C. M., and Lansbury, P. T., Jr. (1997) Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-β protein, Chem. Biol. 4, 951-959.
41. Yong, W., Lomakin, A., Kirkitadze, M. D., Teplow, D. B., Chen, S. H., and Benedek, G. B. (2002) Structure determination of micelle-like intermediates in amyloid β-protein fibril assembly by using small angle neutron scattering, Proc. Natl. Acad. Sci. U.S.A. 99, 150-154.
42. Lomakin, A., Teplow, D. B., Kirschner, D. A., and Benedek, G. B. (1997) Kinetic theory of fibrillogenesis of amyloid β-protein, Proc. Natl. Acad. Sci. U.S.A. 94, 7942-7947.
43. Huang, T. H., Yang, D. S., Plaskos, N. P., Go, S., Yip, C. M., Fraser, P. E., and Chakrabartty, A. (2000) Structural studies of soluble oligomers of the Alzheimer β-amyloid peptide, J. Mol. Biol. 297, 73-87.
44. Kuo, Y. M., Emmerling, M. R., Vigo-Pelfrey, C., Kasunic, T. C., Kirkpatrick, J. B., Murdoch, G. H., Ball, M. J., and Roher, A. E. (1996) Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer disease brains, J. Biol. Chem. 271, 4077-4081.
45. Roher, A. E., Chaney, M. O., Kuo, Y. M., Webster, S. D., Stine, W. B., Haverkamp, L. J., Woods, A. S., Cotter, R. J., Tuohy, J. M., Krafft, G. A., Bonnell, B. S., and Emmerling, M. R. (1996) Morphology and toxicity of Aβ-(1-42) dimer derived from neuritic and vascular amyloid deposits of Alzheimer's disease, J. Biol. Chem. 271, 20631-20635.
46. Walsh, D. M., Lomakin, A., Benedek, G. B., Condron, M. M., and Teplow, D. B. (1997) Amyloid β-protein fibrillogenesis. Detection of a protofibrillar intermediate, J. Biol. Chem. 272, 22364-22372.
47. Harper, J. D., Wong, S. S., Lieber, C. M., and Lansbury, P. T. (1997) Observation of metastable Aβ amyloid protofibrils by atomic force microscopy, Chem. Biol. 4, 119-125.
48. Blackley, H. K., Sanders, G. H., Davies, M. C., Roberts, C. J., Tendler, S. J., and Wilkinson, M. J. (2000) In-situ atomic force microscopy study of β-amyloid fibrillization, J. Mol. Biol. 298, 833-840.
49. Nybo, M., Svehag, S. E., and Holm Nielsen, E. (1999) An ultrastructural study of amyloid intermediates in Aβ1-42 fibrillogenesis, Scand. J. Immunol. 49, 219-223.
50. 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 β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates, J. Biol. Chem. 274, 25945-25952.
51. Kirkitadze, M. D., Condron, M. M., and Teplow, D. B. (2001) Identification and characterization of key kinetic intermediates in amyloid β-protein fibrillogenesis, J. Mol. Biol. 312, 1103-1119.
52. Naiki, H., and Nakakuki, K. (1996) First-order kinetic model of Alzheimer's β-amyloid fibril extension in vitro, Lab. Invest. 74, 374-383.
53. Lomakin, A., Chung, D. S., Benedek, G. B., Kirschner, D. A., and Teplow, D. B. (1996) On the nucleation and growth of amyloid β-protein fibrils: Detection of nuclei and quantitation of rate constants, Proc. Natl. Acad. Sci. U.S.A. 93, 1125-1129.
54. Harper, J. D., Wong, S. S., Lieber, C. M., and Lansbury, P. T., Jr. (1999) Assembly of Aβ amyloid protofibrils: An in vitro model for a possible early event in Alzheimer's disease, Biochemistry 38, 8972-8980.
55. Chromy, B. A., Nowak, R. J., Lambert, M. P., Viola, K. L., Chang, L., Velasco, P. T., Jones, B. W., Fernandez, S. J., Lacor, P. N., Horowitz, P., Finch, C. E., Krafft, G. A., and Klein, W. L. (2003) Self-assembly of Aβ(1-42) into globular neurotoxins, Biochemistry 42, 12749-12760.
56. Yao, Z., Drieu, K., and Papadopoulos, V. (2001) The Ginkgo biloba extract EGb 761 rescues the PC12 neuronal cells from β-amyloid-induced cell death by inhibiting the formation of β-amyloid-derived diffusible neurotoxic ligands, Brain Res. 889, 181-190.
57. 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.
58. Chang, L., Bakhos, L., Wang, Z., Venton, D. L., and Klein, W. L. (2003) Femtomole immunodetection of synthetic and endogenous amyloid-β oligomers and its application to Alzheimer's disease drug candidate screening, J. Mol. Neurosci. 20, 305-313.
59. Yang, F., Lim, G. P., Begum, A. N., Ubeda, O. J., Simmons, M. R., Ambegaokar, S. S., Chen, P. 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.
60. Riha, P. D., Bruchey, A. K., Echevarria, D. J., and Gonzalez-Lima, F. (2005) Memory facilitation by methylene blue: Dose-dependent effect on behavior and brain oxygen consumption, Eur. J. Pharmacol. 511, 151-158.
61. Kupfer, A., Aeschlimann, C., Wermuth, B., and Cerny, T. (1994) Prophylaxis and reversal of ifosfamide encephalopathy with methylene-blue, Lancet 343, 763-764.
62. Peter, C., Hongwan, D., Kupfer, A., and Lauterburg, B. H. (2000) Pharmacokinetics and organ distribution of intravenous and oral methylene blue, Eur. J. Clin. Pharmacol. 56, 247-250.
63. DiSanto, A. R., and Wagner, J. G. (1972) Pharmacokinetics of highly ionized drugs. II. Methylene blue: Absorption, metabolism, and excretion in man and dog after oral administration, J. Pharm. Sci. 61, 1086-1090.
64. Riedel, W., Lang, U., Oetjen, U., Schlapp, U., and Shibata, M. (2003) Inhibition of oxygen radical formation by methylene blue, aspirin, or α-lipoic acid, prevents bacterial-lipopolysaccharide-induced fever, Mol. Cell. Biochem. 247, 83-94.
65. Callaway, N. L., Riha, P. D., Wrubel, K. M., McCollum, D., and Gonzalez-Lima, F. (2002) Methylene blue restores spatial memory retention impaired by an inhibitor of cytochrome oxidase in rats, Neurosci. Lett. 332, 83-86.
66. Taniguchi, S., Suzuki, 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.
67. Roikhel, V. M., Fokina, G. I., and Pogodina, V. V. (1984) Influence of aminasine on experimental scrapie in mice, Acta Virol. 28, 321-324.
68. Dees, C., Wade, W. F., German, T. L., and Marsh, R. F. (1985) Inactivation of the scrapie agent by ultraviolet irradiation in the presence of chlorpromazine, J. Gen. Virol. 66 (Part 4), 845-849.
69. Doh-Ura, K., Iwaki, T., and Caughey, B. (2000) Lysosomotropic agents and cysteine protease inhibitors inhibit scrapie-associated prion protein accumulation, J. Virol. 74, 4894-4897.
70. Korth, C., May, B. C., Cohen, F. E., and Prusiner, S. B. (2001) Acridine and phenothiazine derivatives as pharmacotherapeutics for prion disease, Proc. Natl. Acad. Sci. U.S.A. 98, 9836-9841.
71. Wischik, C. M., Edwards, P. C., Lai, R. Y., Roth, M., and Harrington, C. R. (1996) Selective inhibition of Alzheimer disease-like tau aggregation by phenothiazines, Proc. Natl. Acad. Sci. U.S.A. 93, 11213-11218.
72. 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.
73. Necula, M., Chirita, C. N., and Kuret, J. (2005) Cyanine dye N744 inhibits tau fibrillization by blocking filament extension: Implications for the treatment of tauopathic neurodegenerative diseases, Biochemistry 44, 10227-10237.
74. Uversky, V. N., Li, J., and Fink, A. L. (2001) Evidence for a partially folded intermediate in α-synuclein fibril formation, J. Biol. Chem. 276, 10737-10744.
75. Nielsen, L., Khurana, R., Coats, A., Frokjaer, S., Brange, J., Vyas, S., Uversky, V. N., and Fink, A. L. (2001) Effect of environmental factors on the kinetics of insulin fibril formation: Elucidation of the molecular mechanism, Biochemistry 40, 6036-6046.
76. Chirita, C. N., and Kuret, J. (2004) Evidence for an intermediate in tau filament formation, Biochemistry 43, 1704-1714.
77. Necula, M., Chirita, C. N., and Kuret, J. (2003) Rapid anionic micelle-mediated α-synuclein fibrillization in vitro, J. Biol. Chem. 278, 46674-46680.
78. Evans, K. C., Berger, E. P., Cho, C. G., Weisgraber, K. H., and Lansbury, P. T., Jr. (1995) Apolipoprotein E is a kinetic but not a thermodynamic inhibitor of amyloid formation: Implications for the pathogenesis and treatment of Alzheimer disease, Proc. Natl. Acad. Sci. U.S.A. 92, 763-767.
79. Chirita, C. N., Necula, M., and Kuret, J. (2003) Anionic micelles and vesicles induce tau fibrillization in vitro, J. Biol. Chem. 278, 25644-25650.
80. Jiao, Q., and Liu, Q. (1999) Characterization of the interaction between methylene blue and glycosaminoglycans, Spectrochim. Acta, Part A 55, 1667-1673.
81. Snow, A. D., Lara, S., Nochlin, D., and Wight, T. N. (1989) Cationic dyes reveal proteoglycans structurally integrated within the characteristic lesions of Alzheimer's disease, Acta Neuropathol. 78, 113-123.
82. Snow, A. D., Mar, H., Nochlin, D., Kimata, K., Kato, M., Suzuki, S., Hassell, J., and Wight, T. N. (1988) The presence of heparan sulfate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease, Am. J. Pathol. 133, 456-463.
83. Su, J. H., Cummings, B. J., and Cotman, C. W. (1992) Localization of heparan sulfate glycosaminoglycan and proteoglycan core protein in aged brain and Alzheimer's disease, Neuroscience 51, 801-813.
84. Snow, A. D., Mar, H., Nochlin, D., Kresse, H., and Wight, T. N. (1992) Peripheral distribution of dermatan sulfate proteoglycans (decorin) in amyloid-containing plaques and their presence in neurofibrillary tangles of Alzheimer's disease, J. Histochem. Cytochem. 40, 105-113.
85. Snow, A. D., Nochlin, D., Sekiguichi, R., and Carlson, S. S. (1996) Identification in immunolocalization of a new class of proteoglycan (keratan sulfate) to the neuritic plaques of Alzheimer's disease, Exp. Neurol. 138, 305-317.
86. DeWitt, D. A., Silver, J., Canning, D. R., and Perry, G. (1993) Chondroitin sulfate proteoglycans are associated with the lesions of Alzheimer's disease, Exp. Neurol. 121, 149-152.
87. Nilsson, K. P., Herland, A., Hammarstrom, P., and Inganas, O. (2005) Conjugated polyelectrolytes: Conformation-sensitive optical probes for detection of amyloid fibril formation, Biochemistry 44, 3718-3724.
88. 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.
89. Souillac, P. O., Uversky, V. N., Millett, I. S., Khurana, R., Doniach, S., and Fink, A. L. (2002) Elucidation of the molecular mechanism during the early events in immunoglobulin light chain amyloid fibrillation. Evidence for an off-pathway oligomer at acidic pH, J. Biol. Chem. 277, 12666-12679.
90. Serpell, L. C. (2000) Alzheimer's amyloid fibrils: Structure and assembly, Biochim. Biophys. Acta 1502, 16-30.
91. Santini, S., Wei, G., Mousseau, N., and Derreumaux, P. (2004) Pathway complexity of Alzheimer's β-amyloid Aβ16-22 peptide assembly, Structure 12, 1245-1255.
92. Lashuel, H. A., Hartley, D. M., Petre, B. M., Wall, J. S., Simon, M. N., Walz, T., and Lansbury, P. T., Jr. (2003) Mixtures of wild-type and a pathogenic (E22G) form of Aβ40 in vitro accumulate protofibrils, including amyloid pores, J. Mol. Biol. 332, 795-808.
93. Kayed, R., Bernhagen, J., Greenfield, N., Sweimeh, K., Brunner, H., Voelter, W., and Kapurniotu, A. (1999) Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro, J. Mol. Biol. 287, 781-796.
94. Uversky, V. N., Lee, H. J., Li, J., Fink, A. L., and Lee, S. J. (2001) Stabilization of partially folded conformation during α-synuclein oligomerization in both purified and cytosolic preparations, J. Biol. Chem. 276, 43495-43498.
95. Chirita, C. N., Congdon, E. E., Yin, H., and Kuret, J. (2005) Triggers of full-length tau aggregation: A role for partially folded intermediates, Biochemistry 44, 5862-5872.