Glyconanoparticle aided detection of β-amyloid by magnetic resonance imaging and attenuation of β-amyloid induced cytotoxicity

ACS Chemical Neuroscience

Volumn 4, Issue 4, 2013, Pages 575-584

  Kouyoumdjian, Hovig ^a   Zhu, David C ^a   El Dakdouki, Mohammad H ^a,c   Lorenz, Kelly ^a   Chen, Jianjun ^b   Li, Wei ^b   Huang, Xuefei ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c BEIRUT ARAB UNIVERSITY   (Lebanon)

Author keywords

Amyloid; carbohydrates; cytotoxicity; magnetic glyconanoparticles; magnetic resonance imaging

Indexed keywords

AMYLOID BETA PROTEIN; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

ANIMAL CELL; ARTICLE; BIOMIMETICS; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FLUORESCENCE ANALYSIS; GEL ELECTROPHORESIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; TRANSMISSION ELECTRON MICROSCOPY;

AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; CELL LINE, TUMOR; CELL SURVIVAL; GANGLIOSIDOSIS, GM1; HUMANS; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED C57BL; N-ACETYLNEURAMINIC ACID; NANOPARTICLES;

EID: 84876523375     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn3002015     Document Type: Article

References (89)

1. Alzheimer's Association. Alzheimer's disease facts and figures. Alzheimer's & Dementia; Alzheimer Foundation: Washington, DC, 2011; Vol. 7.
2. Brookmeyer, R., Gray, S., and Kawas, C. (1998) Projections of Alzheimer's disease in the United States and the public health impact of delaying disease onset Am. J. Public Health 88, 1337-1342
3. Coreybloom, J., Thal, L. J., Galasko, D., Folstein, M., Drachman, D., Raskind, M., and Lanska, D. J. (1995) Diagnosis and evaluation of dementia Neurology 45, 211-218
4. Ostwald, S. K., Hepburn, K. W., Caron, W., Burns, T., and Mantell, R. (1999) Reducing caregiver burden: A randomized psychoeducational intervention for caregivers of persons with dementia Gerontologist 39, 299-309
5. Ernst, R. L. and Hay, J. W. (1994) The US economic and social cost of Alzheimers-disease revisited Am. J. Public Health 84, 1261-1264
6. Wimo, A. and Winblad, B. (2004) Economic aspects on drug therapy of dementia Curr. Pharm. Des. 10, 295-301
7. Minati, L., Grisoli, M., and Bruzzone, M. G. (2007) MR spectroscopy, functional MRI, and diffusion-tensor imaging in the aging brain: A conceptual review J. Geriatr. Psych. Neur. 20, 3-21
8. Lehericy, S., Marjanska, M., Mesrob, L., Sarazin, M., and Kinkingnehun, S. (2007) Magnetic resonance imaging of Alzheimer's disease Eur. Radiol. 17, 347-362
9. Sandson, T. A., Oconnor, M., Sperling, R. A., Edelman, R. R., and Warach, S. (1996) Noninvasive perfusion MRI in Alzheimer's disease: A preliminary report Neurology 47, 1339-1342
10. Alsop, D. C., Detre, J. A., and Grossman, M. (2000) Assessment of cerebral blood flow in Alzheimer's disease by spin-labeled magnetic resonance imaging Ann. Neurol. 47, 93-100
11. De Santi, S., de Leon, M. J., Rusinek, H., Convit, A., Tarshish, C. Y., Roche, A., Tsui, W. H., Kandil, E., Boppana, M., Daisley, K., Wang, G. J., Schlyer, D., and Fowler, J. (2001) Hippocampal formation glucose metabolism and volume losses in MCI and AD Neurobiol. Aging 22, 529-539
12. Colloby, S. J., Fenwick, J. D., Williams, E. D., Paling, S. M., Lobotesis, K., Ballard, C., McKeith, I., and O'Brien, J. T. (2002) A comparison of Tc-99m-HMPAO SPET changes in dementia with Lewy bodies and Alzheimer's disease using statistical parametric mapping Eur. J. Nucl. Med. Mol. Imaging 29, 615-622
13. Bonte, F. J., Harris, T. S., Roney, C. A., and Hynan, L. S. (2004) Differential diagnosis between Alzheimer's and frontotemporal disease by the posterior cingulate sign J. Nucl. Med. 45, 771-774
14. Caroli, A., Testa, C., Geroldi, C., Nobili, F., Barnden, L. R., Guerra, U. P., Bonetti, M., and Frisoni, G. B. (2007) Cerebral perfusion correlates of conversion to Alzheimer's disease in amnestic mild cognitive impairment J. Neurol. 254, 1698-1707
15. Mosconi, L., Tsui, W. H., De Santi, S., Li, J., Rusinek, H., Convit, A., Li, Y., Boppana, M., and de Leon, M. J. (2005) Reduced hippocampal metabolism in MCI and AD-automated FDG-PET image analysis Neurology 64, 1860-1867
16. Hardy, J. A. and Higgins, G. A. (1992) Alzheimers-disease-The Amyloid Cascade Hypothesis Science 256, 184-185
17. Selkoe, D. J. (1994) Alzheimers-disease-A central role for amyloid J. Neuropathol. Exp. Neurol. 53, 438-447
18. Hartmann, T., Bieger, S. C., Bruhl, B., Tienari, P. J., Ida, N., Allsop, D., Roberts, G. W., Masters, C. L., Dotti, C. G., Unsicker, K., and Beyreuther, K. (1997) Distinct sites of intracellular production for Alzheimer's disease A beta 40/42 amyloid peptides Nat. Med. 3, 1016-1020
19. Bitan, G., Vollers, S. S., and Teplow, D. B. (2003) Elucidation of primary structure elements controlling early amyloid beta-protein oligomerization J. Biol. Chem. 278, 34882-34889
20. Klunk, W. E., Engler, H., Nordberg, A., Wang, Y. M., Blomqvist, G., Holt, D. P., Bergstrom, M., Savitcheva, I., Huang, G. F., Estrada, S., Ausen, B., Debnath, M. L., Barletta, J., Price, J. C., Sandell, J., Lopresti, B. J., Wall, A., Koivisto, P., Antoni, G., Mathis, C. A., and Langstrom, B. (2004) Imaging brain amyloid in Alzheimer's disease with Pittsburgh compound-B Ann. Neurol. 55, 306-319
21. Vanbroeckhoven, C., Haan, J., Bakker, E., Hardy, J. A., Vanhul, W., Wehnert, A., Vegtervandervlis, M., and Roos, R. A. C. (1990) Amyloid-beta protein-precursor gene and hereditary cerebral-hemorrhage with amyloidosis (Dutch) Science 248, 1120-1122
22. Shoghi-Jadid, K., Small, G. W., Agdeppa, E. D., Kepe, V., Ercoli, L. M., Siddarth, P., Read, S., Satyamurthy, N., Petric, A., Huang, S. C., and Barrio, J. R. (2002) Localization of neurofibrillary tangles and beta-amyloid plaques in the brains of living patients with Alzheimer disease Am. J. Geriat. Psychiatry 10, 24-35
23. Rowe, C. C., Ackerman, U., Browne, W., Mulligan, R., Pike, K. L., O'Keefe, G., Tochon-Danguy, H., Chan, G., Berlangieri, S. U., Jones, G., Dickinson-Rowe, K. L., Kung, H. P., Zhang, W., Kung, M. P., Skovronsky, D., Dyrks, T., Hall, G., Krause, S., Friebe, M., Lehman, L., Lindemann, S., Dinkelborg, L. M., Masters, C. L., and Villemagne, V. L. (2008) Imaging of amyloid beta in Alzheimer's disease with F-18-BAY94-9172, a novel PET tracer: proof of mechanism Lancet Neurol. 7, 129-135
24. Barthel, H., Gertz, H.-J., Dresel, S., Peters, O., Bartenstein, P., Buerger, K., Hiemeyer, F., Wittemer-Rump, S. M., Seibyl, J., Reininger, C., Sabri, O., and Florbetaben Study, G. (2011) Cerebral amyloid-beta PET with Florbetaben (F-18) in patients with Alzheimer's disease and healthy controls: A multicentre phase 2 diagnostic study Lancet Neurol. 10, 424-435
25. Villemagne, V. L., Ong, K., Mulligan, R. S., Holl, G., Pejoska, S., Jones, G., O'Keefe, G., Ackerman, U., Tochon-Danguy, H., Chan, J. G., Reininger, C. B., Fels, L., Putz, B., Rohde, B., Masters, C. L., and Rowe, C. C. (2011) Amyloid imaging with F-18-Florbetaben in Alzheimer disease and other dementias J. Nucl. Med. 52, 1210-1217
26. Wong, D. F., Rosenberg, P. B., Zhou, Y., Kumar, A., Raymont, V., Ravert, H. T., Dannals, R. F., Nandi, A., Brasic, J. R., Ye, W., Hilton, J., Lyketsos, C., Kung, H. F., Joshi, A. D., Skovronsky, D. M., and Pontecorvo, M. J. (2010) In vivo imaging of amyloid deposition in Alzheimer disease using the radioligand F-18-AV-45 (Flobetapir F 18) J. Nucl. Med. 51, 913-920
27. Clark, C. M., Schneider, J. A., Bedell, B. J., Beach, T. G., Bilker, W. B., Mintun, M. A., Pontecorvo, M. J., Hefti, F., Carpenter, A. P., Flitter, M. L., Krautkramer, M. J., Kung, H. F., Coleman, R. E., Doraiswamy, P. M., Fleisher, A. S., Sabbagh, M. N., Sadowsky, C. H., Reiman, P. E. M., Zehntner, S. P., Skovronsky, D. M., and Grp, A. A. S. (2011) Use of Florbetapir-PET for imaging beta-amyloid pathology JAMA, J. Am. Med. Assoc. 305, 275-283
28. Siegemund, T., Paulke, B. R., Schmiedel, H., Bordag, N., Hoffmann, A., Harkany, T., Tanila, H., Kacza, J., and Hartig, W. (2006) Thioflavins released from nanoparticles target fibrillar amyloid beta in the hippocampus of APP/PS1 transgenic mice Int. J. Dev. Neurosci. 24, 195-201
29. Poduslo, J. F., Wengenack, T. M., Curran, G. L., Wisniewski, T., Sigurdsson, E. M., Macura, S. I., Borowski, B. J., and Jack, C. R. (2002) Molecular targeting of Alzheimer's amyloid plaques for contrast-enhanced magnetic resonance imaging Neurobiol. Dis. 11, 315-329
30. Wadghiri, Y. Z., Sigurdsson, E. M., Sadowski, M., Elliott, J. I., Li, Y. S., Scholtzova, H., Tang, C. Y., Aguinaldo, G., Pappolla, M., Duff, K., Wisniewski, T., and Turnbull, D. H. (2003) Detection of Alzheimer's amyloid in transgenic mice using magnetic resonance microimaging Magn. Reson. Med. 50, 293-302
31. Petiet, A., Santina, M., Bertrand, A., Wiggins, C. J., Petit, F., Houitte, D., Hantraye, P., Benavides, J., Debeir, T., Rooney, T., and Dhenain, M. (2012) Gadolinium-staining reveals amyloid plaques in the brain of Alzheimer's transgenic mice Neurobiol. Aging 33, 1533-1544
32. 1H MRI detection of amyloid beta plaques in vivo Nat. Neurosci. 8, 527-533
33. Hintersteiner, M., Enz, A., Frey, P., Jaton, A.-L., Kinzy, W., Kneuer, R., Neumann, U., Rudin, M., Staufenbiel, M., Stoeckli, M., Wiederhold, K.-H., and Gremlich, H.-U. (2005) In vivo detection of amyloid-β deposits by near-infrared imaging using an oxazine-derivative probe Nat. Biotechnol. 23, 577-583
34. Di Domizio, J., Zhang, R., Stagg, L. J., Gagea, M., Zhuo, M., Ladbury, J. E., and Cao, W. (2012) Binding with nucleic acids or glycosaminoglycans converts soluble protein oligomers to amyloid J. Biol. Chem. 287, 736-747
35. Braun, S., Humphreys, C., Fraser, E., Brancale, A., Bochtler, M., and Dale, T. C. (2011) Amyloid-associated nucleic acid hybridisation PLoS One 6, e19125
36. Yanagisawa, K., Odaka, A., Suzuki, N., and Ihara, Y. (1995) GM1 ganglioside-bound amyloid beta-protein (Abeta): A possible form of preamyloid in alzheimer's disease Nat. Med. 1, 1062-1066
37. Ariga, T. and Yu, R. K. (1999) GM1 Inhibits amyloid beta-protein-induced cytokine release Neurochem. Res. 24, 219-226
38. Wakabayashi, M., Okada, T., Kozutsumi, Y., and Matsuzaki, K. (2005) GM1 ganglioside-mediated accumulation of amyloid beta-protein on cell membranes Biochem. Biophys. Res. Commun. 328, 1019-1023
39. Nagai, Y. (1995) Functional roles of gangliosides in bio-signaling Behav. Brain Res. 66, 99-104
40. Williamson, M. P., Suzuki, Y., Bourne, N. T., and Asakura, T. (2006) Binding of amyloid beta-peptide to ganglioside micelles is dependent on histidine-13 Biochem. J. 397, 483-490
41. Kakio, A., Nishimoto, S., Yanagisawa, K., Kozutsumi, Y., and Matsuzaki, K. (2001) Cholesterol-dependent formation of GM1 ganglioside-bound amyloid beta-protein, an endogenous seed for Alzheimer amyloid J. Biol. Chem. 276, 24985-24990
42. Kakio, A., Yano, Y., Takai, D., Kuroda, Y., Matsumoto, O., Kozutsumi, Y., and Matsuzaki, K. (2004) Interaction between amyloid beta-protein aggregates and membranes J. Pept. Sci. 10, 612-621
43. Yamamoto, N., Matsubara, T., Sato, T., and Yanagisawa, K. (2009) Age-dependent high-density clustering of GM1 ganglioside at presynaptic neuritic terminals promotes amyloid β-protein fibrillogenesis Biochim. Biophys. Acta 1778, 2717-2726
44. Patel, D., Henry, J., and Good, T. (2006) Attenuation of beta-amyloid induced toxicity by sialic acid-conjugated dendrimeric polymers Biochim. Biophys. Acta, Gen. Subj. 1760, 1802-1809
45. Cowan, C. B., Cote, G. L., and Good, T. A. (2008) Development of photocrosslinked sialic acid containing polymers for use in Abeta toxicity attenuation Biomaterials 29, 3408-3414
46. Patel, D. A., Henry, J. E., and Good, T. A. (2007) Attenuation of beta-amyloid-induced toxicity by sialic-acid-conjugated dendrimers: Role of sialic acid attachment Brain Res. 1161, 95-105
47. Barnham, K. J., Kenche, V. B., Ciccotosto, G. D., Smith, D. P., Tew, D. J., Liu, X., Perez, K., Cranston, G. A., Johanssen, T. J., Volitakis, I., Bush, A. I., Masters, C. L., White, A. R., Smith, J. P., Cherny, R. A., and Cappai, R. (2008) Platinum-based inhibitors of amyloid-beta as therapeutic agents for Alzheimer's disease Proc. Natl. Acad. Sci. U.S.A. 105, 6813-6818
48. Kim, J. E. and Lee, M. (2003) Fullerene inhibits beta-amyloid peptide aggregation Biochem. Bioph. Res. Co. 303, 576-579
49. Ikeda, K., Okada, T., Sawada, S.-i., Akiyoshi, K., and Matsuzaki, K. (2006) Inhibition of the formation of amyloid beta-protein fibrils using biocompatible nanogels as artificial chaperones FEBS Lett. 580, 6587-6595
50. Geng, J., Li, M., Ren, J., Wang, E., and Qu, X. (2011) Polyoxometalates as inhibitors of the aggregation of amyloid beta peptides associated with Alzheimer's disease Angew. Chem., Int. Ed. 50, 4184-4188
51. Yoo, S. I., Yang, M., Brender, J. R., Subramanian, V., Sun, K., Joo, N. E., Jeong, S.-H., Ramamoorthy, A., and Kotov, N. A. (2011) Inhibition of amyloid peptide fibrillation by inorganic nanoparticles: Functional similarities with proteins Angew. Chem., Int. Ed. 50, 5110-5115
52. Saraiva, A. M., Cardoso, I., Carmo Pereira, M., Coelho, M. A. N., Joao Saraiva, M., Moehwald, H., and Brezesinski, G. (2010) Controlling amyloid-beta peptide(1-42) oligomerization and toxicity by fluorinated nanoparticles ChemBioChem 11, 1905-1913
53. Zhang, D., Neumann, O., Wang, H., Yuwono, V. M., Barhoumi, A., Perham, M., Hartgerink, J. D., Wittung-Stafshede, P., and Halas, N. J. (2009) Gold nanoparticles can induce the formation of protein-based aggregates at physiological pH Nano Lett. 9, 666-671
54. Rocha, S., Thueneman, A. F., Pereira, M. d. C., Coelho, M., Moehwald, H., and Brezesinski, G. (2008) Influence of fluorinated and hydrogenated nanoparticles on the structure and fibrillogenesis of amyloid beta-peptide Biophys. Chem. 137, 35-42
55. Bieschke, J., Herbst, M., Wiglenda, T., Friedrich, R. P., Boeddrich, A., Schiele, F., Kleckers, D., del Amo, J. M. L., Gruening, B. A., Wang, Q., Schmidt, M. R., Lurz, R., Anwyl, R., Schnoegl, S., Faendrich, M., Frank, R. F., Reif, B., Guenther, S., Walsh, D. M., and Wanker, E. E. (2012) Small-molecule conversion of toxic oligomers to nontoxic beta-sheet-rich amyloid fibrils Nat. Chem. Biol. 8, 93-101
56. 2 nanoparticles promote beta-amyloid fibrillation in vitro Biochem. Biophys. Res. Commun. 373, 315-318
57. Xiao, L., Zhao, D., Chan, W.-H., Choi, M. M. F., and Li, H.-W. (2010) Inhibition of beta 1-40 amyloid fibrillation with N -acetyl- l -cysteine capped quantum dots Biomaterials 31, 91-98
58. Brambilla, D., Verpillot, R., Le Droumaguet, B., Nicolas, J., Taverna, M., Kóňa, J., Lettiero, B., Hashemi, S. H., De Kimpe, L., Canovi, M., Gobbi, M., Nicolas, V., Scheper, W., Moghimi, S. M., Tvaroška, I., Couvreur, P., and Andrieux, K. (2012) PEGylated nanoparticles bind to and alter amyloid-beta peptide conformation: Toward engineering of functional nanomedicines for Alzheimer's disease ACS Nano 6, 5897-5908
59. Palmacci, S., Josephson, L., and Groman, E. Synthesis of polysaccharide covered superparamagnetic oxide colloids, U.S. Patent 9505669, 1995.
60. El-Dakdouki, M. H., Zhu, D. C., El-boubbou, K., Kamat, M., Chen, J., Li, W., and Huang, X. (2012) Development of multifunctional hyaluronan-coated nanoparticles for imaging and drug delivery to cancer cells Biomacromolecules 13, 1144-1151
61. Kamat, M., El-boubbou, K., Zhu, D., Lansdell, T., Lu, X., Li, W., and Huang, X. (2010) Hyaluronic acid immobilized magnetic nanoparticles for active targeting and imaging of macrophages Bioconjugate Chem. 21, 2128-2135
62. El-Boubbou, K., Zhu, D. C., Vasileiou, C., Borhan, B., Prosperi, D., Li, W., and Huang, X. (2010) Magnetic glyco-nanoparticles: A tool to detect, differentiate, and unlock the glyco-codes of cancer via magnetic resonance imaging J. Am. Chem. Soc. 132, 4490-4499
63. Wang, Y., El-Boubbou, K., Kouyoumdjian, H., Sun, B., Huang, X., and Zeng, X. (2010) Lipoic acid glyco-conjugates, a new class of agents for controlling nonspecific adsorption of blood serum at biointerfaces for biosensor and biomedical applications Langmuir 26, 4119-4125
64. Roher, A. E., Lowenson, J. D., Clarke, S., Woods, A. S., Cotter, R. J., Gowing, E., and Ball, M. J. (1993) Beta-amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: Implications for the pathology of Alzheimer disease Proc. Natl. Acad. Sci. U.S.A. 90, 10836-10840
65. García-Matas, S., de Vera, N., Aznar, A. O., Marimon, J. M., Adell, A., Planas, A. M., Cristòfol, R., and Sanfeliu, C. (2010) In vitro and in vivo activation of astrocytes by amyloid-beta is potentiated by pro-oxidant agents J. Alzheimer's Dis. 20, 229-245
66. Allaman, I., Gavillet, M., Bélanger, M., Laroche, T., Viertl, D., Lashuel, H. A., and Magistretti, P. J. (2010) Amyloid-beta aggregates cause alterations of astrocytic metabolic phenotype: impact on neuronal viability J. Neurosci. 30, 3326-3338
67. LeVine, H. (1999) Quantification of β-sheet amyloid fibril structures with Thioflavin T Methods Enzymol. 309, 274-284
68. 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
69. Moores, B., Drolle, E., Attwood, S. J., Simons, J., and Leonenko, Z. (2011) Effect of surfaces on amyloid fibril formation PLoS One 6, e25954
70. Inbar, P., Bautista, M. R., Takayama, S. A., and Yang, J. (2008) Assay to screen for molecules that associate with Alzheimer's related beta-amyloid fibrils Anal. Chem. 80, 3502-3506
71. Inbar, P. and Yang, J. (2006) Inhibiting protein-amyloid interactions with small molecules: A surface chemistry approach Bioorg. Med. Chem. Lett. 16, 1076-1079
72. Inbar, P., Li, C. Q., Takayama, S. A., Bautista, M. R., and Yang, J. (2006) Oligo(ethylene glycol) derivatives of Thioflavin T as inhibitors of protein-amyloid interactions ChemBioChem 7, 1563-1566
73. Fraser, P. E., Darabie, A. A., and McLaurin, J. (2001) Amyloid-beta interactions with chondroitin sulfate-derived monosaccharides and disaccharides-Implications for drug development J. Biol. Chem. 276, 6412-6419
74. Bohrmann, B., Tjernberg, L., Kuner, P., Poli, S., Levet-Trafit, B., Naslund, J., Richards, G., Huber, W., Dobeli, H., and Nordstedt, C. (1999) Endogenous proteins controlling amyloid beta-peptide polymerization-Possible implications for beta-amyloid formation in the central nervous system and in peripheral tissues J. Biol. Chem. 274, 15990-15995
75. Jun, Y. W., Lee, J. H., and Cheon, J. (2008) Chemical design of nanoparticle probes for high-performance magnetic resonance imaging Angew. Chem., Int. Ed. 47, 5122-5135
76. Na, H. B., Song, I. C., and Hyeon, T. (2009) Inorganic nanoparticles for MRI contrast agents Adv. Mater. 21, 2133-2148
77. Roch, A., Gossuin, Y., Muller, R. N., and Gillis, P. (2005) Superparamagnetic colloid suspensions: Water magnetic relaxation and clustering J. Magn. Magn. Mater. 293, 532-539
78. Yung, K. T. (2003) Empirical models of transverse relaxation for spherical magnetic perturbers Magn. Reson. Imaging 21, 451-463
79. Lee, H., Sun, E., Ham, D., and Weissleder, R. (2008) Chip-NMR biosensor for detection and molecular analysis of cells Nat. Med. 14, 869-874
80. Koh, I., Hong, R., Weissleder, R., and Josephson, L. (2008) Sensitive NMR sensors detect antibodies to influenza Angew. Chem., Int. Ed. 47, 4119-4121
81. Walsh, D., Lomakin, A., Benedek, G., Condron, M., and Teplow, D. (1997) Amyloid β-protein fibrillogenesis: Detection of a protofibrillar intermediate J. Biol. Chem. 272, 22364-22372
82. Bravo, R., Arimon, M., Valle-Delgado, J. J., García, R., Durany, N., Castel, S., Cruz, M., Ventura, S., and Fernàndez-Busquets, X. (2008) Sulfated polysaccharides promote the assembly of amyloid beta(1-42) peptide into stable fibrils of reduced cytotoxicity J. Biol. Chem. 283, 32471-32483
83. Teplow, D. B. Amyloid, Prions, and Other Protein Aggregates, Part C. In Methods in Enzymology; Academic Press: San Diego, 2006; Vol., 413, pp 20 - 33.
84. Bitan, G. and Teplow, D. B. (2005) Preparation of aggregate-free, low molecular weight amyloid-beta for assembly and toxicity assays Methods Mol. Biol. 299, 3-9
85. Lesne, S., Koh, M. T., Kotilinek, L., Kayed, R., Glabe, C. G., Yang, A., Gallagher, M., and Ashe, K. H. (2006) A specific amyloid-beta protein assembly in the brain impairs memory Nature 440, 352-357
86. 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-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory Nat. Med. 14, 837-842
87. Klein, W. L., Krafft, G. A., and Finch, C. E. (2001) Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci. 24, 219-224
88. Temsamani, J. and Vidal, P. (2004) The use of cell-penetrating peptides for drug delivery Drug Discovery Today 9, 1012-1019
89. Silva, G. A. (2008) Nanotechnology approaches to crossing the blood-brain barrier and drug delivery to the CNS BMC Neurosci. 9 (Suppl 3) S4