Table of Contents Author Guidelines Submit a Manuscript
International Journal of Alzheimer’s Disease
Volume 2018, Article ID 7608038, 12 pages
https://doi.org/10.1155/2018/7608038
Research Article

Oil Palm Phenolics Inhibit the In Vitro Aggregation of β-Amyloid Peptide into Oligomeric Complexes

1Biomaterials Science and Engineering Laboratory, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
2Malaysian Palm Oil Board, No. 6, Persiaran Institusi, Bandar Baru Bangi, 43000 Kajang, Selangor, Malaysia
3Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA

Correspondence should be addressed to ChoKyun Rha; ude.tim@ahrkc

Received 17 August 2017; Revised 23 November 2017; Accepted 7 December 2017; Published 31 January 2018

Academic Editor: Francesco Panza

Copyright © 2018 Robert P. Weinberg et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Wetzel, “Kinetics and thermodynamics of amyloid fibril assembly,” Accounts of Chemical Research, vol. 39, no. 9, pp. 671–679, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. A. M. Morris, M. A. Watzky, and R. G. Finke, “Protein aggregation kinetics, mechanism, and curve-fitting: A review of the literature,” Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, vol. 1794, no. 3, pp. 375–397, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. R. M. Murphy, “Kinetics of amyloid formation and membrane interaction with amyloidogenic proteins,” Biochimica et Biophysica Acta (BBA) - Biomembranes, vol. 1768, no. 8, pp. 1923–1934, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Frieden, “Protein aggregation processes: In search of the mechanism,” Protein Science, vol. 16, no. 11, pp. 2334–2344, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. S. I. A. Cohen, M. Vendruscolo, C. M. Dobson, and T. P. J. Knowles, “From macroscopic measurements to microscopic mechanisms of protein aggregation,” Journal of Molecular Biology, vol. 421, no. 2-3, pp. 160–171, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. D. J. Selkoe, “The molecular pathology of Alzheimer's disease,” Neuron, vol. 6, no. 4, pp. 487–498, 1991. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Hardy, “The Alzheimer family of diseases: Many etiologies, one pathogenesis?” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 94, no. 6, pp. 2095–2097, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. D. M. Holtzman, J. C. Morris, and A. M. Goate, “Alzheimers disease: the challenge of the second century,” Science Translational Medicine, vol. 3, 2011. View at Google Scholar
  9. I. Hajimohammadreza, V. E. R. Anderson, J. B. Cavanagh et al., “β-amyloid precursor protein fragments and lysosomal dense bodies are found in rat brain neurons after ventricular infusion of leupeptin,” Brain Research, vol. 640, no. 1-2, pp. 25–32, 1994. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Waelter, A. Boeddrich, R. Lurz et al., “Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation,” Molecular Biology of the Cell (MBoC), vol. 12, no. 5, pp. 1393–1407, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Bucciantini, E. Giannoni, F. Chiti et al., “Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases,” Nature, vol. 416, no. 6880, pp. 507–511, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. J. Bendiske and B. A. Bahr, “Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis—an approach for slowing alzheimer disease?” Journal of Neuropathology & Experimental Neurology, vol. 62, no. 5, pp. 451–463, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. D. M. Walsh and D. J. Selkoe, “Aβ oligomers: a decade of discovery,” Journal of Neurochemistry, vol. 101, no. 5, pp. 1172–1184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. S. T. Ferreira, M. N. N. Vieira, and F. G. De Felice, “Soluble protein oligomers as emerging toxins in Alzheimer's and other amyloid diseases,” IUBMB Life, vol. 59, no. 4-5, pp. 332–345, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Monsellier and F. Chiti, “Prevention of amyloid-like aggregation as a driving force of protein evolution,” EMBO Reports, vol. 8, no. 8, pp. 737–742, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Eisenberg and M. Jucker, “The amyloid state of proteins in human diseases,” Cell, vol. 148, no. 6, pp. 1188–1203, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. G. G. Glenner and C. W. Wong, “Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein,” Biochemical and Biophysical Research Communications, vol. 122, no. 3, pp. 1131–1135, 1984. View at Publisher · View at Google Scholar · View at Scopus
  18. T. L. S. Benzinger, D. M. Gregory, T. S. Burkoth et al., “Propagating structure of Alzheimer's β-amyloid((10-35)) is parallel β- sheet with residues in exact register,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 95, no. 23, pp. 13407–13412, 1998. View at Publisher · View at Google Scholar · View at Scopus
  19. O. N. Antzutkin, R. D. Leapman, J. J. Balbach, and R. Tycko, “Supramolecular structural constraints on Alzheimer's β-amyloid fibrils from electron microscopy and solid-state nuclear magnetic resonance,” Biochemistry, vol. 41, no. 51, pp. 15436–15450, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. J. J. Balbach, A. T. Petkova, N. A. Oyler et al., “Supramolecular structure in full-length Alzheimer's β-amyloid fibrils: Evidence for a parallel β-sheet organization from solid-state nuclear magnetic resonance,” Biophysical Journal, vol. 83, no. 2, pp. 1205–1216, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Török, S. Milton, R. Kayed et al., “Structural and dynamic features of Alzheimer's Aβ peptide in amyloid fibrils studied by site-directed spin labeling,” The Journal of Biological Chemistry, vol. 277, no. 43, pp. 40810–40815, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Der-Sarkissiant, C. C. Jao, J. Chen, and R. Langen, “Structural organization of α-synuclein fibrils studied by site-directed spin labeling,” The Journal of Biological Chemistry, vol. 278, no. 39, pp. 37530–37535, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. L. C. Serpell, M. Sunde, and C. C. Blake, “The molecular basis of amyloidosis,” Cellular and Molecular Life Sciences, vol. 53, no. 12, p. 871. View at Publisher · View at Google Scholar
  24. R. Kodali and R. Wetzel, “Polymorphism in the intermediates and products of amyloid assembly,” Current Opinion in Structural Biology, vol. 17, no. 1, pp. 48–57, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. O. S. Makin and L. C. Serpell, “Structures for amyloid fibrils,” FEBS Journal, vol. 272, no. 23, pp. 5950–5961, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Margittai and R. Langen, “Fibrils with parallel in-register structure constitute a major class of amyloid fibrils: Molecular insights from electron paramagnetic resonance spectroscopy,” Quarterly Reviews of Biophysics, vol. 41, no. 3-4, pp. 265–297, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. B. L. Kagan, Y. Hirakura, R. Azimov, R. Azimova, and M.-C. Lin, “The channel hypothesis of Alzheimer's disease: Current status,” Peptides, vol. 23, no. 7, pp. 1311–1315, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. B. Caughey and P. T. Lansbury Jr., “Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders,” Annual Review of Neuroscience, vol. 26, pp. 267–298, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. M. P. Mattson, “Oxidative stress, perturbed calcium homeostasis, and immune dysfunction in Alzheimer's disease,” Journal of NeuroVirology, vol. 8, no. 6, pp. 539–550, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Kaltschmidt, M. Uherek, B. Volk, P. A. Baeuerle, and C. Kaltschmidt, “Transcription factor NF-κB is activated in primary neurons by amyloid β peptides and in neurons surrounding early plaques from patients with Alzheimer disease,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 94, no. 6, pp. 2642–2647, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. W. R. Markesbery and J. M. Carney, “Oxidative alterations in Alzheimer's disease,” Brain Pathology, vol. 9, no. 1, pp. 133–146, 1999. View at Google Scholar · View at Scopus
  32. J. Josepha, B. Shukitt-Hale, N. A. Denisova, A. Martin, G. Perry, and M. A. Smith, “Copernicus revisited: Amyloid beta in Alzheimer's disease,” Neurobiology of Aging, vol. 22, no. 1, pp. 131–146, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Behl and B. Moosmann, “Antioxidant neuroprotection in Alzheimer's disease as preventive and therapeutic approach,” Free Radical Biology & Medicine, vol. 33, no. 2, pp. 182–191, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. P. L. McGeer and E. G. McGeer, “Anti-inflammatory drugs in the fight against Alzheimer's disease,” Annals of the New York Academy of Sciences, vol. 777, pp. 213–220, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. R. D. Terry, E. Masliah, and L. A. Hansen, “The neuropathology of Alzheimer disease and the structural basis of its cognitive alterations,” in Alzheimer Disease, R. D. Terry, R. Katzman, K. L. Bick, and., and S. S. Sisodia, Eds., pp. 187–206, Lippincott Williams and Wilkins, Philadelphia, Penn, USA, 1999. View at Google Scholar
  36. C. L. Masters, G. Simms, N. A. Weinman, G. Multhaup, B. L. McDonald, and K. Beyreuther, “Amyloid plaque core protein in Alzheimer disease and Down syndrome,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 82, no. 12, pp. 4245–4249, 1985. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Wisniewski, M. Lalowski, E. Levy, M. R. F. Marques, and B. Frangione, “The amino acid sequence of neuritic plaque amyloid from a familial Alzheimer's disease patient,” Annals of Neurology, vol. 35, no. 2, pp. 245-246, 1994. View at Publisher · View at Google Scholar · View at Scopus
  38. C. W. Wong, V. Quaranta, and G. G. Glenner, “Neuritic plaques and cerebrovascular amyloid in Alzheimer disease are antigenically related.,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 82, no. 24, pp. 8729–8732, 1985. View at Publisher · View at Google Scholar
  39. D. L. Miller, I. A. Papayannopoulos, J. Styles et al., “Peptide compositions of the cerebrovascular and senile plaque core amyloid deposits of Alzheimer's disease,” Archives of Biochemistry and Biophysics, vol. 301, no. 1, pp. 41–52, 1993. View at Publisher · View at Google Scholar · View at Scopus
  40. D. J. Selkoe, C. R. Abraham, M. B. Podlisny, and L. K. Duffy, “Isolation of Low‐Molecular‐Weight Proteins from Amyloid Plaque Fibers in Alzheimer's Disease,” Journal of Neurochemistry, vol. 46, no. 6, pp. 1820–1834, 1986. View at Publisher · View at Google Scholar · View at Scopus
  41. D. J. Selkoe, “Alzheimers disease: genes, proteins, and therapy,” Physiological Reviews, vol. 81, pp. 741–766, 2001. View at Google Scholar
  42. C. B. Andersen, H. Yagi, M. Manno et al., “Branching in amyloid fibril growth,” Biophysical Journal, vol. 96, no. 4, pp. 1529–1536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. T. P. J. Knowles, D. A. White, A. R. Abate et al., “Observation of spatial propagation of amyloid assembly from single nuclei,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 108, no. 36, pp. 14746–14751, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Ferrone, “Analysis of protein aggregation kinetics,” Methods in Enzymology, vol. 309, pp. 256–274, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. T. P. J. Knowles, C. A. Waudby, G. L. Devlin et al., “An analytical solution to the kinetics of breakable filament assembly,” Science, vol. 326, no. 5959, pp. 1533–1537, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. S. I. A. Cohen, M. Vendruscolo, M. E. Welland, C. M. Dobson, E. M. Terentjev, and T. P. J. Knowles, “Nucleated polymerization with secondary pathways. I. Time evolution of the principal moments,” The Journal of Chemical Physics, vol. 135, no. 6, article 065105, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. S. I. A. Cohen, M. Vendruscolo, C. M. Dobson, and T. P. J. Knowles, “Nucleated polymerisation in the presence of pre-formed seed filaments,” International Journal of Molecular Sciences, vol. 12, no. 9, pp. 5844–5852, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. S. B. Padrick and A. D. Miranker, “Islet amyloid: phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis,” Biochemistry, vol. 41, no. 14, pp. 4694–4703, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. F. A. Ferrone, J. Hofrichter, H. R. Sunshine, and W. A. Eaton, “Kinetic studies on photolysis-induced gelation of sickle cell hemoglobin suggest a new mechanism,” Biophysical Journal, vol. 32, no. 1, pp. 361–380, 1980. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Medkour, F. Ferrone, F. Galactéros, and P. Hannaert, “The double nucleation model for sickle cell haemoglobin polymerization: Full integration and comparison with experimental data,” Acta Biotheoretica, vol. 56, no. 1-2, pp. 103–122, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. A. M. Ruschak and A. D. Miranker, “Fiber-dependent amyloid formation as catalysis of an existing reaction pathway,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 104, no. 30, pp. 12341–12346, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. C. J. Roberts, “Non-native protein aggregation kinetics,” Biotechnology and Bioengineering, vol. 98, no. 5, pp. 927–938, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. J. M. Andrews and C. J. Roberts, “A Lumry-Eyring nucleated polymerization model of protein aggregation kinetics: 1. Aggregation with pre-equilibrated unfolding,” The Journal of Physical Chemistry B, vol. 111, no. 27, pp. 7897–7913, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. R. Wetzel, “For protein misassembly, it's the 'I' decade,” Cell, vol. 86, no. 5, pp. 699–702, 1996. View at Publisher · View at Google Scholar · View at Scopus
  55. D. R. Booth, M. Sunde, V. Bellotti et al., “Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis,” Nature, vol. 385, no. 6619, pp. 787–793, 1997. View at Publisher · View at Google Scholar · View at Scopus
  56. F. Chiti, P. Webster, N. Taddei et al., “Designing conditions for in vitro formation of amyloid protofilaments and fibrils,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 96, no. 7, pp. 3590–3594, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. D. Canet, M. Sunde, A. M. Last et al., “Mechanistic studies of the folding of human lysozyme and the origin of amyloidogenic behavior in its disease-related variants,” Biochemistry, vol. 38, no. 20, pp. 6419–6427, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. L. A. Morozova-Roche, J. Zurdo, A. Spencer et al., “Amyloid fibril formation and seeding by wild-type human lysozyme and its disease-related mutational variants,” Journal of Structural Biology, vol. 130, no. 2-3, pp. 339–351, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. J. D. Harper and P. T. Lansbury Jr., “Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins,” Annual Review of Biochemistry, vol. 66, pp. 385–407, 1997. View at Publisher · View at Google Scholar · View at Scopus
  60. L. C. Serpell, M. Sunde, and C. C. Blake, “The molecular basis of amyloidosis,” Cellular and Molecular Life Sciences, vol. 53, no. 12, pp. 871–887. View at Publisher · View at Google Scholar
  61. M. Sunde, L. C. Serpell, M. Bartlam, P. E. Fraser, M. B. Pepys, and C. C. F. Blake, “Common core structure of amyloid fibrils by synchrotron X-ray diffraction,” Journal of Molecular Biology, vol. 273, no. 3, pp. 729–739, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Moniatte, F. G. Van Der Goot, J. T. Buckley, F. Pattus, and A. Van Dorsselaer, “Characterisation of the heptameric pore-forming complex of the Aeromonas toxin aerolysin using MALDI-TOF mass spectrometry,” FEBS Letters, vol. 384, no. 3, pp. 269–272, 1996. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Bleiholder, N. F. Dupuis, T. Wyttenbach, and M. T. Bowers, “Ion mobilityg-mass spectrometry reveals a conformational conversion from random assembly to β-sheet in amyloid fibril formation,” Nature Chemistry, vol. 3, no. 2, pp. 172–177, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. R. Beveridge, Q. Chappuis, C. Macphee, and P. Barran, “Mass spectrometry methods for intrinsically disordered proteins.,” Analyst, vol. 138, no. 1, pp. 32–42, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. H. LeVine III, “4,4-dianilino-1,1-binaphthyl-5,5-disulfonate: Report on non-β-sheet conformers of Alzheimer's peptide β(1-40),” Archives of Biochemistry and Biophysics, vol. 404, no. 1, pp. 106–115, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. H. LeVine, “Thioflavine T interaction with synthetic Alzheimer's disease β-amyloid peptides: detection of amyloid aggregation in solution,” Protein Science, vol. 2, no. 3, pp. 404–410, 1993. View at Google Scholar · View at Scopus
  67. D. Burdick, B. Soreghan, M. Kwon et al., “Assembly and aggregation properties of synthetic Alzheimer's A4/β amyloid peptide analogs,” The Journal of Biological Chemistry, vol. 267, no. 1, pp. 546–554, 1992. View at Google Scholar · View at Scopus
  68. J. D. Harper, C. M. Lieber, and P. T. Lansbury Jr., “Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-β protein,” Chemistry & Biology, vol. 4, no. 12, pp. 951–959, 1997. View at Publisher · View at Google Scholar · View at Scopus
  69. J. D. Harper, S. S. Wong, C. M. Lieber, and P. T. Lansbury Jr., “Observation of metastable Aβ amyloid protofibrils by atomic force microscopy,” Chemistry & Biology, vol. 4, no. 2, pp. 119–125, 1997. View at Publisher · View at Google Scholar · View at Scopus
  70. C. Hilbich, B. Kisters-Woike, J. Reed, C. L. Masters, and K. Beyreuther, “Aggregation and secondary structure of synthetic amyloid βA4 peptides of Alzheimer's disease,” Journal of Molecular Biology, vol. 218, no. 1, pp. 149–163, 1991. View at Publisher · View at Google Scholar · View at Scopus
  71. B. Soreghan, J. Kosmoski, and C. Glabe, “Surfactant properties of Alzheimer's Aβ peptides and the mechanism of amyloid aggregation,” The Journal of Biological Chemistry, vol. 269, no. 46, pp. 28551–28554, 1994. View at Google Scholar · View at Scopus
  72. W. Garzon-Rodriguez, M. Sepulveda-Becerra, S. Milton, and C. G. Glabe, “Soluble amyloid Aβ-(1-40) exists as a stable dimer at low concentrations,” The Journal of Biological Chemistry, vol. 272, no. 34, pp. 21037–21044, 1997. View at Publisher · View at Google Scholar · View at Scopus
  73. W. Garzon-Rodriguez, A. Vega, M. Sepulveda-Becerra et al., “A conformation change in the carboxyl terminus of Alzheimer's Aβ(1-40) accompanies the transition from dimer to fibril as revealed by fluorescence quenching analysis,” The Journal of Biological Chemistry, vol. 275, no. 30, pp. 22645–22649, 2000. View at Publisher · View at Google Scholar · View at Scopus
  74. D. M. Walsh, A. Lomakin, G. B. Benedek, M. M. Condron, and D. B. Teplow, “Amyloid β-protein fibrillogenesis. Detection of a protofibrillar intermediate,” The Journal of Biological Chemistry, vol. 272, no. 35, pp. 22364–22372, 1997. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Kamihira, A. Naito, S. Tuzi, A. Y. Nosaka, and H. Saitô, “Conformational transitions and fibrillation mechanism of human calcitonin as studied by high-resolution solid-state 13C NMR,” Protein Science, vol. 9, no. 5, pp. 867–877, 2000. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Anguiano, R. J. Nowak, and P. T. Lansbury Jr., “Protofibrillar islet amyloid polypeptide permeabilizes synthetic vesicles by a pore-like mechanism that may be relevant to type II diabetes,” Biochemistry, vol. 41, no. 38, pp. 11338–11343, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. H. A. Lashuel, D. Hartley, B. M. Petre, T. Walz, and P. T. Lansbury Jr., “Neurodegenerative disease: amyloid pores from pathogenic mutations,” Nature, vol. 418, no. 6895, p. 291, 2002. View at Google Scholar · View at Scopus
  78. D. M. Hartley, D. M. Walsh, C. P. Ye et al., “Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons,” The Journal of Neuroscience, vol. 19, no. 20, pp. 8876–8884, 1999. View at Google Scholar · View at Scopus
  79. A. Lomakin, D. B. Teplow, D. A. Kirschner, and G. B. Benedeki, “Kinetic theory of fibrillogenesis of amyloid β-protein,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 94, no. 15, pp. 7942–7947, 1997. View at Publisher · View at Google Scholar · View at Scopus
  80. R. Kayed, E. Head, J. L. Thompson et al., “Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis,” Science, vol. 300, no. 5618, pp. 486–489, 2003. View at Publisher · View at Google Scholar · View at Scopus
  81. Y. Gong, L. Chang, K. L. Viola et al., “Alzheimer's disease-affected brain: Presence of oligomeric Aβ ligands (ADDLs) suggests a molecular basis for reversible memory loss,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 100, no. 18, pp. 10417–10422, 2003. View at Publisher · View at Google Scholar · View at Scopus
  82. Y.-M. Kuo, M. R. Emmerling, C. Vigo-Pelfrey et al., “Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer disease brains,” The Journal of Biological Chemistry, vol. 271, no. 8, pp. 4077–4081, 1996. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Pitschke, R. Prior, M. Haupt, and D. Riesner, “Detection of single amyloid β-protein aggregates in the cerebrospinal fluid of Alzheirner's patients by fluorescence correlation spectroscopy,” Nature Medicine, vol. 4, no. 7, pp. 832–834, 1998. View at Publisher · View at Google Scholar · View at Scopus
  84. L.-F. Lue, Y.-M. Kuo, A. E. Roher et al., “Soluble amyloid β peptide concentration as a predictor of synaptic change in Alzheimer's disease,” The American Journal of Pathology, vol. 155, no. 3, pp. 853–862, 1999. View at Publisher · View at Google Scholar · View at Scopus
  85. C. A. McLean, R. A. Cherny, F. W. Fraser et al., “Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease,” Annals of Neurology, vol. 46, no. 6, pp. 860–866, 1999. View at Publisher · View at Google Scholar · View at Scopus
  86. W. L. Klein, G. A. Krafft, and C. E. Finch, “Targeting small Aβ oligomers: the solution to an Alzheimer's disease conundrum?” Trends in Neurosciences, vol. 24, no. 4, pp. 219–224, 2001. View at Publisher · View at Google Scholar · View at Scopus
  87. A. Y. Hsia, E. Masliah, L. McConlogue et al., “Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 96, no. 6, pp. 3228–3233, 1999. View at Publisher · View at Google Scholar · View at Scopus
  88. J. Hardy and D. J. Selkoe, “The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics,” Science, vol. 297, no. 5580, pp. 353–356, 2002. View at Publisher · View at Google Scholar · View at Scopus
  89. M. A. Westerman, D. Cooper-Blacketer, A. Mariash et al., “The relationship between Aβ and memory in the Tg2576 mouse model of Alzheimer's disease,” The Journal of Neuroscience, vol. 22, no. 5, pp. 1858–1867, 2002. View at Google Scholar · View at Scopus
  90. D. M. Walsh, I. Klyubin, J. V. Fadeeva, M. J. Rowan, and D. J. Selkoe, “Amyloid-β oligomers: their production, toxicity and therapeutic inhibition,” Biochemical Society Transactions, vol. 30, no. 4, pp. 552–557, 2002. View at Publisher · View at Google Scholar · View at Scopus
  91. M. D. Kirkitadze, G. Bitan, and D. B. Teplow, “Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies,” Journal of Neuroscience Research, vol. 69, no. 5, pp. 567–577, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. R. Sambanthamurthi, Y. Tan, K. Sundram et al., “Oil palm vegetation liquor: A new source of phenolic bioactives,” British Journal of Nutrition, vol. 106, no. 11, pp. 1655–1663, 2011. View at Publisher · View at Google Scholar · View at Scopus
  93. U.S. Patent No. 7,387,802 issued in 2008.
  94. Z. Ganim, S. C. Hoi, A. W. Smith, L. P. Deflores, K. C. Jones, and A. Tokmakoff, “Amide I two-dimensional infrared spectroscopy of proteins,” Accounts of Chemical Research, vol. 41, no. 3, pp. 432–441, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. H. S. Chung, M. Khalil, and A. Tokmakoff, “Protein denaturing studied with 2D IR and vibrational echo spectroscopy: Equilibrium and temperature-jump measurements,” Biophysical Journal, pp. 526a–526a, 2004. View at Google Scholar
  96. H. S. Chung and A. Tokmakoff, “Visualization and characterization of the infrared active amide i vibrations of proteins,” The Journal of Physical Chemistry B, vol. 110, no. 6, pp. 2888–2898, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. N. Demirdöven, C. M. Cheatum, H. S. Chung, M. Khalil, J. Knoester, and A. Tokmakoff, “Two-dimensional infrared spectroscopy of antiparallel β-sheet secondary structure,” Journal of the American Chemical Society, vol. 126, no. 25, pp. 7981–7990, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Khalil, N. Demirdöven, and A. Tokmakoff, “Coherent 2D IR spectroscopy: Molecular structure and dynamics in solution,” The Journal of Physical Chemistry A, vol. 107, no. 27, pp. 5258–5279, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. J. T. Edward, “Molecular volumes and the Stokes-Einstein equation,” Journal of Chemical Education, vol. 47, no. 4, pp. 261–270, 1970. View at Publisher · View at Google Scholar · View at Scopus
  100. B. S. Johnson, J. M. McCaffery, S. Lindquist, and A. D. Gitler, “A yeast TDP-43 proteinopathy model: Exploring the molecular determinants of TDP-43 aggregation and cellular toxicity,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 105, no. 17, pp. 6439–6444, 2008. View at Publisher · View at Google Scholar · View at Scopus
  101. S. Krobitsch and S. Lindquist, “Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 97, no. 4, pp. 1589–1594, 2000. View at Publisher · View at Google Scholar · View at Scopus
  102. S. Treusch, S. Hamamichi, J. L. Goodman et al., “Functional links between Aβ toxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast,” Science, vol. 334, no. 6060, pp. 1241–1245, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. D. F. Tardiff, M. L. Tucci, K. A. Caldwell, G. A. Caldwell, and S. Lindquist, “Different 8-hydroxyquinolines protect models of TDP-43 protein, α-synuclein, and polyglutamine proteotoxicity through distinct mechanisms,” The Journal of Biological Chemistry, vol. 287, no. 6, pp. 4107–4120, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. J.-C. Dodart, K. R. Bales, K. S. Gannon et al., “Immunization reverses memory deficits without reducing brain Aβ burden in Alzheimer's disease model,” Nature Neuroscience, vol. 5, no. 5, pp. 452–457, 2002. View at Publisher · View at Google Scholar · View at Scopus
  105. I. Klyubin, D. M. Walsh, C. A. Lemere et al., “Amyloid β protein immunotherapy neutralizes Aβ oligomers that disrupt synaptic plasticity in vivo,” Nature Medicine, vol. 11, no. 5, pp. 556–561, 2005. View at Publisher · View at Google Scholar · View at Scopus