Rapid assembly of amyloid-β peptide at a liquid/liquid interface produces unstable β-sheet fibers

Biochemistry

Volumn 44, Issue 1, 2005, Pages 165-173

  Nichols, Michael R ^a,c   Moss, Melissa A ^a,d   Reed, Dana Kim ^a   Hoh, Jan H ^b   Rosenberry, Terrone L ^a  

^a MAYO CLINIC   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^d University of South Carolina   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; ATOMIC FORCE MICROSCOPY; BRAIN; DISEASE CONTROL; FLUORESCENCE; HYDROPHOBICITY; INTERFACES (MATERIALS); MORPHOLOGY; SELF ASSEMBLY;

AQUEOUS BUFFER; GLOBULES; INSOLUBLE FIBRILS; MOLECULAR LEVEL;

PATHOLOGY;

AMYLOID BETA PROTEIN; BUFFER; CHLOROFORM; THIOFLAVINE;

ARTICLE; ATOMIC FORCE MICROSCOPY; BETA SHEET; CIRCULAR DICHROISM; FLUORESCENCE; LIQUID LIQUID EXTRACTION; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; BINDING SITES; FREEZE DRYING; HUMANS; KINETICS; MICROSCOPY, ATOMIC FORCE; PROTEIN STRUCTURE, SECONDARY;

EID: 11844249291     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048846t     Document Type: Article

References (57)

1. Selkoe, D. J. (1994) Normal and abnormal biology of the β-amyloid precursor protein, Annu. Rev. Neurosci. 17, 489-517.
2. Shoji, M., Golde, T. E., Ghiso, J., Cheung, T. T., Estus, S., Shaffer, L. M., Cai, X. D., McKay, D. M., Tintner, R., Frangione, B., and Younkin, S. G. (1992) Production of the Alzheimer amyloid β protein by normal proteolytic processing, Science 258, 126-129.
3. Seubert, P., Vigo-Pelfrey, C., Esch, F., Lee, M., Dovey, H., Davis, D., Sinha, S., Schlossmacher, M., Whaley, J., Swindlehurst, C., McCormack, R., Wolfert, R., Selkoe, D. J., Lieberberg, I., and Schenk, D. (1992) Isolation and quantification of soluble Alzheimer's β-peptide from biological fluids, Nature 359, 325-327.
4. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics, Science 297, 353-356.
5. Selkoe, D. J., and Podlisny, M. B. (2002) Deciphering the genetic basis of Alzheimer's disease, Annu. Rev. Genomics Hum. Genet. 3, 67-99.
6. Nilsberth, C., Westlind-Danielsson, A., Eckman, C. B., Condron, M. M., Axelman, K., Forsell, C., Stenh, C., Luthman, J., Teplow, D. B., Younkin, S. G., Naslund, J., and Lannfelt, L. (2001) The "Artic" APP mutation (E693G) causes Alzheimer's disease by enhanced Aβ protofibril formation, Nat. Neurosci. 4, 887-893.
7. Kirschner, D. A., Inouye, H., Duffy, L. K., Sinclair, A., Lind, M., and Selkoe, D. J. (1987) Synthetic peptide homologous to β protein from Alzheimer disease forms amyloid-like fibrils in vitro, Proc. Natl. Acad. Sci. U.S.A. 84, 6953-6957.
8. Jarrett, J. T., and Lansbury, P. T., Jr. (1993) Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie?, Cell 73, 1055-1058.
9. Harper, J. D., Wong, S. S., Lieber, C. M., and Lansbury, P. T., Jr. (1999) Assembly of Aβ amyloid peptides: An in vitro model for a possible early event in Alzheimer's disease, Biochemistry 38, 8972-8980.
10. 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.
11. Jarrett, J. T., Berger, E. P., and Lansbury, P. T., Jr. (1993) The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease, Biochemistry 32, 4693-4697.
12. 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.
13. Sikorski, P., Atkins, E. D., and Serpell, L. C. (2003) Structure and texture of fibrous crystals formed by Alzheimer's Aβ(11-25) peptide fragment, Structure (Cambridge) 11, 915-926.
14. Petkova, A. T., Tshii, Y., Balbach, J. J., Antzutkin, O. N., Leapman, R. D., Delaglio, F., and Tycko, R. (2002) A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid-state NMR, Proc. Natl. Acad. Sci. U.S.A. 99, 16742-16747.
15. Kraus, M., Bienert, M., and Krause, E. (2003) Hydrogen exchange studies on Alzheimer's amyloid-β peptides by mass spectrometry using matrix-assisted laser desorption/ionization and electrospray ionization, Rapid Commun. Mass. Spectrom. 17, 222-228.
16. Kheterpal, I., Zhou, S., Cook, K. D., and Wetzel, R. (2000) Aβ amyloid fibrils possess a core structure highly resistant to hydrogen exchange, Proc. Natl. Acad. Sci. U.S.A. 97, 13597-13601.
17. Tjernberg, L. O., Naslund, J., Lindqvist, F., Johansson, J., Karlstrom, 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.
18. Nichols, M. R., Moss, M. A., Reed, D. K., Lin, W.-L., Mukhopadhyay, R., Hoh, J. H., and Rosenberry, T. L. (2002) Growth of β-amyloid(1-40) protofibrils by monomer elongation and lateral association. Characterization of distinct products by light scattering and atomic force microscopy, Biochemistry 41, 6115-6127.
19. 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 quantification of rate constants, Proc. Natl. Acad. Sci. U.S.A. 93, 1125-1129.
20. Tjernberg, L. O., Pramanik, A., Bjorling, S., Thyberg, P., Thyberg, J., Nordstedt, C., Berndt, K. D., Terenius, L., and Rigler, R. (1999) Amyloid β-peptide polymerization studied using fluorescence correlation spectroscopy, Chem. Biol. 6, 53-62.
21. Yong, W., Lomakin, A., Kirkitadze, M. D., Teplow, D. B., Chen, S. H., and Benedek, G. B. (2001) 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.
22. Soreghan, B., Kosmoski, J., and Glabe, C. (1994) Surfactant properties of Alzheimer's A beta peptides and the mechanism of amyloid aggregation, J. Biol. Chem. 269, 28551-28554.
23. Pratt, L. R., and Pohorille, A. (2002) Hydrophobic effects and modeling of biophysical aqueous solution interfaces, Chem. Rev. 102, 2671-2692.
24. 6 promotes β-amyloid(1-40) protofibril growth by association but does not alter protofibril effects on cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT), Mol. Pharmacol. 64, 1160-1168.
25. Nichols, M. R., Moss, M. A., Reed, D. K., Hoh, J. H., and Rosenberry, T. L. (2004) Amyloid-β protofibrils differ from amyloid-β aggregates induced in dilute hexafluoroisopropanol in stability and morphology, J. Biol. Chem, Papers in Press, http://dx.doi.org/10.1074/jbc.M410553200.
26. Tseng, B. P., Esler, W. P., Clish, C. B., Stimson, E. R., Ghilardi, J. R., Vinters, H. V., Mantyh, P. W., Lee, J. P., and Maggio, J. E. (1999) Deposition of monomeric, not oligomeric, Aβ mediates growth of Alzheimer's disease amyloid plaques in human brain preparations, Biochemistry 38, 10424-10431.
27. LeVine, H., III (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T, Methods Enzymol. 309, 274-284.
28. De Ferrari, G. V., Mallender, W. D., Inestrosa, N. C., and Rosenberry, T. L. (2001) Thioflavin T is a fluorescent probe of the acetylcholinesterase peripheral site that reveals conformational interactions between the peripheral and acylation sites, J. Biol. Chem. 276, 23282-23287.
29. Sreerama, N., and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set, Anal. Biochem. 287, 252-260.
30. Harper, J. D., Wong, S. S., Lieber, C. M., and Lansbury, P. T., Jr. (1997) Observation of metastable Aβ amyloid protofibrils by atomic force microscopy, Chem. Biol. 4, 119-125.
31. Stine, W. B. J., Dahlgren, K. N., Krafft, G. A., and LaDu, M. J. (2003) In vitro characterization of conditions for amyloid-β peptide oligomerization and fibrillogenesis. J. Biol. Chem. 278, 11612-11622.
32. Pallitto, M. M., Ghanta, J., Heinzelman, P., Kiessling, L. L., and Murphy, R. M. (1999) Recognition sequence design for peptidyl modulators of β-amyloid aggregation and toxicity, Biochemistry 38, 3570-3578.
33. Tycko, R. (2003) Insights into the amyloid folding problem from solid-state NMR, Biochemistry 42, 3151-3159.
34. Schladitz, C., Vieira, E. P., Hermel, H., and Mohwald, H. (1999) Amyloid-β-sheet formation at the air-water interface, Biophys. J. 77, 3305-3310.
35. Zhu, M., Souillac, P. O., Ionescu-Zanetti, C., Carter, S. A., and Fink, A. L. (2002) Surface-catalyzed amyloid fibril formation, J. Biol. Chem. 277, 50914-50922.
36. Kowalewski, T., and Holtzman, D. M. (1999) In situ atomic force microscopy study of Alzheimer's β-amyloid peptide on different substrates: New insights into mechanism of β-sheet formation. Proc. Natl. Acad. Sci. U.S.A. 96, 3688-3693.
37. Hofrichter, J., Ross, P. D., and Eaton, W. A. (1974) Kinetics and mechanism of deoxyhemoglobin S gelation: a new approach to understanding sickle cell disease, Proc. Natl. Acad. Sci. U.S.A. 77, 4864-4868.
38. Cao, Z., and Ferrone, F. A. (1996) A 50th order reaction predicted and observed for sickle hemoglobin nucleation, J. Mol. Biol. 256, 219-222.
39. Costigan, S. C., Booth, P. J., and Templer, R. H. (2000) Estimations of lipid bilayer geometry in fluid lamellar phases, Biochim. Biophys. Acta 1468, 41-54.
40. 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, 8397-8409.
41. Padrick, S. B., and Miranker, A. D. (2002) Islet amyloid: Phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis, Biochemistry 41, 4694-4703.
42. Chen, S., Ferrone, F. A., and Wetzel, R. (2002) Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation, Proc. Natl. Acad. Sci. U.S.A. 99, 11884-11889.
43. Yoshida, K., Yamaguchi, T., Adachi, T., Otomo, T., Matsuo, D., Takamuku, T., and Nishi, N. (2003) Structure and dynamics of hexafluoroisopropanol - water mixtures by X-ray diffraction, small-angle neutron scattering. NMR spectroscopy, and mass spectrometry, J. Chem. Phys. 119, 6132-6142.
44. 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.
45. Zangi, R., de Vocht, M. L., Robijlard, G. T., and Mark, A. E. (2002) Molecular dynamics study of the folding of hydrophobin SC3 at a hydrophilic/hydrophobic interface, Biophys. J. 83, 112-124.
46. Wosten, H., De Vries, O., and Wessels, J. (1993) Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer, Plant Cell 5, 1567-1574.
47. Wosten, H. A., Schuren, F. H., and Wessels, J. G. (1994) Interfacial self-assembly of a hydrophobin into an amphipathic protein membrane mediates fungal attachment to hydrophobic surfaces, EMBO J. 13, 5848-5854.
48. Munishkina, L. A., Phelan, C., Uversky, V. N., and Fink, A. L. (2003) Conformational behavior and aggregation of α-synuclein in organic solvents: Modeling the effects of membranes, Biochemistry 42, 2720-2730.
49. Wu, J., Li, J. B., Zhao, J., and Miller, R. (2000) Dynamic characterization of phospholipid/protein competitive adsorption at the aqueous solution/chloroform interace, Colloids Surf., A 175, 113-120.
50. Choo-Smith, L. P., and Surewicz, W. K. (1997) The interaction between Alzheimer amyloid β(1-40) peptide and ganglioside GM1-containing membranes, FEBS Lett. 402, 95-98.
51. Kakio, A., Nishimoto, S., Yanagisawa, K., Kozutsumi, Y., and Matsuzaki, K. (2001) Cholesterol-dependent formation of GM1 ganglioside-bound amyloid β-protein, an endogenous seed for Alzheimer amyloid, J. Biol. Chem. 276, 24985-24990.
52. Curtain, C. C., Ali, F. E., Smith, D. G., Bush, A. I., Masters, C. L., and Barnham, K. J. (2003) Metal ions, pH, and cholesterol regulate the interactions of Alzheimer's disease amyloid-β peptide with membrane lipid, J. Biol. Chem. 278, 2977-2982.
53. Terzi, E., Holzemann, G., and Seelig, J. (1997) Interaction of Alzheimer β-amyloid peptide(1-40) with lipid membranes, Biochemists 36, 14845-14852.
54. Choo-Smith, L. P., Garzon-Rodriguez, W., Glabe, C. G., and Surewicz, W. K. (1997) Acceleration of amyloid fibril formation by specific binding of Aβ-(1-40) peptide to ganglioside-containing membrane vesicles, J. Biol. Chem. 272, 22987-22990.
55. Matsuzaki, K., and Horikiri, C. (1999) Interactions of amyloid β-peptide(1-40) with ganglioside-containing membranes, Biochemistry 38, 4137-4142.
56. Yip, C. M., and McLaurin, J. (2001) Amyloid-β peptide assembly: A critical step in fibrillogenesis and membrane disruption, Biophys. J. 80, 1359-1371.
57. Chan, W., Fornwald, J., Brawner, M., and Wetzel, R. (1996) Native complex formation between apolipoprotein E isoforms and the Alzheimer's disease peptide A beta, Biochemistry 35, 7123-7130.