Inhibitors of amyloid toxicity based on β-sheet packing of Aβ40 and Aβ42

Biochemistry

Volumn 45, Issue 17, 2006, Pages 5503-5516

  Sato, Takeshi ^a   Kienlen Campard, Pascal ^b   Ahmed, Mahiuddin ^a   Liu, Wei ^a   Li, Huilin ^c   Elliott, James I ^d   Aimoto, Saburo ^e   Constantinescu, Stefan N ^f   Octave, Jean Noel ^b   Smith, Steven O ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c BROOKHAVEN NATIONAL LABORATORY   (United States)

^d YALE UNIVERSITY   (United States)

^e OSAKA UNIVERSITY   (Japan)

^f DE DUVE INSTITUTE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL CULTURE; ELECTRON MICROSCOPY; FLUORESCENCE; HYDROGEN BONDS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; TOXICITY;

ALZHEIMER'S DISEASE; CULTURED RAT CORTICAL NEURONS; FIBRIL AXIS; NEURODEGENERATIVE DISEASES;

PROTEINS;

AMYLOID; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AROMATIC AMINO ACID; GLYCINE; ISOLEUCINE; METHIONINE; PHENYLALANINE; PROTEIN INHIBITOR; THIOFLAVINE;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BETA SHEET; BRAIN CELL; CARBOXY TERMINAL SEQUENCE; DEGENERATIVE DISEASE; ELECTRON MICROSCOPY; FLUORESCENCE ANALYSIS; HYDROGEN BOND; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN INTERACTION; PROTEIN MOTIF; RAT;

AMINO ACID SEQUENCE; AMYLOID; AMYLOID BETA-PROTEIN; ANIMALS; FLUORESCENT DYES; GLYCINE; HUMANS; METHIONINE; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; NEURONS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; SPECTROMETRY, FLUORESCENCE; THIAZOLES;

ANIMALIA;

EID: 33646371260     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052485f     Document Type: Article

References (78)

1. Kirschner, D. A., Abraham, C., and Selkoe, D. J. (1986) X-ray-diffraction from Intraneuronal paired helical filaments and extra-neuronal amyloid fibers in Alzheimer-disease indicates cross-β conformation, Proc. Natl. Acad. Sci. U.S.A. 83, 503-507.
2. 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.
3. Chalifour, R. J., McLaughlin, R. W., Lavoie, L., Morissette, C., Tremblay, N., Boule, M., Sarazin, P., Stea, D., Lacombe, D., Tremblay, P., and Gervais, F. (2003) Stereoselective interactions of peptide inhibitors with the β-amyloid peptide, J. Biol. Chem. 278, 34874-34881.
4. Gordon, D. J., and Meredith, S. C. (2003) Probing the role of backbone hydrogen bonding in β-amyloid fibrils with inhibitor peptides containing ester bonds at alternate positions, Biochemistry 42, 475-485.
5. Hughes, E., Burke, R. M., and Doig, A. J. (2000) Inhibition of toxicity in the β-amyloid peptide fragment β-(25-35) using N-methylated derivatives -A general strategy to prevent amyloid formation, J. Biol. Chem. 275, 25109-25115.
6. Gordon, D. J., Sciarretta, K. L., and Meredith, S. C. (2001) Inhibition of β-amyloid(40) fibrillogenesis and disassembly of β-amyloid(40) fibrils by short β-amyloid congeners containing N-methyl amino acids at alternate residues, Biochemistry 40, 8237-8245.
7. 1-40 fibrillogenesis, J. Pept. Res. 60, 37-55.
8. Kapurniotu, A., Schmauder, A., and Tenidis, K. (2002) Structure-based design and study of nonamyloidogenic, double N-methylated IAPP amyloid core sequences as inhibitors of IAPP amyloid formation and cytotoxicity, J. Mol. Biol. 315, 339-350.
9. Soto, C., Kindy, M. S., Baumann, M., and Frangione, B. (1996) Inhibition of Alzheimer's amyloidosis by peptides that prevent β-sheet conformation, Biochem. Biophys. Res. Commun. 226, 672-680.
10. Soto, C., Sigurdsson, E. M., Morelli, L., Kumar, R. A., Castano, E. M., and Frangione, B. (1998) β-sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: Implications for Alzheimer's therapy, Nat. Med. 4, 822-826.
11. Adessi, C., Frossard, M. J., Boissard, C., Fraga, S., Bieler, S., Ruckle, T., Vilbois, F., Robinson, S. M., Mutter, M., Banks, W. A., and Soto, C. (2003) Pharmacological profiles of peptide drug candidates for the treatment of Alzheimer's disease, J. Biol. Chem. 278, 13905-13911.
12. Tjernberg, L. O., Lilliehook, C., Callaway, D. J. E., Naslund, J., Hahne, S., Thyberg, J., Terenius, L., and Nordstedt, C. (1997) Controlling amyloid β-peptide fibril formation with protease-stable ligands, J. Biol. Chem. 272, 12601-12605.
13. Liu, W., Crocker, E., Zhang, W., Elliott, J. I., Luy, B., Li, H., Aimoto, S., and Smith, S. O. (2005) Structural role of glycine in amyloid fibrils formed from transmembrane α-helices, Biochemistry 44, 3591-3597.
14. Benzinger, T. L. S., Gregory, D. M., Burkoth, T. S., Miller-Auer, H., Lynn, D. G., Botto, R. E., and Meredith, S. C. (1998) Propagating structure of Alzheimer's β-amyloid(10-35) is parallel β-sheet with residues in exact register, Proc. Natl. Acad. Sci. U.S.A. 95, 13407-13412.
15. Antzutkin, O. N., Balbach, J. J., Leapman, R. D., Rizzo, N. W., Reed, J., and Tycko, R. (2000) Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of β-sheets in Alzheimer's β-amyloid fibrils, Proc. Natl. Acad. Sci. U.S.A. 97, 13045-13050.
16. Torok, M., Milton, S., Kayed, R., Wu, P., McIntire, T., Glabe, C. G., and Langen, R. (2002) Structural and dynamic features of Alzheimer's Aβ peptide in amyloid fibrils studied by site-directed spin labeling, J. Biol. Chem. 277, 40810-40815.
17. 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.
18. Selkoe, D. J. (2001) Presenilin, Notch, and the genesis and treatment of Alzheimer's disease, Proc. Natl. Acad. Sci. U.S.A. 98, 11039-11041.
19. Hegde, R. S., Mastrianni, J. A., Scott, M. R., DeFea, K. A., Tremblay, P., Torchia, M., DeArmond, S. J., Prusiner, S. B., and Lingappa, V. R. (1998) A transmembrane form of the prion protein in neurodegenerative disease, Science 279, 827-834.
20. Cohen, F. E., and Prusiner, S. B. (1998) Pathologic conformations of prion proteins, Annu. Rev. Biochem. 67, 793-819.
21. Javadpour, M. M., Eilers, M., Groesbeek, M., and Smith, S. O. (1999) Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association, Biophys. J. 77, 1609-1618.
22. Eilers, M., Patel, A. B., Liu, W., and Smith, S. O. (2002) Comparison of helix interactions in membrane and soluble α-bundle proteins, Biophys. J. 82, 2720-2736.
23. Senes, A., Gerstein, M., and Engelman, D. M. (2000) Statistical analysis of amino acid patterns in transmembrane helices: The GxxxG motif occurs frequently and in association with β-branched residues at neighboring positions, J. Mol. Biol. 296, 921-936.
24. Russ, W. P., and Engelman, D. M. (2000) The GxxxG motif: a framework for transmembrane helix-helix association, J. Mol. Biol. 296, 911-919.
25. Wang, L., Oconnell, T., Tropsha, A., and Hermans, J. (1996) Molecular simulations of β-sheet twisting, J. Mol. Biol. 262, 283-293.
26. Antzutkin, O. N., Balbach, J. J., and Tycko, R. (2003) Site-specific identification of non-β-strand conformations in Alzheimer's β-amyloid fibrils by solid-state NMR, Biophys. J. 84, 3326-3335.
27. Petkova, A. T., Ishii, 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.
28. Kessler, J. C., Rochet, J. C., and Lansbury, P. T. (2003) The N-terminal repeat domain of α-synuclein inhibits β-sheet and amyloid fibril formation, Biochemistry 42, 672-678.
29. 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.
30. Hardy, J. (1997) Amyloid, the presenilins and Alzheimer's disease, Trends Neurosci. 20, 154-159.
31. Mastrangelo, I. A., Ahmed, M., Sato, T., Liu, W., Wang, C., Hough, P., and Smith, S. O. (2006) High-resolution atomic force microscopy of soluble Aβ42 oligomers, J. Mol. Biol. 358, 106-119.
32. Simmons, L. K., May, P. C., Tomaselli, K. J., Rydel, R. E., Fuson, K. S., Brigham, E. F., Wright, S., Lieberburg, I., Becker, G. W., Brems, D. N., and Li, W. Y. (1994) Secondary structure of amyloid β-peptide correlates with neurotoxic activity in vitro, Mol. Pharmacol. 45, 373-379.
33. Soto, C., Castano, E. M., Kumar, R. A., Beavis, R. C., and Frangione, B. (1995) Fibrillogenesis of synthetic amyloid-β peptides is dependent on their initial secondary structure, Neurosci. Lett. 200, 105-108.
34. LeVine, H. (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T, Methods Enzymol. 309, 274-284.
35. Metz, G., Wu, X., and Smith, S. O. (1994) Ramped-amplitude cross polarization in magic angle spinning NMR, J. Magn. Reson., Ser. A 110, 219-227.
36. Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V., and Griffin, R. G. (1995) Heteronuclear decoupling in rotating solids, J. Chem. Phys. 103, 6951-6958.
37. 1H dipolar-assisted rotational resonance in magic-angle spinning NMR, Chem. Phys. Lett. 344, 631-637.
38. Crocker, E., Patel, A. B., Eilers, M., Jayaraman, S., Getmanova, E., Reeves, P. J., Ziliox, M., Khorana, H. G., Sheves, M., and Smith, S. O. (2004) Dipolar assisted rotational resonance NMR of tryptophan and tyrosine in rhodopsin, J. Biomol. NMR 29, 11-20.
39. Kienlen-Campard, P., Miolet, S., Tasiaux, B., and Octave, J. N. (2002) Intracellular amyloid-β 1-42, but not extracellular soluble amyloid-β peptides, induces neuronal apoptosis, J. Biol Chem. 277, 15666-15670.
40. Macq, A. F., Czech, C., Essalmani, R., Brion, J. P., Maron, A., Mercken, L., Pradier, L., and Octave, J. N. (1998) The long-term adenoviral expression of the human amyloid precursor protein shows different secretase activities in rat cortical neurons and astrocytes, J. Biol. Chem. 273, 28931-28936.
41. Kienlen Campard, P., Crochemore, C., Rene, F., Monnier, D., Koch, B., and Loeffler, J. P. (1997) PACAP type I receptor activation promotes cerebellar neuron survival through the cAMP/ PKA signaling pathway, DNA Cell Biol. 16, 323-333.
42. Nilsson, M. R. (2004) Techniques to study amyloid fibril formation in vitro, Methods 34, 151-160.
43. - 43. Wood, S. J., Maleeff, B., Hart, T., and Wetzel, R. (1996) Physical, morphological and functional differences between pH 5.8 and 7.4 aggregates of the Alzheimer's amyloid peptide Aβ, J. Mol. Biol. 256, 870-877.
44. Carulla, N., Caddy, G. L., Hall, D. R., Zurdo, J., Gairi, M., Feliz, M., Giralt, E., Robinson, C. V., and Dobson, C. M. (2005) Molecular recycling within amyloid fibrils, Nature 436, 554-558.
45. O'Nuallain, B., Shivaprasad, S., Kheterpal, I., and Wetzel, R. (2005) Thermodynamics of Aβ(1-40) amyloid fibril elongation, Biochemistry 44, 12709-12718.
46. Williams, A. D., Portelius, E., Kheterpal, I., Guo, J. T., Cook, K. D., Xu, Y., and Wetzel, R. (2004) Mapping Aβ amyloid fibril secondary structure using scanning proline mutagenesis, J. Mol. Biol. 335, 833-842.
47. Morimoto, A., Irie, K., Murakami, K., Masuda, Y., Ohigashi, H., Nagao, M., Fukuda, H., Shimizu, T., and Shirasawa, T. (2004) Analysis of the secondary structure of β-amyloid (Aβ 42) fibrils by systematic proline replacement, J. Biol. Chem. 279, 52781-52788.
48. Williams, A. D., Shivaprasad, S., and Wetzel, R. (2006) Alanine scanning mutagenesis of Aβ(1-40) amyloid fibril stability, J. Mol. Biol. 357, 1283-1294.
49. Shivaprasad, S., and Wetzel, R. (2006) Scanning cysteine mutagenesis analysis of Aβ-(1-40) amyloid fibrils, J. Biol. Chem. 257, 993-1000.
50. Kim, S., Jeon, T. J., Oberai, A., Yang, D., Schmidt, J. J., and Bowie, J. U. (2005) Transmembrane glycine zippers: Physiological and pathological roles in membrane proteins, Proc. Natl. Acad. Sci. U.S.A. 102, 14278-14283.
51. Kanski, J., Varadarajan, S., Aksenova, M., and Butterfield, D. A. (2002) Role of glycine-33 and methionine-35 in Alzheimer's amyloid β-peptide 1-42-associated oxidative stress and neurotoxicity, Biochim. Biophys. Acta 1586, 190-198.
52. Kanski, J., Aksenova, M., and Butterfield, D. A. (2002) The hydrophobic environment of Met35 of Alzheimer's Aβ(1-42) is important for the neurotoxic and oxidative properties of the peptide, Neurotoxic. Res. 4, 219-223.
53. Burkoth, T. S., Benzinger, T. L. S., Urban, V., Morgan, D. M., Gregory, D. M., Thiyagarajan, P., Botto, R. E., Meredith, S. C., and Lynn, D. G. (2000) Structure of the β-amyloid(10-35) fibril, J. Am. Chem. Soc. 122, 7883-7889.
54. Jaroniec, C. P., MacPhee, C. E., Bajaj, V. S., McMahon, M. T., Dobson, C. M., and Griffin, R. G. (2004) High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 101, 711-716.
55. Petkova, A. T., Leapman, R. D., Guo, Z. H., Yau, W. M., Mattson, M. P., and Tycko, R. (2005) Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils, Science 307, 262-265.
56. Lührs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Döbeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimer's amyloid-β(1-42) fibrils, Proc. Natl. Acad. Sci. U.S.A. 102, 17342-17347.
57. Antzutkin, O. N., Leapman, R. D., Balbach, J. J., and Tycko, R. (2002) Supramolecular structural constraints on Alzheimer's β-amyloid fibrils from electron microscopy and solid-state nuclear magnetic resonance, Biochemistry 41, 15436-15450.
58. Goldsbury, C., Frey, P., Olivieri, V., Aebi, U., and Müller, S. A. (2005) Multiple assembly pathways underlie amyloid-β fibril polymorphisms, J. Mol. Biol. 352, 282-298.
59. 1-42 fibrillogenesis with atomic force microscopy, FASEB J. 19, 1344-1346.
60. Goldsbury, C. S., Wirtz, S., Müller, S. A., Sunderji, S., Wicki, P., Aebi, U., and Frey, P. (2000) Studies on the in vitro assembly of Aβ 1-40: Implications for the search for Aβ fibril formation inhibitors, J. Struct. Biol. 130, 217-231.
61. Tycko, R. (2004) Progress towards a molecular-level structural understanding of amyloid fibrils, Curr. Opin. Struct. Biol. 14, 96-103.
62. Sciarretta, K. L., Gordon, D. J., Petkova, A. T., Tycko, R., and Meredith, S. C. (2005) Aβ 40-Lactam(D23/K28) models a conformation highly favorable for nucleation of amyloid, Biochemistry 44, 6003-6014.
63. Petkova, A. T., Yau, W. M., and Tycko, R. (2006) Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils, Biochemistry 45, 498-512.
64. Shivaprasad, S., and Wetzel, R. (2004) An intersheet packing interaction in Aβ fibrils mapped by disulfide cross-linking, Biochemistry 43, 15310-15317.
65. Hou, L. M., Kang, I., Marchant, R. E., and Zagorski, M. G. (2002) Methionine 35 oxidation reduces fibril assembly of the amyloid Aβ-(1-42) peptide of Alzheimer's disease, J. Biol. Chem. 177, 40173-40176.
66. Brunelle, P., and Rauk, A. (2002) The radical model of Alzheimer's disease: Specific recognition of Gly29 and Gly33 by Met35 in a β-sheet model of Abeta: An ONIOM study, J. Alzheimer's Dis. 4, 283-289.
67. Walsh, D. M., Hartley, D. M., Condron, M. M., Selkoe, D. J., and Teplow, D. B. (2001) In vitro studies of amyloid β-protein fibril assembly and toxicity provide clues to the aetiology of Flemish variant (Ala(692) → Gly) Alzheimer's disease, Biochem. J. 355, 869-877.
68. Bitan, G., Tarus, B., Vollers, S. S., Lashuel, H. A., Condron, M. M., Straub, J. E., and Teplow, D. B. (2003) A molecular switch in amyloid assembly: Met(35) and amyloid β-protein oligomerization, J. Am. Chem. Soc. 125, 15359-15365.
69. Ciccotosto, G. D., Tew, D., Curtain, C. C., Smith, D., Carrington, D., Masters, C. L., Bush, A. I., Cherny, R. A., Cappai, R., and Barnham, K. J. (2004) Enhanced toxicity and cellular binding of a modified amyloid β peptide with a methionine to valine substitution, J. Biol. Chem. 279, 42528-42534.
70. Butterfield, D. A., and Kanski, J. (2002) Methionine residue 35 is critical for the oxidative stress and neurotoxic properties of Alzheimer's amyloid β-peptide 1-42, Peptides 23, 1299-1309.
71. Saito, H., Tuzi, S., and Naito, A. (1998) Empirical versus nonempirical evaluation of secondary structure of fibrous and membrane proteins by solid-state NMR: A practical approach, Ann. Rep. NMR Spectrosc. 36, 79-121.
72. Chacon, M. A., Barria, 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.
73. 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.
74. Blanchard, B. J., Chen, A., Rozeboom, L. M., Stafford, K. A., Weigele, P., and Ingram, V. M. (2004) Efficient reversal of Alzheimer's disease fibril formation and elimination of neurotoxicity by a small molecule, Proc. Natl. Acad. Sci. U.S.A, 101, 14326-14332.
75. 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.
76. Egnaczyk, G. F., Greis, K. D., Stimson, E. R., and Maggio, J. E. (2001) Photoaffinity cross-linking of Alzheimer's disease amyloid fibrils reveals interstrand contact regions between assembled β-amyloid peptide subunits, Biochemistry 40, 11706-11714.
77. Yang, F. S., 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.
78. Kheterpal, I., Williams, A., Murphy, C., Bledsoe, B., and Wetzel, R. (2001) Structural features of the Aβ amyloid fibril elucidated by limited proteolysis, Biochemistry 40, 11757-11767.