Designed hairpin peptides interfere with amyloidogenesis pathways: Fibril formation and cytotoxicity inhibition, interception of the preamyloid state

Biochemistry

Volumn 50, Issue 38, 2011, Pages 8202-8212

  Huggins, Kelly N L ^a   Bisaglia, Marco ^b   Bubacco, Luigi ^b   Tatarek Nossol, Marianna ^c,d   Kapurniotu, Aphrodite ^d   Andersen, Niels H ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF PADOVA   (Italy)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABNORMAL MORPHOLOGY; AMYLOID FORMATION; AMYLOIDOGENESIS; FIBRIL FORMATION; INHIBITORY EFFECT; LAG-TIME; PARKINSON'S DISEASE; SEQUENCE SIMILARITY; SYNUCLEIN; THIOFLAVIN; TYPE II;

FLUORESCENCE; GLYCOPROTEINS; TRANSMISSION ELECTRON MICROSCOPY;

PEPTIDES;

ALPHA SYNUCLEIN; AMYLIN; AMYLOID; HAIRPIN PEPTIDE; PEPTIDE; UNCLASSIFIED DRUG;

AMYLOIDOGENESIS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; FIBER; HUMAN; NONHUMAN; PREAMYLOID STATE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; AMYLOID; ANIMALS; DRUG DESIGN; HUMANS; ISLET AMYLOID POLYPEPTIDE; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; RATS; RECOMBINANT PROTEINS; THIAZOLES;

RATTUS;

EID: 80053010466     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200760h     Document Type: Article

References (62)

1. Chiti, F. and Dobson, C. M. (2009) Amyloid formation by globular proteins under native conditions Nat. Chem. Biol. 5, 15-22
2. Cooper, G. J., Willis, A. C., Clark, A., Turner, R. C., Sim, R. B., and Reid, K. B. (1987) Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients Proc. Natl. Acad. Sci. U.S.A. 84, 8628-8632 (Pubitemid 18033465)
3. Goedert, M. (2001) α-Synuclein and neurodegenerative diseases Nat. Rev. Neurosci. 2, 492-501
4. Ferrone, F. (1999) Analysis of protein aggregation kinetics Methods Enzymol. 309, 256-274 (Pubitemid 29446454)
5. Ruschak, A. M. and Miranker, A. D. (2007) Fiber-dependent amyloid formation as catalysis of an existing reaction pathway Proc. Natl. Acad. Sci. U.S.A. 104, 12341-12346 (Pubitemid 47206139)
6. Lansbury, P. T. (1997) Inhibition of amyloid formation: A strategy to delay the onset of Alzheimer's disease Curr. Opin. Chem. Biol. 1, 260-267
7. Roberts, B. E. and Shorter, J. (2008) Escaping amyloid fate Nat. Struct. Mol. Biol. 15, 544-546 (Pubitemid 351799147)
8. Haass, C. and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer's amyloid β-peptide Nat. Rev. Mol. Cell Biol. 8, 101-112 (Pubitemid 46432529)
9. Haataja, L., Gurlo., T., Huang, C. J., and Butler, P. C. (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis Endocr. Rev. 29, 303-316 (Pubitemid 351679701)
10. Ehrnhoefer, D. E., Bieschke, J., Boeddrich, A., Herbst, M., Masino, L., Lurz, R., Engemann, S., Pastire, A., and Wanker, E. E. (2008) EGCG redirects amyloidogenic polypeptides into unsctructured, off-pathway oligomers Nat. Struct. Mol. Biol. 15, 558-566 (Pubitemid 351799141)
11. Hudson, S. A., Ecroyd, H., Dehle, F. C., Musgrave, I. F., and Carver, J. A. (2009) (-)-Epigallocatechin-3-Gallate (EGCG) Maintains κ-Casein in its pre-fibrillar state without redirecting its aggregation pathway J. Mol. Biol. 392, 689-700
12. El-Agnaf, O. M. A., Paleologou, K. E., Greer, B., Abogrein, A. M., King, J. E., Salem, S. A., Fullwood, N. J., Benson, F. E., Hewitt, R., Ford, K. J., Martin, F. L., Harriott, P., Cookson, M. R., and Allsop, D. (2004) A strategy for designing inhibitos of α-synuclein aggregation and toxicity as a novel treatment for Parkinson's disease and related disorders FASEB J. 18, 1315-1317 (Pubitemid 39561588)
13. Austen, B. M., Paleologou, K. E., Ali, S. A. E., Qureshi, M. M., Allsop, D., and El-Agnaf, O. M. A. (2008) Designing peptide inhibitors for oligomerization and toxicity of Alzheimer's β-amyloid peptide Biochemistry 47, 1984-1992 (Pubitemid 351287124)
14. 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 (Pubitemid 34729344)
15. Yan, L.-M., Tararek-Nossol, M., Velkova, A., Kazantzis, A., and Kapumiotu, A. (2006) Design of a mimic of nonamyloidogenic and bioactive human islet amyloid polypeptide (IAPP) as nanomolar affinity of IAPP cytotoxic fibrillogenesis Proc. Natl. Acad. Sci. U.S.A. 103, 2046-2051 (Pubitemid 43271620)
16. Gilead, S. and Gazit, E. (2004) Inhibition of amyloid fibril formation by peptide analogues modified with α-aminoisobutyric acid Angew. Chem., Int. Ed. 43, 4041-4044 (Pubitemid 39257449)
17. Etienne, M. A., Aucoin, J. P., Fu, Y., McCarley, R. L., and Hammer, R. P. (2006) Stoichiometric inhibition of amyloid β-protein aggregation with peptides containing alternating α,α-disubstituted amino acids J. Am. Chem. Soc. 128, 3522-3523
18. Smith, T. J., Stains, C. I., Meyer, S. C., and Ghosh, I. (2006) Inhibition of β-amyloid fibrillization by directed evolution of a β-sheet presenting miniature protein J. Am. Chem. Soc. 128, 14456-14457 (Pubitemid 44749835)
19. Cochran, A. G., Skelton, N. J., and Starovasnik, M. A. (2001) Tryptophan zippers: Stable, monomeric β-hairpins Proc. Natl. Acad. Sci. U.S.A. 98, 5578-5583 (Pubitemid 32435684)
20. Andersen, N. H., Olsen, K. A., Fesinmeyer, R. M., Tan, X., Hudson, F. M., Eidenschink, L. A., and Farazi, S. R. (2006) Minimization and optimization of designed β-hairpin folds J. Am. Chem. Soc. 128, 6101-6110
21. Kier, B. L. and Andersen, N. H. (2008) Probing the lower size limit for protein-like fold stability: Ten-residue microproteins with specific, rigid structures in water J. Am. Chem. Soc. 130, 14675-14683
22. Eidenschink, L. A., Kier, B. L., Huggins, K. N. L., and Andersen, N. H. (2009) Very short peptides with stable folds: Building on the interrelationship of Trp/Trp, Trp/cation, and Trp/backbone-amide interaction geometries Proteins: Struct., Funct., Bioinf. 75, 308-322
23. Kier, B. L., Shu, I., Eidenschink, L. A., and Andersen, N. H. (2010) Stabilizing capping motif for β-hairpins and sheets Proc. Natl. Acad. Sci. U.S.A. 107, 10466-10471
24. Huggins, K. N. L. and Andersen, N. H. (2010) Hairpin peptide inhibitors of amyloid fibril formation. In Chemistry of Peptides in Life Science, Technology and Medicine (Lankinen, H., Ed.) Peptides 2008 (Proceedings of the 30th European Peptide Symposium) pp 590-591.
25. Naiki, H., Higuchi, K., Hosokawa, M., and Takeda, T. (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavine T Anal. Biochem. 177, 244-249 (Pubitemid 19088253)
26. Conway, K. A., Harper, J. D., and Lansbury, P. T. (2000) Fibrils formed in vitro from α-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid Biochemistry 39, 2552-2563 (Pubitemid 30148907)
27. Huang, C., Ren, G., Zhou, H., and Wang, C.-C. (2005) A new method for purification of recombinant human α-synuclein in Escherichia coli Protein Expression Purif. 42, 173-177 (Pubitemid 40793408)
28. Cort, J. R., Liu, Z., Lee, G. M., Huggins, K. N. L., Janes, S., Prickett, K., and Andersen, N. H. (2009) Solution state structures of human pancreatic amylin and pramlintide Protein Eng., Des. Sel. 22, 497-513
29. Yan, L.-M., Velkova, A., Tatarek-Nossol, M., Andreetto, E., and Kapurniotu, A. (2007) Designed IAPP Mimic Blocks Aβ Cytotoxic Self-Assembly: Cross-Suppression of Amyloid Toxicity of Aβ and IAPP Suggests a Molecular Link between Alzheimer's Disease and Type 2 Diabetes Angew. Chem., Int. Ed. 46, 1246-1252 (Pubitemid 46981368)
30. Nilsson, M. R. (2004) Techniques to study amyloid fibril formation in vitro Methods 34, 151-160 (Pubitemid 38993215)
31. Tatarek-Nossol, M., Yan, L. M., Schmauder, A., Tenidis, K., Westermark, G., and Kapurniotu, A. (2005) Inhibition of hIAPP amyloid-fibril formation and apoptotic cell death by a designed hIAPP amyloid-core-containing hexapeptide Chem. Biol. 12, 797-809 (Pubitemid 41009159)
32. Tenidis, K., Waldner, M., Bernhagen, J., Fischle, W., Bergmann, M., Weber, M., Merkle, M. L., Voelter, W., Brinner, H., and Kapurniotu, A. (2000) Identification of a penta- and hexapeptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties J. Mol. Biol. 295, 1055-1071
33. Hoyer, W., Antony, T., Cherny, D., Heim, G., Jovin, T. M., and Subramaniam, V. (2002) Dependence of α-synuclein aggregate morphology on solution conditions J. Mol. Biol. 322, 383-393
34. Fink, A. L. (2006) The aggregation and fibrillation of α-synuclein Acc. Chem. Res. 39, 628-634
35. Miranker, A. D. and Padrick, S. B. (2001) Islet amyloid polypeptide: Identification of long-range contacts and local order on the fibrillogenesis pathway J. Mol. Biol. 308, 783-794 (Pubitemid 32568473)
36. 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 (Pubitemid 34275671)
37. Koo, B. W. and Miranker, A. D. (2005) Contribution of the intrinsic disulfide to the assembly mechanism of islet amyloid Protein Sci. 14, 231-239 (Pubitemid 40054136)
38. Cao, P., Meng, F., Abedini, A., and Raleigh, D. P. (2010) The ability of rodent islet amyloid polypeptide to inhibit amyloid formation by human islet amyloid polypeptide has important implications for the mechanism of amyloid formation and the design of inhibitors Biochemistry 49, 872-881
39. Munishkina, L. A., Phelan, C., Uversy, V. N., and Fink, A. L. (2003) Conformational behaviour and aggregation of α-synuclein in organic solvents: Modeling the effects of membranes Biochemistry 42, 2720-2730 (Pubitemid 36330626)
40. Goldsbury, C., Goldie, K., Pellaud, J., Seeling, J., Frey, P., Muller, S. A., Kistler, J., Cooper, J. S., and Aebi, U. (2000) Amyloid fibril formation from full-length and fragments of amylin J. Struct. Biol. 130, 352-362
41. Puchtler, H., Sweat, F., and Levine, M. (1962) On the binding of congo red by amyloid J. Histochem. Cytochem. 10, 355-364
42. Shim, S.-H., Gupta, R., Ling, Y. L., Strasfeld, D. B., Raleigh, D. P., and Zanni, M. T. (2009) Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residue-specific resolution Proc. Natl. Acad. Sci. U.S.A. 106, 6614-6619
43. Luca, S., Yau, W. M., Leapman, R., and Tycko, R. (2007) Peptide conformation and supramolacular organization in amylin fibrils: Constraints from solid-state NMR Biochemistry 46, 13505-13522 (Pubitemid 350209947)
44. Kajava, A. V., Baxam, U., and Stevem, A. C. (2010) β arcades: Recurring motifs in naturally occurring and disease-related amyloid fibrils FASEB J. 24, 1311-1319
45. Du, H.-N., Li, H.-T., Zhang, F., Lin, X.-J., Shi, J. H., Shi, Y.-H., Ji, L.-N., Hu, J., Lin, D.-H., and Hu, H.-Y. (2006) Acceleration of α-synuclein aggregation by homologous peptides FEBS Lett. 580, 3657-3664 (Pubitemid 43902801)
46. Lashuel, H. A., Petre, B. M., Wall, J., Simon, M., Nowak, R. J., Walz, T., and Lansbury, P. T., Jr. (2002) α-Synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils J. Mol. Biol. 322, 1089-1102 (Pubitemid 35266514)
47. Lowe, R., Pountney, D. L., Jensen, H. P., Gair, W. P., and Voelcker, N. H. (2004) Calcium(II) selectively induces α-synuclein annular oligomers via interaction with the C-terminal domain Protein Sci. 13, 3245-3252 (Pubitemid 39557794)
48. Rochet, J.-C., Conway, K. A., and Lansbury, P. T. (2000) Inhibition of fibrillization and accumulation of prefibrillar oligomers in mixtures of human and mouse α-synuclein Biochemistry 39, 10619-10626
49. Abedini, A. and Raleigh, D. P. (2009) A critical assessment of the role of helical intermediates in amyloid formation by natively unfolded proteins and polypeptides Protein Eng., Des. Sel. 22, 453-459
50. Williamson, J. A., Loria, J. P., and Miranker, A. D. (2009) Helix stabilization precedes aqueous and bilayer-catalyzed fiber formation in islet amyloid polypeptide J. Mol. Biol. 393, 383-396
51. Bisaglia, M., Tessari, I., Pinato, L., Bellanda, M., Giraudo, S., Fasano, M., Bergantino, E., Bubacco, L., and Mammi, S. (2005) A topological model of the interaction between α-synuclein and sodium dodecyl sulfate micelles Biochemistry 44, 329-339 (Pubitemid 40095735)
52. Bisaglia, M., Trolio, A., Bellanda, M., Bergantino, E., Bubacco, L., and Mammi, S. (2006) Structure and topology of human α-synuclein bound to micelles: Implications for the aggregation process Protein Sci. 15, 1408-1416 (Pubitemid 43800012)
53. Munishkina, L. A., Henriques, J., Uversky, V. N., and Fink, A. L. (2004) Role of protein-water interactions and electrostatics in α-synuclein fibril formation Biochemistry 43, 3289-3300 (Pubitemid 38352279)
54. Lee, H. J., Choi, C., and Lee, S. J. (2002) Membrane-bound α-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form J. Biol. Chem. 277, 671-678 (Pubitemid 34952106)
55. Zhu, M. and Fink, A. L. (2003) Lipid Binding Inhibits α-Synuclein Fibril Formation J. Biol. Chem. 278, 16873-16877 (Pubitemid 36799558)
56. Ma, B., Elkayam, T., Wolfson, H., and Nussinov, R. (2003) Protein-protein interactions: Structurally conserved residues distinguish between binding sites and exposed protein surfaces Proc. Natl. Acad. Sci. U.S.A. 100, 5772-5777 (Pubitemid 36576883)
57. Sato, T., Kienlen-Campard, P., Ahmed, M., Liu, W., Li, H., Elliott, J. I., Aimoto, S., Constantinescu, S. N., Octave, J.-N., and Smith, S. O. (2006) Inhibitors of amyloid toxicity based on β-sheet packing of Aβ40 and Aβ42 Biochemistry 45, 5503-5516 (Pubitemid 43673181)
58. Nagai, Y., Inui, T., Popiel, H. A., Fujikake, N., Hasegawa, K., Urade, Y., Goto, Y., Naiki, H., and Toda, T. (2007) A toxic monomeric conformer of the polyglutamine protein Nat. Struct. Mol. Biol. 14, 332-340 (Pubitemid 46608340)
59. Maynard, A. J., Sharman, G. J., and Searle, M. S. (1998) Origin of β-hairpin stability in solution: Structural and thermodynamic analysis of the folding of model peptide supports hydrophobic stabilization in water J. Am. Chem. Soc. 120, 1996-2007 (Pubitemid 28179171)
60. Dyer, R. B., Maness, S. J., Franzen, S., Fesinmeyer, R. M., Olsen, K. A., and Andersen, N. H. (2005) Hairpin Folding Dynamics: The cold-denatured state is predisposed for rapid refolding Biochemistry 44, 10406-10415 (Pubitemid 41076836)
61. Cort, J. R. 1994, β-Structure in human amylin and two designer β-peptides: CD and NMR spectroscopic comparisons suggest soluble β-oligomers and the absence of significant populations of β-strand dimers Biochem. Biophys. Res. Commun. 204, 1088-1095
62. Porat, Y., Mazor, Y., Efrat, S., and Gazit, E. (2004) Inhibition of islet amyloid polypeptide fibril formation: A potential role for heteroaromatic interactions Biochemistry 43, 14454-14462 (Pubitemid 39491980)