Prediction of aggregation rate and aggregation-prone segments in polypeptide sequences

Protein Science

Volumn 14, Issue 10, 2005, Pages 2723-2734

  Tartaglia, Gian Gaetano ^a   Cavalli, Andrea ^a   Pellarin, Riccardo ^a   Caflisch, Amedeo ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Alzheimer's disease; Amyloid; Genetic algorithm; Molecular dynamics; Prion protein; Protein aggregation rate; Species barrier

Indexed keywords

POLYPEPTIDE; PRION PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; FIBER; PHYSICAL CHEMISTRY; PRION DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; THEORETICAL MODEL;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID; DRUG DESIGN; HUMANS; MODELS, CHEMICAL; PARKINSON DISEASE; PRIONS; PROTEIN DENATURATION; PROTEIN STRUCTURE, SECONDARY;

MAMMALIA;

EID: 25844466604     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.051471205     Document Type: Article

References (81)

1. 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. 97: 13045-13050.
2. Antzutkin, O.N., Leapman, R.D., Balbach, J.J., and Tycko, R. 2002. Supramolecular structural constraints on Alzheimer's-amyloid fibrils from electron microscopy and solid-state nuclear magnetic resonance. Biochemistry 41: 15436-15450.
3. Asl, L.H., Liepnieks, J.J., Uemichi, T., Rebibou, J.M., Justrabo, E., Droz, D., Mousson, J.M.C., Benson, M.D., Delpech, M., and Grateau, G. 1997. Renal amyloidosis with a frame shift mutation in fibrinogen α-chain gene producing a novel amyloid protein. Blood 90: 4799-4805.
4. Azriel, R. and Gazit, E. 2001. Analysis of the minimal amyloid-forming fragment of the Islet amyloid polypeptide. J. Biol. Chem. 276: 34156-34161.
5. Balbach, J.J., Ishii, Y., Antzutkin, O.N., Leapman, R.D., Rizzo, N.W., Dyda, F., Reed, J., and Tycko, R. 2000. Amyloid fibril formation by a β16-22, a seven-residue fragment of the Alzheimer's β-amyloid peptide, and structural characterization by solid state NMR. Biochemistry 39: 13748-13759.
6. Balbirnie, M., Grothe, R., and Eisenberg, D. 2001. An amyloid-forming peptide from the yeast prion Sup35 reveals a dehydrated β-sheet structure for amyloid. Proc. Natl. Acad. Sci. 98: 2375-2380.
7. Bitan, G., Kirkitadze, M.D., Lomakin, A., Vollers, S.S., Benedek, G.B., and Teplow, B.D. 2003. Amyloid Aβ-protein Aβ assembly: Aβ40 and Aβ42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. 100: 330-335.
8. Bond, J.P., Deverin, S.P., Inouye, H., El-Agnaf, O.M.A, Teeter, M.M., and Kirschnera, D.A. 2003. Assemblies of Alzheimer's peptides Aβ25-35 and Aβ31-35: Reverse-turn conformation and side-chain interactions revealed by x-ray diffraction. J. Struct. Biol. 141: 156-170.
9. Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, D.J., Swaminathan, S., and Karplus, M. 1983. CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4: 187-217.
10. Broome, B.M. and Hecht, M.H. 2000. Nature disfavors sequences of alternating polar and non-polar amino acids: Implications for amyloidogenesis. J. Mol. Biol. 296: 961-968.
11. Chiti, F., Calamai, M., Taddei, N., Stefani, M., Ramponi, G., and Dobson, C.M. 1999. Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases. Proc. Natl. Acad. Sci. 99: 16419-16426.
12. Chiti, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C.M. 2003. Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 424: 805-808.
13. Dobson, C.M. 1999. Protein misfolding, evolution and disease. Trends Biochem. Sci. 24: 329-332.
14. DuBay, K.F., Pawar, A.P., Chiti, F., Zurdo, J., Dobson, C.M., and Vendruscolo, M. 2004. Predicting absolute aggregation rates of amyloidogenic polypeptide chains. J. Mol. Biol. 341: 1317-1326.
15. Dzwolak, W., Muraki, T., Kato, M., and Taniguchi, Y. 2004. Chain-length dependence of α-helix to β-sheet transition in polylysine: Model of protein aggregation studied by temperature-tuned FTIR spectroscopy. Biopolymers 73: 463-469.
16. El-Agnaf,O.M.A., Sheridan, J.M., Sidera, C., Siligardi, G.,Hussain, R.,Haris, P.I., and Austen, B.M. 2001. Effect of the disulfide bridge and the C-terminal extension on the oligomerization of the amyloid peptide ABri implicated in familial British dementia. Biochemistry 40: 3449-3457.
17. El-Agnaf, O.M.A., Gibson, G., Lee, M., Wright, A., and Austen, B.M. 2004. Properties of neurotoxic peptides related to the Bri gene. Protein Pept. Lett. 11: 202-212.
18. Ferguson, N., Berriman, J., Petrovich, M., Sharpe, T.D., Finch, J.T., and Fersht, A.R. 2003. Rapid amyloid fibril formation from the fast-folding WW domain FBP28. Proc. Natl. Acad. Sci. 100: 9814-9819.
19. Fernandez Escamilla, A.M., Rousseau, F., Schymkowitz, J., and Serrano, L. 2004. Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotech. 22: 1302-1306.
20. Ferrara, P., Apostolakis, J., and Caflisch,A. 2002. Evaluation of a fast implicit solvent model for molecular dynamics simulations. Proteins 46: 24-33.
21. Fersht, A.R. 1999. Structure and mechanism in protein science. Freeman and Co., New York.
22. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R.D., and Bairoch, A. 2003. Expasy: The proteomics server for in depth protein knowledge and analysis. Nucleic Acids Res. 31: 3784-3788.
23. Gazit, E. 2002. A possible role for π-stacking in the self-assembly of amyloid fibrils. FASEB J. 16: 77-83.
24. Gordon, D.J., Balbach, J.J., Tycko, R., and Meredith, S.C. 2004. Increasing the amphiphilicity of an amyloidogenic peptide changes the β-sheet structure in the fibrils from antiparallel to parallel. Biophys. J. 86: 428-434.
25. Gsponer, J., Habertuer, U., and Caflisch, A. 2003. The role of side-chain interactions in the early steps of aggregation: Molecular dynamics simulations of an amyloid-forming peptide from the yeast prion Sup35. Proc. Natl. Acad. Sci. 100: 5154-5159.
26. Haggqvist, B., Naeslund, J., Sletten, K., Westermark, G.T., Mucchiano, G., Tjernberg, L.O., Nordstedt, C., Engstroem, U., and Westermark, P. 1999. Medin: An integral fragment of aortic smooth muscle cell-produced lactadherin forms the most common human amyloid. Proc. Natl. Acad. Sci. 96: 8669-8674.
27. Hill, A.F., Joiner, S., Linehan, J., Desbruslais, M., Lantos, P.L., and Collinge, J. 2000. Species-barrier-independent prion replicates in apparently resistant species. Proc. Natl. Acad. Sci. 97: 10248-10253.
28. Horwich, A.L. and Weissman, J.S. 1997. Deadly conformations-protein misfolding disease. Cell 89: 499-510.
29. Hwang, W., Zhang, S., Kamm, R.D., and Karplus, M. 2004. Kinetic control of dimer structure formation in amyloid fibrillogenesis. Proc. Natl. Acad. Sci. 101: 12916-12921.
30. Jaroniec, C.P., MacPhee, C.E., Astrof, N.S., Dobson, C.M., and Griffin, R.G. 2002. Molecular conformation of a peptide fragment of transthyretin in an amyloid fibril. Proc. Natl. Acad. Sci. 99: 16748-16753.
31. Jarrett, J., Berger, E.P., and Lansbury Jr., P.T. 1993. The carboxyl terminus of the β amyloid protein critical for the seeding of amyloid formation: Implications for the pathogenesis of Alzheimer's disease. Biochemistry 32: 4693-4697.
32. Jenkins, J. and Pickersgill, R. 2001. The architecture of parallel β-helices and related folds. Prog. Biophys. Mol. Biol. 77: 111-115.
33. Jimenez, J.L., Nettleton, E.J., Bouchard, M., Robinson, C.V., Dobson, C.M., and Saibil, H.R. 2002. The protofilament structure of insulin amyloid fibrils. Proc. Natl. Acad. Sci. 99: 9196-9201.
34. 2 microglobulin - Insights into the mechanism of fibril formation in vitro. J. Mol. Biol. 325: 249-257.
35. Kangas, H., Paunio, T., Kalkkinen, N., Jalanko, A., and Peltonen, L. 1996. In vitro expression analysis shows that the secretory form of Gelsolin is the sole source of amyloid in Gelsolin-related amyloidosis. Hum. Mol. Genet. 5: 1237-1244.
36. Kayed, R., Bernhagen, J., Greenfield, N., Sweimeh, K., Brummer, H., Voelter, W., and Kapurniotu, A. 1999a. Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro. J. Mol. Biol. 287: 781-796.
37. _. 1999b. Partial molar volume, surface area, and hydration changes for equilibrium unfolding and formation of aggregation transition state: High-pressure and cosolute studies on recombinant human IFN-γ. J. Mol. Biol. 287: 781-796.
38. Kelly, J. 1998. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 8: 101-106.
39. King, C.Y., Tittmann, P., Gross, H., Gebert, R., Aebi, M., and Wuethrich, K. 1997. Prion-inducing domain 2-114 of yeast Sup35 protein transforms in vitro into amyloid-like filaments. Proc. Natl. Acad. Sci. 94: 6618-6622.
40. Konno, T., Murata, K., and Nagayama, K. 1999. Amyloid-like aggregates of a plant protein: A case of sweet tasting protein, monellin. FEBS Lett. 454: 122-126.
41. Kozin, S.A., Bertho, G., Mazur, A.K., Rabesona, H., Girault, J.P., Haerlthé, T., Takahashi, M., Debey, P., and Hui Bon Hoa, G. 2001. Sheep prion protein synthetic peptide spanning helix 1 and β-strand 2 residues 142-166 shows β-hairpin structure in solution. J. Biol. Chem. 49: 46364-46370.
42. Kusumoto, Y., Lomakin, A., Teplow, D.B., and Benedek, G.B. 1998. Temperature dependence of amyloid β-protein fibrillization. Proc. Natl. Acad. Sci. 95: 12277-12282.
43. Linding, R., Schymkowitz, J., Rousseau, J., Diella, F., and Serrano, L. 2004. A comparative study of the relationship between protein structure and β-aggregation in globular and intrinsically disordered proteins. J. Mol. Biol. 342: 345-353.
44. Litvinovich, S.V., Brew, S.A., Aota, S., Akiyama, S.K., Haudenschild, C., and Ingham, K.C. 1998. Formation of amyloid like fibrils by self-association of a partially unfolded fibronectin type III module. J. Mol. Biol. 280: 245-258.
45. 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 quantitation of rate constants. Proc. Natl. Acad. Sci. 93: 1125-1129.
46. 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. 94: 7942-7947.
47. Makin, O.S., Atkins, E., Sikorski, P., Johansson, J., and Serpell, L.C. 2005. Molecular basis for amyloid fibril formation and stability. Proc. Natl. Acad. Sci. 102: 315-320.
48. Marcotte, E.M. and Eisenberg, D. 1999. Chicken prion tandem repeats form a stable, protease-resistant domain. Biochemistry 38: 667-676.
49. Margittai, M. and Langen, R. 2004. Template-assisted filament growth by parallel stacking of τ. Proc. Natl. Acad. Sci. 101: 10279-10283.
50. Massi, F. and Straub, J.E. 2001. Energy landscape theory for Alzheimer's amyloid β-peptide fibril elongation. Proteins 42: 217-229.
51. Matthews, D. and Cooke, B. 2003. The potential for transmissible spongiform encephalopathies in non-ruminant livestock and fish. Rev. Sci. Tech. 22: 283-296.
52. McGaughey, G.B., Gagné, M., and Rappé, A.K. 1998. π-Stacking interaction. J. Biol. Chem. 273: 15458-15463.
53. Michelitsch, M.D. and Weissman, J.S. 2000. A census of glutamine/asparagine-rich regions: Implications for their conserved function and the prediction of novel prions. Proc. Natl. Acad. Sci. 97: 11910-11915.
54. Munishkina, L.A., Fink, A.L., and Uversky, V.U. 2004. Conformational prerequisites for formation of amyloid fibrils from histones. J. Mol. Biol. 342: 1305-1324.
55. Nahway, N. 1989. The Merck index. Merck and Co., Inc., Whitehouse Station, NJ.
56. Nguyen, J., Baldwin, M.A., Cohen, F.E., and Prusiner, S.B. 1995. Prion protein peptides induce α-helix to β-sheet conformational transitions. Biochemistry 34: 4186-4192.
57. Nichols, W.C., Dwulet, F.E., Liepnieks, J., and Benson, M.D. 1988. Variant apolipoprotein AI as a major constituent of a human hereditary amyloid. Biochem. Biophys. Res. Commun. 156: 762-768.
58. 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.
59. Perutz, M.F. 1999. Glutamine repeats and neurodegenerative diseases: Molecular aspects. Trends Biochem. Sci. 24: 58-64.
60. Perutz, M.F., Johnson, T., Suzuki, M., and Finch, J.T. 1994. Glutamine repeats as polar zippers: Their possible role in inherited neurodegenerative diseases. Proc. Natl. Acad. Sci. 91: 5355-5358.
61. Porat, Y., Stepensky, A., Ding, F.X., Naider, F., and Gazit, E. 2003. Completely different amyloidogenic potential of nearly identical peptide fragments. Biopolymers 69: 161-163.
62. Prusiner, S.B. 1988. Prions. Proc. Natl. Acad. Sci. 95: 13363-13383.
63. Rochet, J.C. and Lansbury Jr., P.T. 2000. Amyloid fibrillogenesis: Themes and variations. Curr. Opin. Struct. Biol. 10: 60-68.
64. Scherzinger, E., Lurz, R., Turmaine, M., Mangiarini, L., Hollenback, B., Hasenbank, R., Bates, G.P., Davies, S.W., Lehrack, H., and Wanker, E. 1997. Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90: 549-558.
65. Soto, C. and Castilla, J. 2004. The controversial protein-only hypothesis of prion propagation. Nat. Med. 10: S63-S67.
66. Stefani, M. and Dobson, C.M. 2003. Protein aggregation and aggregate toxicity: New insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81: 678-699.
67. Tanaka, M., Morishima, I., Akagi, T., Hashikawa, T., and Nukina, N. 2001. Intra and intermolecular β-pleated sheet formation in glutamine-repeat inserted myoglobin as a model for polyglutamine diseases. J. Biol. Chem. 276: 45470-45475.
68. Tartaglia, G.G., Cavalli, A., Pellarin, R., and Caflisch, A. 2004. The role of aromaticity, exposed surface, and dipole moment in determining protein aggregation rates. Protein Sci. 13: 1939-1941.
69. Tartaglia, G.G., Pellarin, R., Cavalli, A., and Caflisch, A. 2005. Organism complexity anti-correlates with proteomic β-aggregation propensity. Protein Sci. (this issue).
70. Tenidis, K., Waldner, M., Bernhagen, J., Fischle, W., Bermann, M., Weber, M., Merkle, M., Voelter, W., Brunner, 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.
71. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
72. Tjernberg, L., Hosia, W., Bark, N., Thyberg, J., and Johansson, J. 2002. Charge attraction and β-propensity are necessary for amyloid fibril formation from tetrapeptides. J. Biol. Chem. 277: 43243-43246.
73. Torok, M., Milton, S., Kayed, R., Wu, P., Intire, T.M., Glabe, C., and Langen, R. 2002. Structural and dynamic features of Alzheimer Aβ peptide in amyloid fibrils studied by site-directed spin labeling. J. Biol. Chem. 277: 40810-40815.
74. Ueda, K., Fukushima, H., Masliah, E., Xia, Y., Iwai, A., Yoshimoto, M., Otero, D.A., Kondo, J., Ihara, Y., and Saitoh, T. 1993. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. 90: 11282-11286.
75. Vanik, D.L., Surewicz, K.A., and Surewicz, W.K. 2004. Molecular basis of barriers for intraspecies transmissibility of mammalian prions. Mol. Cell 14: 139-145.
76. 311) forming β-structure. Proc. Natl. Acad. Sci. 97: 5129-5134.
77. Weidemann, A., Konig, G., Bunke, D., Fisher, P., Salbaum, J.M., Masters, C.L., and Beyreuther, K. 1989. Identification, biogenesis and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell 57: 115-126.
78. Westermark, P., Wernstedt, C., Wilander, E., Hayden, D.W., O'Brien, T.D., and Johnson, K.H. 1987. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl. Acad. Sci. 84: 3881-3885.
79. Westermark, G.T., Engstrom, U., and Westermark, P. 1992. The N-terminal segment of protein AA determines its fibrillogenic propensity. Biochem. Biophys. Res. Commun. 182: 27-32.
80. 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.
81. Zoete, V., Michielin, O., and Karplus, M. 2003. Protein-ligand binding free energy estimation using molecular mechanics and continuum electrostatics. Application to HIV-1 protease inhibitors. J. Comput. Aided Mol. Des. 17: 861-880.