Induction of β-sheet structure in amyloidogenic peptides by neutralization of aspartate: A model for amyloid nucleation

Journal of Molecular Biology

Volumn 289, Issue 2, 1999, Pages 413-428

  Orpiszewski, Jozef ^a   Benson, Merrill D ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Richard L Roudeboush Vet Aff M   (United States)

Author keywords

Alzheimer disease; Amyloid nucleation; Post translational modification; hairpin; sheet

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; ASPARTIC ACID; ESTER; GLUTAMIC ACID; PEPTIDE; SERUM AMYLOID A; SUCCINIMIDE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOIDOSIS; ARTICLE; BETA CHAIN; CHEMICAL MODIFICATION; CYCLIZATION; PH; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

EID: 0033522983     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2768     Document Type: Article

References (57)

1. Aswad D. W. Protein carboxyl methylation in eukaryotes. Curr. Opin. Cell Biol. 1:1989;1182-1187.
2. Aswad, D. W. 1995, Editor of Deamidation and Isoaspartate Formation in Peptides and Proteins, CRC Series in Analytical Biotechnology, CRC Press, Boca Raton.
3. Bai Y., Englander J. J., Mayne L., Milne J. S., Englander S. W. Thermodynamic parameters from hydrogen exchange measurements. Methods Enzymol. 259:1995;344-356.
4. Barrow C. J., Yasuda A., Kenny P. T., Zagorski M. G. Solution conformations and aggregational properties of synthetic amyloid β-peptides of Alzheimer's disease. Analysis of circular dichroism spectra. J. Mol. Biol. 225:1992;1075-1093.
5. Benson M. D. Amyloidosis. Scriver C. R., Beandet A. L., Sly W. S., Valle D. Metabolic Basis of Inherted Disease. 1995;4159-4191 McGraw-Hill Inc. New York.
6. Bischoff R., Kolbe H. V. Deamidation of asparagine and glutamine residues in proteins and peptides: structural determinants and analytical methodology. J. Chromatog. B Biomed. Appl. 662:1994;261-278.
7. Blanco F. J., Jimenez M. A., Pineda A., Rico M., Santoro J., Nieto J. L. NMR solution structure of the isolated N-terminal fragment of protein-G B1 domain. Evidence for trifluoroethanol induced native-like β-hairpin formation. Biochemistry. 33:1994;6004-6014.
8. Blanco F., Ramirez-Alvarado M., Serrano L. Formation and stability of β-hairpin structures in polypeptides. Curr. Opin. Struct. Biol. 8:1998;107-111.
9. Bodkin M. J., Goodfellow J. M. Hydrophobic solvation in aqueous trifluoroethanol solution. Biopolymers. 39:1996;43-50.
10. Bohlen P., Stein S., Dairman W., Udenfriend S. Fluorometric assay of proteins in the nanogram range. Arch. Biochem. Biophys. 155:1973;213-220.
11. Brennan T. V., Clarke S. Deamidation and isoaspartate formation in model synthetic peptides: the effects of sequence and solution environment. Aswad D. W. Deamidation and Isoaspartate Formation in Peptides and Proteins. 1995;65-90 CRC Press, Boca Raton.
12. Cerpa R., Cohen F. E., Kuntz I. D. Conformational switching in designed peptides: the helix/sheet transition. Fold. Des. 1:1996;91-101.
13. Chazin W. J., Kossiakoff A. A. The role of secondary and tertiary structures in intramolecular deamidation of proteins. Aswad D. W. Deamidation and Isoaspartate Formation in Peptides and Proteins. 1995;193-206 CRC Press, Boca Raton.
14. Clarke J., Itzhaki L. S. Hydrogen exchange and protein folding. Curr. Opin. Struct. Biol. 8:1998;112-118.
15. Clarke S. Propensity for spontaneous succinimide formation from aspartyl and asparaginyl residues in cellular proteins. Int. J. Pept. Protein Res. 30:1987;808-821.
16. Cleland J. L., Powell M. F., Shire S. J. The development of stable protein formulations: a closer look at protein aggregation, deamidation, and oxidation. CRC Crit. Rev. Therapeutic Drug Carrier Systems. 10:1993;307-377.
17. David C. L., Orpiszewski J., Zhu X.-C., Reissner K. J., Aswad D. W. Isoaspartate in chrondroitin sulfate proteoglycans of mammalian brain. J. Biol. Chem. 273:1998;32063-32070.
18. Dyson H. J., Bolinger L., Feher V. A., Osterhout J. J., Yao J., Wright P. E. Sequence requirements for stabilization of a peptide reverse turn in water solution. Eur. J. Biochem. 255:1998;462-471.
19. Fabian H., Szendrei G. I., Mantsch H. H., Greenberg B. D., Otvos L. Jr. Synthetic post-translationally modified human A β peptide exhibits a markedly increased tendency to form β-pleated sheets in vitro. Eur. J. Biochem. 221:1994;959-964.
20. Gafni A. Structural modifications of proteins during aging. J. Am. Geriatr. Soc. 45:1997;871-880.
21. Glenner G. G. Amyloid deposits and amyloidosis. The β-fibrilloses (first of two parts). New Engl. J. Med. 302:1980;1283-1292.
22. Ilyina E., Roongta V., Mayo K. H. NMR structure of a de novo designed, peptide 33mer with two distinct, compact β-sheet folds. Biochemistry. 36:1997;5245-5250.
23. Jarrett J. T., Lansbury P. T. Jr. Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry. 31:1992;12345-12352.
24. Johnson B. A., Aswad D. W. Enzymatic protein carboxyl methylation at physiological pH: cyclic imide formation explains rapid methyl turnover. Biochemistry. 24:1985a;2581-2586.
25. Johnson B. A., Aswad D. W. Identification and topography of substrates for protein carboxyl methyltransferase in synaptic membranes and myelin-enriched fractions of bovine and rat brain. J. Neurochem. 45:1985b;1119-1127.
26. Johnson B. A., Shirokawa J. M., Aswad D. W. Deamidation of calmodulin at neutral and alkaline pH: quantitative relationships between ammonia loss and the susceptibility of calmodulin to modification by protein carboxyl methyltransferase. Arch. Biochem. Biophys. 268:1989;276-286.
27. Johnson B. A., Ngo S. Q., Aswad D. W. Widespread phylogenetic distribution of a protein methyltransferase that modifies L-isoaspartyl residues. Biochem. Int. 24:1991;841-847.
28. Johnson B. A., Najbauer J., Aswad D. W. Accumulation of substrates for protein L-isoaspartyl methyltransferase in adenosine dialdehyde-treated PC12 cells. J. Biol. Chem. 268:1993;6174-6181.
29. Kim E., Lowenson J. D., MacLaren D. C., Clarke S., Young S. G. Deficiency of a protein-repair enzyme results in the accumulation of altered proteins, retardation of growth, and fatal seizures in mice. Proc. Natl Acad. Sci. USA. 94:1997;6132-6137.
30. Kirschner D. A., Elliott-Bryant R., Szumowski K. E., Gonnerman W. A., Kindy M. S., Sipe J. D., Cathcart E. S. In vitro amyloid fibril formation by synthetic peptides corresponding to the amino terminus of apoSAA isoforms from amyloid-susceptible and amyloid-resistant mice. J. Struct. Biol. 124:1998;88-98.
31. Kossiakoff A. A. Tertiary structure is a principal determinant to protein deamidation. Science. 240:1988;191-194.
32. Kuo Y.-M., Webster S., Emmerling M. R., De Lima N., Roher A. E. Irreversible dimerization/tetramerization and post-translational modifications inhibit degradation of Aβ peptides of Alzheimer's disease. Biochim. Biophys. Acta. 1406:1998;291-298.
33. Manning M. C., Illangasekare M., Woody R. W. Circular dichroism studies of distorted α-helices, twisted β-sheet, and β-turns. Biophys. Chem. 31:1988;77-86.
34. McFadden P. N., Clarke S. Chemical conversion of aspartyl peptides to isoaspartyl peptides. J. Biol. Chem. 261:1986;11503-11511.
35. Mori H., Ishii K., Tomiyama T., Furiya Y., Sahara N., Asano S., Endo N., Shirasawa T., Takio K. Racemization: its biological significance on neuropathogenesis of Alzheimer's disease. Tohoku J. Expt. Med. 174:1994;251-262.
36. Najbauer J., Orpiszewski J., Aswad D. W. Molecular aging of tubulin: accumulation of isoaspartyl sites in vitro and in vivo. Biochemistry. 35:1996;5183-5190.
37. Noguchi S., Satow Y., Uchida T., Sasaki C., Matsuzaki T. Crystal structure of Ustilago sphaerogena ribonuclease U2 at 1.8 Å resolution. Biochemistry. 34:1995;15583-15591.
38. Noguchi S., Miyawaki K., Satow Y. Succinimide and isoaspartate residues in the crystal structures of hen egg-white lysozyme complexed with tri-N-acetylchitotriose. J. Mol. Biol. 278:1998;231-238.
39. Orpiszewski J., Aswad D. W. High mass methyl-accepting protein (HMAP), a highly effective endogenous substrate for protein L-isoaspartyl methyltransferase in mammalian brain. J. Biol. Chem. 271:1996;22965-22968.
40. Paranandi M. V., Aswad D. W. Spontaneous alterations in the covalent structure of synapsin I during in vitro aging. Biochem. Biophys. Res. Commun. 212:1995;442-448.
41. Radkiewicz J. L., Zipse H., Clarke S., Houk K. N. Accelerated racemization of aspartic acid and asparagine residues via succinimide intermediates: an ab initio theoretical exploration of mechanism. J. Am. Chem. Soc. 118:1996;9148-9155.
42. Reiersen H., Clarke A. R., Rees A. R. Short elastin-like peptides exhibit the same temperature-induced structurel transitions as elastin polymers: implications for protein engineering. J. Mol. Biol. 283:1998;255-264.
43. Richardson J. S., Richardson D. C. Principles and patterns of protein conformation. Fasman G. D. Prediction of Protein Structure and the Principles of Protein Conformation. 1989;1-98 Plenum Press, New York and London.
44. Roher A. E., Lowenson J. D., Clarke S., Wolkow C., Wang R., Cotter R. J., Reardon I. M., Zurcher-Neely H. A., Heinrikson R. L., Ball M. J. et al. Structural alterations in the peptide backbone of β-amyloid core protein may account for its deposition and stability in Alzheimer's disease. J. Biol. Chem. 268:1993a;3072-3083.
45. Roher A. E., Lowenson J. D., Clarke S., Woods A. S., Cotter R. J., Gowing E., Ball M. J. β-Amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer disease. Proc. Natl Acad. Sci. USA. 90:1993b;10836-10840.
46. Schneider J. P., Kelly J. W. Synthesis and efficacy of square planar copper complexes designed to nucleate β-sheet structure. J. Am. Chem. Soc. 117:1995a;2533-2546.
47. Schneider J. P., Kelly J. W. Templates that induce α-helical, β-sheet, and loop conformations. Chem. Rev. 95:1995b;2169-2187.
48. Shahrokh Z., Eberlein G., Buckley D., Paranandi M. V., Aswad D. W., Stratton P., Mischak R., Wang Y. J. Major degradation products of basic fibroblast growth factor: detection of succinimide and iso-aspartate in place of aspartate. Pharmacol. Res. 11:1994;936-944.
49. Shapira R., Austin G. E., Mirra S. S. Neuritic plaque amyloid in Alzheimer's disease is highly racemized. J. Neurochem. 50:1988;69-74.
50. Sibanda B. L., Thornton J. M. Accomodating sequence changes in β-hairpins in proteins. J. Mol. Biol. 229:1993;428-447.
51. Stanger H. E., Gellman S. H. Rules for antiparallel β-sheet design: D-Pro-Gly is superior to L-Asn-Gly for β-hairpin nucleation. J. Am. Chem. Soc. 120:1998;4236-4237.
52. Stephenson R. C., Clarke S. Succinimide formation from aspartyl and asparaginyl peptides as a model for the spontaneous degradation of proteins. J. Biol. Chem. 264:1989;6164-6170.
53. Teshima G., Stults J. T., Ling V., Canova-Davis E. Isolation and characterization of a succinimide variant of methionyl human growth hormone. J. Biol. Chem. 266:1991;13544-13547.
54. Tomiyama T., Asano S., Furiya Y., Shirasawa T., Endo N., Mori H. Racemization of Asp23 residue affects the aggregation properties of Alzheimer amyloid β-protein analogues. J. Biol. Chem. 269:1994;10205-10208.
55. Velazquez P., Cribbs D. H., Poulos T. L., Tenner A. J. Aspartate residue 7 in amyloid β-protein is critical for classical complement pathway activation: implications for Alzheimer's disease pathogenesis. Nature Med. 3:1997;77-79.
56. Yamamoto A., Takagi H., Kitamura D., Tatsuoka H., Nakano H., Kawano H., Kuroyanagi H., Yahagi Y., Kobayashi S., Koizumi K., Sakai T., Saito K., Chiba T., Kawamura K., Suzuki K. et al. Deficiency in protein L-isoaspartyl methyltransferase results in a fatal progressive epilepsy. J. Neurosci. 18:1998;2063-2074.
57. Zhang S., Rich A. Direct conversion of an oligopeptide from a β-sheet to an α-helix: a model for amyloid formation. Proc. Natl Acad. Sci. USA. 94:1997;23-28.