High level of aspartic acid-bond isomerization during the synthesis of an N-linked τ glycopeptide

Journal of Peptide Science

Volumn 5, Issue 10, 1999, Pages 442-456

  Hoffmann, Ralf ^a,b   Craik, David J ^c   Bokonyi, Krisztina ^a   Varga, Istvan ^a   Otvos Jr , Laszlo ^a  

^a WISTAR INSTITUTE   (United States)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

peptide; Chromatography; Edman degradation; Nuclear magnetic resonance spectroscopy; Paired helical filaments

Indexed keywords

ASPARAGINE LINKED OLIGOSACCHARIDE; ASPARTIC ACID; GLYCOPEPTIDE; N ACETYLGLUCOSAMINE; OLIGOPEPTIDE; TAU PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ISOMERISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY;

AMINO ACID SEQUENCE; ASPARTIC ACID; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; ISOMERISM; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; SEQUENCE ANALYSIS, PROTEIN; TAU PROTEINS;

EID: 0032724924     PISSN: 10752617     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1099-1387(199910)5:10<442::AID-PSC214>3.0.CO;2-Q     Document Type: Article

References (52)

1. Kihlberg J, Eloffson M, Salvador LA. Direct synthesis of glycosylated amino acids from carbohydrate peracetates and Fmoc amino acids: solid-phase synthesis of biomedicinally interesting glycopeptides. In Methods in Enzymology, Solid-Phase Peptide Synthesis, vol. 289, Fields GB (ed.). Academic Press: San Diego, 1997; 221-245.
2. Perich JW. Synthesis of phosphopeptides using modern chemical approaches. In Methods in Enzymology, Solid-Phase Peptide Synthesis, vol. 289, Fields GB (ed.). Academic Press: San Diego, 1997; 245-266.
3. Meldal M, St. Hilaire PM. Synthesis methods of Glycopeptide assembly, and biological analysis of glycopeptide products. Curr. Opin. Chem. Biol. 1997; 1: 552-563.
4. Haurum JS, Arsequell G, Lellouch AC, Wong SYC, Dwek RA, McMichael AJ, Elliott T. Recognition of carbohydrate by major histocompatibility complex class I-restricted, glycopeptide-specific cytotoxic T lymphocytes. J. Exp. Med. 1994; 180: 739-744.
5. Hoffmann R, Lee VM-Y, Leight S, Varga I, Otvos Jr L. Unique Alzheimer's disease paired helical filament specific antibodies involve double phosphorylation at specific sites. Biochemistry 1997; 36: 8114-8124.
6. Otvos Jr L, Thurin J, Kollat E, Urge L, Mantsch HH, Hollosi MM. Glycosylation of synthetic peptides breaks helices; phosphorylation results in distorted structure. Int. J. Pept. Protein Res. 1991; 38: 476-482.
7. Otvos Jr L, Cappelletto B, Varga I, Xiang ZQ, Kaiser K, Stephens LDJ, Ertl HCJ. Comparison of the effects of post-translational side-chain modifications on the serum stability, T helper cell stimulatory activity and conformation of synthetic peptides. Biochim. Biophys. Acta 1996; 1267: 55-64.
8. Polt R, Porreca F, Szabo LZ, Bilsky EJ, Davis P, Abbruscato TJ, Davis TP, Horvath R, Yamamura HI, Hruby VJ. Glycopeptide enkephalin analogues produce analgesia in mice: evidence for penetration of the blood-brain barrier. Proc. Natl. Acad. Sci. USA 1994; 91: 7114-7118.
9. Kitas EA, Johns RB, May CN, Tregear GW, Wade JD. Chemical synthesis of an O-phosphorylated tyrosine analogue of human angiotensin II, [Tyr(P)4] angiotensin II, and its vasoconstrictor effect in intact sheep. Pept. Res. 1993; 3: 205-210.
10. Garg HG, von dem Bruch K, Kunz H. Developments in the synthesis of glycopeptides containing glycosyl L-asparagine, L-serine, and L-threonine. Adv. Carbohydr. Chem. Biochem. 1994; 50: 277-310.
11. Arsequell, G, Valencia G. O-glycosyl α-amino acids as building blocks for glycopeptide synthesis. Tetrahedron: Asymmetry 1997; 8: 2839-2876.
12. Taylor CM. Glycopeptides and glycoproteins: focus on the glycosidic linkage. Tetrahedron 1998; 54: 11317-11362.
13. Otvos Jr L, Wroblewski K, Kollat E, Perczel A, Hollosi M, Fasman GD, Ertl HCJ, Thurin J. Coupling strategies in solid-phase synthesis of glycopeptides. Pept. Res. 1989; 2: 362-366.
14. Otvos Jr L, Urge L, Hollosi M, Wroblewski K, Graczyk G, Fasman GD, Thurin J. Automated solid-phase synthesis of glycopeptides. Incorporation of unprotected mono- and disaccharide units of N-glycoprotein antennae into T cell epitopic peptides. Tetrahedron Lett. 1990; 31: 5889-5892.
15. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. Multiple isoforms of human microtubule-associated protein Tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989; 3: 519-526.
16. Kirschner DA, Abraham C, Selkoe DJ. X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer's disease indicates cross-β conformation. Proc. Natl. Acad. Sci. USA 1986; 84: 6953-6957.
17. Lee VM-Y, Balin BJ, Otvos Jr L, Trojanowski JQ. A68: a major subunit of paired helical filaments and derivatized forms of normal Tau. Science 1991; 251: 675-678.
18. Wille H, Drewes G, Biernat J, Mandelkow E-M, Mandelkow E. Alzheimer-like paired helical filaments and antiparallel dlmers formed from microtubule-associated protein Tau in vitro. J. Cell Biol. 1992; 118: 573-584.
19. Wang, J-Z, Grundke-Iqbal I, Iqbal K. Glycosylation of microtubule-associated protein Tau: an abnormal posttranslational modification in Alzheimer's disease. Nature Med. 1996; 2: 871-875.
20. Butner KA, Kirschner MW. Tau protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol. 1991; 115: 717-730.
21. Otvos Jr L, Pease A-M, Wade JD, Hoffmann R. Glycosylation of the fourth repeat unit of human τ protein abolishes binding to the C-terminal acidic τ-binding segment of β-tubulin. Protein Peptide Lett. 1998; 5: 207-213.
22. Fields GB, Noble RL. Solid-phase peptide synthesis using 9-fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 1990; 35: 161-214.
23. Kaiser E, Colescott RL, Bossinger CD, Cook PI. Color test for detection of free terminal amino groups in the solid-phase synthesis of peptides. Anal. Biochem. 1970; 34: 595-598.
24. Bulet P, Urge L, Ohresser S, Hetru C, Otvos Jr L. Enlarged scale chemical synthesis and range of activity of Drosocin, an O-glycosylated antibacterial peptide from Drosophila. Eur. J. Biochem. 1996; 238: 64-69.
25. Fasman GD. A critique of the utility of the prediction of protein secondary structure. J. Biosci. 1985; 8: 15-23.
26. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMm: a program for macromolecular energy minimization and dynamics calculations. J. Comput. Chem. 1983; 4: 187-217.
27. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Comm. 1983; 113: 967-974.
28. Bax A, Davis DG. MLEV-17 based two-dimensional homonuclear magnetization transfer spectroscopy. J. Mag. Res. 1985; 65: 355-360.
29. Otvos Jr L, Urge L, Szendrei GI, Cappelletto B, Varga I, Prammer K, Ertl HCJ. Exploring the diversity of mono-and ollgosaccharide structures in the synthesis, conformational analysis and biomedical application of glycopeptides. In Solid-Phase Synthesis and Combinatorial Libraries, Epton R (ed.). Mayflower Scientific: Birmigham, 1996; 269-276.
30. Otvos Jr L, Krivulka GR, Urge L, Szendrei GI, Nagy L, Xiang ZQ, Ertl HCJ. Comparison of the effects of amino acid substitutions and β-N- vs. α-O-glycosylation on the T-cell stimulatory activity and conformation of an epitope on the rabies virus glycoprotein. Biochim. Biophys. Acta 1995; 1267: 55-64.
31. Hoffmann R, Bulet P, Urge L, Otvos Jr L. Range of activity and metabolic stability of synthetic antibacterial glycopeptides from insects. Biochim. Biophys. Acta 1999; 1426: 459-467.
32. Barany G, Merrifield RB. Solid-phase peptide synthesis. In The Peptides, vol. 2, Gross E, Meienhofer J (eds). Academic Press: New York, 1979; 1-284.
33. Bodanszky M, Martinez J. Side reactions in peptide synthesis. In The Peptides, vol. 5, Gross E, Meienhofer J (eds). Academic Press: New York, 1983; 111-216.
34. Lauer JL, Fields CG, Fields GB. Sequence dependence of aspartimide formation during 9-fluorenylmethoxycarbonyl solid-phase peptide synthesis. Lett. Pept. Sci. 1994; 1: 197-205.
35. Dolling R, Beyermann M, Haenel J, Kernchen F, Krause E, Franke P, Brudel M, Bienert M. Piperidine-mediated side reactions in Fmoc-strategy. In Solid-Phase Synthesis and Combinatorial Libraries, Epton R (ed). Mayflower Worldwide: Birmingham, 1994; 489-492.
36. Gavel Y, von Heijne G. Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications in protein engineering. Prot. Eng. 1990; 3: 433-442.
37. Robinson AB, Robinson LR. Distribution of glutamine and asparagine residues and their near neighbors in peptides and proteins. Proc. Natl. Acad. Sci. USA 1991; 88: 8880-8884.
38. Urge L, Kollat E, Hollosi M, Laczko I, Wroblewski K, Thurin J, Otvos Jr L. Solid-phase synthesis of glycopeptides: synthesis of N-α-fluorenylmethoxycarbonyl L-asparagine N-β-glycosides. Tetrahedron Lett. 1991; 32: 3445-3448.
39. Angell YM, Garcia-Echeverria C, Rich DH. Comparative studies of the coupling of N-methylated, sterically hindered amino acids during solid-phase peptide synthesis. Tetrahedron Lett. 1994; 35: 5891-5894.
40. Payan IL, Chou S-J, Fisher GH, Man EH, Emory C, Frey II WH. Altered aspartate in Alzheimer neurofibrillary tangles. Neurochem. Res. 1992; 17: 187-191.
41. Roher AE, Lowenson JD, Clarke S, Wolkow C, Wang R, Cotter RJ, Reardon IM, Zurcher-Neely HA, Heinrikson RL, Ball M, Greenberg BD. 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. 1993; 268: 3072-3083.
42. Stephenson RC, Clarke S. Succinimide formation from aspartyl and asparaginyl peptides as a model for the spontaneous degradation of proteins. J. Biol. Chem. 1989; 264: 6164-6170.
43. Szendrei GI, Fabian H, Mantsch HH, Lovas S, Nyeki O, Schon I, Otvos Jr L. Aspartate-bond isomerization affects the major conformations of synthetic peptides. Eur. J. Biochem. 1994; 226: 917-924.
44. Meek JJ. Prediction of peptide retention times in high-pressure liquid chromatography on the basis of amino acid composition. Proc. Natl. Acad. Sci. USA 1988; 77: 1632-1636.
45. Browne CA, Bennett HP, Solomon S. The isolation of peptides by high-performance liquid chromatography using predicted elutlon positions. Anal. Biochem. 1982; 124: 201-208.
46. Buttner K, Pinilla C, Appel JR, Houghten RA. Anomalous reversed-phase high performance liquid chromatographic behavior of synthetic peptides related to antigenic helper T cell lines. J. Chromatogr. 1992; 625: 191-198.
47. Hearn MTW, Aguilar MI. High performance liquid chromatography of amino acids, peptides and proteins LXIX. Evaluation of retention and bandwidth relationships of myosin-related peptides separated by gradient elution reverse-phase high performance liquid chromatography. J. Chromatogr. 1987; 392: 33-49.
48. Clark L, Otvos Jr L, Stein P, Zhang X-M, Skorupa AF, Lesh GE, McMorris FA, Heber-Katz E. Golli-induced paralysis: a study in anergy and disease. J. Immunol. 1999; 162: 4300-4310.
49. McManus A, Otvos Jr L, Hoffmann R, Cralk DJ. Conformational studies by NMR of the anti-microbial peptide, Drosocin and its non-glycosylated derivative: effects of glycosylation on solution conformation. Biochemistry 1999; 38: 705-714.
50. Schon I, Nyeki O. Unprecedented transformation of aspartyl peptides by conjugative degradation. J. Chem. Soc. Chem. Commun. 1994; 393-394.
51. Szendrei GI, Prammer KV, Vasko M, Lee VM-Y, Otvos Jr L. The effects of aspartic acid bond isomerization on in vitro properties of the amyloid β-peptide as modeled with N-terminal decapeptide fragments. Int. J. Pept. Protein Res. 1996; 47: 289-296.
52. Watanabe A, Takio K, Ihara Y. Deamination and isoaspartate formation in smeared tau in paired helical filaments: unusual properties of the microtubule-binding domain of tau. J. Biol. Chem. 1999; 274: 7368-7378.