A quantitative analysis of spontaneous isoaspartate formation from N-terminal asparaginyl and aspartyl residues

Amino Acids

Volumn 44, Issue 4, 2013, Pages 1205-1214

  Güttler, Bert H O ^a   Cynis, Holger ^a   Seifert, Franziska ^a,c   Ludwig, Hans Henning ^a   Porzel, Andrea ^b,d   Schilling, Stephan ^a  

^a PROBIODRUG AG   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

1H NMR; Alzheimer's disease; Capillary electrophoresis; Isoaspartate; PIMT

Indexed keywords

ALANYLALANYLASPARAGINYLGLYCYLGLUTAMYLPHENYLALANINE; AMIDE; AMYLOID BETA PROTEIN; ASPARAGINE; ASPARAGINYLGLYCYLGLUTAMYLPHENYLALANINE; ASPARTIC ACID; ISOASPARTIC ACID; ISOTOPE; PEPTIDE; SUCCINIMIDE; UNCLASSIFIED DRUG;

ACIDITY; AMINO ACID ANALYSIS; AMINO TERMINAL SEQUENCE; ARTICLE; CAPILLARY ELECTROPHORESIS; CHEMICAL REACTION; CONTROLLED STUDY; DEPROTONATION; ISOMERIZATION; KINETICS; PH; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; QUANTITATIVE ANALYSIS; VALIDATION STUDY;

ALZHEIMER DISEASE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; ASPARAGINE; ASPARTIC ACID; ELECTROPHORESIS, CAPILLARY; HUMANS; HYDROGEN-ION CONCENTRATION; ISOASPARTIC ACID; ISOMERISM; KINETICS; PLAQUE, AMYLOID; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84876686332     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-012-1454-0     Document Type: Article

References (52)

1. Aswad DW, Paranandi MV, Schurter BT (2000) Isoaspartate in peptides and proteins: formation, significance, and analysis. J Pharm Biomed Anal 21:1129-1136 (Pubitemid 30001541)
2. Barnett RE, Jencks WP (1969) Diffusion-controlled proton transfer in intramolecular thiol ester aminolysis and thiazoline hydrolysis. J Am Chem Soc 91:2358-2369
3. Böhme L, Bär JW, Hoffmann T, Manhart S, Ludwig HH, Rosche F, Demuth HU (2008a) Isoaspartate residues dramatically influence substrate recognition and turnover by proteases. Biol Chem 389:1043-1053
4. Böhme L, Hoffmann T, Manhart S, Wolf R, Demuth HU (2008b) Isoaspartate containing amyloid precursor protein derived peptides alter efficacy and specificity of potential beta-secretases. Biol. Chem. 389:1055-1066
5. Capasso S, Mazzarella L, Sica F, Zagari A, Salvadori S (1993) Kinetics and mechanism of succinimide ring formation in the deamidation process of asparagine residues. J Chem Soc Perkin Trans 2:679-682
6. Carter WG, Aswad DW (2008) Formation, localization, and repair of L-isoaspartyl sites in histones H2A and H2B in nucleosomes from rat liver and chicken erythrocytes. Biochemistry 47:10757-10764
7. Clarke S (1985) Protein carboxyl methyltransferases: two distinct classes of enzymes. Annu Rev Biochem 54:479-506 (Pubitemid 15073655)
8. Cook PF (1991) Enzyme mechanism from isotope effects. CRC press, Boca Raton
9. Corti A, Curnis F (2011) Isoaspartate-dependent molecular switches for integrin-ligand recognition. J Cell Sci 124:515-522
10. Cox MM, Jencks WP (1978) General acid catalysis of the aminolysis of phenyl acetate by a preassociation mechanism. J Am Chem Soc 100:5956-5957
11. Di Fede G, Catania M, Morbin M, Rossi G, Suardi S, Mazzoleni G, Merlin M, Giovagnoli AR, Prioni S, Erbetta A, Falcone C, Gobbi M, Colombo L, Bastone A, Beeg M, Manzoni C, Francescucci B, Spagnoli A, Cantù L, Del Favero E, Levy E, Salmona M, Tagliavini F (2009) A recessive mutation in the APP gene with dominant-negative effect on amyloidogenesis. Science 323:1473-1477
12. Ellis KJ, Morrison JF (1982) Buffers of constant ionic strength for studying pH-dependent processes. Methods Enzymol 87:405-426
13. Geiger T, Clarke S (1987) Deamidation, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation. J Biol Chem 262:785-794 (Pubitemid 17005254)
14. George-Nascimento C, Lowenson J, Borissenko M, Calderon M, Medina-Selby A, Kuo J, Clarke S, Randolph A (1990) Replacement of a labile aspartyl residue increases the stability of human epidermal growth factor. Biochemistry 29:9584-9591 (Pubitemid 20355205)
15. Haass C, Lemere CA, Capell A, Citron M, Seubert P, Schenk D, Lannfelt L, Selkoe DJ (1995) The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway. Nat Med 1:1291-1296
16. He W, Barrow CJ (1999) The A beta 3-pyroglutamyl and 11-pyroglutamyl peptides found in senile plaque have greater beta-sheet forming and aggregation propensities in vitro than full-length A beta. Biochemistry 38:10871-10877 (Pubitemid 29404419)
17. Jonsson T, Atwal JK, Steinberg S, Snaedal J, Jonsson PV, Bjornsson S, Stefansson H, Sulem P, Gudbjartsson D, Maloney J, Hoyte K, Gustafson A, Liu Y, Lu Y, Bhangale T, Graham RR, Huttenlocher J, Bjornsdottir G, Andreassen OA, Jonsson EG, Palotie A, Behrens TW, Magnusson OT, Kong A, Thorsteinsdottir U, Watts RJ, Stefansson K (2012) A mutation in APP protects against Alzheimer's disease and age-related cognitive decline. Nature 488:96-99
18. Kummer MP, Hermes M, Delekarte A, Hammerschmidt T, Kumar S, Terwel D, Walter J, Pape HC, König S, Roeber S, Jessen F, Klockgether T, Korte M, Heneka MT (2011) Nitration of tyrosine 10 critically enhances amyloid β aggregation and plaque formation. Neuron 71:833-844
19. Lee JC, Kang SU, Jeon Y, Park JW, You JS, Ha SW, Bae N, Lubec G, Kwon SH, Lee JS, Cho EJ, Han JW (2012) Protein l-isoaspartyl methyltransferase regulates p53 activity. Nat. Commun. 3:927
20. Lowenson JD, Clarke S (1990) Identification of isoaspartyl-containing sequences in peptides and proteins that are usually poor substrates for the class II protein carboxyl methyltransferase. J Biol Chem 265:3106-3110
21. Lowenson JD, Clarke S (1991) Structural elements affecting the recognition of l-isoaspartyl residues by the l-isoaspartyl/d-aspartyl protein methyltransferase. Implications for the repair hypothesis. J Biol Chem 266:19396-19406 (Pubitemid 21908245)
22. Lowenson JD, Clarke S (1992) Recognition of d-aspartyl residues in polypeptides by the erythrocyte l-isoaspartyl/d-aspartyl protein methyltransferase. Implications for the repair hypothesis. J Biol Chem 267:5985-5995
23. Lowenson JD, Roher AE, Clarke S (1994) Protein aging extracellular amyloid formation and intracellular repair. Trends Cardiovasc Med 4:3-8 (Pubitemid 24105442)
24. MacLaren DC, Kagan RM, Clarke S (1992) Alternative splicing of the human isoaspartyl protein carboxyl methyltransferase RNA leads to the generation of a C-terminal -RDEL sequence in isozyme II. Biochem Biophys Res Commun 185:277-283
25. Meinwald YC, Stimson ER, Scheraga HA (1986) Deamidation of the asparaginyl-glycyl sequence. Int J Pept Protein Res 28:79-84
26. Ni W, Dai S, Karger BL, Zhou ZS (2010) Analysis of isoaspartic acid by selective proteolysis with Asp-N and electron transfer dissociation mass spectrometry. Anal Chem 82:7485-7491
27. Noguchi S (2010) Conformational variation revealed by the crystal structure of RNase U2A complexed with Ca ion and 2′-adenylic acid at 1.03 Å resolution. Protein Pept Lett 17:1559-1561
28. Nussbaum JM, Schilling S, Cynis H, Silva A, Swanson E, Wangsanut T, Tayler K, Wiltgen B, Hatami A, Ronicke R, Reymann K, Hutter-Paier B, Alexandru A, Jagla W, Graubner S, Glabe CG, Demuth HU, Bloom GS (2012) Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-beta. Nature 485:651-655
29. Park JW, Lee JC, Ha SW, Bang SY, Park EK, Yi SA, Lee MG, Kim DS, Nam KH, Yoo JH, Kwon SH, Han JW (2012) Requirement of protein l-isoaspartyl O-methyltransferase for transcriptional activation of trefoil factor 1 (TFF1) gene by estrogen receptor alpha. Biochem Biophys Res Commun 420:223-229
30. Patel K, Borchardt RT (1990) Chemical pathways of peptide degradation. II. Kinetics of deamidation of an asparaginyl residue in a model hexapeptide. Pharm Res 7:703-711 (Pubitemid 20278366)
31. Potter SM, Johnson BA, Henschen A, Aswad DW, Guzzetta AW (1992) The type II isoform of bovine brain protein l-isoaspartyl methyltransferase has an endoplasmic reticulum retention signal (.RDEL) at its C-terminus. Biochemistry 31:6339-6347
32. Robinson AB (1974) Evolution and the distribution of glutaminyl and asparaginyl residues in proteins. Proc Natl Acad Sci USA 71:885-888
33. Robinson NE, Robinson AB (2001) Molecular clocks. Proc Natl Acad Sci USA 98:944-949 (Pubitemid 32121167)
34. Robinson AB, Rudd CJ (1974) Deamidation of glutaminyl and asparaginyl residues in peptides and proteins. Curr Top Cell Regul 8:247-295
35. Robinson AB, McKerrow JH, Cary P (1970) Controlled deamidation of peptides and proteins: an experimental hazard and a possible biological timer. Proc Natl Acad Sci USA 66:753-757
36. Roher AE, Lowenson JD, Clarke S, Wolkow C, Wang R, Cotter RJ, Reardon IM, Zurcher-Neely HA, Heinrikson RL, Ball MJ (1993) Structural alterations in the peptide backbone of beta-amyloid core protein may account for its deposition and stability in Alzheimer's disease. J Biol Chem 268:3072-3083 (Pubitemid 23070928)
37. Saido TC, Yamao-Harigaya W, Iwatsubo T, Kawashima S (1996) Amino- and carboxyl-terminal heterogeneity of beta-amyloid peptides deposited in human brain. Neurosci Lett 215:173-176 (Pubitemid 26323454)
38. Sargaeva NP, Lin C, O'Connor PB (2011) Differentiating N-terminal aspartic and isoaspartic acid residues in peptides. Anal Chem 83:6675-6682
39. Satterthwait AC, Jencks WP (1974) The mechanism of the aminolysis of acetate esters. J Am Chem Soc 96:7018-7031
40. Schilling S, Hoffmann T, Manhart S, Hoffmann M, Demuth HU (2004) Glutaminyl cyclases unfold glutamyl cyclase activity under mild acid conditions. FEBS Lett 563:191-196 (Pubitemid 38471597)
41. Schilling S, Lauber T, Schaupp M, Manhart S, Scheel E, Bohm G, Demuth HU (2006) On the seeding and oligomerization of pGlu-amyloid peptides (in vitro). Biochemistry 45:12393-12399 (Pubitemid 44583682)
42. Schilling S, Zeitschel U, Hoffmann T, Heiser U, Francke M, Kehlen A, Holzer M, Hutter-Paier B, Prokesch M, Windisch M, Jagla W, Schlenzig D, Lindner C, Rudolph T, Reuter G, Cynis H, Montag D, Demuth HU, Rossner S (2008) Glutaminyl cyclase inhibition attenuates pyroglutamate Abeta and Alzheimer's disease-like pathology. Nat Med 14:1106-1111
43. Schlenzig D, Manhart S, Cinar Y, Kleinschmidt M, Hause G, Willbold D, Funke SA, Schilling S, Demuth HU (2009) Pyroglutamate formation influences solubility and amyloidogenicity of amyloid peptides. Biochemistry 48:7072-7078
44. Seifert F, Schulz K, Koch B, Manhart S, Demuth HU, Schilling S (2009) Glutaminyl cyclases display significant catalytic proficiency for glutamyl substrates. Biochemistry 48:11831-11833
45. Shimizu T, Watanabe A, Ogawara M, Mori H, Shirasawa T (2000) Isoaspartate formation and neurodegeneration in Alzheimer's disease. Arch Biochem Biophys 381:225-234 (Pubitemid 32260308)
46. Stephenson RC, Clarke S (1989) Succinimide formation from aspartyl and asparaginyl peptides as a model for the spontaneous degradation of proteins. J Biol Chem 264:6164-6170 (Pubitemid 19106686)
47. Varshavsky A (1996) The N-end rule: functions, mysteries, uses. Proc Natl Acad Sci USA 93:12142-12149 (Pubitemid 26367109)
48. Velazquez P, Cribbs DH, Poulos TL, Tenner AJ (1997) Aspartate residue 7 in amyloid beta-protein is critical for classical complement pathway activation: implications for Alzheimer's disease pathogenesis. Nat Med 3:77-79 (Pubitemid 27019145)
49. Wagenknecht H-A, Knapp H (2009) Roempp Online. Version 3.5
50. Weber DJ, McFadden PN (1997) Injury-induced enzymatic methylation of aging collagen in the extracellular matrix of blood vessels. J Protein Chem 16:269-281 (Pubitemid 27242351)
51. Young AL, Carter WG, Doyle HA, Mamula MJ, Aswad DW (2001) Structural integrity of histone H2B in vivo requires the activity of protein l-isoaspartate O-methyltransferase, a putative protein repair enzyme. J Biol Chem 276:37161-37165
52. Young GW, Hoofring SA, Mamula MJ, Doyle HA, Bunick GJ, Hu Y, Aswad DW (2005) Protein l-isoaspartyl methyltransferase catalyzes in vivo racemization of aspartate-25 in mammalian histone H2B. J Biol Chem 280:26094-26098 (Pubitemid 41022202)