The role of the cyclic imide in alternate degradation pathways for asparagine-containing peptides and proteins

Journal of Pharmaceutical Sciences

Volumn 96, Issue 10, 2007, Pages 2667-2685

  DeHart, Michael P ^a   Anderson, Bradley D ^a  

^a University of Kentucky   (United States)

Author keywords

Asparagine; Deamidation; Diketopiperazine; Isoasparagine; Kinetics; Peptide delivery; Peptides; Stability

Indexed keywords

AMIDE; AMMONIA; ASPARTIC ACID; BUFFER; GLYCYLISOASPARAGINYLGLYCINE; ISOASPARTIC ACID; PEPTIDE; PHENYLALANYLASPARAGINYLGLYCINE; PIPERAZINEDIONE; SUCCINIMIDE DERIVATIVE; UNCLASSIFIED DRUG;

ALKALINITY; AMINO TERMINAL SEQUENCE; ARTICLE; CONCENTRATION (PARAMETERS); COVALENT BOND; DEAMINATION; DECOMPOSITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOMERIZATION; KINETICS; PEPTIDE SYNTHESIS; PKA; PROTEIN DEGRADATION; PROTEIN STABILITY;

EID: 35349028965     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.20905     Document Type: Article

References (67)

1. Capasso S, Mazzarella L, Zagari A. 1991. Deamidation via cyclic imide of asparaginyl peptides: dependence on salts, buffers, and organic solvents. Peptide Res 4:234-238.
2. Clarke S. 1987. Propensity for spontaneous succinimide formation from aspartyl and asparaginyl residues in celluar proteins. Int J Peptide Protein Res 30:808-821.
3. Clarke S, Stephenson RS, Lowenson JD. 1992. Lability of asparagine and aspartic acid residues in proteins and peptides: spontaneous deamidation and isomerization reactions. In: Ahern TJ, Manning MC, editors. Stability of Protein Pharmaceuticals Part A, New York: Plenum Press. p 1-30.
4. 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.
5. Patel K, Borchardt RT. 1990. Deamidation of asparaginyl residues in proteins: a potential pathway for chemical degradation of proteins in lyophilized dosage forms. J Parent Sci Tech 44:300-301.
6. 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.
7. Wright HT. 1991. Sequence and structure determinants of the nonenzymatic deamidation of asparagine and glutamine residues in proteins. Protein Eng 4:283-294.
8. Meinwald YC, Stimson ER, Scheraga HA. 1986. Deamidation of the asparaginyl-glycyl sequence. Int J Peptide Res 28:79-84.
9. Aswad DW. 1995. Deamidation and isoaspartate formation in peptides and proteins. Boca Raton: CRC Press. p 259.
10. Li B, Borchardt RT, Topp EM, VanderVelde D, Schowen RL. 2003. Racemization of an asparagine residue during peptide deamidation. J Am Chem Soc 125:11486-11487.
11. Robinson AB, Scotchler JW, McKerrow JH. 1973. Rates of nonenzymatic deamidation of glutaminyl and asparaginyl residues in pentapeptides. J Am Chem Soc 95:8156-8159.
12. Wright HT. 1991. Nonenzymatic deamidation of asparaginyl and glutaminyl residues in proteins. Crit Rev Biochem Mol Biol 26:1-52.
13. Capusso S, Mazzarella , Sorrentino G, Balboni G, Kirby AJ. 1996. Kinetics and mechanism of the cleavage of the peptide bond next to asparagine. Peptides 17:1075-1077.
14. Darrington RT, Anderson BD. 1994. The role of intramolecular nucleophilic catalysis and the effects of self-association on the deamidation of human insulin at low pH. Pharm Res 11:784-793.
15. Darrington RT, Anderson BD. 1995. Evidence for a common intermediate in insulin deamidation and covalent dimer formation: effects of pH and aniline trapping in dilute acidic solutions. J Pharm Sci 84:275-282.
16. Patel K, Borchardt RT. 1990. Chemical pathways of peptide degradation. II. Kinetics of deamidation of an asparaginyl residue in a model hexapeptide. Pharm Res 7:703-710.
17. Patel K, Borchardt RT. 1990. Chemical pathways of peptide degradation. III. Effect of primary sequence on the pathways of deamidation of asparaginyl residues in hexapeptides. Pharm Res 7:787-793.
18. Robinson NE, Robinson AB. 2001. Molecular clocks. Proc Natl Acad Sci 98:944-949.
19. Kosky AA, Razzaq UO, Treuheit MJ, Brems DN. 1999. The effects of alpha-helix on the stability of Asn residues: deamidation rates in peptides of varying helicity. Protein Sci 8:2519-2523.
20. Kossiakoff AA. 1988. Tertiary structure is a principal determinant to protein deamidation. Science 240:191-194.
21. McKerrow JH, Robinson AB. 1971. Deamidation of aspariginyl residues as a hazard in experimental protein and peptide procedures. Anal Biochem 42:565-568.
22. Robinson NE, Robinson AB. 2004. Molecular Clocks - Deamidation of Asparaginyl and Glutaminyl Residues in Peptides and Proteins. Cave Junction, OR: Althouse Press. p 419.
23. Robinson NE. 2002. Protein deamidation. Proc Natl Acad Sci 99:5283-5288.
24. Xie M, Schowen RL. 1999. Secondary structure and protein deamidation. J Pharm Sci 88:8-13.
25. Darrington RT, Anderson BD. 1995. Effects of insulin concentration and self-association on the partitioning of its A-21 cyclic anhydride intermediate to desamido insulin and covalent dimer. Pharm Res 12:1077-1084.
26. Strickley RG, Anderson BD. 1996. Solid-state stability of human insulin. I. Mechanism and the effect of water on the kinetics of degradation in lyophiles from pH 2-5 solutions. Pharm Res 13:1142-1153.
27. Strickley RG, Anderson BD. 1997. Solid-state stability of human insulin. II. Effect of water on reactive intermediate partitioning in lyophiles from pH 2-5 solutions - stabilization against covalent dimer formation. J Pharm Sci 86:645-653.
28. Smyth DG, Nagamatsu A, Fruton JS. 1960. Reactions of N-ethylmaleimide. J Am Chem Soc 82:4600-4604.
29. Smyth DG, Tuppy H. 1968. Acylation reactions with cyclic imides. Biochim Biophys Acta 168:173-180.
30. Brange J, Havelund S, Hougaard P. 1992. Chemical stability of insulin. 2. Formation of higher molecular weight transformation products during storage of pharmaceutical preparations. Pharm Res 9:727-734.
31. Helbig H-J. 1976. Insulindimere Aus Der B-Komponente Von Insulinpraparationen Dissertation. Rheinisch-Westfalischen Technischen Hochschule, Aachen.
32. Zale SE, Klibanov AM. 1986. Why does ribonuclease irreversibly inactivate at high temperatures? Biochemistry 25:5432-5444.
33. Hageman MJ, Bauer JM, Possert PL, Darrington RT. 1992. Preformulation studies oriented toward sustained delivery of recombinant somatotropins. J Agric Food Chem 40:348-355.
34. Nguyen TH, Ward C. 1993. Stability characterization and formulation development of alteplase, a recombinant tissue plasminogen activator. In: Wang YJ, Pearlman R, editors. Stability and Characterization of Protein and Peptide Drugs, New York: Plenum Press. p 91-134.
35. Eckhardt BM, Oeswein JQ, Bewley TA. 1991. Effect of freezing on aggregation of human growth hormone. Pharm Res 8:1360-1364.
36. Fisher GH, Payan IL, Chou SJ, Man EH, Cerwinski S, Martin T, Emory C, Frey WH. 1992. Racemized D-aspartate in Alzheimer neurofibrillary tangles. Brain Res Bull 28:127-131.
37. Orpiszewski J, Schormann N, Kluve-Beckerman B, Liepnikes JJ, Benson MD. 2000. Protein aging hypothesis of Alzheimer's disease. FASEB J 14:1255-1263.
38. Shimizu T, Matsuoka Y, Shirasawa T. 2005. Biological significance of isoaspartate and its repair system. Biol Pharm Bull 28:1590-1596.
39. 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.
40. Nilsson MR, Driscoll M, Raleigh DP. 2002. Low levels of asparagine deamidation can have a dramatic effect on aggregation of amyloidogenic peptides: implications for the study of amyloid formation. Protein Sci 11:342-349.
41. Caughy B, Lansbury JPT. 2003. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Ann Rev Neurosci 26:267-298.
42. Sandmeier E, Hunziker P, Kunz B, Sack R, Christen P. 1999. Spontaneous deamidation and isomerization of Asn108 in prion peptide 106-126 and in full-length prion protein. Biochem Biophys Res Commun 261:578-583.
43. Scherzinger E, Sittler A, Schweiger K, Heiser V, Lurz R, Hasenbank R, Bates GP, Lehrach H, Wanker EE. 1999. Self-assembly of polyglutamine-containing huntington fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc Nat Acad Sci USA 96:4604-1609.
44. Jornvall H. 1974. Blocked α-amino groups in peptides due to diketopiperazine formation. FEBS Lett 38:329-333.
45. Lura R, Schirch V. 1988. Role of peptide conformation in the rate and mechanism of deamidation of asparaginyl residues. Biochem 27:7671-7677.
46. Pollina E. 1996. Design and synthesis of RGD mimetics as potent inhibitors of platelet aggregation. J Undergrad Sci 3:119-126.
47. Oliyai C, Borchardt RT. 1993. Chemical pathways of peptide degradation. IV. Pathways, kinetics, and mechanism of degradation of an aspartyl residue in a model hexapeptide. Pharm Res 10:95-102.
48. Morgan ME, Liu K, Anderson BD. 1998. Microscale titrimetric and spectrophotometric methods for determination of ionization constants and partition coefficients of new drug candidates. J Pharm Sci.
49. Brennan TV, Clarke S. 1995. Deamidation and isoasparate formation in model synthetic peptides: the effects of sequence and solution environment. In: Aswad DS, editor. Deamidate and Iso-Aspartate Formation in Peptides and Proteins. Ann Arbor, MI: CRC Press. p 65-90.
50. Song Y, Schowen RL, Borchardt RT, Topp EM. 2001. Effect of 'pH' on the rate of asparagine deamidation in polymeric formulations: 'pH'-rate profile. J Pharm Sci 90:141-156.
51. Capasso S, Balboni G, Cerbo Di P. 2000. Effect of lysine residues on the deamidation reaction of asparagine side chains. Biopolymers 53:213-219.
52. Tyler-Cross R, Schirch V. 1991. Effects of amino acid sequence, buffers, and ionic strength on the rate and mechanism of deamidation of asparagine residues in small peptides. J Biol Chem 266:22549-22556.
53. Johnson BA, Freitag NE, Aswad DW. 1985. Protein carboxyl methyltransferase selectivly modifies an atypical form of calmodulin. J Biol Chem 260:10913-10916.
54. Capasso S, Kirby AJ, Salvadori S, Sica F, Zagari A. 1995. Kinetics and mechanism of the reversible isomerization of aspartic acid residues in tetrapeptides. J Chem Soc Perkin Trans 2:437-442.
55. Almarsson O, Kaufman MJ, Strong JD, Wu Y, Mayr SM, Petrich MA, Williams JM. 1998. Meropenem exists in equilibrium with a carbon dioxide adduct in bicarbonate solution. J Pharm Sci 87:663-666.
56. Archer RA, Kitchell BS. 1966. Chemistry of cephalosporin antibiotics. VI. Carbamate formation in aqueous bicarbonate solutions of 7-ACA. J Org Chem 31:3409-3411.
57. Christensen F, Koefoed HCS, Petersen AC, Rasmussen K. 1978. Equilibrium constants in the ammonium carbonate-carbaminate system. The acid dissociation constant of carbamic acid. Acta Chem Scand A32:15-17.
58. Wen N, Brooker MH. 1995. Ammonium carbonate, ammonium bicarbonate, and ammonium carbamate equilibria: a Raman study. J Phys Chem 99:359-368.
59. 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.
60. Liotta LJ, Gibbs RA, Taylor SD, Benkovic PA, Benkovic SJ. 1995. Antibody-catalyzed rearrangement of a peptide bond: mechanistic and kinetic investigations. J Am Chem Soc 117:4729-4741.
61. Konuklar FA, Aviyente V, Sen TZ, Bahar I. 2001. Modeling the deamidation of asparagine residues via succinimide intermediates. J Mol Model 7:147-160.
62. Konuklar FA, Aviyente V, Lopez MFR. 2002. Theoretical study on the alkaline and neutral hydrolysis of succinimide derivatives in deamidation reactions. J Phys Chem A 106:11205-11214.
63. Xie M, Velde DV, Morton M, Borchardt RT, Schowen RL. 1996. pH-induced change in the rate-determining step for the hydrolysis of the Asp/Asn-derived cyclic-imide intermediate in protein degradation. J Am Chem Soc 118:8955-8956.
64. Blodgett JK, Loudon GM, Collins KD. 1985. Specific cleavage of peptides containing an aspartic acid (b-hydroxamic acid) residue. J Am Chem Soc 107:4305-4313.
65. De Boni S, Oberthur C, Hamburger M, Scriba GKE. 2004. Analysis of aspartyl peptide degradation products by high-performance liquid chromatography and high-performance liquid chromatography-mass spectrometry. J Chromatogr A 1022:95-102.
66. Schon I, Kisfaludy L. 1979. Formation of aminosuccinyl peptides during acidolytic deprotection followed by their transformation to piperazine-2,5-dione derivatives in neutral media. Int J Peptide Protein Res 14:485-495.
67. Smith GG, Baum R. 1987. First-order rate constants for the racemization of each component in a mixture of isomeric dipeptides and their diketopiperazines. J Org Chem 52:2248-2255.