Why do solution additives suppress the heat-induced inactivation of proteins? inhibition of chemical modifications

Biotechnology Progress

Volumn 27, Issue 3, 2011, Pages 855-862

  Tomita, Shunsuke ^a   Shiraki, Kentaro ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

elimination; Deamidation; Lysozyme; Protein inactivation; RNase A

Indexed keywords

AMINO ACID DERIVATIVES; BOVINE PANCREATIC RIBONUCLEASE; CHAOTROPES; CHEMICAL MODIFICATION OF PROTEINS; DEAMIDATION; EXPERIMENTAL EVIDENCE; HEN EGG WHITE LYSOZYME; LYSOZYME; MOLECULAR MECHANISM; POLYAMINES; RNASE A; SOLUTION ADDITIVES; THERMOINACTIVATION;

AMINO ACIDS; CHEMICAL MODIFICATION; ENZYMES;

PROTEINS;

HEN EGG LYSOZYME; LYSOZYME; PANCREATIC RIBONUCLEASE; PRESERVATIVE;

ANIMAL; ARTICLE; CATTLE; CHEMISTRY; DRUG EFFECT; HEAT; PROTEIN DENATURATION;

ANIMALS; CATTLE; HOT TEMPERATURE; MURAMIDASE; PRESERVATIVES, PHARMACEUTICAL; PROTEIN DENATURATION; RIBONUCLEASE, PANCREATIC;

BOVINAE;

EID: 79958272015     PISSN: 87567938     EISSN: 15206033     Source Type: Journal    
DOI: 10.1002/btpr.597     Document Type: Article

References (58)

1. Hamada H, Arakawa T, Shiraki K. Effect of additives on protein aggregation. Curr Pharm Biotechnol. 2009; 10: 400-407.
2. von Hippel PH, Wong KY. On the conformational stability of globular proteins. The effects of various electrolytes and nonelectrolytes on the thermal ribonuclease transition. J Biol Chem. 1965; 240: 3909-3923.
3. Arakawa T, Timasheff SN. The stabilization of proteins by osmolytes. Biophys J. 1985; 47: 411-414.
4. Kaushik JK, Bhat R. Why is trehalose an exceptional protein stabilizer? An analysis of the thermal stability of proteins in the presence of the compatible osmolyte trehalose. J Biol Chem. 2003; 278: 26458-26465.
5. De Bernardez Clark E. Refolding of recombinant proteins. Curr Opin Biotechnol. 1998; 9: 157-163.
6. De Bernardez Clark E, Schwarz E, Rudolph R. Inhibition of aggregation side reactions during in vitro protein folding. Methods Enzymol. 1999; 309: 217-236.
7. Tsumoto K, Umetsu M, Kumagai I, Ejima D, Philo JS, Arakawa T. Role of arginine in protein refolding, solubilization, and purification. Biotechnol Prog. 2004; 20: 1301-1308.
8. Hirano A, Hamada H, Okubo T, Noguchi T, Higashibata H, Shiraki K. Correlation between thermal aggregation and stability of lysozyme with salts described by molar surface tension increment: an exceptional propensity of ammonium salts as aggregation suppressor. Protein J. 2007; 26: 423-433.
9. Shiraki K, Kudou M, Fujiwara S, Imanaka T, Takagi M. Biophysical effect of amino acids on the prevention of protein aggregation. J Biochem. 2002; 132: 591-595.
10. Shiraki K, Kudou M, Nishikori S, Kitagawa H, Imanaka T, Takagi M. Arginine ethylester prevents thermal inactivation and aggregation of lysozyme. Eur J Biochem. 2004; 271: 3242-3247.
11. Shiraki K, Kudou M, Sakamoto R, Yanagihara I, Takagi M. Amino acid esters prevent thermal inactivation and aggregation of lysozyme. Biotechnol Prog. 2005; 21: 640-643.
12. Matsuoka T, Tomita S, Hamada H, Shiraki K. Amidated amino acids are prominent additives for preventing heat-induced aggregation of lysozyme. J Biosci Bioeng. 2007; 103: 440-443.
13. Kudou M, Shiraki K, Fujiwara S, Imanaka T, Takagi M. Prevention of thermal inactivation and aggregation of lysozyme by polyamines. Eur J Biochem. 2003; 270: 4547-4554.
14. Okanojo M, Shiraki K, Kudou M, Nishikori S, Takagi M. Diamines prevent thermal aggregation and inactivation of lysozyme. J Biosci Bioeng. 2005; 100: 556-561.
15. Hirano A, Hamada H, Shiraki K. trans-Cyclohexanediamines prevent thermal inactivation of protein: role of hydrophobic and electrostatic interactions. Protein J. 2008; 27: 253-257.
16. Ganguli S, Yoshimoto K, Tomita S, Sakuma H, Matsuoka T, Shiraki K, Nagasaki Y. Regulation of lysozyme activity based on thermotolerant protein/smart polymer complex formation. J Am Chem Soc. 2009; 131: 6549-6553.
17. Hamada H, Takahashi R, Noguchi T, Shiraki K. Differences in the effects of solution additives on heat- and refolding-induced aggregation. Biotechnol Prog. 2008; 24: 436-443.
18. Matsuoka T, Hamada H, Matsumoto K, Shiraki K. Indispensable structure of solution additives to prevent inactivation of lysozyme for heating and refolding. Biotechnol Prog. 2009; 25: 1515-1524.
19. Daniel RM, Dines M, Petach HH. The denaturation and degradation of stable enzymes at high temperatures. Biochem J. 1996; 317: 1-11.
20. Volkin DB, Mach H, Middaugh CR. Degradative covalent reactions important to protein stability. Mol Biotechnol. 1997; 8: 105-122.
21. Manning MC, Chou DK, Murphy BM, Payne RW, Katayama DS. Stability of protein pharmaceuticals: an update. Pharm Res. 2010; 27: 544-575.
22. Ahern TJ, Klibanov AM. The mechanisms of irreversible enzyme inactivation at 100°C. Science. 1985; 228: 1280-1284.
23. Zale SE, Klibanov AM. Why does ribonuclease irreversibly inactivate at high temperatures? Biochemistry. 1986; 25: 5432-5444.
24. Ahern TJ, Klibanov AM. Analysis of processes causing thermal inactivation of enzymes. Methods Biochem Anal. 1988; 33: 91-127.
25. Gekko K, Timasheff SN. Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures. Biochemistry. 1981; 20: 4667-4676.
26. Kun E, Kearney EB. Ammonia. Methods Enzyme Anal. 1974; 4: 1802-1806.
27. Florence TM. Degradation of protein disulphide bonds in dilute alkali. Biochem J. 1980; 189: 507-520.
28. Volkin DB, Klibanov AM. Thermal destruction processes in proteins involving cystine residues. J Biol Chem. 1987; 262: 2945-2950.
29. Arakawa T, Tsumoto K. The effects of arginine on refolding of aggregated proteins: not facilitate refolding, but suppress aggregation. Biochem Biophys Res Commun. 2003; 304: 148-152.
30. Tomizawa H, Yamada H, Tanigawa K, Imoto T. Effects of additives on irreversible inactivation of lysozyme at neutral pH and 100°C. J Biochem. 1995; 117: 369-373.
31. Tyler-Cross R, Schirch V. 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. 1991; 266: 22549-22556.
32. Robinson NE. Protein deamidation. Proc Natl Acad Sci USA. 2002; 99: 5283-5288.
33. Zheng JY, Janis LJ. Influence of pH, buffer species, and storage temperature on physicochemical stability of a humanized monoclonal antibody LA298. Int J Pharm. 2006; 308: 46-51.
34. Zhang Z, Pan H, Chen X. Mass spectrometry for structural characterization of therapeutic antibodies. Mass Spectrom Rev. 2009; 28: 147-176.
35. Geiger T, Clarke S. Deamidation, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation. J Biol Chem. 1987; 262: 785-794.
36. Raines RT. Ribonuclease A. Chem Rev. 1998; 98: 1045-1066.
37. Blake CCF, Johnson LN, Mair GA, North ACT, Phillips DC, Sarma VR. Crystallographic studies of the activity of hen egg-white lysozyme. Proc R Soc Lond B. 1967; 167: 378-388.
38. Clarke S. Propensity for spontaneous succinimide formation from aspartyl and asparaginyl residues in cellular proteins. Int J Pept Protein Res. 1987; 30: 808-821.
39. Kosky AA, Razzaq UO, Treuheit MJ, Brems DN. The effects of alpha-helix on the stability of Asn residues: deamidation rates in peptides of varying helicity. Protein Sci. 1999; 8: 2519-2523.
40. Xie M, Shahrokh Z, Kadkhodayan M, Henzel WJ, Powell MF, Borchardt RT, Schowen RL. Asparagine deamidation in recombinant human lymphotoxin: hindrance by three-dimensional structures. J Pharm Sci. 2003; 92: 869-880.
41. Kossiakoff AA. Tertiary structure is a principal determinant to protein deamidation. Science. 1988; 240: 191-194.
42. Chelius D, Rehder DS, Bondarenko PV. Identification and characterization of deamidation sites in the conserved regions of human immunoglobulin gamma antibodies. Anal Chem. 2005; 77: 6004-6011.
43. DeLuna A, Quezada H, Gomez-Puyou A, Gonzalez A. Asparaginyl deamidation in two glutamate dehydrogenase isoenzymes from Saccharomyces cerevisiae. Biochem Biophys Res Commun. 2005; 328: 1083-1090.
44. Stratton LP, Kelly RM, Rowe J, Shively JE, Smith DD, Carpenter JF, Manning MC. Controlling deamidation rates in a model peptide: effects of temperature, peptide concentration, and additives. J Pharm Sci. 2001; 90: 2141-2148.
45. Ueda T, Nagata M, Imoto T. Aggregation and chemical reaction in hen lysozyme caused by heating at pH 6 are depressed by osmolytes, sucrose and trehalose. J Biochem. 2001; 130: 491-496.
46. Miroliaei M, Nemat-Gorgani M. Sugars protect native and apo yeast alcohol dehydrogenase against irreversible thermoinactivation. Enzyme Microb Tech. 2001; 29: 554-559.
47. Wu SL, Leung D, Tretyakov L, Hu J, Guzzetta A, Wang YJ. The formation and mechanism of multimerization in a freeze-dried peptide. Int J Pharm. 2000; 200: 1-16.
48. Kim JS, Kim HJ. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometric observation of a peptide triplet induced by thermal cleavage of cystine. Rapid Commun Mass Spectrom. 2001; 15: 2296-2300.
49. Galande AK, Trent JO, Spatola AF. Understanding base-assisted desulfurization using a variety of disulfide-bridged peptides. Biopolymers. 2003; 71: 534-551.
50. Nakanishi T, Sato T, Sakoda S, Yoshioka M, Shimizu A. Modification of cysteine residue in transthyretin and a synthetic peptide: analyses by electrospray ionization mass spectrometry. Biochim Biophys Acta. 2004; 1698: 45-53.
51. Wang Z, Rejtar T, Zhou ZS, Karger BL. Desulfurization of cysteine-containing peptides resulting from sample preparation for protein characterization by mass spectrometry. Rapid Commun Mass Spectrom. 2010; 24: 267-275.
52. Kaneko R, Kitabatake N. Heat-induced formation of intermolecular disulfide linkages between thaumatin molecules that do not contain cysteine residues. J Agric Food Chem. 1999; 47: 4950-4955.
53. Cohen SL, Price C, Vlasak J. β-Elimination and peptide bond hydrolysis: two distinct mechanisms of human IgG1 hinge fragmentation upon storage. J Am Chem Soc. 2007; 129: 6976-6977.
54. Gaza-Bulseco G, Liu H. Fragmentation of a recombinant monoclonal antibody at various pH. Pharm Res. 2008; 25: 1881-1890.
55. Harris RJ, Shire SJS, Winter C. Commercial manufacturing scale formulation and analytical characterization of therapeutic recombinant antibodies. Drug Dev Res. 2004; 61: 137-154.
56. Liu H, Gaza-Bulseco G, Faldu D, Chumsae C, Sun J. Heterogeneity of monoclonal antibodies. J Pharm Sci. 2008; 97: 2426-2447.
57. Krokhin OV, Antonovici M, Ens W, Wilkins JA, Standing KG. Deamidation of -Asn-Gly- sequences during sample preparation for proteomics: consequences for MALDI and HPLC-MALDI analysis. Anal Chem. 2006; 78: 6645-6650.
58. Gaza-Bulseco G, Li B, Bulseco A, Liu H. Method to differentiate Asn deamidation that occurred prior to and during sample preparation of a monoclonal antibody. Anal Chem. 2008; 80: 9491-9498.