Mechanism for benzyl alcohol-induced aggregation of recombinant human interleukin-1 receptor antagonist in aqueous solution

Journal of Pharmaceutical Sciences

Volumn 93, Issue 12, 2004, Pages 3076-3089

  Zhang, Ye ^a   Roy, Shouvik ^a   Jones, Latoya S ^a   Krishnan, Sampathkumar ^a,b   Kerwin, Bruce A ^b   Chang, Byeong S ^b,d   Manning, Mark C ^a   Randolph, Theodore W ^c   Carpenter, John F ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b AMGEN INC   (United States)

^c UCB 450   (United States)

^d Integrity Biosolution   (United States)

Author keywords

Benzyl alcohol; Protein aggregation; Sucrose

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; BENZYL ALCOHOL; GUANIDINE; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; SUCROSE; UREA;

AQUEOUS SOLUTION; ARTICLE; DIFFERENTIAL SCANNING CALORIMETRY; DRUG STRUCTURE; ENERGY; FLUORESCENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROPHOBICITY; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; TEMPERATURE DEPENDENCE;

EID: 10644283956     PISSN: 00223549     EISSN: None     Source Type: Journal    
DOI: 10.1002/jps.20219     Document Type: Article

References (46)

1. Akers MJ. 1984. Considerations in selecting antimicrobial agents for parenteral product development. Pharm Technol 8:36-46.
2. Jorgensen JT, Mortenseri HB, Jorgensen JO. 1991. Patient acceptance of Nordiject: A new drug delivery system for growth hormone. DICP: Ann Pharmacother 25:585-588.
3. Belgaumi AF, Patrick CC, Deitcher SR. 1999. Stability and sterility of a recombinant Factor VIII concentrate prepared for continuous infusion administration. Am J Hematol 62:13-18.
4. Batorova A, Martinowitz U. 2002. Continuous infusion of coagulation factors. Haemophilia 8:170-177.
5. Tan EL, Shah HS, Leister KJ, Kozick LM, Pasciak P, Vanderlaan RK, Yu CD, Patel B. 1993. Transforming growth factor-alpha (TGF-alpha) in a semisolid dosage form: Preservative and vehicle selection. Pharm Res 10:1238-1242.
6. Maa YF, Hsu CC. 1996. Aggregation of recombinant human growth hormone induced by phenolic compounds. Int J Pharm Sci 140:155-168.
7. Fransson J, Hallen D, Florin-Robertsson E. 1997. Solvent effects on the solubility and physical stability of human insulin-like growth factor I. Pharm Res 14:606-612.
8. Lam XM, Patapoff TW, Nguyen TH. 1997. The effect of benzyl alcohol on recombinant human interferon-γ. Pharm Res 14:725-729.
9. Remmele RL Jr, Nightlinger NS, Srinivasan S, Gombotz WR. 1998. Interleukin-1 receptor (IL-IR) liquid formulation development using differential scanning calorimentry. Pharm Res 15:200-208.
10. Rodrigues-Silva R, Antunes GFC, Velarde DT, Santoro MM. 1999. Thermal stability studies of hyperimmune horse antivenoms. Toxicon 37:33-45.
11. Gupta S, Kaisheva E. 2003. Development of a multidose formulation for a humanized monoclonal antibody using experimental design techniques. AAPS PharmSci 5:E8.
12. Moore WV, Leppert P. 1980. Role of aggregated human growth hormone (Hgh) in development of antibodies to Hgh. J Clin Endocrin Metab 51:691-697.
13. Ratner RE, Phillips TM, Steiner M. 1990. Persistent cutaneous insulin allergy resulting from high-molecular weight insulin aggregates. Diabetes 39:728-733.
14. Thornton CA, Ballow M. 1993. Safety of intravenous immunoglobulin. Arch Neurol 50:135-136.
15. Narhi LO, Philo JS, Sun B, Chang BS, Arakawa T. 1999. Reversibility of heat-induced denaturation of the recombinant human megakaryocyte growth and development factor. Pharm Res 16:799-807.
16. Chi EY, Krishnan S, Randolph TW, Carpenter JF. 2003. Physical stability of proteins in aqueous solution: Mechanism and driving forces in nonnative protein aggregation. Pharm Res 20:1325-1336.
17. Krishnan S, Chi EY, Webb JN, Chang BS, Shan D, Goldenberg M, Manning MC, Randolph TW, Carpenter JF. 2002. Aggregation of granulocyte colony stimulating factor under physiological conditions: Characterization and thermodynamic inhibition. Biochemistry 41:6422-6431.
18. Wetzel R. 1996. For protein misassembly, it's the "I" decade. Cell 86:699-702.
19. Fink AL. 1998. Protein aggregation: Folding aggregates, inclusion bodies and amyloid. Fold Des 3: R9-R23.
20. Kendrick BS, Chang BS, Arakawa T, Peterson B, Randolph TW, Manning MC, Carpenter JF. 1997. Preferential exclusion of sucrose from recombinant interleukin-1 receptor antagonist: role in restricted conformational mobility and compaction of native state. Proc Natl Acad Sci USA 94:11917-11922.
21. Kim YS, Randolph TW, Manning MC, Stevens FJ, Carpenter JF. 2003. Congo red populates partially unfolded states of an amyloidogenic protein to enhance aggregation and amyloid fibril formation. J Biol Chem 278:10842-10850.
22. Kendrick BS, Carpenter JF, Cleland JL, Randolph TW. 1998. A transient expansion of the native state precedes aggregation of recombinant human interferon-gamma. Proc Natl Acad Sci USA 95:14142-14146.
23. Kendrick BS, Randolph TW, Cleland J, Lam X, Nguyen T, Manning MC, Carpenter JF. 1998. Aggregation of recombinant human interferon-gamma: Kinetics and structural transitions. J Pharm Sci 87:1069-1080.
24. Kim YS, Wall JS, Meyer J, Murphy C, Randolph TW, Manning MC, Solomon A, Carpenter JF. 2000. Thermodynamic modulation of light chain amyloid fibril formation. J Biol Chem 275:1570-1574.
25. Kim YS, Randolph TW, Stevens FJ, Carpenter JF. 2002. Kinetics and energetics of assembly, nucleation, and growth of aggregates and fibrils for an amyloidogenic protein: Insights into transition states from pressure, temperature and co-solute studies. J Biol Chem 277:27240-27246.
26. Tobler SA, Holmes BW, Cromwell MEM, Fernandez EJ. 2004. Benzyl alcohol-induced destabilization of interferon-γ: A study by hydrogendeuterium isotope exchange. J Pharm Sci 93:1605-1617.
27. Chang BS, Beauvais RM, Arakawa T, Narhi LO, Dong A, Aparisio DI, Carpenter JF. 1996. Formation of an active dimer during storage of interleukin-1 receptor antagonist in aqueous solution. Biophys J 71:3399-3406.
28. Webb JN, Webb SD, Cleland JL, Carpenter JF, Randolph TW. 2001. Partial molar volume, surface area, and hydration changes for equilibrium unfolding and formation of aggregation transition state: High-pressure and cosolute studies on recombinant human IFN-γ. Proc Natl Acad Sci USA 98:7259-7264.
29. Lee JC, Timasheff SN. 1981. The stabilization of proteins by sucrose. J Biol Chem 256:7193-7201.
30. Timasheff SN. 1993. The control of protein stability and association by weak interactions with water: How do solvents affect these processes? Annu Rev Biophys Biomol Struct 22:67-97.
31. Kim YS, Cape SP, Chi E, Raffen R, Wilkins-Stevens P, Stevens FJ, Manning MC, Randolph TW, Solomon A, Carpenter JF. 2001. Counteracting effects of renal solutes on amyloid fibril formation by immunoglobulin light chains. J Biol Chem 276:1626-1633.
32. Dong A, Huang P, Caughey WS. 1990. Protein secondary structures in water from second-derivative amide I infrared spectra. Biochemistry 29:3303-3308.
33. Ragone R, Colonna G, Balestrieri C, Servillo L, Irace G. 1984. Determination of tyrosine exposure in proteins by second-derivative spectroscopy. Biochemistry 23:1871-1875.
34. Huyghues-Despointes BMP, Scholtz JM, Pace CN. 1999. Protein conformational stabilities can be determined from hydrogen exchange rates. Nat Struct Biol 6:910-912.
35. Kim YS, Jones LS, Dong A, Kendrick BS, Chang BS, Manning MC, Randolph TW, Carpenter JF. 2003. Effects of sucrose on conformational equilibria and fluctuations within the native-state ensemble of proteins. Protein Sci 12:1252-1261.
36. Strickland EH. 1974. Aromatic contributions to circular dichroism spectra of proteins. CRC Crit Rev Biochem 2:113-175.
37. Pace CN, Shirley BA, Thomson JA. 1989. Measuring the conformational stability of a protein. In: Creighton TE, editor. Protein structure: A practical approach. New York: IRL Press at Oxford University Press, pp 311-330.
38. Stockman BJ, Scahill TA, Roy M, Ulrich EL, Strakalaitis NA, Brunner DP, Yem AW, Deibel MR Jr. 1992. Secondary structure and topology of interleukin-1 receptor antagonist protein determined by heteronuclear three-dimensional NMR spectroscopy. Biochemistry 31:5237-5245.
39. Vigers GP, Gaffes P, Evans RJ, Thompson RC, Eisenberg SP, Brandhuber BJ. 1994. X-ray structure of interleukin-1 receptor antagonist at 2.0-A resolution. J Biol Chem 269:12874-12879.
40. Schreuder HA, Rondeau JM, Tardif C, Soffientini A, Sarubbi E, Akeson A, Bowlin TL, Yanofsky S, Barrett RW. 1995. Refined crystal structure of the interleukin-1 receptor antagonist. Presence of a disulfide link and a cis-proline. Eur J Biochem 227:838-847.
41. Mach H, Middaugh CR. 1994. Simultaneous monitoring of the environment of tryptophan, tyrosine, and phenylalanine residues in proteins by nearultraviolet second-derivative spectroscopy. Anal Biochem 222:323-331.
42. Uversky VN, Winter S, Lober G. 1996. Use of fluorescence decay times of 8-ANS-protein complexes to study the conformational transitions in proteins which unfold through the molten globule state. Biophys Chem 60:79-88.
43. Wiseman T, Williston S, Brandts JF, Lin LN. 1989. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179:131-137.
44. Bijma K, Rank E, Engberts JBFN. 1998. Effect of counterion structure on micellar growth of alkylpyridinium surfactants in aqueous solution. J Colloid Interface Sci 205:245-256.
45. Timasheff SN. 1998. Control of protein stability and reactions by weakly interacting cosolvents: The simplicity of the complicated. Adv Protein Chem 51:355-432.
46. Arakawa T, Carpenter JF, Kita YA, Crowe JH. 1990. The basis for toxicity of certain cryoprotectants: A hypothesis. Cryobiology 27:401-415.