Irreversible aggregation of recombinant bovine granulocyte-colony stimulating factor (bG-CSF) and implications for predicting protein shelf life

Journal of Pharmaceutical Sciences

Volumn 92, Issue 5, 2003, Pages 1095-1111

  Roberts, Christopher J ^b   Darrington, Richard T ^a   Whitley, Maureen B ^a  

^a PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United States)

^b University of Delaware   (United States)

Author keywords

bG CSF; Bovine granulocyte colony stimulating factor; Protein aggregation; Protein stability; Shelf life prediction

Indexed keywords

RECOMBINANT GRANULOCYTE COLONY STIMULATING FACTOR;

ARTICLE; CIRCULAR DICHROISM; CONCENTRATION RESPONSE; EQUILIBRIUM CONSTANT; GEL PERMEATION CHROMATOGRAPHY; MOLECULAR MODEL; PH; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SHELF LIFE; TEMPERATURE DEPENDENCE; THERMODYNAMICS;

EID: 0242684664     PISSN: 00223549     EISSN: None     Source Type: Journal    
DOI: 10.1002/jps.10377     Document Type: Article

References (47)

1. Bummer PM, Koppenol S. 2000. Chemical and physical considerations in protein and peptide stability. Drugs Pharm Sci 99:5-69.
2. Cleland JL, Powell MF, Shire SJ. 1993. The development of stable protein formulations: A close look at protein aggregation, deamidation, and oxidation. Crit Rev Ther Drug Carr Sys 10:307-377.
3. Pikal MJ. 1999. Mechanisms of protein stabilization during freeze-drying and storage: The relative importance of thermodynamic stabilization and glassy state relaxation dynamics. In: Rey L, May JC, editors. Freeze-drying/lyophilization of pharmaceutical and biological products. New York: Marcel Dekker, Inc., pp 161-198.
4. Remmele RL, Bhat SD, Phan DH, Gombotz WR. 1999. Minimization of recombinant human Flt3 ligand aggregation at the Tm plateau: A matter of thermal reversibility. Biochemistry 38:5241-5247.
5. Grillo AO, Edwards K-LT, Kashi RS, Shipley KM. Hu L, Besman MJ, Middaugh CR. 2001. Conformational origin of aggregation of recombinant human growth factor VIII. Biochemistry 40:586-595.
6. Kendrick BS, Carpenter JF, Cleland JL, Randolph TW. 1998. A transient expansion of the native state precedes aggregation of recombinant human interferon-γ. Proc Natl Acad Sci USA 95:14142-14146.
7. Middaugh CR, Edwards K-LT. 1998. Recent advances in our understanding of protein conformational stability from a pharmaceutical perspective. Exp Opin Invest Drugs 7:1493-1500.
8. Bartkowski RE, Kitchel R, Peckham NR, Margulis L. 2002. Aggregation of recombinant bovine granulocyte colony stimulating factor in solution. J Protein Chem 21:137-143.
9. Roberts CJ. 2003. Kinetics of irreversible protein aggregation: Analysis of extended Lumry-Eyring models and implications for predicting protein shelf life. J Phys Chem B 107:1194-1207.
10. Abkevich VI, Gutin AM, Shakhnovich EI. 1994. Free energy landscape for protein folding kinetics: Intermediates, traps, and multiple pathways in theory and lattice model simulations. J Chem Phys 101:6052-6062.
11. Lindner RA, Treweek TM, Carver JA. 2001. The molecular chaperone α-crystallin is in kinetic competition with aggregation to stabilize a monomeric molten-globule form of α-lactalbumin. Biochem J 354:79-87.
12. Kasraian K, Kuzniar A, Earley D, Kamicker B, Wilson G, Manion T, Hong J, Reiber C, Canning P. 2001. Sustained in vivo activity of recombinant bovine granulocyte colony stimulating factor (rbGCSF) using HEPES buffer. Pharm Dev Technol 6: 439-445.
13. Lovejoy B, Cascio D, Eisenberg D. 1993. Crystal structure of canine and bovine granulocyte-colony stimulating factor (G-CSF). J Mol Biol 234:640-653.
14. obs obeys the Arrhenius relation over the T range of interest.
15. Lumry R, Eyring H. 1954. Conformational changes of proteins. J Phys Chem 58:110-120.
16. Zale SE, Klibanov AM. 1983. On the role of reversible denaturation (unfolding) in the irreversible thermal inactivation of enzymes. Biotech Bioeng 25:2221-2230.
17. Sanchez-Ruiz JM. 1992. Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys J 61:921-935.
18. Tello-Solis S, Hernandez-Arana A. 1995. Effect of irreversibility on the thermodynamic characterization of the thermal denaturation of Aspergillus saitoi acid proteinase. Biochem J 31:969-974.
19. La Rosa C, Milardi D, Grasso D, Guzzi R, Sportelli L. 1995. Thermodynamics of the thermal unfolding of Azurin. J Phys Chem 99:14864-14870.
20. Kueltzo LA, Ralston J, Middaugh CR, submitted to J Pharm Sci.
21. Pace CN, Shirley BA, Thomson JA. 1990. Measuring the conformational stability of a protein. In: Creighton TE, editor. Protein structure. Oxford: Oxford University Press, pp 311-330.
22. -1 bG-CSF solutions for up to 4 h at ambient conditions immediately prior to the scan showed no detectable difference from blanks using freshly washed (acid + SDS) cuvettes. Also, thermal scans (to 75° C) with bG-CSF at each solution condition were followed immediately by a thermal scan using the same cuvette, singly rinsed and filled with the corresponding buffer alone. In no cases was the resulting signal distinguishable from the blank signal for buffer in a clean cuvette.
23. Yoshioka S, Aso Y, Izutsu K-I, Kojima S. 1994. Is stability prediction possible for protein drugs? Denaturation kinetics of β-galactosidase in solution. Pharm Res 11:1721-1725.
24. 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.
25. Kim Y-S, 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.
26. Privalov PL. 1982. Stability of proteins. Proteins which do not present a single cooperative system. Adv Protein Chem 35:1-104.
27. Privalov PL. 1979. Stability of proteins. Adv Protein Chem 33:167-241.
28. Sturtevant JM. 1987. Biochemical applications of differential scanning calorimetry. Annu Rev Phys Chem 38:463-488.
29. Laidler KJ. 1987. Chemical kinetics, 3rd ed. New York: HarperCollins Pub.
30. Collins FC, Kimball GEJ. 1949. Diffusion-controlled reaction rates. Colloid Sci 4:425-437.
31. 2/s, whereas most experimental data for diffusion of proteins of the dimensions of bG-CSF in dilute aqueous solution are an order of magnitude or more higher than this value, and so may cancel with any orientation effects.
32. Solc K, Stockmayer WH. 1973. Kinetics of diffusion controlled reaction between chemically asymmetric molecules. II. Approximate steady-state solutions. Int J Chem Kinetics 5:733-752.
33. Lide DR, ed. 1992. CRC handbook of chemistry and physics, 73rd ed. Boca Raton: CRC Press, pp 6-10.
34. Rice SA. 1985. Comprehensive chemical kinetics, v. 25: Diffusion-limited reactions. Amsterdam: Elsevier.
35. Oliveberg M. 1998. Alternative explanations for "multistate" kinetics in protein folding: Transient aggregation and changing transition-state ensembles. Ace Chem Res 31:765-772.
36. Segawa S-I, Sugihara M. 1984. Characterization of the transition state of lysozyme unfolding. I. Effect of protein-solvent interactions on the transition state. Biopolymers 23:2473-2488.
37. Oliveberg M, Tan Y-J, Fersht AR. 1995. Negative activation enthalpies in the kinetics of protein folding. Proc Natl Acad Sci USA 92:8926-8929.
38. Plaza del Pino IM, Ibarra-Molero B, Sanchez-Ruiz JM. 2000. Lower kinetic limit to protein thermal stability: A proposal regarding protein stability in vivo and its relation with misfolding diseases. Proteins Struct Funct Genet 40:58-70.
39. Karplus M. 2000. Aspects of protein reaction dynamics: Deviations from simple behavior. J Phys Chem B 104:11-27.
40. Pascher T. 2001. Temperature and driving force dependence of the folding rate of reduced horse heart cytochrome c. Biochemistry 40:5812-5820.
41. 21
42. Yoshioka S, Izutsu K, Aso Y, Takeda Y. 1991. Inactivation kinetics of enzyme pharmaceuticals in aqueous solution. Pharm Res 8:480-484.
43. Mulkerrin MG, Wetzel R. 1989. pH dependence of the reversible and irreversible thermal denaturation of γ interferons. Biochemistry 28:6556-6561.
44. Remmele RL. 2002. Arrhenius consequences of IL-1R(II) aggregation in the vicinity of the Tm. Presented at Formulation Strategies for Biopharmaceuticals. IBC USA, Miami, FL.
45. Becktel WJ, Schellman JA. 1987. Protein stability curves. Biopolymers 26:1859-1877.
46. Wood SJ, Wypych J, Steavenson S, Louis J-C, Citron M, Biere AL. 1999. α-Synuclein fibrillogenesis is nucleation-dependent. J Biol Chem 274: 19509-19512.
47. Esler WP, Stimson ER, Ghilardi JR, Vinters HV, Lee JP, Mantyh PW, Maggio JE. 1996. In vitro growth of Alzheimer's disease β-amyloid plaques displays first-order kinetics. Biochemistry 35:749-757.