Factors affecting short-term and long-term stabilities of proteins

Advanced Drug Delivery Reviews

Volumn 46, Issue 1-3, 2001, Pages 307-326

  Arakawa, Tsutomu ^a   Prestrelski, Steven J ^a   Kenney, William C ^a   Carpenter, John F ^b  

^a AMGEN INC   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Co solute induced stabilization of proteins; Cryoprotectant; Freeze induced denaturation; Lyophilization induced denaturation; Protein degradation; Protein stabilization

Indexed keywords

EXCIPIENT; PROTEIN;

CHEMISTRY; DRUG STABILITY; FREEZE DRYING; FREEZING; REVIEW;

DRUG STABILITY; EXCIPIENTS; FREEZE DRYING; FREEZING; PROTEINS;

EID: 0035287319     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-409X(00)00144-7     Document Type: Article

References (113)

1. C. Tanford, C.E. Buckley, P.K. De, E.P. Lively, Effect of ethylene glycol on the conformation of γ-globulin and β-lactoglobulin, J. Biol. Chem. 237 (1962) 1168-1171.
2. M.F. Utter, D.B. Keeth, M.C. Scrutton, A possible role of acetyl CoA in the control of gluconeogenesis, Adv. Enzyme Regul. 2 (1964) 49-68.
3. J. Neucere, A.J. St. Angelo, Physicochemical properties of peanut proteins in sucrose, Anal. Biochem. 47 (1972) 80-89.
4. R.P. Frigon, J.C. Lee, The stabilization of calf-brain microtubule protein by sucrose, Arch. Biochem. Biophys. 153 (1972) 587-589.
5. M.L. Shelanski, F. Gaskin, C.R. Canton, Microtubule assembly in the absence of added nucleotides, Proc. Natl. Acad. Sci. USA 70 (1973) 765-768.
6. G.C. Na, S.N. Timasheff, Interaction of calf-brain tubulin with glycerol, J. Mol. Biol. 151 (1981) 165-178.
7. K.C. Aune, C. Tanford, Thermodynamics of the denaturation of lysozyme by guanidine hydrochloride. II. Dependence on denaturant concentration at 25, Biochemistry 8 (1969) 4586-4590.
8. J.F. Brants, R. Lumry, The thermodynamics of protein denaturation. IV. The denaturation of ribonuclease in water and in aqueous urea and aqueous ethanol mixtures, J. Am. Chem. Soc. 91 (1969) 4256-4264.
9. P.L. Privalov, N.N. Khechinashvili, A thermodynamic approach to the problem of stabilization of globular protein structure: a calorimetric study, J. Mol. Biol. 86 (1974) 665-684.
10. N. Pace, Conformational stability of globular proteins, Trends Biochem. Sci. 15 (1970) 14-17.
11. S.Y. Gerlsma, Reversible denaturation of ribonuclease in aqueous solution as influenced by polyhydric alcohols, J. Biol. Chem. 243 (1968) 957-961.
12. S.Y. Gerlsma, The effects of polyhydric and monohydric alcohols on the heat induced reversible denaturation of chymotrypsinogen A, Eur. J. Biochem. 14 (1970) 140-153.
13. S.Y. Gerlsma, E.R. Stuur, The effect of polyhydric and monohydric alcohols on the heat-induced reversible denaturation of lysozyme and ribonuclease, Int. J. Pept. Protein Res. 4 (1972) 377-383.
14. S.Y. Gerlsma, E.R. Stuur, The effects of combining two different alcohols on the heat-induced reversible denaturation of ribonuclease, Int. J. Pept. Protein Res. 6 (1974) 65-74.
15. T. Arakawa, S.N. Timasheff, Preferential interactions of proteins with solvent components in aqueous amino acid solutions, Arch. Biochem. Biophys. 224 (1983) 169-1677.
16. T. Arakawa, S.N. Timasheff, The mechanism of actino of Na glutamate, lysine HCl, and diperazine-N,N′-bis(2-ethanesulfonic acid) in the stabilization of tubulin and microtubule formation, J. Biol. Chem. 259 (1984) 4979.
17. K. Gekko, S.N. Timasheff, Thermodynamic and kinetic examination of protein stabilization by glycerol, Biochemistry 26 (1981) 4677-4686.
18. L.C. Lee, S.N. Timasheff, The stabilization of proteins by sucrose, J. Biol. Chem. 256 (1981) 7193-7201.
19. P.S. Low, in: R. Gilles, M. Gilles-Baillien (Eds.), Transport Processes, Iono- and Osmoregulation, Spring-Verlag, Berlin, 1985, pp. 469-477.
20. N.K.D. Kalla, J.E. Kinsella, Structural stability of β-lactoglobulin in the presence of kosmotrophic salts, Int. J. Pept. Protein Res. 32 (1988) 396-405.
21. K. Gekko, Y Kuwana, T. Sasaki, S. Makino, Polyol-induced stabilization of a cold-labile protein, Agric. Biol. Chem. 55 (1991) 1663-1664.
22. J.R. Back, D. Oakenfull, M.B. Smith, Increased thermal stability of proteins in the presence of sugars and polyols, Biochemistry 18 (1979) 5191-5196.
23. T. Arakawa, S.N. Timasheff, Stabilization of protein structure by sugars, Biochemistry 21 (1982) 6536-6544.
24. T. Arakawa, S.N. Timasheff, Mechanism of protein setting in and setting out by divalent cation salts: balance between hydration and salt binding, Biochemistry 23 (1984) 5912-5923.
25. T.F. Busby, O.H. Atha, K.C. Ingham, Thermal denaturation of antithrombin. III. Stabilization by heparin and lyotrophic anions, J. Biol. Chem. 256 (1981) 12140-12147.
26. K. Gekko, Calorimetric study on thermal denaturation of lysozyme in polyol-water mixtures, J. Biochem. 91 (1982) 1197-1204.
27. K. Gekko, S. Koga, Increased thermal stability of collagen in the presence of sugars and polyols, J. Biochem. 94 (1983) 199-1204.
28. L. Wicker, J.A. Knopp, The binding of 8-anilino-1-naphthalene sulfonate (ANS) to fish myosin and the effect of salts on the thermal transitions of fish myosin-ANS complex, Arch. Biochem. Biophys. 266 (1988) 452-461.
29. T. Arakawa, The stabilization of β-lactoglobulin by glycine and NaCl, Biopolymers 28 (1989) 1397-1401.
30. J.F. Carpenter, J.H. Crowe, The mechanism of cryoprotection of proteins by solutes, Cryobiology 25 (1988) 244-255.
31. J.F. Carpenter, S.C. Hand, L.M. Crowe, J.H. Crowe, Cryoprotection of phosphofructokinase with organic solutes: characterization of enhanced protection in the presence of divalent cations, Arch. Biochem. Biophys. 250 (1986) 505-512.
32. J.F. Carpenter, L.M. Crowe, J.H. Crowe, Stabilization of phosphofructokinase with sugars during freeze-drying: characterization of enhanced protection in the presence of divalent cations, Biochim. Biophys. Acta 923 (1987) 109-115.
33. J.F. Carpenter, B. Martin, L.M. Crowe, J.H. Crowe, Stabilization of phosphofructokinase during air-drying with sugars and sugars/transition metal mixtures, Cryobiology 24 (1987) 455-464.
34. G.A. MacDonal, T. Lanier, Carbohydrates as cryoprotectants for meats and surimi, J. Food Technol. 45 (1991) 150-159.
35. J.F. Carpenter, J.H. Crowe, Modes of stabilization of a protein by organic solutes during desiccation, Cryobiology 25 (1988) 459-470.
36. J.F. Carpenter, J.H. Crowe, An infrared spectroscopic study of the interactions of carbohydrates with dried protein, Biochemistry 28 (1989) 3916-3922.
37. J.H. Crowe, J.F. Carpenter, L.M. Crowe, T.J. Anchordoguy, Are freezing and dehydration similar stress vectors? A comparison of modes of interaction of stabilizing solutes with biomolecules, Cryobiology 27 (1990) 219-231.
38. M.M. Santoro, Y. Liu, S.M.A. Khan, L.-X. Hou, D.W. Bolen, Increased thermal stability of proteins in the presence of natural occurring osmolytes, Biochemistry 31 (1992) 5278-5283.
39. S.V. Ambudkar, P.C. Maloney, Bacterial anion exchange: use of osmolytes during solubilization and reconstitution of phosphate-linked antiport from Streptococcus lactis, J. Biol. Chem. 261 (1986) 10079-10086.
40. S.V. Ambudkar, A.R. Lynn, P.C. Maloney, B.P. Rosen, Reconstitution of ATP dependent calcium transport from streptococci, J. Biol. Chem. 261 (1986) 15596-15600.
41. M.P. D'Souza, S.V. Ambudkar, J.T. August, P.C. Maloney, Reconstitution of lysosomal proton pump, Proc. Natl. Acad. Sci. USA 84 (1987) 6980-6984.
42. P.C. Maloney, S.V. Ambudkar, Functional reconstitution of prokaryote and eukaryote membrane proteins, Arch. Biochem. Biophys. 269 (1989) 1-10.
43. M.K. Nishiguchi, G.N. Somero, Temperature- and concentration-dependence of compatibility of the organic osmolyte β-dimethylsulfoniopropionate, Cryobiology 29 (1992) 118-124.
44. J.H. Crowe, J.S. Clegg, Dry Biological Systems, Academic Press, New York, 1978.
45. J.H. Crowe, L.M. Crowe, D. Chapman, Preservation of membranes in anhydrobiotic organisms - the role of trehalose, Science 223 (1984) 701-703.
46. C. Womersley, Biochemical and physiological aspects of anhydrobiosis, Comp. Biochem. Physiol. B70 (1981) 669-678.
47. K.A.C. Madin, J.H. Crowe, Anhydrobiosis in nematodes carbohydrate and lipid metabolism during dehydration, J. Exp. Zool. 193 (1985) 335-342.
48. L.M. Crowe, J.H. Crowe, A. Rudolph, C. Womersley, L. Appel, Preservation of freeze-dried liposomes by trehalose, Arch. Biochem. Biophys. 242 (1985) 240-247.
49. S.N. Timasheff, T. Arakawa, Stabilization of protein structure by solvents, in: T.E. Creighton) (Ed.), Protein Structure. A Practical Approach, IRL Press, New York, 1989, pp. 331-345.
50. L.M. Crowe, C. Womersley, J.H. Crowe, D. Reid, L. Appel, A. Rudolph, Prevention of fusion and leakage in freeze-dried liposomes by carbohydrates, Biochim. Biophys. Acta 861 (1986) 131-140.
51. T. Arakawa, Y. Kita, J.F. Carpenter, Protein solvent interaction in pharmaceutical formulations, Pharm. Res. 8 (1991) 285-291.
52. J.F. Carpenter, L.H. Crowe, T. Arakawa, Comparison of solute-induced protein stabilization in aqueous solution and in the frozen and dried states, J. Dairy Sci. 73 (1990) 3627-3636.
53. J.C. Lee, K. Gekko, S.N. Timasheff, Measurements of preferential solvent interactions by densimetric techniques, Methods Enzymol. 81 (1979) 26-49.
54. J.A. Schellman, The thermodynamic stability of proteins, Annu. Rev. Biophys. Chem. 16 (1987) 115-137.
55. J.A. Schellman, Solvent denaturation, Biopolymers 17 (1978) 1305-1322.
56. J.A. Schellman, Selective binding and solvent denaturation, Biopolymers 26 (1987) 549-559.
57. E.F. Casassa, H. Eisenberg, Thermodynamic analysis of multicomponent solutions, Adv. Protein Chem. 19 (1964) 287-395.
58. E. Selinioti, D. Nikolopoulose, Y. Manetas, Organic co-solutes as stabilizers of phosphoenolpyruvate carboxylase in storage: an interpretation of their action, Aust. J. Plant Physiol. 143 (1987) 203-210.
59. L. Wilson, Properties of colchicine binding protein from chick embryo brain. Interactions with vinca alkaloids and podophyllotoxin, Biochemistry 9 (1970) 4999-5007.
60. T. Arakawa, S.N. Timasheff, Preferential interactions of proteins with salts in concentrated solutions, Biochemistry 21 (1982) 6545-6552.
61. T. Arakawa, S.N. Timasheff, Protein stabilization and destabilization by guanidinium salts, Biochemistry 23 (1984) 5924-5929.
62. T. Arakawa, S.N. Timasheff, The stabilization of proteins by osmolytes, Biophys. J. 47 (1985) 411-414.
63. T. Arakawa, S.N. Timasheff, Mechanism of polyethylene glycol interactions with proteins, Biochemistry 24 (1985) 6756.
64. K. Gekko, T. Morikawa, Preferential hydration of bovine serum albumin in polyhydric alcohol-water mixtures, J. Biochem. 90 (1981) 38-50.
65. T. Arakawa, S.N. Timasheff, Abnormal solubility behavior of β-lactoglobulin: salting-in by glycine and NaCl, Biochemistry 26 (1987) 5147-5153.
66. K.C. Aune, S.N. Timasheff, Some observations of the sedimentation of chicken heart glyceraldehyde 3-phosphate dehydrogenase, Biochemistry 9 (1970) 1481-1484.
67. K. Gekko, S.N. Timasheff, Mechanism of protein stabilization by glycerol. Preferential hydration in glycerol-water mixtures, Biochemistry 20 (1981) 4667-4676.
68. S.N. Timasheff, J.C. Lee, E.P. Pittz, N. Tweedy, The interaction of tubulin and other proteins with structure stabilizing solvents, J. Colloid Interf. Sci. 55 (1976) 658-663.
69. G.C. Na, Interaction of calf skin collagen with glycerol: linked function analysis, Biochemistry 25 (1986) 967-973.
70. 2 system, Biochemistry 29 (1990) 1914-1923.
71. J.C. Lee, S.N. Timasheff, Partial specific volumes and interactions with solvent components of proteins in guanidine hydrochloride, Biochemistry 13 (1974) 257-265.
72. V. Prakash, C. Loucheux, S.D. Scheuffeld, M.J. Gorbunoff, S.N. Timasheff, Interactions of proteins with solvent components in 8 M urea, Arch. Biochem. Biophys. 210 (1981) 455-464.
73. S.N. Timasheff, H. Inoue, Preferential binding of solvent components to proteins in mixed water-organic solvent systems, Biochemistry 7 (1968) 2501-2513.
74. T. Arakawa, R. Bhat, S.N. Timasheff, Why preferential hydration does not always stabilize the native structure of globular proteins, Biochemistry 29 (1990) 1924-1931.
75. J.C. Lee, L.L.Y. Lee, Interaction of calf brain tubulin with poly(ethylene glycols), Biochemistry 18 (1979) 5518-5526.
76. J.C. Lee, L.L.Y. Lee, Preferential solvent interactions between proteins and polyethylene glycols, J. Biol. Chem. 256 (1981) 625-631.
77. E.P. Pittz, S.N. Timasheff, Interaction of ribonuclease A with aqueous 2-methyl-2,4-pentanediol, Biochemistry 17 (1978) 615-623.
78. J.C. Lee, L.L.Y. Lee, Thermal stability of proteins in the presence of polyethylene glycols, Biochemistry 26 (1987) 7813-7819.
79. T. Arakawa, J.F. Carpenter, Y.A. Kita, J.H. Crowe, The basis for toxicity of certain cryoprotectants: a hypothesis, Cryobiology 27 (1990) 401-415.
80. J.F. Brandts, J. Fu, J.F. Nordin, The low temperature denaturation of chymotrypsinogen in aqueous solution and in frozen aqueous solution, in: G.E.W. Wolstenholme, M.O. O'Conner (Eds.), The Frozen Cell, Churchill, London, 1970, pp. 189-212.
81. W.J. Becktel, J.A. Schellman, Protein stability curves, Biopolymers 26 (1987) 1859-1877.
82. P.L. Privaloy, Cold denaturation of proteins, Crit. Rev. Biochem. Mol. Biol. 25 (1990) 281-305.
83. P.H. von Hippel, T. Shleich, The effects of neutral salts on the conformational stability of macromolecules in solution, in: S.N. Timasheff, G.D. Fasman (Eds.), Structure and Stability of Macromolecules, Vol. 2, Dekker, New York, 1969, pp. 417-574.
84. K. Shikama, I. Yamazaki, Denaturation of catalase by freezing and thawing, Nature 190 (1961) 83-84.
85. O.P. Chilson, L.A. Costello, N.O. Kaplan, Effects of freezing on enzymes, Fed. Proc. 24 (2) (1965) S55-S65.
86. 2O, Arch. Biochem. Biophys. 81 (1959) 319-329.
87. F.S. Soliman, L. van den Berg, Factors affecting freezing damage of lactic dehydrogenase, Cryobiology 8 (1971) 73-78.
88. J.H. Whittam, H.L. Rosano, Effects of the freeze-thaw process on α-amylase, Cryobiology 10 (1973) 240-243.
89. W.N. Fishbein, J.W. Winkert, Parameters of biological freezing damage in simple solutions: catalase, Cryobiology 15 (1978) 168-177.
90. J.F. Carpenter, T. Arakawa, J.H. Crowe, Interactions of stabilizing additives with proteins during freeze-thawing and freeze-drying, Dev. Biol. Stand. 74 (1991) 225-239.
91. S.H. Loomis, J.F. Carpenter, T.J. Anchordoguy, J.H. Crowe, B.R. Branchini, Cryoprotective capacity of end products of anaerobic metabolism, J. Exp. Zool. 252 (1989) 9-15.
92. M.J. Pikal, Freeze-drying of proteins. I. Process design, Biopharmaceutics 3 (1990) 18-27.
93. K. Hellman, D.S. Miller, R.A. Cammack, The effect of freeze-drying on the quaternary structure of L-asparaginase from Erwinia carotovora, Biochim. Biophys. Acta 749 (1983) 133-142.
94. M.W. Townsend, P.P. DeLuca, Use of lyoprotectants in freeze-drying of a model protein, J. Parenter. Sci. Technol. 42 (1988) 190-199.
95. M.W. Townsend, P.R. Byron, P.P. DeLuca, The effects of formulation additives on degradation of freeze-dried ribonuclease A, Pharm. Res. 7 (1990) 1086-1091.
96. K. Izutsu, S. Yoshioka, Y. Takeda, The effects of additives on the stability of freeze-dried β-galactose stored at elevated temperature, Int. J. Pharm. 71 (1991) 137-146.
97. M.W. Townsend, P.P. DeLuca, Nature of aggregates formed during storage of freeze-dried ribonuclease A, J. Pharm. Sci. 80 (1991) 63-66.
98. M.J. Pikal, K.M. Dellerman, M.L. Roy, R.M. Riggin, The effects of formulation variables on the stability of freeze-dried human growth hormone, Pharm. Res. 8 (1991) 427-436.
99. M.S. Hora, R.K. Rana, F.W. Smith, Lyophilized formulations of recombinant tumor necrosis factor, Pharm. Res. 9 (1992) 33-36.
100. 2 monoclonal antibody (MN12), Pharm. Res. 9 (1992) 266-270.
101. R. Tanaka, T. Takeda, R. Miyajima, Cryoprotective effect of saccharides on denaturation of catalase during freeze-drying, Chem. Pharm. Biol. 39 (1991) 1091-1094.
102. K. Lippert, E.A. Galinski, Enzyme stabilization by ectoine-type compatible solutes: protection against heating, freezing and drying, Appl. Microbiol. Biotechnol. 37 (1992) 61-65.
103. F. Franks, R.H.M. Hatley, S.F. Mathias, Materials science and production of shelf-stable biologicals, Biopharmaceutics 4 (1991) 38-42.
104. H. Levine, L. Slade, in: H. Schwartzberg, R.W. Hartel (Eds.), Physical Chemistry of Foods, Marcel Dekker, New York, 1992, pp. 83-221.
105. S.J. Prestrelski, N. Tedeschi, T. Arakawa, J.F. Carpenter, Dehydration induced conformational transitions in proteins and their inhibition by stabilizers, Biophys. J. 65 (1993) 661-671.
106. P.H. Yancey, M.E. Clark, S.C. Hand, R.D. Bowlus, G.N. Somero, Living with water stress: evolution of osmotic systems, Science 217 (1982) 1214-1222.
107. J.F. Carpenter, S.J. Prestrelski, T. Arakawa, Separation of freezing- and drying-induced denaturation of lyophilized proteins using stress-specific stabilization. I. Enzyme activity and calorimetric studies, Arch. Biochem. Biophys. 303 (1993) 456-464.
108. S.J. Prestrelski, T. Arakawa, J.F. Carpenter, Separation of freezing- and drying-induced denaturation of lyophilized proteins using stress-specific stabilization. II. Structural studies using infrared spectroscopy, Arch. Biochem. Biophys. 303 (1993) 465-473.
109. T. Boone, V. Chazin, W. Kenney, E. Swanson, B. Altrock, Construction, purification and biological activities of recombinant human interleukin-2 analogs, Dev. Biol. Stand. 69 (1988) 157-168.
110. A. Wang, S.-D. Lu, D.F. Mark, Site-specific mutagenesis of the human interleukin-2 gene: structure-function analysis of the cysteine residues, Science 224 (1984) 1431-1433.
111. H.S. Lu, T.C. Boone, L.M. Souza, R-H. Lai, Disulfide and secondary structures of recombinant human granulocyte colony stimulating factor, Arch. Biochem. Biophys. 268 (1989) 81-92.
112. X. Zhu, H. Komiya, A. Chirino, S. Faham, G.M. Fox, T. Arakawa, B.T. Hsu, D.C. Rees, Three-dimensional structures of acidic and basic fibroblast growth factors, Science 251 (1991) 90-93.
113. G.M. Fox, S.G. Schiffer, M.F. Rohde, L.B. Tsai, A.R. Banks, T. Arakawa, Production, biological activity, and structure of recombinant basic fibroblast growth factor and an analog with cysteine replaced by serine, J. Biol. Chem. 263 (1988) 18452-18458.