Study of the individual contributions of ice formation and freeze-concentration on isothermal stability of lactate dehydrogenase during freezing

Journal of Pharmaceutical Sciences

Volumn 97, Issue 2, 2008, Pages 798-814

  Bhatnagar, Bakul S ^a   Pikal, Michael J ^a   Bogner, Robin H ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Freeze concentration; Freeze drying; Freeze thawing; Ice nucleation; Ice surface area; Lyophilization; Preformulation; Protein formulation; Protein stability and freezing

Indexed keywords

BUFFER; CITRIC ACID; ICE; LACTATE DEHYDROGENASE; SUCROSE;

ARTICLE; DIFFERENTIAL SCANNING CALORIMETRY; ENZYME DENATURATION; ENZYME STABILITY; FREEZE DRYING; FREEZE THAWING; PH; SOLUTE; SURFACE PROPERTY;

EID: 39749167996     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.21017     Document Type: Article

References (72)

1. Pikal MJ. 2004. 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. 2nd edition. Marcel Dekker, Inc., New York, pp 63-107.
2. Franks F. 1992. Freeze-drying: From empiricism to predictability. The significance of glass transitions. Dev Biol Stand 74:9-19.
3. Carpenter JF, Pikal MJ, Chang BS, Randolph TW. 1997. Rational design of stable lyophilized protein formulations: Some practical advice. Pharm Res 14:969-975.
4. Tang X, Pikal MJ. 2004. Design of freeze-drying processes for pharmaceuticals: Practical advice. Pharm Res 21:191-200.
5. Chang BS, Patro SY. 2004. Freeze-drying process development for protein pharmaceuticals. In: Cost-antino HR, Pikal Michael J, editors. Lyophilization of biopharmaceuticals. edition. AAPS Press, Arlington, VA, pp 113-138.
6. Privalov PL. 1990. Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25:281-305.
7. Franks F. 1995. Protein destabilization at low temperatures. Adv Protein Chem 46:105-139.
8. Tang XC, Pikal MJ. 2005. Measurement of the kinetics of protein unfolding in viscous systems and implications for protein stability in freeze-drying. Pharm Res 22:1176-1185.
9. Szkudlarek BA. 1997. Selective crystallization of phosphate buffer components and pH changes during freezing: Implications to protein stability. University of Michigan, Ann Arbor, MI, USA, 188 p.
10. Pikal-Cleland KA, Rodriguez-Hornedo N, Amidon GL, Carpenter JF. 2000. Protein denaturation during freezing and thawing in phosphate buffer systems: Monomeric and tetrameric β-galactosidase. Arch Biochem Biophys 384:398-406.
11. Heller MC, Carpenter JF, Randolph TW. 1996. Effects of phase separating systems on lyophilized hemoglobin. J Pharm Sci 85:1358-1362.
12. Izutsu K-I, Kojima S. 2000. Freeze-concentration separates proteins and polymer excipients into different amorphous phases. Pharm Res 17:1316-1322.
13. Strambini GB, Gabellieri E. 1996. Proteins in frozen solutions: Evidence of ice-induced partial unfolding. Biophys J 70:971-976.
14. Chang BS, Kendrick BS, Carpenter JF. 1996. Surface-induced denaturation of proteins during freezing and its inhibition by surfactants. J Pharm Sci 85:1325-1330.
15. Gabellieri E, Strambini GB. 2003. Perturbation of protein tertiary structure in frozen solutions revealed by 1-anilino-8-naphthalene sulfonate fluorescence. Biophys J 85:3214-3220.
16. Kiermeier F. 1947. Influence of freezing on the activity of enzymes. Biochem Z 318:275-296.
17. Shikama K, Yamazaki I. 1961. Denaturation of catalase by freezing and thawing. Nature 190:83-84.
18. Chilson OP, Costello LA, Kaplan NO. 1965. Effects of freezing on enzymes. Fed Proc 24:55-65.
19. Greiff D, Kelly RT. 1966. Cryotolerance of enzymes. I. Freezing of lactic dehydrogenase. Cryobiology 2:335-341.
20. Brandts JF, Fu J, Nordin JH. 1970. Low temperature denaturation of chymotrypsinogen in aqueous solution and in frozen aqueous solution. In: Wolstenholme GEW, O'Connor M, editors. The frozen cell, A Ciba foundation symposium, edition. J & A Churchill, London, pp 189-212.
21. Soliman FS, Van den Berg L. 1971. Factors affecting freezing damage of lactic dehydrogenase. Cryobiology 8:73-78.
22. Pincock RE, Lin W-S. 1973. Denaturation of α-chymotrypsin in frozen aqueous solutions. J Agric Food Chem 21:2-5.
23. Whittam JH, Rosano HL. 1973. Effects of the freeze-thaw process on α-amylase. Cryobiology 10:240-243.
24. Fishbein WN, Winkert JW. 1977. Parameters of biological freezing damage in simple solutions: Catalase. I. The characteristic pattern of intracellular freezing damage exhibited in a membraneless system. Cryobiology 14:389-398.
25. Tamiya T, Okahashi N, Sakuma R, Aoyama T, Akahane T, Matsumoto JJ. 1985. Freeze denaturation of enzymes and its prevention with additives. Cryobiology 22:446-456.
26. Carpenter JF, Crowe JH, Arakawa T. 1990. Comparison of solute-induced protein stabilization in aqueous solution and in the frozen and dried states. J Dairy Sci 73:3627-3636.
27. Eckhardt BM, Oeswein JQ, Bewley TA. 1991. Effect of freezing on aggregation of human growth hormone. Pharm Res 8:1360-1364.
28. Carpenter JF, Prestrelski SJ, Arakawa T. 1993. Separation of freezing- and drying-induced denaturation of lyophilized proteins using stress-specific stabilization. I. Enzyme activity and calorimetric studies. Arch Biochem Biophys 303:456-464.
29. Nema S, Avis KE. 1993. Freeze-thaw studies of a model protein, lactate dehydrogenase, in the presence of cryoprotectants. J Parenter Sci Technol 47:76-83.
30. Izutsu K-I, Yoshioka S, Terao T. 1994. Stabilizing effect of amphiphilic excipients on the freeze-thawing and freeze-drying of lactate dehydrogenase. Biotechnol Bioeng 43:1102-1107.
31. Hsu CC, Nguyen HM, Yeung DA, Brooks DA, Koe GS, Bewley TA, Pearlman R. 1995. Surface denaturation at solid-void interface-a possible pathway by which opalescent particulates form during the storage of lyophilized tissue-type plasminogen activator at high temperatures. Pharm Res 12:69-77.
32. Jameel F, Kalonia D, Bogner R. 1995. The effect of hetastarch on the stability of L-asparaginase during freeze-thaw cycling. PDA J Pharm Sci Technol 49:127-131.
33. Anchordoquy TJ, Carpenter JF. 1996. Polymers protect lactate dehydrogenase during freeze-drying by inhibiting dissociation in the frozen state. Arch Biochem Biophys 332:231-238.
34. Allison SD, Dong A, Carpenter JF. 1996. Counter-acting effects of thiocyanate and sucrose on chymotrypsinogen secondary structure and aggregation during freezing, drying, and rehydration. Biophys J 71:2022-2032.
35. Jiang S, Nail SL. 1998. Effect of process conditions on recovery of protein activity after freezing and freeze-drying. Eur J Pharm Biopharm 45:249-257.
36. Sane SU. 1999. Secondary structure characterization of proteins using amide I band raman spectroscopy: Methods development and applications to bioprocessing. Rensselaer Polytechnic Institute, Troy, NY, USA, 178 p.
37. Anchordoquy TJ, Izutsu K-I, Randolph TW, Carpenter JF. 2001. Maintenance of quaternary structure in the frozen state stabilizes lactate dehydrogenase during freeze-drying. Arch Biochem Biophys 390:35-41.
38. Hillgren A, Lindgren J, Alden M. 2002. Protection mechanism of Tween 80 during freeze-thawing of a model protein, LDH. Int J Pharm 237:57-69.
39. Mi Y, Wood G, Thoma L, Rashed S. 2002. Effects of polyethylene glycol molecular weight and concentration on lactate dehydrogenase activity in solution and after freeze-thawing. PDA J Pharm Sci Technol 56:115-123.
40. Webb SD, Golledge SL, Cleland JL, Carpenter JF, Randolph TW. 2002. Surface adsorption of recombinant human interferon-γ in lyophilized and spray-lyophilized formulations. J Pharm Sci 91:1474-1487.
41. Cao E, Chen Y, Cui Z, Foster PR. 2003. Effect of freezing and thawing rates on denaturation of proteins in aqueous solutions. Biotechnol Bioeng 82:684-690.
42. Hatley RHM, Franks F, Mathias SF. 1987. The stabilization of labile biochemicals by undercooling. Process Biochem 22:169-172.
43. Taborsky G. 1979. Protein alterations at low temperatures: An overview. In: Fennema O, editor. Proteins at low temperatures, edition. American Chemical Society, Washington, DC, pp 1-26.
44. Larsen SS. 1973. Stability of drugs in frozen systems. VT. Effect of freezing upon pH for buffered aqueous solutions. Arch Pharm Chemi Sci Ed 1:41-53.
45. Sarciaux J-M, Mansour S, Hageman MJ, Nail SL. 1999. Effects of buffer composition and processing conditions on aggregation of bovine IgG during freeze-drying. J Pharm Sci 88:1354-1361.
46. Webb SD, Cleland JL, Carpenter JF, Randolph TW. 2003. Effects of annealing lyophilized and spray-lyophilized formulations of recombinant human interferon-γ. J Pharm Sci 92:715-729.
47. Gabellieri E, Strambini Giovanni B. 2006. ANS fluorescence detects widespread perturbations of protein tertiary structure in ice. Biophys J 90:3239-3245.
48. Workman EJ, Reynolds SE. 1950. Electrical phenomena occurring during the freezing of dilute aqueous solutions and their possible relation to thunderstorm electricity. Phys Rev 78:254-259.
49. Lodge JP, Jr., Baker ML, Pierrard JM. 1956. Ion separation in dilute solutions by freezing. J Chem Phys 24:716-719.
50. Cobb AW, Gross GW. 1969. Interfacial electrical effects observed during the freezing of dilute electrolytes in water. J Electrochem Soc 116:796-804.
51. Nanis L, Klein I. 1970. Effect of substrate on the freezing potential. J Colloid Interface Sci 32:449-455.
52. Gross GW. 1972. Solute interference effects in freezing potentials of dilute electrolytes. In: Jellinek HHG, editor. Water structure at the water-polymer interface, edition. Plenum Press, New York, pp 106-125.
53. Hubel A, Koerber C, Cravalho EG, Rau G. 1988. Transient electrical potentials measured during the unidirectional freezing of sodium chloride/water solutions. J Cryst Growth 87:69-78.
54. Rastogi RP, Tripathi AK. 1985. Effect of nonionic solutes on the freezing potential of dilute ionic aqueous solutions. J Chem Phys 83:1404-1405.
55. Taborsky G. 1970. Effect of freezing and thawing on the conformation of phosvitin. J Biol Chem 245:1054-1062.
56. Bhatnagar BS, Nehm SJ, Pikal MJ, Bogner RH. 2005. Post-thaw aging affects activity of lactate dehydrogenase. J Pharm Sci 94:1382-1388.
57. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
58. Bhatnagar BS, Cardon S, Pikal MJ, Bogner RH. 2005. Reliable determination of freeze-concentration using DSC. Thermochim Acta 425:149-163.
59. Gomez G, Pikal MJ, Rodriguez-Hornedo N. 2001. Effect of initial buffer composition on pH changes during far-from-equilibrium freezing of sodium phosphate buffer solutions. Pharm Res 18:90-97.
60. Dawson PJ, Hockley DJ. 1992. Scanning electron microscopy of freeze-dried preparations: Relationship of morphology to freeze-drying parameters. Dev Biol Stand 74:185-192 (Biol. Prod. Freeze-Drying Formulation).
61. Kasraian K, DeLuca PP. 1995. The effect of tertiary butyl alcohol on the resistance of the dry product layer during primary drying. Pharm Res 12:491-495.
62. Rambhatla S, Ramot R, Bhugra C, Pikal Michael J. 2004. Heat and mass transfer scale-up issues during freeze drying: II. Control and characterization of the degree of supercooling. AAPS PharmSciTech 5:e58.
63. Izutsu K-I, Yoshioka S, Terao T. 1994. Effect of mannitol crystallinity on the stabilization of enzymes during freeze-drying. Chem Pharm Bull 42:5-8.
64. Chatterjee K, Shalaev EY, Suryanarayanan R. 2005. Raffinose crystallization during freeze-drying and its impact on recovery of protein activity. Pharm Res 22:303-309.
65. Pikal-Cleland KA, Carpenter JF. 2001. Lyophilization-induced protein denaturation in phosphate buffer systems: Monomeric and tetrameric β-galactosidase. J Pharm Sci 90:1255-1268.
66. Mi Y, Wood G, Thoma L. 2004. Cryoprotection mechanisms of polyethylene glycols on lactate dehydrogenase during freeze-thawing. AAPS J6:e22.
67. Yamamoto S, Storey KB. 1988. Dissociation-association of lactate dehydrogenase isozymes: Influences on the formation of tetramers versus dimers of M4-LDH and H4-LDH. Int J Biochem 20:1261-1265.
68. Searles JA. 2004. Freezing and annealing phenomena in lyophilization. In: Rey L, May JC, editors. Freeze-drying/lyophilization of pharmaceutical and biological products, edition. Marcel Dekker, Inc., New York, NY, pp 109-145.
69. Shalaev EY, Franks F. 1995. Structural glass transitions and thermophysical processes in amorphous carbohydrates and their super-saturated solutions. J Chem Soc, Faraday Trans 91:1511-1517.
70. Roos YH. 1997. Frozen state transitions in relation to freeze drying. J Therm Anal 48:535-544.
71. Hatley RHM, Franks F. 1989. The cold-induced denaturation of lactate dehydrogenase at sub-zero temperatures in the absence of perturbants. FEBS Lett 257:171-173.
72. Tang XC, Pikal MJ. 2005. The effect of stabilizers and denaturants on the cold denaturation temperatures of proteins and implications for freeze-drying. Pharm Res 22:1167-1175.