Size and molecular flexibility of sugars determine the storage stability of freeze-dried proteins

Molecular Pharmaceutics

Volumn 12, Issue 3, 2015, Pages 684-694

  Tonnis, W F ^a   Mensink, M A ^a   De Jager, A ^a   Van Der Voort Maarschalk, K ^a   Frijlink, H W ^a   Hinrichs, W L J ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

dextran; inulin; lyophilization; mobility; oligosaccharides; stabilization; steric hindrance; trehalose; vitrification; water replacement

Indexed keywords

CARBOHYDRATE; DEXTRAN 70; DISACCHARIDE; INULIN; OLIGOSACCHARIDE; POLYSACCHARIDE; PROTEIN; STABILIZING AGENT; TREHALOSE; WATER;

AQUEOUS SOLUTION; ARTICLE; CHEMICAL INTERACTION; DIFFERENTIAL SCANNING CALORIMETRY; FLUORESCENCE SPECTROSCOPY; FREEZE DRYING; GLASS TRANSITION TEMPERATURE; HUMIDITY; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR SIZE; PRIORITY JOURNAL; PROTEIN STABILITY; SENSITIVITY ANALYSIS; STEREOSPECIFICITY; STORAGE TEMPERATURE; WATER TRANSPORT; CHEMICAL STRUCTURE; CHEMISTRY; DRUG STABILITY; DRUG STORAGE; HUMAN; MEDICINAL CHEMISTRY; MOLECULAR WEIGHT; PHARMACEUTICS; SPECTROFLUOROMETRY; TRANSITION TEMPERATURE;

BIOPHARMACEUTICS; CARBOHYDRATES; CHEMISTRY, PHARMACEUTICAL; DRUG STABILITY; DRUG STORAGE; FREEZE DRYING; HUMANS; MOLECULAR STRUCTURE; MOLECULAR WEIGHT; PROTEIN STABILITY; PROTEINS; SPECTROMETRY, FLUORESCENCE; TRANSITION TEMPERATURE;

EID: 84923875549     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp500423z     Document Type: Article

References (36)

1. Wang, W. Lyophilization and Development of Solid Protein Pharmaceuticals Int. J. Pharm. 2000, 203, 1-60
2. Chang, L.; Pikal, M. Mechanisms of Protein Stabilization in the Solid State J. Pharm. Sci. 2009, 98, 2886-2908
3. Chang, L. L.; Shepherd, D.; Sun, J.; Ouellette, D.; Grant, K. L.; Tang, X. C.; Pikal, M. J. Mechanism of Protein Stabilization by Sugars during Freeze-Drying and Storage: Native Structure Preservation, Specific Interaction, And/or Immobilization in a Glassy Matrix? J. Pharm. Sci. 2005, 94, 1427-1444
4. Grasmeijer, N.; Stankovic, M.; de Waard, H.; Frijlink, H. W.; Hinrichs, W. L. J. Unraveling Protein Stabilization Mechanisms: Vitrification and Water Replacement in a Glass Transition Temperature Controlled System Biochim. Biophys. Acta 2013, 1834, 763-769
5. Anchordoquy, T. J.; Izutsu, K. I.; Randolph, T. W.; Carpenter, J. F. Maintenance of Quaternary Structure in the Frozen State Stabilizes Lactate Dehydrogenase during Freeze-Drying Arch. Biochem. Biophys. 2001, 390, 35-41
6. Allison, S. D.; Chang, B.; Randolph, T. W.; Carpenter, J. F. Hydrogen Bonding between Sugar and Protein Is Responsible for Inhibition of Dehydration-Induced Protein Unfolding Arch. Biochem. Biophys. 1999, 365, 289-298
7. Carpenter, J. F.; Crowe, J. H. An Infrared Spectroscopic Study of the Interactions of Carbohydrates with Dried Proteins Biochemistry 1989, 28, 3916-3922
8. Cicerone, M. T.; Douglas, J. F. B-Relaxation Governs Protein Stability in Sugar-Glass Matrices Soft Matter 2012, 8, 2983
9. Hedoux, A.; Paccou, L.; Achir, S.; Guinet, Y. Mechanism of Protein Stabilization by Trehalose during Freeze-Drying Analyzed by in Situ Micro-Raman Spectroscopy J. Pharm. Sci. 2013, 102, 2484-2494
10. Lerbret, A.; Affouard, F.; Hédoux, A.; Krenzlin, S.; Siepmann, J.; Bellissent-Funel, M.-C.; Descamps, M. How Strongly Does Trehalose Interact with Lysozyme in the Solid State? Insights from Molecular Dynamics Simulation and Inelastic Neutron Scattering J. Phys. Chem. B 2012, 116, 11103-11116
11. Francia, F.; Dezi, M.; Mallardi, A.; Palazzo, G.; Cordone, L.; Venturoli, G. Protein- Matrix Coupling/Uncoupling in "Dry" Systems of Photosynthetic Reaction Center Embedded in Trehalose/Sucrose: The Origin of Trehalose Peculiarity J. Am. Chem. Soc. 2008, 10240-10246
12. Frauenfelder, H.; Chen, G.; Berendzen, J.; Fenimore, P. W.; Jansson, H.; McMahon, B. H.; Stroe, I. R.; Swenson, J.; Young, R. D. A Unified Model of Protein Dynamics Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 5129-5134
13. Martins, S. I. F. S.; Jongen, W. M. F.; Boekel, M. A. J. S. Van. A Review of Maillard Reaction in Food and Implications to Kinetic Modelling Trends Food Sci. Technol. 2001, 11, 364-373
14. Lievonen, S. M.; Laaksonen, T. J.; Roos, Y. H. Glass Transition and Reaction Rates: Nonenzymatic Browning in Glassy and Liquid Systems J. Agric. Food Chem. 1998, 8561, 2778-2784
15. Hinrichs, W. L. J.; Sanders, N. N.; De Smedt, S. C.; Demeester, J.; Frijlink, H. W. Inulin Is a Promising Cryo- and Lyoprotectant for PEGylated Lipoplexes J. Controlled Release 2005, 103, 465-479
16. Jain, N. K.; Roy, I. Effect of Trehalose on Protein Structure Protein Sci. 2008, 18, 24-36
17. Fox, T. G.; Flory, P. J. Second-Order Transition Temperatures and Related Properties of Polystyrene. I. Influence of Molecular Weight J. Appl. Phys. 1950, 21, 581-591
18. Allison, S. D.; Manning, M. C.; Randolph, T. W.; Middleton, K.; Davis, a; Carpenter, J. F. Optimization of Storage Stability of Lyophilized Actin Using Combinations of Disaccharides and Dextran J. Pharm. Sci. 2000, 89, 199-214
19. Garzon-Rodriguez, W.; Koval, R. L.; Chongprasert, S.; Krishnan, S.; Randolph, T. W.; Warne, N. W.; Carpenter, J. F. Optimizing Storage Stability of Lyophilized Recombinant Human Interleukin-11 with Disaccharide/hydroxyethyl Starch Mixtures J. Pharm. Sci. 2004, 93, 684-696
20. Tonnis, W. F.; Amorij, J.-P.; Vreeman, M. a; Frijlink, H. W.; Kersten, G. F.; Hinrichs, W. L. J. Improved Storage Stability and Immunogenicity of Hepatitis B Vaccine after Spray-Freeze Drying in Presence of Sugars Eur. J. Pharm. Sci. 2014, 55, 36-45
21. Hinrichs, W. L.; Prinsen, M. G.; Frijlink, H. W. Inulin Glasses for the Stabilization of Therapeutic Proteins Int. J. Pharm. 2001, 215, 163-174
22. Vereyken, I. J.; van Kuik, J. A.; Evers, T. H.; Rijken, P. J.; de Kruijff, B. Structural Requirements of the Fructan-Lipid Interaction Biophys. J. 2003, 84, 3147-3154
23. Albertsson, P. Partition of Cell Particles and Macromolecules; Wiley-Interscience: New York, 1986.
24. Barclay, T.; Ginic-Markovic, M.; Cooper, P.; Petrovsky, N. Inulin: A Versatile Polysaccharide with Multiple Pharmaceutical and Food Chemical Uses J. Excipients Food Chem. 2010, 1, 27-50
25. Livingston, D.; Hincha, D.; Heyer, A. The Relationship of Fructan to Abiotic Stress Tolerance in Plants. In Recent advances in fructooligosaccharides research; Norio, S.; Noureddine, B.; Shuichi, O., Eds.; Research Signpost: Kerala, India, 2007; Vol. 661, pp 181-199.
26. Zhao, Q.; Wang, Y.; Freed, D.; Fu, T.; Gimenez, J. A.; Sitrin, R. D.; Washabaugh, M. W. Maturation of Recombinant Hepatitis B Virus Surface Antigen Particles Hum. Vaccines 2006, 2, 174-180
27. Franssen, O.; Vos, O. P.; Hennink, W. E. Delayed Release of a Model Protein from Enzymatically-Degrading Dextran Hydrogels J. Controlled Release 1997, 44, 237-245
28. United States Pharmacopeial Convention. Insulin. In The United States Pharmacopeia; 2006; pp 1132-1134.
29. Yuan, W.; Wu, F.; Geng, Y.; Xu, S.; Jin, T. Preparation of Dextran Glassy Particles through Freezing-Induced Phase Separation Int. J. Pharm. 2007, 339, 76-83
30. Velikov, V.; Borick, S.; Angell, C. A. The Glass Transition of Water, Based on Hyperquenching Experiments Science 2001, 294, 2335-2338
31. Giovambattista, N.; Angell, C. A.; Sciortino, F.; Stanley, H. E. The Glass Transition Temperature of Water: A Simulation Study Phys. Rev. Lett. 2004, 93, 047801
32. Isbell, H.; Snyder, C.; Holt, N. B.; Dryden, M. R. Determination of Molecular Weights of Dextrans by Means of Alkaline Copper Reagents J. Res. Natl. Bur. Stand. 1953, 50, 81-86
33. Hancock, B. C.; Shamblin, S. L. Molecular Mobility of Amorphous Pharmaceuticals Determined Using Differential Scanning Calorimetry Thermochim. Acta 2001, 380, 95-107
34. Mizuno, M.; Pikal, M. J. Is the Pre-Tg DSC Endotherm Observed with Solid State Proteins Associated with the Protein Internal Dynamics? Investigation of Bovine Serum Albumin by Solid State Hydrogen/deuterium Exchange Eur. J. Pharm. Biopharm. 2013, 85, 170-176
35. Pieters, S.; De Beer, T.; Kasper, J. C.; Boulpaep, D.; Waszkiewicz, O.; Goodarzi, M.; Tistaert, C.; Friess, W.; Remon, J.-P.; Vervaet, C.; Vander Heyden, Y. Near-Infrared Spectroscopy for in-Line Monitoring of Protein Unfolding and Its Interactions with Lyoprotectants during Freeze-Drying Anal. Chem. 2012, 84, 947-955
36. Walstra, P. Physical Chemistry of Foods; Food Science and Technology; CRC Press: Boca Raton, FL, 2002.