Inulin sugar glasses preserve the structural integrity and biological activity of influenza virosomes during freeze-drying and storage

European Journal of Pharmaceutical Sciences

Volumn 32, Issue 1, 2007, Pages 33-44

  de Jonge, Jørgen ^a   Amorij, Jean Pierre ^b   Hinrichs, Wouter L J ^b   Wilschut, Jan ^a   Huckriede, Anke ^a   Frijlink, Henderik W ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Delivery vehicle; Formulation of virosomes; Gene delivery; Influenza vaccine; Lyophilization; Stabilization

Indexed keywords

INULIN; PLASMID DNA; VIROSOME; VIROSOME VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG STABILITY; DRY POWDER; FEMALE; FREEZE DRYING; IMMUNIZATION; IMMUNOGENICITY; INFLUENZA; MACROMOLECULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHELF LIFE; STORAGE;

AMMONIUM CHLORIDE; ANIMALS; ANTIBODY FORMATION; CELL LINE; CENTRIFUGATION, DENSITY GRADIENT; CRICETINAE; DRUG STABILITY; DRUG STORAGE; ERYTHROCYTE MEMBRANE; FEMALE; FREEZE DRYING; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HEMAGGLUTINATION INHIBITION TESTS; INFLUENZA A VIRUS; INULIN; MEMBRANE FUSION; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, TRANSMISSION; PLASMIDS; TRANSFECTION; VACCINES, VIROSOME; VIROSOMES; VIRUS INTERNALIZATION;

EID: 34547104614     PISSN: 09280987     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejps.2007.05.112     Document Type: Article

References (57)

1. Allison S.D., Molina M.C., and Anchordoquy T.J. Stabilization of lipid/DNA complexes during the freezing step of the lyophilization process: the particle isolation hypothesis. Biochim. Biophys. Acta 1468 (2000) 127-138
2. Almeida J.D., Edwards D.C., Brand C.M., and Heath T.D. Formation of virosomes from influenza subunits and liposomes. LANCET 2 (1975) 899-901
3. Anchordoquy T.J., Carpenter J.F., and Kroll D.J. Maintenance of transfection rates and physical characterization of lipid/DNA complexes after freeze-drying and rehydration. Arch. Biochem. Biophys. 348 (1997) 199-206
4. Arkema A., Huckriede A., Schoen P., Wilschut J., and Daemen T. Induction of cytotoxic T lymphocyte activity by fusion-active peptide-containing virosomes. Vaccine 18 (2000) 1327-1333
5. Bieganski R.M., Fowler A., Morgan J.R., and Toner M. Stabilization of active recombinant retroviruses in an amorphous dry state with trehalose. Biotechnol. Prog. 14 (1998) 615-620
6. Böttcher C.J.F., van Gent C.M., and Pries C. A rapid and sensitive sub-micro phosphorus determination. Anal. Chim. Acta 24 (1961) 203-204
7. Bron R., Ortiz A., Dijkstra J., Stegmann T., and Wilschut J. Preparation, properties, and applications of reconstituted influenza virus envelopes (virosomes). Meth. Enzymol. 220 (1993) 313-331
8. Bron R., Ortiz A., and Wilschut J. Cellular cytoplasmic delivery of a polypeptide toxin by reconstituted influenza virus envelopes (virosomes). Biochemistry 33 (1994) 9110-9117
9. Bungener L., Serre K., Bijl L., Leserman L., Wilschut J., Daemen T., and Machy P. Virosome-mediated delivery of protein antigens to dendritic cells. Vaccine 20 (2002) 2287-2295
10. Bungener L., Huckriede A., de Mare A., de Vries-Idema J., Wilschut J., and Daemen T. Virosome-mediated delivery of protein antigens in vivo: efficient induction of class I MHC-restricted cytotoxic T lymphocyte activity. Vaccine 23 (2005) 1232-1241
11. Carpenter J.F., and Crowe J.H. An infrared spectroscopic study of the interactions of carbohydrates with dried proteins. Biochemistry 28 (1989) 3916-3922
12. Coenen F., Tolboom J.T., and Frijlink H.W. Stability of influenza sub-unit vaccine. Does a couple of days outside the refrigerator matter?. Vaccine 24 (2006) 525-531
13. Crowe L.M., Crowe J.H., Rudolph A., Womersley C., and Appel L. Preservation of freeze-dried liposomes by trehalose. Arch. Biochem. Biophys. 242 (1985) 240-247
14. Crowe J.H., Crowe L.M., Carpenter J.F., and Aurell Wistrom C. Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem. J. 242 (1987) 1-10
15. Croyle M.A., Roessler B.J., Davidson B.L., Hilfinger J.M., and Amidon G.L. Factors that influence stability of recombinant adenoviral preparations for human gene therapy. Pharm. Dev. Technol. 3 (1998) 373-383
16. Cruz P.E., Silva A.C., Roldao A., Carmo M., Carrondo M.J., and Alves P.M. Screening of novel excipients for improving the stability of retroviral and adenoviral vectors. Biotechnol. Prog. 22 (2006) 568-576
17. Daemen T., de Mare A., Bungener L., de Jonge J., Huckriede A., and Wilschut J. Virosomes for antigen and DNA delivery. Adv. Drug Deliv. Rev. 57 (2005) 451-463
18. Dass C.R. Lipoplex-mediated delivery of nucleic acids: factors affecting in vivo transfection. J. Mol. Med. 82 (2004) 579-591
19. de Bruijn I.A., Nauta J., Gerez L., and Palache A.M. Virosomal influenza vaccine: a safe and effective influenza vaccine with high efficacy in elderly and subjects with low pre-vaccination antibody titers. Virus Res. 103 (2004) 139-145
20. de Bruijn I.A., Nauta J., Cramer W.C., Gerez L., and Palache A.M. Clinical experience with inactivated, virosomal influenza vaccine. Vaccine 23 Suppl. 1 (2005) S39-S49
21. de Jonge J., Holtrop M., Wilschut J., and Huckriede A. Reconstituted influenza virus envelopes as an efficient carrier system for cellular delivery of small-interfering RNAs. Gene Ther. 13 (2006) 400-411
22. de Jonge J., Schoen P., ter Veer W., Stegmann T., Wilschut J., and Huckriede A. Use of a dialyzable short-chain phospholipid for efficient solubilization and reconstitution of influenza virus envelopes. Biochim. Biophys. Acta 1758 (2006) 527-536
23. Eriksson H.J., Hinrichs W.L., van Veen B., Somsen G.W., de Jong G.J., and Frijlink H.W. Investigations into the stabilisation of drugs by sugar glasses. I. Tablets prepared from stabilised alkaline phosphatase. Int. J. Pharm. 249 (2002) 59-70
24. Eriksson J.H., Hinrichs W.L., de Jong G.J., Somsen G.W., and Frijlink H.W. Investigations into the stabilization of drugs by sugar glasses. III. The influence of various high-pH buffers. Pharm. Res. 20 (2003) 1437-1443
25. European Pharmacopoeia. Immunochemical methods (2.7.1). European Pharmacopoeia. 5th ed. (2004), Council of Europe, Strasbourg p. 187
26. European Pharmacopoeia. Influenza vaccine (surface antigen, inactivated). European Pharmacopoeia. 5th ed. (2004), Council of Europe, Strasbourg pp. 673-674
27. Ferrari M.E., Nguyen C.M., Zelphati O., Tsai Y., and Felgner P.L. Analytical methods for the characterization of cationic lipid-nucleic acid complexes. Hum. Gene Ther. 9 (1998) 341-351
28. Gluck R., Mischler R., Brantschen S., Just M., Althaus B., and Cryz Jr. S.J. Immunopotentiating reconstituted influenza virus virosome vaccine delivery system for immunization against hepatitis A. J. Clin. Invest. 90 (1992) 2491-2495
29. Gluck U., Gebbers J.O., and Gluck R. Phase 1 evaluation of intranasal virosomal influenza vaccine with and without Escherichia coli heat-labile toxin in adult volunteers. J. Virol. 73 (1999) 7780-7786
30. Gomez G., Pikal M.J., and Rodriguez-Hornedo N. Effect of initial buffer composition on pH changes during far-from-equilibrium freezing of sodium phosphate buffer solutions. Pharm. Res. 18 (2001) 90-97
31. Haan L., Verweij W.R., Holtrop M., Brands R., van Scharrenburg G.J., Palache A.M., Agsteribbe E., and Wilschut J. Nasal or intramuscular immunization of mice with influenza subunit antigen and the B subunit of Escherichia coli heat-labile toxin induces IgA- or IgG-mediated protective mucosal immunity. Vaccine 19 (2001) 2898-2907
32. Hincha D.K., Zuther E., Hellwege E.M., and Heyer A.G. Specific effects of fructo- and gluco-oligosaccharides in the preservation of liposomes during drying. Glycobiology 12 (2002) 103-110
33. Hinrichs W.L., Prinsen M.G., and Frijlink H.W. Inulin glasses for the stabilization of therapeutic proteins. Int. J. Pharm. 215 (2001) 163-174
34. Hinrichs W.L., Sanders N.N., De Smedt S.C., Demeester J., and Frijlink H.W. Inulin is a promising cryo- and lyoprotectant for PEGylated lipoplexes. J. Control. Release 103 (2005) 465-479
35. Hinrichs W.L., Mancenido F.A., Sanders N.N., Braeckmans K., De Smedt S.C., Demeester J., and Frijlink H.W. The choice of a suitable oligosaccharide to prevent aggregation of PEGylated nanoparticles during freeze thawing and freeze drying. Int. J. Pharm. 311 (2006) 237-244
36. Huckriede A., Bungener L., ter Veer W., Holtrop M., Daemen T., Palache A.M., and Wilschut J. Influenza virosomes: combining optimal presentation of hemagglutinin with immunopotentiating activity. Vaccine 21 (2003) 925-931
37. Lamb R.A., and Krug R.M. In: K.D. M., and H.P. M. (Eds). Orthomyxoviridae: The Viruses and their Replication, vol. 4 (2001), Lippincott Williams & Wilkins, Philadelphia pp. 1487-1531
38. Levy J.A., and Fieldsteel A.H. Freeze-drying is an effective method for preserving infectious type C retroviruses. J. Virol. Meth. 5 (1982) 165-171
39. Li B., Li S., Tan Y., Stolz D.B., Watkins S.C., Block L.H., and Huang L. Lyophilization of cationic lipid-protamine-DNA (LPD) complexes. J. Pharm. Sci. 89 (2000) 355-364
40. Molina M.C., Armstrong T.K., Zhang Y., Patel M.M., Lentz Y.K., and Anchordoquy T.J. The stability of lyophilized lipid/DNA complexes during prolonged storage. J. Pharm. Sci. 93 (2004) 2259-2273
41. Ohkuma S., and Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. U.S.A. 75 (1978) 3327-3331
42. Peterson G.L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83 (1977) 346-356
43. Puri A., Booy F.P., Doms R.W., White J.M., and Blumenthal R. Conformational changes and fusion activity of influenza virus hemagglutinin of the H2 and H3 subtypes: effects of acid pretreatment. J. Virol. 64 (1990) 3824-3832
44. Randolph T.W. Phase separation of excipients during lyophilization: effects on protein stability. J. Pharm. Sci. 86 (1997) 1198-1203
45. Schebor C., Burin L., Buera M.P., Aguilera J.M., and Chirife J. Glassy state and thermal inactivation of invertase and lactase in dried amorphous matrices. Biotechnol. Prog. 13 (1997) 857-863
46. Schoen P., Chonn A., Cullis P.R., Wilschut J., and Scherrer P. Gene transfer mediated by fusion protein hemagglutinin reconstituted in cationic lipid vesicles. Gene Ther. 6 (1999) 823-832
47. Slade L., and Levine H. Non-equilibrium behavior of small carbohydrate-water systems. Pure Appl. Chem. 60 (1988) 1841-1864
48. Slade L., and Levine H. Water and the glass transition: dependance of the glass transition on the composition and chemical structure: special implications for flour functionality in cooky baking. J. Food Eng. 24 (1995) 431-509
49. Stegmann T., Morselt H.W., Booy F.P., van Breemen J.F., Scherphof G., and Wilschut J. Functional reconstitution of influenza virus envelopes. EMBO J. 6 (1987) 2651-2659
50. Stegmann T., Schoen P., Bron R., Wey J., Bartoldus I., Ortiz A., Nieva J.L., and Wilschut J. Evaluation of viral membrane fusion assays. Comparison of the octadecylrhodamine dequenching assay with the pyrene excimer assay. Biochemistry 32 (1993) 11330-11337
51. Sun W.Q., Leopold A.C., Crowe L.M., and Crowe J.H. Stability of dry liposomes in sugar glasses. Biophys. J. 70 (1996) 1769-1776
52. 2O. Arch. Biochem. Biophys. 81 (1959) 319-329
53. Vereyken I.J., Chupin V., Hoekstra F.A., Smeekens S.C., and de Kruijff B. The effect of fructan on membrane lipid organization and dynamics in the dry state. Biophys. J. 84 (2003) 3759-3766
54. Vereyken I.J., Chupin V., Islamov A., Kuklin A., Hincha D.K., and de Kruijff B. The effect of fructan on the phospholipid organization in the dry state. Biophys. J. 85 (2003) 3058-3065
55. Waelti E.R., and Gluck R. Delivery to cancer cells of antisense l-myc oligonucleotides incorporated in fusogenic, cationic-lipid-reconstituted influenza-virus envelopes (cationic virosomes). Int. J. Cancer 77 (1998) 728-733
56. Wang W. Instability, stabilization, and formulation of liquid protein pharmaceuticals. Int. J. Pharm. 185 (1999) 129-188
57. Yannarell D.A., Goldberg K.M., and Hjorth R.N. Stabilizing cold-adapted influenza virus vaccine under various storage conditions. J. Virol. Meth. 102 (2002) 15-25