Pulmonary delivery of an inulin-stabilized influenza subunit vaccine prepared by spray-freeze drying induces systemic, mucosal humoral as well as cell-mediated immune responses in BALB/c mice

Vaccine

Volumn 25, Issue 52, 2007, Pages 8707-8717

  Amorij, J P ^a   Saluja, V ^a   Petersen, A H ^b   Hinrichs, W L J ^a   Huckriede, A ^b   Frijlink, H W ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Dry powder formulation; Influenza vaccine; Respiratory tract

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INFLUENZA VACCINE; INTERLEUKIN 4; INULIN; OLIGOSACCHARIDE; STABILIZING AGENT; SUBUNIT VACCINE;

AEROSOL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BAGG ALBINO MOUSE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG DELIVERY SYSTEM; FEMALE; FREEZE DRYING; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; INFLUENZA; INFLUENZA VACCINATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; POWDER; PRIORITY JOURNAL; VACCINE PRODUCTION;

ADMINISTRATION, INHALATION; AEROSOLS; ANIMALS; ANTIBODIES, VIRAL; BRONCHOALVEOLAR LAVAGE FLUID; CRYOPROTECTIVE AGENTS; FEMALE; FREEZE DRYING; HEMAGGLUTINATION INHIBITION TESTS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INFLUENZA VACCINES; INTERFERON TYPE II; INTERLEUKIN-4; INULIN; LYMPHOCYTES; MICE; MICE, INBRED BALB C; NASAL LAVAGE FLUID; SPLEEN; VACCINES, SUBUNIT;

EID: 36749056289     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2007.10.035     Document Type: Article

References (66)

1. Couch R.B., and Kasel J.A. Immunity to influenza in man. Annu Rev Microbiol 37 (1983) 529-549
2. Cox R.J., Brokstad K.A., and Ogra P. Influenza virus: immunity and vaccination strategies. Comparison of the immune response to inactivated and live, attenuated influenza vaccines. Scand J Immunol 59 1 (2004) 1-15
3. Wong S.S., and Yuen K.Y. Avian influenza virus infections in humans. Chest 129 1 (2006) 156-168
4. Liew F.Y., Russell S.M., Appleyard G., Brand C.M., and Beale J. Cross-protection in mice infected with influenza A virus by the respiratory route is correlated with local IgA antibody rather than serum antibody or cytotoxic T cell reactivity. Eur J Immunol 14 4 (1984) 350-356
5. Tumpey T.M., Renshaw M., Clements J.D., and Katz J.M. Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J Virol 75 11 (2001) 5141-5150
6. Asahi-Ozaki Y., Yoshikawa T., Iwakura Y., Suzuki Y., Tamura S., Kurata T., et al. Secretory IgA antibodies provide cross-protection against infection with different strains of influenza B virus. J Med Virol 74 2 (2004) 328-335
7. Tamura S., and Kurata T. Defense mechanisms against influenza virus infection in the respiratory tract mucosa. Jpn J Infect Dis 57 6 (2004) 236-247
8. Sweet C., and Smith H. Pathogenicity of influenza virus. Microbiol Rev 44 2 (1980) 303-330
9. Potter C.W., and Jennings R. Intranasal immunization with inactivated influenza vaccine. Pharm Sci Technol Today 2 10 (1999) 402-408
10. Cassetti M.C., Katz J.M., and Wood J. Report of a consultation on role of immunological assays to evaluate efficacy of influenza vaccines. Initiative for Vaccine Research and Global Influenza Programme, World Health Organization, Geneva, Switzerland, 25 January 2005. Vaccine 24 5 (2006) 541-543
11. Chen D., Endres R.L., Erickson C.A., Weis K.F., McGregor M.W., Kawaoka Y., et al. Epidermal immunization by a needle-free powder delivery technology: immunogenicity of influenza vaccine and protection in mice. Nat Med 6 10 (2000) 1187-1190
12. Joseph A., Itskovitz-Cooper N., Samira S., Flasterstein O., Eliyahu H., Simberg D., et al. A new intranasal influenza vaccine based on a novel polycationic lipid-ceramide carbamoyl-spermine (CCS) I. Immunogenicity and efficacy studies in mice. Vaccine 24 18 (2006) 3990-4006
13. Read R.C., Naylor S.C., Potter C.W., Bond J., Jabbal-Gill I., Fisher A., et al. Effective nasal influenza vaccine delivery using chitosan. Vaccine 23 35 (2005) 4367-4374
14. Haan L., Verweij W.R., Holtrop M., Brands R., van Scharrenburg G.J., Palache A.M., et al. 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 20-22 (2001) 2898-2907
15. Holmgren J., and Czerkinsky C. Mucosal immunity and vaccines. Nat Med 11 Suppl. 4 (2005) S45-S53
16. McCluskie M.J., Weeratna R.D., Clements J.D., and Davis H.L. Mucosal immunization of mice using CpG DNA and/or mutants of the heat-labile enterotoxin of Escherichia coli as adjuvants. Vaccine 19 27 (2001) 3759-3768
17. Stephenson I., Zambon M.C., Rudin A., Colegate A., Podda A., Bugarini R., et al. Phase I evaluation of intranasal trivalent inactivated influenza vaccine with nontoxigenic Escherichia coli enterotoxin and novel biovector as mucosal adjuvants, using adult volunteers. J Virol 80 10 (2006) 4962-4970
18. Davis S.S., and Illum L. Absorption enhancers for nasal drug delivery. Clin Pharmacokinet 42 13 (2003) 1107-1128
19. Amidi M., Romeijn S.G., Verhoef J.C., Junginger H.E., Bungener L., Huckriede A., et al. N-Trimethyl chitosan (TMC) nanoparticles loaded with influenza subunit antigen for intranasal vaccination: biological properties and immunogenicity in a mouse model. Vaccine (2006)
20. Boyce T.G., Hsu H.H., Sannella E.C., Coleman-Dockery S.D., Baylis E., Zhu Y., et al. Safety and immunogenicity of adjuvanted and unadjuvanted subunit influenza vaccines administered intranasally to healthy adults. Vaccine 19 2-3 (2000) 217-226
21. Belshe R.B., Gruber W.C., Mendelman P.M., Cho I., Reisinger K., Block S.L., et al. Efficacy of vaccination with live attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine against a variant (A/Sydney) not contained in the vaccine. J Pediatr 136 2 (2000) 168-175
22. Fujihashi K., Koga T., van Ginkel F.W., Hagiwara Y., and McGhee J.R. A dilemma for mucosal vaccination: efficacy versus toxicity using enterotoxin-based adjuvants. Vaccine 20 19-20 (2002) 2431-2438
23. McCarthy M.W., and Kockler D.R. Trivalent intranasal influenza vaccine, live. Ann Pharmacother 38 12 (2004) 2086-2093
24. Giudice E.L., and Campbell J.D. Needle-free vaccine delivery. Adv Drug Deliv Rev 58 1 (2006) 68-89
25. Dean H.J. Alternative routes of influenza vaccine delivery. Expert Opin Drug Deliv 3 5 (2006) 557-561
26. Amorij J.-P., Meulenaar J., Hinrichs W.L., Stegmann T., Huckriede A., Coenen F., et al. Rational design of an influenza subunit vaccine powder with sugar glass technology: preventing conformational changes of haemagglutinin during freezing and freeze-drying. Vaccine 25 35 (2007) 6447-6457
27. Maa Y.F., Ameri M., Shu C., Payne L.G., and Chen D. Influenza vaccine powder formulation development: spray-freeze-drying and stability evaluation. J Pharm Sci 93 7 (2004) 1912-1923
28. Huang J., Garmise R.J., Crowder T.M., Mar K., Hwang C.R., Hickey A.J., et al. A novel dry powder influenza vaccine and intranasal delivery technology: induction of systemic and mucosal immune responses in rats. Vaccine 23 6 (2004) 794-801
29. Shoyele S.A., and Slowey A. Prospects of formulating proteins/peptides as aerosols for pulmonary drug delivery. Int J Pharm 314 1 (2006) 1-8
30. Sullivan V.J., Mikszta J.A., Laurent P., Huang J., and Ford B. Noninvasive delivery technologies: respiratory delivery of vaccines. Expert Opin Drug Deliv 3 1 (2006) 87-95
31. Lambrecht B.N., Prins J.B., and Hoogsteden H.C. Lung dendritic cells and host immunity to infection. Eur Respir J 18 4 (2001) 692-704
32. von Garnier C., Filgueira L., Wikstrom M., Smith M., Thomas J.A., Strickland D.H., et al. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J Immunol 175 3 (2005) 1609-1618
33. Holt P.G. Pulmonary dendritic cells in local immunity to inert and pathogenic antigens in the respiratory tract. Proc Am Thorac Soc 2 2 (2005) 116-120
34. Holmgren J., Czerkinsky C., Lycke N., and Svennerholm A.M. Mucosal immunity: implications for vaccine development. Immunobiology 184 2-3 (1992) 157-179
35. Immunochemical methods (2.7.1). In: European Pharmacopoeia, 5th ed. Strasbourg, Council of Europe, 2004: 187.
36. Beck S.E., Laube B.L., Adams R.J., Chesnut K., Flotte T.R., and Guggino W.B. Deposition of aerosolized AAV vectors in the lungs of rhesus macaques. Ped Pulm Suppl. (1999) 228-229
37. Century T.J. A new intrapulmonary aerosol delivery device. Respir. Drug Deliv. VII (2000) 1-4
38. Loebenberg R, Finlay WH, Roa WH, Ely L, inventors; Effervescent powders for inhalation patent 490331. 2007.
39. Preparations for inhalation: aerodynamic assessment of fine particles (2.9.18). In: European Pharmacopoeia, 5th ed. Strasbourg, Council of Europe, 2004: 244-251.
40. Eriksson H.J., Verweij W.R., Poelstra K., Hinrichs W.L., de Jong G.J., Somsen G.W., et al. Investigations into the stabilisation of drugs by sugar glasses: II. Delivery of an inulin-stabilised alkaline phosphatase in the intestinal lumen via the oral route. Int J Pharm 257 1-2 (2003) 273-281
41. Bivas-Benita M., Zwier R., Junginger H.E., and Borchard G. Non-invasive pulmonary aerosol delivery in mice by the endotracheal route. Eur J Pharm Biopharm 61 3 (2005) 214-218
42. 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 10 (2005) 1232-1241
43. McCutcheon M., Wehner N., Wensky A., Kushner M., Doan S., Hsiao L., et al. A sensitive ELISPOT assay to detect low-frequency human T lymphocytes. J Immunol Methods 210 2 (1997) 149-166
44. Concessio N.M., and Hickey A.J. Descriptors of irregular particle morphology and powder properties. Adv Drug Deliv Rev 26 1 (1997) 29-40
45. Edwards D.A., Hanes J., Caponetti G., Hrkach J., Ben-Jebria A., Eskew M.L., et al. Large porous particles for pulmonary drug delivery. Science 276 5320 (1997) 1868-1871
46. Irngartinger M., Camuglia V., Damm M., Goede J., and Frijlink H.W. Pulmonary delivery of therapeutic peptides via dry powder inhalation: effects of micronisation and manufacturing. Eur J Pharm Biopharm 58 1 (2004) 7-14
47. Maa Y.F., Nguyen P.A., Sweeney T., Shire S.J., and Hsu C.C. Protein inhalation powders: spray drying vs. spray freeze drying. Pharm Res 16 2 (1999) 249-254
48. Zijlstra G.S., Hinrichs W.L., de Boer A.H., and Frijlink H.W. The role of particle engineering in relation to formulation and de-agglomeration principle in the development of a dry powder formulation for inhalation of cetrorelix. Eur J Pharm Sci 23 2 (2004) 139-149
49. Bot A., Bot S., and Bona C.A. Protective role of gamma interferon during the recall response to influenza virus. J Virol 72 8 (1998) 6637-6645
50. Swain S.L., Agrewala J.N., Brown D.M., Jelley-Gibbs D.M., Golech S., Huston G., et al. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza. Immunol Rev 211 (2006) 8-22
51. Committee for Proprietary Medicinal Products (CPMP). Note for Guidance on Harmonisation of Requirements for Influenza Vaccines (CPMP/BWP/214/96).
52. Clements M.L., Betts R.F., Tierney E.L., and Murphy B.R. Serum and nasal wash antibodies associated with resistance to experimental challenge with influenza A wild-type virus. J Clin Microbiol 24 1 (1986) 157-160
53. Renegar K.B., and Small Jr. P.A. Passive transfer of local immunity to influenza virus infection by IgA antibody. J Immunol 146 6 (1991) 1972-1978
54. Mbawuike I.N., Pacheco S., Acuna C.L., Switzer K.C., Zhang Y., and Harriman G.R. Mucosal immunity to influenza without IgA: an IgA knockout mouse model. J Immunol 162 5 (1999) 2530-2537
55. Zhang Y., Pacheco S., Acuna C.L., Switzer K.C., Wang Y., Gilmore X., et al. Immunoglobulin A-deficient mice exhibit altered T helper 1-type immune responses but retain mucosal immunity to influenza virus. Immunology 105 3 (2002) 286-294
56. McDermott M.R., and Bienenstock J. Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. J Immunol 122 5 (1979) 1892-1898
57. Neutra M.R., Pringault E., and Kraehenbuhl J.P. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 14 (1996) 275-300
58. Smith D.J., Bot S., Dellamary L., and Bot A. Evaluation of novel aerosol formulations designed for mucosal vaccination against influenza virus. Vaccine 21 21-22 (2003) 2805-2812
59. Reynolds H.Y. Respiratory host defenses-surface immunity. Immunobiology 191 4-5 (1994) 402-412
60. Geiser M. Morphological aspects of particle uptake by lung phagocytes. Microsc Res Tech 57 6 (2002) 512-522
61. Brain J.D. Lung macrophages: how many kinds are there? What do they do?. Am Rev Respir Dis 137 3 (1988) 507-509
62. Ferro T.J., Kern J.A., Elias J.A., Kamoun M., Daniele R.P., and Rossman M.D. Alveolar macrophages, blood monocytes, and density-fractionated alveolar macrophages differ in their ability to promote lymphocyte proliferation to mitogen and antigen. Am Rev Respir Dis 135 3 (1987) 682-687
63. Gong J.L., McCarthy K.M., Rogers R.A., and Schneeberger E.E. Interstitial lung macrophages interact with dendritic cells to present antigenic peptides derived from particulate antigens to T cells. Immunology 81 3 (1994) 343-351
64. de Haan A., Groen G., Prop J., van Rooijen N., and Wilschut J. Mucosal immunoadjuvant activity of liposomes: role of alveolar macrophages. Immunology 89 4 (1996) 488-493
65. Thepen T., Hoeben K., Breve J., and Kraal G. Alveolar macrophages down-regulate local pulmonary immune responses against intratracheally administered T-cell-dependent, but not T-cell-independent antigens. Immunology 76 1 (1992) 60-64
66. Hinrichs W.L., Prinsen M.G., and Frijlink H.W. Inulin glasses for the stabilization of therapeutic proteins. Int J Pharm 215 1-2 (2001) 163-174