Stabilization of influenza vaccine enhances protection by microneedle delivery in the mouse skin

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Quan, Fu Shi ^a   Kim, Yeu Chun ^b   Yoo, Dae Goon ^a   Compans, Richard W ^a   Prausnitz, Mark R ^b   Kang, Sang Moo ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Georgia Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; IMMUNOGLOBULIN G; TREHALOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG ADMINISTRATION ROUTE; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG STABILITY; FEMALE; HEMAGGLUTINATION TEST; IMMUNE RESPONSE; IMMUNOASSAY; INFLUENZA; INTERMETHOD COMPARISON; MATERIAL COATING; MICRONEEDLE; MOUSE; NONHUMAN; VACCINATION; VIRUS NEUTRALIZATION; VIRUS REPLICATION; ANIMAL; BAGG ALBINO MOUSE; INSTRUMENTATION; INTRADERMAL DRUG ADMINISTRATION; INTRAMUSCULAR DRUG ADMINISTRATION; METABOLISM; METHODOLOGY; NEEDLE; SKIN;

ORTHOMYXOVIRIDAE;

ANIMALS; DRUG DELIVERY SYSTEMS; FEMALE; IMMUNOGLOBULIN G; INFLUENZA VACCINES; INJECTIONS, INTRADERMAL; INJECTIONS, INTRAMUSCULAR; MICE; MICE, INBRED BALB C; NEEDLES; SKIN; TREHALOSE; VACCINATION;

EID: 70349684566     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007152     Document Type: Article

References (57)

1. Belshe RB, Newman FK, Cannon J, Duane C, Treanor J, et al. (2004) Serum antibody responses after intradermal vaccination against influenza. N Engl J Med 351: 2286-2294.
2. Tumpey TM, Renshaw M, Clements JD, Katz JM (2001) Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J Virol 75: 5141-5150.
3. Compans RW, Klenk HD, Caliguiri LA, Choppin PW (1970) Influenza virus proteins. I. Analysis of polypeptides of the virion and identification of spike glycoproteins. Virology 42: 880-889.
4. Schulze IT (1970) The structure of influenza virus. I. The polypeptides of the virion. Virology 42: 890-904.
5. Rappuoli R (2007) Bridging the knowledge gaps in vaccine design. Nat Biotechnol 25: 1361-1366.
6. Glenn GM, Scharton-Kersten T, Alving CR (1999) Advances in vaccine delivery: transcutaneous immunisation. Expert Opin Investig Drugs 8: 797-805.
7. Glenn GM, Taylor DN, Li X, Frankel S, Montemarano A, et al. (2000) Transcutaneous immunization: a human vaccine delivery strategy using a patch. Nat Med 6: 1403-1406.
8. Chen D, Endres RL, Erickson CA, Weis KF, McGregor MW, et al. (2000) Epidermal immunization by a needle-free powder delivery technology: immunogenicity of influenza vaccine and protection in mice. Nat Med 6: 1187-1190.
9. Flacher V, Bouschbacher M, Verronese E, Massacrier C, Sisirak V, et al. (2006) Human Langerhans cells express a specific TLR profile and differentially respond to viruses and Gram-positive bacteria. J Immunol 177: 7959-7967.
10. Kenney RT, Frech SA, Muenz LR, Villar CP, Glenn GM (2004) Dose sparing with intradermal injection of influenza vaccine. N Engl J Med 351: 2295-2301.
11. Auewarakul P, Kositanont U, Sornsathapornkul P, Tothong P, Kanyok R, et al. (2007) Antibody responses after dose-sparing intradermal influenza vaccination. Vaccine 25: 659-663.
12. Khanlou H, Sanchez S, Babaie M, Chien C, Hamwi G, et al. (2006) The safety and efficacy of dose-sparing intradermal administration of influenza vaccine in human immunodeficiency virus-positive patients. Arch Intern Med 166: 1417.
13. Chiu SS, Peiris JS, Chan KH, Wong WH, Lau YL (2007) Immunogenicity and safety of intradermal influenza immunization at a reduced dose in healthy children. Pediatrics 119: 1076-1082.
14. Beran J, Ambrozaitis A, Laiskonis A, Mickuviene N, Bacart P, et al. (2009) Intradermal influenza vaccination of healthy adults using a new microinjection system: a 3-year randomised controlled safety and immunogenicity trial. BMC Med 7: 13.
15. Belshe RB, Newman FK, Wilkins K, Graham IL, Babusis E, et al. (2007) Comparative immunogenicity of trivalent influenza vaccine administered by intradermal or intramuscular route in healthy adults. Vaccine 25: 6755-6763.
16. Holland D, Booy R, De Looze F, Eizenberg P, McDonald J, et al. (2008) Intradermal influenza vaccine administered using a new microinjection system produces superior immunogenicity in elderly adults: a randomized controlled trial. J Infect Dis 198: 650-658.
17. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, et al. (2003) Mortality associated with influenza and respiratory syncytial virus in the United States. Jama 289: 179-186.
18. Sugimura T, Ito Y, Tananari Y, Ozaki Y, Maeno Y, et al. (2008) Improved antibody responses in infants less than 1 year old using intradermal influenza vaccination. Vaccine 26: 2700-2705.
19. Van Damme P, Oosterhuis-Kafeja F, Van der Wielen M, Almagor Y, Sharon O, et al. (2009) Safety and efficacy of a novel microneedle device for dose sparing intradermal influenza vaccination in healthy adults. Vaccine 27: 454-459.
20. Alarcon JB, Hartley AW, Harvey NG, Mikszta JA (2007) Preclinical evaluation of microneedle technology for intradermal delivery of influenza vaccines. Clin Vaccine Immunol 14: 375-381.
21. La Montagne JR, Fauci AS (2004) Intradermal influenza vaccination-can less be more? N Engl J Med 351: 2330-2332.
22. Matriano JA, Cormier M, Johnson J, Young WA, Buttery M, et al. (2002) Macroflux microprojection array patch technology: a new and efficient approach for intracutaneous immunization. Pharm Res 19: 63-70.
23. Gill HS, Prausnitz MR (2007a) Coated microneedles for transdermal delivery. J Control Release 117: 227-237.
24. Koutsonanos DG, del Pilar Martin M, Zarnitsyn VG, Sullivan SP, Compans RW, et al. (2009) Transdermal influenza immunization with vaccine-coated microneedle arrays. PLoS ONE 4: e4773.
25. Zhu Q, Zarnitsyn VG, Ye L, Wen Z, Gao Y, et al. (2009) Immunization by vaccine-coated microneedle arrays protects against lethal influenza virus challenge. Proc Natl Acad Sci U S A.
26. Amorij JP, Meulenaar J, Hinrichs WL, Stegmann T, Huckriede A, et al. (2007) Rational design of an influenza subunit vaccine powder with sugar glass technology: preventing conformational changes of haemagglutinin during freezing and freeze-drying. Vaccine 25: 6447-6457.
27. Markine-Goriaynoff D, van der Logt JT, Truyens C, Nguyen TD, Heessen FW, et al. (2000) IFN-gamma-independent IgG2a production in mice infected with viruses and parasites. Int Immunol 12: 223-230.
28. Bright RA, Carter DM, Crevar CJ, Toapanta FR, Steckbeck JD, et al. (2008) Cross-Clade Protective Immune Responses to Influenza Viruses with H5N1 HA and NA Elicited by an Influenza Virus-Like Particle. PLoS ONE 3: e1501.
29. Bright RA, Carter DM, Daniluk S, Toapanta FR, Ahmad A, et al. (2007) Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 25: 3871-3878.
30. Quan FS, Yoo DG, Song JM, Clements JD, Compans RW, et al. (2009) Kinetics of immune responses to influenza virus-like particles and dose-dependence of protection with a single vaccination. J Virol 83: 4489-4497.
31. Tumpey TM, Garcia-Sastre A, Taubenberger JK, Palese P, Swayne DE, et al. (2005) Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J Virol 79: 14933-14944.
32. Van Reeth K, Van Gucht S, Pensaert M (2002) Correlations between lung proinflammatory cytokine levels, virus replication, and disease after swine influenza virus challenge of vaccination-immune pigs. Viral Immunol 15: 583-594.
33. Stevens TL, Bossie A, Sanders VM, Fernandez-Botran R, Coffman RL, et al. (1988) Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334: 255-258.
34. Coutelier JP, van der Logt JT, Heessen FW, Warnier G, Van Snick J (1987) IgG2a restriction of murine antibodies elicited by viral infections. J Exp Med 165: 64-69.
35. Fazekas G, Rosenwirth B, Dukor P, Gergely J, Rajnavolgyi E (1994) IgG isotype distribution of local and systemic immune responses induced by influenza virus infection. Eur J Immunol 24: 3063-3067.
36. Huber VC, Lynch JM, Bucher DJ, Le J, Metzger DW (2001) Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J Immunol 166: 7381-7388.
37. Neuberger MS, Rajewsky K (1981) Activation of mouse complement by monoclonal mouse antibodies. Eur J Immunol 11: 1012-1016.
38. Heusser CH, Anderson CL, Grey HM (1977) Receptors for IgG: subclass specificity of receptors on different mouse cell types and the definition of two distinct receptors on a macrophage cell line. J Exp Med 145: 1316-1327.
39. Gessner JE, Heiken H, Tamm A, Schmidt RE (1998) The IgG Fc receptor family. Ann Hematol 76: 231-248.
40. Mozdzanowska K, Feng J, Eid M, Zharikova D, Gerhard W (2006) Enhancement of neutralizing activity of influenza virus-specific antibodies by serum components. Virology 352: 418-426.
41. Jayasekera JP, Moseman EA, Carroll MC (2007) Natural antibody and complement mediate neutralization of influenza virus in the absence of prior immunity. J Virol 81: 3487-3494.
42. Geeraedts F, Goutagny N, Hornung V, Severa M, de Haan A, et al. (2008) Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling. PLoS Pathog 4: e1000138.
43. Mitsui H, Watanabe T, Saeki H, Mori K, Fujita H, et al. (2004) Differential expression and function of Toll-like receptors in Langerhans cells: comparison with splenic dendritic cells. J Invest Dermatol 122: 95-102.
44. Pulendran B (2004) Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol Rev 199: 227-250.
45. Geeraedts F, Bungener L, Pool J, ter Veer W, Wilschut J, et al. (2008b) Whole inactivated virus influenza vaccine is superior to subunit vaccine in inducing immune responses and secretion of proinflammatory cytokines by DCs. Influenza Other Respi Viruses 2: 41-51.
46. De Becker G, Sornasse T, Nabavi N, Bazin H, Tielemans F, et al. (1994) Immunoglobulin isotype regulation by antigen-presenting cells in vivo. Eur J Immunol 24: 1523-1528.
47. Nicolas JF, Guy B (2008) Intradermal, epidermal and transcutaneous vaccination: from immunology to clinical practice. Expert Rev Vaccines 7: 1201-1214.
48. Belyakov IM, Hammond SA, Ahlers JD, Glenn GM, Berzofsky JA (2004) Transcutaneous immunization induces mucosal CTLs and protective immunity by migration of primed skin dendritic cells. J Clin Invest 113: 998-1007.
49. Guebre-Xabier M, Hammond SA, Epperson DE, Yu J, Ellingsworth L, et al. (2003) Immunostimulant patch containing heat-labile enterotoxin from Escherichia coli enhances immune responses to injected influenza virus vaccine through activation of skin dendritic cells. J Virol 77: 5218-5225.
50. Hon H, Jacob J (2004) Tracking dendritic cells in vivo: insights into DC biology and function. Immunol Res 29: 69-80.
51. Novak M, Moldoveanu Z, Schafer DP, Mestecky J, Compans RW (1993) Murine model for evaluation of protective immunity to influenza virus. Vaccine 11: 55-60.
52. Sha Z, Compans RW (2000) Induction of CD4(+) T-cell-independent immunoglobulin responses by inactivated influenza virus. J Virol 74: 4999-5005.
53. Quan FS, Compans RW, Nguyen HH, Kang SM (2008) Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J Virol 82: 1350-1359.
54. Quan FS, Huang C, Compans RW, Kang SM (2007) Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus. J Virol 81: 3514-3524.
55. Gill HS, Prausnitz MR (2007b) Coating formulations for microneedles. Pharm Res 24: 1369-1380.
56. Deng Y, Yewdell JW, Eisenlohr LC, Bennink JR (1997) MHC affinity, peptide liberation, T cell repertoire, and immunodominance all contribute to the paucity of MHC class I-restricted peptides recognized by antiviral CTL. J Immunol 158: 1507-1515.
57. Oran AE, Robinson HL (2003) DNA vaccines, combining form of antigen and method of delivery to raise a spectrum of IFN-gamma and IL-4-producing CD4+ and CD8+ T cells. J Immunol 171: 1999-2005.