Intradermal vaccination with influenza virus-like particles by using microneedles induces protection superior to that with intramuscular immunization

Journal of Virology

Volumn 84, Issue 15, 2010, Pages 7760-7769

  Quan, Fu Shi ^a   Kim, Yeu Chun ^b   Vunnava, Aswani ^a   Yoo, Dae Goon ^a   Song, Jae Min ^a   Prausnitz, Mark R ^b   Compans, Richard W ^a   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

DISACCHARIDE; HEMAGGLUTININ; IMMUNOGLOBULIN G2A; NEUTRALIZING ANTIBODY; TREHALOSE; VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; INFLUENZA VIRUS; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN STABILITY; VACCINATION; VIRUS LIKE AGENT;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; INJECTIONS, INTRADERMAL; INJECTIONS, INTRAMUSCULAR; LUNG; MICE; MICE, INBRED BALB C; NEUTRALIZATION TESTS; ORTHOMYXOVIRIDAE INFECTIONS; PLASMA CELLS; SURVIVAL ANALYSIS; VACCINES, VIROSOME;

MUS; ORTHOMYXOVIRIDAE;

EID: 77954521860     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01849-09     Document Type: Article

References (53)

1. Akbari, O., N. Panjwani, S. Garcia, R. Tascon, D. Lowrie, and B. Stockinger. 1999. DNA vaccination: transfection and activation of dendritic cells as key events for immunity. J. Exp. Med. 189:169-178.
2. Amorij, J. P., J. Meulenaar, W. L. Hinrichs, T. Stegmann, A. Huckriede, F. Coenen, and H. W. Frijlink. 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.
3. Anders, E. M., A. A. Scalzo, and D. O. White. 1985. Mitogenic activity of influenza virus and haemagglutinin. Vaccine 3:241-244.
4. Auewarakul, P., U. Kositanont, P. Sornsathapornkul, P. Tothong, R. Kanyok, and P. Thongcharoen. 2007. Antibody responses after dose-sparing intradermal influenza vaccination. Vaccine 25:659-663.
5. Barker, J. N., R. S. Mitra, C. E. Griffiths, V. M. Dixit, and B. J. Nickoloff. 1991. Keratinocytes as initiators of inflammation. Lancet 337:211-214.
6. Belshe, R. B., F. K. Newman, J. Cannon, C. Duane, J. Treanor, C. Van Hoecke, B. J. Howe, and G. Dubin. 2004. Serum antibody responses after intradermal vaccination against influenza. N. Engl. J. Med. 351:2286-2294.
7. Belshe, R. B., F. K. Newman, K. Wilkins, I. L. Graham, E. Babusis, M. Ewell, and S. E. Frey. 2007. Comparative immunogenicity of trivalent influenza vaccine administered by intradermal or intramuscular route in healthy adults. Vaccine 25:6755-6763.
8. Beran, J., A. Ambrozaitis, A. Laiskonis, N. Mickuviene, P. Bacart, Y. Calozet, E. Demanet, S. Heijmans, P. Van Belle, F. Weber, and C. Salamand. 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.
9. Bright, R. A., D. M. Carter, C. J. Crevar, F. R. Toapanta, J. D. Steckbeck, K. S. Cole, N. M. Kumar, P. Pushko, G. Smith, T. M. Tumpey, and T. M. Ross. 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.
10. Chen, D., R. L. Endres, C. A. Erickson, K. F. Weis, M. W. McGregor, Y. Kawaoka, and L. G. Payne. 2000. Epidermal immunization by a needle-free powder delivery technology: immunogenicity of influenza vaccine and protection in mice. Nat. Med. 6:1187-1190.
11. Chiu, S. S., J. S. Peiris, K. H. Chan, W. H. Wong, and Y. L. Lau. 2007. Immunogenicity and safety of intradermal influenza immunization at a reduced dose in healthy children. Pediatrics 119:1076-1082.
12. Dubois, B., C. Massacrier, and C. Caux. 2001. Selective attraction of naive and memory B cells by dendritic cells. J. Leukoc. Biol. 70:633-641.
13. Enioutina, E. Y., D. Visic, and R. A. Daynes. 2000. The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: alterations in the migratory properties of dendritic cells appears to be important for stimulating mucosal immunity. Vaccine 18:2753-2767.
14. Flacher, V., M. Bouschbacher, E. Verronese, C. Massacrier, V. Sisirak, O. Berthier-Vergnes, B. de Saint-Vis, C. Caux, C. Dezutter-Dambuyant, S. Lebecque, and J. Valladeau. 2006. Human Langerhans cells express a specific TLR profile and differentially respond to viruses and Gram-positive bacteria. J. Immunol. 177:7959-7967. (Pubitemid 44846312)
15. Galarza, J. M., T. Latham, and A. Cupo. 2005. Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol. 18:244-251.
16. Geeraedts, F., N. Goutagny, V. Hornung, M. Severa, A. de Haan, J. Pool, J. Wilschut, K. A. Fitzgerald, and A. Huckriede. 2008. Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling. PLoS Pathog. 4:e1000138.
17. Gill, H. S., and M. R. Prausnitz. 2007. Coated microneedles for transdermal delivery. J. Control Release 117:227-237.
18. Gill, H. S., J. Söderholm, M. R. Prausnitz, and M. Sällbeng. 2010. Cutaneous vaccination using microneedles coated with hepatitis C DNA vaccine. Gene Ther. 17:811-814.
19. Glenn, G. M., R. T. Kenney, L. R. Ellingsworth, S. A. Frech, S. A. Hammond, and J. P. Zoeteweij. 2003. Transcutaneous immunization and immunostimulant strategies: capitalizing on the immunocompetence of the skin. Expert Rev. Vaccines 2:253-267.
20. Haynes, J. R., L. Dokken, J. A. Wiley, A. G. Cawthon, J. Bigger, A. G. Harmsen, and C. Richardson. 2009. Influenza-pseudotyped Gag virus-like particle vaccines provide broad protection against highly pathogenic avian influenza challenge. Vaccine 27:530-541.
21. Heer, A. K., A. Shamshiev, A. Donda, S. Uematsu, S. Akira, M. Kopf, and B. J. Marsland. 2007. TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses. J. Immunol. 178:2182-2191.
22. Holland, D., R. Booy, F. De Looze, P. Eizenberg, J. McDonald, J. Karrasch, M. McKeirnan, H. Salem, G. Mills, J. Reid, F. Weber, and M. Saville. 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.
23. Hon, H., and J. Jacob. 2004. Tracking dendritic cells in vivo: insights into DC biology and function. Immunol. Res. 29:69-80.
24. Huang, J., R. J. Garmise, T. M. Crowder, K. Mar, C. R. Hwang, A. J. Hickey, J. A. Mikszta, and V. J. Sullivan. 2004. A novel dry powder influenza vaccine and intranasal delivery technology: induction of systemic and mucosal immune responses in rats. Vaccine 23:794-801.
25. Huber, V. C., J. M. Lynch, D. J. Bucher, J. Le, and D. W. Metzger. 2001. Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J. Immunol. 166:7381-7388.
26. Itano, A. A., S. J. McSorley, R. L. Reinhardt, B. D. Ehst, E. Ingulli, A. Y. Rudensky, and M. K. Jenkins. 2003. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 19:47-57.
27. Jayasekera, J. P., E. A. Moseman, and M. C. Carroll. 2007. Natural antibody and complement mediate neutralization of influenza virus in the absence of prior immunity. J. Virol. 81:3487-3494.
28. Kang, S. M., D. G. Yoo, A. S. Lipatov, J. M. Song, C. T. Davis, F. S. Quan, L. M. Chen, R. O. Donis, and R. W. Compans. 2009. Induction of long-term protective immune responses by influenza H5N1 virus-like particles. PLoS One 4:e4667.
29. Kenney, R. T., S. A. Frech, L. R. Muenz, C. P. Villar, and G. M. Glenn. 2004. Dose sparing with intradermal injection of influenza vaccine. N. Engl. J. Med. 351:2295-2301.
30. Khanlou, H., S. Sanchez, M. Babaie, C. Chien, G. Hamwi, J. C. Ricaurte, T. Stein, L. Bhatti, P. Denouden, and C. Farthing. 2006. The safety and efficacy of dose-sparing intradermal administration of influenza vaccine in human immunodeficiency virus-positive patients. Arch. Intern. Med. 166:1417.
31. Kim, Y. C., F. S. Quan, R. W. Compans, S. M. Kang, and M. R. Prausnitz. 2009. Formulation and coating of microneedles with inactivated influenza virus to improve vaccine stability and immunogenicity. J. Control Release 42:187-195.
32. Kobasa, D., A. Takada, K. Shinya, M. Hatta, P. Halfmann, S. Theriault, H. Suzuki, H. Nishimura, K. Mitamura, N. Sugaya, T. Usui, T. Murata, Y. Maeda, S. Watanabe, M. Suresh, T. Suzuki, Y. Suzuki, H. Feldmann, and Y. Kawaoka. 2004. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431:703-707.
33. Koutsonanos, D. G., M. del Pilar Martin, V. G. Zarnitsyn, S. P. Sullivan, R. W. Compans, M. R. Prausnitz, and I. Skountzou. 2009. Transdermal influenza immunization with vaccine-coated microneedle arrays. PLoS One 4:e4773.
34. Lanford, R. E., V. Luckow, R. C. Kennedy, G. R. Dreesman, L. Notvall, and M. D. Summers. 1989. Expression and characterization of hepatitis B virus surface antigen polypeptides in insect cells with a baculovirus expression system. J. Virol. 63:1549-1557. (Pubitemid 19085967)
35. Lin, L., A. J. Gerth, and S. L. Peng. 2004. CpG DNA redirects class-switching towards "Th1-like" Ig isotype production via TLR9 and MyD88. Eur. J. Immunol. 34:1483-1487.
36. Mahmood, K., R. A. Bright, N. Mytle, D. M. Carter, C. J. Crevar, J. E. Achenbach, P. M. Heaton, T. M. Tumpey, and T. M. Ross. 2008. H5N1 VLP vaccine induced protection in ferrets against lethal challenge with highly pathogenic H5N1 influenza viruses. Vaccine 26:5393-5399.
37. Marshall-Clarke, S., L. Tasker, O. Buchatska, J. Downes, J. Pennock, S. Wharton, P. Borrow, and D. Z. Wiseman. 2006. Influenza H2 haemagglutinin activates B cells via a MyD88-dependent pathway. Eur. J. Immunol. 36:95-106.
38. Mozdzanowska, K., J. Feng, M. Eid, D. Zharikova, and W. Gerhard. 2006. Enhancement of neutralizing activity of influenza virus-specific antibodies by serum components. Virology 352:418-426.
39. Nava, G. M., M. S. Attene-Ramos, J. K. Ang, and M. Escorcia. 2009. Origins of the new influenza A (H1N1) virus: time to take action. Euro Surveill. 14:pii19228.
40. Nemazee, D., A. Gavin, K. Hoebe, and B. Beutler. 2006. Immunology: Toll-like receptors and antibody responses. Nature 441:E4.
41. Pape, K. A., D. M. Catron, A. A. Itano, and M. K. Jenkins. 2007. The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity 26:491-502.
42. Perrone, L. A., A. Ahmad, V. Veguilla, X. Lu, G. Smith, J. M. Katz, P. Pushko, and T. M. Tumpey. 2009. Intranasal vaccination with 1918 influenza virus-like particles protects mice and ferrets from lethal 1918 and H5N1 influenza virus challenge. J. Virol. 83:5726-5734.
43. Pushko, P., T. M. Tumpey, F. Bu, J. Knell, R. Robinson, and G. Smith. 2005. Influenza virus-like particles comprised of the HA, NA, and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine 23:5751-5759.
44. Qi, H., J. G. Egen, A. Y. Huang, and R. N. Germain. 2006. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 312:1672-1676.
45. Quan, F. S., C. Huang, R. W. Compans, and S. M. Kang. 2007. Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus. J. Virol. 81:3514-3524.
46. Quan, F. S., Y. C. Kim, D. G. Yoo, R. W. Compans, M. R. Prausnitz, and S. M. Kang. 2009. Stabilization of influenza vaccine enhances protection by microneedle delivery in the mouse skin. PLoS One 4:e7152.
47. Quan, F. S., D. G. Yoo, J. M. Song, J. D. Clements, R. W. Compans, and S. M. Kang. 2009. Kinetics of immune responses to influenza virus-like particles and dose-dependence of protection with a single vaccination. J. Virol. 83:4489-4497.
48. Scalzo, A. A., and E. M. Anders. 1985. Influenza viruses as lymphocyte mitogens. II. Role of I-E molecules in B cell mitogenesis by influenza A viruses of the H2 and H6 subtypes. J. Immunol. 135:3524-3529.
49. Thompson, W. W., D. K. Shay, E. Weintraub, L. Brammer, C. B. Bridges, N. J. Cox, and K. Fukuda. 2004. Influenza-associated hospitalizations in the United States. JAMA 292:1333-1340.
50. Thompson, W. W., D. K. Shay, E. Weintraub, L. Brammer, N. Cox, L. J. Anderson, and K. Fukuda. 2003. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289:179-186.
51. Van Damme, P., F. Oosterhuis-Kafeja, M. Van der Wielen, Y. Almagor, O. Sharon, and Y. Levin. 2009. Safety and efficacy of a novel microneedle device for dose sparing intradermal influenza vaccination in healthy adults. Vaccine 27:454-459.
52. Wykes, M., A. Pombo, C. Jenkins, and G. G. MacPherson. 1998. Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 161:1313-1319. (Pubitemid 28380559)
53. Zhu, Q., V. G. Zarnitsyn, L. Ye, Z. Wen, Y. Gao, L. Pan, I. Skountzou, H. S. Gill, M. R. Prausnitz, C. Yang, and R. W. Compans. 2009. Immunization by vaccine-coated microneedle arrays protects against lethal influenza virus challenge. Proc. Natl. Acad. Sci. U. S. A. 106:7968-7973.