Mucosal immunization with recombinant influenza hemagglutinin protein and poly gamma-glutamate/chitosan nanoparticles induces protection against highly pathogenic influenza A virus

Veterinary Microbiology

Volumn 160, Issue 3-4, 2012, Pages 277-289

  Moon, Ho Jin ^a   Lee, Jong Soo ^a   Talactac, Melbourne R ^a   Chowdhury, Mohammed Y E ^a   Kim, Jae Hoon ^a   Park, Min Eun ^a   Choi, Young Ki ^b   Sung, Moon Hee ^c,d   Kim, Chul Joong ^a  

^a Chungnam National University   (South Korea)

^b Chungbuk National University College of Medicine   (South Korea)

^c Kookmin University   (South Korea)

^d Bioleaders Corporation   (South Korea)

Author keywords

Cytotoxic T lymphocyte (CTL) response; Highly pathogenic avian influenza (HPAI) virus (H5N1); Mucosal immunity; Neutralizing antibody; Poly glutamate chitosan nanoparticles (PC NPs); Subunit vaccine

Indexed keywords

CHITOSAN; GLUTAMIC ACID DERIVATIVE; HEMAGGLUTININ; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INFLUENZA VACCINE; NANOPARTICLE; NEUTRALIZING ANTIBODY; POLY GAMMA GLUTAMATE; RECOMBINANT HEMAGGLUTININ; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; IMMUNIZATION; INFLUENZA VIRUS A; INFLUENZA VIRUS A H5N1; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PROKARYOTE; PROTEIN EXPRESSION; RESPIRATORY SYSTEM;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES, VIRAL; CHITOSAN; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNITY, CELLULAR; IMMUNITY, MUCOSAL; IMMUNIZATION; IMMUNOGLOBULIN ISOTYPES; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; NANOPARTICLES; ORTHOMYXOVIRIDAE INFECTIONS; POLYGLUTAMIC ACID; VACCINES, SYNTHETIC;

AVIAN INFLUENZA VIRUS; INFLUENZA A VIRUS; MUS; ORTHOMYXOVIRIDAE; PROKARYOTA;

EID: 84869080311     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2012.05.035     Document Type: Article

References (44)

1. Akagi T., Higashi M., Kaneko T., Kida T., Akashi M. In vitro enzymatic degradation of nanoparticles prepared from hydrophobically-modified poly (γ-glutamic acid). Macromol. Biosci. 2005, 5(7):598-602.
2. Akagi T., Kaneko T., Kida T., Akashi M. Multifunctional conjugation of proteins on/into bio-nanoparticles prepared by amphiphilic poly (γ-glutamic acid). J. Biomater. Sci. Polym. Ed. 2006, 17(8):875-892.
3. Andreakos E., Williams R.O., Wales J., Foxwell B.M., Feldmann M. Activation of NF-kappaB by the intracellular expression of NF-kappaB-inducing kinase acts as a powerful vaccine adjuvant. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:14459-14464.
4. Benne C.A., Harmsen M., De Jong J.C., Kraaijeveld C.A. Neutralization enzyme immunoassay for influenza virus. J. Clin. Microbiol. 1994, 32:987-990.
5. Brazolot Millan C.L., Weeratna R., Krieg A.M., Siegrist C.A., Davis H.L. CpG DNA can induce strong Th1 humoral and cell-mediated immune responses against hepatitis B surface antigen in young mice. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:15553-15558.
6. Cao W., Chen Y., Alkan S., Subramaniam A., Long F., Liu H., Diao R., Delohery T., McCormick J., Chen R., Ni D., Wright P.S., Zhang X., Busch S., Zilberstein A. Human T helper (Th) cell lineage commitment is not directly linked to the secretion of IFN-gamma or IL-4: characterization of Th cells isolated by FACS based on IFN-gamma and IL-4 secretion. Eur. J. Immunol. 2005, 35(9):2709-2717.
7. Fan S., Gao Y., Shinya K., Li C.K., Li Y., Shi J., Jiang Y., Suo Y., Tong T., Zhong G., Song J., Zhang Y., Tian G., Guan Y., Xu X.N., Bu Z., Kawaoka Y., Chen H. Immunogenicity and protective efficacy of a live attenuated H5N1 vaccine in nonhuman primates. PLoS Pathog. 2009, 5(5):e1000409.
8. Gluck R., Mischler R., Durrer P., Furer E., Lang A.B., Herzog C., Cryz S.J. Safety and immunogenicity of intranasally administered inactivated trivalent virosome-formulated influenza vaccine containing Escherichia coli heat-labile toxin as a mucosal adjuvant. J. Infect. Dis. 2000, 181:1129-1132.
9. Greenbaum E., Furst A., Kiderman A., Stewart B., Levy R., Schlesinger M., Morag A., Zakay-Rones Z. Serum and mucosal immunologic responses in children following the administration of a new inactivated intranasal anti-influenza vaccine. J. Med. Virol. 2001, 65:178-184.
10. Jindrich C., Martin M., Hans W.D. The threat of avian influenza A(H5N1). Part IV: development of vaccines. Med. Microbiol. Immun. 2007, 196:213-225.
11. Kim T.W., Lee T.Y., Bae H.C., Hahm J.H., Kim Y.H., Park C., Kang T.H., Kim C.J., Sung M.H., Poo H. Oral administration of high molecular mass poly-gamma-glutamate induces NK cell-mediated antitumor immunity. J. Immunol. 2007, 179:775-780.
12. Korteweg C., Gu J. Pandemic influenza A (H1N1) virus infection and avian influenza A (H5N1) virus infection: a comparative analysis. Biochem. Cell Biol. 2010, 88(4):575-587.
13. Khurana S., Verma S., Verma N., Crevar C.J., Carter D.M., Manischewitz J., King L.R., Ross T.M., Golding H. Properly folded bacterially expressed H1N1 hemagglutinin globular head and ectodomain vaccines protect ferrets against H1N1 pandemic influenza virus. PLoS ONE 2010, 5(7):e11548.
14. Labeur M.S., Roters B., Pers B., Mehling A., Luger T.A., Schwarz T., Grabbe S. Generation of tumor immunity by bone marrow-derived dendritic cells correlates with dendritic cell maturation stage. J. Immunol. 1999, 162:168-175.
15. Lee T.Y., Kim Y.H., Yoon S.W., Choi J.C., Yang J.M., Kim C.J., Schiller J.T., Sung M.H., Poo H. Oral administration of poly-gamma-glutamate induces TLR4- and dendritic cell-dependent antitumor effect. Cancer Immunol. Immunother. 2009, 58(11):1781-1794.
16. Lee Y.J., Choi Y.K., Kim Y.J., Song M.S., Jeong O.M., Lee E.K., Jeon W.J., Jeong W., Joh S.J., Choi K.S., Her M., Kim M.C., Kim A., Kim M.J., Lee E.H., Oh T.G., Moon H.J., Yoo D.W., Kim J.H., Sung M.H., Poo H., Kwon J.H., Kim C.J. Highly pathogenic avian influenza virus (H5N1) in domestic poultry and relationship with migratory birds, South Korea. Emerg. Infect. Dis. 2008, 14(3):487-490.
17. Liew F.Y., Russell S.M., Appleyard G., Brand C.M., Beale J. Crossprotection 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. 1984, 14(4):350-356.
18. Lin L., Gerth A.J., Peng S.L. CpG DNA redirects class-switching towards "Th1-like" Ig isotype production via TLR9 and MyD88. Eur. J. Immunol. 2004, 34:1483-1487.
19. Lin Y.H., Chung C.K., Chen C.T., Liang H.F., Chen S.C., Sung H.W. Preparation of nanoparticles composed of chitosan/poly-γ-glutamic acid and evaluation of their permeability through Caco-2 cells. Biomacromolecules 2005, 6:1104-1112.
20. Lin Y.H., Mi F.L., Chen C.T., Chang W.C., Peng S.F., Liang H.F., Sung H.W. Preparation and characterization of nanoparticles shelled with chitosan for oral insulin delivery. Biomacromolecules 2007, 8(1):146-152.
21. Lu X., Tumpey T.M., Morken T., Zaki S.R., Cox N.J., Katz J.M. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J. Virol. 1999, 73(7):5903-5911.
22. Matsuoka Y., Lamirande E.W., Subbarao K. The mouse model for influenza. Curr. Protoc. Microbiol 2009, 13. pp. 15G.3.1-15G.3.30.
23. Mizuno D., Ide-Kurihara M., Ichinomiya T., Kubo I., Kido H. Modified pulmonary surfactant is a potent adjuvant that stimulates the mucosal IgA production in response to the influenza virus antigen. J. Immunol. 2006, 176(2):1122-1130.
24. Moschos S.A., Bramwell V.W., Somavarapu S., Alpar H.O. Adjuvant synergy: the effects of nasal coadministration of adjuvants. Immunol. Cell Biol. 2004, 82:628-637.
25. Mountford A.P., Fisher A., Wilson R.A. The profile of IgG1 and IgG2a antibody responses in mice exposed to Schistosoma mansoni. Parasite Immunol. 1994, 16(10):521-527.
26. Mutsch M., Zhou W., Rhodes P., Bopp M., Chen R.T., Linder T., Spyr C., Steffen R. Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. N. Engl. J. Med. 2004, 350(9):896-903.
27. Okamoto S., Kawabata S., Fujitaka H., Uehira T., Okuno Y., Hamada S. Vaccination with formalin-inactivated influenza vaccine protects mice against lethal influenza Streptococcus pyogenes superinfection. Vaccine 2004, 22(21-22):2887-2893.
28. Okamoto S., Yoshii H., Akagi T., Akashi M., Ishikawa T., Okuno Y., Takahashi M., Yamanishi K., Mori Y. Influenza hemagglutinin vaccine with poly (γ-glutamic acid) nanoparticles enhances the protection against influenza virus infection through both humoral and cell-mediated immunity. Vaccine 2007, 25:8270-8278.
29. Okamoto S., Matsuura M., Akagi T., Akashi M., Tanimoto T., Ishikawa T., Takahashi M., Yamanishi K., Mori Y. Poly (γ-glutamic acid) nano-particles combined with mucosal influenza virus hemagglutinin vaccine protects against influenza virus infection in mice. Vaccine 2009, 27:5896-5905.
30. Poo H., Park C., Kwak M.S., Choi D.Y., Hong S.P., Lee I.H., Lim Y.T., Choi Y.K., Bae S.R., Uyama H., Kim C.J., Sung M.H. New biological functions and applications of high-molecular-mass poly-γ-glutamic acid. Chem. Biodivers. 2010, 7:1555-1562.
31. Quan F.S., Compans R.W., Nguyen H., Kang S.M. Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J. Virol. 2008, 82:1350-1359.
32. Reed L.J., Muench H. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 1938, 27:493-497.
33. Sonaje K., Lin Y.H., Juang J.H., Wey S.P., Chen C.T., Sung H.W. In vivo evaluation of safety and efficacy of self-assembled nanoparticles for oral insulin delivery. Biomaterials 2009, 30(12):2329-2339.
34. Song M.S., Oh T.K., Pascua P.N., Moon H.J., Lee J.H., Baek Y.H., Woo K.J., Yoon Y., Sung M.H., Poo H., Kim C.J., Choi Y.K. Investigation of the biological indicator for vaccine efficacy against highly pathogenic avian influenza (HPAI) H5N1 virus challenge in mice and ferrets. Vaccine 2009, 27:3145-3152.
35. Taguchi F., Hashimoto O., Matsuzaki T., Lee S.M. A new neutralization method for influenza virus in cell culture. Kitasato Arch. Exp. Med. 1992, 65:181-186.
36. Tamura S., Yamanaka A., Shimohara M., Tomita T., Komase K., Tsuda Y., Suzuki Y., Nagamine T., Kawahara K., Danbara H., Aizawa C., Oya A., Kurata T. Synergistic action of cholera toxin B subunit (and E. coli heat-labile toxin B subunit) and a trace amount of cholera whole toxin as an adjuvant for nasal influenza vaccine. Vaccine 1994, 12:419-426.
37. Thanou M., Verhoef J.C., Junginger H.E. Chitosan and its derivatives as intestinal absorption enhancers. Adv. Drug Deliv. Rev. 2001, 50(Suppl. 1):S91-S101.
38. Uto T., Wang X., Sato K., Haraguchi M., Akagi T., Akashi M., Baba M. Targeting of antigen to dendritic cells with poly (γ-glutamic acid) nanoparticles induces antigen-specific humoral and cellular immunity. J. Immunol. 2007, 178(5):2979-2986.
39. van Ginkel F.W., Jackson R.J., Yuki Y., McGhee J.R. Cutting edge: the mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J. Immunol. 2000, 165:4778-4782.
40. Vila A., Sanchez A., Janes K., Behrens I., Kissel T., Vila Jato J.L., Alonso M.J. Low molecular weight chitosan nanoparticles as new carriers for nasal vaccine delivery in mice. Eur. J. Pharm. Biopharm. 2004, 57(1):123-131.
41. WHO, 2011. H5N1 avian influenza: Timeline of major events. From http://www.who.int/csr/disease/avian_influenza/H5N1_avian_%20influenza_update.
42. Wright P.F., Neuman G., Kawaoka Y. Orthomyxo viruses. Fields Virology 2007, 1691-1740. Lippincott-Raven, Philadelphia. 5th ed. D.M. Knipe, P.M. Howley, D.E. Griffin, M.A. Martin, R.A. Ramb, B. Roizman, S.E. Straus (Eds.).
43. Yuki Y., Kiyono H. New generation of mucosal adjuvants for the induction of protective immunity. Rev. Med. Virol. 2003, 13:293-310.
44. Zhao G., Sun S., Du L., Xiao W., Ru Z., Kou Z., Guo Y., Yu H., Jiang S., Lone Y., Zheng B.J., Zhou Y. An H5N1 M2e-based multiple antigenic peptide vaccine confers heterosubtypic protection from lethal infection with pandemic 2009 H1N1 virus. Virol. J. 2010, 7:151.