Influenza virus-like particles containing M2 induce broadly cross protective immunity

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Song, Jae Min ^a   Wang, Bao Zhong ^a   Park, Kyoung Mi ^a   van Rooijen, Nico ^b   Quan, Fu Shi ^a   Kim, Min Chul ^a   Jin, Hyun Tak ^a   Pekosz, Andrew ^c   Compans, Richard W ^a   Kang, Sang Moo ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLODRONIC ACID; IMMUNOGLOBULIN A; INFLUENZA VACCINE; PROTEIN M2; M2 PROTEIN, INFLUENZA A VIRUS; MATRIX PROTEIN; VIRUS ANTIBODY;

2009 H1N1 INFLUENZA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CROSS PROTECTION; DENDRITIC CELL; DEPLETION; DRUG EFFICACY; FEMALE; IMMUNE RESPONSE; IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; IMMUNOPROPHYLAXIS; INFLUENZA A; INFLUENZA VACCINATION; INFLUENZA VIRUS A H3N2; INSECT CELL; LEPIDOPTERA; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; SINGLE DRUG DOSE; SURVIVAL RATE; T LYMPHOCYTE; VIRUS IMMUNITY; VIRUS LIKE AGENT; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; HUMAN; IMMUNOLOGY; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; ORTHOMYXOVIRUS INFECTION; VIRION; VIROLOGY;

MUS; ORTHOMYXOVIRIDAE;

ANIMALS; ANTIBODIES, VIRAL; CROSS PROTECTION; DENDRITIC CELLS; HUMANS; IMMUNITY; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; MACROPHAGES; MICE; ORTHOMYXOVIRIDAE INFECTIONS; VIRAL MATRIX PROTEINS; VIRION;

EID: 79251575047     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014538     Document Type: Article

References (53)

1. Bush RM, Bender CA, Subbarao K, Cox NJ, Fitch WM (1999) Predicting the evolution of human influenza A. Science 286: 1921-1925.
2. Plotkin JB, Dushoff J (2003) Codon bias and frequency-dependent selection on the hemagglutinin epitopes of influenza A virus. Proc Natl Acad Sci U S A 100: 7152-7157.
3. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, et al. (2004) Mapping the antigenic and genetic evolution of influenza virus. Science 305: 371-376.
4. Nicholson KG, Wood JM, Zambon M (2003) Influenza. Lancet 362: 1733-1745.
5. Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, et al. (2009) Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med 361: 1945-1952.
6. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, et al. (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122-1125.
7. Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, et al. (1999) A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med 5: 1157-1163.
8. Fan J, Liang X, Horton MS, Perry HC, Citron MP, et al. (2004) Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 22: 2993-3003.
9. De Filette M, Ramne A, Birkett A, Lycke N, Lowenadler B, et al. (2006) The universal influenza vaccine M2e-HBc administered intranasally in combination with the adjuvant CTA1-DD provides complete protection. Vaccine 24: 544-551.
10. Ionescu RM, Przysiecki CT, Liang X, Garsky VM, Fan J, et al. (2006) Pharmaceutical and immunological evaluation of human papillomavirus viruslike particle as an antigen carrier. J Pharm Sci 95: 70-79.
11. Tompkins SM, Zhao ZS, Lo CY, Misplon JA, Liu T, et al. (2007) Matrix protein 2 vaccination and protection against influenza viruses, including subtype H5N1. Emerg Infect Dis 13: 426-435.
12. Fu TM, Grimm KM, Citron MP, Freed DC, Fan J, et al. (2009) Comparative immunogenicity evaluations of influenza A virus M2 peptide as recombinant virus like particle or conjugate vaccines in mice and monkeys. Vaccine 27: 1440-1447.
13. Ernst WA, Kim HJ, Tumpey TM, Jansen AD, Tai W, et al. (2006) Protection against H1, H5, H6 and H9 influenza A infection with liposomal matrix 2 epitope vaccines. Vaccine 24: 5158-5168.
14. Huleatt JW, Nakaar V, Desai P, Huang Y, Hewitt D, et al. (2008) Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine 26: 201-214.
15. Frace AM, Klimov AI, Rowe T, Black RA, Katz JM (1999) Modified M2 proteins produce heterotypic immunity against influenza A virus. Vaccine 17: 2237-2244.
16. Eliasson DG, Bakkouri KE, Schon K, Ramne A, Festjens E, et al. (2008) CTA1- M2e-DD: A novel mucosal adjuvant targeted influenza vaccine. Vaccine 26: 1243-1252.
17. Mozdzanowska K, Zharikova D, Cudic M, Otvos L, Gerhard W (2007) Roles of adjuvant and route of vaccination in antibody response and protection engendered by a synthetic matrix protein 2-based influenza A virus vaccine in the mouse. Virol J 4: 118.
18. Kang SM, Song JM, Quan FS, Compans RW (2009c) Influenza vaccines based on virus-like particles. Virus Res 143: 140-146.
19. Lamb RA, Zebedee SL, Richardson CD (1985) Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40: 627-633.
20. Holsinger LJ, Lamb RA (1991) Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology 183: 32-43.
21. Zebedee SL, Lamb RA (1988) Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J Virol 62: 2762-2772.
22. De Filette M, Martens W, Roose K, Deroo T, Vervalle F, et al. (2008) An influenza A vaccine based on tetrameric ectodomain of matrix protein 2. J Biol Chem 283: 11382-11387.
23. Okuda K, Ihata A, Watabe S, Okada E, Yamakawa T, et al. (2001) Protective immunity against influenza A virus induced by immunization with DNA plasmid containing influenza M gene. Vaccine 19: 3681-3691.
24. Price GE, Soboleski MR, Lo CY, Misplon JA, Pappas C, et al. (2009) Vaccination focusing immunity on conserved antigens protects mice and ferrets against virulent H1N1 and H5N1 influenza A viruses. Vaccine 27: 6512-6521.
25. Quan FS, Compans RW, Nguyen HH, Kang SM (2008) Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J Virol 82: 1350-1359.
26. 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.
27. Quan FS, Vunnava A, Compans RW, Kang SM (2010) Virus-Like Particle Vaccine Protects against 2009 H1N1 Pandemic Influenza Virus in Mice. PLoS One 5: e9161.
28. Bosio CM, Dow SW (2005) Francisella tularensis induces aberrant activation of pulmonary dendritic cells. J Immunol 175: 6792-6801.
29. McGill J, Van Rooijen N, Legge KL (2008) Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J Exp Med 205: 1635-1646.
30. Schotsaert M, De Filette M, Fiers W, Saelens X (2009) Universal M2 ectodomain-based influenza A vaccines: preclinical and clinical developments. Expert Rev Vaccines 8: 499-508.
31. Bessa J, Schmitz N, Hinton HJ, Schwarz K, Jegerlehner A, et al. (2008) Efficient induction of mucosal and systemic immune responses by virus-like particles administered intranasally: implications for vaccine design. Eur J Immunol 38: 114-126.
32. Jimenez GS, Planchon R, Wei Q, Rusalov D, Geall A, et al. (2007) Vaxfectinformulated influenza DNA vaccines encoding NP and M2 viral proteins protect mice against lethal viral challenge. Hum Vaccin 3: 157-164.
33. Skountzou I, Quan FS, Gangadhara S, Ye L, Vzorov A, et al. (2007) Incorporation of Glycosylphosphatidylinositol-Anchored Granulocyte- Macrophage Colony-Stimulating Factor or CD40 Ligand Enhances Immunogenicity of Chimeric Simian Immunodeficiency Virus-Like Particles. J Virol 81: 1083-1094.
34. Jegerlehner A, Schmitz N, Storni T, Bachmann MF (2004) Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J Immunol 172: 5598-5605.
35. Fu TM, Freed DC, Horton MS, Fan J, Citron MP, et al. (2009) Characterizations of four monoclonal antibodies against M2 protein ectodomain of influenza A virus. Virology 385: 218-226.
36. Huber VC, Lynch JM, Bucher DJ, Le J, Metzger DW (2001) Fc receptormediated 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. Huber VC, McKeon RM, Brackin MN, Miller LA, Keating R, et al. (2006) Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin Vaccine Immunol 13: 981-990.
41. 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.
42. 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.
43. Zinkernagel RM, Bachmann MF, Kundig TM, Oehen S, Pirchet H, et al. (1996) On immunological memory. Annu Rev Immunol 14: 333-367.
44. Bachmann MF, Zinkernagel RM (1997) Neutralizing antiviral B cell responses. Annu Rev Immunol 15: 235-270.
45. Ahmed R, Gray D (1996) Immunological memory and protective immunity: understanding their relation. Science 272: 54-60.
46. Misplon JA, Lo CY, Gabbard JD, Tompkins SM, Epstein SL () Genetic control of immune responses to influenza A matrix 2 protein (M2). Vaccine 28: 5817-5827.
47. Gianfrani C, Oseroff C, Sidney J, Chesnut RW, Sette A (2000) Human memory CTL response specific for influenza A virus is broad and multispecific. Hum Immunol 61: 438-452.
48. Yao Q, Zhang R, Guo L, Li M, Chen C (2004) Th cell-independent immune responses to chimeric hemagglutinin/simian human immunodeficiency viruslike particles vaccine. J Immunol 173: 1951-1958.
49. Kang SM, Yoo DG, Lipatov AS, Song JM, Davis CT, et al. (2009) Induction of long-term protective immune responses by influenza H5N1 virus-like particles. PLoS ONE 4: e4667.
50. Grantham ML, Stewart SM, Lalime EN, Pekosz A Tyrosines in the influenza A virus M2 protein cytoplasmic tail are critical for production of infectious virus particles. J Virol 84: 8765-8776.
51. Van Rooijen N, Sanders A (1994) Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174: 83-93.
52. Thepen T, McMenamin C, Oliver J, Kraal G, Holt PG (1991) Regulation of immune response to inhaled antigen by alveolar macrophages: differential effects of in vivo alveolar macrophage elimination on the induction of tolerance vs. immunity. Eur J Immunol 21: 2845-2850.
53. Quan FS, Kim YC, Yoo DG, Compans RW, Prausnitz MR, et al. (2009) Stabilization of influenza vaccine enhances protection by microneedle delivery in the mouse skin. PLoS One 4: e7152.