Cold-Adapted influenza and recombinant adenovirus vaccines induce Cross-Protective immunity against PH1N1 challenge in mice

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Soboleski, Mark R ^a   Gabbard, Jon D ^b   Price, Graeme E ^a   Misplon, Julia A ^a   Lo, Chia Yun ^a   Perez, Daniel R ^c   Ye, Jianqiang ^c   Tompkins, S Mark ^b   Epstein, Suzanne L ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; NUCLEOPROTEIN; PROTEIN M2; RECOMBINANT ADENOVIRUS VACCINE; RECOMBINANT VACCINE; UNCLASSIFIED DRUG; VIRUS VACCINE; EPITOPE; VIRUS ANTIBODY;

2009 H1N1 INFLUENZA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; CROSS PROTECTION; CROSS REACTION; DRUG EFFICACY; EPITOPE MAPPING; FEMALE; GENE SEQUENCE; IMMUNITY; IMMUNIZATION; INFLUENZA VIRUS A H1N1; LUNG ALVEOLUS CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SINGLE DRUG DOSE; T LYMPHOCYTE; TEMPERATURE SENSITIVE MUTANT; ADAPTATION; ADENOVIRUS; AMINO ACID SEQUENCE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; C57BL MOUSE; CHEMISTRY; COLD; IMMUNOLOGY; LUNG; MOLECULAR GENETICS; ORTHOMYXOVIRUS INFECTION; PANDEMIC; PATHOLOGY; VACCINATION; VIROLOGY; VIRUS LOAD;

ADENOVIRIDAE; MUS; ORTHOMYXOVIRIDAE;

ADAPTATION, PHYSIOLOGICAL; ADENOVIRIDAE; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, VIRAL; COLD TEMPERATURE; CROSS PROTECTION; EPITOPES; IMMUNITY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; LUNG; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE INFECTIONS; PANDEMICS; T-LYMPHOCYTES; VACCINATION; VACCINES, SYNTHETIC; VIRAL LOAD;

EID: 79960330452     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021937     Document Type: Article

References (48)

1. Thompson WW, Weintraub E, Dhankhar P, Cheng PY, Brammer L, et al. (2009) Estimates of US influenza-associated deaths made using four different methods. Influenza Other Respi Viruses 3: 37-49.
2. Fraser C, Donnelly CA, Cauchemez S, Hanage WP, Van Kerkhove MD, et al. (2009) Pandemic potential of a strain of influenza A (H1N1): early findings. Science 324: 1557-1561.
3. Ulmer JB, Donnelly JJ, Parker SE, Rhodes GH, Felgner PL, et al. (1993) Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259: 1745-1749.
4. Oukka M, Manugerra JC, Livaditis N, Tourdot S, Riche N, et al. (1996) Protection against lethal viral infection by vaccination with nonimmunodominant peptides. J Immunol 157: 3039-3045.
5. Webby RJ, Andreansky S, Stambas J, Rehg JE, Webster RG, et al. (2003) Protection and compensation in the influenza virus-specific CD8+ T cell response. Proc Natl Acad Sci U S A 100: 7235-7240.
6. Roy S, Kobinger GP, Lin J, Figueredo J, Calcedo R, et al. (2007) Partial protection against H5N1 influenza in mice with a single dose of a chimpanzee adenovirus vector expressing nucleoprotein. Vaccine 25: 6845-6851.
7. Epstein SL, Price GE, (2010) Cross-protective immunity to influenza A viruses. Expert Rev Vaccines 9: 1325-1341.
8. Tompkins SM, Zhao ZS, Lo C-Y, 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.
9. Zhou D, Wu TL, Lasaro MO, Latimer BP, Parzych EM, et al. (2010) A universal influenza A vaccine based on adenovirus expressing matrix-2 ectodomain and nucleoprotein protects mice from lethal challenge. Mol Ther 18: 2182-2189.
10. Andrew ME, Coupar BE, Ada GL, Boyle DB, (1986) Cell-mediated immune responses to influenza virus antigens expressed by vaccinia virus recombinants. Microb Pathog 1: 443-452.
11. 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.
12. Slepushkin VA, Katz JM, Black RA, Gamble WC, Rota PA, et al. (1995) Protection of mice against influenza A virus challenge by vaccination with baculovirus-expressed M2 protein. Vaccine 13: 1399-1402.
13. Mozdzanowska K, Feng J, Eid M, Kragol G, Cudic M, et al. (2003) Induction of influenza type A virus-specific resistance by immunization of mice with a synthetic multiple antigenic peptide vaccine that contains ectodomains of matrix protein 2. Vaccine 21: 2616-2626.
14. Lo CY, Wu Z, Misplon JA, Price GE, Pappas C, et al. (2008) Comparison of vaccines for induction of heterosubtypic immunity to influenza A virus: Cold-adapted vaccine versus DNA prime-adenovirus boost strategies. Vaccine 26: 2062-2072.
15. 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.
16. Price GE, Soboleski MR, Lo CY, Misplon JA, Quirion MR, et al. (2010) Single-dose mucosal immunization with a candidate universal influenza vaccine provides rapid protection from virulent H5N1, H3N2 and H1N1 viruses. PLoS One 5 Available: e13162. 10.1371/journal.pone.0013162.
17. Tannock GA, Paul JA, (1987) Homotypic and heterotypic immunity of influenza A viruses induced by recombinants of the cold-adapted master strain A/Ann Arbor/6/60-ca. Arch Virol 92: 121-133.
18. Powell TJ, Strutt T, Reome J, Hollenbaugh JA, Roberts AD, et al. (2007) Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J Immunol 178: 1030-1038.
19. Epstein SL, Kong WP, Misplon JA, Lo CY, Tumpey TM, et al. (2005) Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine 23: 5404-5410.
20. Murphy BR, Coelingh K, (2002) Principles underlying the development and use of live attenuated cold-adapted influenza A and B virus vaccines. Vir Immunol 15: 295-323.
21. Ye J, Sorrell EM, Cai Y, Shao H, Xu K, et al. (2010) Variations in the hemagglutinin of the 2009 H1N1 pandemic virus: potential for strains with altered virulence phenotype? PLoS Pathog 6 Available: e1001145. 10.1371/journal.ppat.1001145.
22. Benton KA, Misplon JA, Lo C-Y, Brutkiewicz RR, Prasad SA, et al. (2001) Heterosubtypic immunity to influenza A virus in mice lacking either IgA, all Ig, NKT cells, or γδ T cells. J Immunol 166: 7437-7445.
23. Reed LJ, Muench H, (1938) A simple method of estimating fifty percent endpoints. American Journal of Hygiene 27: 493-497.
24. 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.
25. Townsend AR, Rothbard J, Gotch FM, Bahadur G, Wraith D, et al. (2006) The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. 1986. J Immunol 176: 5141-5150.
26. Vitiello A, Yuan L, Chesnut RW, Sidney J, Southwood S, et al. (1996) Immunodominance analysis of CTL responses to influenza PR8 virus reveals two new dominant and subdominant Kb-restricted epitopes. J Immunol 157: 5555-5562.
27. Carragher DM, Kaminski DA, Moquin A, Hartson L, Randall TD, (2008) A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J Immunol 181: 4168-4176.
28. Lamere MW, Moquin A, Lee FE, Misra RS, Blair PJ, et al. (2011) Regulation of antinucleoprotein IgG by systemic vaccination and its effect on influenza virus clearance. J Virol 85: 5027-5035.
29. Lamere MW, Lam HT, Moquin A, Haynes L, Lund FE, et al. (2011) Contributions of antinucleoprotein IgG to heterosubtypic immunity against influenza virus. J Immunol 186: 4331-4339.
30. Graham MB, Braciale TJ, (1997) Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice. J Exp Med 186: 2063-2068.
31. Kobinger GP, Meunier I, Patel A, Pillet S, Gren J, et al. (2010) Assessment of the efficacy of commercially available and candidate vaccines against a pandemic H1N1 2009 virus. J Infect Dis 201: 1000-1006.
32. Lau YF, Santos C, Torres-Velez FJ, Subbarao K, (2011) The magnitude of local immunity in the lungs of mice induced by live attenuated influenza vaccines is determined by local viral replication and induction of cytokines. J Virol 85: 76-85.
33. 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.
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. Misplon JA, Lo CY, Gabbard JD, Tompkins SM, Epstein SL, (2010) Genetic control of immune responses to influenza A matrix 2 protein (M2). Vaccine 28: 5817-5827.
36. Brown LE, Kelso A, (2009) Prospects for an influenza vaccine that induces cross-protective cytotoxic T lymphocytes. Immunol Cell Biol 87: 300-308.
37. Kedzierska K, Guillonneau C, Gras S, Hatton LA, Webby R, et al. (2008) Complete modification of TCR specificity and repertoire selection does not perturb a CD8+ T cell immunodominance hierarchy. Proc Natl Acad Sci U S A 105: 19408-19413.
38. Price GE, Ou R, Jiang H, Huang L, Moskophidis D, (2000) Viral escape by selection of cytotoxic T cell-resistant variants in influenza A virus pneumonia. J Exp Med 191: 1853-1867.
39. Haanen JB, Wolkers MC, Kruisbeek AM, Schumacher TN, (1999) Selective expansion of cross-reactive CD8(+) memory T cells by viral variants. J Exp Med 190: 1319-1328.
40. Greenbaum JA, Kotturi MF, Kim Y, Oseroff C, Vaughan K, et al. (2009) Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc Natl Acad Sci U S A 106: 20365-20370.
41. Ge X, Tan V, Bollyky PL, Standifer NE, James EA, et al. (2010) Assessment of seasonal influenza A virus-specific CD4 T-cell responses to 2009 pandemic H1N1 swine-origin influenza A virus. J Virol 84: 3312-3319.
42. Tu W, Mao H, Zheng J, Liu Y, Chiu SS, et al. (2010) Cytotoxic T lymphocytes established by seasonal human influenza cross-react against 2009 pandemic H1N1 influenza virus. J Virol 84: 6527-6535.
43. Lee LY, Ha do LA, Simmons C, de Jong MD, Chau NV, et al. (2008) Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J Clin Invest 118: 3478-3490.
44. Ennis FA, Yi-Hua Q, Schild GC, (1982) Antibody and cytotoxic T lymphocyte responses of humans to live and inactivated influenza vaccines. J Gen Virol 58: 273-281.
45. Thorner AR, Lemckert AA, Goudsmit J, Lynch DM, Ewald BA, et al. (2006) Immunogenicity of heterologous recombinant adenovirus prime-boost vaccine regimens is enhanced by circumventing vector cross-reactivity. J Virol 80: 12009-12016.
46. Sun K, Ye J, Perez DR, Metzger DW, (2011) Seasonal FluMist vaccination induces cross-reactive T cell immunity against H1N1 (2009) influenza and secondary bacterial infections. J Immunol 186: 987-993.
47. Wesley RD, Tang M, Lager KM, (2004) Protection of weaned pigs by vaccination with human adenovirus 5 recombinant viruses expressing the hemagglutinin and the nucleoprotein of H3N2 swine influenza virus. Vaccine 22: 3427-3434.
48. Barefoot B, Thornburg NJ, Barouch DH, Yu JS, Sample C, et al. (2008) Comparison of multiple vaccine vectors in a single heterologous prime-boost trial. Vaccine 26: 6108-6118.