DNA vaccines encoding antigen targeted to MHC class II induce influenza-specific CD8+ T cell responses, enabling faster resolution of influenza disease

Frontiers in Immunology

Volumn 7, Issue AUG, 2016, Pages

  Lambert, Laura ^a   Kinnear, Ekaterina ^a   McDonald, Jacqueline U ^a   Grodeland, Gunnveig ^b   Bogen, Bjarne ^b   Stubsrud, Elisabeth ^c   Lindeberg, Mona M ^c   Fredriksen, Agnete Brunsvik ^c   Tregoning, John S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c Vaccibody AS Oslo Science Park   (Norway)

Author keywords

CD8+ T lymphocytes; DNA vaccines; Immune targeting; Influenza vaccines; MHC II

Indexed keywords

DNA VACCINE; IMMUNOGLOBULIN G; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; BLOOD SAMPLING; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; ELECTROPORATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE DOSAGE; GENOTYPE; IMMUNIZATION; INFLUENZA; MOUSE; NONHUMAN; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; VIRUS LOAD;

EID: 84990026817     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00321     Document Type: Article

References (33)

1. Nair H, Brooks WA, Katz M, Roca A, Berkley JA, Madhi SA, et al. Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis. Lancet (2011) 378:1917-30. doi:10.1016/S0140-6736(11)61051-9
2. Reber A, Katz J. Immunological assessment of influenza vaccines and immune correlates of protection. Expert Rev Vaccines (2013) 12:519-36. doi:10.1586/erv.13.35
3. Altenburg AF, Rimmelzwaan GF, De Vries RD. Virus-specific T cells as correlate of (cross-) protective immunity against influenza. Vaccine (2015) 33:500-6. doi:10.1016/j.vaccine.2014.11.054
4. Brown LE, Kelso A. Prospects for an influenza vaccine that induces cross-protective cytotoxic T lymphocytes. Immunol Cell Biol (2009) 87:300-8. doi:10.1038/icb.2009.16
5. Sridhar S, Begom S, Bermingham A, Hoschler K, Adamson W, Carman W, et al. Cellular immune correlates of protection against symptomatic pandemic influenza. Nat Med (2013) 19:1305-12. doi:10.1038/nm.3350
6. Barber BH. The immunotargeting approach to adjuvant-independent subunit vaccine design. Semin Immunol (1997) 9:293-301. doi:10.1006/smim.1997.0085
7. Grodeland G, Bogen B. Efficient vaccine against pandemic influenza: combining DNA vaccination and targeted delivery to MHC class II molecules. Expert Rev Vaccines (2015) 14:805-14. doi:10.1586/14760584.2015.1029919
8. Grodeland G, Mjaaland S, Roux KH, Fredriksen AB, Bogen B. DNA vaccine that targets hemagglutinin to MHC class II molecules rapidly induces antibody-mediated protection against influenza. J Immunol (2013) 191:3221-31. doi:10.4049/jimmunol.1300504
9. Fossum E, Grodeland G, Terhorst D, Tveita AA, Vikse E, Mjaaland S, et al. Vaccine molecules targeting Xcr1 on cross-presenting DCs induce protective CD8+ T-cell responses against influenza virus. Eur J Immunol (2015) 45:624-35. doi:10.1002/eji.201445080
10. Fredriksen AB, Sandlie I, Bogen B. DNA vaccines increase immunogenicity of idiotypic tumor antigen by targeting novel fusion proteins to antigen-presenting cells. Mol Ther (2006) 13:776-85. doi:10.1016/j.ymthe.2005.10.019
11. Tregoning JS, Wang BL, Mcdonald JU, Yamaguchi Y, Harker JA, Goritzka M, et al. Neonatal antibody responses are attenuated by interferon-gamma produced by NK and T cells during RSV infection. Proc Natl Acad Sci U S A (2013) 110:5576-81. doi:10.1073/pnas.1214247110
12. Baillie GJ, Galiano M, Agapow PM, Myers R, Chiam R, Gall A, et al. Evolutionary dynamics of local pandemic H1N1/2009 influenza virus lineages revealed by whole-genome analysis. J Virol (2012) 86:11-8. doi:10.1128/JVI.05347-11
13. Elleman CJ, Barclay WS. The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology (2004) 321:144-53. doi:10.1016/j.virol.2003.12.009
14. Russell RF, Mcdonald JU, Lambert L, Tregoning JS. Use of the microparticle NanoSiO2 as an adjuvant to boost vaccine immune responses in neonatal mice against influenza. J Virol (2016) 90:4735-44. doi:10.1128/JVI.03159-15
15. Siggins MK, Gill SK, Langford PR, Li Y, Ladhani SN, Tregoning JS. PHiD-CV induces anti-protein D antibodies but does not augment pulmonary clearance of nontypeable Haemophilus influenzae in mice. Vaccine (2015) 33:4954-61. doi:10.1016/j.vaccine.2015.07.034
16. Tregoning JS, Kinnear E. Using plasmids as DNA vaccines for infectious diseases. Microbiol Spectr (2014) 2. doi:10.1128/microbiolspec.PLAS-0028-2014
17. Grodeland G, Fossum E, Bogen B. Polarizing T and B cell responses by APC-targeted subunit vaccines. Front Immunol (2015) 6:367. doi:10.3389/fimmu.2015.00367
18. Tregoning JS, Yamaguchi Y, Wang B, Mihm D, Harker JA, Bushell ES, et al. Genetic susceptibility to the delayed sequelae of neonatal respiratory syncytial virus infection is MHC dependent. J Immunol (2010) 185:5384-91. doi:10.4049/jimmunol.1001594
19. Enelow RI, Mohammed AZ, Stoler MH, Liu AN, Young JS, Lou YH, et al. Structural and functional consequences of alveolar cell recognition by CD8(+) T lymphocytes in experimental lung disease. J Clin Invest (1998) 102:1653-61. doi:10.1172/JCI4174
20. Tregoning JS, Yamaguchi Y, Harker J, Wang B, Openshaw PJ. The role of T cells in the enhancement of respiratory syncytial virus infection severity during adult reinfection of neonatally sensitized mice. J Virol (2008) 82:4115-24. doi:10.1128/JVI.02313-07
21. Baranowska M, Hauge AG, Hoornaert C, Bogen B, Grodeland G. Targeting of nucleoprotein to chemokine receptors by DNA vaccination results in increased CD8(+)-mediated cross protection against influenza. Vaccine (2015) 33:6988-96. doi:10.1016/j.vaccine.2015.08.094
22. Pham N-LL, Pewe LL, Fleenor CJ, Langlois RA, Legge KL, Badovinac VP, et al. Exploiting cross-priming to generate protective CD8 T-cell immunity rapidly. Proc Natl Acad Sci U S A (2010) 107:12198-203. doi:10.1073/pnas.1004661107
23. Moskophidis D, Kioussis D. Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J Exp Med (1998) 188:223-32. doi:10.1084/jem.188.2.223
24. Walters AA, Kinnear E, Shattock RJ, Mcdonald JU, Caproni LJ, Porter N, et al. Comparative analysis of enzymatically produced novel linear DNA constructs with plasmids for use as DNA vaccines. Gene Ther (2014) 21:645-52. doi:10.1038/gt.2014.37
25. Kinnear E, Caproni LJ, Tregoning JS. A comparison of red fluorescent proteins to model DNA vaccine expression by whole animal in vivo imaging. PLoS One (2015) 10(6):e0130375. doi:10.1371/journal.pone.0130375
26. Wakim LM, Smith J, Caminschi I, Lahoud MH, Villadangos JA. Antibody-targeted vaccination to lung dendritic cells generates tissue-resident memory CD8 T cells that are highly protective against influenza virus infection. Mucosal Immunol (2015) 8:1060-71. doi:10.1038/mi.2014.133
27. Chen GL, Lau YF, Lamirande EW, Mccall AW, Subbarao K. Seasonal influenza infection and live vaccine prime for a response to the 2009 pandemic H1N1 vaccine. Proc Natl Acad Sci U S A (2011) 108:1140-5. doi:10.1073/pnas.1009908108
28. Badamchi-Zadeh A, Mckay PF, Korber BT, Barinaga G, Walters AA, Nunes A, et al. A multi-component prime-boost vaccination regimen with a consensus MOMP antigen enhances chlamydia trachomatis clearance. Front Immunol (2016) 7:162. doi:10.3389/fimmu.2016.00162
29. Wilkinson TM, Li CKF, Chui CSC, Huang AKY, Perkins M, Liebner JC, et al. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med (2012) 18:274-80. doi:10.1038/nm.2612
30. Nakanishi Y, Lu B, Gerard C, Iwasaki A. CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature (2009) 462:510-3. doi:10.1038/nature08511
31. van de Berg PJ, van Leeuwen EM, Ten Berge IJ, van Lier R. Cytotoxic human CD4(+) T cells. Curr Opin Immunol (2008) 20:339-43. doi:10.1016/j.coi.2008.03.007
32. Grodeland G, Mjaaland S, Tunheim G, Fredriksen AB, Bogen B. The specificity of targeted vaccines for APC surface molecules influences the immune response phenotype. PLoS One (2013) 8:e80008. doi:10.1371/journal.pone.0080008
33. Habibi MS, Jozwik A, Makris S, Dunning J, Paras A, Devincenzo JP, et al. Impaired antibody-mediated protection and defective IgA B-cell memory in experimental infection of adults with respiratory syncytial virus. Am J Respir Crit Care Med (2015) 191:1040-9. doi:10.1164/rccm.201412-2256OC