Protein transduction domain-mediated influenza NP subunit vaccine generates a potent immune response and protection against influenza virus in mice

References

• Rolfes M, Blanton L, Brammer L, et al. Update: influenza activity – United States, September 28–December 6, 2014. MMWR Morb Mortal Wkly Rep. 2014;63(50):1189–1194.
   PubMed Web of Science ®Google Scholar
• Levine MZ, Martin JM, Gross FL, et al. Neutralizing antibody responses to antigenically drifted influenza A(H3N2) viruses among children and adolescents following 2014–2015 inactivated and live attenuated influenza vaccination. Clin Vaccine Immunol. 2016;23(10):831–839. doi: 10.1128/CVI.00297-16
   PubMedGoogle Scholar
• Uyeki TM, Peiris M. Novel avian influenza a virus infections of humans. Infect Dis Clin North Am. 2019;33(4):907–932. doi: 10.1016/j.idc.2019.07.003
   PubMed Web of Science ®Google Scholar
• Krammer F. Emerging influenza viruses and the prospect of a universal influenza virus vaccine. Biotechnol J. 2015;10(5):690–701. doi: 10.1002/biot.201400393
   PubMed Web of Science ®Google Scholar
• To KK, Tsang AK, Chan JF, et al. Emergence in China of human disease due to avian influenza A(H10N8)–cause for concern? J Infect. 2014;68(3):205–215. doi: 10.1016/j.jinf.2013.12.014
   PubMed Web of Science ®Google Scholar
• McMahon M, Asthagiri Arunkumar G, Liu WC, et al. Vaccination with viral vectors expressing chimeric hemagglutinin, NP and M1 antigens protects ferrets against influenza virus challenge. Front Immunol. 2019;10:2005:1–11.
   Web of Science ®Google Scholar
• Zheng M, Luo J, Chen Z. Development of universal influenza vaccines based on influenza virus M and NP genes. Infection. 2014;42(2):251–262. doi: 10.1007/s15010-013-0546-4
   PubMed Web of Science ®Google Scholar
• Epstein SL, Kong WP, Misplon JA, et al. Protection against multiple influenza a subtypes by vaccination with highly conserved nucleoprotein. Vaccine. 2005;23(46-47):5404–5410. doi: 10.1016/j.vaccine.2005.04.047
   PubMed Web of Science ®Google Scholar
• Grant E, Wu C, Chan KF, et al. Nucleoprotein of influenza a virus is a major target of immunodominant CD8+ T-cell responses. Immunol Cell Biol. 2013;91(2):184–194. doi: 10.1038/icb.2012.78
   PubMed Web of Science ®Google Scholar
• Portela A, Digard P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol. 2002;83(Pt 4):723–734. doi: 10.1099/0022-1317-83-4-723
   PubMed Web of Science ®Google Scholar
• Alexander J, Bilsel P, del Guercio MF, et al. Universal influenza DNA vaccine encoding conserved CD4+ T cell epitopes protects against lethal viral challenge in HLA-DR transgenic mice. Vaccine. 2010;28(3):664–672. doi: 10.1016/j.vaccine.2009.10.103
   PubMed Web of Science ®Google Scholar
• McKinstry KK, Strutt TM, Kuang Y, et al. Memory CD4+ T cells protect against influenza through multiple synergizing mechanisms. J Clin Invest. 2012;122(8):2847–2856. doi: 10.1172/JCI63689
   PubMed Web of Science ®Google Scholar
• Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell. 1988;55(6):1189–1193. doi: 10.1016/0092-8674(88)90263-2
   PubMed Web of Science ®Google Scholar
• Green M, Loewenstein PM. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell. 1988;55(6):1179–1188. doi: 10.1016/0092-8674(88)90262-0
   PubMed Web of Science ®Google Scholar
• Jiang Y, Li M, Zhang Z, et al. Cell-penetrating peptides as delivery enhancers for vaccine. Curr Pharm Biotechnol. 2014;15(3):256–266. doi: 10.2174/1389201015666140813130114
   PubMed Web of Science ®Google Scholar
• Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol. 2010;10(11):787–796. doi: 10.1038/nri2868
   PubMed Web of Science ®Google Scholar
• Schutze-Redelmeier MP, Gournier H, Garcia-Pons F, et al. Introduction of exogenous antigens into the MHC class I processing and presentation pathway by Drosophila antennapedia homeodomain primes cytotoxic T cells in vivo. J Immunol. 1996;157(2):650–655.
   PubMed Web of Science ®Google Scholar
• Kim DT, Mitchell DJ, Brockstedt DG, et al. Introduction of soluble proteins into the MHC class I pathway by conjugation to an HIV tat peptide. J Immunol. 1997;159(4):1666–1668.
   PubMed Web of Science ®Google Scholar
• Guo L, Zheng M, Ding Y, et al. Protection against multiple influenza a virus subtypes by intranasal administration of recombinant nucleoprotein. Arch Virol. 2010;155(11):1765–1775. doi: 10.1007/s00705-010-0756-3
   PubMed Web of Science ®Google Scholar
• Sui Z, Chen Q, Fang F, et al. Cross-protection against influenza virus infection by intranasal administration of M1-based vaccine with chitosan as an adjuvant. Vaccine. 2010;28(48):7690–7698. doi: 10.1016/j.vaccine.2010.09.019
   PubMed Web of Science ®Google Scholar
• Luo J, Zheng D, Zhang W, et al. Induction of cross-protection against influenza a virus by DNA prime-intranasal protein boost strategy based on nucleoprotein. Virol J. 2012;9:286:1–11.
   Web of Science ®Google Scholar
• Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol. 2006;6(2):148–158. doi: 10.1038/nri1777
   PubMed Web of Science ®Google Scholar
• Schotsaert M, Saelens X, Leroux-Roels G. Influenza vaccines: T-cell responses deserve more attention. Expert Rev Vaccines. 2012;11(8):949–962. doi: 10.1586/erv.12.71
   PubMed Web of Science ®Google Scholar
• Vivès E, Brodin P, Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem. 1997;272(25):16010–16017. doi: 10.1074/jbc.272.25.16010
   PubMed Web of Science ®Google Scholar
• Ziegler A. Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans. Adv Drug Deliv Rev. 2008;60:580–597. doi: 10.1016/j.addr.2007.10.005
   PubMed Web of Science ®Google Scholar
• Gump JM, June RK, Dowdy SF. Revised role of glycosaminoglycans in TAT protein transduction domain-mediated cellular transduction. J Biol Chem. 2010;285:1500–1507. doi: 10.1074/jbc.M109.021964
   PubMed Web of Science ®Google Scholar
• Koren E, Torchilin VP. Cell-penetrating peptides: breaking through to the other side. Trends Mol Med. 2012;18:385–393. doi: 10.1016/j.molmed.2012.04.012
   PubMed Web of Science ®Google Scholar
• Kim SG, Park MY, Kim CH, et al. Modification of CEA with both CRT and TAT PTD induces potent anti-tumor immune responses in RNA-pulsed DC vaccination. Vaccine. 2008;26(50):6433–6440. doi: 10.1016/j.vaccine.2008.08.072
   PubMed Web of Science ®Google Scholar
• Shibagaki N, Udey MC. Dendritic cells transduced with TAT protein transduction domain-containing tyrosinase-related protein 2 vaccinate against murine melanoma. Eur J Immunol. 2003;33(4):850–860. doi: 10.1002/eji.200323709
   PubMed Web of Science ®Google Scholar
• Ackerman AL, Cresswell P. Cellular mechanisms governing cross-presentation of exogenous antigens. Nat Immunol. 2004;5(7):678–684. doi: 10.1038/ni1082
   PubMed Web of Science ®Google Scholar
• Carragher DM, Kaminski DA, Moquin A, et al. A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J Immunol. 2008;181(6):4168–4176. doi: 10.4049/jimmunol.181.6.4168
   PubMed Web of Science ®Google Scholar
• Mozdzanowska K, Maiese K, Furchner M, et al. Treatment of influenza virus-infected SCID mice with nonneutralizing antibodies specific for the transmembrane proteins matrix 2 and neuraminidase reduces the pulmonary virus titer but fails to clear the infection. Virology. 1999;254(1):138–146. doi: 10.1006/viro.1998.9534
   PubMed Web of Science ®Google Scholar
• Gerhard W, Mozdzanowska K, Furchner M, et al. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunol Rev. 1997;159:95–103. doi: 10.1111/j.1600-065X.1997.tb01009.x
   PubMed Web of Science ®Google Scholar
• Virelizier JL, Allison AC, Oxford JS, et al. Early presence of ribonucleoprotein antigen on surface of influenza virus-infected cells. Nature. 1977;266(5597):52–54. doi: 10.1038/266052a0
   PubMed Web of Science ®Google Scholar
• Yewdell JW, Frank E, Gerhard W. Expression of influenza a virus internal antigens on the surface of infected P815 cells. J Immunol. 1981;126(5):1814–1819.
   PubMed Web of Science ®Google Scholar
• LaMere MW, Lam HT, Moquin A, et al. Contributions of antinucleoprotein IgG to heterosubtypic immunity against influenza virus. J Immunol. 2011;186(7):4331–4339. doi: 10.4049/jimmunol.1003057
   PubMed Web of Science ®Google Scholar
• Mazanec MB, Kaetzel CS, Lamm ME, et al. Intracellular neutralization of virus by immunoglobulin A antibodies. Proc Natl Acad Sci U S A. 1992;89(15):6901–6905. doi: 10.1073/pnas.89.15.6901
   PubMed Web of Science ®Google Scholar
• Mazanec MB, Coudret CL, Fletcher DR. Intracellular neutralization of influenza virus by immunoglobulin A anti-hemagglutinin monoclonal antibodies. J Virol. 1995;69(2):1339–1343. doi: 10.1128/JVI.69.2.1339-1343.1995
   PubMed Web of Science ®Google Scholar
• Aiyegbo MS, Sapparapu G, Spiller BW, et al. Human rotavirus VP6-specific antibodies mediate intracellular neutralization by binding to a quaternary structure in the transcriptional pore. PLoS One. 2013;8(5):e61101. doi: 10.1371/journal.pone.0061101
   PubMed Web of Science ®Google Scholar
• Sanchez MV, Ebensen T, Schulze K, et al. Intranasal delivery of influenza rNP adjuvanted with c-di-AMP induces strong humoral and cellular immune responses and provides protection against virus challenge. PLoS One. 2014;9(8):e104824. doi: 10.1371/journal.pone.0104824
   PubMed Web of Science ®Google Scholar