Evaluation of heterosubtypic cross-protection against highly pathogenic H5N1 by active infection with human seasonal influenza A virus or trivalent inactivated vaccine immunization in ferret models
The threat of highly pathogenic avian influenza (HPAI) H5N1 viruses to cause the next pandemic remains a major concern. Here, we evaluated the cross-protection induced by natural infection of human seasonal influenza strains or immunization with trivalent inactivated influenza vaccine (TIV) against HPAI H5N1 (A/Vietnam/1203/2004) virus in ferrets. Groups were treated with PBS (group A), infected with H1N1 (group B) or H3N2 (group C) virus, or immunized with TIV (group D). Twelve weeks after the last treatment, serological assays revealed that groups B and C, but not group D, sustained moderate immunogenicity against homologous viruses; cross-reactivity against the H5N1 virus was not detected in any group. Following challenge with A/Vietnam/1203/2004 (H5N1) virus, only groups B and C exhibited attenuated viral loads leading to 100 % survival. Our data suggest that natural infection with human seasonal strains could potentially provide better heterosubtypic protection against HPAI H5N1 virus infection compared to TIV immunization.
AirG. M.1981; Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus. Proc Natl Acad Sci U S A 78:7639–7643 [View Article][PubMed]
BeigelJ. H., FarrarJ., HanA. M., HaydenF. G., HyerR., de JongM. D., LochindaratS., NguyenT. K., NguyenT. H.other authors2005; Avian influenza A (H5N1) infection in humans. N Engl J Med 353:1374–1385 [View Article][PubMed]
BodewesR., KreijtzJ. H., BaasC., Geelhoed-MierasM. M., de MutsertG., van AmerongenG., van den BrandJ. M., FouchierR. A., OsterhausA. D., RimmelzwaanG. F.2009; Vaccination against human influenza A/H3N2 virus prevents the induction of heterosubtypic immunity against lethal infection with avian influenza A/H5N1 virus. PLoS ONE 4:e5538 [View Article][PubMed]
BodewesR., KreijtzJ. H., Geelhoed-MierasM. M., van AmerongenG., VerburghR. J., van TrierumS. E., KuikenT., FouchierR. A., OsterhausA. D., RimmelzwaanG. F.2011; Vaccination against seasonal influenza A/H3N2 virus reduces the induction of heterosubtypic immunity against influenza A/H5N1 virus infection in ferrets. J Virol 85:2695–2702 [View Article][PubMed]
BragstadK., JørgensenP. H., HandbergK., HammerA. S., KabellS., FomsgaardA.2007; First introduction of highly pathogenic H5N1 avian influenza A viruses in wild and domestic birds in Denmark, Northern Europe. Virol J 4:43 [View Article][PubMed]
BrewooJ. N., PowellT. D., JonesJ. C., GundlachN. A., YoungG. R., ChuH., DasS. C., PartidosC. D., StinchcombD. T., OsorioJ. E.2013; Cross-protective immunity against multiple influenza virus subtypes by a novel modified vaccinia Ankara (MVA) vectored vaccine in mice. Vaccine 31:1848–1855 [View Article][PubMed]
CattoliG., MonneI., FusaroA., JoannisT. M., LombinL. H., AlyM. M., ArafaA. S., Sturm-RamirezK. M., Couacy-HymannE.other authors2009; Highly pathogenic avian influenza virus subtype H5N1 in Africa: a comprehensive phylogenetic analysis and molecular characterization of isolates. PLoS ONE 4:e4842 [View Article][PubMed]
ChenZ., KimL., SubbaraoK., JinH.2012; The 2009 pandemic H1N1 virus induces anti-neuraminidase (NA) antibodies that cross-react with the NA of H5N1 viruses in ferrets. Vaccine 30:2516–2522 [View Article][PubMed]
ClaasE. C., OsterhausA. D., van BeekR., De JongJ. C., RimmelzwaanG. F., SenneD. A., KraussS., ShortridgeK. F., WebsterR. G.1998; Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351:472–477 [View Article][PubMed]
HeinyA. T., MiottoO., SrinivasanK. N., KhanA. M., ZhangG. L., BrusicV., TanT. W., AugustJ. T.2007; Evolutionarily conserved protein sequences of influenza a viruses, avian and human, as vaccine targets. PLoS ONE 2:e1190 [View Article][PubMed]
HoftD. F., BabusisE., WorkuS., SpencerC. T., LottenbachK., TruscottS. M., AbateG., SakalaI. G., EdwardsK. M.other authors2011; Live and inactivated influenza vaccines induce similar humoral responses, but only live vaccines induce diverse T-cell responses in young children. J Infect Dis 204:845–853 [View Article][PubMed]
KreijtzJ. H., de MutsertG., van BaalenC. A., FouchierR. A., OsterhausA. D., RimmelzwaanG. F.2008; Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J Virol 82:5161–5166 [View Article][PubMed]
KreijtzJ. H., SuezerY., de MutsertG., van den BrandJ. M., van AmerongenG., SchnierleB. S., KuikenT., FouchierR. A., LöwerJ.other authors2009; Preclinical evaluation of a modified vaccinia virus Ankara (MVA)-based vaccine against influenza A/H5N1 viruses. Vaccine 27:6296–6299 [View Article][PubMed]
LambR. A., ZebedeeS. L., RichardsonC. D.1985; Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40:627–633 [View Article][PubMed]
LeeL. Y., HaL. A., SimmonsC., de JongM. D., ChauN. V., SchumacherR., PengY. C., McMichaelA. J., FarrarJ. J.other authors2008; 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[PubMed]
MoskophidisD., KioussisD.1998; 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 188:223–232 [View Article][PubMed]
PappaioanouM.2009; Highly pathogenic H5N1 avian influenza virus: cause of the next pandemic?. Comp Immunol Microbiol Infect Dis 32:287–300 [View Article][PubMed]
SchulmanJ. L., KilbourneE. D.1965; Induction of partial specific heterotypic immunity in mice by a single infection with influenza A virus. J Bacteriol 89:170–174[PubMed]
WangT. T., TanG. S., HaiR., PicaN., NgaiL., EkiertD. C., WilsonI. A., García-SastreA., MoranT. M., PaleseP.2010; Vaccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes. Proc Natl Acad Sci U S A 107:18979–18984 [View Article][PubMed]
YewdellJ. W., BenninkJ. R., SmithG. L., MossB.1985; Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc Natl Acad Sci U S A 82:1785–1789 [View Article][PubMed]
Evaluation of heterosubtypic cross-protection against highly pathogenic H5N1 by active infection with human seasonal influenza A virus or trivalent inactivated vaccine immunization in ferret models