Induction of Virus-Specific Cytotoxic T Lymphocytes as a Basis for the Development of Broadly Protective Influenza Vaccines
Identifieur interne : 000816 ( Pmc/Checkpoint ); précédent : 000815; suivant : 000817Induction of Virus-Specific Cytotoxic T Lymphocytes as a Basis for the Development of Broadly Protective Influenza Vaccines
Auteurs : Marine L. B. Hillaire [Pays-Bas] ; Albert D. M. E. Osterhaus ; Guus F. RimmelzwaanSource :
- Journal of Biomedicine and Biotechnology [ 1110-7243 ] ; 2011.
Abstract
There is considerable interest in the development of broadly protective influenza vaccines because of the continuous emergence of antigenic drift variants of seasonal influenza viruses and the threat posed by the emergence of antigenically distinct pandemic influenza viruses. It has been recognized more than three decades ago that influenza A virus-specific cytotoxic T lymphocytes recognize epitopes located in the relatively conserved proteins like the nucleoprotein and that they cross-react with various subtypes of influenza A viruses. This implies that these CD8+ T lymphocytes may contribute to protective heterosubtypic immunity induced by antecedent influenza A virus infections. In the present paper, we review the evidence for the role of virus-specific CD8+ T lymphocytes in protective immunity against influenza virus infections and discuss vaccination strategies that aim at the induction of cross-reactive virus-specific T-cell responses.
Url:
DOI: 10.1155/2011/939860
PubMed: 22007149
PubMed Central: 3189652
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Induction of Virus-Specific Cytotoxic T Lymphocytes as a Basis for the Development of Broadly Protective Influenza Vaccines</title><author><name sortKey="Hillaire, Marine L B" sort="Hillaire, Marine L B" uniqKey="Hillaire M" first="Marine L. B." last="Hillaire">Marine L. B. Hillaire</name><affiliation wicri:level="1"><nlm:aff id="I1">Department of Virology, Erasmus Medical Center, P.O. Box 2040, 3000 CA Rotterdam, The Netherlands</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Department of Virology, Erasmus Medical Center, P.O. Box 2040, 3000 CA Rotterdam</wicri:regionArea><wicri:noRegion>3000 CA Rotterdam</wicri:noRegion></affiliation></author><author><name sortKey="Osterhaus, Albert D M E" sort="Osterhaus, Albert D M E" uniqKey="Osterhaus A" first="Albert D. M. E." last="Osterhaus">Albert D. M. E. Osterhaus</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Rimmelzwaan, Guus F" sort="Rimmelzwaan, Guus F" uniqKey="Rimmelzwaan G" first="Guus F." last="Rimmelzwaan">Guus F. Rimmelzwaan</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22007149</idno><idno type="pmc">3189652</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3189652</idno><idno type="RBID">PMC:3189652</idno><idno type="doi">10.1155/2011/939860</idno><date when="2011">2011</date><idno type="wicri:Area/Pmc/Corpus">000D88</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000D88</idno><idno type="wicri:Area/Pmc/Curation">000D88</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000D88</idno><idno type="wicri:Area/Pmc/Checkpoint">000816</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000816</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Induction of Virus-Specific Cytotoxic T Lymphocytes as a Basis for the Development of Broadly Protective Influenza Vaccines</title><author><name sortKey="Hillaire, Marine L B" sort="Hillaire, Marine L B" uniqKey="Hillaire M" first="Marine L. B." last="Hillaire">Marine L. B. Hillaire</name><affiliation wicri:level="1"><nlm:aff id="I1">Department of Virology, Erasmus Medical Center, P.O. Box 2040, 3000 CA Rotterdam, The Netherlands</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Department of Virology, Erasmus Medical Center, P.O. Box 2040, 3000 CA Rotterdam</wicri:regionArea><wicri:noRegion>3000 CA Rotterdam</wicri:noRegion></affiliation></author><author><name sortKey="Osterhaus, Albert D M E" sort="Osterhaus, Albert D M E" uniqKey="Osterhaus A" first="Albert D. M. E." last="Osterhaus">Albert D. M. E. Osterhaus</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Rimmelzwaan, Guus F" sort="Rimmelzwaan, Guus F" uniqKey="Rimmelzwaan G" first="Guus F." last="Rimmelzwaan">Guus F. Rimmelzwaan</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author></analytic><series><title level="j">Journal of Biomedicine and Biotechnology</title><idno type="ISSN">1110-7243</idno><idno type="eISSN">1110-7251</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>There is considerable interest in the development of broadly protective influenza vaccines because of the continuous emergence of antigenic drift variants of seasonal influenza viruses and the threat posed by the emergence of antigenically distinct pandemic influenza viruses. It has been recognized more than three decades ago that influenza A virus-specific cytotoxic T lymphocytes recognize epitopes located in the relatively conserved proteins like the nucleoprotein and that they cross-react with various subtypes of influenza A viruses. This implies that these CD8<sup>+</sup> T lymphocytes may contribute to protective heterosubtypic immunity induced by antecedent influenza A virus infections. In the present paper, we review the evidence for the role of virus-specific CD8<sup>+</sup> T lymphocytes in protective immunity against influenza virus infections and discuss vaccination strategies that aim at the induction of cross-reactive virus-specific T-cell responses.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="De Jong, Jc" uniqKey="De Jong J">JC de Jong</name></author><author><name sortKey="Palache, Am" uniqKey="Palache A">AM Palache</name></author><author><name sortKey="Beyer, We" uniqKey="Beyer W">WE Beyer</name></author><author><name sortKey="Rimmelzwaan, Gf" uniqKey="Rimmelzwaan G">GF Rimmelzwaan</name></author><author><name sortKey="Boon, Ac" uniqKey="Boon A">AC Boon</name></author><author><name sortKey="Osterhaus, Ad" uniqKey="Osterhaus A">AD Osterhaus</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Abelin, A" uniqKey="Abelin 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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Biomed Biotechnol</journal-id><journal-id journal-id-type="publisher-id">JBB</journal-id><journal-title-group><journal-title>Journal of Biomedicine and Biotechnology</journal-title></journal-title-group><issn pub-type="ppub">1110-7243</issn><issn pub-type="epub">1110-7251</issn><publisher><publisher-name>Hindawi Publishing Corporation</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22007149</article-id><article-id pub-id-type="pmc">3189652</article-id><article-id pub-id-type="doi">10.1155/2011/939860</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review Article</subject></subj-group></article-categories><title-group><article-title>Induction of Virus-Specific Cytotoxic T Lymphocytes as a Basis for the Development of Broadly Protective Influenza Vaccines</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Hillaire</surname><given-names>Marine L. B.</given-names></name><xref ref-type="aff" rid="I1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Osterhaus</surname><given-names>Albert D. M. E.</given-names></name><xref ref-type="aff" rid="I1"><sup>1, 2</sup></xref><xref ref-type="aff" rid="I2"></xref></contrib><contrib contrib-type="author"><name><surname>Rimmelzwaan</surname><given-names>Guus F.</given-names></name><xref ref-type="aff" rid="I1"><sup>1, 2</sup></xref><xref ref-type="aff" rid="I2"></xref><xref ref-type="corresp" rid="cor1">*</xref></contrib></contrib-group><aff id="I1"><sup>1</sup>Department of Virology, Erasmus Medical Center, P.O. Box 2040, 3000 CA Rotterdam, The Netherlands</aff><aff id="I2"><sup>2</sup>Viroclinics Biosciences BV, Parklaan 44, 3016 BC Rotterdam, Rotterdam, The Netherlands</aff><author-notes><corresp id="cor1">*Guus F. Rimmelzwaan: <email>g.rimmelzwaan@erasmusmc.nl</email></corresp><fn fn-type="other"><p>Academic Editor: Zhengguo Xiao</p></fn></author-notes><pub-date pub-type="ppub"><year>2011</year></pub-date><pub-date pub-type="epub"><day>5</day><month>10</month><year>2011</year></pub-date><volume>2011</volume><elocation-id>939860</elocation-id><history><date date-type="received"><day>3</day><month>6</month><year>2011</year></date><date date-type="rev-recd"><day>1</day><month>7</month><year>2011</year></date><date date-type="accepted"><day>2</day><month>8</month><year>2011</year></date></history><permissions><copyright-statement>Copyright © 2011 Marine L. B. Hillaire et al.</copyright-statement><copyright-year>2011</copyright-year><license license-type="open-access"><license-p>This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><abstract><p>There is considerable interest in the development of broadly protective influenza vaccines because of the continuous emergence of antigenic drift variants of seasonal influenza viruses and the threat posed by the emergence of antigenically distinct pandemic influenza viruses. It has been recognized more than three decades ago that influenza A virus-specific cytotoxic T lymphocytes recognize epitopes located in the relatively conserved proteins like the nucleoprotein and that they cross-react with various subtypes of influenza A viruses. This implies that these CD8<sup>+</sup> T lymphocytes may contribute to protective heterosubtypic immunity induced by antecedent influenza A virus infections. In the present paper, we review the evidence for the role of virus-specific CD8<sup>+</sup> T lymphocytes in protective immunity against influenza virus infections and discuss vaccination strategies that aim at the induction of cross-reactive virus-specific T-cell responses.</p></abstract></article-meta></front><floats-group><table-wrap id="tab1" position="float"><label>Table 1</label><caption><p>Evidence for cross-reactivity of influenza virus-specific CTL.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" colspan="2" rowspan="1">Subtype</th><th align="left" rowspan="1" colspan="1"></th><th align="left" rowspan="2" colspan="1">Comments</th><th align="center" rowspan="2" colspan="1">Ref.</th></tr><tr><th align="left" rowspan="1" colspan="1">Priming subtype</th><th align="center" rowspan="1" colspan="1">Cross-reaction with</th><th align="left" rowspan="1" colspan="1">Species</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">H2N1</td><td align="center" rowspan="1" colspan="1">H3N2</td><td align="left" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Cross-reactivity confirmed in Cr-release assays using cultured splenocytes of primed mice</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B34">28</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">H2N2<break></break>H3N2</td><td align="left" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Cross-reactivity confirmed in Cr-release assays using splenocytes of primed mice</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B24">24</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="left" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Target cells expressing NP from H1N1 recognized by cultured splenocytes from primed mice</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B32">29</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="left" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Cross-reactive cultured splenocytes recognize inner proteins of influenza A virus</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B155">30</xref>] </td></tr><tr><td align="center" colspan="5" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="left" rowspan="1" colspan="1">Human</td><td align="left" rowspan="1" colspan="1">Cross-reactive CTLs recognize NP, M1, or PB2</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B31">31</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">Seasonal influenza</td><td align="center" rowspan="1" colspan="1">H5N1</td><td align="left" rowspan="1" colspan="1">Human</td><td align="left" rowspan="1" colspan="1">Cross-reactive CTLs were detected in the blood of healthy human subjects not exposed to H5N1 virus</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B35">32</xref>–<xref ref-type="bibr" rid="B37">34</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">pH1N1</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="left" rowspan="1" colspan="1">Human</td><td align="left" rowspan="1" colspan="1">T cells specific for the NP418 epitope induced by the 2009 pH1N1 cross-react with the 1918-H1N1 variant but not with contemporary variants</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B40">35</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">Seasonal influenza</td><td align="center" rowspan="1" colspan="1">2009 pH1N1</td><td align="left" rowspan="1" colspan="1">Human</td><td align="left" rowspan="1" colspan="1">Cross-reactive CTLs were detected in the blood of healthy human subjects not exposed to 2009 pH1N1 virus</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B39">36</xref>]</td></tr></tbody></table></table-wrap><table-wrap id="tab2" position="float"><label>Table 2</label><caption><p>Evidence for a role of CTLs in cross-protective immunity against influenza virus infections.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" colspan="2" rowspan="1">Subtype used</th><th align="center" rowspan="1" colspan="1"></th><th align="left" rowspan="1" colspan="1"></th><th align="left" rowspan="1" colspan="1"></th><th align="center" rowspan="1" colspan="1"></th></tr><tr><th align="left" rowspan="1" colspan="1">Priming</th><th align="center" rowspan="1" colspan="1">Challenge</th><th align="center" rowspan="1" colspan="1">Species</th><th align="left" rowspan="1" colspan="1">Experiment</th><th align="left" rowspan="1" colspan="1">Comments</th><th align="center" rowspan="1" colspan="1">Ref</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Adoptive transfer</td><td align="left" rowspan="1" colspan="1">Splenocytes depleted from CD8<sup>+</sup> T cells failed to protect against infection.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B25">25</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H1N1 or H3N2</td><td align="center" rowspan="1" colspan="1">H1N1 or H3N2</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Adoptive transfer</td><td align="left" rowspan="1" colspan="1">T cells afford protection against infection with heterosubtypic strain.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B50">48</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">Nude mouse</td><td align="left" rowspan="1" colspan="1">Adoptive transfer</td><td align="left" rowspan="1" colspan="1">Immune spleen cells from Balb-c mice mediated more rapid clearance of virus infection and correlated with cytolytic activity.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B47">49</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H1N1 <break></break>H3N2<break></break>H2N2</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Adoptive transfer</td><td align="left" rowspan="1" colspan="1">Mouse NP-specific CTL clone afforded protection.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B49">50</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">NP from H3N2</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">NP priming promoted recovery and was attributed to cross-reactive CTLs.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B156">51</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H2N2</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Adoptive transfer</td><td align="left" rowspan="1" colspan="1">Cross-reactive CTL clones conferred protection.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B48">52</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Adoptive transfer</td><td align="left" rowspan="1" colspan="1">NP-specific CTL clone reduced lung virus titers and mortality rates.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B157">53</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Depletion of T cells</td><td align="left" rowspan="1" colspan="1">CTLs conferred heterosubtypic immunity and reduced virus titers in the respiratory tract.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B53">54</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Protection correlated with CTL response.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B44">45</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H9N2</td><td align="center" rowspan="1" colspan="1">H5N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Protection correlated with CTL response to NP or PB2.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B45">46</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">H2N2</td><td align="center" rowspan="1" colspan="1">Mice KO for Ig or <italic>γ</italic>/<italic>δ</italic> T cells</td><td align="left" rowspan="1" colspan="1">Acute depletion of CD8<sup>+</sup> T cells</td><td align="left" rowspan="1" colspan="1">In absence of Ig or <italic>γ</italic>/<italic>δ</italic> T cells, CTLs conferred protection.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B43">44</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Protection correlated with CTL response to NP.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B42">43</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H5N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Protection correlated with CTL response to NP and PA.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B41">42</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">Gamma-irradiated viruses</td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Adoptive transfer of CD8<sup>+</sup> T cells</td><td align="left" rowspan="1" colspan="1">CTL but not B cells afforded protection.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B39">36</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">2009 pH1N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Depletion of CD8<sup>+</sup> T cells</td><td align="left" rowspan="1" colspan="1">CTL conferred heterosubtypic immunity to 2009 pH1N1 virus.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B52">55</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">2009 pH1N1</td><td align="center" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Adoptive transfer of CD8<sup>+</sup> and CD4<sup>+</sup> T cells</td><td align="left" rowspan="1" colspan="1">CTL conferred heterosubtypic immunity to 2009 pH1N1 virus.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B22">22</xref>] </td></tr><tr><td align="center" colspan="6" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">H9N2</td><td align="center" rowspan="1" colspan="1">H5N1</td><td align="center" rowspan="1" colspan="1">Chicken</td><td align="left" rowspan="1" colspan="1">Adoptive transfer of CD8<sup>+</sup> T cells</td><td align="left" rowspan="1" colspan="1">CTLs reduced mortality rates.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B51">56</xref>]</td></tr><tr><td align="left" rowspan="1" colspan="1">H9N2</td><td align="center" rowspan="1" colspan="1">H5N1</td><td align="center" rowspan="1" colspan="1">Chicken</td><td align="left" rowspan="1" colspan="1">Depletion</td><td align="left" rowspan="1" colspan="1">CTLs reduced mortality rates.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B55">57</xref>] </td></tr><tr><td align="center" colspan="6" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">H3N2</td><td align="center" rowspan="1" colspan="1">H5N1</td><td align="center" rowspan="1" colspan="1">Ferret</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Protection correlated with CTL response.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B158">58</xref>] </td></tr><tr><td align="center" colspan="6" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1">H1N1</td><td align="center" rowspan="1" colspan="1">Human</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">CTL activity correlated with protection in absence of antibodies.</td><td align="center" rowspan="1" colspan="1">[<xref ref-type="bibr" rid="B28">37</xref>]</td></tr></tbody></table></table-wrap></floats-group></pmc><affiliations><list><country><li>Pays-Bas</li></country></list><tree><noCountry><name sortKey="Osterhaus, Albert D M E" sort="Osterhaus, Albert D M E" uniqKey="Osterhaus A" first="Albert D. 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