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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Differential Recognition of Influenza A Viruses by M1<sub>58–66</sub>
Epitope-Specific CD8<sup>+</sup>
T Cells Is Determined by Extraepitopic Amino Acid Residues</title>
<author><name sortKey="Van De Sandt, Carolien E" sort="Van De Sandt, Carolien E" uniqKey="Van De Sandt C" first="Carolien E." last="Van De Sandt">Carolien E. Van De Sandt</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kreijtz, Joost H C M" sort="Kreijtz, Joost H C M" uniqKey="Kreijtz J" first="Joost H. C. M." last="Kreijtz">Joost H. C. M. Kreijtz</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Geelhoed Mieras, Martina M" sort="Geelhoed Mieras, Martina M" uniqKey="Geelhoed Mieras M" first="Martina M." last="Geelhoed-Mieras">Martina M. Geelhoed-Mieras</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Nieuwkoop, Nella J" sort="Nieuwkoop, Nella J" uniqKey="Nieuwkoop N" first="Nella J." last="Nieuwkoop">Nella J. Nieuwkoop</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Spronken, Monique I" sort="Spronken, Monique I" uniqKey="Spronken M" first="Monique I." last="Spronken">Monique I. Spronken</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Van De Vijver, David A M C" sort="Van De Vijver, David A M C" uniqKey="Van De Vijver D" first="David A. M. C." last="Van De Vijver">David A. M. C. Van De Vijver</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fouchier, Ron A M" sort="Fouchier, Ron A M" uniqKey="Fouchier R" first="Ron A. M." last="Fouchier">Ron A. M. Fouchier</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</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 id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">ViroClinics Biosciences BV, Rotterdam, The Netherlands</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 id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">ViroClinics Biosciences BV, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">26537686</idno>
<idno type="pmc">4702701</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4702701</idno>
<idno type="RBID">PMC:4702701</idno>
<idno type="doi">10.1128/JVI.02439-15</idno>
<date when="2015">2015</date>
<idno type="wicri:Area/Pmc/Corpus">000025</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000025</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Differential Recognition of Influenza A Viruses by M1<sub>58–66</sub>
Epitope-Specific CD8<sup>+</sup>
T Cells Is Determined by Extraepitopic Amino Acid Residues</title>
<author><name sortKey="Van De Sandt, Carolien E" sort="Van De Sandt, Carolien E" uniqKey="Van De Sandt C" first="Carolien E." last="Van De Sandt">Carolien E. Van De Sandt</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kreijtz, Joost H C M" sort="Kreijtz, Joost H C M" uniqKey="Kreijtz J" first="Joost H. C. M." last="Kreijtz">Joost H. C. M. Kreijtz</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Geelhoed Mieras, Martina M" sort="Geelhoed Mieras, Martina M" uniqKey="Geelhoed Mieras M" first="Martina M." last="Geelhoed-Mieras">Martina M. Geelhoed-Mieras</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Nieuwkoop, Nella J" sort="Nieuwkoop, Nella J" uniqKey="Nieuwkoop N" first="Nella J." last="Nieuwkoop">Nella J. Nieuwkoop</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Spronken, Monique I" sort="Spronken, Monique I" uniqKey="Spronken M" first="Monique I." last="Spronken">Monique I. Spronken</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Van De Vijver, David A M C" sort="Van De Vijver, David A M C" uniqKey="Van De Vijver D" first="David A. M. C." last="Van De Vijver">David A. M. C. Van De Vijver</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fouchier, Ron A M" sort="Fouchier, Ron A M" uniqKey="Fouchier R" first="Ron A. M." last="Fouchier">Ron A. M. Fouchier</name>
<affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</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 id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">ViroClinics Biosciences BV, Rotterdam, The Netherlands</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 id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">ViroClinics Biosciences BV, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
<idno type="eISSN">1098-5514</idno>
<imprint><date when="2015">2015</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>Natural influenza A virus infections elicit both virus-specific antibody and CD4<sup>+</sup>
and CD8<sup>+</sup>
T cell responses. Influenza A virus-specific CD8<sup>+</sup>
cytotoxic T lymphocytes (CTLs) contribute to clearance of influenza virus infections. Viral CTL epitopes can display variation, allowing influenza A viruses to evade recognition by epitope-specific CTLs. Due to functional constraints, some epitopes, like the immunodominant HLA-A*0201-restricted matrix protein 1 (M1<sub>58–66</sub>
) epitope, are highly conserved between influenza A viruses regardless of their subtype or host species of origin. We hypothesized that human influenza A viruses evade recognition of this epitope by impairing antigen processing and presentation by extraepitopic amino acid substitutions. Activation of specific T cells was used as an indication of antigen presentation. Here, we show that the M1<sub>58–66</sub>
epitope in the M1 protein derived from human influenza A virus was poorly recognized compared to the M1 protein derived from avian influenza A virus. Furthermore, we demonstrate that naturally occurring variations at extraepitopic amino acid residues affect CD8<sup>+</sup>
T cell recognition of the M1<sub>58–66</sub>
epitope. These data indicate that human influenza A viruses can impair recognition by M1<sub>58–66</sub>
-specific CTLs while retaining the conserved amino acid sequence of the epitope, which may represent a yet-unknown immune evasion strategy for influenza A viruses. This difference in recognition may have implications for the viral replication kinetics in HLA-A*0201 individuals and spread of influenza A viruses in the human population. The findings may aid the rational design of universal influenza vaccines that aim at the induction of cross-reactive virus-specific CTL responses.
</p>
<p><bold>IMPORTANCE</bold>
Influenza viruses are an important cause of acute respiratory tract infections. Natural influenza A virus infections elicit both humoral and cellular immunity. CD8<sup>+</sup>
cytotoxic T lymphocytes (CTLs) are directed predominantly against conserved internal proteins and confer cross-protection, even against influenza A viruses of various subtypes. In some CTL epitopes, mutations occur that allow influenza A viruses to evade recognition by CTLs. However, the immunodominant HLA-A*0201-restricted M1<sub>58–66</sub>
epitope does not tolerate mutations without loss of viral fitness. Here, we describe naturally occurring variations in amino acid residues outside the M1<sub>58–66</sub>
epitope that influence the recognition of the epitope. These results provide novel insights into the epidemiology of influenza A viruses and their pathogenicity and may aid rational design of vaccines that aim at the induction of CTL responses.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Virol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Virol</journal-id>
<journal-id journal-id-type="hwp">jvi</journal-id>
<journal-id journal-id-type="pmc">jvi</journal-id>
<journal-id journal-id-type="publisher-id">JVI</journal-id>
<journal-title-group><journal-title>Journal of Virology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-538X</issn>
<issn pub-type="epub">1098-5514</issn>
<publisher><publisher-name>American Society for Microbiology</publisher-name>
<publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26537686</article-id>
<article-id pub-id-type="pmc">4702701</article-id>
<article-id pub-id-type="publisher-id">02439-15</article-id>
<article-id pub-id-type="doi">10.1128/JVI.02439-15</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Pathogenesis and Immunity</subject>
</subj-group>
</article-categories>
<title-group><article-title>Differential Recognition of Influenza A Viruses by M1<sub>58–66</sub>
Epitope-Specific CD8<sup>+</sup>
T Cells Is Determined by Extraepitopic Amino Acid Residues</article-title>
<alt-title alt-title-type="running-head">Extraepitopic Residues Influence IAV CTL Recognition</alt-title>
<alt-title alt-title-type="short-authors">van de Sandt et al.</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>van de Sandt</surname>
<given-names>Carolien E.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kreijtz</surname>
<given-names>Joost H. C. M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Geelhoed-Mieras</surname>
<given-names>Martina M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nieuwkoop</surname>
<given-names>Nella J.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Spronken</surname>
<given-names>Monique I.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>van de Vijver</surname>
<given-names>David A. M. C.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fouchier</surname>
<given-names>Ron A. M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</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="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">*</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Rimmelzwaan</surname>
<given-names>Guus F.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<aff id="aff1"><label>a</label>
Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</aff>
<aff id="aff2"><label>b</label>
ViroClinics Biosciences BV, Rotterdam, The Netherlands</aff>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Schultz-Cherry</surname>
<given-names>S.</given-names>
</name>
<role>Editor</role>
</contrib>
</contrib-group>
<author-notes><corresp id="cor1">Address correspondence to Guus F. Rimmelzwaan, <email>g.rimmelzwaan@erasmusmc.nl</email>
.</corresp>
<fn id="fn1" fn-type="present-address"><label>*</label>
<p>Present address: Joost H. C. M. Kreijtz, BioNovion, Oss, The Netherlands; Albert D. M. E. Osterhaus, Research Center for Emerging Infections and Zoonoses, University of Veterinary Medicine, Hannover, Germany, and Artemis One Health Research Foundation, Utrecht, The Netherlands.</p>
</fn>
<fn fn-type="other"><p><bold>Citation</bold>
van de Sandt CE, Kreijtz JHCM, Geelhoed-Mieras MM, Nieuwkoop NJ, Spronken MI, van de Vijver DAMC, Fouchier RAM, Osterhaus ADME, Rimmelzwaan GF. 2016. Differential recognition of influenza A viruses by M1<sub>58–66</sub>
epitope-specific CD8<sup>+</sup>
T cells is determined by extraepitopic amino acid residues. J Virol 90:1009–1022. doi:<ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.1128/JVI.02439-15">10.1128/JVI.02439-15</ext-link>
.</p>
</fn>
</author-notes>
<pub-date pub-type="epreprint"><day>4</day>
<month>11</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><day>15</day>
<month>1</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>30</day>
<month>12</month>
<year>2015</year>
</pub-date>
<volume>90</volume>
<issue>2</issue>
<fpage>1009</fpage>
<lpage>1022</lpage>
<history><date date-type="received"><day>22</day>
<month>9</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>29</day>
<month>10</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2015, American Society for Microbiology. All Rights Reserved.</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
</permissions>
<self-uri content-type="pdf" xlink:href="zjv00216001009.pdf"></self-uri>
<abstract><title>ABSTRACT</title>
<p>Natural influenza A virus infections elicit both virus-specific antibody and CD4<sup>+</sup>
and CD8<sup>+</sup>
T cell responses. Influenza A virus-specific CD8<sup>+</sup>
cytotoxic T lymphocytes (CTLs) contribute to clearance of influenza virus infections. Viral CTL epitopes can display variation, allowing influenza A viruses to evade recognition by epitope-specific CTLs. Due to functional constraints, some epitopes, like the immunodominant HLA-A*0201-restricted matrix protein 1 (M1<sub>58–66</sub>
) epitope, are highly conserved between influenza A viruses regardless of their subtype or host species of origin. We hypothesized that human influenza A viruses evade recognition of this epitope by impairing antigen processing and presentation by extraepitopic amino acid substitutions. Activation of specific T cells was used as an indication of antigen presentation. Here, we show that the M1<sub>58–66</sub>
epitope in the M1 protein derived from human influenza A virus was poorly recognized compared to the M1 protein derived from avian influenza A virus. Furthermore, we demonstrate that naturally occurring variations at extraepitopic amino acid residues affect CD8<sup>+</sup>
T cell recognition of the M1<sub>58–66</sub>
epitope. These data indicate that human influenza A viruses can impair recognition by M1<sub>58–66</sub>
-specific CTLs while retaining the conserved amino acid sequence of the epitope, which may represent a yet-unknown immune evasion strategy for influenza A viruses. This difference in recognition may have implications for the viral replication kinetics in HLA-A*0201 individuals and spread of influenza A viruses in the human population. The findings may aid the rational design of universal influenza vaccines that aim at the induction of cross-reactive virus-specific CTL responses.
</p>
<p><bold>IMPORTANCE</bold>
Influenza viruses are an important cause of acute respiratory tract infections. Natural influenza A virus infections elicit both humoral and cellular immunity. CD8<sup>+</sup>
cytotoxic T lymphocytes (CTLs) are directed predominantly against conserved internal proteins and confer cross-protection, even against influenza A viruses of various subtypes. In some CTL epitopes, mutations occur that allow influenza A viruses to evade recognition by CTLs. However, the immunodominant HLA-A*0201-restricted M1<sub>58–66</sub>
epitope does not tolerate mutations without loss of viral fitness. Here, we describe naturally occurring variations in amino acid residues outside the M1<sub>58–66</sub>
epitope that influence the recognition of the epitope. These results provide novel insights into the epidemiology of influenza A viruses and their pathogenicity and may aid rational design of vaccines that aim at the induction of CTL responses.</p>
</abstract>
<funding-group><award-group id="award1"><funding-source id="gs1">EU FLUNIVAC</funding-source>
<award-id rid="gs1">602604</award-id>
<principal-award-recipient>Guus F. Rimmelzwaan</principal-award-recipient>
</award-group>
<award-group id="award2"><funding-source id="gs2">HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID)</funding-source>
<award-id rid="gs2">HHSN272201400008C</award-id>
<principal-award-recipient>Monique I. J. Spronken</principal-award-recipient>
<principal-award-recipient>Ron A. M. Fouchier</principal-award-recipient>
</award-group>
</funding-group>
<counts><fig-count count="7"></fig-count>
<table-count count="1"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="75"></ref-count>
<page-count count="14"></page-count>
<word-count count="10803"></word-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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