Back to the Future for Influenza Preimmunity—Looking Back at Influenza Virus History to Infer the Outcome of Future Infections
Identifieur interne : 000E39 ( Pmc/Curation ); précédent : 000E38; suivant : 000E40Back to the Future for Influenza Preimmunity—Looking Back at Influenza Virus History to Infer the Outcome of Future Infections
Auteurs : Magen Ellen Francis ; Morgan Leslie King ; Alyson Ann Kelvin [Canada]Source :
- Viruses [ 1999-4915 ] ; 2019.
Abstract
The influenza virus-host interaction is a classic arms race. The recurrent and evolving nature of the influenza virus family allows a single host to be infected several times. Locked in co-evolution, recurrent influenza virus infection elicits continual refinement of the host immune system. Here we give historical context of circulating influenza viruses to understand how the individual immune history is mirrored by the history of influenza virus circulation.
Url:
DOI: 10.3390/v11020122
PubMed: 30704019
PubMed Central: 6410066
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Back to the Future for Influenza Preimmunity—Looking Back at Influenza Virus History to Infer the Outcome of Future Infections</title><author><name sortKey="Francis, Magen Ellen" sort="Francis, Magen Ellen" uniqKey="Francis M" first="Magen Ellen" last="Francis">Magen Ellen Francis</name><affiliation><nlm:aff id="af1-viruses-11-00122">Department of Microbiology and Immunology, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada;<email>M.Francis@dal.ca</email> (M.E.F.);<email>MorganKing@dal.ca</email> (M.L.K.)</nlm:aff></affiliation></author><author><name sortKey="King, Morgan Leslie" sort="King, Morgan Leslie" uniqKey="King M" first="Morgan Leslie" last="King">Morgan Leslie King</name><affiliation><nlm:aff id="af1-viruses-11-00122">Department of Microbiology and Immunology, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada;<email>M.Francis@dal.ca</email> (M.E.F.);<email>MorganKing@dal.ca</email> (M.L.K.)</nlm:aff></affiliation></author><author><name sortKey="Kelvin, Alyson Ann" sort="Kelvin, Alyson Ann" uniqKey="Kelvin A" first="Alyson Ann" last="Kelvin">Alyson Ann Kelvin</name><affiliation><nlm:aff id="af1-viruses-11-00122">Department of Microbiology and Immunology, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada;<email>M.Francis@dal.ca</email> (M.E.F.);<email>MorganKing@dal.ca</email> (M.L.K.)</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-viruses-11-00122">Department of Pediatrics, Division of Infectious Disease, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada</nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Pediatrics, Division of Infectious Disease, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="af3-viruses-11-00122">Canadian Centre for Vaccinology, IWK Health Centre, Halifax NS B3K 6R8, Canada</nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea>Canadian Centre for Vaccinology, IWK Health Centre, Halifax NS B3K 6R8</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">30704019</idno><idno type="pmc">6410066</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6410066</idno><idno type="RBID">PMC:6410066</idno><idno type="doi">10.3390/v11020122</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000E39</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000E39</idno><idno type="wicri:Area/Pmc/Curation">000E39</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000E39</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Back to the Future for Influenza Preimmunity—Looking Back at Influenza Virus History to Infer the Outcome of Future Infections</title><author><name sortKey="Francis, Magen Ellen" sort="Francis, Magen Ellen" uniqKey="Francis M" first="Magen Ellen" last="Francis">Magen Ellen Francis</name><affiliation><nlm:aff id="af1-viruses-11-00122">Department of Microbiology and Immunology, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada;<email>M.Francis@dal.ca</email> (M.E.F.);<email>MorganKing@dal.ca</email> (M.L.K.)</nlm:aff></affiliation></author><author><name sortKey="King, Morgan Leslie" sort="King, Morgan Leslie" uniqKey="King M" first="Morgan Leslie" last="King">Morgan Leslie King</name><affiliation><nlm:aff id="af1-viruses-11-00122">Department of Microbiology and Immunology, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada;<email>M.Francis@dal.ca</email> (M.E.F.);<email>MorganKing@dal.ca</email> (M.L.K.)</nlm:aff></affiliation></author><author><name sortKey="Kelvin, Alyson Ann" sort="Kelvin, Alyson Ann" uniqKey="Kelvin A" first="Alyson Ann" last="Kelvin">Alyson Ann Kelvin</name><affiliation><nlm:aff id="af1-viruses-11-00122">Department of Microbiology and Immunology, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada;<email>M.Francis@dal.ca</email> (M.E.F.);<email>MorganKing@dal.ca</email> (M.L.K.)</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-viruses-11-00122">Department of Pediatrics, Division of Infectious Disease, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada</nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Pediatrics, Division of Infectious Disease, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="af3-viruses-11-00122">Canadian Centre for Vaccinology, IWK Health Centre, Halifax NS B3K 6R8, Canada</nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea>Canadian Centre for Vaccinology, IWK Health Centre, Halifax NS B3K 6R8</wicri:regionArea></affiliation></author></analytic><series><title level="j">Viruses</title><idno type="eISSN">1999-4915</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The influenza virus-host interaction is a classic arms race. The recurrent and evolving nature of the influenza virus family allows a single host to be infected several times. Locked in co-evolution, recurrent influenza virus infection elicits continual refinement of the host immune system. Here we give historical context of circulating influenza viruses to understand how the individual immune history is mirrored by the history of influenza virus circulation. <italic>Original Antigenic Sin</italic> was first proposed as the negative influence of the host’s first influenza virus infection on the next and <italic>Imprinting</italic> modernizes <italic>Antigenic Sin</italic> incorporating both positive and negative outcomes. Building on imprinting, we refer to <italic>preimmunity</italic> as the continual refinement of the host immune system with each influenza virus infection. We discuss imprinting and the interplay of influenza virus homology, vaccination, and host age establishing preimmunity. We outline host signatures and outcomes of tandem infection according to the sequence of virus and classify these relationships as monosubtypic homologous, monosubtypic heterologous, heterosubtypic, or heterotypic sequential infections. Finally, the preimmunity knowledge gaps are highlighted for future investigation. Understanding the effects of antigenic variable recurrent influenza virus infection on immune refinement will advance vaccination strategies, as well as pandemic preparedness.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Kilbourne, E D" uniqKey="Kilbourne E">E.D. Kilbourne</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Saunders Hastings, P R" uniqKey="Saunders Hastings P">P.R. Saunders-Hastings</name></author><author><name sortKey="Krewski, D" uniqKey="Krewski D">D. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Viruses</journal-id><journal-id journal-id-type="iso-abbrev">Viruses</journal-id><journal-id journal-id-type="publisher-id">viruses</journal-id><journal-title-group><journal-title>Viruses</journal-title></journal-title-group><issn pub-type="epub">1999-4915</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30704019</article-id><article-id pub-id-type="pmc">6410066</article-id><article-id pub-id-type="doi">10.3390/v11020122</article-id><article-id pub-id-type="publisher-id">viruses-11-00122</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Back to the Future for Influenza Preimmunity—Looking Back at Influenza Virus History to Infer the Outcome of Future Infections</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Francis</surname><given-names>Magen Ellen</given-names></name><xref ref-type="aff" rid="af1-viruses-11-00122">1</xref></contrib><contrib contrib-type="author"><name><surname>King</surname><given-names>Morgan Leslie</given-names></name><xref ref-type="aff" rid="af1-viruses-11-00122">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-0940-0847</contrib-id><name><surname>Kelvin</surname><given-names>Alyson Ann</given-names></name><xref ref-type="aff" rid="af1-viruses-11-00122">1</xref><xref ref-type="aff" rid="af2-viruses-11-00122">2</xref><xref ref-type="aff" rid="af3-viruses-11-00122">3</xref><xref rid="c1-viruses-11-00122" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-viruses-11-00122"><label>1</label>Department of Microbiology and Immunology, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada;<email>M.Francis@dal.ca</email> (M.E.F.);<email>MorganKing@dal.ca</email> (M.L.K.)</aff><aff id="af2-viruses-11-00122"><label>2</label>Department of Pediatrics, Division of Infectious Disease, Faculty of Medicine, Dalhousie University, Halifax, NS B3K 6R8, Canada</aff><aff id="af3-viruses-11-00122"><label>3</label>Canadian Centre for Vaccinology, IWK Health Centre, Halifax NS B3K 6R8, Canada</aff><author-notes><corresp id="c1-viruses-11-00122"><label>*</label>Correspondence: <email>akelvin@dal.ca</email>; Tel.: +1-902-470-2760</corresp></author-notes><pub-date pub-type="epub"><day>30</day><month>1</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>2</month><year>2019</year></pub-date><volume>11</volume><issue>2</issue><elocation-id>122</elocation-id><history><date date-type="received"><day>21</day><month>12</month><year>2018</year></date><date date-type="accepted"><day>22</day><month>1</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 by the authors.</copyright-statement><copyright-year>2019</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>).</license-p></license></permissions><abstract><p>The influenza virus-host interaction is a classic arms race. The recurrent and evolving nature of the influenza virus family allows a single host to be infected several times. Locked in co-evolution, recurrent influenza virus infection elicits continual refinement of the host immune system. Here we give historical context of circulating influenza viruses to understand how the individual immune history is mirrored by the history of influenza virus circulation. <italic>Original Antigenic Sin</italic> was first proposed as the negative influence of the host’s first influenza virus infection on the next and <italic>Imprinting</italic> modernizes <italic>Antigenic Sin</italic> incorporating both positive and negative outcomes. Building on imprinting, we refer to <italic>preimmunity</italic> as the continual refinement of the host immune system with each influenza virus infection. We discuss imprinting and the interplay of influenza virus homology, vaccination, and host age establishing preimmunity. We outline host signatures and outcomes of tandem infection according to the sequence of virus and classify these relationships as monosubtypic homologous, monosubtypic heterologous, heterosubtypic, or heterotypic sequential infections. Finally, the preimmunity knowledge gaps are highlighted for future investigation. Understanding the effects of antigenic variable recurrent influenza virus infection on immune refinement will advance vaccination strategies, as well as pandemic preparedness.</p></abstract><kwd-group><kwd>immune response</kwd><kwd>original antigenic sin</kwd><kwd>imprinting</kwd><kwd>preimmunity</kwd><kwd>influenza virus</kwd><kwd>antigenic drift</kwd><kwd>antigenic shift</kwd><kwd>orthomyxoviridae</kwd><kwd>Spanish influenza</kwd><kwd>pandemic</kwd></kwd-group></article-meta></front><floats-group><fig id="viruses-11-00122-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Influenza immune background development following recurrent infections and vaccinations. The schematic illustrates possible immune fluctuations following influenza virus infection or vaccination. Immune fluctuations and potential protection can be conceptualized at both the individual or population level. The heterogeneity of the immune background is dependent on the sequence of virus exposures and their genetic and antigenic relatedness. Immune specificity that is gained during influenza virus immune imprinting during infancy or childhood leading to the generation of virus-specific T and B cells are retained at some level throughout life. T = T cell; B = B cells; Y = antibodies.</p></caption><graphic xlink:href="viruses-11-00122-g001"></graphic></fig><fig id="viruses-11-00122-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Schematic of Influenza A, B, and C virus structure. Influenza A is defined by its surface proteins hemagglutinin (HA) and neuraminidase (NA) of which there are 18 HA and 11 NA. Influenza B viruses are categorized into two lineages (B/Yamagata and B/Victoria). The surface of both A and B viruses contains HA, NA, and the M2 proteins. Internally, A and B viruses both have eight genomic segments. Influenza C viruses have only one external spike protein (HEF) which functions both in viral entry and egress and an ion channel M2 protein. Type C viruses have 7 internal genomic segments. M1 protein line the envelope internally adjacent nuclear export protein (NEP) proteins for type A, B, and C viruses. The genomic segments are encapsidated by the NP protein and form the ribonucleocapsid with the polymerase proteins Polymerase acidic (PA), Polymerase basic 1 (PB1), and Polymerase basic 2 (PB2).</p></caption><graphic xlink:href="viruses-11-00122-g002"></graphic></fig><fig id="viruses-11-00122-f003" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Timeline of the history of influenza virus circulation in humans since 1890s. The timeline shows the history of influenza virus type A and B circulation since 1890. There have been 6 presumptive pandemics in this time period. The Russian pandemic of ~1891 occurred prior to the discovery of the influenza virus and is known only by historical medical records. Seroarcheology has suggested that this outbreak was caused by an H3N8 virus. In 1918 what was known as the Spanish Influenza Pandemic took place. The H1N1 virus which had caused the pandemic was not definitively identified until lung samples from victims of the pandemic were sequenced in 2005. It is estimated that 50 to 100 million deaths were caused by this virus. H1N1 viruses circulated until 1957 when H1N1 was replaced with an H2N2 pandemic virus during the Asian pandemic. The H2N2 virus was replaced with H3N2 during the 1968 Hong Kong pandemic. In 1977, H1N1 resurfaced and since then, H1N1 and H3N2 have co-circulated. In 2009, the emergence of an H1N1 strain of swine origin replaced the former seasonal H1N1 virus ‘lineage’ which was in circulation from the 1977 lineage. In addition to circulating seasonal influenza viruses, avian virus spillover events also lead to human infection. Major avian virus spillover events occurred in 1997 and 2013 for the influenza A viruses H5N1 and H7N9, respectively. During this time period, influenza B viruses have also co-circulated in humans. *Image credit CDC for the 1918 pandemic and the influenza virion [<xref rid="B79-viruses-11-00122" ref-type="bibr">79</xref>].</p></caption><graphic xlink:href="viruses-11-00122-g003"></graphic></fig><fig id="viruses-11-00122-f004" orientation="portrait" position="float"><label>Figure 4</label><caption><p>Influenza immune imprinting and the history of circulating influenza viruses. The timeline illustrates the relationship between virus circulation and influenza virus immune imprinting at infancy. Several published studies have shown that antibodies reactive toward the imprinting virus can last throughout the host’s lifetime. Human studies investigating imprinting serology, epidemiology, or cell reactivity are noted in the figure for the time period of imprinting. The author’s last name and publication date are given. The date in parentheses refers to study subjects’ date of birth if it is not easily deduced from the timeline.</p></caption><graphic xlink:href="viruses-11-00122-g004"></graphic></fig><table-wrap id="viruses-11-00122-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">viruses-11-00122-t001_Table 1</object-id><label>Table 1</label><caption><p>Influenza virus relationships of sequential infection.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Infection Relationship</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Example Sequence</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Example Strain 1</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Example Strain 2</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1"><bold>Monosubtypic Homologous</bold></td><td align="center" valign="middle" rowspan="1" colspan="1">sH1N1 -> sH1N1</td><td align="center" valign="middle" rowspan="1" colspan="1">A/Brisbane/59/2007</td><td align="center" valign="middle" rowspan="1" colspan="1">A/Brisbane/59/2007</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><bold>Monosubtypic Heterologous</bold></td><td align="center" valign="middle" rowspan="1" colspan="1">sH1N1 -> 2009 H1N1</td><td align="center" valign="middle" rowspan="1" colspan="1">A/Brisbane/59/2007</td><td align="center" valign="middle" rowspan="1" colspan="1">A/California/07/2009</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><bold>Heterosubtypic</bold></td><td align="center" valign="middle" rowspan="1" colspan="1">sH1N1 -> H3N2</td><td align="center" valign="middle" rowspan="1" colspan="1">A/FortMonmouth/1/1947</td><td align="center" valign="middle" rowspan="1" colspan="1">A/HongKong/1/1968</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><bold>Heterotypic</bold></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">sH1N1 -> B-V virus</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A/Brisbane/59/2007</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">B/Brisbane/60/2008</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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