Comparison of Antiviral Activity between IgA and IgG Specific to Influenza Virus Hemagglutinin: Increased Potential of IgA for Heterosubtypic Immunity
Identifieur interne : 000522 ( Pmc/Checkpoint ); précédent : 000521; suivant : 000523Comparison of Antiviral Activity between IgA and IgG Specific to Influenza Virus Hemagglutinin: Increased Potential of IgA for Heterosubtypic Immunity
Auteurs : Mieko Muramatsu [Japon] ; Reiko Yoshida [Japon] ; Ayaka Yokoyama [Japon] ; Hiroko Miyamoto [Japon] ; Masahiro Kajihara [Japon] ; Junki Maruyama [Japon] ; Naganori Nao [Japon] ; Rashid Manzoor [Japon] ; Ayato Takada [Japon, Zambie]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
Both IgA and IgG antibodies are known to play important roles in protection against influenza virus infection. While IgG is the major isotype induced systemically, IgA is predominant in mucosal tissues, including the upper respiratory tract. Although IgA antibodies are believed to have unique advantages in mucosal immunity, information on direct comparisons of the in vitro antiviral activities of IgA and IgG antibodies recognizing the same epitope is limited. In this study, we demonstrate differences in antiviral activities between these isotypes using monoclonal IgA and IgG antibodies obtained from hybridomas of the same origin. Polymeric IgA-producing hybridoma cells were successfully subcloned from those originally producing monoclonal antibody S139/1, a hemaggulutinin (HA)-specific IgG that was generated against an influenza A virus strain of the H3 subtype but had cross-neutralizing activities against the H1, H2, H13, and H16 subtypes. These monoclonal S139/1 IgA and IgG antibodies were assumed to recognize the same epitope and thus used to compare their antiviral activities. We found that both S139/1 IgA and IgG antibodies strongly bound to the homologous H3 virus in an enzyme-linked immunosorbent assay, and there were no significant differences in their hemagglutination-inhibiting and neutralizing activities against the H3 virus. In contrast, S139/1 IgA showed remarkably higher cross-binding to and antiviral activities against H1, H2, and H13 viruses than S139/1 IgG. It was also noted that S139/1 IgA, but not IgG, drastically suppressed the extracellular release of the viruses from infected cells. Electron microscopy revealed that S139/1 IgA deposited newly produced viral particles on the cell surface, most likely by tethering the particles. These results suggest that anti-HA IgA has greater potential to prevent influenza A virus infection than IgG antibodies, likely due to increased avidity conferred by its multivalency, and that this advantage may be particularly important for heterosubtypic immunity.
Url:
DOI: 10.1371/journal.pone.0085582
PubMed: 24465606
PubMed Central: 3895000
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>Both IgA and IgG antibodies are known to play important roles in protection against influenza virus infection. While IgG is the major isotype induced systemically, IgA is predominant in mucosal tissues, including the upper respiratory tract. Although IgA antibodies are believed to have unique advantages in mucosal immunity, information on direct comparisons of the in vitro antiviral activities of IgA and IgG antibodies recognizing the same epitope is limited. In this study, we demonstrate differences in antiviral activities between these isotypes using monoclonal IgA and IgG antibodies obtained from hybridomas of the same origin. Polymeric IgA-producing hybridoma cells were successfully subcloned from those originally producing monoclonal antibody S139/1, a hemaggulutinin (HA)-specific IgG that was generated against an influenza A virus strain of the H3 subtype but had cross-neutralizing activities against the H1, H2, H13, and H16 subtypes. These monoclonal S139/1 IgA and IgG antibodies were assumed to recognize the same epitope and thus used to compare their antiviral activities. We found that both S139/1 IgA and IgG antibodies strongly bound to the homologous H3 virus in an enzyme-linked immunosorbent assay, and there were no significant differences in their hemagglutination-inhibiting and neutralizing activities against the H3 virus. In contrast, S139/1 IgA showed remarkably higher cross-binding to and antiviral activities against H1, H2, and H13 viruses than S139/1 IgG. It was also noted that S139/1 IgA, but not IgG, drastically suppressed the extracellular release of the viruses from infected cells. Electron microscopy revealed that S139/1 IgA deposited newly produced viral particles on the cell surface, most likely by tethering the particles. These results suggest that anti-HA IgA has greater potential to prevent influenza A virus infection than IgG antibodies, likely due to increased avidity conferred by its multivalency, and that this advantage may be particularly important for heterosubtypic immunity.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24465606</article-id>
<article-id pub-id-type="pmc">3895000</article-id>
<article-id pub-id-type="publisher-id">PONE-D-13-46212</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0085582</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune Cells</subject>
<subj-group><subject>B Cells</subject>
</subj-group>
</subj-group>
<subj-group><subject>Immunoglobulins</subject>
</subj-group>
</subj-group>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Immunity</subject>
<subj-group><subject>Adaptive Immunity</subject>
<subject>Humoral Immunity</subject>
</subj-group>
</subj-group>
<subj-group><subject>Virology</subject>
<subj-group><subject>Viral Transmission and Infection</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject>
<subj-group><subject>Infectious Diseases</subject>
<subj-group><subject>Viral Diseases</subject>
<subj-group><subject>Influenza</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Comparison of Antiviral Activity between IgA and IgG Specific to Influenza Virus Hemagglutinin: Increased Potential of IgA for Heterosubtypic Immunity</article-title>
<alt-title alt-title-type="running-head">Different Antiviral Activity between IgA and IgG</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Muramatsu</surname>
<given-names>Mieko</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Yoshida</surname>
<given-names>Reiko</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yokoyama</surname>
<given-names>Ayaka</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Miyamoto</surname>
<given-names>Hiroko</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kajihara</surname>
<given-names>Masahiro</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Maruyama</surname>
<given-names>Junki</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nao</surname>
<given-names>Naganori</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Manzoor</surname>
<given-names>Rashid</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Takada</surname>
<given-names>Ayato</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Division of Global Epidemiology, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>School of Veterinary Medicine, the University of Zambia, Lusaka, Zambia</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Kobinger</surname>
<given-names>Gary P.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Public Health Agency of Canada, Canada</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>atakada@czc.hokudai.ac.jp</email>
</corresp>
<fn fn-type="COI-statement"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: MM RY AT. Performed the experiments: MM RY AY HM. Analyzed the data: MM RY HM MK JM NN RM AT. Contributed reagents/materials/analysis tools: RY AY HM JM RM AT. Wrote the paper: MM RY AT.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>17</day>
<month>1</month>
<year>2014</year>
</pub-date>
<volume>9</volume>
<issue>1</issue>
<elocation-id>e85582</elocation-id>
<history><date date-type="received"><day>5</day>
<month>11</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>5</day>
<month>12</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>© 2014 Muramatsu et al</copyright-statement>
<copyright-year>2014</copyright-year>
<copyright-holder>Muramatsu et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p>
</license>
</permissions>
<abstract><p>Both IgA and IgG antibodies are known to play important roles in protection against influenza virus infection. While IgG is the major isotype induced systemically, IgA is predominant in mucosal tissues, including the upper respiratory tract. Although IgA antibodies are believed to have unique advantages in mucosal immunity, information on direct comparisons of the in vitro antiviral activities of IgA and IgG antibodies recognizing the same epitope is limited. In this study, we demonstrate differences in antiviral activities between these isotypes using monoclonal IgA and IgG antibodies obtained from hybridomas of the same origin. Polymeric IgA-producing hybridoma cells were successfully subcloned from those originally producing monoclonal antibody S139/1, a hemaggulutinin (HA)-specific IgG that was generated against an influenza A virus strain of the H3 subtype but had cross-neutralizing activities against the H1, H2, H13, and H16 subtypes. These monoclonal S139/1 IgA and IgG antibodies were assumed to recognize the same epitope and thus used to compare their antiviral activities. We found that both S139/1 IgA and IgG antibodies strongly bound to the homologous H3 virus in an enzyme-linked immunosorbent assay, and there were no significant differences in their hemagglutination-inhibiting and neutralizing activities against the H3 virus. In contrast, S139/1 IgA showed remarkably higher cross-binding to and antiviral activities against H1, H2, and H13 viruses than S139/1 IgG. It was also noted that S139/1 IgA, but not IgG, drastically suppressed the extracellular release of the viruses from infected cells. Electron microscopy revealed that S139/1 IgA deposited newly produced viral particles on the cell surface, most likely by tethering the particles. These results suggest that anti-HA IgA has greater potential to prevent influenza A virus infection than IgG antibodies, likely due to increased avidity conferred by its multivalency, and that this advantage may be particularly important for heterosubtypic immunity.</p>
</abstract>
<funding-group><funding-statement>This work was supported by the Japan Initiative for Global Research Network on Infectious Diseases (J-GRID) (<ext-link ext-link-type="uri" xlink:href="http://www.crnid.riken.jp/jgrid/en/index.html">http://www.crnid.riken.jp/jgrid/en/index.html</ext-link>
), the Global COE Program (<ext-link ext-link-type="uri" xlink:href="http://www.jsps.go.jp/english/e-globalcoe/index.html">http://www.jsps.go.jp/english/e-globalcoe/index.html</ext-link>
), Japan Science and Technology Agency Basic Research Programs, and a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) (<ext-link ext-link-type="uri" xlink:href="http://www.mext.go.jp/english/">http://www.mext.go.jp/english/</ext-link>
). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><page-count count="8"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Japon</li>
<li>Zambie</li>
</country>
</list>
<tree><country name="Japon"><noRegion><name sortKey="Muramatsu, Mieko" sort="Muramatsu, Mieko" uniqKey="Muramatsu M" first="Mieko" last="Muramatsu">Mieko Muramatsu</name>
</noRegion>
<name sortKey="Kajihara, Masahiro" sort="Kajihara, Masahiro" uniqKey="Kajihara M" first="Masahiro" last="Kajihara">Masahiro Kajihara</name>
<name sortKey="Manzoor, Rashid" sort="Manzoor, Rashid" uniqKey="Manzoor R" first="Rashid" last="Manzoor">Rashid Manzoor</name>
<name sortKey="Maruyama, Junki" sort="Maruyama, Junki" uniqKey="Maruyama J" first="Junki" last="Maruyama">Junki Maruyama</name>
<name sortKey="Miyamoto, Hiroko" sort="Miyamoto, Hiroko" uniqKey="Miyamoto H" first="Hiroko" last="Miyamoto">Hiroko Miyamoto</name>
<name sortKey="Nao, Naganori" sort="Nao, Naganori" uniqKey="Nao N" first="Naganori" last="Nao">Naganori Nao</name>
<name sortKey="Takada, Ayato" sort="Takada, Ayato" uniqKey="Takada A" first="Ayato" last="Takada">Ayato Takada</name>
<name sortKey="Yokoyama, Ayaka" sort="Yokoyama, Ayaka" uniqKey="Yokoyama A" first="Ayaka" last="Yokoyama">Ayaka Yokoyama</name>
<name sortKey="Yoshida, Reiko" sort="Yoshida, Reiko" uniqKey="Yoshida R" first="Reiko" last="Yoshida">Reiko Yoshida</name>
</country>
<country name="Zambie"><noRegion><name sortKey="Takada, Ayato" sort="Takada, Ayato" uniqKey="Takada A" first="Ayato" last="Takada">Ayato Takada</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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