A general approach for predicting protein epitopes targeted by antibody repertoires using whole proteomes
Identifieur interne : 001052 ( Pmc/Curation ); précédent : 001051; suivant : 001053A general approach for predicting protein epitopes targeted by antibody repertoires using whole proteomes
Auteurs : Michael L. Paull ; Tim Johnston ; Kelly N. Ibsen ; Joel D. Bozekowski ; Patrick S. DaughertySource :
- PLoS ONE [ 1932-6203 ] ; 2019.
Abstract
Antibodies are essential to functional immunity, yet the epitopes targeted by antibody repertoires remain largely uncharacterized. To aid in characterization, we developed a generalizable strategy to predict antibody-binding epitopes within individual proteins and entire proteomes. Specifically, we selected antibody-binding peptides for 273 distinct sera out of a random library and identified the peptides using next-generation sequencing. To predict antibody-binding epitopes and the antigens from which these epitopes were derived, we tiled the sequences of candidate antigens into short overlapping subsequences of length k (k-mers). We used the enrichment over background of these k-mers in the antibody-binding peptide dataset to predict antibody-binding epitopes. As a positive control, we used this approach, termed K-mer Tiling of Protein Epitopes (K-TOPE), to predict epitopes targeted by monoclonal and polyclonal antibodies of well-characterized specificity, accurately recovering their known epitopes. K-TOPE characterized a commonly targeted antigen from
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DOI: 10.1371/journal.pone.0217668
PubMed: 31490930
PubMed Central: 6730857
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A general approach for predicting protein epitopes targeted by antibody repertoires using whole proteomes</title><author><name sortKey="Paull, Michael L" sort="Paull, Michael L" uniqKey="Paull M" first="Michael L." last="Paull">Michael L. Paull</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Johnston, Tim" sort="Johnston, Tim" uniqKey="Johnston T" first="Tim" last="Johnston">Tim Johnston</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Ibsen, Kelly N" sort="Ibsen, Kelly N" uniqKey="Ibsen K" first="Kelly N." last="Ibsen">Kelly N. Ibsen</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Bozekowski, Joel D" sort="Bozekowski, Joel D" uniqKey="Bozekowski J" first="Joel D." last="Bozekowski">Joel D. Bozekowski</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Daugherty, Patrick S" sort="Daugherty, Patrick S" uniqKey="Daugherty P" first="Patrick S." last="Daugherty">Patrick S. Daugherty</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31490930</idno><idno type="pmc">6730857</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6730857</idno><idno type="RBID">PMC:6730857</idno><idno type="doi">10.1371/journal.pone.0217668</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">001052</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001052</idno><idno type="wicri:Area/Pmc/Curation">001052</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">001052</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A general approach for predicting protein epitopes targeted by antibody repertoires using whole proteomes</title><author><name sortKey="Paull, Michael L" sort="Paull, Michael L" uniqKey="Paull M" first="Michael L." last="Paull">Michael L. Paull</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Johnston, Tim" sort="Johnston, Tim" uniqKey="Johnston T" first="Tim" last="Johnston">Tim Johnston</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Ibsen, Kelly N" sort="Ibsen, Kelly N" uniqKey="Ibsen K" first="Kelly N." last="Ibsen">Kelly N. Ibsen</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Bozekowski, Joel D" sort="Bozekowski, Joel D" uniqKey="Bozekowski J" first="Joel D." last="Bozekowski">Joel D. Bozekowski</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Daugherty, Patrick S" sort="Daugherty, Patrick S" uniqKey="Daugherty P" first="Patrick S." last="Daugherty">Patrick S. Daugherty</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</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>Antibodies are essential to functional immunity, yet the epitopes targeted by antibody repertoires remain largely uncharacterized. To aid in characterization, we developed a generalizable strategy to predict antibody-binding epitopes within individual proteins and entire proteomes. Specifically, we selected antibody-binding peptides for 273 distinct sera out of a random library and identified the peptides using next-generation sequencing. To predict antibody-binding epitopes and the antigens from which these epitopes were derived, we tiled the sequences of candidate antigens into short overlapping subsequences of length k (k-mers). We used the enrichment over background of these k-mers in the antibody-binding peptide dataset to predict antibody-binding epitopes. As a positive control, we used this approach, termed K-mer Tiling of Protein Epitopes (K-TOPE), to predict epitopes targeted by monoclonal and polyclonal antibodies of well-characterized specificity, accurately recovering their known epitopes. K-TOPE characterized a commonly targeted antigen from <italic>Rhinovirus A</italic>, predicting four epitopes recognized by antibodies present in 87% of sera (n = 250). An analysis of 2,908 proteins from 400 viral taxa that infect humans predicted seven enterovirus epitopes and five Epstein-Barr virus epitopes recognized by >30% of specimens. Analysis of <italic>Staphylococcus</italic> and <italic>Streptococcus</italic> proteomes similarly predicted 22 epitopes recognized by >30% of specimens. Twelve of these common viral and bacterial epitopes agreed with previously mapped epitopes with p-values < 0.05. Additionally, we predicted 30 HSV2-specific epitopes that were 100% specific against HSV1 in novel and previously reported antigens. Experimentally validating these candidate epitopes could help identify diagnostic biomarkers, vaccine components, and therapeutic targets. The K-TOPE approach thus provides a powerful new tool to elucidate the organisms, antigens, and epitopes targeted by human antibody repertoires.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Amanna, Ij" uniqKey="Amanna I">IJ Amanna</name></author><author><name sortKey="Carlson, Ne" uniqKey="Carlson N">NE Carlson</name></author><author><name sortKey="Slifka, Mk" uniqKey="Slifka M">MK Slifka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Soria Guerra, Re" uniqKey="Soria Guerra R">RE Soria-Guerra</name></author><author><name sortKey="Nieto Gomez, R" uniqKey="Nieto Gomez R">R Nieto-Gomez</name></author><author><name sortKey="Govea Alonso, Do" uniqKey="Govea Alonso D">DO Govea-Alonso</name></author><author><name sortKey="Rosales Mendoza, S" uniqKey="Rosales Mendoza S">S Rosales-Mendoza</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lemon, Sm" uniqKey="Lemon 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<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, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31490930</article-id><article-id pub-id-type="pmc">6730857</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0217668</article-id><article-id pub-id-type="publisher-id">PONE-D-19-13664</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Proteomes</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Virology</subject><subj-group><subject>Viral Structure</subject><subj-group><subject>Tegument Proteins</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Immune Physiology</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Immune Physiology</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune System Proteins</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune System Proteins</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Immune System Proteins</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Database and Informatics Methods</subject><subj-group><subject>Bioinformatics</subject><subj-group><subject>Sequence Analysis</subject><subj-group><subject>Sequence Motif Analysis</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Extracellular Matrix Proteins</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Glycobiology</subject><subj-group><subject>Glycoproteins</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Enteroviruses</subject><subj-group><subject>Rhinovirus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical Microbiology</subject><subj-group><subject>Microbial Pathogens</subject><subj-group><subject>Viral Pathogens</subject><subj-group><subject>Enteroviruses</subject><subj-group><subject>Rhinovirus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Pathology and Laboratory Medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial Pathogens</subject><subj-group><subject>Viral Pathogens</subject><subj-group><subject>Enteroviruses</subject><subj-group><subject>Rhinovirus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral Pathogens</subject><subj-group><subject>Enteroviruses</subject><subj-group><subject>Rhinovirus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>DNA viruses</subject><subj-group><subject>Herpesviruses</subject><subj-group><subject>Epstein-Barr virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Herpesviruses</subject><subj-group><subject>Epstein-Barr virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Herpesviruses</subject><subj-group><subject>Epstein-Barr virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Herpesviruses</subject><subj-group><subject>Epstein-Barr virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>A general approach for predicting protein epitopes targeted by antibody repertoires using whole proteomes</article-title><alt-title alt-title-type="running-head">Predicting protein epitopes targeted by antibody repertoires using whole proteomes</alt-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-8416-3314</contrib-id><name><surname>Paull</surname><given-names>Michael L.</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Data curation</role><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Project administration</role><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Software</role><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Visualization</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib><contrib contrib-type="author"><name><surname>Johnston</surname><given-names>Tim</given-names></name><role content-type="http://credit.casrai.org/">Data curation</role><role content-type="http://credit.casrai.org/">Software</role><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Ibsen</surname><given-names>Kelly N.</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Resources</role><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Bozekowski</surname><given-names>Joel D.</given-names></name><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Resources</role><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Daugherty</surname><given-names>Patrick S.</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Funding acquisition</role><role content-type="http://credit.casrai.org/">Project administration</role><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><addr-line>Department of Chemical Engineering, University of California Santa Barbara, California, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Cheshenko</surname><given-names>Natalia V</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Albert Einstein College of Medicine, UNITED STATES</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>I have read the journal’s policy and the authors of this manuscript have the following competing interests: PSD is a Director, Officer, and Stockholder, and TJ and JDB are Employees of immune repertoire mapping company SerImmune. This does not alter our adherence to PLOS ONE policies on sharing data and materials.</p></fn><corresp id="cor001">* E-mail: <email>michael.paull444@gmail.com</email> (MLP); <email>psdaug@gmail.com</email> (PSD)</corresp></author-notes><pub-date pub-type="epub"><day>6</day><month>9</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>14</volume><issue>9</issue><elocation-id>e0217668</elocation-id><history><date date-type="received"><day>14</day><month>5</month><year>2019</year></date><date date-type="accepted"><day>22</day><month>8</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 Paull et al</copyright-statement><copyright-year>2019</copyright-year><copyright-holder>Paull 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 <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0217668.pdf"></self-uri><abstract><p>Antibodies are essential to functional immunity, yet the epitopes targeted by antibody repertoires remain largely uncharacterized. To aid in characterization, we developed a generalizable strategy to predict antibody-binding epitopes within individual proteins and entire proteomes. Specifically, we selected antibody-binding peptides for 273 distinct sera out of a random library and identified the peptides using next-generation sequencing. To predict antibody-binding epitopes and the antigens from which these epitopes were derived, we tiled the sequences of candidate antigens into short overlapping subsequences of length k (k-mers). We used the enrichment over background of these k-mers in the antibody-binding peptide dataset to predict antibody-binding epitopes. As a positive control, we used this approach, termed K-mer Tiling of Protein Epitopes (K-TOPE), to predict epitopes targeted by monoclonal and polyclonal antibodies of well-characterized specificity, accurately recovering their known epitopes. K-TOPE characterized a commonly targeted antigen from <italic>Rhinovirus A</italic>, predicting four epitopes recognized by antibodies present in 87% of sera (n = 250). An analysis of 2,908 proteins from 400 viral taxa that infect humans predicted seven enterovirus epitopes and five Epstein-Barr virus epitopes recognized by >30% of specimens. Analysis of <italic>Staphylococcus</italic> and <italic>Streptococcus</italic> proteomes similarly predicted 22 epitopes recognized by >30% of specimens. Twelve of these common viral and bacterial epitopes agreed with previously mapped epitopes with p-values < 0.05. Additionally, we predicted 30 HSV2-specific epitopes that were 100% specific against HSV1 in novel and previously reported antigens. Experimentally validating these candidate epitopes could help identify diagnostic biomarkers, vaccine components, and therapeutic targets. The K-TOPE approach thus provides a powerful new tool to elucidate the organisms, antigens, and epitopes targeted by human antibody repertoires.</p></abstract><funding-group><award-group id="award001"><funding-source><institution>BrightFocus Foundation</institution></funding-source><award-id>M2016219</award-id><principal-award-recipient><name><surname>Daugherty</surname><given-names>Patrick S.</given-names></name></principal-award-recipient></award-group><funding-statement>This work was funded in part by grant M2016219 from the Brightfocus Foundation (<ext-link ext-link-type="uri" xlink:href="https://www.brightfocus.org/">https://www.brightfocus.org/</ext-link>) to PSD. 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><fig-count count="5"></fig-count><table-count count="6"></table-count><page-count count="24"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All 278 antibody-binding peptide files are available from the Dryad Digital Repository (<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.5061/dryad.v7d0350">https://doi.org/10.5061/dryad.v7d0350</ext-link>).</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All 278 antibody-binding peptide files are available from the Dryad Digital Repository (<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.5061/dryad.v7d0350">https://doi.org/10.5061/dryad.v7d0350</ext-link>).</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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