Learning the sequence of influenza A genome assembly during viral replication using point process models and fluorescence in situ hybridization
Identifieur interne : 000F59 ( Ncbi/Merge ); précédent : 000F58; suivant : 000F60Learning the sequence of influenza A genome assembly during viral replication using point process models and fluorescence in situ hybridization
Auteurs : Timothy D. Majarian [États-Unis] ; Robert F. Murphy [États-Unis] ; Seema S. Lakdawala [États-Unis]Source :
- PLoS Computational Biology [ 1553-734X ] ; 2019.
Abstract
Within influenza virus infected cells, viral genomic RNA are selectively packed into progeny virions, which predominantly contain a single copy of 8 viral RNA segments. Intersegmental RNA-RNA interactions are thought to mediate selective packaging of each viral ribonucleoprotein complex (vRNP). Clear evidence of a specific interaction network culminating in the full genomic set has yet to be identified. Using multi-color fluorescence
Url:
DOI: 10.1371/journal.pcbi.1006199
PubMed: 30689627
PubMed Central: 6366722
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Majarian</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Computational Biology Department, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Computational Biology Department, Carnegie Mellon University, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université Carnegie-Mellon</orgName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université Carnegie-Mellon</orgName></affiliation></author><author><name sortKey="Murphy, Robert F" sort="Murphy, Robert F" uniqKey="Murphy R" first="Robert F." last="Murphy">Robert F. Murphy</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Computational Biology Department, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Computational Biology Department, Carnegie Mellon University, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université Carnegie-Mellon</orgName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université Carnegie-Mellon</orgName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff003"><addr-line>Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université Carnegie-Mellon</orgName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff004"><addr-line>Machine Learning Department, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Machine Learning Department, Carnegie Mellon University, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université Carnegie-Mellon</orgName></affiliation></author><author><name sortKey="Lakdawala, Seema S" sort="Lakdawala, Seema S" uniqKey="Lakdawala S" first="Seema S." last="Lakdawala">Seema S. Lakdawala</name><affiliation wicri:level="2"><nlm:aff id="aff005"><addr-line>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author></analytic><series><title level="j">PLoS Computational Biology</title><idno type="ISSN">1553-734X</idno><idno type="eISSN">1553-7358</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>Within influenza virus infected cells, viral genomic RNA are selectively packed into progeny virions, which predominantly contain a single copy of 8 viral RNA segments. Intersegmental RNA-RNA interactions are thought to mediate selective packaging of each viral ribonucleoprotein complex (vRNP). Clear evidence of a specific interaction network culminating in the full genomic set has yet to be identified. Using multi-color fluorescence <italic>in situ</italic> hybridization to visualize four vRNP segments within a single cell, we developed image-based models of vRNP-vRNP spatial dependence. These models were used to construct likely sequences of vRNP associations resulting in the full genomic set. Our results support the notion that selective packaging occurs during cytoplasmic transport and identifies the formation of multiple distinct vRNP sub-complexes that likely form as intermediate steps toward full genomic inclusion into a progeny virion. The methods employed demonstrate a statistically driven, model based approach applicable to other interaction and assembly problems.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Morens, Dm" uniqKey="Morens D">DM Morens</name></author><author><name sortKey="Taubenberger, Jk" uniqKey="Taubenberger J">JK Taubenberger</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sidorenko, Y" uniqKey="Sidorenko Y">Y Sidorenko</name></author><author><name sortKey="Reichl, U" uniqKey="Reichl U">U Reichl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hutchinson, Ec" uniqKey="Hutchinson E">EC Hutchinson</name></author><author><name sortKey="Von Kirchbach, Jc" uniqKey="Von Kirchbach J">JC von Kirchbach</name></author><author><name sortKey="Gog, Jr" uniqKey="Gog J">JR Gog</name></author><author><name sortKey="Digard, P" uniqKey="Digard P">P 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viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></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>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></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>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A 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>Genetics</subject><subj-group><subject>Genomics</subject><subj-group><subject>Microbial Genomics</subject><subj-group><subject>Viral Genomics</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>Microbiology</subject><subj-group><subject>Microbial Genomics</subject><subj-group><subject>Viral Genomics</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 Genomics</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Cytogenetic Techniques</subject><subj-group><subject>Fluorescent in Situ Hybridization</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Molecular Biology</subject><subj-group><subject>Molecular Biology Techniques</subject><subj-group><subject>Molecular Probe Techniques</subject><subj-group><subject>Probe Hybridization</subject><subj-group><subject>Fluorescent in Situ Hybridization</subject></subj-group></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>Molecular Biology Techniques</subject><subj-group><subject>Molecular Probe Techniques</subject><subj-group><subject>Probe Hybridization</subject><subj-group><subject>Fluorescent in Situ Hybridization</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Learning the sequence of influenza A genome assembly during viral replication using point process models and fluorescence in situ hybridization</article-title><alt-title alt-title-type="running-head">Learning the sequence of influenza A genome assembly during viral replication</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Majarian</surname><given-names>Timothy D.</given-names></name><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Software</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"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="author-notes" rid="currentaff001"><sup>¤</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-0358-901X</contrib-id><name><surname>Murphy</surname><given-names>Robert F.</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/">Supervision</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"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref><xref ref-type="aff" rid="aff004"><sup>4</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-7679-2150</contrib-id><name><surname>Lakdawala</surname><given-names>Seema 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/">Supervision</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="aff005"><sup>5</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Computational Biology Department, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Machine Learning Department, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>De Boer</surname><given-names>Rob J.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Utrecht University, NETHERLANDS</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="current-aff" id="currentaff001"><label>¤</label><p>Current address: Program in Medical and Population Genetics, Broad Institute, Cambridge, Massachusetts, United States of America</p></fn><corresp id="cor001">* E-mail: <email>murphy@cmu.edu</email> (RFM); <email>Lakdawala@pitt.edu</email> (SSL)</corresp></author-notes><pub-date pub-type="epub"><day>28</day><month>1</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>1</month><year>2019</year></pub-date><volume>15</volume><issue>1</issue><elocation-id>e1006199</elocation-id><history><date date-type="received"><day>13</day><month>5</month><year>2018</year></date><date date-type="accepted"><day>20</day><month>11</month><year>2018</year></date></history><permissions><copyright-statement>© 2019 Majarian et al</copyright-statement><copyright-year>2019</copyright-year><copyright-holder>Majarian 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="pcbi.1006199.pdf"></self-uri><abstract><p>Within influenza virus infected cells, viral genomic RNA are selectively packed into progeny virions, which predominantly contain a single copy of 8 viral RNA segments. Intersegmental RNA-RNA interactions are thought to mediate selective packaging of each viral ribonucleoprotein complex (vRNP). Clear evidence of a specific interaction network culminating in the full genomic set has yet to be identified. Using multi-color fluorescence <italic>in situ</italic> hybridization to visualize four vRNP segments within a single cell, we developed image-based models of vRNP-vRNP spatial dependence. These models were used to construct likely sequences of vRNP associations resulting in the full genomic set. Our results support the notion that selective packaging occurs during cytoplasmic transport and identifies the formation of multiple distinct vRNP sub-complexes that likely form as intermediate steps toward full genomic inclusion into a progeny virion. The methods employed demonstrate a statistically driven, model based approach applicable to other interaction and assembly problems.</p></abstract><abstract abstract-type="summary"><title>Author summary</title><p>Influenza virus consists of eight viral ribonucleoproteins (vRNPs) that are assembled by infected cells to produce new virions. The process by which all eight vRNPs are assembled is not yet understood. We therefore used images from a previous study in which up to four vRNPs had been visualized in the same cell to construct spatial point process models that measure how well the subcellular distribution of one vRNP can be predicted from one or more other vRNPs. We used the likelihood of these models as an estimate of the extent of association between vRNPs and thereby constructed likely sequences of vRNP assembly that would produce full virions. Our work identifies the formation of multiple distinct vRNP sub-complexes that likely form as intermediate steps toward production of a virion. The results may be of use in designing strategies to interfere with virus assembly. We also anticipate that the approach may be useful for studying other assembly processes, especially for complexes with modest affinities and more components than can be visualized simultaneously.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000057</institution-id><institution>National Institute of General Medical Sciences</institution></institution-wrap></funding-source><award-id>GM090033</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-0358-901X</contrib-id><name><surname>Murphy</surname><given-names>Robert F.</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000060</institution-id><institution>National Institute of Allergy and Infectious Diseases</institution></institution-wrap></funding-source><award-id>AI108600</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-7679-2150</contrib-id><name><surname>Lakdawala</surname><given-names>Seema S.</given-names></name></principal-award-recipient></award-group><award-group id="award003"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000057</institution-id><institution>National Institute of General Medical Sciences</institution></institution-wrap></funding-source><award-id>GM103712</award-id></award-group><award-group id="award004"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000076</institution-id><institution>Directorate for Biological Sciences</institution></institution-wrap></funding-source><award-id>MCB1616492</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-0358-901X</contrib-id><name><surname>Murphy</surname><given-names>Robert F.</given-names></name></principal-award-recipient></award-group><funding-statement>This study was supported in part by National Institutes of Health grants AI108600-01 (SL), GM090033 (RFM), and GM103712 and by National Science Foundation grant MCB1616492 (RFM). 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="4"></fig-count><table-count count="6"></table-count><page-count count="20"></page-count></counts><custom-meta-group><custom-meta><meta-name>PLOS Publication Stage</meta-name><meta-value>vor-update-to-uncorrected-proof</meta-value></custom-meta><custom-meta><meta-name>Publication Update</meta-name><meta-value>2019-02-07</meta-value></custom-meta><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the manuscript and its Supporting Information files. All source code and results of calculations are available at <ext-link ext-link-type="uri" xlink:href="http://murphylab.cbd.cmu.edu/software">http://murphylab.cbd.cmu.edu/software</ext-link>.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the manuscript and its Supporting Information files. All source code and results of calculations are available at <ext-link ext-link-type="uri" xlink:href="http://murphylab.cbd.cmu.edu/software">http://murphylab.cbd.cmu.edu/software</ext-link>.</p></notes></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Pennsylvanie</li></region><settlement><li>Pittsburgh</li></settlement><orgName><li>Université Carnegie-Mellon</li></orgName></list><tree><country name="États-Unis"><region name="Pennsylvanie"><name sortKey="Majarian, Timothy D" sort="Majarian, Timothy D" uniqKey="Majarian T" first="Timothy D." last="Majarian">Timothy D. Majarian</name></region><name sortKey="Lakdawala, Seema S" sort="Lakdawala, Seema S" uniqKey="Lakdawala S" first="Seema S." last="Lakdawala">Seema S. Lakdawala</name><name sortKey="Majarian, Timothy D" sort="Majarian, Timothy D" uniqKey="Majarian T" first="Timothy D." last="Majarian">Timothy D. Majarian</name><name sortKey="Murphy, Robert F" sort="Murphy, Robert F" uniqKey="Murphy R" first="Robert F." last="Murphy">Robert F. Murphy</name><name sortKey="Murphy, Robert F" sort="Murphy, Robert F" uniqKey="Murphy R" first="Robert F." last="Murphy">Robert F. Murphy</name><name sortKey="Murphy, Robert F" sort="Murphy, Robert F" uniqKey="Murphy R" first="Robert F." last="Murphy">Robert F. Murphy</name><name sortKey="Murphy, Robert F" sort="Murphy, Robert F" uniqKey="Murphy R" first="Robert F." last="Murphy">Robert F. Murphy</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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