Tracking Changes in SARS-CoV-2 Spike: Evidence that D614G Increases Infectivity of the COVID-19 Virus.
Identifieur interne : 000020 ( Main/Corpus ); précédent : 000019; suivant : 000021Tracking Changes in SARS-CoV-2 Spike: Evidence that D614G Increases Infectivity of the COVID-19 Virus.
Auteurs : Bette Korber ; Will M. Fischer ; Sandrasegaram Gnanakaran ; Hyejin Yoon ; James Theiler ; Werner Abfalterer ; Nick Hengartner ; Elena E. Giorgi ; Tanmoy Bhattacharya ; Brian Foley ; Kathryn M. Hastie ; Matthew D. Parker ; David G. Partridge ; Cariad M. Evans ; Timothy M. Freeman ; Thushan I. De Silva ; Charlene Mcdanal ; Lautaro G. Perez ; Haili Tang ; Alex Moon-Walker ; Sean P. Whelan ; Celia C. Labranche ; Erica O. Saphire ; David C. MontefioriSource :
- Cell [ 1097-4172 ] ; 2020.
Abstract
A SARS-CoV-2 variant carrying the Spike protein amino acid change D614G has become the most prevalent form in the global pandemic. Dynamic tracking of variant frequencies revealed a recurrent pattern of G614 increase at multiple geographic levels: national, regional, and municipal. The shift occurred even in local epidemics where the original D614 form was well established prior to introduction of the G614 variant. The consistency of this pattern was highly statistically significant, suggesting that the G614 variant may have a fitness advantage. We found that the G614 variant grows to a higher titer as pseudotyped virions. In infected individuals, G614 is associated with lower RT-PCR cycle thresholds, suggestive of higher upper respiratory tract viral loads, but not with increased disease severity. These findings illuminate changes important for a mechanistic understanding of the virus and support continuing surveillance of Spike mutations to aid with development of immunological interventions.
DOI: 10.1016/j.cell.2020.06.043
PubMed: 32697968
PubMed Central: PMC7332439
Links to Exploration step
pubmed:32697968Le document en format XML
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<author><name sortKey="Korber, Bette" sort="Korber, Bette" uniqKey="Korber B" first="Bette" last="Korber">Bette Korber</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA; New Mexico Consortium, Los Alamos, NM 87545, USA. Electronic address: btk@lanl.gov.</nlm:affiliation>
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<author><name sortKey="Gnanakaran, Sandrasegaram" sort="Gnanakaran, Sandrasegaram" uniqKey="Gnanakaran S" first="Sandrasegaram" last="Gnanakaran">Sandrasegaram Gnanakaran</name>
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<author><name sortKey="Yoon, Hyejin" sort="Yoon, Hyejin" uniqKey="Yoon H" first="Hyejin" last="Yoon">Hyejin Yoon</name>
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<author><name sortKey="Theiler, James" sort="Theiler, James" uniqKey="Theiler J" first="James" last="Theiler">James Theiler</name>
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<author><name sortKey="Abfalterer, Werner" sort="Abfalterer, Werner" uniqKey="Abfalterer W" first="Werner" last="Abfalterer">Werner Abfalterer</name>
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<author><name sortKey="Hengartner, Nick" sort="Hengartner, Nick" uniqKey="Hengartner N" first="Nick" last="Hengartner">Nick Hengartner</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
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<author><name sortKey="Giorgi, Elena E" sort="Giorgi, Elena E" uniqKey="Giorgi E" first="Elena E" last="Giorgi">Elena E. Giorgi</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
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<author><name sortKey="Bhattacharya, Tanmoy" sort="Bhattacharya, Tanmoy" uniqKey="Bhattacharya T" first="Tanmoy" last="Bhattacharya">Tanmoy Bhattacharya</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
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<author><name sortKey="Foley, Brian" sort="Foley, Brian" uniqKey="Foley B" first="Brian" last="Foley">Brian Foley</name>
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<author><name sortKey="Hastie, Kathryn M" sort="Hastie, Kathryn M" uniqKey="Hastie K" first="Kathryn M" last="Hastie">Kathryn M. Hastie</name>
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<author><name sortKey="Parker, Matthew D" sort="Parker, Matthew D" uniqKey="Parker M" first="Matthew D" last="Parker">Matthew D. Parker</name>
<affiliation><nlm:affiliation>Sheffield Biomedical Research Centre & Sheffield Bioinformatics Core, University of Sheffield, Sheffield S10 2HQ, UK.</nlm:affiliation>
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<author><name sortKey="Partridge, David G" sort="Partridge, David G" uniqKey="Partridge D" first="David G" last="Partridge">David G. Partridge</name>
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<author><name sortKey="Evans, Cariad M" sort="Evans, Cariad M" uniqKey="Evans C" first="Cariad M" last="Evans">Cariad M. Evans</name>
<affiliation><nlm:affiliation>Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield S10 2JF, UK.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Freeman, Timothy M" sort="Freeman, Timothy M" uniqKey="Freeman T" first="Timothy M" last="Freeman">Timothy M. Freeman</name>
<affiliation><nlm:affiliation>Sheffield Biomedical Research Centre & Sheffield Bioinformatics Core, University of Sheffield, Sheffield S10 2HQ, UK.</nlm:affiliation>
</affiliation>
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<author><name sortKey="De Silva, Thushan I" sort="De Silva, Thushan I" uniqKey="De Silva T" first="Thushan I" last="De Silva">Thushan I. De Silva</name>
<affiliation><nlm:affiliation>Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield S10 2JF, UK; Department of Infection, Immunity and Cardiovascular Disease, Medical School, University of Sheffield, Sheffield S10 2RX, UK.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Mcdanal, Charlene" sort="Mcdanal, Charlene" uniqKey="Mcdanal C" first="Charlene" last="Mcdanal">Charlene Mcdanal</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Perez, Lautaro G" sort="Perez, Lautaro G" uniqKey="Perez L" first="Lautaro G" last="Perez">Lautaro G. Perez</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Tang, Haili" sort="Tang, Haili" uniqKey="Tang H" first="Haili" last="Tang">Haili Tang</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Moon Walker, Alex" sort="Moon Walker, Alex" uniqKey="Moon Walker A" first="Alex" last="Moon-Walker">Alex Moon-Walker</name>
<affiliation><nlm:affiliation>La Jolla Institute for Immunology, La Jolla, CA 92037, USA; Program in Virology, Harvard University, Boston, MA 02115, USA; Department of Molecular Microbiology, Washington University in Saint Louis, St. Louis, MO 63130, USA.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Whelan, Sean P" sort="Whelan, Sean P" uniqKey="Whelan S" first="Sean P" last="Whelan">Sean P. Whelan</name>
<affiliation><nlm:affiliation>Department of Molecular Microbiology, Washington University in Saint Louis, St. Louis, MO 63130, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Labranche, Celia C" sort="Labranche, Celia C" uniqKey="Labranche C" first="Celia C" last="Labranche">Celia C. Labranche</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Saphire, Erica O" sort="Saphire, Erica O" uniqKey="Saphire E" first="Erica O" last="Saphire">Erica O. Saphire</name>
<affiliation><nlm:affiliation>La Jolla Institute for Immunology, La Jolla, CA 92037, USA.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Montefiori, David C" sort="Montefiori, David C" uniqKey="Montefiori D" first="David C" last="Montefiori">David C. Montefiori</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Tracking Changes in SARS-CoV-2 Spike: Evidence that D614G Increases Infectivity of the COVID-19 Virus.</title>
<author><name sortKey="Korber, Bette" sort="Korber, Bette" uniqKey="Korber B" first="Bette" last="Korber">Bette Korber</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA; New Mexico Consortium, Los Alamos, NM 87545, USA. Electronic address: btk@lanl.gov.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Fischer, Will M" sort="Fischer, Will M" uniqKey="Fischer W" first="Will M" last="Fischer">Will M. Fischer</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Gnanakaran, Sandrasegaram" sort="Gnanakaran, Sandrasegaram" uniqKey="Gnanakaran S" first="Sandrasegaram" last="Gnanakaran">Sandrasegaram Gnanakaran</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Yoon, Hyejin" sort="Yoon, Hyejin" uniqKey="Yoon H" first="Hyejin" last="Yoon">Hyejin Yoon</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Theiler, James" sort="Theiler, James" uniqKey="Theiler J" first="James" last="Theiler">James Theiler</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Abfalterer, Werner" sort="Abfalterer, Werner" uniqKey="Abfalterer W" first="Werner" last="Abfalterer">Werner Abfalterer</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Hengartner, Nick" sort="Hengartner, Nick" uniqKey="Hengartner N" first="Nick" last="Hengartner">Nick Hengartner</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Giorgi, Elena E" sort="Giorgi, Elena E" uniqKey="Giorgi E" first="Elena E" last="Giorgi">Elena E. Giorgi</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Bhattacharya, Tanmoy" sort="Bhattacharya, Tanmoy" uniqKey="Bhattacharya T" first="Tanmoy" last="Bhattacharya">Tanmoy Bhattacharya</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Foley, Brian" sort="Foley, Brian" uniqKey="Foley B" first="Brian" last="Foley">Brian Foley</name>
<affiliation><nlm:affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Hastie, Kathryn M" sort="Hastie, Kathryn M" uniqKey="Hastie K" first="Kathryn M" last="Hastie">Kathryn M. Hastie</name>
<affiliation><nlm:affiliation>La Jolla Institute for Immunology, La Jolla, CA 92037, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Parker, Matthew D" sort="Parker, Matthew D" uniqKey="Parker M" first="Matthew D" last="Parker">Matthew D. Parker</name>
<affiliation><nlm:affiliation>Sheffield Biomedical Research Centre & Sheffield Bioinformatics Core, University of Sheffield, Sheffield S10 2HQ, UK.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Partridge, David G" sort="Partridge, David G" uniqKey="Partridge D" first="David G" last="Partridge">David G. Partridge</name>
<affiliation><nlm:affiliation>Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield S10 2JF, UK.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Evans, Cariad M" sort="Evans, Cariad M" uniqKey="Evans C" first="Cariad M" last="Evans">Cariad M. Evans</name>
<affiliation><nlm:affiliation>Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield S10 2JF, UK.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Freeman, Timothy M" sort="Freeman, Timothy M" uniqKey="Freeman T" first="Timothy M" last="Freeman">Timothy M. Freeman</name>
<affiliation><nlm:affiliation>Sheffield Biomedical Research Centre & Sheffield Bioinformatics Core, University of Sheffield, Sheffield S10 2HQ, UK.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="De Silva, Thushan I" sort="De Silva, Thushan I" uniqKey="De Silva T" first="Thushan I" last="De Silva">Thushan I. De Silva</name>
<affiliation><nlm:affiliation>Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield S10 2JF, UK; Department of Infection, Immunity and Cardiovascular Disease, Medical School, University of Sheffield, Sheffield S10 2RX, UK.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Mcdanal, Charlene" sort="Mcdanal, Charlene" uniqKey="Mcdanal C" first="Charlene" last="Mcdanal">Charlene Mcdanal</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Perez, Lautaro G" sort="Perez, Lautaro G" uniqKey="Perez L" first="Lautaro G" last="Perez">Lautaro G. Perez</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Tang, Haili" sort="Tang, Haili" uniqKey="Tang H" first="Haili" last="Tang">Haili Tang</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Moon Walker, Alex" sort="Moon Walker, Alex" uniqKey="Moon Walker A" first="Alex" last="Moon-Walker">Alex Moon-Walker</name>
<affiliation><nlm:affiliation>La Jolla Institute for Immunology, La Jolla, CA 92037, USA; Program in Virology, Harvard University, Boston, MA 02115, USA; Department of Molecular Microbiology, Washington University in Saint Louis, St. Louis, MO 63130, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Whelan, Sean P" sort="Whelan, Sean P" uniqKey="Whelan S" first="Sean P" last="Whelan">Sean P. Whelan</name>
<affiliation><nlm:affiliation>Department of Molecular Microbiology, Washington University in Saint Louis, St. Louis, MO 63130, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Labranche, Celia C" sort="Labranche, Celia C" uniqKey="Labranche C" first="Celia C" last="Labranche">Celia C. Labranche</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Saphire, Erica O" sort="Saphire, Erica O" uniqKey="Saphire E" first="Erica O" last="Saphire">Erica O. Saphire</name>
<affiliation><nlm:affiliation>La Jolla Institute for Immunology, La Jolla, CA 92037, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Montefiori, David C" sort="Montefiori, David C" uniqKey="Montefiori D" first="David C" last="Montefiori">David C. Montefiori</name>
<affiliation><nlm:affiliation>Duke Human Vaccine Institute & Department of Surgery, Durham, NC 27710, USA.</nlm:affiliation>
</affiliation>
</author>
</analytic>
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<front><div type="abstract" xml:lang="en">A SARS-CoV-2 variant carrying the Spike protein amino acid change D614G has become the most prevalent form in the global pandemic. Dynamic tracking of variant frequencies revealed a recurrent pattern of G614 increase at multiple geographic levels: national, regional, and municipal. The shift occurred even in local epidemics where the original D614 form was well established prior to introduction of the G614 variant. The consistency of this pattern was highly statistically significant, suggesting that the G614 variant may have a fitness advantage. We found that the G614 variant grows to a higher titer as pseudotyped virions. In infected individuals, G614 is associated with lower RT-PCR cycle thresholds, suggestive of higher upper respiratory tract viral loads, but not with increased disease severity. These findings illuminate changes important for a mechanistic understanding of the virus and support continuing surveillance of Spike mutations to aid with development of immunological interventions.</div>
</front>
</TEI>
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<DateRevised><Year>2020</Year>
<Month>07</Month>
<Day>25</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1097-4172</ISSN>
<JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year>
<Month>Jul</Month>
<Day>03</Day>
</PubDate>
</JournalIssue>
<Title>Cell</Title>
<ISOAbbreviation>Cell</ISOAbbreviation>
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<ArticleTitle>Tracking Changes in SARS-CoV-2 Spike: Evidence that D614G Increases Infectivity of the COVID-19 Virus.</ArticleTitle>
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<Abstract><AbstractText>A SARS-CoV-2 variant carrying the Spike protein amino acid change D614G has become the most prevalent form in the global pandemic. Dynamic tracking of variant frequencies revealed a recurrent pattern of G614 increase at multiple geographic levels: national, regional, and municipal. The shift occurred even in local epidemics where the original D614 form was well established prior to introduction of the G614 variant. The consistency of this pattern was highly statistically significant, suggesting that the G614 variant may have a fitness advantage. We found that the G614 variant grows to a higher titer as pseudotyped virions. In infected individuals, G614 is associated with lower RT-PCR cycle thresholds, suggestive of higher upper respiratory tract viral loads, but not with increased disease severity. These findings illuminate changes important for a mechanistic understanding of the virus and support continuing surveillance of Spike mutations to aid with development of immunological interventions.</AbstractText>
<CopyrightInformation>Published by Elsevier Inc.</CopyrightInformation>
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<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Korber</LastName>
<ForeName>Bette</ForeName>
<Initials>B</Initials>
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</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Fischer</LastName>
<ForeName>Will M</ForeName>
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<AffiliationInfo><Affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Gnanakaran</LastName>
<ForeName>Sandrasegaram</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yoon</LastName>
<ForeName>Hyejin</ForeName>
<Initials>H</Initials>
<AffiliationInfo><Affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Theiler</LastName>
<ForeName>James</ForeName>
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</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Abfalterer</LastName>
<ForeName>Werner</ForeName>
<Initials>W</Initials>
<AffiliationInfo><Affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</Affiliation>
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<Author ValidYN="Y"><LastName>Hengartner</LastName>
<ForeName>Nick</ForeName>
<Initials>N</Initials>
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<Author ValidYN="Y"><LastName>Giorgi</LastName>
<ForeName>Elena E</ForeName>
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<AffiliationInfo><Affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Bhattacharya</LastName>
<ForeName>Tanmoy</ForeName>
<Initials>T</Initials>
<AffiliationInfo><Affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Foley</LastName>
<ForeName>Brian</ForeName>
<Initials>B</Initials>
<AffiliationInfo><Affiliation>Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Hastie</LastName>
<ForeName>Kathryn M</ForeName>
<Initials>KM</Initials>
<AffiliationInfo><Affiliation>La Jolla Institute for Immunology, La Jolla, CA 92037, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Parker</LastName>
<ForeName>Matthew D</ForeName>
<Initials>MD</Initials>
<AffiliationInfo><Affiliation>Sheffield Biomedical Research Centre & Sheffield Bioinformatics Core, University of Sheffield, Sheffield S10 2HQ, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Partridge</LastName>
<ForeName>David G</ForeName>
<Initials>DG</Initials>
<AffiliationInfo><Affiliation>Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield S10 2JF, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Evans</LastName>
<ForeName>Cariad M</ForeName>
<Initials>CM</Initials>
<AffiliationInfo><Affiliation>Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield S10 2JF, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Freeman</LastName>
<ForeName>Timothy M</ForeName>
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<Initials>D</Initials>
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