Structural basis of development of multi-epitope vaccine against Middle East respiratory syndrome using in silico approach
Identifieur interne : 000596 ( Pmc/Curation ); précédent : 000595; suivant : 000597Structural basis of development of multi-epitope vaccine against Middle East respiratory syndrome using in silico approach
Auteurs : Sukrit Srivastava ; Mohit Kamthania [Inde] ; Soni Singh ; Ajay K. Saxena ; Nishi SharmaSource :
- Infection and Drug Resistance [ 1178-6973 ] ; 2018.
Abstract
Middle East respiratory syndrome (MERS) is caused by MERS coronavirus (MERS-CoV). Thus far, MERS outbreaks have been reported from Saudi Arabia (2013 and 2014) and South Korea (2015). No specific vaccine has yet been reported against MERS.
To address the urgent need for an MERS vaccine, in the present study, we have designed two multi-epitope vaccines (MEVs) against MERS utilizing several in silico methods and tools.
The design of both the multi-epitope vaccines (MEVs) are composed of cytotoxic T lymphocyte (CTL) and helper T lymphocyte (HTL) epitopes, screened form thirteen different proteins of MERS-CoV. Both the MEVs also carry potential B-cell linear epitope regions, B-cell discontinuous epitopes as well as interferon-γ-inducing epitopes. Human β-defensin-2 and β-defensin-3 were used as adjuvants to enhance the immune response of MEVs. To design the MEVs, short peptide molecular linkers were utilized to link screened most potential CTL epitopes, HTL epitopes and the adjuvants. Tertiary models for both the MEVs were generated, refined, and further studied for their molecular interaction with toll-like receptor 3. The cDNAs of both MEVs were generated and analyzed in silico for their expression in a mammalian host cell line (human).
Screened CTL and HTL epitopes were found to have high propensity for stable molecular interaction with HLA alleles molecules. CTL epitopes were also found to have favorable molecular interaction within the cavity of transporter associated with antigen processing. The selected CTL and HTL epitopes jointly cover upto 94.0% of worldwide human population. Both the CTL and HTL MEVs molecular models have shown to have stable binding and complex formation propensity with toll-like receptor 3. The cDNA analysis of both the MEVs have shown high expression tendency in mammalian host cell line (human).
After multistage in silico analysis, both the MEVs are predicted to elicit humoral as well as cell mediated immune response. Epitopes of the designed MEVs are predicted to cover large human population worldwide. Hence both the designed MEVs could be tried in vivo as potential vaccine candidates against MERS.
Url:
DOI: 10.2147/IDR.S175114
PubMed: 30538505
PubMed Central: 6254671
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Structural basis of development of multi-epitope vaccine against Middle East respiratory syndrome using in silico approach</title><author><name sortKey="Srivastava, Sukrit" sort="Srivastava, Sukrit" uniqKey="Srivastava S" first="Sukrit" last="Srivastava">Sukrit Srivastava</name><affiliation><nlm:aff id="af1-idr-11-2377">Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation><affiliation><nlm:aff id="af2-idr-11-2377">Molecular Medicine Lab, School of Life Sciences, Jawaharlal Nehru University, New Delhi, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Kamthania, Mohit" sort="Kamthania, Mohit" uniqKey="Kamthania M" first="Mohit" last="Kamthania">Mohit Kamthania</name><affiliation><nlm:aff id="af1-idr-11-2377">Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af3-idr-11-2377">Department of Biotechnology, Faculty of Life Sciences, Institute of Applied Medicines and Research, Ghaziabad, Uttar Pradesh, India</nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>Department of Biotechnology, Faculty of Life Sciences, Institute of Applied Medicines and Research, Ghaziabad, Uttar Pradesh</wicri:regionArea></affiliation></author><author><name sortKey="Singh, Soni" sort="Singh, Soni" uniqKey="Singh S" first="Soni" last="Singh">Soni Singh</name><affiliation><nlm:aff id="af1-idr-11-2377">Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Saxena, Ajay K" sort="Saxena, Ajay K" uniqKey="Saxena A" first="Ajay K" last="Saxena">Ajay K. Saxena</name><affiliation><nlm:aff id="af2-idr-11-2377">Molecular Medicine Lab, School of Life Sciences, Jawaharlal Nehru University, New Delhi, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Sharma, Nishi" sort="Sharma, Nishi" uniqKey="Sharma N" first="Nishi" last="Sharma">Nishi Sharma</name><affiliation><nlm:aff id="af1-idr-11-2377">Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">30538505</idno><idno type="pmc">6254671</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6254671</idno><idno type="RBID">PMC:6254671</idno><idno type="doi">10.2147/IDR.S175114</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">000596</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000596</idno><idno type="wicri:Area/Pmc/Curation">000596</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000596</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Structural basis of development of multi-epitope vaccine against Middle East respiratory syndrome using in silico approach</title><author><name sortKey="Srivastava, Sukrit" sort="Srivastava, Sukrit" uniqKey="Srivastava S" first="Sukrit" last="Srivastava">Sukrit Srivastava</name><affiliation><nlm:aff id="af1-idr-11-2377">Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation><affiliation><nlm:aff id="af2-idr-11-2377">Molecular Medicine Lab, School of Life Sciences, Jawaharlal Nehru University, New Delhi, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Kamthania, Mohit" sort="Kamthania, Mohit" uniqKey="Kamthania M" first="Mohit" last="Kamthania">Mohit Kamthania</name><affiliation><nlm:aff id="af1-idr-11-2377">Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af3-idr-11-2377">Department of Biotechnology, Faculty of Life Sciences, Institute of Applied Medicines and Research, Ghaziabad, Uttar Pradesh, India</nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>Department of Biotechnology, Faculty of Life Sciences, Institute of Applied Medicines and Research, Ghaziabad, Uttar Pradesh</wicri:regionArea></affiliation></author><author><name sortKey="Singh, Soni" sort="Singh, Soni" uniqKey="Singh S" first="Soni" last="Singh">Soni Singh</name><affiliation><nlm:aff id="af1-idr-11-2377">Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Saxena, Ajay K" sort="Saxena, Ajay K" uniqKey="Saxena A" first="Ajay K" last="Saxena">Ajay K. Saxena</name><affiliation><nlm:aff id="af2-idr-11-2377">Molecular Medicine Lab, School of Life Sciences, Jawaharlal Nehru University, New Delhi, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Sharma, Nishi" sort="Sharma, Nishi" uniqKey="Sharma N" first="Nishi" last="Sharma">Nishi Sharma</name><affiliation><nlm:aff id="af1-idr-11-2377">Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></nlm:aff></affiliation></author></analytic><series><title level="j">Infection and Drug Resistance</title><idno type="eISSN">1178-6973</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Middle East respiratory syndrome (MERS) is caused by MERS coronavirus (MERS-CoV). Thus far, MERS outbreaks have been reported from Saudi Arabia (2013 and 2014) and South Korea (2015). No specific vaccine has yet been reported against MERS.</p></sec><sec><title>Purpose</title><p>To address the urgent need for an MERS vaccine, in the present study, we have designed two multi-epitope vaccines (MEVs) against MERS utilizing several in silico methods and tools.</p></sec><sec><title>Methods</title><p>The design of both the multi-epitope vaccines (MEVs) are composed of cytotoxic T lymphocyte (CTL) and helper T lymphocyte (HTL) epitopes, screened form thirteen different proteins of MERS-CoV. Both the MEVs also carry potential B-cell linear epitope regions, B-cell discontinuous epitopes as well as interferon-γ-inducing epitopes. Human β-defensin-2 and β-defensin-3 were used as adjuvants to enhance the immune response of MEVs. To design the MEVs, short peptide molecular linkers were utilized to link screened most potential CTL epitopes, HTL epitopes and the adjuvants. Tertiary models for both the MEVs were generated, refined, and further studied for their molecular interaction with toll-like receptor 3. The cDNAs of both MEVs were generated and analyzed in silico for their expression in a mammalian host cell line (human).</p></sec><sec><title>Results</title><p>Screened CTL and HTL epitopes were found to have high propensity for stable molecular interaction with HLA alleles molecules. CTL epitopes were also found to have favorable molecular interaction within the cavity of transporter associated with antigen processing. The selected CTL and HTL epitopes jointly cover upto 94.0% of worldwide human population. Both the CTL and HTL MEVs molecular models have shown to have stable binding and complex formation propensity with toll-like receptor 3. The cDNA analysis of both the MEVs have shown high expression tendency in mammalian host cell line (human).</p></sec><sec><title>Conclusion</title><p>After multistage in silico analysis, both the MEVs are predicted to elicit humoral as well as cell mediated immune response. Epitopes of the designed MEVs are predicted to cover large human population worldwide. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Infect Drug Resist</journal-id><journal-id journal-id-type="iso-abbrev">Infect Drug Resist</journal-id><journal-id journal-id-type="publisher-id">Infection and Drug Resistance</journal-id><journal-title-group><journal-title>Infection and Drug Resistance</journal-title></journal-title-group><issn pub-type="epub">1178-6973</issn><publisher><publisher-name>Dove Medical Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30538505</article-id><article-id pub-id-type="pmc">6254671</article-id><article-id pub-id-type="doi">10.2147/IDR.S175114</article-id><article-id pub-id-type="publisher-id">idr-11-2377</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Research</subject></subj-group></article-categories><title-group><article-title>Structural basis of development of multi-epitope vaccine against Middle East respiratory syndrome using in silico approach</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Srivastava</surname><given-names>Sukrit</given-names></name><xref ref-type="aff" rid="af1-idr-11-2377">1</xref><xref ref-type="aff" rid="af2-idr-11-2377">2</xref><xref ref-type="corresp" rid="c1-idr-11-2377"></xref></contrib><contrib contrib-type="author"><name><surname>Kamthania</surname><given-names>Mohit</given-names></name><xref ref-type="aff" rid="af1-idr-11-2377">1</xref><xref ref-type="aff" rid="af3-idr-11-2377">3</xref></contrib><contrib contrib-type="author"><name><surname>Singh</surname><given-names>Soni</given-names></name><xref ref-type="aff" rid="af1-idr-11-2377">1</xref></contrib><contrib contrib-type="author"><name><surname>Saxena</surname><given-names>Ajay K</given-names></name><xref ref-type="aff" rid="af2-idr-11-2377">2</xref></contrib><contrib contrib-type="author"><name><surname>Sharma</surname><given-names>Nishi</given-names></name><xref ref-type="aff" rid="af1-idr-11-2377">1</xref></contrib></contrib-group><aff id="af1-idr-11-2377"><label>1</label>Department of Biotechnology, Mangalayatan University, Aligarh, India,<email>srivastav.sukrit@gmail.com</email></aff><aff id="af2-idr-11-2377"><label>2</label>Molecular Medicine Lab, School of Life Sciences, Jawaharlal Nehru University, New Delhi, India,<email>srivastav.sukrit@gmail.com</email></aff><aff id="af3-idr-11-2377"><label>3</label>Department of Biotechnology, Faculty of Life Sciences, Institute of Applied Medicines and Research, Ghaziabad, Uttar Pradesh, India</aff><author-notes><corresp id="c1-idr-11-2377">Correspondence: Sukrit Srivastava, Department of Biotechnology, Mangalayatan University, Aligarh, Uttar Pradesh 202146, India, Email <email>srivastav.sukrit@gmail.com</email></corresp></author-notes><pub-date pub-type="collection"><year>2018</year></pub-date><pub-date pub-type="epub"><day>21</day><month>11</month><year>2018</year></pub-date><volume>11</volume><fpage>2377</fpage><lpage>2391</lpage><permissions><copyright-statement>© 2018 Srivastava et al. This work is published and licensed by Dove Medical Press Limited</copyright-statement><copyright-year>2018</copyright-year><license><license-p>The full terms of this license are available at <ext-link ext-link-type="uri" xlink:href="https://www.dovepress.com/terms.php">https://www.dovepress.com/terms.php</ext-link> and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/">http://creativecommons.org/licenses/by-nc/3.0/</ext-link>). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed.</license-p></license></permissions><abstract><sec><title>Background</title><p>Middle East respiratory syndrome (MERS) is caused by MERS coronavirus (MERS-CoV). Thus far, MERS outbreaks have been reported from Saudi Arabia (2013 and 2014) and South Korea (2015). No specific vaccine has yet been reported against MERS.</p></sec><sec><title>Purpose</title><p>To address the urgent need for an MERS vaccine, in the present study, we have designed two multi-epitope vaccines (MEVs) against MERS utilizing several in silico methods and tools.</p></sec><sec><title>Methods</title><p>The design of both the multi-epitope vaccines (MEVs) are composed of cytotoxic T lymphocyte (CTL) and helper T lymphocyte (HTL) epitopes, screened form thirteen different proteins of MERS-CoV. Both the MEVs also carry potential B-cell linear epitope regions, B-cell discontinuous epitopes as well as interferon-γ-inducing epitopes. Human β-defensin-2 and β-defensin-3 were used as adjuvants to enhance the immune response of MEVs. To design the MEVs, short peptide molecular linkers were utilized to link screened most potential CTL epitopes, HTL epitopes and the adjuvants. Tertiary models for both the MEVs were generated, refined, and further studied for their molecular interaction with toll-like receptor 3. The cDNAs of both MEVs were generated and analyzed in silico for their expression in a mammalian host cell line (human).</p></sec><sec><title>Results</title><p>Screened CTL and HTL epitopes were found to have high propensity for stable molecular interaction with HLA alleles molecules. CTL epitopes were also found to have favorable molecular interaction within the cavity of transporter associated with antigen processing. The selected CTL and HTL epitopes jointly cover upto 94.0% of worldwide human population. Both the CTL and HTL MEVs molecular models have shown to have stable binding and complex formation propensity with toll-like receptor 3. The cDNA analysis of both the MEVs have shown high expression tendency in mammalian host cell line (human).</p></sec><sec><title>Conclusion</title><p>After multistage in silico analysis, both the MEVs are predicted to elicit humoral as well as cell mediated immune response. Epitopes of the designed MEVs are predicted to cover large human population worldwide. Hence both the designed MEVs could be tried in vivo as potential vaccine candidates against MERS.</p></sec></abstract><kwd-group><title>Keywords</title><kwd>Middle East respiratory syndrome</kwd><kwd>MERS</kwd><kwd>Middle East respiratory syndrome coronavirus</kwd><kwd>MERS-CoV</kwd><kwd>human transporter associated with antigen processing</kwd><kwd>TAP</kwd><kwd>toll-like receptor 3</kwd><kwd>TLR-3</kwd><kwd>epitope</kwd><kwd>immunoinformatics</kwd><kwd>molecular docking</kwd><kwd>molecular dynamics simulation</kwd><kwd>MD simulation</kwd><kwd>multi-epitope vaccine</kwd></kwd-group></article-meta></front><floats-group><fig id="f1-idr-11-2377" position="float"><label>Figure 1</label><caption><p>Multi-epitope vaccine design.</p><p><bold>Notes:</bold> (<bold>A</bold>) CTL and (<bold>B</bold>) HTL epitopes were linked by the short peptide linker GGGGS. Human β-defensin-2 and β-defensin-3 were used as adjuvant at N and C terminals, respectively, linked by the short peptide linker EAAAK. Epitopes from different proteins are colored in different colors. C-terminal 6xHis is designated as His tag.</p><p><bold>Abbreviations:</bold> CTL, cytotoxic T lymphocyte; HTL, helper T lymphocyte.</p></caption><graphic xlink:href="idr-11-2377Fig1"></graphic></fig><fig id="f2-idr-11-2377" position="float"><label>Figure 2</label><caption><p>Overlapping regions of the BepiPred linear B-cell epitopes and the epitopes predicted by other methods.</p><p><bold>Notes:</bold> This analysis shows a strong consensus between the BepiPred linear B-cell epitopes and the epitopes predicted by other sequence-based and structure-based epitope prediction methods. Different colors are used to highlight overlapping regions of epitopes predicted by the different methods.</p></caption><graphic xlink:href="idr-11-2377Fig2"></graphic></fig><fig id="f3-idr-11-2377" position="float"><label>Figure 3</label><caption><p>Overlapping CTL, HTL, and B-cell epitopes.</p><p><bold>Notes:</bold> Overlapping CTL (red), HTL (blue), and B-cell epitopes (green) were sorted out by MSA using Clustal Omega at EBI server. The ringed clusters of epitopes involve all three types of epitopes, epitopes with full sequence overlap, and the epitopes with highest number of HLA allele binders.</p><p><bold>Abbreviations:</bold> CTL, cytotoxic T lymphocyte; EBI, European Bioinformatics Institute; HLA, human leukocyte antigen; HTL, helper T lymphocyte; MSA, multiple sequence alignment.</p></caption><graphic xlink:href="idr-11-2377Fig3"></graphic></fig><fig id="f4-idr-11-2377" position="float"><label>Figure 4</label><caption><p>Molecular docking study of CTL and HTL epitopes with respective HLA allele binders.</p><p><bold>Notes:</bold> (<bold>A</bold>) CTL and (<bold>B</bold>) HTL epitopes docked with their respective HLA allele binders. The docking study shows acceptable negative binding energy and hydrogen bonds (green balls) formation between epitopes (magenta sticks) and HLA alleles (cyan cartoons). (*) Residues forming hydrogen bonds with more than one residue. <bold>Abbreviations:</bold> CTL, cytotoxic T lymphocyte; HLA, human leukocyte antigen; HTL, helper T lymphocyte.</p></caption><graphic xlink:href="idr-11-2377Fig4"></graphic></fig><fig id="f5-idr-11-2377" position="float"><label>Figure 5</label><caption><p>Molecular dynamics simulation study of the epitope and HLA allele complexes.</p><p><bold>Notes:</bold> Molecular dynamics simulation study of (<bold>A</bold>) CTL and (<bold>B</bold>) HTL epitope complexes with their respective HLA allele binders. The reasonably invariable RMSD value indicates a stable complex formation.</p><p><bold>Abbreviations:</bold> CTL, cytotoxic T lymphocyte; HLA, human leukocyte antigen; HTL, helper T lymphocyte; RMSD, root mean square deviation.</p></caption><graphic xlink:href="idr-11-2377Fig5"></graphic></fig><fig id="f6-idr-11-2377" position="float"><label>Figure 6</label><caption><p>Molecular docking study of CTL epitopes with the TAP cavity.</p><p><bold>Notes:</bold> TAP is shown by cyan ribbon, and epitopes are shown by magenta. In every panel of the epitope–TAP complex, (<bold>A</bold>) shows the binding of epitope at two different sites of the TAP cavity, (<bold>B</bold>) and (<bold>C</bold>) show the hydrogen bond formation between epitopes and TAP cavity residues at two respective sites of the TAP cavity. (*) Residues forming hydrogen bonds with more than one residue. (a and b) Chain A and B of TAP. Binding energy is shown in kcal/mol. Hydrogen bonds are shown by yellow dots.</p><p><bold>Abbreviations:</bold> CTL, cytotoxic T lymphocyte; TAP, transporter associated with antigen processing.</p></caption><graphic xlink:href="idr-11-2377Fig6"></graphic></fig><fig id="f7-idr-11-2377" position="float"><label>Figure 7</label><caption><p>3D structure modeling of CTL and HTL MEVs.</p><p><bold>Notes:</bold> (<bold>A</bold> and <bold>E</bold>) 3D structure of CTL and HTL MEVs models, respectively, showing epitopes from different proteins in different colors (epitope colors are the same as those shown in <xref ref-type="fig" rid="f1-idr-11-2377">Figure 1</xref>). (<bold>B</bold> and <bold>F</bold>) Overlapping regions belonging to B-cell linear epitopes from both CTL and HTL MEVs, respectively, are shown by spheres. From (<bold>C</bold>) CTL and (<bold>G</bold>) HTL MEVs, IFN-γ-inducing epitopes are shown in cyan, while discontinuous B-cell epitopes are shown in magenta. The regions shown in wheat color are common to both IFN-γ and discontinuous B-cell epitopes. (<bold>D</bold> and <bold>H</bold>) RAMPAGE analysis of refined CTL and HTL MEV models, respectively.</p><p><bold>Abbreviations:</bold> CTL, cytotoxic T lymphocyte; HTL, helper T lymphocyte; IFN, interferon; MEV, multi-epitope vaccine.</p></caption><graphic xlink:href="idr-11-2377Fig7"></graphic></fig><fig id="f8-idr-11-2377" position="float"><label>Figure 8</label><caption><p>Molecular docking and MD simulation study of CTL and HTL MEVs with TLR-3.</p><p><bold>Notes:</bold> (<bold>A</bold>) CTL and (<bold>E</bold>) HTL MEVs (cartoon) docked complex with TLR-3 (ribbon), respectively. B-factor of the complexes is shown by rainbow (VIBGYOR) presentation; the regions in blue are very stable, and the region in red is unstable. In the above complexes, most of the regions are in blue and a very small region is in yellow and orange, indicating that both complexes are very stable. (<bold>B</bold> and <bold>F</bold>) MD simulation study of CTL and HTL MEV complexes with TLR-3, respectively. (<bold>C</bold> and <bold>G</bold>) Rg across the time window of 6,000 ps for CTL and HTL MEV complexes with TLR-3, respectively. (<bold>D</bold> and <bold>H</bold>) RMSF for all the atoms of the CTL and HTL MEV complex with TLR-3, respectively.</p><p><bold>Abbreviations:</bold> CTL, cytotoxic T lymphocyte; HTL, helper T lymphocyte; MD, molecular dynamics; MEV, multi-epitope vaccine; Rg, radius of gyration; RMSD, root mean square deviation; RMSF, root mean square fluctuation; TLR-3, toll-like receptor 3.</p></caption><graphic xlink:href="idr-11-2377Fig8"></graphic></fig></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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