Griffithsin: An Antiviral Lectin with Outstanding Therapeutic Potential
Identifieur interne : 000582 ( Ncbi/Merge ); précédent : 000581; suivant : 000583Griffithsin: An Antiviral Lectin with Outstanding Therapeutic Potential
Auteurs : Sabrina Lusvarghi ; Carole A. BewleySource :
- Viruses [ 1999-4915 ] ; 2016.
Abstract
Griffithsin (GRFT), an algae-derived lectin, is one of the most potent viral entry inhibitors discovered to date. It is currently being developed as a microbicide with broad-spectrum activity against several enveloped viruses. GRFT can inhibit human immunodeficiency virus (HIV) infection at picomolar concentrations, surpassing the ability of most anti-HIV agents. The potential to inhibit other viruses as well as parasites has also been demonstrated. Griffithsin’s antiviral activity stems from its ability to bind terminal mannoses present in high-mannose oligosaccharides and crosslink these glycans on the surface of the viral envelope glycoproteins. Here, we review structural and biochemical studies that established mode of action and facilitated construction of GRFT analogs, mechanisms that may lead to resistance, and in vitro and pre-clinical results that support the therapeutic potential of this lectin.
Url:
DOI: 10.3390/v8100296
PubMed: 27783038
PubMed Central: 5086628
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Griffithsin: An Antiviral Lectin with Outstanding Therapeutic Potential</title><author><name sortKey="Lusvarghi, Sabrina" sort="Lusvarghi, Sabrina" uniqKey="Lusvarghi S" first="Sabrina" last="Lusvarghi">Sabrina Lusvarghi</name></author><author><name sortKey="Bewley, Carole A" sort="Bewley, Carole A" uniqKey="Bewley C" first="Carole A." last="Bewley">Carole A. Bewley</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27783038</idno><idno type="pmc">5086628</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5086628</idno><idno type="RBID">PMC:5086628</idno><idno type="doi">10.3390/v8100296</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000803</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000803</idno><idno type="wicri:Area/Pmc/Curation">000803</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000803</idno><idno type="wicri:Area/Pmc/Checkpoint">000269</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000269</idno><idno type="wicri:Area/Ncbi/Merge">000582</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Griffithsin: An Antiviral Lectin with Outstanding Therapeutic Potential</title><author><name sortKey="Lusvarghi, Sabrina" sort="Lusvarghi, Sabrina" uniqKey="Lusvarghi S" first="Sabrina" last="Lusvarghi">Sabrina Lusvarghi</name></author><author><name sortKey="Bewley, Carole A" sort="Bewley, Carole A" uniqKey="Bewley C" first="Carole A." last="Bewley">Carole A. Bewley</name></author></analytic><series><title level="j">Viruses</title><idno type="eISSN">1999-4915</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Griffithsin (GRFT), an algae-derived lectin, is one of the most potent viral entry inhibitors discovered to date. It is currently being developed as a microbicide with broad-spectrum activity against several enveloped viruses. GRFT can inhibit human immunodeficiency virus (HIV) infection at picomolar concentrations, surpassing the ability of most anti-HIV agents. The potential to inhibit other viruses as well as parasites has also been demonstrated. Griffithsin’s antiviral activity stems from its ability to bind terminal mannoses present in high-mannose oligosaccharides and crosslink these glycans on the surface of the viral envelope glycoproteins. Here, we review structural and biochemical studies that established mode of action and facilitated construction of GRFT analogs, mechanisms that may lead to resistance, and in vitro and pre-clinical results that support the therapeutic potential of this lectin.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Doms, R W" uniqKey="Doms R">R.W. Doms</name></author><author><name sortKey="Moore, J P" uniqKey="Moore J">J.P. Moore</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Harrison, S C" uniqKey="Harrison S">S.C. Harrison</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Burton, D R" uniqKey="Burton D">D.R. Burton</name></author><author><name sortKey="Poignard, P" uniqKey="Poignard P">P. Poignard</name></author><author><name sortKey="Stanfield, R L" uniqKey="Stanfield R">R.L. Stanfield</name></author><author><name sortKey="Wilson, I A" uniqKey="Wilson I">I.A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Viruses</journal-id><journal-id journal-id-type="iso-abbrev">Viruses</journal-id><journal-id journal-id-type="publisher-id">viruses</journal-id><journal-title-group><journal-title>Viruses</journal-title></journal-title-group><issn pub-type="epub">1999-4915</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27783038</article-id><article-id pub-id-type="pmc">5086628</article-id><article-id pub-id-type="doi">10.3390/v8100296</article-id><article-id pub-id-type="publisher-id">viruses-08-00296</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Griffithsin: An Antiviral Lectin with Outstanding Therapeutic Potential</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Lusvarghi</surname><given-names>Sabrina</given-names></name></contrib><contrib contrib-type="author"><name><surname>Bewley</surname><given-names>Carole A.</given-names></name><xref rid="c1-viruses-08-00296" ref-type="corresp">*</xref></contrib></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>O’Keefe</surname><given-names>Barry R.</given-names></name><role>Academic Editor</role></contrib></contrib-group><aff id="af1-viruses-08-00296">Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA;<email>sabrinal@mail.nih.gov</email></aff><author-notes><corresp id="c1-viruses-08-00296"><label>*</label>Correspondence: <email>caroleb@mail.nih.gov</email>; Tel.: +1-301-594-5187</corresp></author-notes><pub-date pub-type="epub"><day>24</day><month>10</month><year>2016</year></pub-date><pub-date pub-type="collection"><month>10</month><year>2016</year></pub-date><volume>8</volume><issue>10</issue><elocation-id>296</elocation-id><history><date date-type="received"><day>02</day><month>9</month><year>2016</year></date><date date-type="accepted"><day>13</day><month>10</month><year>2016</year></date></history><permissions><copyright-statement>© 2016 by the authors; licensee MDPI, Basel, Switzerland.</copyright-statement><copyright-year>2016</copyright-year><license><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>).</license-p></license></permissions><abstract><p>Griffithsin (GRFT), an algae-derived lectin, is one of the most potent viral entry inhibitors discovered to date. It is currently being developed as a microbicide with broad-spectrum activity against several enveloped viruses. GRFT can inhibit human immunodeficiency virus (HIV) infection at picomolar concentrations, surpassing the ability of most anti-HIV agents. The potential to inhibit other viruses as well as parasites has also been demonstrated. Griffithsin’s antiviral activity stems from its ability to bind terminal mannoses present in high-mannose oligosaccharides and crosslink these glycans on the surface of the viral envelope glycoproteins. Here, we review structural and biochemical studies that established mode of action and facilitated construction of GRFT analogs, mechanisms that may lead to resistance, and in vitro and pre-clinical results that support the therapeutic potential of this lectin.</p></abstract><kwd-group><kwd>carbohydrate binding agent</kwd><kwd>viral envelope glycoproteins</kwd><kwd>multivalency</kwd><kwd>resistance</kwd><kwd>immunogenicity</kwd><kwd>HIV</kwd><kwd>HSV</kwd><kwd>HCV</kwd></kwd-group></article-meta></front><floats-group><fig id="viruses-08-00296-f001" position="float"><label>Figure 1</label><caption><p>Sequence and three-dimensional structure of griffithsin (GRFT). (<bold>A</bold>) Sequence of wild-type GRFT. Amino acids located within beta strands are colored red and the black arrows correspond to secondary structure. X represents an unknown amino acid of mass 151.05 present in the natural alga-derived material. The blue triangle shows the site of the Gly-Ser insertion used to produce the monomeric version of GRFT (mGRFT). The three Asp residues located in the three mannose-binding sites are shown in bold; (<bold>B</bold>) Ribbon drawing showing the three-dimensional structure of GRFT. Each monomer of the domain swapped dimer is colored yellow or blue. Mannose residues bound to the carbohydrate binding sites are shown in stick representation. Aspartic acids present in the binding sites are colored purple; (<bold>C</bold>) Rotated view of GRFT showing the carbohydrate binding face and mannose binding sites. (<bold>B</bold>,<bold>C</bold>) were generated using the program Pymol (Delano Scientific LLC, Palo Alto, CA, USA) and protein data bank accession number 2GUD.</p></caption><graphic xlink:href="viruses-08-00296-g001"></graphic></fig><fig id="viruses-08-00296-f002" position="float"><label>Figure 2</label><caption><p>Model of a GRFT-Man9 complex. (<bold>A</bold>) Representation of the structure of monomeric GRFT (gray surface) bound to nonamannoside (green sticks), Protein Data Bank accession 3LL2. Aspartic acid residues from each of the three glycan-binding sites are highlighted in grey. The structures of a GRFT:synthetic nonamannoside complex and a 1:3 mGRFT:mannose complex have been superimposed to compare the mannose binding sites. Only the D1 and D2 terminal mannoses are bound to a single GRFT monomer. Figure was rendered using PyMol. (<bold>B</bold>) Chemical structure of nonamannoside showing the D1, D2 and D3 arms; (<bold>C</bold>) Symbol representation of nonamannoside.</p></caption><graphic xlink:href="viruses-08-00296-g002"></graphic></fig><fig id="viruses-08-00296-f003" position="float"><label>Figure 3</label><caption><p>Schematic showing distribution of the predicted asparagine-linked glycosylation sites of envelope glycoproteins belonging to different viruses inhibited by GRFT. HIV: human immunodeficiency virus; HCV: hepatitis C virus; SARS-CoV: severe acute respiratory syndrome coronavirus; JEV: Japanese encephalitis virus; gp120: envelope glycoprotein gp120; gp41: transmembrane protein gp41; E1 and E2: envelope glycoprotein 1 and 2 respectively; S: spyke protein; E: envelope glycoprotein; prM: premembrane gycoprotein.</p></caption><graphic xlink:href="viruses-08-00296-g003"></graphic></fig><fig id="viruses-08-00296-f004" position="float"><label>Figure 4</label><caption><p>Structure of glycosylated HIV-1 gp120 trimer with full-length glycans modeled onto the protein. The surface envelope glycoprotein gp120 and transmembrane protein gp41 are shown as yellow and gray surfaces, respectively. CD4 receptor and co-receptor binding sites are colored blue and purple, respectively. Glycans found to be deleted in resistance studies are colored red (glycans 234, 295, 339, 386, 392 and 448). Other glycans shown to be deleted in GRFT-resistant strains but not present in this structure include glycans 230, 241 and 298. Model was rendered with Pymol. Model was constructed by C. Soto, PDB Accession Number 5FYK [<xref rid="B44-viruses-08-00296" ref-type="bibr">44</xref>] and rendered with Pymol.</p></caption><graphic xlink:href="viruses-08-00296-g004"></graphic></fig><table-wrap id="viruses-08-00296-t001" position="float"><object-id pub-id-type="pii">viruses-08-00296-t001_Table 1</object-id><label>Table 1</label><caption><p>Recombinant expression of griffithsin.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Expression System</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Yield</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Recovery after Purification</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>E. coli</italic> BL21(DE3)—shake flasks</td><td align="center" valign="middle" rowspan="1" colspan="1">12 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B10-viruses-08-00296" ref-type="bibr">10</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>E. coli</italic> BL21(DE3)—fermenter</td><td align="center" valign="middle" rowspan="1" colspan="1">819 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">542 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B10-viruses-08-00296" ref-type="bibr">10</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Tobacco leaves (<italic>Nicotiana benthamiana</italic>)</td><td align="center" valign="middle" rowspan="1" colspan="1">1 g/kg leaf</td><td align="center" valign="middle" rowspan="1" colspan="1">300 mg/kg</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B11-viruses-08-00296" ref-type="bibr">11</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Rice seeds (<italic>Oryza sativa</italic> endosperm)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">301 mg/kg dry seed</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">223 mg/kg</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B13-viruses-08-00296" ref-type="bibr">13</xref>]</td></tr></tbody></table></table-wrap><table-wrap id="viruses-08-00296-t002" position="float"><object-id pub-id-type="pii">viruses-08-00296-t002_Table 2</object-id><label>Table 2</label><caption><p>Effective concentrations to inhibit 50% of virus infection (EC<sub>50</sub>) of GRFT against different viruses.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Sample</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Virus <sup>a</sup></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Target Cell <sup>b</sup></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">EC<sub>50</sub> (nM)</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Native GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HIV-1<sub>RF</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">CEM-SS</td><td align="center" valign="middle" rowspan="1" colspan="1">0.043</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B9-viruses-08-00296" ref-type="bibr">9</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HIV-1<sub>RF</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">CEM-SS</td><td align="center" valign="middle" rowspan="1" colspan="1">0.039</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B9-viruses-08-00296" ref-type="bibr">9</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Native GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HIV-1<sub>RoJo</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">PBMC</td><td align="center" valign="middle" rowspan="1" colspan="1">0.63</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B9-viruses-08-00296" ref-type="bibr">9</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Native GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HIV-1<sub>ADA</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Macrophage</td><td align="center" valign="middle" rowspan="1" colspan="1">0.5</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B9-viruses-08-00296" ref-type="bibr">9</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Native GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HIV-1<sub>Ba-L</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Macrophage</td><td align="center" valign="middle" rowspan="1" colspan="1">0.098</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B9-viruses-08-00296" ref-type="bibr">9</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HIV-1<sub>Ba-L</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">PMBC</td><td align="center" valign="middle" rowspan="1" colspan="1">0.01</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B28-viruses-08-00296" ref-type="bibr">28</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HIV-1<sub>LAI</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">MT-4</td><td align="center" valign="middle" rowspan="1" colspan="1">0.01</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B28-viruses-08-00296" ref-type="bibr">28</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HIV-2<sub>ROD</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">MT-4</td><td align="center" valign="middle" rowspan="1" colspan="1">0.17</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B29-viruses-08-00296" ref-type="bibr">29</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">SIV <sub>mac251</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">CEMx174</td><td align="center" valign="middle" rowspan="1" colspan="1">0.35</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B28-viruses-08-00296" ref-type="bibr">28</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">SARS-CoV<sub>200300592</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Vero 76</td><td align="center" valign="middle" rowspan="1" colspan="1">280</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-viruses-08-00296" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">SARS-CoV<sub>200300592</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Vero 76</td><td align="center" valign="middle" rowspan="1" colspan="1">960</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-viruses-08-00296" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">SARS-CoV<sub>Urbani</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Vero 76</td><td align="center" valign="middle" rowspan="1" colspan="1">48</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B30-viruses-08-00296" ref-type="bibr">30</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">SARS-CoV<sub>Tor-II</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Vero 76</td><td align="center" valign="middle" rowspan="1" colspan="1">48</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B30-viruses-08-00296" ref-type="bibr">30</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">SARS-CoV<sub>CuHK</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Vero 76</td><td align="center" valign="middle" rowspan="1" colspan="1">61</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B30-viruses-08-00296" ref-type="bibr">30</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">SARS-CoV<sub>Frank</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Vero 76</td><td align="center" valign="middle" rowspan="1" colspan="1">94</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B30-viruses-08-00296" ref-type="bibr">30</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HCV<sub>JFH1</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Huh-7</td><td align="center" valign="middle" rowspan="1" colspan="1">13.9</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B31-viruses-08-00296" ref-type="bibr">31</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HCV<sub>JFH-1</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">Huh 7.5.1</td><td align="center" valign="middle" rowspan="1" colspan="1">0.4</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B32-viruses-08-00296" ref-type="bibr">32</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">JEV</td><td align="center" valign="middle" rowspan="1" colspan="1">BHK-21</td><td align="center" valign="middle" rowspan="1" colspan="1">20</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B33-viruses-08-00296" ref-type="bibr">33</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HPV<sub>16 PsV</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">HeLa</td><td align="center" valign="middle" rowspan="1" colspan="1">1390</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B34-viruses-08-00296" ref-type="bibr">34</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" rowspan="1" colspan="1">HPV<sub>18 PsV</sub></td><td align="center" valign="middle" rowspan="1" colspan="1">HeLa</td><td align="center" valign="middle" rowspan="1" colspan="1">428</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B34-viruses-08-00296" ref-type="bibr">34</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Recombinant GRFT</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HPV<sub>45 PsV</sub></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HeLa</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">928</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B34-viruses-08-00296" ref-type="bibr">34</xref>]</td></tr></tbody></table><table-wrap-foot><fn><p><sup>a</sup> HIV-1: human immunodeficiency virus type 1; HIV-2: human immunodeficiency virus type 2; SIV: simian immunodeficiency virus; SARS-CoV: severe acute respiratory syndrome corona virus; HCV: hepatitis C virus; JEV: Japanese encephalitis virus; HPV: humanpapillomavirus. <sup>b</sup> CEM-SS: human T-lymphoblastoid cell line; PBMC: peripheral blood mononuclear cell; BHK-21: baby hamster kidney fibroblasts; MT-4 human T cells isolated from a patient with adult T cell leukemia; CEMx174: somatic cell hybrid culture between CEM and B cell like 174 both of human origin; Vero 76: kidney epithelial cells extracted from an African green monkey; Huh: differentiated hepatocyte-derived carcinoma cell line.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list></list><tree><noCountry><name sortKey="Bewley, Carole A" sort="Bewley, Carole A" uniqKey="Bewley C" first="Carole A." last="Bewley">Carole A. 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