Molecular basis of the structure and function of H1 hemagglutinin of influenza virus
Identifieur interne : 000783 ( Ncbi/Merge ); précédent : 000782; suivant : 000784Molecular basis of the structure and function of H1 hemagglutinin of influenza virus
Auteurs : Nongluk Sriwilaijaroen ; Yasuo SuzukiSource :
- Proceedings of the Japan Academy. Series B, Physical and Biological Sciences [ 0386-2208 ] ; 2012.
Abstract
Influenza virus hemagglutinin (HA) contains antigenic sites recognized by the host immune system, cleavage sites cleaved by host proteases, receptor binding sites attaching to sialyl receptors on the target cell, and fusion peptides mediating membrane fusion. Change in an amino acid(s) in these sites may affect the potential of virus infection and spread within and between hosts. Influenza viruses with H1 HA infect birds, pigs and humans and have caused two of the four pandemics in the past 100 years: 1918 pandemic that killed 21–50 million people
Url:
DOI: 10.2183/pjab.88.226
PubMed: 22728439
PubMed Central: 3410141
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Molecular basis of the structure and function of H1 hemagglutinin of influenza virus</title><author><name sortKey="Sriwilaijaroen, Nongluk" sort="Sriwilaijaroen, Nongluk" uniqKey="Sriwilaijaroen N" first="Nongluk" last="Sriwilaijaroen">Nongluk Sriwilaijaroen</name><affiliation><nlm:aff id="aff01">Faculty of Medicine, Thammasat University (Rangsit Campus),<addr-line>Pathumthani, Thailand</addr-line>.</nlm:aff></affiliation><affiliation><nlm:aff id="aff02">Health Science Hills, College of Life and Health Sciences, Chubu University,<addr-line>Aichi, Japan</addr-line>.</nlm:aff></affiliation></author><author><name sortKey="Suzuki, Yasuo" sort="Suzuki, Yasuo" uniqKey="Suzuki Y" first="Yasuo" last="Suzuki">Yasuo Suzuki</name><affiliation><nlm:aff id="aff02">Health Science Hills, College of Life and Health Sciences, Chubu University,<addr-line>Aichi, Japan</addr-line>.</nlm:aff></affiliation><affiliation><nlm:aff id="aff03">Global COE Program for Innovation in Human Health Sciences,<addr-line>Shizuoka, Japan</addr-line>.</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22728439</idno><idno type="pmc">3410141</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3410141</idno><idno type="RBID">PMC:3410141</idno><idno type="doi">10.2183/pjab.88.226</idno><date when="2012">2012</date><idno type="wicri:Area/Pmc/Corpus">000E14</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000E14</idno><idno type="wicri:Area/Pmc/Curation">000E14</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000E14</idno><idno type="wicri:Area/Pmc/Checkpoint">000706</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000706</idno><idno type="wicri:Area/Ncbi/Merge">000783</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Molecular basis of the structure and function of H1 hemagglutinin of influenza virus</title><author><name sortKey="Sriwilaijaroen, Nongluk" sort="Sriwilaijaroen, Nongluk" uniqKey="Sriwilaijaroen N" first="Nongluk" last="Sriwilaijaroen">Nongluk Sriwilaijaroen</name><affiliation><nlm:aff id="aff01">Faculty of Medicine, Thammasat University (Rangsit Campus),<addr-line>Pathumthani, Thailand</addr-line>.</nlm:aff></affiliation><affiliation><nlm:aff id="aff02">Health Science Hills, College of Life and Health Sciences, Chubu University,<addr-line>Aichi, Japan</addr-line>.</nlm:aff></affiliation></author><author><name sortKey="Suzuki, Yasuo" sort="Suzuki, Yasuo" uniqKey="Suzuki Y" first="Yasuo" last="Suzuki">Yasuo Suzuki</name><affiliation><nlm:aff id="aff02">Health Science Hills, College of Life and Health Sciences, Chubu University,<addr-line>Aichi, Japan</addr-line>.</nlm:aff></affiliation><affiliation><nlm:aff id="aff03">Global COE Program for Innovation in Human Health Sciences,<addr-line>Shizuoka, Japan</addr-line>.</nlm:aff></affiliation></author></analytic><series><title level="j">Proceedings of the Japan Academy. Series B, Physical and Biological Sciences</title><idno type="ISSN">0386-2208</idno><idno type="eISSN">1349-2896</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Influenza virus hemagglutinin (HA) contains antigenic sites recognized by the host immune system, cleavage sites cleaved by host proteases, receptor binding sites attaching to sialyl receptors on the target cell, and fusion peptides mediating membrane fusion. Change in an amino acid(s) in these sites may affect the potential of virus infection and spread within and between hosts. Influenza viruses with H1 HA infect birds, pigs and humans and have caused two of the four pandemics in the past 100 years: 1918 pandemic that killed 21–50 million people<sup><xref ref-type="bibr" rid="r01">1</xref>)</sup> and 2009 pandemic that caused more than 18,000 deaths.<sup><xref ref-type="bibr" rid="r02">2</xref>)</sup> Understanding the relationship between antigenic structure and immune specificity, the receptor binding specificity in virus transmission, how the cleavage site controls pathogenicity, and how the fusion peptide causes membrane fusion for the entry of influenza virus into the host cell should provide information to find more effective ways to prevent and control influenza.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Johnson, N P" uniqKey="Johnson N">N.P. Johnson</name></author><author><name sortKey="Mueller, J" uniqKey="Mueller J">J. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Jpn Acad Ser B Phys Biol Sci</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci</journal-id><journal-id journal-id-type="publisher-id">PJAB</journal-id><journal-title-group><journal-title>Proceedings of the Japan Academy. Series B, Physical and Biological Sciences</journal-title></journal-title-group><issn pub-type="ppub">0386-2208</issn><issn pub-type="epub">1349-2896</issn><publisher><publisher-name>The Japan Academy</publisher-name><publisher-loc>Tokyo, Japan</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22728439</article-id><article-id pub-id-type="pmc">3410141</article-id><article-id pub-id-type="publisher-id">pjab-88-226</article-id><article-id pub-id-type="doi">10.2183/pjab.88.226</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Molecular basis of the structure and function of H1 hemagglutinin of influenza virus</article-title><alt-title alt-title-type="recto-running-head">Molecular basis of the structure and function of H1 hemagglutinin of influenza virus</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>SRIWILAIJAROEN</surname><given-names>Nongluk</given-names></name><xref ref-type="aff" rid="aff01">*1</xref><xref ref-type="aff" rid="aff02">*2</xref></contrib><contrib contrib-type="author"><name><surname>SUZUKI</surname><given-names>Yasuo</given-names></name><xref ref-type="aff" rid="aff02">*2</xref><xref ref-type="aff" rid="aff03">*3</xref><xref ref-type="corresp" rid="cor01">†</xref></contrib></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>KIDA</surname><given-names>Hiroshi</given-names></name></contrib></contrib-group><aff id="aff01"><label>*1</label>Faculty of Medicine, Thammasat University (Rangsit Campus),<addr-line>Pathumthani, Thailand</addr-line>.</aff><aff id="aff02"><label>*2</label>Health Science Hills, College of Life and Health Sciences, Chubu University,<addr-line>Aichi, Japan</addr-line>.</aff><aff id="aff03"><label>*3</label>Global COE Program for Innovation in Human Health Sciences,<addr-line>Shizuoka, Japan</addr-line>.</aff><author-notes><corresp id="cor01"><label>†</label>Correspondence should be addressed: Y. Suzuki, Health Science Hills, College of Life and Health Sciences, Chubu University, Kasugai, Aichi 487-8501, Japan (e-mail: <email xlink:href="suzukiy@isc.chubu.ac.jp">suzukiy@isc.chubu.ac.jp</email>).</corresp><fn fn-type="com"><p>(Communicated by Hiroshi KIDA, M.J.A.)</p></fn></author-notes><pub-date pub-type="ppub"><day>11</day><month>6</month><year>2012</year></pub-date><volume>88</volume><issue>6</issue><fpage>226</fpage><lpage>249</lpage><history><date date-type="received"><day>3</day><month>8</month><year>2011</year></date><date date-type="accepted"><day>30</day><month>3</month><year>2012</year></date></history><permissions><copyright-statement>© 2012 The Japan Academy</copyright-statement><copyright-year>2012</copyright-year><license license-type="open-access"><license-p>This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><abstract><p>Influenza virus hemagglutinin (HA) contains antigenic sites recognized by the host immune system, cleavage sites cleaved by host proteases, receptor binding sites attaching to sialyl receptors on the target cell, and fusion peptides mediating membrane fusion. Change in an amino acid(s) in these sites may affect the potential of virus infection and spread within and between hosts. Influenza viruses with H1 HA infect birds, pigs and humans and have caused two of the four pandemics in the past 100 years: 1918 pandemic that killed 21–50 million people<sup><xref ref-type="bibr" rid="r01">1</xref>)</sup> and 2009 pandemic that caused more than 18,000 deaths.<sup><xref ref-type="bibr" rid="r02">2</xref>)</sup> Understanding the relationship between antigenic structure and immune specificity, the receptor binding specificity in virus transmission, how the cleavage site controls pathogenicity, and how the fusion peptide causes membrane fusion for the entry of influenza virus into the host cell should provide information to find more effective ways to prevent and control influenza.</p></abstract><kwd-group kwd-group-type="author"><kwd>influenza</kwd><kwd>hemagglutinin</kwd><kwd>antigenic variation</kwd><kwd>glycan binding</kwd><kwd>fusion</kwd><kwd>pandemic</kwd></kwd-group></article-meta></front><floats-group><fig id="fig01" fig-type="figure" orientation="portrait" position="float"><label>Figure 1. </label><caption><p>Influenza virus multiplication life cycle. (i) HA spikes on the viral envelope allow viral entry into the host cell by attaching sialic acid-containing receptors on the host cell membrane. (ii) Following receptor binding and receptor-mediated endocytosis, low pH in the endosome induces a conformational change in HA resulting in fusion of the viral and endosomal membranes. (iii) This fusion allows viral ribonucleoproteins (vRNPs) to be released into the cytoplasm and enter the host nucleus, where viral transcription and replication occur. (iv) Positive sense mRNAs after transcription and processing are exported and translated using the host-cell machinery in the cytoplasm to produce viral protein components. (v) Viral proteins PB1, PB2, PA and NP making up the vRNP, NS2 (NEP) functioning in control of viral transcription and regulation and vRNP export,<sup><xref ref-type="bibr" rid="r132">132</xref>)</sup> and M1 related to nuclear import and export of vRNP<sup><xref ref-type="bibr" rid="r133">133</xref>)</sup> are imported into the nucleus. The NS1 protein is a non-structural protein of a virion that possesses inhibitory activity against host immune responses.<sup><xref ref-type="bibr" rid="r10">10</xref>)</sup> PB1-F2 localizes to mitochondria and enhances apoptosis.<sup><xref ref-type="bibr" rid="r134">134</xref>)</sup> (vi) HA, NA and M2 are synthesized on the rough endoplasmic reticulum and matured in the Golgi complex. (vii and viii) The mature glycosylated HA and NA, non-glycosylated M2, NS2-M1-vRNPs, and other M1 and NS2 forming beneath the virus envelope<sup><xref ref-type="bibr" rid="r135">135</xref>)</sup> are transported to the apical cell membrane, where they are assembled into a progeny virion that finally buds from the host cell surface. Broken boxes represent influenza life cycle steps in which HA spike glycoproteins function and that are explained in detail in this review.</p></caption><graphic xlink:href="pjab-88-226-g001"></graphic></fig><fig id="fig02" fig-type="figure" orientation="portrait" position="float"><label>Figure 2. </label><caption><p>Structural features of the influenza virus hemagglutinin. a) A drawing of an unfolded polypeptide chain of HA0 of H1 virus, which is composed of HA1 and HA2 containing 3 different regions: (i) fusion (comprised of the <italic>N</italic>- and <italic>C</italic>-terminal regions of HA1 (F′ subdomain) and HA2 (F subdomain), which are located in the stem domain (Fig. <xref ref-type="fig" rid="fig02">2</xref>c), a main structure responsible for membrane fusion machinery), (ii) esterase (comprised of two subdomains between F′ and receptor binding regions, which are located in the middle of folded HA (Fig. <xref ref-type="fig" rid="fig02">2</xref>c)) and (iii) receptor binding (almost in the middle of HA1 of unfolded HA and at the top of folded HA (Fig. <xref ref-type="fig" rid="fig02">2</xref>c)) regions as indicated. b) A schematic of the influenza virus particle. Hemagglutinins are found on the viral surface as trimeric forms coded from a gene segment 4. c) A cartoon diagram of α-helices and β-sheets of HA0 folded into a compact monomer of about 135 Å in length, which is shown in side view (PDB: 1rd8); Salmon, HA1; Warmpink, HA2. Receptor binding site (white) is a pocket made up by 130 loop, 190 helix and 220 loop, located on the top of the globular domain. Amino acid at position 77 (dark blue) in the esterase domain below the receptor binding site of about 20 Å is species-specific, D in avain HAs and E in most human HAs (Fig. <xref ref-type="fig" rid="fig03">3</xref>), suggesting that this residue may correlate with the shift in receptor binding specificity.<sup><xref ref-type="bibr" rid="r73">73</xref>)</sup> Antigenic sites surround (green) the receptor binding sites (white and dark blue) on the globular domain. Glycosylation sites (spheres) can be found all over the HA molecule of the seasonal H1 viruses (magenta and red spheres). Both 1918-H1 and 2009-H1 pandemic viruses carry glycosylation sites only below the receptor binding site (red sphere), and the 2009-H1 HA has an extra glycosylation site at position 278 (forest green sphere).</p></caption><graphic xlink:href="pjab-88-226-g002"></graphic></fig><fig id="fig03" fig-type="figure" orientation="portrait" position="float"><label>Figure 3. </label><caption><p>Comparison of amino acid sequences of HAs of influenza A (H1N1) viruses. The glycosylation sites found in almost all H1N1 viruses are shown in red and those found only in the seasonal H1 HAs are shown in magenta; the glycosylation site in forest color is found only in the pandemic 2009 HA. Antigenic sites are indicated by arrows under the sequences. The residues related to receptor binding are shown in white and blue. Vestigial esterase, 130 loop, 190 helix and 220 loop are indicated in the blankets above the sequences. The basic residues are located in boxes. The cleavage site and fusion peptide are shown in cyan and light green, respectively. The <italic>N</italic>- (residues 41–55) and <italic>C</italic>- (residues 77–100) terminal heptad repeats are shown in deepteal; residues that vary between different strains are shown in distinct colors. C in cyan and C in yellow form a disulfide bond that links HA1 and HA2. The residues 185 through 212 (crimson) are the transmembrane region.</p></caption><graphic xlink:href="pjab-88-226-g003"></graphic></fig><fig id="fig05" fig-type="figure" orientation="portrait" position="float"><label>Figure 5. </label><caption><p>Chemical structures of (a) the common molecular species of sialic acids and (b) some terminal sialo-sugar chains bound by some influenza A viruses as mentioned in the text.</p></caption><graphic xlink:href="pjab-88-226-g005"></graphic></fig><fig id="fig06" fig-type="figure" orientation="portrait" position="float"><label>Figure 6. </label><caption><p>Structures of human- and avian-type receptors and their interactions with the H1 receptor binding site (modified from Chandrasekaran <italic>et al.</italic>, 2008).<sup><xref ref-type="bibr" rid="r69">69</xref>)</sup> Left panel: Structures of human α2-6-linked (Neu5Acα2-6Galβ1-4GlcNAcβ1-3Galβ1-4Glc (LSTc), upper pannel) and avian α2-3-linked (Neu5Acα2-3Galβ1-3GlcNAc, which is a sialyl-neo-<italic>N</italic>-acetyllactosamine part of LSTa, lower pannel) sialic acid receptors. Black (pointing up) and green (pointing down) arrows indicate cis- and trans-conformations, respectively, which generate low-energy conformations of α2-6- and α2-3-linkages, respectively, in their specific binding pockets of HAs. Middle panel: Interactions between sialic acid receptor analogs and H1 HAs. a) Superposition of H1 HAs of huBM18 (PDB code 2wrg) in gray and sw30 (PDB code 1rvt) in green complexed with LSTc. b) Superimposition of the receptor binding sites of WDK05 HA (PDB code 3htp) in green and huPR34 HA (PDB code 1rvx) in gray in complex with Neu5Acα2-3Galβ1-3/4GlcNAc. Right panel: Interactions between amino acid residue(s) at position(s) 225 and/or 226 of the HA of influenza A (H1N1) viruses indicated at the top and Gal-2 sugar. PDB codes are in parentheses. Numbers on the dashed lines are the bond distance between two atoms in angstroms.</p></caption><graphic xlink:href="pjab-88-226-g006"></graphic></fig><fig id="fig04" fig-type="figure" orientation="portrait" position="float"><label>Figure 4. </label><caption><p>Schematic surface diagram of antigenic sites, basic patches and glycosylation sites of an H1 HA monomer (PDB code H1N1 1977 from Igarashi <italic>et al.</italic>).<sup><xref ref-type="bibr" rid="r31">31</xref>)</sup> Five antigenic sites, Sa (green), Sb (blue), Ca1 (gray), Ca2 (chocolate) and Cb (slate), are located at the tip (Sa and Sb), halfway down (Ca1 and Ca2) and at the base (Cb) of the HA1 globular head. The first basic patch and the second basic patch are in the solid line ellipse. The first one is situated near the cleavage site, whereas the second is located at the base of the HA1 globular domain. There are three conserved basic residues (HA1: His18 and His38; HA2: His111) in the first patch and 6 possible basic residues (HA1: His47, His275, His/Lys285, His298, Lys46 and Lys50) in the second patch. Residues in cyan indicate nonbasic residue mutations found in most seasonal H1 HAs. Glycosylation sites are distributed over the entire H1 monomer. From 1918, H1 HAs that circulated in humans showed a tendency towards more glycosylation sites. Glycosylation sites (such as N19a, N131, N158, N163, N95 and N290) near or in antigenic regions and/or basic sites could interfere with immunity and infectivity. N278 (green) is an extra glycosylation site found only in the pandemic 2009 H1 HAs. <italic>N</italic>-glycans were added <italic>in silico</italic> into the H1N1 1977 3D protein structure using GlycoProt.</p></caption><graphic xlink:href="pjab-88-226-g004"></graphic></fig><fig id="fig07" fig-type="figure" orientation="portrait" position="float"><label>Figure 7. </label><caption><p>Conformational changes of influenza HA structure at the pH of membrane fusion. a) Primary structure of HA0 protein showing a disulfide bridge (S-S) linked (cyan and yellow line linkage) between HA1 (salmon) and HA2 (magenta), cleavage site (dark blue and red), fusion peptide (green), heptad repeat regions (marine), conformational change regions when HA is in acidic pH (gray) and transmembrane domain (chocolate). b) Tertiary structure of an HA monomer is cleaved between R329 (red) and 1G (green) into a fusion-competent HA1-S-S-HA2 form and unfolds in an acidic environment leading to conformational change. HA2 in the absence of HA1 refolds to the fusion-active form. The fusion peptide (green) pops out and then moves toward and is inserted into the host endosomal membrane, leading to membrane fusion. Colors indicated in a) correspond to those in b).</p></caption><graphic xlink:href="pjab-88-226-g007"></graphic></fig><fig id="fig08" fig-type="figure" orientation="portrait" position="float"><label>Figure 8. </label><caption><p>Consequences of membrane fusion by influenza HA. a) In the pre-fusion state, the fusion peptides (green) at the <italic>N</italic>-terminus of HA2 are sequestered in the interior of the structure (PDB code 1ruz). b) Following proteolytic cleavage at HA2 arginine residue 329, the acidic environment induces conformational changes resulting in removal of the HA1s and exposure of fusion peptides (PDB code 1htm). Since the fusion peptides are hydrophobic, they interact with the bilayer membrane (extended intermediate state) by folding into a boomerang-shaped structure for tight interactions with the membrane. In the inset, the kink of the boomerang structure required for membrane fusion is stabilized by a tryptophan (W) residue at HA2 position 14 (red). c) Further conformation rearrangements in HA2 lead to apposition of the viral envelope and endosomal membrane (collapse of the extended intermediate). When the two bilayers come into contact, they induce hemifusion, d) making bilayers open into a fusion pore (fusion pore formation state). After HA2 rearranges until it is fully symmetric, the pore cannot be resealed (post-fusion state).</p></caption><graphic xlink:href="pjab-88-226-g008"></graphic></fig><table-wrap id="tbl01" orientation="portrait" position="float"><label>Table 1.</label><caption><p>Influenza virus hemagglutinins used for analysis</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="top" rowspan="1" colspan="1">Virus/HA</th><th align="center" valign="top" rowspan="1" colspan="1">Abbreviation</th><th align="center" valign="top" rowspan="1" colspan="1">Protein resource</th><th align="center" valign="top" rowspan="1" colspan="1">PDB* structure</th></tr></thead><tbody><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/mallard/Alberta/35/1976</td><td align="center" valign="middle" rowspan="1" colspan="1">malAlb76</td><td align="center" valign="middle" rowspan="1" colspan="1">BAA01280</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td rowspan="2" align="left" valign="middle" colspan="1">A/WDK/JX/12416/2005</td><td rowspan="2" align="center" valign="middle" colspan="1">WDK05</td><td rowspan="2" align="center" valign="middle" colspan="1">CBA17655</td><td align="center" valign="middle" rowspan="1" colspan="1">3htp<sup><xref ref-type="bibr" rid="r89">89</xref>)</sup></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">3htq<sup><xref ref-type="bibr" rid="r89">89</xref>)</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">1930-swine H1 HA</td><td align="center" valign="middle" rowspan="1" colspan="1">sw30</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td><td align="center" valign="middle" rowspan="1" colspan="1">1rvt<sup><xref ref-type="bibr" rid="r71">71</xref>)</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/swine/Iowa/15/1930</td><td align="center" valign="middle" rowspan="1" colspan="1">swIowa30</td><td align="center" valign="middle" rowspan="1" colspan="1">ABV25634</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td rowspan="2" align="left" valign="middle" colspan="1">A/Puerto Rico/8/1934 (Mount Sinai)</td><td rowspan="2" align="center" valign="middle" colspan="1">huPR34</td><td rowspan="2" align="center" valign="middle" colspan="1">AAM75158</td><td align="center" valign="middle" rowspan="1" colspan="1">1rvz<sup><xref ref-type="bibr" rid="r71">71</xref>)</sup></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">1rvx<sup><xref ref-type="bibr" rid="r71">71</xref>)</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/Bellamy/1942</td><td align="center" valign="middle" rowspan="1" colspan="1">huBel42</td><td align="center" valign="middle" rowspan="1" colspan="1">ABD62843</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/Albany/4836/1950</td><td align="center" valign="middle" rowspan="1" colspan="1">huAlb50</td><td align="center" valign="middle" rowspan="1" colspan="1">ABP49316</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/USSR/90/1977</td><td align="center" valign="middle" rowspan="1" colspan="1">huUSSR77</td><td align="center" valign="middle" rowspan="1" colspan="1">ABF21277</td><td align="center" valign="middle" rowspan="1" colspan="1">H1N1 1977<sup><xref ref-type="bibr" rid="r31">31</xref>)</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/Singapore/6/1986</td><td align="center" valign="middle" rowspan="1" colspan="1">huSing86</td><td align="center" valign="middle" rowspan="1" colspan="1">ABO38395</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/Texas/36/1991</td><td align="center" valign="middle" rowspan="1" colspan="1">huTex91</td><td align="center" valign="middle" rowspan="1" colspan="1">AAP34322</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/Hong Kong/1035/1998</td><td align="center" valign="middle" rowspan="1" colspan="1">huHK98</td><td align="center" valign="middle" rowspan="1" colspan="1">AAK70453</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/Brisbane/59/2007</td><td align="center" valign="middle" rowspan="1" colspan="1">huBB07</td><td align="center" valign="middle" rowspan="1" colspan="1">ACA28844</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">1918-human H1 HA precursor (HA0)</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td><td align="center" valign="middle" rowspan="1" colspan="1">1rd8<sup><xref ref-type="bibr" rid="r118">118</xref>)</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/South Carolina/1/1918</td><td align="center" valign="middle" rowspan="1" colspan="1">huSC18</td><td align="center" valign="middle" rowspan="1" colspan="1">AAD17229</td><td align="center" valign="middle" rowspan="1" colspan="1">1ruz<sup><xref ref-type="bibr" rid="r71">71</xref>)</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/Brevig Mission/1/1918**</td><td align="center" valign="middle" rowspan="1" colspan="1">huBM18</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td><td align="center" valign="middle" rowspan="1" colspan="1">2wrg<sup><xref ref-type="bibr" rid="r130">130</xref>)</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">A/California/04/2009</td><td align="center" valign="middle" rowspan="1" colspan="1">huCA09</td><td align="center" valign="middle" rowspan="1" colspan="1">ACP41105</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">Influenza viral HA at the pH of membrane fusion</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td><td align="center" valign="middle" rowspan="1" colspan="1">—</td><td align="center" valign="middle" rowspan="1" colspan="1">1htm<sup><xref ref-type="bibr" rid="r131">131</xref>)</sup></td></tr></tbody></table><table-wrap-foot><p>*PDB: protein data bank; **A/Brevig Mission/1/1918: huBM18 HA contains one nucleotide different from huSC18 HA, but this different nucleotide provides different codons that code for the same amino acid; —: not used in this review.</p></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list></list><tree><noCountry><name sortKey="Sriwilaijaroen, Nongluk" sort="Sriwilaijaroen, Nongluk" uniqKey="Sriwilaijaroen N" first="Nongluk" last="Sriwilaijaroen">Nongluk Sriwilaijaroen</name><name sortKey="Suzuki, Yasuo" sort="Suzuki, Yasuo" uniqKey="Suzuki Y" first="Yasuo" last="Suzuki">Yasuo Suzuki</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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