Spike protein recognition of mammalian ACE2 predicts the host range and an optimized ACE2 for SARS-CoV-2 infection
Identifieur interne : 000830 ( Pmc/Corpus ); précédent : 000829; suivant : 000831Spike protein recognition of mammalian ACE2 predicts the host range and an optimized ACE2 for SARS-CoV-2 infection
Auteurs : Junwen Luan ; Yue Lu ; Xiaolu Jin ; Leiliang ZhangSource :
- Biochemical and Biophysical Research Communications [ 0006-291X ] ; 2020.
Abstract
SARS-CoV-2 causes the recent global COVID-19 public health emergency. ACE2 is the receptor for both SARS-CoV-2 and SARS-CoV. To predict the potential host range of SARS-CoV-2, we analyzed the key residues of ACE2 for recognizing S protein. We found that most of the selected mammals including pets (dog and cat), pangolin and
Url:
DOI: 10.1016/j.bbrc.2020.03.047
PubMed: 32201080
PubMed Central: 7102515
Links to Exploration step
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Spike protein recognition of mammalian ACE2 predicts the host range and an optimized ACE2 for SARS-CoV-2 infection</title><author><name sortKey="Luan, Junwen" sort="Luan, Junwen" uniqKey="Luan J" first="Junwen" last="Luan">Junwen Luan</name><affiliation><nlm:aff id="aff1">Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</nlm:aff></affiliation></author><author><name sortKey="Lu, Yue" sort="Lu, Yue" uniqKey="Lu Y" first="Yue" last="Lu">Yue Lu</name><affiliation><nlm:aff id="aff1">Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, 250200, Shandong, China</nlm:aff></affiliation></author><author><name sortKey="Jin, Xiaolu" sort="Jin, Xiaolu" uniqKey="Jin X" first="Xiaolu" last="Jin">Xiaolu Jin</name><affiliation><nlm:aff id="aff1">Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, 250200, Shandong, China</nlm:aff></affiliation></author><author><name sortKey="Zhang, Leiliang" sort="Zhang, Leiliang" uniqKey="Zhang L" first="Leiliang" last="Zhang">Leiliang Zhang</name><affiliation><nlm:aff id="aff1">Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32201080</idno><idno type="pmc">7102515</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7102515</idno><idno type="RBID">PMC:7102515</idno><idno type="doi">10.1016/j.bbrc.2020.03.047</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000830</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000830</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Spike protein recognition of mammalian ACE2 predicts the host range and an optimized ACE2 for SARS-CoV-2 infection</title><author><name sortKey="Luan, Junwen" sort="Luan, Junwen" uniqKey="Luan J" first="Junwen" last="Luan">Junwen Luan</name><affiliation><nlm:aff id="aff1">Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</nlm:aff></affiliation></author><author><name sortKey="Lu, Yue" sort="Lu, Yue" uniqKey="Lu Y" first="Yue" last="Lu">Yue Lu</name><affiliation><nlm:aff id="aff1">Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, 250200, Shandong, China</nlm:aff></affiliation></author><author><name sortKey="Jin, Xiaolu" sort="Jin, Xiaolu" uniqKey="Jin X" first="Xiaolu" last="Jin">Xiaolu Jin</name><affiliation><nlm:aff id="aff1">Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, 250200, Shandong, China</nlm:aff></affiliation></author><author><name sortKey="Zhang, Leiliang" sort="Zhang, Leiliang" uniqKey="Zhang L" first="Leiliang" last="Zhang">Leiliang Zhang</name><affiliation><nlm:aff id="aff1">Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</nlm:aff></affiliation></author></analytic><series><title level="j">Biochemical and Biophysical Research Communications</title><idno type="ISSN">0006-291X</idno><idno type="eISSN">1090-2104</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>SARS-CoV-2 causes the recent global COVID-19 public health emergency. ACE2 is the receptor for both SARS-CoV-2 and SARS-CoV. To predict the potential host range of SARS-CoV-2, we analyzed the key residues of ACE2 for recognizing S protein. We found that most of the selected mammals including pets (dog and cat), pangolin and <italic>Circetidae</italic> mammals remained the most of key residues for association with S protein from SARS-CoV and SARS-CoV-2. The interaction interface between cat/dog/pangolin/Chinese hamster ACE2 and SARS-CoV/SARS-CoV-2 S protein was simulated through homology modeling. We identified that N82 in ACE2 showed a closer contact with SARS-CoV-2 S protein than M82 in human ACE2. Our finding will provide important insights into the host range of SARS-CoV-2 and a new strategy to design an optimized ACE2 for SARS-CoV-2 infection.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zhu, N" uniqKey="Zhu N">N. Zhu</name></author><author><name sortKey="Zhang, D" uniqKey="Zhang D">D. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Biochem Biophys Res Commun</journal-id><journal-id journal-id-type="iso-abbrev">Biochem. Biophys. Res. Commun</journal-id><journal-title-group><journal-title>Biochemical and Biophysical Research Communications</journal-title></journal-title-group><issn pub-type="ppub">0006-291X</issn><issn pub-type="epub">1090-2104</issn><publisher><publisher-name>Elsevier Inc.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">32201080</article-id><article-id pub-id-type="pmc">7102515</article-id><article-id pub-id-type="publisher-id">S0006-291X(20)30526-X</article-id><article-id pub-id-type="doi">10.1016/j.bbrc.2020.03.047</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Spike protein recognition of mammalian ACE2 predicts the host range and an optimized ACE2 for SARS-CoV-2 infection</article-title></title-group><contrib-group><contrib contrib-type="author" id="au1"><name><surname>Luan</surname><given-names>Junwen</given-names></name><xref rid="aff1" ref-type="aff">a</xref><xref rid="fn1" ref-type="fn">1</xref></contrib><contrib contrib-type="author" id="au2"><name><surname>Lu</surname><given-names>Yue</given-names></name><xref rid="aff1" ref-type="aff">a</xref><xref rid="aff2" ref-type="aff">b</xref><xref rid="fn1" ref-type="fn">1</xref></contrib><contrib contrib-type="author" id="au3"><name><surname>Jin</surname><given-names>Xiaolu</given-names></name><xref rid="aff1" ref-type="aff">a</xref><xref rid="aff2" ref-type="aff">b</xref><xref rid="fn1" ref-type="fn">1</xref></contrib><contrib contrib-type="author" id="au4"><name><surname>Zhang</surname><given-names>Leiliang</given-names></name><email>armzhang@hotmail.com</email><xref rid="aff1" ref-type="aff">a</xref><xref rid="cor1" ref-type="corresp">∗</xref></contrib></contrib-group><aff id="aff1"><label>a</label>Institute of Basic Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250062, Shandong, China</aff><aff id="aff2"><label>b</label>School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, 250200, Shandong, China</aff><author-notes><corresp id="cor1"><label>∗</label>Corresponding author. <email>armzhang@hotmail.com</email></corresp><fn id="fn1"><label>1</label><p id="ntpara0010">Co-first author.</p></fn></author-notes><pub-date pub-type="pmc-release"><day>19</day><month>3</month><year>2020</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="epub"><day>19</day><month>3</month><year>2020</year></pub-date><elocation-id></elocation-id><history><date date-type="received"><day>27</day><month>2</month><year>2020</year></date><date date-type="accepted"><day>9</day><month>3</month><year>2020</year></date></history><permissions><copyright-statement>© 2020 Elsevier Inc. All rights reserved.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Elsevier Inc.</copyright-holder><license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p></license></permissions><abstract id="abs0010"><p>SARS-CoV-2 causes the recent global COVID-19 public health emergency. ACE2 is the receptor for both SARS-CoV-2 and SARS-CoV. To predict the potential host range of SARS-CoV-2, we analyzed the key residues of ACE2 for recognizing S protein. We found that most of the selected mammals including pets (dog and cat), pangolin and <italic>Circetidae</italic> mammals remained the most of key residues for association with S protein from SARS-CoV and SARS-CoV-2. The interaction interface between cat/dog/pangolin/Chinese hamster ACE2 and SARS-CoV/SARS-CoV-2 S protein was simulated through homology modeling. We identified that N82 in ACE2 showed a closer contact with SARS-CoV-2 S protein than M82 in human ACE2. Our finding will provide important insights into the host range of SARS-CoV-2 and a new strategy to design an optimized ACE2 for SARS-CoV-2 infection.</p></abstract><abstract abstract-type="author-highlights" id="abs0015"><title>Highlights</title><p><list list-type="simple" id="ulist0010"><list-item id="u0010"><label>•</label><p id="p0010">Pets (dog and cat), pangolin and <italic>Circetidae</italic> remained the key residues for association with S from SARS-CoV and SARS-CoV-2.</p></list-item><list-item id="u0015"><label>•</label><p id="p0015">The interface of the interaction between cat/dog/pangolin/Chinese hamster ACE2 and SARS-CoV/SARS-CoV-2 RBD was simulated.</p></list-item><list-item id="u0020"><label>•</label><p id="p0020">N82 of ACE2 showed a closer contact with SARS-CoV-2 S than M82, suggesting an optimized ACE2 for SARS-CoV-2 infection.</p></list-item></list></p></abstract><kwd-group id="kwrds0010"><title>Keywords</title><kwd>SARS-CoV-2</kwd><kwd>Spike protein</kwd><kwd>ACE2</kwd><kwd>Structure</kwd><kwd>Host range</kwd></kwd-group><kwd-group id="kwrds0015"><title>Abbreviations</title><kwd>COVID-19, Corona Virus Disease 2019</kwd><kwd>SARS-CoV-2, Severe Acute Respiratory Syndrome Corona Virus 2</kwd><kwd>SARSr-CoV, SARS-related coronavirus</kwd><kwd>S, spike protein</kwd><kwd>M, membrane protein</kwd><kwd>E, envelope protein</kwd><kwd>N, nucleocapsid protein</kwd><kwd>ACE2, angiotensin-converting enzyme 2</kwd><kwd>RBM, receptor-binding motif</kwd><kwd>RBD, receptor-binding domain</kwd><kwd>JTT, Jones-Taylor-Thornton</kwd></kwd-group></article-meta></front><body><sec id="sec1"><label>1</label><title>Introduction</title><p id="p0025">Corona Virus Disease 2019 (COVID-19), which was reported from Wuhan city, Hubei province of China, has caused over 78,000 human infections and more than 2700 deaths (as of February 25, 2020) [<xref rid="bib1" ref-type="bibr">1</xref>,<xref rid="bib2" ref-type="bibr">2</xref>]. Severe Acute Respiratory Syndrome Corona Virus 2 (SARS-CoV-2) was identified as the pathogen of COVID-19 [<xref rid="bib1" ref-type="bibr">[1]</xref>, <xref rid="bib2" ref-type="bibr">[2]</xref>, <xref rid="bib3" ref-type="bibr">[3]</xref>]. After SARS-CoV and MERS-CoV, SARS-CoV-2 has become the third coronavirus that causes severe respiratory disease and human death [<xref rid="bib4" ref-type="bibr">4</xref>,<xref rid="bib5" ref-type="bibr">5</xref>].</p><p id="p0030">Belonging to the subgenus sarbecvirus of <italic>Coronaviridae</italic>, both SARS-CoV-2 and SARS-CoV are human SARS-related coronavirus (SARSr-CoV). Its genome is a single-stranded RNA composed of about 30 kb nucleotides. SARS-CoV-2 encodes at least four major structural proteins, namely spike protein (S), membrane protein (M), envelope protein (E), and nucleocapsid protein (N) [<xref rid="bib6" ref-type="bibr">6</xref>]. S protein, which is a type I glycoprotein, protrudes from the surface of the virus and can contact the host cell earlier. S protein has attracted great attention because of its function in receptor binding.</p><p id="p0035">Angiotensin-converting enzyme 2 (ACE2) binds to the receptor-binding motif (RBM) in the receptor-binding domain (RBD) of SARS-CoV and functions as a receptor for SARS-CoV [<xref rid="bib7" ref-type="bibr">7</xref>,<xref rid="bib8" ref-type="bibr">8</xref>]. ACE2 is widely distributed in heart, liver, testis, kidney, intestine and other tissues. It has the physiological functions of regulating heart and kidney function and controlling blood pressure [<xref rid="bib9" ref-type="bibr">9</xref>]. Recently, it has been found that human ACE2 promoted the entry of SARS-CoV-2 into the cells [<xref rid="bib3" ref-type="bibr">3</xref>,<xref rid="bib10" ref-type="bibr">10</xref>]. RBD domain of SARS-CoV-2 interacts with human ACE2. Thus, ACE2 is defined as the receptor for SARS-CoV-2.</p><p id="p0040">The specificity of the interaction between virus and receptor determines the host tropism and host range. The origin of SARS-CoV-2 is presumed to be bat [<xref rid="bib3" ref-type="bibr">3</xref>]. However, the intermediate host is not clear, and some studies suggest that pangolin is involved in the evolution of SARS-CoV-2 [<xref rid="bib11" ref-type="bibr">11</xref>,<xref rid="bib12" ref-type="bibr">12</xref>]. It is not clear which mammals are involved in the evolution of SARS-CoV-2 and which animals may be infected by SARS-CoV-2. By sequence alignment of key amino acids binding to RBD in ACE2, the interaction between RBD of SARS-CoV-2/SARS-CoV and mammalian ACE2 was predicted. Based on the potential interaction between S protein and mammalian ACE2, it was speculated that SARS-CoV-2/SARS-CoV preserved the ability to infect many mammals including cat, dog, pangolin and Chinese hamster. From the structure stimulation, we identified N82 in ACE2 show closer contact with F486 of SARS-CoV-2 S protein compared with M82 of ACE2.</p></sec><sec id="sec2"><label>2</label><title>Methods</title><sec id="sec2.1"><label>2.1</label><title>Sequence analysis of RBM of S from SARS-CoV-2 and SARS-CoV</title><p id="p0045">The S protein sequence of SARS-CoV-2 is YP_009724390.1, and the S protein sequence of SARS-CoV is NP_828851.1. RBM of SARS-CoV is from 424 to 494. RBM of SARS-CoV-2 is from 437 to 508.</p></sec><sec id="sec2.2"><label>2.2</label><title>Sequence analysis of mammal ACE2</title><p id="p0050">A total of 42 mammalian ACE2 protein sequences were selected from the wild animal protection lists of Hubei Province and Jiangxi Province, primates, bats, dog, and cat. These sequences are as follows: hACE2: <italic>Homo sapiens</italic> (BAB40370.1), RhiACE2: <italic>Rhinopithecus roxellana</italic> (XP_010364367.2), MacmACE2: <italic>Macaca mulatta</italic> (NP_001129168.1), MuseACE2: <italic>Mustela erminea</italic> (XP_032187679.1), CamdACE2: <italic>Camelus dromedarius</italic> (XP_031301717.1), PlACE2: <italic>Procyon lotor</italic> (XP_031301717.1), PcACE2: <italic>Paguma larvata</italic> (AAX63775.1), RmACE2: <italic>Rhinolophus macrotis</italic> (ADN93471.1), RfACE2: <italic>Rhinolophus ferrumequinum</italic> (BAH02663.1), RsACE2: <italic>Rhinolophus sinicus</italic> (ADN93472.1), RlACE2: <italic>Rousettus leschenaultii</italic> (BAF50705.1), SsACE2: <italic>Sus scrofa</italic> (NP_001116542.1), MpfACE2: <italic>Mustela putorius furo</italic> (BAE53380.1), RatACE2: <italic>Rattus norvegicus</italic> (Q5EGZ1), MmACE2: <italic>Mus musculus</italic> (Q3URC9), ClfACE2: <italic>Canis lupus familiaris</italic> (J9P7Y2), FcACE2: <italic>Felis catus</italic> (A0A384DV19), MjACE2: <italic>Manis javanica</italic> (XP_017505752.1), RpACE2: <italic>Rhinolophus pearsonii</italic> (ABU54053.1), PvACE2: <italic>Pteropus vampyrus</italic> (XP_011361275.1), PoaACE2: <italic>Pongo abelii</italic> (NP_001124604.1), EcACE2: <italic>Equus caballus</italic> (F6V9L3), BtACE2: <italic>Bos taurus</italic> (Q58DD0), PtACE2: <italic>Pan troglodytes</italic> (A0A2J8KU96), OraACE2: <italic>Ornithorhynchus anatinus</italic> (F7FDA2), OvaACE2: <italic>Ovis aries</italic> (W5PSB6), PanACE2: <italic>Papio Anubis</italic> (A0A096N4X9), LaACE2: <italic>Loxodonta africana</italic> (G3T6Q2), SsdACE2: <italic>Sus scrofa domesticus</italic> (A0A220QT48), EeACE2: <italic>Erinaceus europaeus</italic> (A0A1S3APE5), OcACE2: <italic>Oryctolagus cuniculus</italic> (G1TEF4), NpACE2: <italic>Nyctereutes procyonoides</italic> (B4XEP4), VvACE2: <italic>Vulpes vulpes</italic> (A0A3Q7RAT9), PhcACE2: <italic>Phodopus campbelli</italic> (C7ECU7), MaACE2: <italic>Mesocricetus auratus</italic> (C7ECV1), CjACE2: <italic>Callithrix jacchus</italic> (F7CNJ6), SusACE2: <italic>Suricata suricatta</italic> (XP_029786256.1), HgACE2: <italic>Heterocephalus glaber</italic> (A0A0N8EUX7), DoACE2: <italic>Dipodomys ordii</italic> (A0A1S3GHT7), ItACE2: <italic>Ictidomys tridecemlineatus</italic> (XP_005316051.3), CpACE2: <italic>Cavia porcellus</italic> (XP_023417808.1), CgACE2: <italic>Cricetulus griseus</italic> (A0A061HZ66). Based on the known key sites in SARS-CoV S protein interacting with human ACE2, we analyzed whether these sites were conserved on ACE2 from wild mammals and domestic pets. Phylogenetic and molecular evolutionary analyses of ACE2 were conducted using MEGA version X [<xref rid="bib13" ref-type="bibr">13</xref>]. Phylogenetic tree was generated with Jones-Taylor-Thornton (JTT) evolutionary model using Maximum Likelihood method.</p></sec><sec id="sec2.3"><label>2.3</label><title>Structure simulation of ACE2-RBD complex</title><p id="p0055">The interaction interfaces of SARSr-CoV S and ACE2 from cat/dog/pangolin/Chinese hamster were simulated by Chimera software Ver 1.14 [<xref rid="bib14" ref-type="bibr">14</xref>]. The simulation were based on the structures of hACE2 with SARS-CoV S RBD (PDB: <ext-link ext-link-type="uri" xlink:href="pdb:2AJF" id="intref0010">2AJF</ext-link>) [<xref rid="bib7" ref-type="bibr">7</xref>] and hACE2 with SARS-CoV-2 S RBD (PDB: <ext-link ext-link-type="uri" xlink:href="pdb:6LZG" id="intref0015">6LZG</ext-link>).</p></sec></sec><sec id="sec3"><label>3</label><title>Results</title><sec id="sec3.1"><label>3.1</label><title>Sequence alignment of RBM from SARS-CoV-2 and SARS-CoV</title><p id="p0060">Human ACE2 is the receptor for both SARS-CoV and SARS-CoV-2. According to the literature [<xref rid="bib15" ref-type="bibr">15</xref>], the key amino acids (AAs) in the S protein of SARS-CoV interacting with human ACE2 are Y442, L472, N479, D480, T487, Y491 [<xref rid="bib7" ref-type="bibr">7</xref>,<xref rid="bib15" ref-type="bibr">15</xref>]. We compared the RBM in S protein of SARS-CoV-2 with that of SARS-CoV (<xref rid="fig1" ref-type="fig">Fig. 1</xref>A). These amino acids corresponding to SARS-CoV-2 are L455, F486, Q493, S494, N501 and Y505 (<xref rid="fig1" ref-type="fig">Fig. 1</xref>A). Although five of six key AAs in SARS-CoV-2 are changed compared with SARS-CoV, the overall structure of interfaces of ACE2-RBM are similar (<xref rid="fig1" ref-type="fig">Fig. 1</xref>B).<fig id="fig1"><label>Fig. 1</label><caption><p><bold>Alignment of RBM region of S proteins from SARS-CoV-2 and SARS-CoV.</bold> (A) Sequence alignment of RBM region of S protein from SARS-CoV-2 and SARS-CoV. ▲ represents the six key amino acids in the S protein interacting with human ACE2. For SARS-CoV, they are Y442, L472, N479, D480, T487 and Y491. The S protein sequence of SARS-CoV-2 comes from YP_009724390.1, and the S protein sequence of SARS-CoV comes from NP_828851.1. (B) Alignment of the structure of ACE2 recognition of RBD from SARS-CoV-2 and SARS-CoV. Human ACE2 (hACE2), SARS-CoV-2 RBD, and SARS-CoV RBD are in orange red, blue, and green, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</p></caption><alt-text id="alttext0015">Fig. 1</alt-text><graphic xlink:href="gr1_lrg"></graphic></fig></p></sec><sec id="sec3.2"><label>3.2</label><title>Sequence alignment of ACE2</title><p id="p0065">The key AAs in hACE2 for interacting with RBM are K31, E35, D38, M82 and K353 [<xref rid="bib7" ref-type="bibr">7</xref>,<xref rid="bib15" ref-type="bibr">15</xref>]. Among them, K31 and K353 in hACE2 are most critical residues for RBM recognition. Because the overall structure of interfaces of ACE2-RBM in SARS-CoV-2 and SARS-CoV are similar, we analyzed the key RBD recognizing AAs of ACE2 protein from selected mammals, as shown in <xref rid="tbl1" ref-type="table">Table 1</xref>. We predicted that the mammals whose ACE2 could bind to the S protein of SARS-CoV-2 and SARS-CoV were <italic>Homo sapiens, Rhinopithecus roxellana</italic>, <italic>Macaca mulatta</italic>, <italic>Mustela erminea</italic>, <italic>Paguma larvata, Rhinolophus macrotis</italic>, <italic>Rhinolophus sinicus</italic>, <italic>Rousettus leschenaultii</italic>, <italic>Sus scrofa</italic>, <italic>Mustela putorius furo</italic>, <italic>Canis lupus familiaris</italic>, <italic>Felis catus</italic>, <italic>Manis javanica</italic> (pangolin), <italic>Rhinolophus pearsonii</italic>, <italic>Pteropus vampyrus</italic>, <italic>Pongo abelii</italic>, <italic>Equus caballus</italic>, <italic>Bos taurus</italic>, <italic>Pan troglodytes</italic>, <italic>Ovis aries</italic>, <italic>Papio Anubis</italic>, <italic>Sus scrofa domesticus</italic>, <italic>Oryctolagus cuniculus</italic>, <italic>Vulpes vulpes</italic>, <italic>Phodopus campbelli</italic>, <italic>Mesocricetus auratus</italic>, <italic>Callithrix jacchus, Heterocephalus glaber</italic>, <italic>Ictidomys tridecemlineatus</italic>, and <italic>Cricetulus griseus</italic> (Chinese hamster). The mammals whose ACE2 could not bind to S protein of SARS-CoV-2 and SARS-CoV included <italic>Camelus dromedarius</italic>, <italic>Procyon lotor</italic>, <italic>Rhinolophus ferrumequinum</italic>, <italic>Rattus norvegicus</italic>, <italic>Mus musculus</italic>, <italic>Ornithorhynchus anatinus</italic>, <italic>Loxodonta africana</italic>, <italic>Erinaceus europaeus</italic>, <italic>Nyctereutes procyonoides, Suricata suricatta</italic>, <italic>Dipodomys ordii</italic>, and <italic>Cavia porcellus</italic>.<table-wrap position="float" id="tbl1"><label>Table 1</label><caption><p>Prediction of the RBD binding capacity of mammalian ACE2.</p></caption><alt-text id="alttext0030">Table 1</alt-text><table frame="hsides" rules="groups"><thead><tr><th rowspan="2">ACE2</th><th colspan="5">AA position<hr></hr></th><th rowspan="2">matched AA</th><th rowspan="2">binding capacity</th></tr><tr><th>31</th><th>35</th><th>38</th><th>82</th><th>353</th></tr></thead><tbody><tr><td align="left">hACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">M</td><td align="left">K</td><td align="left">5/5</td><td align="left">+</td></tr><tr><td align="left">RhiACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">M</td><td align="left">K</td><td align="left">5/5</td><td align="left">+</td></tr><tr><td align="left">MacmACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">M</td><td align="left">K</td><td align="left">5/5</td><td align="left">+</td></tr><tr><td align="left">MuseACE2</td><td align="left">K</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">CamdACE2</td><td align="left">E</td><td align="left">E</td><td align="left">D</td><td align="left">T</td><td align="left">K</td><td align="left">3/5</td><td align="left">–</td></tr><tr><td align="left">PlACE2</td><td align="left">N</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">K</td><td align="left">2/5</td><td align="left">–</td></tr><tr><td align="left">PcACE2</td><td align="left">T</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">K</td><td align="left">2/5</td><td align="left">+</td></tr><tr><td align="left">RmACE2</td><td align="left">K</td><td align="left">K</td><td align="left">D</td><td align="left">N</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">RfACE2</td><td align="left">D</td><td align="left">E</td><td align="left">N</td><td align="left">N</td><td align="left">K</td><td align="left">2/5</td><td align="left">–</td></tr><tr><td align="left">RsACE2</td><td align="left">K</td><td align="left">K</td><td align="left">D</td><td align="left">N</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">RlACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">T</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">SsACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">T</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">MpfACE2</td><td align="left">K</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">RatACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">N</td><td align="left">H</td><td align="left">3/5</td><td align="left">–</td></tr><tr><td align="left">MmACE2</td><td align="left">N</td><td align="left">E</td><td align="left">D</td><td align="left">S</td><td align="left">H</td><td align="left">2/5</td><td align="left">–</td></tr><tr><td align="left">ClfACE2</td><td align="left">K</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">FcACE2</td><td align="left">K</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">MjACE2</td><td align="left">K</td><td align="left">E</td><td align="left">E</td><td align="left">N</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">RpACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">D</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">PvACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">A</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">PoaACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">M</td><td align="left">K</td><td align="left">5/5</td><td align="left">+</td></tr><tr><td align="left">EcACE2</td><td align="left">K</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">BtACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">T</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">PtACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">M</td><td align="left">K</td><td align="left">5/5</td><td align="left">+</td></tr><tr><td align="left">OraACE2</td><td align="left">Q</td><td align="left">Q</td><td align="left">D</td><td align="left">K</td><td align="left">K</td><td align="left">2/5</td><td align="left">–</td></tr><tr><td align="left">OvaACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">T</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">PanACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">M</td><td align="left">K</td><td align="left">5/5</td><td align="left">+</td></tr><tr><td align="left">LaACE2</td><td align="left">T</td><td align="left">E</td><td align="left">D</td><td align="left">D</td><td align="left">K</td><td align="left">3/5</td><td align="left">–</td></tr><tr><td align="left">SsdACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">T</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">EeACE2</td><td align="left">D</td><td align="left">Q</td><td align="left">N</td><td align="left">N</td><td align="left">N</td><td align="left">0/5</td><td align="left">–</td></tr><tr><td align="left">OcACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">T</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">NpACE2</td><td align="left">K</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">R</td><td align="left">2/5</td><td align="left">–</td></tr><tr><td align="left">VvACE2</td><td align="left">K</td><td align="left">E</td><td align="left">E</td><td align="left">T</td><td align="left">K</td><td align="left">3/5</td><td align="left">+</td></tr><tr><td align="left">PhcACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">N</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">MaACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">N</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">CjACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">T</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">SusACE2</td><td align="left">Q</td><td align="left">E</td><td align="left">E</td><td align="left">A</td><td align="left">K</td><td align="left">2/5</td><td align="left">–</td></tr><tr><td align="left">HgACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">A</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">DoACE2</td><td align="left">N</td><td align="left">E</td><td align="left">D</td><td align="left">I</td><td align="left">K</td><td align="left">3/5</td><td align="left">–</td></tr><tr><td align="left">ItACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">A</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr><tr><td align="left">CpACE2</td><td align="left">E</td><td align="left">K</td><td align="left">D</td><td align="left">A</td><td align="left">K</td><td align="left">2/5</td><td align="left">–</td></tr><tr><td align="left">CgACE2</td><td align="left">K</td><td align="left">E</td><td align="left">D</td><td align="left">N</td><td align="left">K</td><td align="left">4/5</td><td align="left">+</td></tr></tbody></table></table-wrap></p><p id="p0070">Next, we constructed a phylogenetic tree for mammalian ACE2 proteins. The ACE2 protein sequences of 42 mammalian animals were compared by ClustalW method of MEGA-X software. Then the JTT model of maximum likelihood method was used to construct ACE2 phylogenetic tree. As shown in <xref rid="fig2" ref-type="fig">Fig. 2</xref>, species that cannot bind to S protein are marked in red, and species that can bind to S protein are marked in green. No correlation between genetic distance and the interaction of ACE2/S was found. Some Pets including dog (<italic>Canis lupus familiaris</italic>) and cat (<italic>Felis catus</italic>) potentially recognize S protein, indicating the importance to monitor the pets for SARS-CoV-2 infection. We found that four members of <italic>Circetidae</italic> including <italic>Mesocricetus auratus, Phodopus campbelli</italic>, <italic>Ictidomys tridecemlineatus</italic>, and <italic>Cricetulus griseus</italic> remained the key residues for association with S protein from SARS-CoV and SARS-CoV-2, though two members of <italic>Muridae</italic> (<italic>Rattus norvegicus</italic>, <italic>Mus musculus</italic>) could not bind to S protein. This founding suggested that <italic>Circetidae</italic> mammals could be developed as SARSr-CoV small animal models.<fig id="fig2"><label>Fig. 2</label><caption><p><bold>Phylogenetic tree of mammalian ACE2 proteins.</bold> ACE2 sequences from a total of 42 mammals were analyzed by MEGA-X and the phylogenetic tree was constructed with JTT evolutionary model using Maximum Likelihood method. The red represents the species whose ACE2 cannot bind to S protein, and the green is the species whose ACE2 associate with S protein. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</p></caption><alt-text id="alttext0020">Fig. 2</alt-text><graphic xlink:href="gr2_lrg"></graphic></fig></p></sec><sec id="sec3.3"><label>3.3</label><title>Structure simulation of the protein complex of SARSr-CoV RBD and cat/dog/pangolin/Chinese hamster ACE2</title><p id="p0075">We noticed that ACE2 from dog, cat, pangolin and Chinese hamster potentially associated with S protein (<xref rid="tbl1" ref-type="table">Table 1</xref>). Next, we predicted the structure of cat/dog/pangolin/Chinese hamster ACE2 with SARSr-CoV RBD. The structure of protein complex between RBD region of S protein of SARS-CoV and human ACE2 has been resolved (PDB: <ext-link ext-link-type="uri" xlink:href="pdb:2AJF" id="intref0020">2AJF</ext-link>) [<xref rid="bib7" ref-type="bibr">7</xref>]. Recently, the structure of SARS-CoV-2 RBD with human ACE2 was also determined [<xref rid="bib16" ref-type="bibr">16</xref>,<xref rid="bib17" ref-type="bibr">17</xref>]. We used Chimera software to display homologous model, and obtained the interaction complex structure of RBD region of SARSr-CoV (SARS-CoV-2 and SARS-CoV) and cat/dog/pangolin/Chinese hamster ACE2. Overall, the RBM structures of S protein of SARS-CoV-2 and SARS-CoV are similar (<xref rid="fig3" ref-type="fig">Fig. 3</xref>). Interaction interface of SARSr-CoV RBD and cat/dog/pangolin/Chinese hamster ACE2 confirmed the potential interaction between SARS-CoV-2 and cat/dog/pangolin/Chinese hamster ACE2, indicating that these ACE2 could support SARS-CoV-2 entry. The AA in 82 position of human ACE2 is M82, while the corresponding AA in cat, dog, pangolin and Chinese hamster ACE2 is T82, T81, N82 and N82, respectively. The distance between F486 of SARS-CoV-2 S protein and the corresponding AA in ACE2 is 3.753Å for human (<xref rid="fig1" ref-type="fig">Fig. 1</xref>A), 2.695Å for dog (<xref rid="fig3" ref-type="fig">Fig. 3</xref>A), 3.753Å for cat (<xref rid="fig3" ref-type="fig">Fig. 3</xref>B), 1.621Å for pangolin (<xref rid="fig3" ref-type="fig">Fig. 3</xref>C), and 2.024Å for Chinese hamster (<xref rid="fig3" ref-type="fig">Fig. 3</xref>D), respectively. We concluded that N82 in ACE2 showed closer contact with F486 of SARS-CoV-2 S protein than M82 of ACE2.<fig id="fig3"><label>Fig. 3</label><caption><p><bold>Structure simulation of SARSr-CoV RBD with ACE2 from dog, cat, pangolin and Chinese hamster.</bold> (A) Structural simulation of the protein complex of dog ACE2 and SARSr-CoV RBD. Dog ACE2, SARS-CoV-2 RBD, SARS-CoV RBD are in gold, blue, and green, respectively. (B) Structural simulation of the protein complex of cat ACE2 and SARSr-CoV RBD. Cat ACE2, SARS-CoV-2 RBD, and SARS-CoV RBD are in pulm, blue and green, respectively. (C) Structural simulation of the protein complex of pangolin ACE2 and SARSr-CoV RBD. Pangolin ACE2, SARS-CoV-2 RBD, and SARS-CoV RBD are in sandy brown, blue and green, respectively. (D) Structural simulation of the protein complex of Chinese hamster ACE2 and SARSr-CoV RBD. Chinese hamster ACE2, SARS-CoV-2 RBD, and SARS-CoV RBD are in dim gray, blue and green, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</p></caption><alt-text id="alttext0025">Fig. 3</alt-text><graphic xlink:href="gr3_lrg"></graphic></fig></p></sec></sec><sec id="sec4"><label>4</label><title>Discussion</title><p id="p0080">The host tropism of zoonotic coronavirus is hybrid, and it is important to determine the natural host and host range of coronavirus. In the past two decades, SARS-CoV, MERS-CoV and SARS-CoV-2 have caused serious outbreaks of human infectious diseases. All the three human coronaviruses originated from bats, but the intermediate hosts were different. SARS-CoV is believed to come from the <italic>Paguma larvata</italic> [<xref rid="bib18" ref-type="bibr">18</xref>], and the intermediate host of MERS-CoV is <italic>Camelus dromedaries</italic> [<xref rid="bib19" ref-type="bibr">19</xref>]. The new coronavirus SARS-CoV-2 has recently caused a serious epidemic in China, but its intermediate hosts are not clear.</p><p id="p0085">S protein of SARS-CoV-2 interacts with human ACE2, which promotes the entry of SARS-CoV-2, indicating that human ACE2 is the receptor of SARS-CoV-2 [<xref rid="bib3" ref-type="bibr">3</xref>]. ACE2 contains at least five key amino acids critical for binding S protein of SARSr-CoV [<xref rid="bib15" ref-type="bibr">15</xref>]. Based on these five amino acids, we analyzed the corresponding amino acids of different mammals to determine which mammalian ACE2 could interact with S protein of human SARSr-CoV. By analyzing the protein sequence of mammalian ACE2, we found that the ACE2 of <italic>Camelus dromedarius</italic>, <italic>Procyon lotor</italic>, <italic>Rhinolophus ferrumequinum</italic>, <italic>Rattus norvegicus</italic>, <italic>Mus musculus</italic>, <italic>Ornithorhynchus anatinus</italic>, <italic>Loxodonta africana</italic>, <italic>Erinaceus europaeus</italic>, <italic>Nyctereutes procyonoides</italic>, <italic>Suricata suricatta, Dipodomys ordii</italic>, and <italic>Cavia porcellus</italic> lose the capability to associate with S protein (<xref rid="tbl1" ref-type="table">Table 1</xref>). These mammals could be ruled out from the potential host list for SARS-CoV-2. We found that S protein may bind to ACE2 from some wild mammals, which suggests that we should investigate whether these animals may be intermediate hosts for SARS-CoV-2. It has been reported that the RBM region in S protein of pangolin coronavirus is similar to that of S protein of SARS-CoV-2 [<xref rid="bib11" ref-type="bibr">11</xref>,<xref rid="bib12" ref-type="bibr">12</xref>], which may be involved in the recombination of SARS-CoV-2. We identified that N82 of pangolin ACE2 showed closer contact with RBD than human ACE2 (<xref rid="fig3" ref-type="fig">Fig. 3</xref>C), indicating that pangolin ACE2 might show better affinity to SARS-CoV-2. This finding further supports the hypothesis that pangolin is involved in SARS-CoV-2 evolution. In current study, only a limited list of wild mammals is covered. In the future, we should select more mammals for study. Although no SARS-CoV-2 has been found in domestic cats and dogs, cat/dog ACE2 may bind to S protein of SARS-CoV-2. In the future, we should pay attention to monitoring whether domestic cats and dogs could be infected by SARS-CoV-2.</p><p id="p0090">Animal model is an important tool in the study of infectious diseases. ACE2 of mice cannot interact with SARS-CoV-2, so it cannot be used as animal model of SARS-CoV-2 directly. Some studies have generated mice transfected with human ACE2 as the models to study SARS-CoV [<xref rid="bib20" ref-type="bibr">20</xref>], and these mice can also be used as animal models for SARS-CoV-2 infection. Interestingly, we identified that N82 in ACE2 is closer to RBD than M82 (<xref rid="fig3" ref-type="fig">Fig. 3</xref>C and D), indicating a novel strategy to design an optimized ACE2 for SARS-CoV-2 infection. We speculated that small peptide based on N82 of ACE2 might show higher affinity to SARS-CoV-2 RBD. We proposed that if M82 in human ACE2 was mutated to N82, the modified human ACE2 will enhance SARS-CoV-2 infection. In the future, those ideas will be tested in cell culture and animal model. We noticed that the ACE2 proteins from <italic>Circetidae</italic> (<italic>Mesocricetus auratus, Phodopus campbelli</italic>, <italic>Ictidomys tridecemlineatus</italic>, and <italic>Cricetulus griseus</italic>) are capable to recognize RBD. <italic>Mesocricetus auratus</italic> (golden hamster) and <italic>Cricetulus griseus</italic> (Chinese hamster) are experimental animals and our finding indicates the possibility to develop small animal models for SARS-CoV-2 infection using Chinese hamster and golden hamster.</p></sec><sec sec-type="COI-statement"><title>Declaration of competing interest</title><p id="p0095">The authors declare that there are no conflicts of interest.</p></sec></body><back><ref-list id="cebib0010"><title>References</title><ref id="bib1"><label>1</label><element-citation publication-type="journal" id="sref1"><person-group person-group-type="author"><name><surname>Zhu</surname><given-names>N.</given-names></name><name><surname>Zhang</surname><given-names>D.</given-names></name><name><surname>Wang</surname><given-names>W.</given-names></name><name><surname>Li</surname><given-names>X.</given-names></name><name><surname>Yang</surname><given-names>B.</given-names></name><name><surname>Song</surname><given-names>J.</given-names></name><name><surname>Zhao</surname><given-names>X.</given-names></name><name><surname>Huang</surname><given-names>B.</given-names></name><name><surname>Shi</surname><given-names>W.</given-names></name><name><surname>Lu</surname><given-names>R.</given-names></name><name><surname>Niu</surname><given-names>P.</given-names></name><name><surname>Zhan</surname><given-names>F.</given-names></name><name><surname>Ma</surname><given-names>X.</given-names></name><name><surname>Wang</surname><given-names>D.</given-names></name><name><surname>Xu</surname><given-names>W.</given-names></name><name><surname>Wu</surname><given-names>G.</given-names></name><name><surname>Gao</surname><given-names>G.F.</given-names></name><name><surname>Tan</surname><given-names>W.</given-names></name></person-group><article-title>A novel coronavirus from patients with pneumonia in China, 2019</article-title><source>N. 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Med.</source><volume>57</volume><year>2007</year><fpage>450</fpage><lpage>459</lpage><pub-id pub-id-type="pmid">17974127</pub-id></element-citation></ref></ref-list><sec id="appsec1" sec-type="supplementary-material"><title>Transparency document</title><p id="p0105"><supplementary-material content-type="local-data" id="mmc1"><caption><title>coi</title></caption><media xlink:href="mmc1.zip"><alt-text>coi</alt-text></media></supplementary-material></p></sec><ack id="ack0010"><title>Acknowledgements</title><p>This work was supported by grants from <funding-source id="gs1">National Key Plan for Research and Development of China</funding-source> [2016YFD0500300], <funding-source id="gs2">National Natural Science Foundation of China</funding-source> [81871663 and 81672035], <funding-source id="gs3">Shandong Academy of Medical Sciences</funding-source> Grant [2017-52] and Academic promotion programme of Shandong First Medical University. Molecular graphics and analyses performed with UCSF Chimera, developed by the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco, with support from <funding-source id="gs4">NIH</funding-source>P41-GM103311. We thank Dr. Jianxun Qi for sharing the structure of 6LZG.</p></ack><fn-group><fn id="appsec2" fn-type="supplementary-material"><p id="p0110">Transparency document related to this article can be found online at <ext-link ext-link-type="doi" xlink:href="10.1016/j.bbrc.2020.03.047" id="intref0025">https://doi.org/10.1016/j.bbrc.2020.03.047</ext-link>.</p></fn></fn-group></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Corpus/RBID.i -Sk "pubmed:32201080" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Corpus/biblio.hfd \
| NlmPubMed2Wicri -a SrasV1
| This area was generated with Dilib version V0.6.33. |  |