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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">MERS Coronavirus: An Emerging Zoonotic Virus</title><author><name sortKey="Li, Fang" sort="Li, Fang" uniqKey="Li F" first="Fang" last="Li">Fang Li</name><affiliation><nlm:aff id="af1-viruses-11-00663">Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN 55108, USA</nlm:aff></affiliation></author><author><name sortKey="Du, Lanying" sort="Du, Lanying" uniqKey="Du L" first="Lanying" last="Du">Lanying Du</name><affiliation><nlm:aff id="af2-viruses-11-00663">Lindsley F. Kimball Research Institute, New York Blood Center, New York, NY 10065, USA</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31331035</idno><idno type="pmc">6669680</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6669680</idno><idno type="RBID">PMC:6669680</idno><idno type="doi">10.3390/v11070663</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000857</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000857</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">MERS Coronavirus: An Emerging Zoonotic Virus</title><author><name sortKey="Li, Fang" sort="Li, Fang" uniqKey="Li F" first="Fang" last="Li">Fang Li</name><affiliation><nlm:aff id="af1-viruses-11-00663">Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN 55108, USA</nlm:aff></affiliation></author><author><name sortKey="Du, Lanying" sort="Du, Lanying" uniqKey="Du L" first="Lanying" last="Du">Lanying Du</name><affiliation><nlm:aff id="af2-viruses-11-00663">Lindsley F. Kimball Research Institute, New York Blood Center, New York, NY 10065, USA</nlm:aff></affiliation></author></analytic><series><title level="j">Viruses</title><idno type="eISSN">1999-4915</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zaki, A M" uniqKey="Zaki A">A.M. Zaki</name></author><author><name sortKey="Van Boheemen, S" uniqKey="Van Boheemen S">S. van Boheemen</name></author><author><name sortKey="Bestebroer, T M" uniqKey="Bestebroer T">T.M. Bestebroer</name></author><author><name sortKey="Osterhaus, A D" uniqKey="Osterhaus A">A.D. Osterhaus</name></author><author><name sortKey="Fouchier, R A" uniqKey="Fouchier R">R.A. Fouchier</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yang, Y" uniqKey="Yang Y">Y. 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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">31331035</article-id><article-id pub-id-type="pmc">6669680</article-id><article-id pub-id-type="doi">10.3390/v11070663</article-id><article-id pub-id-type="publisher-id">viruses-11-00663</article-id><article-categories><subj-group subj-group-type="heading"><subject>Editorial</subject></subj-group></article-categories><title-group><article-title>MERS Coronavirus: An Emerging Zoonotic Virus</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Li</surname><given-names>Fang</given-names></name><xref ref-type="aff" rid="af1-viruses-11-00663">1</xref><xref rid="c1-viruses-11-00663" ref-type="corresp">*</xref></contrib><contrib contrib-type="author"><name><surname>Du</surname><given-names>Lanying</given-names></name><xref ref-type="aff" rid="af2-viruses-11-00663">2</xref><xref rid="c1-viruses-11-00663" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-viruses-11-00663"><label>1</label>Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN 55108, USA</aff><aff id="af2-viruses-11-00663"><label>2</label>Lindsley F. Kimball Research Institute, New York Blood Center, New York, NY 10065, USA</aff><author-notes><corresp id="c1-viruses-11-00663"><label>*</label>Correspondence: <email>lifang@umn.edu</email> (F.L.); <email>ldu@nybc.org</email> (L.D.); Tel.: +1-612-625-6149 (F.L.); +1-212-570-3459 (L.D.)</corresp></author-notes><pub-date pub-type="epub"><day>19</day><month>7</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>7</month><year>2019</year></pub-date><volume>11</volume><issue>7</issue><elocation-id>663</elocation-id><history><date date-type="received"><day>16</day><month>7</month><year>2019</year></date><date date-type="accepted"><day>17</day><month>7</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 by the authors.</copyright-statement><copyright-year>2019</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. 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></article-meta></front><body><p>Middle East respiratory syndrome coronavirus (MERS-CoV) is an emerging virus that was first reported in humans in June 2012 [<xref rid="B1-viruses-11-00663" ref-type="bibr">1</xref>]. To date, MERS-CoV continues to infect humans with a fatality rate of ~35%. At least 27 countries have reported human infections with MERS-CoV (<uri xlink:href="https://www.who.int/emergencies/mers-cov/en/">https://www.who.int/emergencies/mers-cov/en/</uri>). MERS-CoV is a zoonotic virus. Like severe acute respiratory syndrome coronavirus (SARS-CoV), MERS-CoV is believed to have originated from bats [<xref rid="B2-viruses-11-00663" ref-type="bibr">2</xref>,<xref rid="B3-viruses-11-00663" ref-type="bibr">3</xref>]. However, whereas the bat-to-human transmission of SARS-CoV was likely mediated by palm civets as intermediate hosts, humans likely acquired MERS-CoV from dromedary camels [<xref rid="B4-viruses-11-00663" ref-type="bibr">4</xref>,<xref rid="B5-viruses-11-00663" ref-type="bibr">5</xref>,<xref rid="B6-viruses-11-00663" ref-type="bibr">6</xref>]. Human-to-human transmission of MERS-CoV does occur, but it is limited mostly to health care environments [<xref rid="B7-viruses-11-00663" ref-type="bibr">7</xref>,<xref rid="B8-viruses-11-00663" ref-type="bibr">8</xref>]. Moreover, whereas SARS-CoV recognizes angiotensin-converting enzyme 2 (ACE2) as a cellular receptor [<xref rid="B9-viruses-11-00663" ref-type="bibr">9</xref>,<xref rid="B10-viruses-11-00663" ref-type="bibr">10</xref>], MERS-CoV uses dipeptidyl peptidase 4 (DPP4) to enter target cells [<xref rid="B11-viruses-11-00663" ref-type="bibr">11</xref>,<xref rid="B12-viruses-11-00663" ref-type="bibr">12</xref>]. Currently, no vaccines or antiviral therapeutics have been approved for the prevention or treatment of MERS-CoV infection, although a number of them have been developed preclinically and/or tested clinically [<xref rid="B13-viruses-11-00663" ref-type="bibr">13</xref>,<xref rid="B14-viruses-11-00663" ref-type="bibr">14</xref>,<xref rid="B15-viruses-11-00663" ref-type="bibr">15</xref>,<xref rid="B16-viruses-11-00663" ref-type="bibr">16</xref>].</p><p>The articles in this special issue of <italic>Viruses</italic> were written by researchers working in the MERS-CoV field. The main aims of this issue are to (i) better understand MERS-CoV transmission, epidemiology, and pathogenesis; (ii) summarize current progress on MERS-CoV animal models, vaccines, and therapeutics; and (iii) discuss future prospects for MERS-CoV research. This issue includes seven review articles and nine original research papers, each providing detailed updates on current MERS-CoV studies.</p><p>Studies on the transmission, epidemiology, and pathogenesis of MERS-CoV form one of the foundations of MERS-CoV research. In this issue, Farag and colleagues summarize the possible drivers of the emergence of MERS-CoV and its spillover to humans in Qatar, explaining the potential reasons for the camel-to-human transmission of MERS-CoV [<xref rid="B17-viruses-11-00663" ref-type="bibr">17</xref>]. The review article by Song and colleagues provides an overall description of the epidemiology, pathogenesis, and other important aspects of MERS-CoV [<xref rid="B18-viruses-11-00663" ref-type="bibr">18</xref>]. Widagdo and colleagues review the host determinants of the transmission and pathogenesis of MERS-CoV, indicating that receptor DPP4 plays an important role in these processes [<xref rid="B19-viruses-11-00663" ref-type="bibr">19</xref>]. A research article by Yan and colleagues characterizes the role of lipid profiles in the pathogenesis and infectivity of human coronaviruses, including MERS-CoV, suggesting that lipid metabolism may be involved in the propagations of these coronaviruses [<xref rid="B20-viruses-11-00663" ref-type="bibr">20</xref>]. These reports provide insights into how MERS-CoV infects cells and spreads within and across host species. They have also laid the foundations for developing animal models.</p><p>Animal models are essential tools for the preclinical evaluation of anti-MERS-CoV countermeasures. Dromedary camels, alpacas, and non-human primates are susceptible to MERS-CoV infection [<xref rid="B21-viruses-11-00663" ref-type="bibr">21</xref>,<xref rid="B22-viruses-11-00663" ref-type="bibr">22</xref>,<xref rid="B23-viruses-11-00663" ref-type="bibr">23</xref>]; however, the virus does not infect small animals such as mice, hamsters, and ferrets [<xref rid="B24-viruses-11-00663" ref-type="bibr">24</xref>,<xref rid="B25-viruses-11-00663" ref-type="bibr">25</xref>,<xref rid="B26-viruses-11-00663" ref-type="bibr">26</xref>]. Several mouse models that express human DPP4 (hDPP4) have been established for MERS-CoV infection [<xref rid="B27-viruses-11-00663" ref-type="bibr">27</xref>,<xref rid="B28-viruses-11-00663" ref-type="bibr">28</xref>,<xref rid="B29-viruses-11-00663" ref-type="bibr">29</xref>]. In this issue, Widagdo and colleagues examine rabbits as potential hosts for MERS-CoV, showing that MERS-CoV infects rabbits without causing symptoms; they also analyze the route of MERS-CoV transmission in rabbits [<xref rid="B30-viruses-11-00663" ref-type="bibr">30</xref>]. Fan and colleagues report the development of an hDPP4-expressing mouse model through inserting hDPP4 gene into a constitutive and ubiquitous gene expression locus using CRISPR/Cas9 technology. This mouse model is susceptible to MERS-CoV infection [<xref rid="B31-viruses-11-00663" ref-type="bibr">31</xref>]. These articles have established platforms for testing vaccines and therapeutic agents targeting MERS-CoV.</p><p>Effective vaccines are essential for preventing MERS-CoV infection. The MERS-CoV surface spike (S) protein is a key target for vaccine design [<xref rid="B14-viruses-11-00663" ref-type="bibr">14</xref>]. The S protein comprises two subunits: the S1 subunit is responsible for binding to the DPP4 receptor via a receptor-binding domain (RBD), and the S2 subunit mediates virus–host membrane fusion [<xref rid="B32-viruses-11-00663" ref-type="bibr">32</xref>,<xref rid="B33-viruses-11-00663" ref-type="bibr">33</xref>,<xref rid="B34-viruses-11-00663" ref-type="bibr">34</xref>,<xref rid="B35-viruses-11-00663" ref-type="bibr">35</xref>]. Several MERS-CoV S protein-based vaccines have been developed; when tested in animal models, they showed protective efficacy against MERS-CoV [<xref rid="B14-viruses-11-00663" ref-type="bibr">14</xref>]. In this issue, Schindewolf and Menachery summarize the progress of MERS-CoV S-protein-based vaccine development and also describe potential challenges [<xref rid="B36-viruses-11-00663" ref-type="bibr">36</xref>]. Zhou and colleagues review current advances in RBD-based MERS-CoV vaccines [<xref rid="B37-viruses-11-00663" ref-type="bibr">37</xref>]. A research paper by Adney and colleagues evaluates the efficacy of a MERS-CoV S1 subunit vaccine aided by adjuvants; the authors report reduced and delayed viral shedding in dromedary camels as well as the complete protection of alpacas from MERS-CoV infection [<xref rid="B38-viruses-11-00663" ref-type="bibr">38</xref>]. This and other studies demonstrate that the protective efficacy of MERS vaccines positively correlates with neutralizing antibody titers in serum [<xref rid="B38-viruses-11-00663" ref-type="bibr">38</xref>,<xref rid="B39-viruses-11-00663" ref-type="bibr">39</xref>]. In addition to inducing neutralizing antibodies, some types of vaccines can induce cellular immune responses against MERS-CoV. Other than the S protein, structural proteins such as the nucleocapsid (N) protein may also serve as vaccine targets. Here, Veit and colleagues report that a MERS-CoV N protein-based vaccine, which is delivered through a modified Vaccinia virus, induces CD8<sup>+</sup> T cell responses in a mouse model; they further identify a MERS-CoV N protein-specific CD8<sup>+</sup> T cell epitope on the vaccine [<xref rid="B40-viruses-11-00663" ref-type="bibr">40</xref>]. Overall, these reports demonstrate that a variety of promising vaccine tools are available to prevent MERS-CoV infection in humans and other animals.</p><p>Therapeutics are critical tools for treating MERS-CoV infection. Again, the MERS-CoV S protein is an important target for therapeutic development [<xref rid="B16-viruses-11-00663" ref-type="bibr">16</xref>]. MERS-CoV S2 contains two heptad repeat regions, HR1 and HR2, that are critical for S protein-mediated membrane fusion [<xref rid="B34-viruses-11-00663" ref-type="bibr">34</xref>]. Hence, peptides mimicking HR1 or HR2 may interfere with the viral membrane-fusion process [<xref rid="B34-viruses-11-00663" ref-type="bibr">34</xref>]. Moreover, RBD-targeting neutralizing monoclonal antibodies (mAbs) can block the viral attachment step [<xref rid="B37-viruses-11-00663" ref-type="bibr">37</xref>]. In addition to conventional mAbs, single-domain antibodies isolated from camelids, called nanobodies (Nbs), can also block RBD/receptor interactions; these Nbs have been gaining popularity as therapeutic agents due to their small size and high stability [<xref rid="B41-viruses-11-00663" ref-type="bibr">41</xref>,<xref rid="B42-viruses-11-00663" ref-type="bibr">42</xref>]. Thus, both the HR1/HR2 peptide mimics and RBD-targeting mAbs and Nbs may serve as MERS-CoV entry inhibitors. Furthermore, small molecules targeting the S protein or nonstructural proteins may serve as therapeutic alternatives to peptide mimics and antibodies [<xref rid="B16-viruses-11-00663" ref-type="bibr">16</xref>,<xref rid="B43-viruses-11-00663" ref-type="bibr">43</xref>]. In this issue, two review articles report the current advances in therapeutic neutralizing antibodies, one by Han and colleagues and the other by Zhou and colleagues [<xref rid="B37-viruses-11-00663" ref-type="bibr">37</xref>,<xref rid="B44-viruses-11-00663" ref-type="bibr">44</xref>]. The latter article also discusses potential strategies and challenges to improving the efficacy of therapeutic neutralizing antibodies. In a research article, He and colleagues describe the construction and expression of dimeric and trimeric Nbs that target MERS-CoV RBD and further demonstrate the strong stability and high neutralizing activity of these Nbs against multiple MERS-CoV strains [<xref rid="B42-viruses-11-00663" ref-type="bibr">42</xref>]. In another research article, Xia and colleagues report that three peptides mimicking HR2 from HKU4 (which is a MERS-related coronavirus from bats) strongly inhibit MERS-CoV infection [<xref rid="B45-viruses-11-00663" ref-type="bibr">45</xref>]. Interestingly, Wang and colleagues report that the combination of a MERS-CoV HR2 peptide mimic and an RBD-targeting neutralizing mAb demonstrate potent synergistic effects in inhibiting MERS-CoV S protein-mediated viral entry [<xref rid="B46-viruses-11-00663" ref-type="bibr">46</xref>]. In another research article, Jiang and colleagues report that an antibody targeting complement receptor C5aR1 inhibits MERS-CoV infection, indicating that MERS-CoV infection elicits the over-activation of the complement system, and this process can be blocked by anti-C5aR1 antibodies [<xref rid="B47-viruses-11-00663" ref-type="bibr">47</xref>]. Moreover, Liang and colleagues review advances in the development of small-molecular MERS-CoV inhibitors [<xref rid="B48-viruses-11-00663" ref-type="bibr">48</xref>]. Overall, these articles confirm that anti-MERS-CoV therapeutics have great potentials in treating MERS-CoV infections in humans and other animals. </p><p>To summarize, significant progress has been made in MERS-CoV research in the past seven years since the virus was discovered. This progress includes, but is not limited to, the epidemiology, transmission, and pathogenesis of MERS-CoV, as well as animal models, vaccines, and antivirals for MERS-CoV. This special issue of <italic>Viruses</italic> provides updated reports on this progress. However, challenges remain. For example, we still do not understand how exactly MERS-CoV transmits from bats to camels or humans. Moreover, compared to HIV and influenza viruses, the potential market for MERS-CoV vaccines and therapeutics is much smaller, making commercialization of MERS-related products more challenging. Nevertheless, the past two decades have witnessed the emergence of two highly pathogenic coronaviruses, MERS-CoV and SARS-CoV. While these two viruses remain significant threats to global health, future novel coronaviruses with pandemic potential may emerge from their animal reservoirs and infect humans. Thus, research into MERS-CoV should remain a high priority for the virology community. In fact, the impressive progress in MERS-CoV research has benefitted tremendously from previous research into coronaviruses including SARS-CoV. Therefore, scientists’ current efforts regarding MERS-CoV will prepare humans to battle any future novel coronaviruses with pandemic potential.</p></body><back><ack><title>Acknowledgments</title><p>Our studies are supported by the NIH grants (R01AI139092, R01AI137472, R01AI089728, and R01AI110700). 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