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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Immune responses in influenza A virus and human coronavirus infections: an ongoing battle between the virus and host</title><author><name sortKey="Zheng, Jian" sort="Zheng, Jian" uniqKey="Zheng J" first="Jian" last="Zheng">Jian Zheng</name></author><author><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29172107</idno><idno type="pmc">5835172</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5835172</idno><idno type="RBID">PMC:5835172</idno><idno type="doi">10.1016/j.coviro.2017.11.002</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">001305</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001305</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Immune responses in influenza A virus and human coronavirus infections: an ongoing battle between the virus and host</title><author><name sortKey="Zheng, Jian" sort="Zheng, Jian" uniqKey="Zheng J" first="Jian" last="Zheng">Jian Zheng</name></author><author><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name></author></analytic><series><title level="j">Current Opinion in Virology</title><idno type="ISSN">1879-6257</idno><idno type="eISSN">1879-6265</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Highlights</title><p><list list-type="simple" id="lis0005"><list-item id="lsti0005"><label>•</label><p id="par0005">Host immune responses play both protective and pathogenic roles in IAV and CoV infections.</p></list-item><list-item id="lsti0010"><label>•</label><p id="par0010">Synergy of adaptive and innate immunity is required for efficient control of virus infection.</p></list-item><list-item id="lsti0015"><label>•</label><p id="par0015">Novel strategies are needed to suppress immunoevasion and to improve antiviral effects.</p></list-item><list-item id="lsti0020"><label>•</label><p id="par0020">Vaccine-mediated protection could be improved by optimizing immune responses.</p></list-item><list-item id="lsti0025"><label>•</label><p id="par0025">Understanding co-evolution of host and virus is key to predicting viral mutation and transmission.</p></list-item></list></p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zhao, J" uniqKey="Zhao J">J. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Curr Opin Virol</journal-id><journal-id journal-id-type="iso-abbrev">Curr Opin Virol</journal-id><journal-title-group><journal-title>Current Opinion in Virology</journal-title></journal-title-group><issn pub-type="ppub">1879-6257</issn><issn pub-type="epub">1879-6265</issn><publisher><publisher-name>Elsevier</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">29172107</article-id><article-id pub-id-type="pmc">5835172</article-id><article-id pub-id-type="publisher-id">S1879-6257(17)30119-0</article-id><article-id pub-id-type="doi">10.1016/j.coviro.2017.11.002</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Immune responses in influenza A virus and human coronavirus infections: an ongoing battle between the virus and host</article-title></title-group><contrib-group><contrib contrib-type="author" id="aut0005"><name><surname>Zheng</surname><given-names>Jian</given-names></name></contrib><contrib contrib-type="author" id="aut0010"><name><surname>Perlman</surname><given-names>Stanley</given-names></name><email>Stanley-perlman@uiowa.edu</email></contrib></contrib-group><aff id="aff0005">Department of Microbiology and Immunology, The University of Iowa, Iowa City, IA 52242, United States</aff><pub-date pub-type="pmc-release"><day>21</day><month>11</month><year>2017</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>2</month><year>2018</year></pub-date><pub-date pub-type="epub"><day>21</day><month>11</month><year>2017</year></pub-date><volume>28</volume><fpage>43</fpage><lpage>52</lpage><permissions><copyright-statement>© 2017 Elsevier B.V. All rights reserved.</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>Elsevier B.V.</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 abstract-type="author-highlights" id="abs0005"><title>Highlights</title><p><list list-type="simple" id="lis0005"><list-item id="lsti0005"><label>•</label><p id="par0005">Host immune responses play both protective and pathogenic roles in IAV and CoV infections.</p></list-item><list-item id="lsti0010"><label>•</label><p id="par0010">Synergy of adaptive and innate immunity is required for efficient control of virus infection.</p></list-item><list-item id="lsti0015"><label>•</label><p id="par0015">Novel strategies are needed to suppress immunoevasion and to improve antiviral effects.</p></list-item><list-item id="lsti0020"><label>•</label><p id="par0020">Vaccine-mediated protection could be improved by optimizing immune responses.</p></list-item><list-item id="lsti0025"><label>•</label><p id="par0025">Understanding co-evolution of host and virus is key to predicting viral mutation and transmission.</p></list-item></list></p></abstract><abstract id="abs0010"><p>Respiratory viruses, especially influenza A viruses and coronaviruses such as MERS-CoV, represent continuing global threats to human health. Despite significant advances, much needs to be learned. Recent studies in virology and immunology have improved our understanding of the role of the immune system in protection and in the pathogenesis of these infections and of co-evolution of viruses and their hosts. These findings, together with sophisticated molecular structure analyses, omics tools and computer-based models, have helped delineate the interaction between respiratory viruses and the host immune system, which will facilitate the development of novel treatment strategies and vaccines with enhanced efficacy.</p></abstract></article-meta></front><body><p id="par0030"><boxed-text id="tb0005"><p id="par0035"><bold>Current Opinion in Virology</bold> 2018, <bold>28</bold>:43–52</p><p id="par0040">This review comes from a themed issue on <bold>Viral immunology</bold></p><p id="par0045">Edited by <bold>Heather D Hickman</bold> and <bold>Mehul Suthar</bold></p><p id="par1050">For a complete overview see the <ext-link ext-link-type="uri" xlink:href="http://www.sciencedirect.com/science/journal/18796257/28" id="intr9065"><underline>Issue</underline></ext-link> and the <ext-link ext-link-type="doi" xlink:href="10.1016/j.coviro.2018.02.003" id="intr9070"><underline>Editorial</underline></ext-link></p><p id="par9220">Available online 21st November 2017</p><p id="par0050"><ext-link ext-link-type="doi" xlink:href="10.1016/j.coviro.2017.11.002" id="intr0005"><bold>https://doi.org/10.1016/j.coviro.2017.11.002</bold></ext-link></p><p id="par0055">1879-6257/© 2017 Elsevier B.V. All rights reserved.</p></boxed-text></p><p id="par0060">The structure of the respiratory tract facilitates gas exchange between the exterior environment and interior milieu of the host, while it is a susceptible target and feasible gateway for diverse invasive pathogens. The immune system consists of multiple physical, cellular and molecular components and plays a crucial role in the host defense against microbial invasion. In this mini-review, we will summarize recent findings in respiratory virus immunology research focusing on influenza A virus (IAV) and coronaviruses including SARS (Severe Acute Respiratory Syndrome)-CoV and MERS (Middle East Respiratory Syndrome)-CoV. We will also discuss some key questions that remain to be answered and potential applications of our current knowledge to prevent and treat respiratory virus infection in the clinic.</p><sec id="sec0005"><title>Immune response: protective or pathogenic?</title><p id="par0065">The host immune system is composed of multiple tissues, cells and molecules and can protect hosts from infectious diseases by recognizing and eliminating pathogens efficiently. In one example, our studies of mice infected with SARS-CoV showed that the severity of SARS correlated with the ability to develop a virus-specific immune response, while inhibitory alveolar macrophages and inefficient activation of dendritic cells (DCs) delayed this process and aggravated disease [<xref rid="bib0750" ref-type="bibr">1</xref>]. In another study, Channappanavar <italic>et al.</italic> further demonstrated that dysregulated type I interferon (IFN) and inflammatory monocyte-macrophage responses led to lethal pneumonia in SARS-CoV-infected mice [<xref rid="bib0755" ref-type="bibr">2</xref>]. In support of these data, inhibition of nuclear factor-kappaB (NF-κB)-mediated inflammation in SARS-CoV-infected mice increased survival [<xref rid="bib0760" ref-type="bibr">3</xref>]. Similar to their pathological roles in coronavirus infections, inappropriate or dysfunctional immune responses such as overactivation of NACHT, LRR and PYD domains-containing protein 3 (NLRP3), high-mobility group box 1 protein (HMGB-1) and interleukin-1beta (IL-1β), have been implicated in host tissue destruction [<xref rid="bib0765" ref-type="bibr">4</xref>, <xref rid="bib0770" ref-type="bibr">5</xref>, <xref rid="bib0775" ref-type="bibr">6</xref>, <xref rid="bib0780" ref-type="bibr">7</xref>, <xref rid="bib0785" ref-type="bibr">8</xref>] and persistent pathological changes in IAV-infected hosts [<xref rid="bib0790" ref-type="bibr">9</xref>]. Expression of the complex of tumor necrosis factor (TNF) superfamily 10 (TNFSF10), histone deacetylase 4 (HDAC4) and HDAC5 negatively correlated with the levels of TNF-α, NF-κB and cyclooxygenase 2 (COX-2) and increases in their expression was correlated with improved prognosis of IAV-infected hosts [<xref rid="bib0795" ref-type="bibr">10</xref>]. In addition to their cell-intrinsic properties, lung macrophage and monocyte heterogeneity in localization in IAV infections also contributed to differences in outcomes [<xref rid="bib0800" ref-type="bibr">11</xref>].</p></sec><sec id="sec0010"><title>Both adaptive and innate immune responses are required for host protection</title><p id="par0070">The adaptive immune response efficiently recognizes and destroys specific pathogens [<xref rid="bib0805" ref-type="bibr">12</xref>], and thus restricts the spread of pathogens usually without causing significant non-specific inflammation. However, despite intensive investigations and substantial advances in past decades, questions about the initiation, development, regulation, contraction and re-activation of adaptive immune responses upon pathogen challenge remain areas of research [<xref rid="bib0810" ref-type="bibr">13</xref>, <xref rid="bib0815" ref-type="bibr">14</xref>, <xref rid="bib0820" ref-type="bibr">15</xref>, <xref rid="bib0825" ref-type="bibr">16</xref>, <xref rid="bib0830" ref-type="bibr">17•</xref>, <xref rid="bib0835" ref-type="bibr">18</xref>, <xref rid="bib0840" ref-type="bibr">19</xref>, <xref rid="bib0845" ref-type="bibr">20</xref>, <xref rid="bib0850" ref-type="bibr">21</xref>, <xref rid="bib0855" ref-type="bibr">22</xref>, <xref rid="bib0860" ref-type="bibr">23</xref>, <xref rid="bib0865" ref-type="bibr">24</xref>, <xref rid="bib0870" ref-type="bibr">25</xref>, <xref rid="bib0875" ref-type="bibr">26</xref>, <xref rid="bib0880" ref-type="bibr">27</xref>, <xref rid="bib0885" ref-type="bibr">28</xref>, <xref rid="bib0890" ref-type="bibr">29</xref>, <xref rid="bib0895" ref-type="bibr">30•</xref>, <xref rid="bib0900" ref-type="bibr">31</xref>, <xref rid="bib0905" ref-type="bibr">32••</xref>, <xref rid="bib0910" ref-type="bibr">33</xref>] (summarized in <xref rid="tbl0005" ref-type="table">Table 1</xref>.)<table-wrap position="float" id="tbl0005"><label>Table 1</label><caption><p>Recent findings related to adaptive immune responses against IAV and CoV infections</p></caption><alt-text id="at1">Table 1</alt-text><table frame="hsides" rules="groups"><thead><tr><th align="left">Response type</th><th align="center">Virus strain</th><th align="center">Major findings</th><th align="center">Ref.</th></tr></thead><tbody><tr><td align="left">B cell/antibody response</td><td align="left">IAV</td><td align="left">Repertoire diversity is a driving force behind IAV-specific B-cell immunity.</td><td align="left">[<xref rid="bib0810" ref-type="bibr">13</xref>]</td></tr><tr><td></td><td></td><td align="left">Broadly neutralizing antibodies generally target conserved functional regions on HA.</td><td align="left">[<xref rid="bib0850" ref-type="bibr">21</xref>]</td></tr><tr><td></td><td></td><td align="left">Binding of antibody to an epitope masks the epitope and prevents the stimulation and proliferation of specific B cells.</td><td align="left">[<xref rid="bib0895" ref-type="bibr">30</xref>]</td></tr><tr><td></td><td align="left">MERS-CoV</td><td align="left">Recombinant receptor-binding domains of multiple MERS-CoVs induce cross-neutralizing antibodies against divergent human and camel MERS-CoVs.</td><td align="left">[<xref rid="bib0885" ref-type="bibr">28</xref>]</td></tr><tr><td align="left">T cell response</td><td align="left">IAV</td><td align="left">Vaccine-generated lung-resident memory CD8 T cells provide heterosubtypic protection to IAV infection.</td><td align="left">[<xref rid="bib0900" ref-type="bibr">31</xref>]</td></tr><tr><td></td><td></td><td align="left">Potential challenges in translating protective memory CD4 T cell responses in experimental animal models to patients.</td><td align="left">[<xref rid="bib0840" ref-type="bibr">19</xref>]</td></tr><tr><td></td><td align="left">MERS-CoV</td><td align="left">MERS-CoV efficiently infects human primary T cells and induces apoptosis.</td><td align="left">[<xref rid="bib0815" ref-type="bibr">14</xref>]</td></tr><tr><td></td><td align="left">SARS-CoV</td><td align="left">Memory T cell responses targeting the SARS coronavirus persist for up to 11 years postinfection.</td><td align="left">[<xref rid="bib0860" ref-type="bibr">23</xref>]</td></tr><tr><td align="left">Crosstalk between immune components</td><td align="left">IAV</td><td align="left">Cooperativity between CD8+ T cells, non-neutralizing antibodies, and alveolar macrophages is important for heterosubtypic IAV immunity.</td><td align="left">[<xref rid="bib0845" ref-type="bibr">20</xref>]</td></tr><tr><td></td><td></td><td align="left">Antibody specificity plays an important role in the regulation of ADCC.<break></break>Cross-talk among antibodies of varying specificities determines the magnitude of Fc receptor-mediated effector functions.</td><td align="left">[<xref rid="bib0830" ref-type="bibr">17</xref>]</td></tr><tr><td></td><td></td><td align="left">IgE cross-linking impairs monocyte antiviral responses and inhibits IAV-driven Th1 differentiation.</td><td align="left">[<xref rid="bib0880" ref-type="bibr">27</xref>]</td></tr><tr><td></td><td align="left">MERS-CoV</td><td align="left">Recovery from the Middle East respiratory syndrome is associated with antibody and T-cell responses.</td><td align="left">[<xref rid="bib0905" ref-type="bibr">32</xref>]</td></tr><tr><td align="left">Maintenance of immune memory</td><td align="left">IAV</td><td align="left">Levels of neutralizing antibodies against previously encountered IAV strains (‘original antigenic sin’) increase over time.</td><td align="left">[<xref rid="bib0855" ref-type="bibr">22</xref>]</td></tr><tr><td></td><td></td><td align="left">Low levels of circulating CD8+ T effector and central memory cells are associated with IAV infection severity upon re-challenge.</td><td align="left">[<xref rid="bib0825" ref-type="bibr">16</xref>]</td></tr><tr><td></td><td></td><td align="left">Regimen of a CTL-based vaccine/vaccine-component benefits from periodic boosting to prevent clinically evident IAV infection.</td><td align="left">[<xref rid="bib0875" ref-type="bibr">26</xref>]</td></tr><tr><td></td><td></td><td align="left">Multifunctional CD4+ T-cell responses were maintained only in patients with recurrent infections.</td><td align="left">[<xref rid="bib0890" ref-type="bibr">29</xref>]</td></tr><tr><td align="left">Immunopathology</td><td align="left">IAV</td><td align="left">IAV-specific CD8+ T cells exacerbate infection following high dose challenge of aged mice.</td><td align="left">[<xref rid="bib0870" ref-type="bibr">25</xref>]</td></tr><tr><td></td><td></td><td align="left">Different subsets of CD8+ T cells interact with subsets of innate cells through costimulatory molecules to balance protection and immunopathology.</td><td align="left">[<xref rid="bib0820" ref-type="bibr">15</xref>]</td></tr><tr><td></td><td></td><td align="left">Identification of protective and pathogenic T cell epitopes in IAV H7N9-infected patients.</td><td align="left">[<xref rid="bib0835" ref-type="bibr">18</xref>]</td></tr><tr><td align="left">Immunotherapy</td><td align="left">IAV, CoV</td><td align="left">High titer anti-IAV or CoV sera may be useful prophylactically and therapeutically in exposed and infected patients.</td><td align="left">[<xref rid="bib0865" ref-type="bibr">24</xref>, <xref rid="bib0910" ref-type="bibr">33</xref>]</td></tr></tbody></table></table-wrap></p><p id="par0075">The innate immune system is responsible for initial responses to pathogens and is critical even in the context of vaccinated IAV individuals or mice, in which hemagglutinin (HA), neuraminidase (NA) and glycosylation pattern mutations [<xref rid="bib0865" ref-type="bibr">24</xref>], might hinder an effective antibody and T cell response. The contribution of innate immunity to immune defense is not limited in direct anti-viral effects [<xref rid="bib0915" ref-type="bibr">34</xref>]. Innate immune signals such as IFN-I not only interact with other innate immune elements such as monocytes and type-II IFN to limit IAV-caused tissue inflammation [<xref rid="bib0920" ref-type="bibr">35</xref>], but also directly modulated the adaptive immune response. Both IFN-I and toll-like receptor 7 (TLR7) were also found to shape B cell-mediated immune responses against IAV [<xref rid="bib0925" ref-type="bibr">36</xref>], while RIG-I signaling was critical for efficient polyfunctional T cell responses [<xref rid="bib0930" ref-type="bibr">37</xref>]. Moreover, the increased mortality of IAV-infected mice in the absence of mitochondrial antiviral signaling (Mavs) and TLR7 was found to independent of viral load or myeloid differentiation primary response 88 (MYD88)-dependent signaling but dependent on secondary bacterial burden, caspase-1/11, and neutrophil-dependent tissue damage [<xref rid="bib0935" ref-type="bibr">38<sup>••</sup></xref>].</p><p id="par0080">As for innate immune cells, a population of lung-resident innate lymphoid cells (ILCs) in mice and humans that expressed CD90, CD25, CD127 and ST2 was found to contribute to airway epithelial integrity and its depletion resulted in diminished lung function and impaired airway remodeling [<xref rid="bib0940" ref-type="bibr">39</xref>]. In other reports, pulmonary endothelial cells [<xref rid="bib0945" ref-type="bibr">40</xref>], lung microvascular endothelial cells [<xref rid="bib0950" ref-type="bibr">41</xref>], neutrophils [<xref rid="bib0955" ref-type="bibr">42</xref>], eosinophils [<xref rid="bib0960" ref-type="bibr">43</xref>], lung mast cells [<xref rid="bib0965" ref-type="bibr">44</xref>], plasmacytoid dendritic cells (pDC) and invariant natural killer cells (iNKT) [<xref rid="bib0970" ref-type="bibr">45</xref>] were all identified as therapeutic targets in severe IAV and CoV infections. However, the involvement of innate immunity in specific populations, such as infants [<xref rid="bib0975" ref-type="bibr">46<sup>•</sup></xref>], children [<xref rid="bib0980" ref-type="bibr">47</xref>], the aged [<xref rid="bib0985" ref-type="bibr">48</xref>] and patients suffering from chronic airway diseases [<xref rid="bib0990" ref-type="bibr">49</xref>] or frequent re-infection with IAV [<xref rid="bib0995" ref-type="bibr">50<sup>•</sup></xref>], needs further investigations.</p><p id="par0085">With the increasing accumulation of knowledge of molecular interactions between host cells and viruses, additional host molecules and normal biological processes [<xref rid="bib1000" ref-type="bibr">51</xref>, <xref rid="bib1005" ref-type="bibr">52</xref>, <xref rid="bib1010" ref-type="bibr">53</xref>, <xref rid="bib1015" ref-type="bibr">54</xref>, <xref rid="bib1020" ref-type="bibr">55</xref>, <xref rid="bib1025" ref-type="bibr">56</xref>, <xref rid="bib1030" ref-type="bibr">57</xref>, <xref rid="bib1035" ref-type="bibr">58</xref>, <xref rid="bib1040" ref-type="bibr">59</xref>, <xref rid="bib1045" ref-type="bibr">60</xref>, <xref rid="bib1050" ref-type="bibr">61</xref>, <xref rid="bib1055" ref-type="bibr">62</xref>, <xref rid="bib1060" ref-type="bibr">63</xref>, <xref rid="bib1065" ref-type="bibr">64</xref>, <xref rid="bib1070" ref-type="bibr">65</xref>, <xref rid="bib1075" ref-type="bibr">66•</xref>, <xref rid="bib1080" ref-type="bibr">67</xref>, <xref rid="bib1085" ref-type="bibr">68</xref>, <xref rid="bib1090" ref-type="bibr">69</xref>] were found to participate in the viral replication cycle (summarized in <xref rid="tbl0010" ref-type="table">Table 2</xref>). To clarify the roles of these molecules and processes in virus infection, host genetic determinant screening [<xref rid="bib1095" ref-type="bibr">70</xref>, <xref rid="bib1100" ref-type="bibr">71</xref>, <xref rid="bib1105" ref-type="bibr">72</xref>], immunomics and Public Health Omics [<xref rid="bib1110" ref-type="bibr">73</xref>], host lipid omics [<xref rid="bib1115" ref-type="bibr">74<sup>••</sup></xref>] and characterization of the epigenetic landscape [<xref rid="bib1120" ref-type="bibr">75</xref>] were used to supplement conventional analyses. Moreover, information about interaction between immune and parenchymal cells also facilitated efforts to optimize antiviral response while reducing unwanted side effects [<xref rid="bib1125" ref-type="bibr">76•</xref>, <xref rid="bib1130" ref-type="bibr">77•</xref>]. Computer modeling of host-pathogen interactions is likely to be used more in the future, as additional parameters are identified. Thus, computer modeling helped in prediction of clinical outcomes, demonstrating key roles for the innate immune response and the interval between infections [<xref rid="bib1135" ref-type="bibr">78</xref>]. These novel methodologies are likely to provide additional approaches to identifying targets for novel antiviral therapies.<table-wrap position="float" id="tbl0010"><label>Table 2</label><caption><p>Recent findings related to intrinsic molecules and biological processes involved in IAV and CoV infectionss.</p></caption><alt-text id="at2">Table 2</alt-text><table frame="hsides" rules="groups"><thead><tr><th align="left">Molecules/processes</th><th align="center">Virus strain</th><th align="center">Major findings</th><th align="left">Ref.</th></tr></thead><tbody><tr><td align="left">Cell cycling proteins</td><td align="left">IAV</td><td align="left">Competitive inhibition of IAV M1–M2 interaction by cyclin D3 impairs infectious virus packaging, resulting in attenuation</td><td align="left">[<xref rid="bib1030" ref-type="bibr">57</xref>]</td></tr><tr><td align="left">Apoptosis-related signals</td><td align="left">IAV</td><td align="left">Apoptosis signaling modulates IAV propagation, innate host defense, and lung injury.</td><td align="left">[<xref rid="bib1045" ref-type="bibr">60</xref>]</td></tr><tr><td align="left">Sex hormones-related signals</td><td align="left">IAV</td><td align="left">Progesterone-based contraceptives reduce adaptive immune responses and protection against subsequent IAV infections.</td><td align="left">[<xref rid="bib1040" ref-type="bibr">59</xref>]</td></tr><tr><td></td><td align="left">SARS-CoV</td><td align="left">Male mice were more susceptible to SARS-CoV infection compared with age-matched females, while estrogen receptor signaling played a critical role in protecting females from SARS-CoV-mediated pathogenesis.</td><td align="left">[<xref rid="bib1010" ref-type="bibr">53</xref>]</td></tr><tr><td align="left">CHD chromatin remodeler</td><td align="left">IAV</td><td align="left">CHD1 is a proviral regulator of IAV multiplication.</td><td align="left">[<xref rid="bib1060" ref-type="bibr">63</xref>]</td></tr><tr><td align="left">Nuclear import and export machinery</td><td align="left">IAV</td><td align="left">IAV have evolved different mechanisms to utilize importin-alpha isoforms, affecting importation on both sides of the nuclear envelope.</td><td align="left">[<xref rid="bib1070" ref-type="bibr">65</xref>]</td></tr><tr><td></td><td></td><td align="left">Activation of the interferon induction cascade by IAV requires viral RNA synthesis and nuclear export.</td><td align="left">[<xref rid="bib1050" ref-type="bibr">61</xref>]</td></tr><tr><td></td><td></td><td align="left">Human heat shock protein 40 promotes IAV replication by assisting in the nuclear import of viral ribonucleoproteins.</td><td align="left">[<xref rid="bib1005" ref-type="bibr">52</xref>]</td></tr><tr><td></td><td></td><td align="left">Preferential usage of importin-alpha7 isoforms by seasonal IAV in the human upper respiratory tract makes it a target of selective pressure.</td><td align="left">[<xref rid="bib1065" ref-type="bibr">64</xref>]</td></tr><tr><td align="left">Vesicular trafficking</td><td align="left">IAV</td><td align="left">IAV infection modulates vesicular trafficking and induces Golgi complex disruption.</td><td align="left">[<xref rid="bib1085" ref-type="bibr">68</xref>]</td></tr><tr><td></td><td></td><td align="left">IAV enhances its propagation through modulating Annexin-A1 dependent endosomal trafficking.</td><td align="left">[<xref rid="bib1000" ref-type="bibr">51</xref>]</td></tr><tr><td></td><td></td><td align="left">IAV ribonucleoproteins modulate host recycling by competing with Rab11 effectors.</td><td align="left">[<xref rid="bib1080" ref-type="bibr">67</xref>]</td></tr><tr><td></td><td align="left">SARS-CoV</td><td align="left">A predicted beta-hairpin structural motif in the cytoplasmic tail of the SARS-CoV E protein is sufficient for Golgi complex localization of a reporter protein and functions as a Golgi complex-targeting signal.</td><td align="left">[<xref rid="bib1015" ref-type="bibr">54</xref>]</td></tr><tr><td></td><td align="left">MERS-CoV</td><td align="left">CD9-facilitated condensation of receptors and proteases allows MERS-CoV pseudoviruses to enter cells rapidly and efficiently.</td><td align="left">[<xref rid="bib1025" ref-type="bibr">56</xref>]</td></tr><tr><td align="left">Exosome secretion</td><td align="left">IAV</td><td align="left">Exosome deficiency uncoupled chromatin targeting of the viral polymerase complex and the formation of cellular-viral RNA hybrids, which are essential RNA intermediates that license transcription of antisense genomic viral RNAs</td><td align="left">[<xref rid="bib1075" ref-type="bibr">66</xref>]</td></tr><tr><td align="left">Autophagy</td><td align="left">IAV</td><td align="left">Autophagy induction regulates IAV replication in a time-dependent manner.</td><td align="left">[<xref rid="bib1035" ref-type="bibr">58</xref>]</td></tr><tr><td></td><td align="left">SARS-CoV</td><td align="left">CoV nsp6 restricts autophagosome expansion.</td><td align="left">[<xref rid="bib1020" ref-type="bibr">55</xref>]</td></tr><tr><td align="left">Cellular senescence</td><td align="left">IAV</td><td align="left">Cellular senescence enhances viral replication.</td><td align="left">[<xref rid="bib1055" ref-type="bibr">62</xref>]</td></tr><tr><td align="left">Coagulation</td><td align="left">IAV</td><td align="left">Beneficial effects of inflammation-coagulation interactions during IAV infection</td><td align="left">[<xref rid="bib1090" ref-type="bibr">69</xref>]</td></tr></tbody></table></table-wrap></p></sec><sec id="sec0015"><title>Immune evasion by respiratory viruses</title><p id="par0090">The IAV non-structural protein NS1, perhaps the best-characterized viral immunoevasive protein, binds double-stranded RNA (dsRNA) to inhibit host innate immune responses [<xref rid="bib1140" ref-type="bibr">79</xref>, <xref rid="bib1145" ref-type="bibr">80</xref>, <xref rid="bib1150" ref-type="bibr">81</xref>]. Recently, NS1 was also found to bind cellular dsDNA and prevent the loading of transcriptional machinery onto the DNA, thus attenuating expression of antiviral genes [<xref rid="bib1155" ref-type="bibr">82</xref>]. Meanwhile, the C-terminal domain of NS1 blocked IFN-beta production by targeting TNF receptor-associated factor 3 (TRAF-3) [<xref rid="bib1160" ref-type="bibr">83</xref>], while other domains of the protein inhibited interferon regulatory transcription factor 3 (IRF3) [<xref rid="bib1165" ref-type="bibr">84</xref>] and RNA-dependent protein kinase (PKR) activation [<xref rid="bib1170" ref-type="bibr">85</xref>]. Another IAV protein, neuraminidase (NA), was shown to remove sialic acid residues from NKp46, resulting in reduced recognition of HA and enhancing immune evasion of NK cells [<xref rid="bib1175" ref-type="bibr">86</xref>]. In addition, the IAV M2 protein was shown to reverse bone marrow stromal antigen 2 (BST-2)-mediated restriction of virus release via proteasomal pathways [<xref rid="bib1180" ref-type="bibr">87</xref>]. To evade the host immune system, IAV also inhibits host but not viral mRNA nuclear export [<xref rid="bib1185" ref-type="bibr">88</xref>], without impairing nuclear viral ribonucleoprotein (vRNP) import [<xref rid="bib1190" ref-type="bibr">89</xref>]. In addition, productive viral replication in macrophages resulted in decreased phagocytosis via downregulation of Fc receptors CD16 and CD32, potentially playing a role in IAV pathogenesis [<xref rid="bib1195" ref-type="bibr">90</xref>].</p><p id="par0095">The crucial role of the IFN response makes it a preferred target for viral evasion. Besides NS1, multiple virus-encoded molecules including the nucleoprotein [<xref rid="bib1065" ref-type="bibr">64</xref>], the fusion peptide of HA2 (HA2-FP), HA1 and some variants of polymerase subunits PB1-F2, PB1, PB2, PA all counteract the interferon response [<xref rid="bib1200" ref-type="bibr">91</xref>]. Interestingly, some host cellular molecules are also utilized by IAV to block IFN expression. Using RNA interference, knockdown of a host factor, the double PHD fingers 2 gene (DPF2) [<xref rid="bib1205" ref-type="bibr">92</xref>], resulted in decreased expression of IAV proteins, by releasing IFN-β production from DPF2-mediated suppression [<xref rid="bib1205" ref-type="bibr">92</xref>].</p><p id="par0100">The CoV endonuclease, nsp15, efficiently prevented activation of host cell dsRNA sensors including melanoma differentiation-associated protein 5 (Mda5), 2′–5′ oligoadenylate synthetase (OAS) and PKR [<xref rid="bib1210" ref-type="bibr">93</xref>, <xref rid="bib1215" ref-type="bibr">94•</xref>], while coronavirus-encoded proteases countered innate immunity, including the IFN response, through diverse pathways [<xref rid="bib1220" ref-type="bibr">95</xref>]. A recent investigation further showed that SARS-CoV nucleocapsid inhibited Type I interferon production by interfering with tripartite motif protein 25 (TRIM25)-mediated RIG-I ubiquitination [<xref rid="bib1225" ref-type="bibr">96</xref>].</p></sec><sec id="sec0020"><title>Modulation of immune responses against respiratory virus infection: novel targets</title><p id="par0105">Recent studies of cellular metabolic processes [<xref rid="bib1230" ref-type="bibr">97</xref>, <xref rid="bib1235" ref-type="bibr">98</xref>] and post-transcriptional protein modification [<xref rid="bib1240" ref-type="bibr">99</xref>, <xref rid="bib1245" ref-type="bibr">100</xref>] identified additional approaches used by viruses to evade host immune responses [<xref rid="bib1250" ref-type="bibr">101</xref>], and to facilitate optimal replication [<xref rid="bib1255" ref-type="bibr">102</xref>].</p><p id="par0110">For example, IAV delayed apoptosis of infected cells by activating a signal transducer and activator of transcription 3 (stat-3)-related pathway, allowing prolonged replication [<xref rid="bib1260" ref-type="bibr">103</xref>]. Nicotinamide adenine dinucleotide phosphate (NADPH) oxidase 2 (NOX2), critical for expression of reactive oxygen species (ROS), is often activated in endocytic compartments by RNA and DNA viruses, exacerbating virus-mediated pathogenicity [<xref rid="bib1265" ref-type="bibr">104<sup>•</sup></xref>]. In addition to important roles for host proteins [<xref rid="bib1270" ref-type="bibr">105</xref>], the role of lipids [<xref rid="bib1115" ref-type="bibr">74<sup>••</sup></xref>] in respiratory virus infections has also drawn increasing attention. Zhao <italic>et al.</italic> reported that age-related increases in prostaglandin D2 (PGD<sub>2</sub>) expression in mouse lungs correlated with a progressive impairment in DC migration to DLNs, causing diminished T cell responses upon IAV or SARS-CoV infection [<xref rid="bib1275" ref-type="bibr">106</xref>]. In a subsequent study, Vijay <italic>et al.</italic> demonstrated a critical role for phospholipase A2 group IID (PLA<sub>2</sub>G2D) in impaired DC migration to DLN and age-related susceptibility to SARS-CoV infection [<xref rid="bib1280" ref-type="bibr">107</xref>]. PLA<sub>2</sub>G2D is upstream of PGD<sub>2</sub> in the prostaglandin synthesis pathway. Both molecules may be useful targets for anti-viral therapies.</p><p id="par0115">As mentioned above, SARS-CoV nucleocapsid protein was reported to interfere with RIG-I ubiquitination [<xref rid="bib1225" ref-type="bibr">96</xref>], while decreased deubiquitination mediated by MERS-CoV nsp3 deubiquitinase also inhibited the host immune response [<xref rid="bib1285" ref-type="bibr">108</xref>]. Recently, Fehr <italic>et al.</italic> found that mutation of the macrodomain of nsp3, important for countering ADP-ribosylation, resulted in virus attenuation [<xref rid="bib1290" ref-type="bibr">109</xref>], while another report demonstrated that binding of the methyl donor S-adenosyl-<sc>l</sc>-methionine (SAM) to 2′-O-methyltransferase nsp16 enhanced MERS-CoV replication, promoting the recruitment of the allosteric activator nsp10 [<xref rid="bib1295" ref-type="bibr">110</xref>]. On the other hand, IAV induced host histone deacetylase 1 dysregulation in lung epithelial cells, inhibiting IAV infection [<xref rid="bib1300" ref-type="bibr">111</xref>] while NEDDylation (conjugation of a ubiquitin-like protein, neural precursor cell expressed developmentally down-regulated 8 (NEDD8)) of PB2 protein reduced its stability, suppressing IAV replication [<xref rid="bib1305" ref-type="bibr">112</xref>]. Nevertheless, the role of epigenetic modification during respiratory virus infection is not well understood; the application of phosphoproteomics to characterization of the human macrophage response to IAV infection [<xref rid="bib1310" ref-type="bibr">113</xref>] serves as a model for future studies.</p><p id="par0120">Other putative targets for modulating the immune response are carbohydrates present on host and viral proteins. Recently, integrated omics and computational glycobiology revealed the structural basis for IAV glycan microheterogeneity and host interactions [<xref rid="bib1315" ref-type="bibr">114</xref>, <xref rid="bib1320" ref-type="bibr">115</xref>, <xref rid="bib1325" ref-type="bibr">116</xref>]. Glycosylation of the HA protein not only mediated virus entry into host cells [<xref rid="bib1320" ref-type="bibr">115</xref>, <xref rid="bib1325" ref-type="bibr">116</xref>, <xref rid="bib1330" ref-type="bibr">117</xref>], but also modulated IAV replication and transmission [<xref rid="bib1335" ref-type="bibr">118</xref>], and the immune response against the virus [<xref rid="bib1340" ref-type="bibr">119</xref>, <xref rid="bib1345" ref-type="bibr">120</xref>, <xref rid="bib1350" ref-type="bibr">121</xref>], thus representing a potential target for vaccine and drug development [<xref rid="bib1355" ref-type="bibr">122</xref>, <xref rid="bib1360" ref-type="bibr">123•</xref>].</p></sec><sec id="sec0025"><title>Vaccine development update: establishing immune memory</title><p id="par0125">Vaccines remain as the most efficient tools for preventing the occurrence and spread of viral respiratory diseases. Distinct from conventional adjuvants, novel reagents are being used to shape as well as augment the strength of the induced immune responses. Targeting IAV HA to the chemokine receptor, Xcr1, present on some dendritic cells enhanced protective antibody responses against the virus [<xref rid="bib1365" ref-type="bibr">124</xref>]. In addition, knowledge of the microbiota [<xref rid="bib1370" ref-type="bibr">125</xref>], and manipulation of apoptosis [<xref rid="bib1375" ref-type="bibr">126</xref>] and mTOR (mechanistic target of rapamycin) [<xref rid="bib1380" ref-type="bibr">127</xref>]-related signaling pathways have been used to predict or modulate responsiveness and efficiency of vaccines, respectively. A major goal of IAV and CoV vaccine development is to develop vaccines able to induce broadly acting antibodies; these efforts require more precise definition of useful conserved protective antibody epitopes [<xref rid="bib1385" ref-type="bibr">128</xref>]. Further, monocyte-derived dendritic cells (moDCs) [<xref rid="bib1390" ref-type="bibr">129</xref>] dominated the activation of CD8+ T cells at late times after infection of C57BL/6 mice, triggering a switch in immunodominance from PA to NP-specificity. This differential expression of T cell epitopes has implications for DC-based vaccine design. Additionally, neutrophil-targeting [<xref rid="bib0955" ref-type="bibr">42</xref>] and Th1-targeting strategies [<xref rid="bib1395" ref-type="bibr">130</xref>] might help in establishing tissue-resident memory (TRM) and heterosubtypic immunity.</p><p id="par0130">Inducing effective resident immune memory represents an ideal strategy for protecting the host from respiratory virus infection, especially at very early phases of virus invasion. Recent technical advances have facilitated distinguishing tissue-resident cell populations from those in the periphery. In a recent publication, airway memory CD4(+) T cells induced by a single conserved N protein-specific epitope present in both SARS-CoV and MERS-CoV mediated protection against challenge with either pathogen [<xref rid="bib1400" ref-type="bibr">131<sup>•</sup></xref>]. IAV-specific resident memory CD8 cells in the upper respiratory tract or bronchoalveolar fluid provided superior protection compared to those in the lung, although some studies questioned whether these were truly resident memory as opposed to memory cells at these sites [<xref rid="bib1405" ref-type="bibr">132</xref>]. In a recent report, Slutter <italic>et al.</italic> delineated the dynamics of IAV-induced lung-resident memory T cells that underlies waning heterosubtypic immunity [<xref rid="bib1410" ref-type="bibr">133</xref>], illustrating the tight collaboration of resident and peripheral T cell memory in respiratory virus control. In the future, use of sophisticated cell sorting methods and mass spectrometric flow cytometry will provide more precise information about resident memory immune cells.</p><p id="par0135">The IAV-specific antibody response is well known to be a key host factor in protection from subsequent challenge [<xref rid="bib1415" ref-type="bibr">134</xref>, <xref rid="bib1420" ref-type="bibr">135</xref>]. Recent work has identified nasopharyngeal protein biomarkers in immunized mice useful for predicting the severity and outcome of acute respiratory virus infection [<xref rid="bib1425" ref-type="bibr">136</xref>]. Other studies have identified an important synergistic role for immune responses in inducible bronchus-associated lymphoid tissue (iBALT) and draining lymph nodes for optimal IAV-specific CD4+ T cell responses [<xref rid="bib1430" ref-type="bibr">137</xref>]. In contrast, nasal-associated lymphoid tissues (NALTs) have been shown to support the recall but not priming of IAV-specific cytotoxic T cells [<xref rid="bib1435" ref-type="bibr">138<sup>•</sup></xref>].</p></sec><sec id="sec0030"><title>Co-evolution of respiratory viruses and the host</title><p id="par0140">Genomics, next-generation sequencing [<xref rid="bib1440" ref-type="bibr">139</xref>] and single cell imaging and analysis [<xref rid="bib1445" ref-type="bibr">140</xref>] facilitated in-depth investigation of the evolution, recombination and spread of infectious pathogens and extend the scope of virology research. In addition to these molecular biology tools, methods such as analyses of DC responses [<xref rid="bib1450" ref-type="bibr">141</xref>] and digital cell quantification (DCQ), which combine genome-wide gene expression data with immune cell functional studies, will help identify immune cell subpopulations [<xref rid="bib1455" ref-type="bibr">142</xref>]. Especially critical for understanding the ecology of RNA viruses, such as IAV and CoV, will be obtaining respiratory samples from camels (MERS-CoV) and patients in both cross-sectional and longitudinal studies. These samples will be useful for identifying carriers and understanding virus evolution and transmission dynamics [<xref rid="bib1460" ref-type="bibr">143</xref>, <xref rid="bib1465" ref-type="bibr">144</xref>]. Recent analyses of MERS-CoV-infected camels [<xref rid="bib1470" ref-type="bibr">145</xref>] have also increased our knowledge of virus demography and evolution across diverse populations.</p><p id="par0145">Although gene sequencing and crystallographic analyses have provided insight into the molecular evolution of IAV, the inability to predict future virus evolution remains an obstacle in managing epidemic and pandemic spread. Models using canalized evolutionary trajectory induced by selective dynamics [<xref rid="bib1475" ref-type="bibr">146</xref>], intra-host IAV dynamics [<xref rid="bib1480" ref-type="bibr">147</xref>], sequence based epidemiology [<xref rid="bib1485" ref-type="bibr">148</xref>], genomic diversification and adaptation during experimental serial passages [<xref rid="bib1490" ref-type="bibr">149</xref>] will help in the development of accurate prediction models. However, successful modeling to prospectively predict the emergence of new virus strains relies on solid experimental data obtained from field investigations. The standardization of protocols and normalization of data are key challenges in developing useful models of virus evolution.</p></sec><sec id="sec0035"><title>Summary</title><p id="par0150">This brief review outlines how the host immune response plays both protective and pathogenic roles in respiratory virus infections. 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