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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The Potential Role of Th17 Immune Responses in Coronavirus Immunopathology and Vaccine-induced Immune Enhancement</title>
<author><name sortKey="Hotez, Peter J" sort="Hotez, Peter J" uniqKey="Hotez P" first="Peter J." last="Hotez">Peter J. Hotez</name>
<affiliation><nlm:aff id="aff1">Texas Children’s Hospital Center for Vaccine Development, Departments of Pediatrics and Molecular Virology & Microbiology, National School of Tropical Medicine, Baylor College of Medicine, Houston TX</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">Department of Biology, Baylor University, Waco TX</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff3">Hagler Institute of Advanced Study at Texas A&M University, College Station TX</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Bottazzi, Maria Elena" sort="Bottazzi, Maria Elena" uniqKey="Bottazzi M" first="Maria Elena" last="Bottazzi">Maria Elena Bottazzi</name>
<affiliation><nlm:aff id="aff1">Texas Children’s Hospital Center for Vaccine Development, Departments of Pediatrics and Molecular Virology & Microbiology, National School of Tropical Medicine, Baylor College of Medicine, Houston TX</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">Department of Biology, Baylor University, Waco TX</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Corry, David B" sort="Corry, David B" uniqKey="Corry D" first="David B." last="Corry">David B. Corry</name>
<affiliation><nlm:aff id="aff4">Biology of Inflammation Center, Departments of Medicine and Pathology & Immunology, and the Michael E. DeBakey Center for Translational Research in Inflammatory Diseases, Baylor College of Medicine, Houston TX</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmc">7162764</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7162764</idno>
<idno type="RBID">PMC:7162764</idno>
<idno type="doi">10.1016/j.micinf.2020.04.005</idno>
<idno type="pmid">NONE</idno>
<date when="2020">2020</date>
<idno type="wicri:Area/Pmc/Corpus">000A54</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000A54</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Potential Role of Th17 Immune Responses in Coronavirus Immunopathology and Vaccine-induced Immune Enhancement</title>
<author><name sortKey="Hotez, Peter J" sort="Hotez, Peter J" uniqKey="Hotez P" first="Peter J." last="Hotez">Peter J. Hotez</name>
<affiliation><nlm:aff id="aff1">Texas Children’s Hospital Center for Vaccine Development, Departments of Pediatrics and Molecular Virology & Microbiology, National School of Tropical Medicine, Baylor College of Medicine, Houston TX</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">Department of Biology, Baylor University, Waco TX</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff3">Hagler Institute of Advanced Study at Texas A&M University, College Station TX</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Bottazzi, Maria Elena" sort="Bottazzi, Maria Elena" uniqKey="Bottazzi M" first="Maria Elena" last="Bottazzi">Maria Elena Bottazzi</name>
<affiliation><nlm:aff id="aff1">Texas Children’s Hospital Center for Vaccine Development, Departments of Pediatrics and Molecular Virology & Microbiology, National School of Tropical Medicine, Baylor College of Medicine, Houston TX</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">Department of Biology, Baylor University, Waco TX</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Corry, David B" sort="Corry, David B" uniqKey="Corry D" first="David B." last="Corry">David B. Corry</name>
<affiliation><nlm:aff id="aff4">Biology of Inflammation Center, Departments of Medicine and Pathology & Immunology, and the Michael E. DeBakey Center for Translational Research in Inflammatory Diseases, Baylor College of Medicine, Houston TX</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Microbes and Infection</title>
<idno type="ISSN">1286-4579</idno>
<idno type="eISSN">1769-714X</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>Increasing evidence points to host Th17 inflammatory responses as contributing to the severe lung pathology and mortality of lower respiratory tract infections from coronaviruses. This includes host inflammatory and cytokine responses to COVID-19 caused by the SARS-2 coronavirus (SARS CoV2). From studies conducted in laboratory animals, there are additional concerns about immune enhancement and the role of potential host immunopathology resulting from experimental human COVID-19 vaccines. Here we summarize evidence suggesting there may be partial overlap between the underlying immunopathologic processes linked to both coronavirus infection and vaccination, and a role for Th17 in immune enhancement and eosinophilic pulmonary immunopathology. Such findings help explain the link between viral-vectored coronavirus vaccines and immune enhancement and its reduction through alum adjuvants. Additional research may also clarify links between COVID-19 pulmonary immunopathology and heart disease.</p>
</div>
</front>
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<pmc article-type="editorial"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Microbes Infect</journal-id>
<journal-id journal-id-type="iso-abbrev">Microbes Infect</journal-id>
<journal-title-group><journal-title>Microbes and Infection</journal-title>
</journal-title-group>
<issn pub-type="ppub">1286-4579</issn>
<issn pub-type="epub">1769-714X</issn>
<publisher><publisher-name>Published by Elsevier Masson SAS on behalf of Institut Pasteur.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmc">7162764</article-id>
<article-id pub-id-type="publisher-id">S1286-4579(20)30072-1</article-id>
<article-id pub-id-type="doi">10.1016/j.micinf.2020.04.005</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>The Potential Role of Th17 Immune Responses in Coronavirus Immunopathology and Vaccine-induced Immune Enhancement</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" id="au1"><name><surname>Hotez</surname>
<given-names>Peter J.</given-names>
</name>
<email>hotez@bcm.edu</email>
<xref rid="aff1" ref-type="aff">a</xref>
<xref rid="aff2" ref-type="aff">b</xref>
<xref rid="aff3" ref-type="aff">c</xref>
<xref rid="cor1" ref-type="corresp">∗</xref>
</contrib>
<contrib contrib-type="author" id="au2"><name><surname>Bottazzi</surname>
<given-names>Maria Elena</given-names>
</name>
<email>bottazzi@bcm.edu</email>
<xref rid="aff1" ref-type="aff">a</xref>
<xref rid="aff2" ref-type="aff">b</xref>
<xref rid="cor2" ref-type="corresp">∗∗</xref>
</contrib>
<contrib contrib-type="author" id="au3"><name><surname>Corry</surname>
<given-names>David B.</given-names>
</name>
<email>dcorry@bcm.edu</email>
<xref rid="aff4" ref-type="aff">d</xref>
<xref rid="cor3" ref-type="corresp">∗∗∗</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>a</label>
Texas Children’s Hospital Center for Vaccine Development, Departments of Pediatrics and Molecular Virology & Microbiology, National School of Tropical Medicine, Baylor College of Medicine, Houston TX</aff>
<aff id="aff2"><label>b</label>
Department of Biology, Baylor University, Waco TX</aff>
<aff id="aff3"><label>c</label>
Hagler Institute of Advanced Study at Texas A&M University, College Station TX</aff>
<aff id="aff4"><label>d</label>
Biology of Inflammation Center, Departments of Medicine and Pathology & Immunology, and the Michael E. DeBakey Center for Translational Research in Inflammatory Diseases, Baylor College of Medicine, Houston TX</aff>
<author-notes><corresp id="cor1"><label>∗</label>
Corresponding author. Texas Children’s Hospital Center for Vaccine Development, Departments of Pediatrics and Molecular Virology & Microbiology, National School of Tropical Medicine, Baylor College of Medicine, Houston TX., <email>hotez@bcm.edu</email>
</corresp>
<corresp id="cor2"><label>∗∗</label>
Corresponding author. Texas Children’s Hospital Center for Vaccine Development, Departments of Pediatrics and Molecular Virology & Microbiology, National School of Tropical Medicine, Baylor College of Medicine, Houston TX., <email>bottazzi@bcm.edu</email>
</corresp>
<corresp id="cor3"><label>∗∗∗</label>
Corresponding author. <email>dcorry@bcm.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release"><day>17</day>
<month>4</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>17</day>
<month>4</month>
<year>2020</year>
</pub-date>
<history><date date-type="received"><day>11</day>
<month>4</month>
<year>2020</year>
</date>
<date date-type="accepted"><day>14</day>
<month>4</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© 2020 Published by Elsevier Masson SAS on behalf of Institut Pasteur.</copyright-statement>
<copyright-year>2020</copyright-year>
<copyright-holder></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>Increasing evidence points to host Th17 inflammatory responses as contributing to the severe lung pathology and mortality of lower respiratory tract infections from coronaviruses. This includes host inflammatory and cytokine responses to COVID-19 caused by the SARS-2 coronavirus (SARS CoV2). From studies conducted in laboratory animals, there are additional concerns about immune enhancement and the role of potential host immunopathology resulting from experimental human COVID-19 vaccines. Here we summarize evidence suggesting there may be partial overlap between the underlying immunopathologic processes linked to both coronavirus infection and vaccination, and a role for Th17 in immune enhancement and eosinophilic pulmonary immunopathology. Such findings help explain the link between viral-vectored coronavirus vaccines and immune enhancement and its reduction through alum adjuvants. Additional research may also clarify links between COVID-19 pulmonary immunopathology and heart disease.</p>
</abstract>
</article-meta>
</front>
<body><sec id="sec1"><title>Introduction: COVID19 and Th17</title>
<p id="p0010">COVID19 caused by the SARS-2 coronavirus (SARS CoV2) has emerged as the third major lower respiratory tract coronavirus infection in the 21<sup>st</sup>
century, after severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS). The hallmark of each of these infections is a viral pneumonia accompanied by host inflammation leading to pulmonary edema and a syndrome that resembles acute respiratory distress syndrome (ARDS) (<xref rid="bib1" ref-type="bibr">1</xref>
). New information has highlighted a critical role for host Th17 inflammatory responses in the pathogenesis of COVID19 pneumonia and edema (<xref rid="bib2" ref-type="bibr">2</xref>
). This includes the release of key cytokines including IL-17 and GM-CSF (<xref rid="bib2" ref-type="bibr">2</xref>
), and other elements of exacerbating viral immnopathogenesis through downregulating Treg cells, promoting neutrophil migration, but simultaneously inducing Th2 responses (<xref rid="bib2" ref-type="bibr">2</xref>
, <xref rid="bib3" ref-type="bibr">3</xref>
). Importantly, IL-17 can also induce pulmonary eosinophilic responses and allergic disease, in part by promoting eosinophil production from the bone marrow and recruitment and extravasation into the lungs (<xref rid="bib4" ref-type="bibr">4</xref>
, <xref rid="bib5" ref-type="bibr">5</xref>
, <xref rid="bib6" ref-type="bibr">6</xref>
).</p>
<p id="p0015">Th17 cells differentiate in part through the actions of IL-6 (<xref rid="bib7" ref-type="bibr">7</xref>
), and IL-6 has been shown to have an important role in the lung pathology associated with SARS infection (<xref rid="bib8" ref-type="bibr">8</xref>
). There is additional evidence to suggest the SARS N protein is a potent inducer of IL-6 responses, and may mediate coronavirus lung pathology (<xref rid="bib9" ref-type="bibr">9</xref>
).</p>
<p id="p0020">Although confirmatory studies have yet to be performed, IL-6 induced by the presence of coronaviruses in the lung appears to promote in susceptible hosts Th17 responses that may lead to severe lung pathology that includes eosinophilia. These findings potentially provide a rational basis for evaluating anti-IL-6 monoclonal antibodies as new therapies for COVID19 (<xref rid="bib10" ref-type="bibr">10</xref>
). In addition, IL-8 production is also generated under Th17-polarizing conditions (<xref rid="bib11" ref-type="bibr">11</xref>
).</p>
</sec>
<sec id="sec2"><title>Immune Enhancement and Coronavirus Vaccines</title>
<p id="p0025">Beyond direct virus-induced pathology, immune enhancement associated with eosinophilic infiltration and immunopathology is a potential safety concern linked to first-generation vaccines to prevent severe acute respiratory syndrome (SARS) (<xref rid="bib12" ref-type="bibr">12</xref>
). A similar phenomenon may have derailed early efforts to develop an inactivated whole virus human vaccine against respiratory syncytial virus (RSV)(<xref rid="bib13" ref-type="bibr">13</xref>
).</p>
<p id="p0030">The mechanisms of immune enhancement from SARS vaccinations are still not well understood. In some cases, they have been postulated as a component of antibody-dependent enhancement (ADE) seen in several other human viral infections such as dengue fever (<xref rid="bib14" ref-type="bibr">14</xref>
), while others differentiate eosinophilic immunopathology from ADE. A key element of eosinophilic immunopathology is the appearance of inflammatory infiltrates comprised of mononuclear cells, especially eosinophils, in histopathologic sections of the lungs or livers of vaccinated experimental animals, following live virus challenge. The prominence of lung eosinophils has led some investigators to conclude that immune enhancement occurs through Th2-type immunity (<xref rid="bib15" ref-type="bibr">15</xref>
). Indeed, an unpublished and unreferenced scientific consensus document from the CEPI alliance (<ext-link ext-link-type="uri" xlink:href="http://CEPI.net" id="intref0010">CEPI.net</ext-link>
) has argued against the use of alum and other adjuvants that might promote Th2 responses.</p>
<p id="p0035">However, some of the published literature argues against the primary role of Th2 cells in directly promoting immune enhancement (<xref rid="bib16" ref-type="bibr">16</xref>
). For example, alum actually diminishes immune enhancement in laboratory animals vaccinated against the SARS coronavirus using either inactivated virus or virus-like particle vaccines (<xref rid="bib17" ref-type="bibr">17</xref>
, <xref rid="bib18" ref-type="bibr">18</xref>
). We have made a similar observation with a recombinant protein receptor binding domain vaccine (<xref rid="bib19" ref-type="bibr">19</xref>
).</p>
<p id="p0040">Moreover, immune enhancement occurs primarily following the use of virus-vectored vaccines, especially using vaccinia constructs expressing coronavirus antigens (<xref rid="bib20" ref-type="bibr">20</xref>
, <xref rid="bib21" ref-type="bibr">21</xref>
, <xref rid="bib22" ref-type="bibr">22</xref>
, <xref rid="bib23" ref-type="bibr">23</xref>
, <xref rid="bib24" ref-type="bibr">24</xref>
). In at least one study, mice exhibiting immune enhancement following SARS virus challenge were noted to upregulate their Th1 cytokines and downregulate their anti-inflammatory cytokines such as IL-10, despite exhibiting eosinophilic infiltrates (<xref rid="bib24" ref-type="bibr">24</xref>
), although another study concluded lack of adequate Th1 induction was responsible (<xref rid="bib25" ref-type="bibr">25</xref>
).</p>
<p id="p0045">Aside from mixed Th1 and Th2 responses, could Th17 responses also explain coronavirus-vaccine immune enhancement (<xref rid="fig1" ref-type="fig">Fig. 1</xref>
)? While vaccinia and other vectored vaccines induce substantial immune enhancement in both the lungs and liver of experimental animals (<xref rid="bib20" ref-type="bibr">20</xref>
, <xref rid="bib21" ref-type="bibr">21</xref>
, <xref rid="bib22" ref-type="bibr">22</xref>
, <xref rid="bib23" ref-type="bibr">23</xref>
, <xref rid="bib24" ref-type="bibr">24</xref>
), which in some cases have been linked to viral expression of the N protein (<xref rid="bib15" ref-type="bibr">15</xref>
), none of these studies specifically examined Th17 responses. However, it is notable that immune enhancement is linked to both IL-6 and IL-8 production (<xref rid="bib22" ref-type="bibr">22</xref>
, <xref rid="bib24" ref-type="bibr">24</xref>
), each a prominent cytokine associated with Th17, as well as many other types of immune responses.<fig id="fig1"><label>Fig. 1</label>
<caption><p>Mechanisms of eosinophilic immunopathology linked to viral-vectored coronavirus vaccines.</p>
</caption>
<alt-text id="alttext0010">Fig. 1</alt-text>
<graphic xlink:href="gr1_lrg"></graphic>
</fig>
</p>
<p id="p0050">As highlighted above, the presence of eosinophilic immunopathology can be linked to Th17 responses (<xref rid="bib4" ref-type="bibr">4</xref>
, <xref rid="bib5" ref-type="bibr">5</xref>
, <xref rid="bib6" ref-type="bibr">6</xref>
). While commonly thought of as the product of Th2 responses, numerous studies confirm that tissue eosinophilia can also fall under the control of Th17 responses. IL-17 and Th17 induction promote eosinophilic activation and infiltration (<xref rid="bib15" ref-type="bibr">15</xref>
), and eosinophil extravasation from the bone marrow into the lungs (<xref rid="bib4" ref-type="bibr">4</xref>
). Moreover, eosinophilia has been shown to be sustained by Th17 cells (<xref rid="bib26" ref-type="bibr">26</xref>
, <xref rid="bib27" ref-type="bibr">27</xref>
).</p>
</sec>
<sec id="sec3"><title>Heart Disease</title>
<p id="p0055">Despite these concerns, notwithstanding the fact that COVID-19 involves severe pulmonary dysfunction, there remains the unknown contribution of cytokine storm, enhanced Th17 responses, or pulmonary eosinophilia to end-stage mortality (<xref rid="bib28" ref-type="bibr">28</xref>
). Indeed, evidence increasingly suggests that severe morbidity and mortality as seen during COVID-19 may have far more to do with heart dysfunction than pulmonary failure (<xref rid="bib29" ref-type="bibr">29</xref>
, <xref rid="bib30" ref-type="bibr">30</xref>
). Severe heart failure could in fact be the main cause of respiratory and other organ system failure in severe, life-threatening disease. In this respect, heart failure from myocarditis and cardiomyopathy has also been linked to IL-17 producing T cells and IL-17-promoting cytokines (<xref rid="bib31" ref-type="bibr">31</xref>
).</p>
</sec>
<sec id="sec4"><title>Concluding comments</title>
<p id="p0060">More research is needed into the underlying mechanisms of eosinophilic immunopathology associated with coronavirus vaccines and the relevance of this observation to clinical outcomes. However, the potential role of Th17 responses has a number of implications in terms of the production and clinical development of COVID-19 vaccines. These include adjuvant selection and vaccine dose and route. Implicating Th17 also can also inform on the selection of the safest vaccine strategy among the virus-vectored and nucleic acid-based platforms, as well as recombinant protein subunit vaccines. Such decisions will be validated in the coming months as several vaccines for COVID-19 enter the clinical pipeline and undergo extensive evaluation for both efficacy and safety. In addition to the possibility of Th17 and eosinophil-dependent immunopathology, future COVID-19 vaccine studies might focus on the cardioprotective effects of vaccination.</p>
</sec>
</body>
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