Impaired Cytotoxic CD8+ T Cell Response in Elderly COVID-19 Patients.
Identifieur interne : 000160 ( Main/Curation ); précédent : 000159; suivant : 000161Impaired Cytotoxic CD8+ T Cell Response in Elderly COVID-19 Patients.
Auteurs : Jaana Westmeier [Allemagne] ; Krystallenia Paniskaki [Allemagne] ; Zehra Karaköse [Allemagne] ; Tanja Werner [Allemagne] ; Kathrin Sutter [Allemagne, République populaire de Chine] ; Sebastian Dolff [Allemagne] ; Marvin Overbeck [Allemagne] ; Andreas Limmer [Allemagne] ; Jia Liu [République populaire de Chine] ; Xin Zheng [République populaire de Chine] ; Thorsten Brenner [Allemagne] ; Marc M. Berger [Allemagne] ; Oliver Witzke [Allemagne] ; Mirko Trilling [Allemagne, République populaire de Chine] ; Mengji Lu [Allemagne, République populaire de Chine] ; Dongliang Yang [République populaire de Chine] ; Nina Babel [Allemagne] ; Timm Westhoff [Allemagne] ; Ulf Dittmer [Allemagne, République populaire de Chine] ; Gennadiy Zelinskyy [Allemagne, République populaire de Chine]Source :
- mBio [ 2150-7511 ] ; 2020.
Descripteurs français
- KwdFr :
- Adulte d'âge moyen (MeSH), Antigènes CD (métabolisme), Betacoronavirus (pathogénicité), Cytotoxines (métabolisme), Femelle (MeSH), Humains (MeSH), Immunité cellulaire (MeSH), Infections à coronavirus (immunologie), Lymphocytes T CD4+ (anatomopathologie), Lymphocytes T CD4+ (immunologie), Lymphocytes T CD8+ (anatomopathologie), Lymphocytes T CD8+ (immunologie), Lymphocytes T cytotoxiques (anatomopathologie), Lymphocytes T cytotoxiques (immunologie), Mâle (MeSH), Pandémies (MeSH), Pneumopathie virale (immunologie), Sous-populations de lymphocytes T (anatomopathologie), Sous-populations de lymphocytes T (immunologie), Sujet âgé de 80 ans ou plus (MeSH).
- MESH :
- anatomopathologie : Lymphocytes T CD4+, Lymphocytes T CD8+, Lymphocytes T cytotoxiques, Sous-populations de lymphocytes T.
- immunologie : Infections à coronavirus, Lymphocytes T CD4+, Lymphocytes T CD8+, Lymphocytes T cytotoxiques, Pneumopathie virale, Sous-populations de lymphocytes T.
- métabolisme : Antigènes CD, Cytotoxines.
- pathogénicité : Betacoronavirus.
- Adulte d'âge moyen, Femelle, Humains, Immunité cellulaire, Mâle, Pandémies, Sujet âgé de 80 ans ou plus.
English descriptors
- KwdEn :
- Aged, 80 and over (MeSH), Antigens, CD (metabolism), Betacoronavirus (pathogenicity), CD4-Positive T-Lymphocytes (immunology), CD4-Positive T-Lymphocytes (pathology), CD8-Positive T-Lymphocytes (immunology), CD8-Positive T-Lymphocytes (pathology), Coronavirus Infections (immunology), Cytotoxins (metabolism), Female (MeSH), Humans (MeSH), Immunity, Cellular (MeSH), Male (MeSH), Middle Aged (MeSH), Pandemics (MeSH), Pneumonia, Viral (immunology), T-Lymphocyte Subsets (immunology), T-Lymphocyte Subsets (pathology), T-Lymphocytes, Cytotoxic (immunology), T-Lymphocytes, Cytotoxic (pathology).
- MESH :
- chemical , metabolism : Antigens, CD, Cytotoxins.
- immunology : CD4-Positive T-Lymphocytes, CD8-Positive T-Lymphocytes, Coronavirus Infections, Pneumonia, Viral, T-Lymphocyte Subsets, T-Lymphocytes, Cytotoxic.
- pathogenicity : Betacoronavirus.
- pathology : CD4-Positive T-Lymphocytes, CD8-Positive T-Lymphocytes, T-Lymphocyte Subsets, T-Lymphocytes, Cytotoxic.
- Aged, 80 and over, Female, Humans, Immunity, Cellular, Male, Middle Aged, Pandemics.
Abstract
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection induces a T cell response that most likely contributes to virus control in COVID-19 patients but may also induce immunopathology. Until now, the cytotoxic T cell response has not been very well characterized in COVID-19 patients. Here, we analyzed the differentiation and cytotoxic profile of T cells in 30 cases of mild COVID-19 during acute infection. SARS-CoV-2 infection induced a cytotoxic response of CD8+ T cells, but not CD4+ T cells, characterized by the simultaneous production of granzyme A and B as well as perforin within different effector CD8+ T cell subsets. PD-1-expressing CD8+ T cells also produced cytotoxic molecules during acute infection, indicating that they were not functionally exhausted. However, in COVID-19 patients over the age of 80 years, the cytotoxic T cell potential was diminished, especially in effector memory and terminally differentiated effector CD8+ cells, showing that elderly patients have impaired cellular immunity against SARS-CoV-2. Our data provide valuable information about T cell responses in COVID-19 patients that may also have important implications for vaccine development.IMPORTANCE Cytotoxic T cells are responsible for the elimination of infected cells and are key players in the control of viruses. CD8+ T cells with an effector phenotype express cytotoxic molecules and are able to perform target cell killing. COVID-19 patients with a mild disease course were analyzed for the differentiation status and cytotoxic profile of CD8+ T cells. SARS-CoV-2 infection induced a vigorous cytotoxic CD8+ T cell response. However, this cytotoxic profile of T cells was not detected in COVID-19 patients over the age of 80 years. Thus, the absence of a cytotoxic response in elderly patients might be a possible reason for the more frequent severity of COVID-19 in this age group than in younger patients.
DOI: 10.1128/mBio.02243-20
PubMed: 32948688
PubMed Central: PMC7502863
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Berger</name><affiliation wicri:level="1"><nlm:affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Witzke, Oliver" sort="Witzke, Oliver" uniqKey="Witzke O" first="Oliver" last="Witzke">Oliver Witzke</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, West German Centre of Infectious Diseases, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Infectious Diseases, West German Centre of Infectious Diseases, University Hospital Essen, University Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Trilling, Mirko" 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Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Yang, Dongliang" sort="Yang, Dongliang" uniqKey="Yang D" first="Dongliang" last="Yang">Dongliang Yang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Babel, Nina" sort="Babel, Nina" uniqKey="Babel N" first="Nina" last="Babel">Nina Babel</name><affiliation wicri:level="1"><nlm:affiliation>Center for Translational Medicine, Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr-University Bochum, Herne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Center for Translational Medicine, Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr-University Bochum, Herne</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Berlin Institute of Health, Berlin-Brandenburg Center for Regenerative Therapies, Berlin, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Berlin Institute of Health, Berlin-Brandenburg Center for Regenerative Therapies, Berlin</wicri:regionArea></affiliation></author><author><name sortKey="Westhoff, Timm" sort="Westhoff, Timm" uniqKey="Westhoff T" first="Timm" last="Westhoff">Timm Westhoff</name><affiliation wicri:level="1"><nlm:affiliation>Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr University of Bochum, Bochum, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr University of Bochum, Bochum</wicri:regionArea></affiliation></author><author><name sortKey="Dittmer, Ulf" sort="Dittmer, Ulf" uniqKey="Dittmer U" first="Ulf" last="Dittmer">Ulf Dittmer</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany ulf.dittmer@uni-due.de gennadiy.zelinskyy@uni-due.de.</nlm:affiliation><country wicri:rule="url">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Zelinskyy, Gennadiy" sort="Zelinskyy, Gennadiy" uniqKey="Zelinskyy G" first="Gennadiy" last="Zelinskyy">Gennadiy Zelinskyy</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany ulf.dittmer@uni-due.de gennadiy.zelinskyy@uni-due.de.</nlm:affiliation><country wicri:rule="url">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32948688</idno><idno type="pmid">32948688</idno><idno type="doi">10.1128/mBio.02243-20</idno><idno type="pmc">PMC7502863</idno><idno type="wicri:Area/Main/Corpus">000160</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000160</idno><idno type="wicri:Area/Main/Curation">000160</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000160</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Impaired Cytotoxic CD8<sup>+</sup> T Cell Response in Elderly COVID-19 Patients.</title><author><name sortKey="Westmeier, Jaana" sort="Westmeier, Jaana" uniqKey="Westmeier J" first="Jaana" last="Westmeier">Jaana Westmeier</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Paniskaki, Krystallenia" sort="Paniskaki, Krystallenia" uniqKey="Paniskaki K" first="Krystallenia" last="Paniskaki">Krystallenia Paniskaki</name><affiliation wicri:level="1"><nlm:affiliation>Center for Translational Medicine, Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr-University Bochum, Herne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Center for Translational Medicine, Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr-University Bochum, Herne</wicri:regionArea></affiliation></author><author><name sortKey="Karakose, Zehra" sort="Karakose, Zehra" uniqKey="Karakose Z" first="Zehra" last="Karaköse">Zehra Karaköse</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Werner, Tanja" sort="Werner, Tanja" uniqKey="Werner T" first="Tanja" last="Werner">Tanja Werner</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Sutter, Kathrin" sort="Sutter, Kathrin" uniqKey="Sutter K" first="Kathrin" last="Sutter">Kathrin Sutter</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Dolff, Sebastian" sort="Dolff, Sebastian" uniqKey="Dolff S" first="Sebastian" last="Dolff">Sebastian Dolff</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, West German Centre of Infectious Diseases, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Infectious Diseases, West German Centre of Infectious Diseases, University Hospital Essen, University Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Overbeck, Marvin" sort="Overbeck, Marvin" uniqKey="Overbeck M" first="Marvin" last="Overbeck">Marvin Overbeck</name><affiliation wicri:level="1"><nlm:affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Limmer, Andreas" sort="Limmer, Andreas" uniqKey="Limmer A" first="Andreas" last="Limmer">Andreas Limmer</name><affiliation wicri:level="1"><nlm:affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Liu, Jia" sort="Liu, Jia" uniqKey="Liu J" first="Jia" last="Liu">Jia Liu</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Zheng, Xin" sort="Zheng, Xin" uniqKey="Zheng X" first="Xin" last="Zheng">Xin Zheng</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Brenner, Thorsten" sort="Brenner, Thorsten" uniqKey="Brenner T" first="Thorsten" last="Brenner">Thorsten Brenner</name><affiliation wicri:level="1"><nlm:affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Berger, Marc M" sort="Berger, Marc M" uniqKey="Berger M" first="Marc M" last="Berger">Marc M. Berger</name><affiliation wicri:level="1"><nlm:affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Witzke, Oliver" sort="Witzke, Oliver" uniqKey="Witzke O" first="Oliver" last="Witzke">Oliver Witzke</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, West German Centre of Infectious Diseases, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Infectious Diseases, West German Centre of Infectious Diseases, University Hospital Essen, University Duisburg-Essen, Essen</wicri:regionArea></affiliation></author><author><name sortKey="Trilling, Mirko" sort="Trilling, Mirko" uniqKey="Trilling M" first="Mirko" last="Trilling">Mirko Trilling</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Lu, Mengji" sort="Lu, Mengji" uniqKey="Lu M" first="Mengji" last="Lu">Mengji Lu</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Yang, Dongliang" sort="Yang, Dongliang" uniqKey="Yang D" first="Dongliang" last="Yang">Dongliang Yang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Babel, Nina" sort="Babel, Nina" uniqKey="Babel N" first="Nina" last="Babel">Nina Babel</name><affiliation wicri:level="1"><nlm:affiliation>Center for Translational Medicine, Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr-University Bochum, Herne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Center for Translational Medicine, Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr-University Bochum, Herne</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Berlin Institute of Health, Berlin-Brandenburg Center for Regenerative Therapies, Berlin, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Berlin Institute of Health, Berlin-Brandenburg Center for Regenerative Therapies, Berlin</wicri:regionArea></affiliation></author><author><name sortKey="Westhoff, Timm" sort="Westhoff, Timm" uniqKey="Westhoff T" first="Timm" last="Westhoff">Timm Westhoff</name><affiliation wicri:level="1"><nlm:affiliation>Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr University of Bochum, Bochum, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr University of Bochum, Bochum</wicri:regionArea></affiliation></author><author><name sortKey="Dittmer, Ulf" sort="Dittmer, Ulf" uniqKey="Dittmer U" first="Ulf" last="Dittmer">Ulf Dittmer</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany ulf.dittmer@uni-due.de gennadiy.zelinskyy@uni-due.de.</nlm:affiliation><country wicri:rule="url">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author><author><name sortKey="Zelinskyy, Gennadiy" sort="Zelinskyy, Gennadiy" uniqKey="Zelinskyy G" first="Gennadiy" last="Zelinskyy">Gennadiy Zelinskyy</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany ulf.dittmer@uni-due.de gennadiy.zelinskyy@uni-due.de.</nlm:affiliation><country wicri:rule="url">Allemagne</country><wicri:regionArea>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Joint International Laboratory of Infection and Immunity, HUST, Wuhan</wicri:regionArea></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Aged, 80 and over (MeSH)</term><term>Antigens, CD (metabolism)</term><term>Betacoronavirus (pathogenicity)</term><term>CD4-Positive T-Lymphocytes (immunology)</term><term>CD4-Positive T-Lymphocytes (pathology)</term><term>CD8-Positive T-Lymphocytes (immunology)</term><term>CD8-Positive T-Lymphocytes (pathology)</term><term>Coronavirus Infections (immunology)</term><term>Cytotoxins (metabolism)</term><term>Female (MeSH)</term><term>Humans (MeSH)</term><term>Immunity, Cellular (MeSH)</term><term>Male (MeSH)</term><term>Middle Aged (MeSH)</term><term>Pandemics (MeSH)</term><term>Pneumonia, Viral (immunology)</term><term>T-Lymphocyte Subsets (immunology)</term><term>T-Lymphocyte Subsets (pathology)</term><term>T-Lymphocytes, Cytotoxic (immunology)</term><term>T-Lymphocytes, Cytotoxic (pathology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Adulte d'âge moyen (MeSH)</term><term>Antigènes CD (métabolisme)</term><term>Betacoronavirus (pathogénicité)</term><term>Cytotoxines (métabolisme)</term><term>Femelle (MeSH)</term><term>Humains (MeSH)</term><term>Immunité cellulaire (MeSH)</term><term>Infections à coronavirus (immunologie)</term><term>Lymphocytes T CD4+ (anatomopathologie)</term><term>Lymphocytes T CD4+ (immunologie)</term><term>Lymphocytes T CD8+ (anatomopathologie)</term><term>Lymphocytes T CD8+ (immunologie)</term><term>Lymphocytes T cytotoxiques (anatomopathologie)</term><term>Lymphocytes T cytotoxiques (immunologie)</term><term>Mâle (MeSH)</term><term>Pandémies (MeSH)</term><term>Pneumopathie virale (immunologie)</term><term>Sous-populations de lymphocytes T (anatomopathologie)</term><term>Sous-populations de lymphocytes T (immunologie)</term><term>Sujet âgé de 80 ans ou plus (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Antigens, CD</term><term>Cytotoxins</term></keywords><keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr"><term>Lymphocytes T CD4+</term><term>Lymphocytes T CD8+</term><term>Lymphocytes T cytotoxiques</term><term>Sous-populations de lymphocytes T</term></keywords><keywords scheme="MESH" qualifier="immunologie" xml:lang="fr"><term>Infections à coronavirus</term><term>Lymphocytes T CD4+</term><term>Lymphocytes T CD8+</term><term>Lymphocytes T cytotoxiques</term><term>Pneumopathie virale</term><term>Sous-populations de lymphocytes T</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>CD4-Positive T-Lymphocytes</term><term>CD8-Positive T-Lymphocytes</term><term>Coronavirus Infections</term><term>Pneumonia, Viral</term><term>T-Lymphocyte Subsets</term><term>T-Lymphocytes, Cytotoxic</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Antigènes CD</term><term>Cytotoxines</term></keywords><keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en"><term>Betacoronavirus</term></keywords><keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr"><term>Betacoronavirus</term></keywords><keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>CD4-Positive T-Lymphocytes</term><term>CD8-Positive T-Lymphocytes</term><term>T-Lymphocyte Subsets</term><term>T-Lymphocytes, Cytotoxic</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Aged, 80 and over</term><term>Female</term><term>Humans</term><term>Immunity, Cellular</term><term>Male</term><term>Middle Aged</term><term>Pandemics</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Adulte d'âge moyen</term><term>Femelle</term><term>Humains</term><term>Immunité cellulaire</term><term>Mâle</term><term>Pandémies</term><term>Sujet âgé de 80 ans ou plus</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection induces a T cell response that most likely contributes to virus control in COVID-19 patients but may also induce immunopathology. Until now, the cytotoxic T cell response has not been very well characterized in COVID-19 patients. Here, we analyzed the differentiation and cytotoxic profile of T cells in 30 cases of mild COVID-19 during acute infection. SARS-CoV-2 infection induced a cytotoxic response of CD8<sup>+</sup> T cells, but not CD4<sup>+</sup> T cells, characterized by the simultaneous production of granzyme A and B as well as perforin within different effector CD8<sup>+</sup> T cell subsets. PD-1-expressing CD8<sup>+</sup> T cells also produced cytotoxic molecules during acute infection, indicating that they were not functionally exhausted. However, in COVID-19 patients over the age of 80 years, the cytotoxic T cell potential was diminished, especially in effector memory and terminally differentiated effector CD8<sup>+</sup> cells, showing that elderly patients have impaired cellular immunity against SARS-CoV-2. Our data provide valuable information about T cell responses in COVID-19 patients that may also have important implications for vaccine development.<b>IMPORTANCE</b> Cytotoxic T cells are responsible for the elimination of infected cells and are key players in the control of viruses. CD8<sup>+</sup> T cells with an effector phenotype express cytotoxic molecules and are able to perform target cell killing. COVID-19 patients with a mild disease course were analyzed for the differentiation status and cytotoxic profile of CD8<sup>+</sup> T cells. SARS-CoV-2 infection induced a vigorous cytotoxic CD8<sup>+</sup> T cell response. However, this cytotoxic profile of T cells was not detected in COVID-19 patients over the age of 80 years. Thus, the absence of a cytotoxic response in elderly patients might be a possible reason for the more frequent severity of COVID-19 in this age group than in younger patients.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">32948688</PMID><DateCompleted><Year>2020</Year><Month>10</Month><Day>05</Day></DateCompleted><DateRevised><Year>2020</Year><Month>10</Month><Day>05</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2150-7511</ISSN><JournalIssue CitedMedium="Internet"><Volume>11</Volume><Issue>5</Issue><PubDate><Year>2020</Year><Month>09</Month><Day>18</Day></PubDate></JournalIssue><Title>mBio</Title><ISOAbbreviation>mBio</ISOAbbreviation></Journal><ArticleTitle>Impaired Cytotoxic CD8<sup>+</sup> T Cell Response in Elderly COVID-19 Patients.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e02243-20</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.02243-20</ELocationID><Abstract><AbstractText>Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection induces a T cell response that most likely contributes to virus control in COVID-19 patients but may also induce immunopathology. Until now, the cytotoxic T cell response has not been very well characterized in COVID-19 patients. Here, we analyzed the differentiation and cytotoxic profile of T cells in 30 cases of mild COVID-19 during acute infection. SARS-CoV-2 infection induced a cytotoxic response of CD8<sup>+</sup> T cells, but not CD4<sup>+</sup> T cells, characterized by the simultaneous production of granzyme A and B as well as perforin within different effector CD8<sup>+</sup> T cell subsets. PD-1-expressing CD8<sup>+</sup> T cells also produced cytotoxic molecules during acute infection, indicating that they were not functionally exhausted. However, in COVID-19 patients over the age of 80 years, the cytotoxic T cell potential was diminished, especially in effector memory and terminally differentiated effector CD8<sup>+</sup> cells, showing that elderly patients have impaired cellular immunity against SARS-CoV-2. Our data provide valuable information about T cell responses in COVID-19 patients that may also have important implications for vaccine development.<b>IMPORTANCE</b> Cytotoxic T cells are responsible for the elimination of infected cells and are key players in the control of viruses. CD8<sup>+</sup> T cells with an effector phenotype express cytotoxic molecules and are able to perform target cell killing. COVID-19 patients with a mild disease course were analyzed for the differentiation status and cytotoxic profile of CD8<sup>+</sup> T cells. SARS-CoV-2 infection induced a vigorous cytotoxic CD8<sup>+</sup> T cell response. However, this cytotoxic profile of T cells was not detected in COVID-19 patients over the age of 80 years. Thus, the absence of a cytotoxic response in elderly patients might be a possible reason for the more frequent severity of COVID-19 in this age group than in younger patients.</AbstractText><CopyrightInformation>Copyright © 2020 Westmeier et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Westmeier</LastName><ForeName>Jaana</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Paniskaki</LastName><ForeName>Krystallenia</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Center for Translational Medicine, Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr-University Bochum, Herne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Karaköse</LastName><ForeName>Zehra</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Werner</LastName><ForeName>Tanja</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sutter</LastName><ForeName>Kathrin</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dolff</LastName><ForeName>Sebastian</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, West German Centre of Infectious Diseases, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Overbeck</LastName><ForeName>Marvin</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Limmer</LastName><ForeName>Andreas</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Jia</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zheng</LastName><ForeName>Xin</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brenner</LastName><ForeName>Thorsten</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Berger</LastName><ForeName>Marc M</ForeName><Initials>MM</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Witzke</LastName><ForeName>Oliver</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, West German Centre of Infectious Diseases, University Hospital Essen, University Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Trilling</LastName><ForeName>Mirko</ForeName><Initials>M</Initials><Identifier Source="ORCID">0000-0003-3659-3541</Identifier><AffiliationInfo><Affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lu</LastName><ForeName>Mengji</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Dongliang</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Union Hospital of Tonji Medical College, Huazhong University of Science and Technology, Wuhan, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Babel</LastName><ForeName>Nina</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Center for Translational Medicine, Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr-University Bochum, Herne, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Berlin Institute of Health, Berlin-Brandenburg Center for Regenerative Therapies, Berlin, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Westhoff</LastName><ForeName>Timm</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Medical Department I, Marien Hospital Herne, University Hospital of the Ruhr University of Bochum, Bochum, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dittmer</LastName><ForeName>Ulf</ForeName><Initials>U</Initials><AffiliationInfo><Affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany ulf.dittmer@uni-due.de gennadiy.zelinskyy@uni-due.de.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zelinskyy</LastName><ForeName>Gennadiy</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Institute for Virology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany ulf.dittmer@uni-due.de gennadiy.zelinskyy@uni-due.de.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Joint International Laboratory of Infection and Immunity, HUST, Wuhan, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D003160">Comparative Study</PublicationType><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>18</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>mBio</MedlineTA><NlmUniqueID>101519231</NlmUniqueID></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D015703">Antigens, CD</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D003603">Cytotoxins</NameOfSubstance></Chemical></ChemicalList><SupplMeshList><SupplMeshName Type="Disease" UI="C000657245">COVID-19</SupplMeshName><SupplMeshName Type="Organism" UI="C000656484">severe acute respiratory syndrome coronavirus 2</SupplMeshName></SupplMeshList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000369" MajorTopicYN="N">Aged, 80 and over</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015703" MajorTopicYN="N">Antigens, CD</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000073640" MajorTopicYN="N">Betacoronavirus</DescriptorName><QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D015496" MajorTopicYN="N">CD4-Positive T-Lymphocytes</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018414" MajorTopicYN="N">CD8-Positive T-Lymphocytes</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000473" MajorTopicYN="Y">pathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018352" MajorTopicYN="N">Coronavirus Infections</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D003603" MajorTopicYN="N">Cytotoxins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D007111" MajorTopicYN="N">Immunity, Cellular</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008297" MajorTopicYN="N">Male</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008875" MajorTopicYN="N">Middle Aged</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D058873" MajorTopicYN="N">Pandemics</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011024" MajorTopicYN="N">Pneumonia, Viral</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D016176" MajorTopicYN="N">T-Lymphocyte Subsets</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013602" MajorTopicYN="N">T-Lymphocytes, Cytotoxic</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000473" MajorTopicYN="Y">pathology</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">CD4+
</Keyword><Keyword MajorTopicYN="Y">CD8+
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