Cross-reactive CD4 + T cells enhance SARS-CoV-2 immune responses upon infection and vaccination
There is mounting evidence that immunological memory after infection with seasonal human coronaviruses (hCoVs) contributes to cross-protection against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Loyal et al . identified a universal immunodominant coronavirus peptide found within th...
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| Published in | Science (American Association for the Advancement of Science) Vol. 374; no. 6564; p. eabh1823 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
08.10.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | There is mounting evidence that immunological memory after infection with seasonal human coronaviruses (hCoVs) contributes to cross-protection against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Loyal
et al
. identified a universal immunodominant coronavirus peptide found within the fusion peptide domain of coronavirus spike protein. This peptide is recognized by CD4
+
T cells in 20% of unexposed individuals, more than 50% of SARS-CoV-2 convalescents, and 97% of subjects treated with the Pfizer–BioNTech COVID-19 vaccine. Although ubiquitous, these coronavirus-reactive T cells decreased with age, which may explain in part the increased susceptibility of elderly people to COVID-19. —STS
Preexisting spike–cross-reactive T cells correlate with higher neutralizing anti-spike protein antibodies in SARS-CoV-2 infection and vaccination
The functional relevance of preexisting cross-immunity to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a subject of intense debate. Here, we show that human endemic coronavirus (HCoV)–reactive and SARS-CoV-2–cross-reactive CD4
+
T cells are ubiquitous but decrease with age. We identified a universal immunodominant coronavirus-specific spike peptide (S816-830) and demonstrate that preexisting spike- and S816-830–reactive T cells were recruited into immune responses to SARS-CoV-2 infection and their frequency correlated with anti–SARS-CoV-2-S1-IgG antibodies. Spike–cross-reactive T cells were also activated after primary BNT162b2 COVID-19 messenger RNA vaccination and displayed kinetics similar to those of secondary immune responses. Our results highlight the functional contribution of preexisting spike–cross-reactive T cells in SARS-CoV-2 infection and vaccination. Cross-reactive immunity may account for the unexpectedly rapid induction of immunity after primary SARS-CoV-2 immunization and the high rate of asymptomatic or mild COVID-19 disease courses. |
|---|---|
| AbstractList | The functional relevance of preexisting cross-immunity to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a subject of intense debate. Here, we show that human endemic coronavirus (HCoV)–reactive and SARS-CoV-2–cross-reactive CD4
T cells are ubiquitous but decrease with age. We identified a universal immunodominant coronavirus-specific spike peptide (S816-830) and demonstrate that preexisting spike- and S816-830–reactive T cells were recruited into immune responses to SARS-CoV-2 infection and their frequency correlated with anti–SARS-CoV-2-S1-IgG antibodies. Spike–cross-reactive T cells were also activated after primary BNT162b2 COVID-19 messenger RNA vaccination and displayed kinetics similar to those of secondary immune responses. Our results highlight the functional contribution of preexisting spike–cross-reactive T cells in SARS-CoV-2 infection and vaccination. Cross-reactive immunity may account for the unexpectedly rapid induction of immunity after primary SARS-CoV-2 immunization and the high rate of asymptomatic or mild COVID-19 disease courses. Cross-reactive T cells aid in the fightThere is mounting evidence that immunological memory after infection with seasonal human coronaviruses (hCoVs) contributes to cross-protection against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Loyal et al. identified a universal immunodominant coronavirus peptide found within the fusion peptide domain of coronavirus spike protein. This peptide is recognized by CD4+ T cells in 20% of unexposed individuals, more than 50% of SARS-CoV-2 convalescents, and 97% of subjects treated with the Pfizer–BioNTech COVID-19 vaccine. Although ubiquitous, these coronavirus-reactive T cells decreased with age, which may explain in part the increased susceptibility of elderly people to COVID-19. —STSINTRODUCTIONThe clinical manifestations of COVID-19 vary from asymptomatic infection to respiratory failure. Severe disease courses are primarily associated with advanced age, immune dysfunctions, and comorbidities. Initially, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) was thought to encounter an immunologically unprotected population. However, SARS-CoV-2 has significant homologies with endemic seasonal cold coronaviruses (HCoVs), and recent HCoV infection is associated with a less severe course of COVID-19, suggesting a protective role of cross-reactive immunity.RATIONALEThe preexistence of SARS-CoV-2–cross-reactive CD4+ T cells in unexposed individuals has been repeatedly demonstrated, but their contribution to host responses is an active area of investigation. Here, we investigated the functional role of preexisting SARS-CoV-2–cross-reactive and HCoV-reactive CD4+ T cells with high resolution.RESULTSWe demonstrate broad CD4+ T cell cross-reactivity in unexposed individuals, with the spike glycoprotein serving as one of the immunodominant targets. Although the N-terminal part of spike (covered by the S-I peptide pool) did not elicit cross-reactive T cell responses, the more HCoV-homologous C-terminal section (covered by the S-II peptide pool) induced T cell responses in unexposed donors. We identified a universal immunodominant coronavirus peptide located within the fusion peptide domain of spike (S816-830) recognized by CD4+ T cells in 20% of unexposed individuals, 50 to 60% of SARS-CoV-2 convalescents, and 97% of BNT162b2-vaccinated individuals. S816-830– and spike–cross-reactive T cells were recruited in immune responses to SARS-CoV-2 infection and BNT162b2 COVID-19 mRNA vaccination. S816-830-reactive T cells initially contributed up to 100% of the S-II–reactive CD4+ T cells but their proportion decreased during the course of the S-II–specific immune response. Upon primary vaccination, cross-reactive cellular and humoral immunity exhibited kinetics typical for secondary immune responses. The frequencies of preexisting cross-reactive T cells correlated positively with functional avidity of the T cell receptor, as well as with the induction and stabilization of anti–SARS-CoV-2-S1-IgG and neutralizing antibodies. Although HCoV-responsive T cells are ubiquitous, their frequencies and the frequencies of SARS-CoV-2–cross-reactive CD4+ T cells decreased with age, consistent with an increased vulnerability of the elderly to severe COVID-19 disease.CONCLUSIONPreexisting cross-reactive CD4+ T cells enhance immune responses in SARS-CoV-2 infection and BNT162b2 vaccination. Because these cells are greatly diminished in the elderly, our results suggest that their decrease may contribute to the increased susceptibility of this population to severe COVID-19. Preexisting cross-reactive immunity may be responsible for the unexpectedly rapid induction of protective immunity after primary SARS-CoV-2 immunization and the high rate of asymptomatic and mild COVID-19 disease courses.The functional relevance of preexisting cross-immunity to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a subject of intense debate. Here, we show that human endemic coronavirus (HCoV)–reactive and SARS-CoV-2–cross-reactive CD4+ T cells are ubiquitous but decrease with age. We identified a universal immunodominant coronavirus-specific spike peptide (S816-830) and demonstrate that preexisting spike- and S816-830–reactive T cells were recruited into immune responses to SARS-CoV-2 infection and their frequency correlated with anti–SARS-CoV-2-S1-IgG antibodies. Spike–cross-reactive T cells were also activated after primary BNT162b2 COVID-19 messenger RNA vaccination and displayed kinetics similar to those of secondary immune responses. Our results highlight the functional contribution of preexisting spike–cross-reactive T cells in SARS-CoV-2 infection and vaccination. Cross-reactive immunity may account for the unexpectedly rapid induction of immunity after primary SARS-CoV-2 immunization and the high rate of asymptomatic or mild COVID-19 disease courses. The functional relevance of preexisting cross-immunity to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a subject of intense debate. Here, we show that human endemic coronavirus (HCoV)–reactive and SARS-CoV-2–cross-reactive CD4+ T cells are ubiquitous but decrease with age. We identified a universal immunodominant coronavirus-specific spike peptide (S816-830) and demonstrate that preexisting spike- and S816-830–reactive T cells were recruited into immune responses to SARS-CoV-2 infection and their frequency correlated with anti–SARS-CoV-2-S1-IgG antibodies. Spike–cross-reactive T cells were also activated after primary BNT162b2 COVID-19 messenger RNA vaccination and displayed kinetics similar to those of secondary immune responses. Our results highlight the functional contribution of preexisting spike–cross-reactive T cells in SARS-CoV-2 infection and vaccination. Cross-reactive immunity may account for the unexpectedly rapid induction of immunity after primary SARS-CoV-2 immunization and the high rate of asymptomatic or mild COVID-19 disease courses.The functional relevance of preexisting cross-immunity to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a subject of intense debate. Here, we show that human endemic coronavirus (HCoV)–reactive and SARS-CoV-2–cross-reactive CD4+ T cells are ubiquitous but decrease with age. We identified a universal immunodominant coronavirus-specific spike peptide (S816-830) and demonstrate that preexisting spike- and S816-830–reactive T cells were recruited into immune responses to SARS-CoV-2 infection and their frequency correlated with anti–SARS-CoV-2-S1-IgG antibodies. Spike–cross-reactive T cells were also activated after primary BNT162b2 COVID-19 messenger RNA vaccination and displayed kinetics similar to those of secondary immune responses. Our results highlight the functional contribution of preexisting spike–cross-reactive T cells in SARS-CoV-2 infection and vaccination. Cross-reactive immunity may account for the unexpectedly rapid induction of immunity after primary SARS-CoV-2 immunization and the high rate of asymptomatic or mild COVID-19 disease courses. There is mounting evidence that immunological memory after infection with seasonal human coronaviruses (hCoVs) contributes to cross-protection against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Loyal et al . identified a universal immunodominant coronavirus peptide found within the fusion peptide domain of coronavirus spike protein. This peptide is recognized by CD4 + T cells in 20% of unexposed individuals, more than 50% of SARS-CoV-2 convalescents, and 97% of subjects treated with the Pfizer–BioNTech COVID-19 vaccine. Although ubiquitous, these coronavirus-reactive T cells decreased with age, which may explain in part the increased susceptibility of elderly people to COVID-19. —STS Preexisting spike–cross-reactive T cells correlate with higher neutralizing anti-spike protein antibodies in SARS-CoV-2 infection and vaccination The functional relevance of preexisting cross-immunity to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a subject of intense debate. Here, we show that human endemic coronavirus (HCoV)–reactive and SARS-CoV-2–cross-reactive CD4 + T cells are ubiquitous but decrease with age. We identified a universal immunodominant coronavirus-specific spike peptide (S816-830) and demonstrate that preexisting spike- and S816-830–reactive T cells were recruited into immune responses to SARS-CoV-2 infection and their frequency correlated with anti–SARS-CoV-2-S1-IgG antibodies. Spike–cross-reactive T cells were also activated after primary BNT162b2 COVID-19 messenger RNA vaccination and displayed kinetics similar to those of secondary immune responses. Our results highlight the functional contribution of preexisting spike–cross-reactive T cells in SARS-CoV-2 infection and vaccination. Cross-reactive immunity may account for the unexpectedly rapid induction of immunity after primary SARS-CoV-2 immunization and the high rate of asymptomatic or mild COVID-19 disease courses. |
| Author | Wenschuh, Holger Sawitzki, Birgit Corman, Victor M. Dingeldey, Manuela Schnatbaum, Karsten Müller, Marcel A. Giesecke-Thiel, Claudia Sander, Leif-Erik Meyer-Arndt, Lil Hocke, Andreas Rosowski, Jennifer Kadler, Shirin Paul, Friedemann Kern, Florian Voigt, Sebastian Loyal, Lucie Miltenyi, Stefan Mall, Marcus A. Drosten, Christian Gürcan, Kübrah Dörfler, Friederike Lachman, Nils Frentsch, Marco Lauster, Roland Schwarz, Tatjana Uyar-Aydin, Zehra Reimer, Ulf Thiel, Andreas Kurth, Florian Röhmel, Jobst Mangold, Maike Eckey, Maren Hippenstiel, Stefan Unger, Clara Braun, Julian Henze, Larissa Kruse, Beate |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34465633$$D View this record in MEDLINE/PubMed |
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| Snippet | There is mounting evidence that immunological memory after infection with seasonal human coronaviruses (hCoVs) contributes to cross-protection against severe... The functional relevance of preexisting cross-immunity to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a subject of intense debate. Here, we... Cross-reactive T cells aid in the fightThere is mounting evidence that immunological memory after infection with seasonal human coronaviruses (hCoVs)... |
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| SubjectTerms | Adult Age Age Factors Aged Aged, 80 and over Antibodies Asymptomatic Asymptomatic Diseases Asymptomatic infection Avidity BNT162 Vaccine CD3 Complex - immunology CD4 antigen CD4-Positive T-Lymphocytes - immunology Coronaviridae Coronaviruses COVID-19 COVID-19 - immunology COVID-19 vaccines COVID-19 Vaccines - immunology Cross Reactions Cross-protection Cross-reactivity Female Glycoproteins Homology Humans Humoral immunity Immune response Immune system Immunity Immunization Immunodominant Epitopes - immunology Immunoglobulin G Immunological memory Immunology Infections Kinetics Logical Thinking Lymphocytes Lymphocytes T Male Memory cells Middle Aged mRNA Older people Open Reading Frames Peptide Fragments - immunology Peptides Respiratory diseases Respiratory failure SARS-CoV-2 - genetics SARS-CoV-2 - immunology Severe acute respiratory syndrome coronavirus 2 Spike glycoprotein Spike Glycoprotein, Coronavirus - immunology Spike protein T cell receptors Vaccination Vaccines Viral diseases Young Adult |
| Title | Cross-reactive CD4 + T cells enhance SARS-CoV-2 immune responses upon infection and vaccination |
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