Cross-reactive and mono-reactive SARS-CoV-2 CD4+ T cells in prepandemic and COVID-19 convalescent individuals

Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell epitopes. A total of 112, 28 and 42 epitopes specific for Spike, Membrane and Nucleocapsid, respectively, with defined HLA-restriction were identifie...

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Published inPLoS pathogens Vol. 17; no. 12; p. e1010203
Main Authors Johansson, Alexandra M., Malhotra, Uma, Kim, Yeseul G., Gomez, Rebecca, Krist, Maxwell P., Wald, Anna, Koelle, David M., Kwok, William W.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.12.2021
Public Library of Science (PLoS)
Subjects
Alleles
Amino acid sequence
Amino acids
Antigenic determinants
Avidity
Biology and Life Sciences
CD4 antigen
CD4-Positive T-Lymphocytes - immunology
Cell lines
Convalescence
Coronaviruses
COVID-19
COVID-19 - epidemiology
COVID-19 - immunology
Cross Reactions
Cross-reactivity
Epidemiology
Epitopes
Epitopes, T-Lymphocyte - immunology
Experiments
Frequency analysis
Histocompatibility antigen HLA
Humans
Identification and classification
Influenza
Lymphocytes
Lymphocytes T
Medicine and Health Sciences
Nucleocapsids
Pandemics
Peptides
Peripheral blood mononuclear cells
Population genetics
Proteins
Reagents
Research and Analysis Methods
SARS-CoV-2 - immunology
Severe acute respiratory syndrome
Severe acute respiratory syndrome coronavirus 2
Spike Glycoprotein, Coronavirus - immunology
T cell receptors
T cells
Viral diseases
Viruses
World population
United States
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Abstract Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell epitopes. A total of 112, 28 and 42 epitopes specific for Spike, Membrane and Nucleocapsid, respectively, with defined HLA-restriction were identified. Direct ex vivo staining of PBMC with tetramer reagents was used to define immunodominant and subdominant T cell epitopes and estimate the frequencies of these T cells in SARS-CoV-2 exposed and naïve individuals. Majority of SARS-CoV-2 epitopes identified have <67% amino acid sequence identity with endemic coronaviruses and are unlikely to elicit high avidity cross-reactive T cell responses. Four SARS-CoV-2 Spike reactive epitopes, including a DPB1*04:01 restricted epitope, with ≥67% amino acid sequence identity to endemic coronavirus were identified. SARS-CoV-2 T cell lines for three of these epitopes elicited cross-reactive T cell responses to endemic cold viruses. An endemic coronavirus Spike T cell line showed cross-reactivity to the fourth SARS-CoV-2 epitope. Three of the Spike cross-reactive epitopes were subdominant epitopes, while the DPB1*04:01 restricted epitope was a dominant epitope. Frequency analyses showed Spike cross-reactive T cells as detected by tetramers were present at relatively low frequency in unexposed people and only contributed a small proportion of the overall Spike-specific CD4+ T cells in COVID-19 convalescent individuals. In total, these results suggested a very limited number of SARS-CoV-2 T cells as detected by tetramers are capable of recognizing ccCoV with relative high avidity and vice versa. The potentially supportive role of these high avidity cross-reactive T cells in protective immunity against SARS-CoV-2 needs further studies.
AbstractList Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell epitopes. A total of 112, 28 and 42 epitopes specific for Spike, Membrane and Nucleocapsid, respectively, with defined HLA-restriction were identified. Direct ex vivo staining of PBMC with tetramer reagents was used to define immunodominant and subdominant T cell epitopes and estimate the frequencies of these T cells in SARS-CoV-2 exposed and naïve individuals. Majority of SARS-CoV-2 epitopes identified have <67% amino acid sequence identity with endemic coronaviruses and are unlikely to elicit high avidity cross-reactive T cell responses. Four SARS-CoV-2 Spike reactive epitopes, including a DPB1*04:01 restricted epitope, with ≥67% amino acid sequence identity to endemic coronavirus were identified. SARS-CoV-2 T cell lines for three of these epitopes elicited cross-reactive T cell responses to endemic cold viruses. An endemic coronavirus Spike T cell line showed cross-reactivity to the fourth SARS-CoV-2 epitope. Three of the Spike cross-reactive epitopes were subdominant epitopes, while the DPB1*04:01 restricted epitope was a dominant epitope. Frequency analyses showed Spike cross-reactive T cells as detected by tetramers were present at relatively low frequency in unexposed people and only contributed a small proportion of the overall Spike-specific CD4+ T cells in COVID-19 convalescent individuals. In total, these results suggested a very limited number of SARS-CoV-2 T cells as detected by tetramers are capable of recognizing ccCoV with relative high avidity and vice versa. The potentially supportive role of these high avidity cross-reactive T cells in protective immunity against SARS-CoV-2 needs further studies.
Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell epitopes. A total of 112, 28 and 42 epitopes specific for Spike, Membrane and Nucleocapsid, respectively, with defined HLA-restriction were identified. Direct ex vivo staining of PBMC with tetramer reagents was used to define immunodominant and subdominant T cell epitopes and estimate the frequencies of these T cells in SARS-CoV-2 exposed and naïve individuals. Majority of SARS-CoV-2 epitopes identified have <67% amino acid sequence identity with endemic coronaviruses and are unlikely to elicit high avidity cross-reactive T cell responses. Four SARS-CoV-2 Spike reactive epitopes, including a DPB1*04:01 restricted epitope, with ≥67% amino acid sequence identity to endemic coronavirus were identified. SARS-CoV-2 T cell lines for three of these epitopes elicited cross-reactive T cell responses to endemic cold viruses. An endemic coronavirus Spike T cell line showed cross-reactivity to the fourth SARS-CoV-2 epitope. Three of the Spike cross-reactive epitopes were subdominant epitopes, while the DPB1*04:01 restricted epitope was a dominant epitope. Frequency analyses showed Spike cross-reactive T cells as detected by tetramers were present at relatively low frequency in unexposed people and only contributed a small proportion of the overall Spike-specific CD4+ T cells in COVID-19 convalescent individuals. In total, these results suggested a very limited number of SARS-CoV-2 T cells as detected by tetramers are capable of recognizing ccCoV with relative high avidity and vice versa. The potentially supportive role of these high avidity cross-reactive T cells in protective immunity against SARS-CoV-2 needs further studies.
Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell epitopes. A total of 112, 28 and 42 epitopes specific for Spike, Membrane and Nucleocapsid, respectively, with defined HLA-restriction were identified. Direct ex vivo staining of PBMC with tetramer reagents was used to define immunodominant and subdominant T cell epitopes and estimate the frequencies of these T cells in SARS-CoV-2 exposed and naïve individuals. Majority of SARS-CoV-2 epitopes identified have <67% amino acid sequence identity with endemic coronaviruses and are unlikely to elicit high avidity cross-reactive T cell responses. Four SARS-CoV-2 Spike reactive epitopes, including a DPB1*04:01 restricted epitope, with ≥67% amino acid sequence identity to endemic coronavirus were identified. SARS-CoV-2 T cell lines for three of these epitopes elicited cross-reactive T cell responses to endemic cold viruses. An endemic coronavirus Spike T cell line showed cross-reactivity to the fourth SARS-CoV-2 epitope. Three of the Spike cross-reactive epitopes were subdominant epitopes, while the DPB1*04:01 restricted epitope was a dominant epitope. Frequency analyses showed Spike cross-reactive T cells as detected by tetramers were present at relatively low frequency in unexposed people and only contributed a small proportion of the overall Spike-specific CD4+ T cells in COVID-19 convalescent individuals. In total, these results suggested a very limited number of SARS-CoV-2 T cells as detected by tetramers are capable of recognizing ccCoV with relative high avidity and vice versa. The potentially supportive role of these high avidity cross-reactive T cells in protective immunity against SARS-CoV-2 needs further studies. Previous studies with activation induced marker assays in monitoring antigen-specific CD4+ T cells have shown that common cold coronavirus T cells can cross-react with SARS-CoV-2 antigens and these cross-reactive T cells are present in up to 60% of the unexposed population. In this current study, sets of overlapping peptides for Spike, Membrane, and Nucleocapsid proteins were used to identify epitopes across 11 HLA-DR and 1 HLA-DP alleles in SARS-CoV-2 convalescent samples using peptide-loaded MHC-II tetramers. Using these tetramers ex vivo , frequencies of these epitope-specific T cells were estimated in convalescent and pre-pandemic samples. Based on these frequencies, epitopes were stratified into immunodominant and subdominant epitopes. Amino acid sequences of epitopes identified were compared with 4 common cold coronaviruses. Potential cross-reactive epitopes were defined as having ≥67% sequence identity between common cold viruses and SARS-CoV-2. Four potential Spike specific cross-reactive epitopes were identified and functional cross-reactivity was demonstrated. Of the four cross-reactive epitopes identified, three were subdominant epitopes eliciting relatively low frequencies in both unexposed and convalescent subjects. In contrast to the results from the activation induced marker assays, the current data suggests that only a limited number of high avidity SARS-CoV-2 T cells as detected by tetramers are cross-reactive.
Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell epitopes. A total of 112, 28 and 42 epitopes specific for Spike, Membrane and Nucleocapsid, respectively, with defined HLA-restriction were identified. Direct ex vivo staining of PBMC with tetramer reagents was used to define immunodominant and subdominant T cell epitopes and estimate the frequencies of these T cells in SARS-CoV-2 exposed and naïve individuals. Majority of SARS-CoV-2 epitopes identified have <67% amino acid sequence identity with endemic coronaviruses and are unlikely to elicit high avidity cross-reactive T cell responses. Four SARS-CoV-2 Spike reactive epitopes, including a DPB1*04:01 restricted epitope, with [greater than or equal to]67% amino acid sequence identity to endemic coronavirus were identified. SARS-CoV-2 T cell lines for three of these epitopes elicited cross-reactive T cell responses to endemic cold viruses. An endemic coronavirus Spike T cell line showed cross-reactivity to the fourth SARS-CoV-2 epitope. Three of the Spike cross-reactive epitopes were subdominant epitopes, while the DPB1*04:01 restricted epitope was a dominant epitope. Frequency analyses showed Spike cross-reactive T cells as detected by tetramers were present at relatively low frequency in unexposed people and only contributed a small proportion of the overall Spike-specific CD4+ T cells in COVID-19 convalescent individuals. In total, these results suggested a very limited number of SARS-CoV-2 T cells as detected by tetramers are capable of recognizing ccCoV with relative high avidity and vice versa. The potentially supportive role of these high avidity cross-reactive T cells in protective immunity against SARS-CoV-2 needs further studies.
Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell epitopes. A total of 112, 28 and 42 epitopes specific for Spike, Membrane and Nucleocapsid, respectively, with defined HLA-restriction were identified. Direct ex vivo staining of PBMC with tetramer reagents was used to define immunodominant and subdominant T cell epitopes and estimate the frequencies of these T cells in SARS-CoV-2 exposed and naïve individuals. Majority of SARS-CoV-2 epitopes identified have <67% amino acid sequence identity with endemic coronaviruses and are unlikely to elicit high avidity cross-reactive T cell responses. Four SARS-CoV-2 Spike reactive epitopes, including a DPB1*04:01 restricted epitope, with ≥67% amino acid sequence identity to endemic coronavirus were identified. SARS-CoV-2 T cell lines for three of these epitopes elicited cross-reactive T cell responses to endemic cold viruses. An endemic coronavirus Spike T cell line showed cross-reactivity to the fourth SARS-CoV-2 epitope. Three of the Spike cross-reactive epitopes were subdominant epitopes, while the DPB1*04:01 restricted epitope was a dominant epitope. Frequency analyses showed Spike cross-reactive T cells as detected by tetramers were present at relatively low frequency in unexposed people and only contributed a small proportion of the overall Spike-specific CD4+ T cells in COVID-19 convalescent individuals. In total, these results suggested a very limited number of SARS-CoV-2 T cells as detected by tetramers are capable of recognizing ccCoV with relative high avidity and vice versa. The potentially supportive role of these high avidity cross-reactive T cells in protective immunity against SARS-CoV-2 needs further studies.Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell epitopes. A total of 112, 28 and 42 epitopes specific for Spike, Membrane and Nucleocapsid, respectively, with defined HLA-restriction were identified. Direct ex vivo staining of PBMC with tetramer reagents was used to define immunodominant and subdominant T cell epitopes and estimate the frequencies of these T cells in SARS-CoV-2 exposed and naïve individuals. Majority of SARS-CoV-2 epitopes identified have <67% amino acid sequence identity with endemic coronaviruses and are unlikely to elicit high avidity cross-reactive T cell responses. Four SARS-CoV-2 Spike reactive epitopes, including a DPB1*04:01 restricted epitope, with ≥67% amino acid sequence identity to endemic coronavirus were identified. SARS-CoV-2 T cell lines for three of these epitopes elicited cross-reactive T cell responses to endemic cold viruses. An endemic coronavirus Spike T cell line showed cross-reactivity to the fourth SARS-CoV-2 epitope. Three of the Spike cross-reactive epitopes were subdominant epitopes, while the DPB1*04:01 restricted epitope was a dominant epitope. Frequency analyses showed Spike cross-reactive T cells as detected by tetramers were present at relatively low frequency in unexposed people and only contributed a small proportion of the overall Spike-specific CD4+ T cells in COVID-19 convalescent individuals. In total, these results suggested a very limited number of SARS-CoV-2 T cells as detected by tetramers are capable of recognizing ccCoV with relative high avidity and vice versa. The potentially supportive role of these high avidity cross-reactive T cells in protective immunity against SARS-CoV-2 needs further studies.
Audience Academic
Author Kwok, William W.
Malhotra, Uma
Krist, Maxwell P.
Koelle, David M.
Johansson, Alexandra M.
Gomez, Rebecca
Kim, Yeseul G.
Wald, Anna
AuthorAffiliation 2 Virginia Mason Franciscan Health, Seattle, Washington, United States of America
3 Department of Medicine, University of Washington, Seattle, Washington, United States of America
6 Department of Laboratory Medicine and Pathology, University of Washington, Seattle, Washington, United States of America
University of Rochester Medical Center, UNITED STATES
7 Department of Global Health, University of Washington, Seattle, Washington, United States of America
1 Benaroya Research Institute at Virginia Mason, Seattle, Washington, United States of America
5 Department of Epidemiology, University of Washington, Seattle, Washington, United States of America
4 Vaccine and Infectious Diseases Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America
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– name: 6 Department of Laboratory Medicine and Pathology, University of Washington, Seattle, Washington, United States of America
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/34965282$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1126/sciimmunol.abd2071
10.1016/j.immuni.2021.04.006
10.1038/s41589-018-0130-4
10.1172/JCI8476
10.1016/j.immuni.2020.11.016
10.1093/intimm/dxm099
10.1038/s41586-020-2550-z
10.1126/sciimmunol.abf7550
10.1038/s41590-021-00902-8
10.1038/s41590-020-0782-6
10.1172/JCI145476
10.1038/s41577-020-00460-4
10.3389/fimmu.2020.565096
10.1038/s41591-020-01143-2
10.1016/j.virusres.2014.03.018
10.1038/s41590-020-00808-x
10.1038/s41598-021-83730-y
10.1038/ncomms12614
10.1038/s41586-020-2521-4
10.1016/j.cell.2020.05.015
10.1126/science.abd4570
10.1038/s41586-020-2818-3
10.1016/j.cell.2020.09.038
10.1172/JCI143120
10.1056/NEJMoa2001017
10.1111/tan.13811
10.1073/pnas.92.22.10398
10.1093/nar/gkaa379
10.4049/jimmunol.0903655
10.1038/s41586-020-2598-9
10.1172/JCI143380
10.1038/s41467-021-21856-3
10.1002/jmv.25681
10.1172/JCI144930
10.1126/science.abd3871
10.1016/j.cell.2020.08.017
10.1056/NEJMoa2020283
10.1016/j.clim.2006.03.008
10.1038/s41586-020-03065-y
10.1038/s41577-020-0389-z
10.1038/s41564-020-0695-z
10.1172/JCI149335
10.1016/j.celrep.2021.108728
10.1016/j.immuni.2021.04.009
10.1007/s15010-020-01531-3
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2021 Johansson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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– notice: 2021 Johansson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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References J Sidney (ppat.1010203.ref043) 2010; 184
B Meyer (ppat.1010203.ref036) 2014; 194
CK Hurley (ppat.1010203.ref037) 2020; 95
IQ Phan (ppat.1010203.ref049) 2021; 11
J Zuo (ppat.1010203.ref017) 2021; 22
B Reynisson (ppat.1010203.ref041) 2020; 48
EJ Williamson (ppat.1010203.ref003) 2020; 584
N Le Bert (ppat.1010203.ref026) 2020; 584
Y Chen (ppat.1010203.ref029) 2020; 92
H Zeberg (ppat.1010203.ref007) 2020; 587
EA James (ppat.1010203.ref039) 2007; 19
B Salzberger (ppat.1010203.ref002) 2021; 49
Q Zhang (ppat.1010203.ref005) 2020; 370
A Ogbe (ppat.1010203.ref014) 2021; 12
E Pairo-Castineira (ppat.1010203.ref006) 2021; 591
TP Riley (ppat.1010203.ref046) 2018; 14
M Lipsitch (ppat.1010203.ref034) 2020; 20
T Sekine (ppat.1010203.ref012) 2020; 183
AT Tan (ppat.1010203.ref016) 2021; 34
I Schulien (ppat.1010203.ref022) 2021; 27
N Zhu (ppat.1010203.ref001) 2020; 382
Coronaviridae Study Group of the International Committee on Taxonomy of V (ppat.1010203.ref028) 2020; 5
D Weiskopf (ppat.1010203.ref009) 2020; 5
JM Dan (ppat.1010203.ref011) 2021; 371
H Kared (ppat.1010203.ref024) 2021; 131
M Sagar (ppat.1010203.ref035) 2021; 131
EJ Novak (ppat.1010203.ref050) 1999; 104
SK Saini (ppat.1010203.ref021) 2021; 6
Y Peng (ppat.1010203.ref013) 2020; 21
A Grifoni (ppat.1010203.ref008) 2020; 181
J Boonyaratanakornkit (ppat.1010203.ref048) 2021; 131
J Yang (ppat.1010203.ref038) 2006; 120
JS Low (ppat.1010203.ref018) 2021
GG Severe Covid (ppat.1010203.ref004) 2020; 383
BA Woldemeskel (ppat.1010203.ref044) 2021; 131
AG Dykema (ppat.1010203.ref032) 2021
S Quaratino (ppat.1010203.ref045) 1995; 92
P Bacher (ppat.1010203.ref027) 2020; 53
BA Woldemeskel (ppat.1010203.ref031) 2020; 130
A Tarke (ppat.1010203.ref019) 2020
A Tarke (ppat.1010203.ref042) 2021
CH Lee (ppat.1010203.ref047) 2020; 11
A Nelde (ppat.1010203.ref020) 2021; 22
KE Lineburg (ppat.1010203.ref030) 2021; 54
J Mateus (ppat.1010203.ref025) 2020; 370
THO Nguyen (ppat.1010203.ref023) 2021; 54
J Braun (ppat.1010203.ref015) 2020; 587
C Rydyznski Moderbacher (ppat.1010203.ref010) 2020; 183
A Sette (ppat.1010203.ref033) 2020; 20
H Uchtenhagen (ppat.1010203.ref040) 2016; 7
J Yang (ppat.1010203.ref051) 2005; 25
References_xml – volume: 5
  issue: 48
  year: 2020
  ident: ppat.1010203.ref009
  article-title: Phenotype and kinetics of SARS-CoV-2-specific T cells in COVID-19 patients with acute respiratory distress syndrome
  publication-title: Sci Immunol
  doi: 10.1126/sciimmunol.abd2071
– volume: 54
  start-page: 1055
  issue: 5
  year: 2021
  ident: ppat.1010203.ref030
  article-title: CD8(+) T cells specific for an immunodominant SARS-CoV-2 nucleocapsid epitope cross-react with selective seasonal coronaviruses
  publication-title: Immunity
  doi: 10.1016/j.immuni.2021.04.006
– volume: 14
  start-page: 934
  issue: 10
  year: 2018
  ident: ppat.1010203.ref046
  article-title: T cell receptor cross-reactivity expanded by dramatic peptide-MHC adaptability
  publication-title: Nat Chem Biol
  doi: 10.1038/s41589-018-0130-4
– year: 2021
  ident: ppat.1010203.ref042
  article-title: Negligible impact of SARS-CoV-2 variants on CD4 (+) and CD8 (+) T cell reactivity in COVID-19 exposed donors and vaccinees
  publication-title: bioRxiv
– volume: 104
  start-page: R63
  issue: 12
  year: 1999
  ident: ppat.1010203.ref050
  article-title: MHC class II tetramers identify peptide-specific human CD4(+) T cells proliferating in response to influenza A antigen
  publication-title: J Clin Invest
  doi: 10.1172/JCI8476
– volume: 53
  start-page: 1258
  issue: 6
  year: 2020
  ident: ppat.1010203.ref027
  article-title: Low-Avidity CD4(+) T Cell Responses to SARS-CoV-2 in Unexposed Individuals and Humans with Severe COVID-19
  publication-title: Immunity
  doi: 10.1016/j.immuni.2020.11.016
– volume: 19
  start-page: 1291
  issue: 11
  year: 2007
  ident: ppat.1010203.ref039
  article-title: Tetramer-guided epitope mapping reveals broad, individualized repertoires of tetanus toxin-specific CD4+ T cells and suggests HLA-based differences in epitope recognition
  publication-title: Int Immunol
  doi: 10.1093/intimm/dxm099
– volume: 584
  start-page: 457
  issue: 7821
  year: 2020
  ident: ppat.1010203.ref026
  article-title: SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls
  publication-title: Nature
  doi: 10.1038/s41586-020-2550-z
– year: 2020
  ident: ppat.1010203.ref019
  article-title: Comprehensive analysis of T cell immunodominance and immunoprevalence of SARS-CoV-2 epitopes in COVID-19 cases
  publication-title: bioRxiv
– volume: 6
  issue: 58
  year: 2021
  ident: ppat.1010203.ref021
  article-title: SARS-CoV-2 genome-wide T cell epitope mapping reveals immunodominance and substantial CD8(+) T cell activation in COVID-19 patients
  publication-title: Sci Immunol
  doi: 10.1126/sciimmunol.abf7550
– volume: 22
  start-page: 620
  issue: 5
  year: 2021
  ident: ppat.1010203.ref017
  article-title: Robust SARS-CoV-2-specific T cell immunity is maintained at 6 months following primary infection
  publication-title: Nat Immunol
  doi: 10.1038/s41590-021-00902-8
– volume: 21
  start-page: 1336
  issue: 11
  year: 2020
  ident: ppat.1010203.ref013
  article-title: Broad and strong memory CD4(+) and CD8(+) T cells induced by SARS-CoV-2 in UK convalescent individuals following COVID-19
  publication-title: Nat Immunol
  doi: 10.1038/s41590-020-0782-6
– volume: 131
  issue: 5
  year: 2021
  ident: ppat.1010203.ref024
  article-title: SARS-CoV-2-specific CD8+ T cell responses in convalescent COVID-19 individuals
  publication-title: J Clin Invest
  doi: 10.1172/JCI145476
– volume: 20
  start-page: 709
  issue: 11
  year: 2020
  ident: ppat.1010203.ref034
  article-title: Cross-reactive memory T cells and herd immunity to SARS-CoV-2
  publication-title: Nat Rev Immunol
  doi: 10.1038/s41577-020-00460-4
– volume: 11
  start-page: 565096
  year: 2020
  ident: ppat.1010203.ref047
  article-title: Predicting Cross-Reactivity and Antigen Specificity of T Cell Receptors
  publication-title: Front Immunol
  doi: 10.3389/fimmu.2020.565096
– volume: 27
  start-page: 78
  issue: 1
  year: 2021
  ident: ppat.1010203.ref022
  article-title: Characterization of pre-existing and induced SARS-CoV-2-specific CD8(+) T cells
  publication-title: Nat Med
  doi: 10.1038/s41591-020-01143-2
– year: 2021
  ident: ppat.1010203.ref032
  article-title: Functional characterization of CD4+ T-cell receptors cross-reactive for SARS-CoV-2 and endemic coronaviruses
  publication-title: J Clin Invest
– volume: 194
  start-page: 175
  year: 2014
  ident: ppat.1010203.ref036
  article-title: Serological assays for emerging coronaviruses: challenges and pitfalls
  publication-title: Virus Res
  doi: 10.1016/j.virusres.2014.03.018
– year: 2021
  ident: ppat.1010203.ref018
  article-title: Clonal analysis of immunodominance and cross-reactivity of the CD4 T cell response to SARS-CoV-2
  publication-title: Science
– volume: 22
  start-page: 74
  issue: 1
  year: 2021
  ident: ppat.1010203.ref020
  article-title: SARS-CoV-2-derived peptides define heterologous and COVID-19-induced T cell recognition
  publication-title: Nat Immunol
  doi: 10.1038/s41590-020-00808-x
– volume: 11
  start-page: 4290
  issue: 1
  year: 2021
  ident: ppat.1010203.ref049
  article-title: In silico detection of SARS-CoV-2 specific B-cell epitopes and validation in ELISA for serological diagnosis of COVID-19
  publication-title: Sci Rep
  doi: 10.1038/s41598-021-83730-y
– volume: 7
  start-page: 12614
  year: 2016
  ident: ppat.1010203.ref040
  article-title: Efficient ex vivo analysis of CD4+ T-cell responses using combinatorial HLA class II tetramer staining
  publication-title: Nat Commun
  doi: 10.1038/ncomms12614
– volume: 584
  start-page: 430
  issue: 7821
  year: 2020
  ident: ppat.1010203.ref003
  article-title: Factors associated with COVID-19-related death using OpenSAFELY
  publication-title: Nature
  doi: 10.1038/s41586-020-2521-4
– volume: 181
  start-page: 1489
  issue: 7
  year: 2020
  ident: ppat.1010203.ref008
  article-title: Targets of T Cell Responses to SARS-CoV-2 Coronavirus in Humans with COVID-19 Disease and Unexposed Individuals
  publication-title: Cell
  doi: 10.1016/j.cell.2020.05.015
– volume: 370
  issue: 6515
  year: 2020
  ident: ppat.1010203.ref005
  article-title: Inborn errors of type I IFN immunity in patients with life-threatening COVID-19
  publication-title: Science
  doi: 10.1126/science.abd4570
– volume: 587
  start-page: 610
  issue: 7835
  year: 2020
  ident: ppat.1010203.ref007
  article-title: The major genetic risk factor for severe COVID-19 is inherited from Neanderthals
  publication-title: Nature
  doi: 10.1038/s41586-020-2818-3
– volume: 183
  start-page: 996
  issue: 4
  year: 2020
  ident: ppat.1010203.ref010
  article-title: Antigen-Specific Adaptive Immunity to SARS-CoV-2 in Acute COVID-19 and Associations with Age and Disease Severity
  publication-title: Cell
  doi: 10.1016/j.cell.2020.09.038
– volume: 130
  start-page: 6631
  issue: 12
  year: 2020
  ident: ppat.1010203.ref031
  article-title: Healthy donor T cell responses to common cold coronaviruses and SARS-CoV-2
  publication-title: J Clin Invest
  doi: 10.1172/JCI143120
– volume: 25
  start-page: 428
  issue: 5
  year: 2005
  ident: ppat.1010203.ref051
  article-title: Expression of HLA-DP0401 molecules for identification of DP0401 restricted antigen specific T cells
– volume: 382
  start-page: 727
  issue: 8
  year: 2020
  ident: ppat.1010203.ref001
  article-title: A Novel Coronavirus from Patients with Pneumonia in China, 2019
  publication-title: N Engl J Med
  doi: 10.1056/NEJMoa2001017
– volume: 95
  start-page: 516
  issue: 6
  year: 2020
  ident: ppat.1010203.ref037
  article-title: Common, intermediate and well-documented HLA alleles in world populations: CIWD version 3.0.0
  publication-title: HLA
  doi: 10.1111/tan.13811
– volume: 92
  start-page: 10398
  issue: 22
  year: 1995
  ident: ppat.1010203.ref045
  article-title: Similar antigenic surfaces, rather than sequence homology, dictate T-cell epitope molecular mimicry
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.92.22.10398
– volume: 48
  start-page: W449
  issue: W1
  year: 2020
  ident: ppat.1010203.ref041
  article-title: NetMHCpan-4.1 and NetMHCIIpan-4.0: improved predictions of MHC antigen presentation by concurrent motif deconvolution and integration of MS MHC eluted ligand data
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkaa379
– volume: 184
  start-page: 2492
  issue: 5
  year: 2010
  ident: ppat.1010203.ref043
  article-title: Five HLA-DP molecules frequently expressed in the worldwide human population share a common HLA supertypic binding specificity
  publication-title: J Immunol
  doi: 10.4049/jimmunol.0903655
– volume: 587
  start-page: 270
  issue: 7833
  year: 2020
  ident: ppat.1010203.ref015
  article-title: SARS-CoV-2-reactive T cells in healthy donors and patients with COVID-19
  publication-title: Nature
  doi: 10.1038/s41586-020-2598-9
– volume: 131
  issue: 1
  year: 2021
  ident: ppat.1010203.ref035
  article-title: Recent endemic coronavirus infection is associated with less-severe COVID-19
  publication-title: J Clin Invest
  doi: 10.1172/JCI143380
– volume: 12
  start-page: 2055
  issue: 1
  year: 2021
  ident: ppat.1010203.ref014
  article-title: T cell assays differentiate clinical and subclinical SARS-CoV-2 infections from cross-reactive antiviral responses
  publication-title: Nat Commun
  doi: 10.1038/s41467-021-21856-3
– volume: 92
  start-page: 418
  issue: 4
  year: 2020
  ident: ppat.1010203.ref029
  article-title: Emerging coronaviruses: Genome structure, replication, and pathogenesis
  publication-title: J Med Virol
  doi: 10.1002/jmv.25681
– volume: 131
  issue: 3
  year: 2021
  ident: ppat.1010203.ref048
  article-title: Clinical, laboratory, and temporal predictors of neutralizing antibodies against SARS-CoV-2 among COVID-19 convalescent plasma donor candidates
  publication-title: J Clin Invest
  doi: 10.1172/JCI144930
– volume: 370
  start-page: 89
  issue: 6512
  year: 2020
  ident: ppat.1010203.ref025
  article-title: Selective and cross-reactive SARS-CoV-2 T cell epitopes in unexposed humans
  publication-title: Science
  doi: 10.1126/science.abd3871
– volume: 371
  issue: 6529
  year: 2021
  ident: ppat.1010203.ref011
  article-title: Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection
  publication-title: Science
– volume: 183
  start-page: 158
  issue: 1
  year: 2020
  ident: ppat.1010203.ref012
  article-title: Robust T Cell Immunity in Convalescent Individuals with Asymptomatic or Mild COVID-19
  publication-title: Cell
  doi: 10.1016/j.cell.2020.08.017
– volume: 383
  start-page: 1522
  issue: 16
  year: 2020
  ident: ppat.1010203.ref004
  article-title: Genomewide Association Study of Severe Covid-19 with Respiratory Failure
  publication-title: N Engl J Med
  doi: 10.1056/NEJMoa2020283
– volume: 120
  start-page: 21
  issue: 1
  year: 2006
  ident: ppat.1010203.ref038
  article-title: Multiplex mapping of CD4 T cell epitopes using class II tetramers
  publication-title: Clin Immunol
  doi: 10.1016/j.clim.2006.03.008
– volume: 591
  start-page: 92
  issue: 7848
  year: 2021
  ident: ppat.1010203.ref006
  article-title: Genetic mechanisms of critical illness in COVID-19
  publication-title: Nature
  doi: 10.1038/s41586-020-03065-y
– volume: 20
  start-page: 457
  issue: 8
  year: 2020
  ident: ppat.1010203.ref033
  article-title: Pre-existing immunity to SARS-CoV-2: the knowns and unknowns
  publication-title: Nat Rev Immunol
  doi: 10.1038/s41577-020-0389-z
– volume: 5
  start-page: 536
  issue: 4
  year: 2020
  ident: ppat.1010203.ref028
  article-title: The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2
  publication-title: Nat Microbiol
  doi: 10.1038/s41564-020-0695-z
– volume: 131
  issue: 10
  year: 2021
  ident: ppat.1010203.ref044
  article-title: SARS-CoV-2 mRNA vaccines induce broad CD4+ T cell responses that recognize SARS-CoV-2 variants and HCoV-NL63
  publication-title: J Clin Invest
  doi: 10.1172/JCI149335
– volume: 34
  start-page: 108728
  issue: 6
  year: 2021
  ident: ppat.1010203.ref016
  article-title: Early induction of functional SARS-CoV-2-specific T cells associates with rapid viral clearance and mild disease in COVID-19 patients
  publication-title: Cell Rep
  doi: 10.1016/j.celrep.2021.108728
– volume: 54
  start-page: 1066
  issue: 5
  year: 2021
  ident: ppat.1010203.ref023
  article-title: CD8(+) T cells specific for an immunodominant SARS-CoV-2 nucleocapsid epitope display high naive precursor frequency and TCR promiscuity
  publication-title: Immunity
  doi: 10.1016/j.immuni.2021.04.009
– volume: 49
  start-page: 233
  issue: 2
  year: 2021
  ident: ppat.1010203.ref002
  article-title: Epidemiology of SARS-CoV-2
  publication-title: Infection
  doi: 10.1007/s15010-020-01531-3
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Snippet Class II tetramer reagents for eleven common DR alleles and a DP allele prevalent in the world population were used to identify SARS-CoV-2 CD4+ T cell...
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StartPage e1010203
SubjectTerms Alleles
Amino acid sequence
Amino acids
Antigenic determinants
Avidity
Biology and Life Sciences
CD4 antigen
CD4-Positive T-Lymphocytes - immunology
Cell lines
Convalescence
Coronaviruses
COVID-19
COVID-19 - epidemiology
COVID-19 - immunology
Cross Reactions
Cross-reactivity
Epidemiology
Epitopes
Epitopes, T-Lymphocyte - immunology
Experiments
Frequency analysis
Histocompatibility antigen HLA
Humans
Identification and classification
Influenza
Lymphocytes
Lymphocytes T
Medicine and Health Sciences
Nucleocapsids
Pandemics
Peptides
Peripheral blood mononuclear cells
Population genetics
Proteins
Reagents
Research and Analysis Methods
SARS-CoV-2 - immunology
Severe acute respiratory syndrome
Severe acute respiratory syndrome coronavirus 2
Spike Glycoprotein, Coronavirus - immunology
T cell receptors
T cells
Viral diseases
Viruses
World population
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Title Cross-reactive and mono-reactive SARS-CoV-2 CD4+ T cells in prepandemic and COVID-19 convalescent individuals
URI https://www.ncbi.nlm.nih.gov/pubmed/34965282
https://www.proquest.com/docview/2620154268
https://www.proquest.com/docview/2615475644
https://pubmed.ncbi.nlm.nih.gov/PMC8769337
https://doaj.org/article/bf0a3bb224e14a84a33c8c5b5c198afa
http://dx.doi.org/10.1371/journal.ppat.1010203
Volume 17
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