The HLA-II immunopeptidome of SARS-CoV-2

Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive knowledge of viral immunogens. Here, we report severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) peptides that are naturally processed and...

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Published inCell reports (Cambridge) Vol. 43; no. 1; p. 113596
Main Authors Weingarten-Gabbay, Shira, Chen, Da-Yuan, Sarkizova, Siranush, Taylor, Hannah B., Gentili, Matteo, Hernandez, Gabrielle M., Pearlman, Leah R., Bauer, Matthew R., Rice, Charles M., Clauser, Karl R., Hacohen, Nir, Carr, Steven A., Abelin, Jennifer G., Saeed, Mohsan, Sabeti, Pardis C.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 23.01.2024
Elsevier
Subjects
antigen processing and presentation
CD4+ T cell
CP: Immunology
CP: Microbiology
HLA-II
immunity
immunopeptidome
noncanonical protein
SARS-CoV-2
viral antigen
CP: Immunology
SARS-CoV-2
CD4+ T cell
noncanonical protein
CP: Microbiology
immunopeptidome
HLA-II
antigen processing and presentation
immunity
viral antigen
CD4(+) T cell
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Abstract Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive knowledge of viral immunogens. Here, we report severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) peptides that are naturally processed and loaded onto human leukocyte antigen-II (HLA-II) complexes in infected cells. We identify over 500 unique viral peptides from canonical proteins as well as from overlapping internal open reading frames. Most HLA-II peptides colocalize with known CD4+ T cell epitopes in coronavirus disease 2019 patients, including 2 reported immunodominant regions in the SARS-CoV-2 membrane protein. Overall, our analyses show that HLA-I and HLA-II pathways target distinct viral proteins, with the structural proteins accounting for most of the HLA-II peptidome and nonstructural and noncanonical proteins accounting for the majority of the HLA-I peptidome. These findings highlight the need for a vaccine design that incorporates multiple viral elements harboring CD4+ and CD8+ T cell epitopes to maximize vaccine effectiveness. [Display omitted] •Immunopeptidome analysis of SARS-CoV-2 peptides naturally presented on HLA class II•Some HLA-II peptides originate from noncanonical SARS-CoV-2 proteins ORF9b and ORF3c•Class I and class II HLA complexes present different subsets of viral proteins Weingarten-Gabbay et al. map the repertoire of SARS-CoV-2 peptides naturally presented on HLA-II. The authors uncover HLA-II peptides originating from noncanonical ORFs and highlight striking differences between viral proteins that are presented on class I and class II HLAs, resulting in distinct targets for killer and helper T cells.
AbstractList Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive knowledge of viral immunogens. Here, we report severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) peptides that are naturally processed and loaded onto human leukocyte antigen-II (HLA-II) complexes in infected cells. We identify over 500 unique viral peptides from canonical proteins as well as from overlapping internal open reading frames. Most HLA-II peptides colocalize with known CD4 T cell epitopes in coronavirus disease 2019 patients, including 2 reported immunodominant regions in the SARS-CoV-2 membrane protein. Overall, our analyses show that HLA-I and HLA-II pathways target distinct viral proteins, with the structural proteins accounting for most of the HLA-II peptidome and nonstructural and noncanonical proteins accounting for the majority of the HLA-I peptidome. These findings highlight the need for a vaccine design that incorporates multiple viral elements harboring CD4 and CD8 T cell epitopes to maximize vaccine effectiveness.
Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive knowledge of viral immunogens. Here, we report severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) peptides that are naturally processed and loaded onto human leukocyte antigen-II (HLA-II) complexes in infected cells. We identify over 500 unique viral peptides from canonical proteins as well as from overlapping internal open reading frames. Most HLA-II peptides colocalize with known CD4+ T cell epitopes in coronavirus disease 2019 patients, including 2 reported immunodominant regions in the SARS-CoV-2 membrane protein. Overall, our analyses show that HLA-I and HLA-II pathways target distinct viral proteins, with the structural proteins accounting for most of the HLA-II peptidome and nonstructural and noncanonical proteins accounting for the majority of the HLA-I peptidome. These findings highlight the need for a vaccine design that incorporates multiple viral elements harboring CD4+ and CD8+ T cell epitopes to maximize vaccine effectiveness.
Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive knowledge of viral immunogens. Here, we report severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) peptides that are naturally processed and loaded onto human leukocyte antigen-II (HLA-II) complexes in infected cells. We identify over 500 unique viral peptides from canonical proteins as well as from overlapping internal open reading frames. Most HLA-II peptides colocalize with known CD4+ T cell epitopes in coronavirus disease 2019 patients, including 2 reported immunodominant regions in the SARS-CoV-2 membrane protein. Overall, our analyses show that HLA-I and HLA-II pathways target distinct viral proteins, with the structural proteins accounting for most of the HLA-II peptidome and nonstructural and noncanonical proteins accounting for the majority of the HLA-I peptidome. These findings highlight the need for a vaccine design that incorporates multiple viral elements harboring CD4+ and CD8+ T cell epitopes to maximize vaccine effectiveness. [Display omitted] •Immunopeptidome analysis of SARS-CoV-2 peptides naturally presented on HLA class II•Some HLA-II peptides originate from noncanonical SARS-CoV-2 proteins ORF9b and ORF3c•Class I and class II HLA complexes present different subsets of viral proteins Weingarten-Gabbay et al. map the repertoire of SARS-CoV-2 peptides naturally presented on HLA-II. The authors uncover HLA-II peptides originating from noncanonical ORFs and highlight striking differences between viral proteins that are presented on class I and class II HLAs, resulting in distinct targets for killer and helper T cells.
Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive knowledge of viral immunogens. Here, we report severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) peptides that are naturally processed and loaded onto human leukocyte antigen-II (HLA-II) complexes in infected cells. We identify over 500 unique viral peptides from canonical proteins as well as from overlapping internal open reading frames. Most HLA-II peptides colocalize with known CD4+ T cell epitopes in coronavirus disease 2019 patients, including 2 reported immunodominant regions in the SARS-CoV-2 membrane protein. Overall, our analyses show that HLA-I and HLA-II pathways target distinct viral proteins, with the structural proteins accounting for most of the HLA-II peptidome and nonstructural and noncanonical proteins accounting for the majority of the HLA-I peptidome. These findings highlight the need for a vaccine design that incorporates multiple viral elements harboring CD4+ and CD8+ T cell epitopes to maximize vaccine effectiveness.Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive knowledge of viral immunogens. Here, we report severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) peptides that are naturally processed and loaded onto human leukocyte antigen-II (HLA-II) complexes in infected cells. We identify over 500 unique viral peptides from canonical proteins as well as from overlapping internal open reading frames. Most HLA-II peptides colocalize with known CD4+ T cell epitopes in coronavirus disease 2019 patients, including 2 reported immunodominant regions in the SARS-CoV-2 membrane protein. Overall, our analyses show that HLA-I and HLA-II pathways target distinct viral proteins, with the structural proteins accounting for most of the HLA-II peptidome and nonstructural and noncanonical proteins accounting for the majority of the HLA-I peptidome. These findings highlight the need for a vaccine design that incorporates multiple viral elements harboring CD4+ and CD8+ T cell epitopes to maximize vaccine effectiveness.
Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive knowledge of viral immunogens. Here, we report severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) peptides that are naturally processed and loaded onto human leukocyte antigen-II (HLA-II) complexes in infected cells. We identify over 500 unique viral peptides from canonical proteins as well as from overlapping internal open reading frames. Most HLA-II peptides colocalize with known CD4 + T cell epitopes in coronavirus disease 2019 patients, including 2 reported immunodominant regions in the SARS-CoV-2 membrane protein. Overall, our analyses show that HLA-I and HLA-II pathways target distinct viral proteins, with the structural proteins accounting for most of the HLA-II peptidome and nonstructural and noncanonical proteins accounting for the majority of the HLA-I peptidome. These findings highlight the need for a vaccine design that incorporates multiple viral elements harboring CD4 + and CD8 + T cell epitopes to maximize vaccine effectiveness. Weingarten-Gabbay et al. map the repertoire of SARS-CoV-2 peptides naturally presented on HLA-II. The authors uncover HLA-II peptides originating from noncanonical ORFs and highlight striking differences between viral proteins that are presented on class I and class II HLAs, resulting in distinct targets for killer and helper T cells.
ArticleNumber 113596
Author Bauer, Matthew R.
Saeed, Mohsan
Hacohen, Nir
Sabeti, Pardis C.
Clauser, Karl R.
Sarkizova, Siranush
Abelin, Jennifer G.
Chen, Da-Yuan
Rice, Charles M.
Carr, Steven A.
Gentili, Matteo
Hernandez, Gabrielle M.
Weingarten-Gabbay, Shira
Taylor, Hannah B.
Pearlman, Leah R.
AuthorAffiliation 4 Department of Biochemistry & Cell Biology, Boston University Chobanian and Avedisian School of Medicine, Boston, MA, USA
12 These authors contributed equally
9 Massachusetts Consortium on Pathogen Readiness, Boston, MA, USA
14 Lead contact
1 Broad Institute of MIT and Harvard University, Cambridge, MA, USA
3 Laboratory of Virology and Infectious Disease, The Rockefeller University, New York, NY, USA
7 Department of Medicine, Massachusetts General Hospital, Boston, MA, USA
13 Senior author
2 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA
5 National Emerging Infectious Diseases Laboratories, Boston University, Boston, MA, USA
10 Department of Immunology and Infectious Disease, Harvard T.H. Chan School of Public Health, Boston, MA, USA
11 Howard Hughes Medical Institute, Chevy Chase, MD, USA
6 Harvard Program in Biological and Biomedical Sciences, Division of Medical Sciences, Harvard University Medical School, Boston, MA, USA
8 Center for Cancer Research,
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– name: 10 Department of Immunology and Infectious Disease, Harvard T.H. Chan School of Public Health, Boston, MA, USA
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– name: 6 Harvard Program in Biological and Biomedical Sciences, Division of Medical Sciences, Harvard University Medical School, Boston, MA, USA
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Keywords CP: Immunology
SARS-CoV-2
CD4+ T cell
noncanonical protein
CP: Microbiology
immunopeptidome
HLA-II
antigen processing and presentation
immunity
viral antigen
CD4(+) T cell
Language English
License This is an open access article under the CC BY license.
Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.
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AUTHOR CONTRIBUTIONS
S.W.-G. and J.G.A. conceptualized the study. S.W.-G., J.G.A., and M.S. designed the experiments. D.-Y.C., H.B.T., M.G., G.M.H., L.R.P., and M.R.B. performed experiments. S.W.-G., S.S., H.B.T., K.R.C., and J.G.A. performed data analysis. N.H., S.A.C., M.S., and P.C.S. supervised the work. S.W.-G., J.G.A., M.S., and P.C.S. wrote the manuscript, with contributions from all of the authors.
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Snippet Targeted synthetic vaccines have the potential to transform our response to viral outbreaks, yet the design of these vaccines requires a comprehensive...
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SubjectTerms antigen processing and presentation
CD4+ T cell
CP: Immunology
CP: Microbiology
HLA-II
immunity
immunopeptidome
noncanonical protein
SARS-CoV-2
viral antigen
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Title The HLA-II immunopeptidome of SARS-CoV-2
URI https://dx.doi.org/10.1016/j.celrep.2023.113596
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