Cited by 147vaccines and immunoinformatics approachesSARS-CoV-2 and COVID-19 ResearchImmunotherapy and Immune Responses

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Profiling SARS-CoV-2 HLA-I peptidome reveals T cell epitopes from out-of-frame ORFs

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Weingarten-Gabbay, Shira, Klaeger, Susan, Sarkizova, Siranush, Pearlman, Leah R., Chen, Da-Yuan, Gallagher, Kathleen M.E., Bauer, Matthew R., Taylor, Hannah B., Dunn, W. Augustine, Tarr, Christina, Sidney, John, Rachimi, Suzanna, Conway, Hasahn L., Katsis, Katelin, Wang, Yuntong, Leistritz-Edwards, Del, Durkin, Melissa R., Tomkins-Tinch, Christopher H., Finkel, Yaara, Nachshon, Aharon, Gentili, Matteo, Rivera, Keith D., Carulli, Isabel P., Chea, Vipheaviny A., Chandrashekar, Abishek, Bozkus, Cansu Cimen, Carrington, Mary, Lavin-Parsons, Kendall, Parry, Blair, Lilley, Brendan, Lodenstein, Carl, McKaig, Brenna, Charland, Nicole, Khanna, Hargun, Margolin, Justin, Gonye, Anna, Gushterova, Irena, Lasalle, Tom, Sharma, Nihaarika, Russo, Brian C., Rojas-Lopez, Maricarmen, Sade-Feldman, Moshe, Manakongtreecheep, Kasidet, Tantivit, Jessica, Fisher Thomas, Molly, Bhardwaj, Nina, Barouch, Dan H., Sette, Alessandro, Maus, Marcela V., Rice, Charles M., Clauser, Karl R., Keskin, Derin B., Pregibon, Daniel C., Hacohen, Nir, Carr, Steven A., Abelin, Jennifer G., Saeed, Mohsan, Sabeti, Pardis C.·2021·Cell

DOI 10.1016/j.cell.2021.05.046PMC PMC8173604

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Abstract

T cell-mediated immunity plays an important role in controlling SARS-CoV-2 infection, but the repertoire of naturally processed and presented viral epitopes on class I human leukocyte antigen (HLA-I) remains uncharacterized. Here, we report the first HLA-I immunopeptidome of SARS-CoV-2 in two cell lines at different times post infection using mass spectrometry. We found HLA-I peptides derived not only from canonical open reading frames (ORFs) but also from internal out-of-frame ORFs in spike and nucleocapsid not captured by current vaccines. Some peptides from out-of-frame ORFs elicited T cell responses in a humanized mouse model and individuals with COVID-19 that exceeded responses to canonical peptides, including some of the strongest epitopes reported to date. Whole-proteome analysis of infected cells revealed that early expressed viral proteins contribute more to HLA-I presentation and immunogenicity. These biological insights, as well as the discovery of out-of-frame ORF epitopes, will facilitate selection of peptides for immune monitoring and vaccine development.

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Authors: Weingarten-Gabbay, S., Klaeger, S., Sarkizova, S., Pearlman, L. R., Chen, D.-Y., Gallagher, K. M. E., Bauer, M. R., Taylor, H. B., Dunn, W. A., Tarr, C., Sidney, J., Rachimi, S., Conway, H. L., Katsis, K., Wang, Y., Leistritz-Edwards, D., Durkin, M. R., Tomkins-Tinch, C. H., Finkel, Y., Nachshon, A., Gentili, M., Rivera, K. D., Carulli, I. P., Chea, V. A., Chandrashekar, A., Bozkus, C. C., Carrington, M., Lavin-Parsons, K., Parry, B., Lilley, B., Lodenstein, C., McKaig, B., Charland, N., Khanna, H., Margolin, J., Gonye, A., Gushterova, I., Lasalle, T., Sharma, N., Russo, B. C., Rojas-Lopez, M., Sade-Feldman, M., Manakongtreecheep, K., Tantivit, J., Fisher Thomas, M., Bhardwaj, N., Barouch, D. H., Sette, A., Maus, M. V., Rice, C. M., Clauser, K. R., Keskin, D. B., Pregibon, D. C., Hacohen, N., Carr, S. A., Abelin, J. G., Saeed, M., & Sabeti, P. C.
Affiliations: Broad Institute (US)
Harvard University (US)
La Jolla Institute for Immunology (US)
Boston University (US)
Massachusetts General Hospital (US)
Weizmann Institute of Science (IL)
Dana-Farber Cancer Institute (US)
Beth Israel Deaconess Medical Center (US)
Mount Sinai Hospital (US)
Ragon Institute of MGH, MIT and Harvard (US)
Rockefeller University (US)
Corresponding author: Weingarten-Gabbay, Shira
Klaeger, Susan
Saeed, Mohsan
ORCID: Weingarten-Gabbay, Shira
Klaeger, Susan
Sarkizova, Siranush
Gallagher, Kathleen M.E.
Bauer, Matthew R.
Taylor, Hannah B.
Sidney, John
Rachimi, Suzanna
Conway, Hasahn L.
Leistritz-Edwards, Del
Durkin, Melissa R.
Tomkins-Tinch, Christopher H.
Finkel, Yaara
Nachshon, Aharon
Gentili, Matteo
Rivera, Keith D.
Carulli, Isabel P.
Chea, Vipheaviny A.
Chandrashekar, Abishek
Bozkus, Cansu Cimen
Carrington, Mary
Parry, Blair
Lilley, Brendan
McKaig, Brenna
Charland, Nicole
Khanna, Hargun
Margolin, Justin
Gonye, Anna
Gushterova, Irena
Russo, Brian C.
Sade-Feldman, Moshe
Manakongtreecheep, Kasidet
Tantivit, Jessica
Bhardwaj, Nina
Barouch, Dan H.
Sette, Alessandro
Maus, Marcela V.
Rice, Charles M.
Clauser, Karl R.
Keskin, Derin B.
Pregibon, Daniel C.
Hacohen, Nir
Carr, Steven A.
Abelin, Jennifer G.
Saeed, Mohsan
Sabeti, Pardis C.
Venue: Cell
Publisher: Elsevier BV
Published: 2021-07
Volume: 184
Issue: 15
Pages: 3962-3980.e17
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2021.05.046
PMC: PMC8173604
OpenAlex: W3172192134
Cited by: 147
References: 103
Citations by year: 2026: 6 · 2025: 23 · 2024: 32 · 2023: 38 · 2022: 33 · 2021: 15
FWCI: 9.26
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Cell (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (U24-CA210986, U24CA210979, U01 CA214125)
NIAID (U19AI110818, 3 R01-AI091707-10S1, U19AI082630)
Cancer Research Institute
Parker Institute for Cancer Immunotherapy
Broad Institute
Frederick National Laboratory for Cancer Research (HHSN261200800001E)
Human Frontier Science Program (LT-000396/2018)
European Molecular Biology Organization (ALTF 883-2017)
Iran National Science Foundation (CRI2993, 1745303, R21 CA216772-01A1, ALTF 486-2018)
Harvard University
Gilead Sciences
National Institutes of Health
G. Harold and Leila Y. Mathers Charitable Foundation
Novartis
Neos Therapeutics
U.S. Department of Health and Human Services
Massachusetts Institute of Technology
Boston University
BioMarin Pharmaceutical
Pfizer
Celldex Therapeutics
Biogen
Government of South Australia
Exelixis
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: SARS-CoV-2, T cell epitopes, viral peptide presentation, spike protein, nucleocapsid protein, T cell immunity, humanized mice, COVID-19 pandemic, vaccine development, early viral proteins
MeSH terms: A549 Cells, COVID-19, SARS-CoV-2, Alleles, Amino Acid Sequence, Animals, Female, Humans, Kinetics, Male, Peptides, T-Lymphocytes, Histocompatibility Antigens Class I, Open Reading Frames, Antigen Presentation, Epitopes, T-Lymphocyte, Proteome, Mice, HEK293 Cells

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Profiling SARS-CoV-2 HLA-I peptidome reveals T cell epitopes from out-of-frame ORFs

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