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Article ; Online: Cytotoxic T Cells Targeting Spike Glycoprotein Are Associated with Hybrid Immunity to SARS-CoV-2.

Phan, Jolie M / Layton, Erik D / Yu, Krystle K Q / Aguilar, Melissa S / Golez, Inah / Franko, Nicholas M / Logue, Jennifer K / Rodda, Lauren B / Howard, Christian A / Pepper, Marion / Gale, Michael / Chu, Helen Y / Seshadri, Chetan

Journal of immunology (Baltimore, Md. : 1950)

2023 Volume 210, Issue 9, Page(s) 1236–1246

Abstract: mRNA vaccination of individuals with prior SARS-CoV-2 infection provides superior protection against breakthrough infections with variants of concern compared with vaccination in the absence of prior infection. However, the immune mechanisms by which ... ...

Abstract	mRNA vaccination of individuals with prior SARS-CoV-2 infection provides superior protection against breakthrough infections with variants of concern compared with vaccination in the absence of prior infection. However, the immune mechanisms by which this hybrid immunity is generated and maintained are unknown. Whereas genetic variation in spike glycoprotein effectively subverts neutralizing Abs, spike-specific T cells are generally maintained against SARS-CoV-2 variants. Thus, we comprehensively profiled human T cell responses against the S1 and S2 domains of spike glycoprotein in a cohort of SARS-CoV-2-naive (n = 13) or -convalescent (n = 17) individuals who received two-dose mRNA vaccine series and were matched by age, sex, and vaccine type. Using flow cytometry, we observed that the overall functional breadth of CD4 T cells and polyfunctional Th1 responses was similar between the two groups. However, polyfunctional cytotoxic CD4 T cell responses against both S1 and S2 domains trended higher among convalescent subjects. Multimodal single-cell RNA sequencing revealed diverse functional programs in spike-specific CD4 and CD8 T cells in both groups. However, convalescent individuals displayed enhanced cytotoxic and antiviral CD8 T cell responses to both S1 and S2 in the absence of cytokine production. Taken together, our data suggest that cytotoxic CD4 and CD8 T cells targeting spike glycoprotein may partially account for hybrid immunity and protection against breakthrough infections with SARS-CoV-2.
MeSH term(s)	Humans ; T-Lymphocytes, Cytotoxic ; SARS-CoV-2 ; Spike Glycoprotein, Coronavirus/genetics ; COVID-19 ; Breakthrough Infections ; RNA, Messenger ; Vaccination ; Adaptive Immunity ; Glycoproteins ; Antibodies, Viral ; Antibodies, Neutralizing
Chemical Substances	spike protein, SARS-CoV-2 ; Spike Glycoprotein, Coronavirus ; RNA, Messenger ; Glycoproteins ; Antibodies, Viral ; Antibodies, Neutralizing
Language	English
Publishing date	2023-03-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2200815
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Article ; Online: Durable Expansion of TCR-δ Meta-Clonotypes After BCG Revaccination in Humans.

James, Charlotte A / Yu, Krystle K Q / Mayer-Blackwell, Koshlan / Fiore-Gartland, Andrew / Smith, Malisa T / Layton, Erik D / Johnson, John L / Hanekom, Willem A / Scriba, Thomas J / Seshadri, Chetan

Frontiers in immunology

2022 Volume 13, Page(s) 834757

Abstract: Mycobacterium ... ...

Abstract	Mycobacterium bovis
MeSH term(s)	Adult ; BCG Vaccine ; Child ; Child, Preschool ; Humans ; Immunization, Secondary ; Leukocytes, Mononuclear ; Mycobacterium tuberculosis ; Receptors, Antigen, T-Cell
Chemical Substances	BCG Vaccine ; Receptors, Antigen, T-Cell
Language	English
Publishing date	2022-03-30
Publishing country	Switzerland
Document type	Clinical Trial, Phase I ; Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.834757
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Article ; Online: CD4 and CD8 co-receptors modulate functional avidity of CD1b-restricted T cells.

James, Charlotte A / Xu, Yuexin / Aguilar, Melissa S / Jing, Lichen / Layton, Erik D / Gilleron, Martine / Minnaard, Adriaan J / Scriba, Thomas J / Day, Cheryl L / Warren, Edus H / Koelle, David M / Seshadri, Chetan

Nature communications

2022 Volume 13, Issue 1, Page(s) 78

Abstract: T cells recognize mycobacterial glycolipid (mycolipid) antigens presented by CD1b molecules, but the role of CD4 and CD8 co-receptors in mycolipid recognition is unknown. Here we show CD1b-mycolipid tetramers reveal a hierarchy in which circulating T ... ...

Abstract	T cells recognize mycobacterial glycolipid (mycolipid) antigens presented by CD1b molecules, but the role of CD4 and CD8 co-receptors in mycolipid recognition is unknown. Here we show CD1b-mycolipid tetramers reveal a hierarchy in which circulating T cells expressing CD4 or CD8 co-receptor stain with a higher tetramer mean fluorescence intensity than CD4-CD8- T cells. CD4+ primary T cells transduced with mycolipid-specific T cell receptors bind CD1b-mycolipid tetramer with a higher fluorescence intensity than CD8+ primary T cells. The presence of either CD4 or CD8 also decreases the threshold for interferon-γ secretion. Co-receptor expression increases surface expression of CD3ε, suggesting a mechanism for increased tetramer binding and activation. Targeted transcriptional profiling of mycolipid-specific T cells from individuals with active tuberculosis reveals canonical markers associated with cytotoxicity among CD8+ compared to CD4+ T cells. Thus, expression of co-receptors modulates T cell receptor avidity for mycobacterial lipids, leading to in vivo functional diversity during tuberculosis disease.
MeSH term(s)	Antigens, CD1/genetics ; Antigens, CD1/immunology ; CD3 Complex/genetics ; CD3 Complex/immunology ; CD4-Positive T-Lymphocytes/immunology ; CD4-Positive T-Lymphocytes/microbiology ; CD8-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/microbiology ; Cytotoxicity, Immunologic ; Gene Expression ; Glycolipids/immunology ; Glycolipids/metabolism ; Humans ; Interferon-gamma/genetics ; Interferon-gamma/immunology ; Lymphocyte Activation ; Mycobacterium tuberculosis/growth & development ; Mycobacterium tuberculosis/immunology ; Primary Cell Culture ; Protein Binding ; Protein Multimerization ; Transduction, Genetic ; Tuberculosis/genetics ; Tuberculosis/immunology ; Tuberculosis/microbiology
Chemical Substances	Antigens, CD1 ; CD1b antigen ; CD3 Complex ; CD3E protein, human ; Glycolipids ; sulfoglycolipids ; Interferon-gamma (82115-62-6)
Language	English
Publishing date	2022-01-10
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-27764-w
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Article ; Online: T Cells Specific for a Mycobacterial Glycolipid Expand after Intravenous Bacillus Calmette-Guérin Vaccination.

Layton, Erik D / Barman, Soumik / Wilburn, Damien B / Yu, Krystle K Q / Smith, Malisa T / Altman, John D / Scriba, Thomas J / Tahiri, Nabil / Minnaard, Adriaan J / Roederer, Mario / Seder, Robert A / Darrah, Patricia A / Seshadri, Chetan

Journal of immunology (Baltimore, Md. : 1950)

2021 Volume 206, Issue 6, Page(s) 1240–1250

Abstract: Intradermal vaccination ... ...

Abstract	Intradermal vaccination with
MeSH term(s)	Adolescent ; Animals ; Antigens, Bacterial/immunology ; Antigens, Bacterial/metabolism ; Antigens, CD1/metabolism ; BCG Vaccine/administration & dosage ; Cell Line ; Child ; Cohort Studies ; Disease Models, Animal ; Female ; Glycolipids/immunology ; Glycoproteins/metabolism ; Healthy Volunteers ; Humans ; Injections, Intravenous ; Lung/cytology ; Lung/immunology ; Lung/microbiology ; Macaca mulatta ; Male ; Mycobacterium bovis/immunology ; Mycobacterium tuberculosis/immunology ; Primary Cell Culture ; T-Lymphocytes/immunology ; T-Lymphocytes/metabolism ; Tuberculosis/blood ; Tuberculosis/immunology ; Tuberculosis/microbiology ; Tuberculosis/prevention & control
Chemical Substances	Antigens, Bacterial ; Antigens, CD1 ; BCG Vaccine ; CD1C protein, human ; CD1b antigen ; Glycolipids ; Glycoproteins
Language	English
Publishing date	2021-02-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2001065
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Article ; Online: IFN-γ independent markers of Mycobacterium tuberculosis exposure among male South African gold miners.

Davies, Leela R L / Smith, Malisa T / Cizmeci, Deniz / Fischinger, Stephanie / Shih-Lu Lee, Jessica / Lu, Lenette L / Layton, Erik D / Grant, Alison D / Fielding, Katherine / Stein, Catherine M / Boom, W Henry / Hawn, Thomas R / Fortune, Sarah M / Wallis, Robert S / Churchyard, Gavin J / Alter, Galit / Seshadri, Chetan

EBioMedicine

2023 Volume 93, Page(s) 104678

Abstract: Background: The prevalence of tuberculosis among men who work in the gold mines of South Africa is among the highest in the world, but a fraction of miners demonstrate consistently negative results upon tuberculin skin test (TST) and IFN-γ release assay ...

Abstract	Background: The prevalence of tuberculosis among men who work in the gold mines of South Africa is among the highest in the world, but a fraction of miners demonstrate consistently negative results upon tuberculin skin test (TST) and IFN-γ release assay (IGRA). We hypothesized that these "resisters" (RSTRs) may display unconventional immune signatures of exposure to M. tuberculosis (M.tb). Methods: In a cohort of RSTRs and matched controls with latent TB infection (LTBI), we profiled the functional breadth of M.tb antigen-specific T cell and antibody responses using multi-parameter flow cytometry and systems serology, respectively. Findings: RSTRs and LTBI controls both exhibited IFN-γ independent T-cell and IgG antibody responses to M.tb-specific antigens ESAT-6 and CFP-10. Antigen-specific antibody Fc galactosylation and sialylation were higher among RSTRs. In a combined T-cell and antibody analysis, M.tb lysate-stimulated TNF secretion by T cells correlated positively with levels of purified protein derivative-specific IgG. A multivariate model of the combined data was able to differentiate RSTR and LTBI subjects. Interpretation: IFN-γ independent immune signatures of exposure to M.tb, which are not detected by approved clinical diagnostics, are readily detectable in an occupational cohort uniquely characterized by intense and long-term infection pressure. Further, TNF may mediate a coordinated response between M.tb-specific T-cells and B-cells. Funding: This work was supported by the US National Institutes of Health (R01-AI124348 to Boom, Stein, and Hawn; R01-AI125189 and R01-AI146072 to Seshadri; and 75N93019C00071 to Fortune, Alter, Seshadri, and Boom), the Doris Duke Charitable Foundation (Davies), the Bill & Melinda Gates Foundation (OPP1151836 and OPP1109001 to Hawn; and OPP1151840 to Alter), Mass Life Science Foundation (Fortune), and Good Ventures Fund (Fortune).
MeSH term(s)	Male ; Humans ; Mycobacterium tuberculosis ; South Africa/epidemiology ; Tuberculosis/diagnosis ; Tuberculosis/epidemiology ; Antigens, Bacterial ; Interferon-gamma ; Tuberculin Test
Chemical Substances	Antigens, Bacterial ; Interferon-gamma (82115-62-6)
Language	English
Publishing date	2023-06-26
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2851331-9
ISSN	2352-3964
ISSN (online)	2352-3964
DOI	10.1016/j.ebiom.2023.104678
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Article ; Online: Where Does the Electron Go? Stable and Metastable Peptide Cation Radicals Formed by Electron Transfer.

Pepin, Robert / Layton, Erik D / Liu, Yang / Afonso, Carlos / Tureček, František

Journal of the American Society for Mass Spectrometry

2016 Volume 28, Issue 1, Page(s) 164–181

Abstract: Electron transfer to doubly and triply charged heptapeptide ions containing polar residues Arg, Lys, and Asp in combination with nonpolar Gly, Ala, and Pro or Leu generates stable and metastable charge-reduced ions, (M + 2H) ...

Abstract	Electron transfer to doubly and triply charged heptapeptide ions containing polar residues Arg, Lys, and Asp in combination with nonpolar Gly, Ala, and Pro or Leu generates stable and metastable charge-reduced ions, (M + 2H)
MeSH term(s)	Amino Acid Sequence ; Cations/chemistry ; Electron Transport ; Electrons ; Free Radicals/chemistry ; Models, Molecular ; Peptides/chemistry ; Spectrometry, Mass, Electrospray Ionization
Chemical Substances	Cations ; Free Radicals ; Peptides
Language	English
Publishing date	2016-10-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	1073671-2
ISSN	1879-1123 ; 1044-0305
ISSN (online)	1879-1123
ISSN	1044-0305
DOI	10.1007/s13361-016-1512-z
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Zs.A 4618: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Validation of a CD1b tetramer assay for studies of human mycobacterial infection or vaccination.

Layton, Erik D / Yu, Krystle K Q / Smith, Malisa T / Scriba, Thomas J / De Rosa, Stephen C / Seshadri, Chetan

Journal of immunological methods

2018 Volume 458, Page(s) 44–52

Abstract: CD1 tetramers loaded with lipid antigens facilitate the identification of rare lipid-antigen specific T cells present in human blood and tissue. Because CD1 proteins are structurally non-polymorphic, these tetramers can be applied to genetically diverse ... ...

Abstract	CD1 tetramers loaded with lipid antigens facilitate the identification of rare lipid-antigen specific T cells present in human blood and tissue. Because CD1 proteins are structurally non-polymorphic, these tetramers can be applied to genetically diverse human populations, unlike MHC-I and MHC-II tetramers. However, there are no standardized assays to quantify and characterize lipid antigen-specific T cells present within clinical samples. We incorporated CD1b tetramers loaded with the mycobacterial lipid glucose monomycolate (GMM) into a multi-parameter flow cytometry assay. Using a GMM-specific T-cell line, we demonstrate that the assay is linear, reproducible, repeatable, precise, accurate, and has a limit of detection of approximately 0.007%. Having formally validated this assay, we performed a cross-sectional study of healthy U.S. controls and South African adolescents with and without latent tuberculosis infection (LTBI). We show that GMM-specific T cells are specifically detected in South African subjects with LTBI and not in U.S. healthy controls. This assay can be expanded to include additional tetramers or phenotypic markers to characterize GMM-specific T cells in studies of mycobacterial infection, disease, or vaccination.
MeSH term(s)	Adolescent ; Adult ; Antigens, Bacterial/immunology ; Antigens, CD1/immunology ; Antigens, CD1/metabolism ; Cell Culture Techniques ; Cell Line ; Cross-Sectional Studies ; Epitopes, T-Lymphocyte/immunology ; Flow Cytometry/instrumentation ; Flow Cytometry/methods ; Glycolipids/chemistry ; Glycolipids/immunology ; Healthy Volunteers ; Humans ; Immunogenicity, Vaccine ; Latent Tuberculosis/diagnosis ; Latent Tuberculosis/immunology ; Latent Tuberculosis/microbiology ; Latent Tuberculosis/prevention & control ; Mycobacterium tuberculosis/immunology ; Mycobacterium tuberculosis/isolation & purification ; Protein Multimerization/immunology ; South Africa ; T-Lymphocytes/immunology ; T-Lymphocytes/metabolism ; Tuberculosis Vaccines/administration & dosage ; Tuberculosis Vaccines/immunology ; United States
Chemical Substances	Antigens, Bacterial ; Antigens, CD1 ; CD1b antigen ; Epitopes, T-Lymphocyte ; Glycolipids ; Tuberculosis Vaccines ; glucose mycolate
Language	English
Publishing date	2018-04-21
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Validation Study
ZDB-ID	120142-6
ISSN	1872-7905 ; 0022-1759
ISSN (online)	1872-7905
ISSN	0022-1759
DOI	10.1016/j.jim.2018.04.004
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Article: Validation of a CD1b tetramer assay for studies of human mycobacterial infection or vaccination

Layton, Erik D / Yu, Krystle K.Q / Smith, Malisa T / Scriba, Thomas J / De Rosa, Stephen C / Seshadri, Chetan

Journal of immunological methods. 2017,

2017

Abstract	CD1 tetramers loaded with lipid antigens facilitate the identification of rare lipid-antigen specific T cells present in human blood and tissue. Because CD1 proteins are structurally non-polymorphic, these tetramers can be applied to genetically diverse human populations, unlike MHC-I and MHC-II tetramers. However, there are no standardized assays to quantify and characterize lipid antigen-specific T cells present within clinical samples. We incorporated CD1b tetramers loaded with the mycobacterial lipid glucose monomycolate (GMM) into a multi-parameter flow cytometry assay. Using a GMM-specific T-cell line, we demonstrate that the assay is linear, reproducible, repeatable, precise, accurate, and has a limit of detection of approximately 0.007%. Having formally validated this assay, we performed a cross-sectional study of healthy U.S. controls and South African adolescents with and without latent tuberculosis infection (LTBI). We show that GMM-specific T cells are specifically detected in South African subjects with LTBI and not in U.S. healthy controls. This assay can be expanded to include additional tetramers or phenotypic markers to characterize GMM-specific T cells in studies of mycobacterial infection, disease, or vaccination.
Keywords	Africans ; T-lymphocytes ; adolescents ; antigens ; cross-sectional studies ; detection limit ; flow cytometry ; glucose ; human population ; humans ; lipids ; phenotype ; proteins ; tuberculosis ; vaccination ; United States
Language	English
Publishing place	Elsevier B.V.
Document type	Article
Note	Pre-press version
ZDB-ID	120142-6
ISSN	1872-7905 ; 0022-1759
ISSN (online)	1872-7905
ISSN	0022-1759
DOI	10.1016/j.jim.2018.04.004
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Comorbid illnesses are associated with altered adaptive immune responses to SARS-CoV-2.

JCI insight

2021 Volume 6, Issue 6

Abstract: Comorbid medical illnesses, such as obesity and diabetes, are associated with more severe COVID-19, hospitalization, and death. However, the role of the immune system in mediating these clinical outcomes has not been determined. We used multiparameter ... ...

Abstract	Comorbid medical illnesses, such as obesity and diabetes, are associated with more severe COVID-19, hospitalization, and death. However, the role of the immune system in mediating these clinical outcomes has not been determined. We used multiparameter flow cytometry and systems serology to comprehensively profile the functions of T cells and antibodies targeting spike, nucleocapsid, and envelope proteins in a convalescent cohort of COVID-19 subjects who were either hospitalized (n = 20) or not hospitalized (n = 40). To avoid confounding, subjects were matched by age, sex, ethnicity, and date of symptom onset. Surprisingly, we found that the magnitude and functional breadth of virus-specific CD4+ T cell and antibody responses were consistently higher among hospitalized subjects, particularly those with medical comorbidities. However, an integrated analysis identified more coordination between polyfunctional CD4+ T cells and antibodies targeting the S1 domain of spike among subjects who were not hospitalized. These data reveal a functionally diverse and coordinated response between T cells and antibodies targeting SARS-CoV-2, which is reduced in the presence of comorbid illnesses that are known risk factors for severe COVID-19.
MeSH term(s)	Adult ; Aged ; Antibodies, Neutralizing/metabolism ; Antibodies, Neutralizing/physiology ; Antibodies, Viral/metabolism ; Antibodies, Viral/physiology ; CD4-Positive T-Lymphocytes/metabolism ; CD4-Positive T-Lymphocytes/physiology ; COVID-19/epidemiology ; COVID-19/immunology ; COVID-19/virology ; Cardiovascular Diseases/epidemiology ; Cardiovascular Diseases/immunology ; Comorbidity ; Diabetes Mellitus/epidemiology ; Diabetes Mellitus/immunology ; Female ; Hospitalization ; Humans ; Immunity, Humoral ; Male ; Middle Aged ; Nucleocapsid ; SARS-CoV-2/immunology ; Severity of Illness Index ; Spike Glycoprotein, Coronavirus ; Viral Envelope ; Viral Proteins ; Virion ; Young Adult
Chemical Substances	Antibodies, Neutralizing ; Antibodies, Viral ; Spike Glycoprotein, Coronavirus ; Viral Proteins
Language	English
Publishing date	2021-03-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, P.H.S.
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.146242
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Article ; Online: Tissue-Resident-Memory CD8

Frontiers in immunology

2021 Volume 12, Page(s) 735643

Abstract: Tissue-resident-memory T cells (TRM) populate the body's barrier surfaces, functioning as frontline responders against reencountered pathogens. Understanding of the mechanisms by which CD8TRM achieve effective immune protection remains incomplete in a ... ...

Abstract	Tissue-resident-memory T cells (TRM) populate the body's barrier surfaces, functioning as frontline responders against reencountered pathogens. Understanding of the mechanisms by which CD8TRM achieve effective immune protection remains incomplete in a naturally recurring human disease. Using laser capture microdissection and transcriptional profiling, we investigate the impact of CD8TRM on the tissue microenvironment in skin biopsies sequentially obtained from a clinical cohort of diverse disease expression during herpes simplex virus 2 (HSV-2) reactivation. Epithelial cells neighboring CD8TRM display elevated and widespread innate and cell-intrinsic antiviral signature expression, largely related to IFNG expression. Detailed evaluation
MeSH term(s)	Adaptive Immunity/genetics ; Adult ; Aged ; Antigens, Viral/immunology ; CD8-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/metabolism ; CD8-Positive T-Lymphocytes/virology ; Cells, Cultured ; Epithelial Cells/immunology ; Epithelial Cells/metabolism ; Epithelial Cells/virology ; Female ; Gene Expression Profiling ; Herpes Genitalis/genetics ; Herpes Genitalis/immunology ; Herpes Genitalis/metabolism ; Herpes Genitalis/virology ; Herpesvirus 2, Human/immunology ; Herpesvirus 2, Human/pathogenicity ; Host-Pathogen Interactions ; Humans ; Immunity, Innate/genetics ; Immunologic Memory ; Interferon-gamma/genetics ; Interferon-gamma/metabolism ; Male ; Memory T Cells/immunology ; Memory T Cells/metabolism ; Memory T Cells/virology ; Middle Aged ; Phenotype ; Skin/immunology ; Skin/metabolism ; Skin/virology ; Transcriptome
Chemical Substances	Antigens, Viral ; IFNG protein, human ; Interferon-gamma (82115-62-6)
Language	English
Publishing date	2021-09-06
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2021.735643
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